Hepatokines and non-alcoholic fatty liver disease

Lebensztejn, Dariusz M.; Flisiak-Jackiewicz, Marta; Białokoz-Kalinowska, Irena; Bobrus-Chociej, Anna; Kowalska, Irina

doi:10.18388/abp.2016_1252

Cited by 90Liver Disease Diagnosis and TreatmentAdipokines, Inflammation, and Metabolic DiseasesLiver physiology and pathology

Hepatokines and non-alcoholic fatty liver disease

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Lebensztejn, Dariusz M., Flisiak-Jackiewicz, Marta, Białokoz-Kalinowska, Irena, Bobrus-Chociej, Anna, Kowalska, Irina·2016·Acta Biochimica Polonica

DOI 10.18388/abp.2016_1252

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Abstract

Nowadays non-alcoholic fatty liver disease (NAFLD) is becoming the most common chronic liver pathology both in adults and children. NAFLD manifestation ranges from a simple liver steatosis to steatohepatitis (nonalcoholic steatohepatitis - NASH), which may progress to advanced fibrosis, cirrhosis and end-stage liver disease. Due to the coexistence of visceral obesity, insulin resistance and dyslipidemia, NAFLD is considered to be the hepatic manifestation of metabolic syndrome. In recent years, in the pathogenesis of metabolic syndrome, type 2 diabetes mellitus, cardiovascular disease and also NAFLD, more and more attention has been paid to the so-called organokines, proteins with both paracrine or/and endocrine activities. These include most known adipokines (mainly produced by adipose tissue), myokines (mainly produced by skeletal muscles) and hepatokines exclusively or predominantly produced by the liver. It was shown that the liver may affect the lipids and glucose metabolism by hepatokines released into the blood and NAFLD seems to be associated with altered hepatokines production. Fetuin-A, fibroblast growth factor-21 (FGF-21), selenoprotein P, sex hormone-binding globulin (SHBG), angiopoietin-related growth factor (also known as angiopoietin-related protein 6) and leukocyte derived chemotaxin 2 (LECT2) are considered as the most important hepatokines. In this review, we provide an overview of the main hepatokines and we summarize the association of liver-derived proteins with the development and progression of NAFLD.

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Low serum level of sex hormone-binding globulin (SHBG) is associated with nonalcoholic fatty liver disease (NAFLD) in post-menopausal women.
“At first, an association of this pathology with a low serum level of SHBG was found in post-menopausal women with NAFLD [70].”
From Adipokines, Myokines, and Hepatokines: Crosstalk and Metabolic Repercussions (2021) · cites this paper as [70]
An increase in serum ANGPTL4 may be related to insulin resistance in patients with metabolic syndrome compared to normal patients.
“However, the increase in serum ANGPTL4 may be related to insulin resistance in patients with metabolic syndrome compared to normal patients [70].”
From Adipokines, Myokines, and Hepatokines: Crosstalk and Metabolic Repercussions (2021) · cites this paper as [70]

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Background
α2-Heremans-Schmid Glycoprotein/ Fetuin-A Is Associated With Insulin Resistance and Fat Accumulation in the Liver in Humans
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BackgroundMethodInfluential
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BackgroundInfluential
Improved Insulin Sensitivity and Resistance to Weight Gain in Mice Null for the Ahsg Gene
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Background
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Background
Plasma Fetuin-A Levels and the Risk of Myocardial Infarction and Ischemic Stroke
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Background
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Background
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Background
Fetuin, a New Globulin Isolated from Serum
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Background
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Background
Serum alpha 2-HS-glycoprotein is an inhibitor of the human insulin receptor at the tyrosine kinase level
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Result
Genetic Predisposition in NAFLD and NASH: Impact on Severity of Liver Disease and Response to Treatment
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Background
Fetuin-A: a multifunctional protein.
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BackgroundResult
Angiopoietin-related growth factor antagonizes obesity and insulin resistance
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Background
Association of Serum Fetuin-A With Insulin Resistance in Type 2 Diabetic and Nondiabetic Subjects
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Background
Fetuin-A and Its Relation to Metabolic Syndrome and Fatty Liver Disease in Obese Children Before and After Weight Loss
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Pediatric nonalcoholic fatty liver disease, metabolic syndrome and cardiovascular risk.
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Background
Increased serum FGF21 levels in patients with nonalcoholic fatty liver disease
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BackgroundResultInfluential
TNF-α Represses β-Klotho Expression and Impairs FGF21 Action in Adipose Cells: Involvement of JNK1 in the FGF21 Pathway
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Result
Non-Alcoholic Fatty Liver Disease, Non-Alcoholic Steatohepatitis and Orthotopic Liver Transplantation
Burke, A., & Lucey, M. R. (2004) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2004.00432.x · Cited by 192 · see citing works
Serum selenoprotein P levels in patients with type 2 diabetes and prediabetes: implications for insulin resistance, inflammation, and atherosclerosis
Yang, S. J., Hwang, S. Y., Choi, H. Y., Yoo, H. J., Seo, J. A., Kim, S. G., Kim, N. H., Baik, S. H., Choi, D. S., & Choi, K. M. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-0620 · Cited by 191 · cited 1× · see citing works
“Similarly, a positive correlation with the parameters associated with cardiovascular risk factors (circumference waist, hsCRP, triglycerides level, carotid intima media thickness) as well as aspartate aminotransferase activity was noted (Yang et al., 2011).”
Background
Int J Cancer：戒烟可以改善恶性肿瘤患者预后
Cao, L. (2017) · Medical Research & Publication · doi:10.14218/mrp.2017.061 · Cited by 187
Fetuin A in nonalcoholic fatty liver disease: in vivo and in vitro studies
Haukeland, J. W., Dahl, T. B., Yndestad, A., Gladhaug, I. P., Løberg, E. M., Haaland, T., Konopski, Z., Wium, C., Aasheim, E. T., Johansen, O. E., et al. (2011) · European Journal of Endocrinology · doi:10.1530/eje-11-0864 · Cited by 186 · cited 9× · see citing works
“Moreover, the administration of metformin in patients with NAFLD (randomized placebo control trial), although did not cause histological improvement (Haukeland et al., 2009), resulted in the reduction of the serum concentration of fetuin-A (Haukeland et al., 2012).”
BackgroundResultInfluential
Nrf2 Represses FGF21 During Long-Term High-Fat Diet–Induced Obesity in Mice
Chartoumpekis, D. V., Ziros, P. G., Psyrogiannis, A. I., Papavassiliou, A. G., Kyriazopoulou, V. E., Sykiotis, G. P., & Habeos, I. G. (2011) · Diabetes · doi:10.2337/db11-0112 · Cited by 184 · cited 1× · see citing works
“This data was supported by animal studies which showed that tumor necrosis factor alpha and NFE2 (oxidative stress-activated transcription factors) may impair FGF21 transcription and release (Chartoumekis et al., 2011; Diaz-Delfin et al., 2012).”
Result
Purification and primary amino acid sequence of a novel neutrophil chemotactic factor LECT2
Yamagoe, S., Yamakawa, Y., Matsuo, Y., Minowada, J., Mizuno, S., & Suzuki, K. (1996) · Immunology Letters · doi:10.1016/0165-2478(96)02572-2 · Cited by 178 · cited 1× · see citing works
“Firstly, LECT2 was identified as a novel neutrophil chemotactic protein (Yamagoe et al., 1996).”
Background
The Natural History of Non-Alcoholic Fatty Liver Disease
Caldwell, S. H., & Argo, C. K. (2010) · Digestive Diseases · doi:10.1159/000282081 · Cited by 177 · cited 2× · see citing works
“…entity; depending on the severity of the pathological process, it may present as an isolated hepatic steatosis (simple steatosis), nonalcoholic steatohepatitis (NASH), or may lead to liver cirrhosis and hepatocellular carcinoma (HCC) (Caldwell & Argo, 2010; Vernon et al., 2011; Ertle et al., 2011).”
Background
NF-κB mediates lipid-induced fetuin-A expression in hepatocytes that impairs adipocyte function effecting insulin resistance
Dasgupta, S., Bhattacharya, S., Biswas, A., Majumdar, S. S., Mukhopadhyay, S., Ray, S., & Bhattacharya, S. (2010) · Biochemical Journal · doi:10.1042/bj20100330 · Cited by 168 · cited 1× · see citing works
“The high concentration of saturated fatty acids (via NF-kB activation) and increased blood glucose (via ERK 1 or 2 signaling pathways activation) induce the hepatic synthesis of this hepatokine (Takata et al., 2009; Dasgupta et al., 2010).”
Background
Rational Design of a Fibroblast Growth Factor 21-Based Clinical Candidate, LY2405319
Kharitonenkov, A., Beals, J. M., Micanovic, R., Strifler, B. A., Rathnachalam, R., Wroblewski, V. J., Li, S., Köester, A., Ford, A. M., Coşkun, T., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058575 · Cited by 168 · cited 2× · see citing works
“Subcutaneously administered short-acting FGF-21 analog (LY2405319) improved insulin sensitivity and lipid profile in ob/ob and diet-induced obese mice (Kharitonenkov et al., 2013).”
Background
FGF21 Analogs of Sustained Action Enabled by Orthogonal Biosynthesis Demonstrate Enhanced Antidiabetic Pharmacology in Rodents
Mu, J., Pinkstaff, J. K., Li, Z., Skidmore, L. K., Li, N., Myler, H. A., Dallas-Yang, Q., Hays, A. A., Yao, J., Bussell, S., et al. (2011) · Diabetes · doi:10.2337/db11-0838 · Cited by 162 · see citing works
Circulating fetuin-A and free fatty acids interact to predict insulin resistance in humans
Stefan, N., & Häring, H.-U. (2013) · Nature Medicine · doi:10.1038/nm.3116 · Cited by 160 · see citing works
Fibroblast Growth Factor 21 (FGF-21) and Its Relation to Obesity, Metabolic Syndrome, and Nonalcoholic Fatty Liver in Children: A Longitudinal Analysis
Reinehr, T., Woelfle, J., Wunsch, R., & Roth, C. L. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1221 · Cited by 160 · cited 1× · see citing works
“It should be emphasized that NAFLD was diagnosed on the basis of different diagnostic criteria (ultrasound, MRI and liver biopsy) ( Li et al., 2010; Yilmaz et al., 2010; Reinehr et al., 2012; Giannini et al., 2013).”
Background
LECT2 functions as a hepatokine that links obesity to skeletal muscle insulin resistance
Lan, F., Misu, H., Chikamoto, K., Takayama, H., Kikuchi, A., Mohri, K., Takata, N., Hayashi, H., Matsuzawa-Nagata, N., Takeshita, Y., et al. (2014) · Diabetes · doi:10.2337/db13-0728 · Cited by 158 · cited 6× · see citing works
“…non-alcoholic fatty liver disease, fetuin-A, fibroblast growth factor-21, selenoprotein P, sex hormone-binding globulin, angiopoietin-related growth factor, leukocyte derived chemotaxin 2 Received: 19 January, 2016; revised: 10 May, 2016; accepted: 18 May, 2016; available on-line: 6 June, 2016”
BackgroundInfluential
Relationships of Circulating Sex Hormone–Binding Globulin With Metabolic Traits in Humans
Peter, A., Kantartzis, K., Machann, J., Schick, F., Staiger, H., Machicao, F. E., Schleicher, E. D., Fritsche, A., Häring, H., & Stefan, N. (2010) · Diabetes · doi:10.2337/db10-0179 · Cited by 156 · cited 5× · see citing works
“…non-alcoholic fatty liver disease, fetuin-A, fibroblast growth factor-21, selenoprotein P, sex hormone-binding globulin, angiopoietin-related growth factor, leukocyte derived chemotaxin 2 Received: 19 January, 2016; revised: 10 May, 2016; accepted: 18 May, 2016; available on-line: 6 June, 2016”
BackgroundInfluential
Angiopoietin-like proteins: emerging targets for treatment of obesity and related metabolic diseases
Kadomatsu, T., Tabata, M., & Oike, Y. (2010) · FEBS Journal · doi:10.1111/j.1742-4658.2010.07979.x · Cited by 141 · see citing works
The role of fibroblast growth factor 21 in the pathogenesis of non-alcoholic fatty liver disease and implications for therapy
Liu, J., Xu, Y., Hu, Y., & Wang, G. (2014) · Metabolism · doi:10.1016/j.metabol.2014.11.009 · Cited by 137 · cited 3× · see citing works
“Review of the data indicates that accumulation of DAG in hepatocytes and subsequent activation of PKCε in the liver are responsible for the hepatic insulin resistance (Perry et al., 2014, Bierkenfeld et al., 2014).”
Background
Angiopoietin-related growth factor (AGF) promotes epidermal proliferation, remodeling, and regeneration
Oike, Y., Yasunaga, K., Ito, Y., Matsumoto, S.-I., Maekawa, H., Morisada, T., Arai, F., Nakagata, N., Takeya, M., Masuho, Y., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1531901100 · Cited by 130 · cited 2× · see citing works
“Angiopoietin-related growth factor (AGF) (also known as angiopoietin-related protein 6) encoded by the gene Angptl6, secreted into the circulation predominantly from the liver, was identified by Oike et al. (2003).”
Background
Fibroblast growth factor 21 participates in adaptation to endoplasmic reticulum stress and attenuates obesity-induced hepatic metabolic stress
Kim, S. H., Kim, K. H., Kim, H.-K., Kim, M.-J., Back, S. H., Konishi, M., Itoh, N., & Lee, M.-S. (2015) · Diabetologia · doi:10.1007/s00125-014-3475-6 · Cited by 124 · cited 1× · see citing works
“It affects selected elements of the “multi-hits theory”, such as oxidative stress, endoplasmic reticulum stress, mitochondrial dysfunction, and low-grade chronic inflammation (Nishimura et al., 2000; Jiang et al., 2014; Fisher et al., 2014; Kim et al., 2015).”
Background
Role of fibroblast growth factor 21 in the early stage of NASH induced by methionine- and choline-deficient diet
Tanaka, N., Takahashi, S., Zhang, Y., Krausz, K. W., Smith, P. B. W., Patterson, A. D., & Gonzalez, F. J. (2015) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2015.02.012 · Cited by 120 · cited 1× · see citing works
“In the animal model, studies demonstrated that FGF-21 is induced in response to toxic lipid accumulation in the early stage of methionine- and choline-deficient NASH (Tanaka et al., 2015).”
Background
High serum level of fibroblast growth factor 21 is an independent predictor of non-alcoholic fatty liver disease: A 3-year prospective study in China
Li, H., Dong, K., Fang, Q., Hou, X., Zhou, M., Bao, Y., Xiang, K., Xu, A., & Jia, W. (2012) · Journal of Hepatology · doi:10.1016/j.jhep.2012.10.029 · Cited by 118 · see citing works
SECRETION OF TESTOSTERONE-ESTRADIOL-BINDING GLOBULIN BY A HUMAN HEPATOMA-DERIVED CELL LINE
Khan, M., Knowles, B. B., Aden, D. P., & ROSNE, R. (1981) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-53-2-448 · Cited by 116 · cited 2× · see citing works
“FGF-21 is a 209 amino acid peptide produced mainly in the liver, but the expression of this protein in the lower extent was also found in the pancreas, testes, duodenum and adipose tissue; gene for FGF-21 is localized on chromosome 19 (Nishimura et al., 2000; Fon Tacer et al., 2010; Li et al.,…”
Background
Increased selenoprotein P levels in subjects with visceral obesity and nonalcoholic Fatty liver disease
Choi, H. Y., Hwang, S. Y., Lee, C. H., Hong, H. C., Yang, S. J., Yoo, H. J., Seo, J. A., Kim, S. G., Kim, N. H., Baik, S. H., et al. (2013) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2013.37.1.63 · Cited by 111 · cited 4× · see citing works
“(Choi et al., 2013) Liver Liver Impairs insulin signaling in”
BackgroundInfluential
The link between fibroblast growth factor 21 and sterol regulatory element binding protein 1c during lipogenesis in hepatocytes
Zhang, Y., Lei, T., Huang, J., Wang, S. B., Zhou, L., Yang, Z., & Chen, X. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.05.003 · Cited by 110 · cited 1× · see citing works
“FGF-21 directly regulates lipid metabolism and reduces hepatic lipid accumulation in an insulin-independent manner (Zhang et al., 2011; Li et al., 2012; Lee et al., 2014).”
Background
Inverse correlation between serum levels of selenoprotein P and adiponectin in patients with type 2 diabetes
Misu, H., Ishikura, K., Kurita, S., Takeshita, Y., Ota, T., Saito, Y., Takahashi, K., Kaneko, S., & Takamura, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034952 · Cited by 105 · cited 1× · see citing works
“An inverse correlation of selenoproteins P level with the adiponectin was also observed (Misu et al., 2012).”
Background
Association between Serum Atypical Fibroblast Growth Factors 21 and 19 and Pediatric Nonalcoholic Fatty Liver Disease
Alisi, A., Ceccarelli, S., Panera, N., Prono, F., Petrini, S., Stefanis, C. D., Pezzullo, M., Tozzi, A. E., Villani, A., Bedogni, G., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067160 · Cited by 105 · cited 2× · see citing works
“In pediatric population, Alisi et al. (2013) found a strong inverse correlation between FGF21 circulating level and NAFLD severity (fibrosis).”
Background
Molecular cloning of human and bovine LECT2 having a neutrophil chemotactic activity and its specific expression in the liver
Yamagoe, S., Mizuno, S., & Suzuki, K. T. (1998) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(97)00181-4 · Cited by 98 · see citing works
Circulating Levels of FGF-21 in Obese Youth: Associations With Liver Fat Content and Markers of Liver Damage
Giannini, C., Feldstein, A. E., Santoro, N., Kim, G. J., Kursawe, R., Pierpont, B. M., & Caprio, S. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1250 · Cited by 95 · cited 3× · see citing works
“, 2011), MRI (HFF%) (Giannini et al., 2013); moreover, the correlation of this peptide with intrahepatic triglycerides assessed in liver biopsy was also confirmed (Li et al.”
Background
Circulating Fibroblast Growth Factor 21 Levels Are Closely Associated with Hepatic Fat Content: A Cross-Sectional Study
Yan, H., Xia, M., Chang, X., Xu, Q., Bian, H., Zeng, M., Rao, S., Yao, X., Tu, Y., Jia, W., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024895 · Cited by 95 · cited 3× · see citing works
“In the studies conducted on patients with NAFLD, it was confirmed that circulating FGF-21 was significantly positively correlated with the hepatic fat content assessed in proton magnetic resonance spectroscopy (Yan et al., 2011), MRI (HFF”
Background
Hepatokines as a Link between Obesity and Cardiovascular Diseases
Yoo, H. J., & Choi, K. M. (2015) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2015.39.1.10 · Cited by 94 · cited 1× · see citing works
“This paper is the comprehensive review outlining the most recent updates on association of hepatokines with”
Background
Association Between Endogenous Sex Hormones and Liver Fat in a Multiethnic Study of Atherosclerosis
Lazo, M., Zeb, I., Nasir, K., Tracy, R. P., Budoff, M. J., Ouyang, P., & Vaidya, D. M. (2015) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2014.12.033 · Cited by 91 · cited 4× · see citing works
“The main function of this hepatokine is the sex hormone transport, however, SHBG circulating concentration is also associated with glucose metabolism, adiposity and metabolic syndrome components (Sutton-Tyrrell et al., 2005; Peter et al., 2010; Lazo et al., 2015).”
BackgroundInfluential
Plasma fetuin‐ A is associated with endothelial dysfunction and subclinical atherosclerosis in subjects with nonalcoholic fatty liver disease
Doğru, T., Genç, H., Tapan, S., Aslan, F., Erçin, C. N., Örs, F., Kara, M., Sertoğlu, E., Karslıoğlu, Y., Bağcı, S., et al. (2012) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2012.04460.x · Cited by 90 · cited 7× · see citing works
“It is also considered as a biomarker for neurodegenerative diseases as well as indicator of insulin resistance, cardiovascular risk, endothelial dysfunction and subclinical atherosclerosis (Stefan et al., 2006; Roos et al., 2010; Mori et al., 2011; Mori et al., 2012; Dogru et al., 2013).”
BackgroundResultInfluential
Fetuin-A and the cardiovascular system
Mori, K., Emoto, M., & Inaba, M. (2012) · Advances in clinical chemistry · doi:10.1016/b978-0-12-394317-0.00010-8 · Cited by 86 · cited 1× · see citing works
“It is also considered as a biomarker for neurodegenerative diseases as well as indicator of insulin resistance, cardiovascular risk, endothelial dysfunction and subclinical atherosclerosis (Stefan et al., 2006; Roos et al., 2010; Mori et al., 2011; Mori et al., 2012; Dogru et al., 2013).”
Background
Impact of the Adipokine Adiponectin and the Hepatokine Fetuin-A on the Development of Type 2 Diabetes: Prospective Cohort- and Cross-Sectional Phenotyping Studies
Stefan, N., Sun, Q., Fritsche, A., Machann, J., Schick, F., Gerst, F., Jeppesen, C., Joost, H., Hu, F. B., Boeing, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092238 · Cited by 80 · cited 3× · see citing works
“Accordingly, the strong relationship between plasma fetuin A and insulin resistance (Matsuda index) in patients with NAFLD was reported (Stefan et al., 2014).”
Background
Obesity as the common soil of non‐alcoholic fatty liver disease and diabetes: Role of adipokines
Hui, E., Xu, A., Yang, H. B., & Lam, K. S. L. (2013) · Journal of Diabetes Investigation · doi:10.1111/jdi.12093 · Cited by 79 · cited 4× · see citing works
“It was also shown that adenovirus-mediated knockdown of hepatic FGF-21 leads to the development of hepatic steatosis and dyslipidemia due to impaired expression of genes involved in lipid metabolism in the liver (Hui et al., 2013).”
BackgroundInfluential
Fetuin-A: the missing link in lipid-induced inflammation
Heinrichsdorff, J., & Olefsky, J. M. (2012) · Nature Medicine · doi:10.1038/nm.2869 · Cited by 76 · cited 1× · see citing works
“…that both disorders are characterized by an increased tendency to develop an earlier atherosclerotic process than in the general population, and the results of the recent studies indicate that NAFLD is an independent factor associated with the progression of atherosclerosis (Targher et al., 2010).”
Result
A Synonymous Coding Polymorphism in the α2-Heremans-Schmid Glycoprotein Gene Is Associated With Type 2 Diabetes in French Caucasians
Siddiq, A., Leprêtre, F., Herçberg, S., Froguel, P., & Gibson, F. (2005) · Diabetes · doi:10.2337/diabetes.54.8.2477 · Cited by 75 · cited 1× · see citing works
“In humans, fetuin-A gene is located on chromosome 3q27, which was identified as susceptibility locus for type 2 diabetes and metabolic syndrome (Siddiq et al., 2005).”
Background
Fetuin‐A negatively correlates with liver and vascular fibrosis in nonalcoholic fatty liver disease subjects
Sato, M., Kamada, Y., Takeda, Y., Kida, S., Ohara, Y., Fujii, H., Akita, M., Mizutani, K., Yoshida, Y., Yamada, M., et al. (2014) · Liver International · doi:10.1111/liv.12478 · Cited by 72 · cited 8× · see citing works
“In the studies conducted on patients with NAFLD, it was confirmed that circulating FGF-21 was significantly positively correlated with the hepatic fat content assessed in proton magnetic resonance spectroscopy (Yan et al., 2011), MRI (HFF”
BackgroundResultInfluential
Fibroblast Growth Factor 21 Analogs for Treating Metabolic Disorders
Zhang, J., & Li, Y. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00168 · Cited by 70 · cited 1× · see citing works
“…non-alcoholic fatty liver disease, fetuin-A, fibroblast growth factor-21, selenoprotein P, sex hormone-binding globulin, angiopoietin-related growth factor, leukocyte derived chemotaxin 2 Received: 19 January, 2016; revised: 10 May, 2016; accepted: 18 May, 2016; available on-line: 6 June, 2016”
Fibroblast growth factor 21: a novel metabolic regulator from pharmacology to physiology
Li, H., Zhang, J., & Jia, W. (2013) · Frontiers of Medicine · doi:10.1007/s11684-013-0244-8 · Cited by 69 · cited 2× · see citing works
“The study of Li et al. (2013) suggested that high level of serum FGF-21 may be considered to be an independent predictor of NAFLD.”
Background
Fetuin-A is linked to improved glucose tolerance after short-term exercise training in nonalcoholic fatty liver disease
Malin, S. K., Mulya, A., Fealy, C. E., Haus, J. M., Pagadala, M. R., Scelsi, A. R., Huang, H., Flask, C. A., McCullough, A. J., & Kirwan, J. P. (2013) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00237.2013 · Cited by 68 · cited 5× · see citing works
“It was also shown that even short–term, 7-day lasting physical exercise, brought a positive response in lowering the serum concentration of this hepatokine despite the fact, that there was no effect on body weight or hepatic triglyceride content in proton MRI (Malin et al., 2013).”
BackgroundInfluential
Sex Hormone–Binding Globulin and Risk of Type 2 Diabetes
Stefan, N., Schick, F., & Häring, H.-U. (2009) · New England Journal of Medicine · doi:10.1056/nejmc0910143 · Cited by 66 · cited 2× · see citing works
“In addition, it was also shown that serum concentrations of SHBG decreased with an increase of intrahepatic fat content and that introduction of lifestyle modification as a therapy for obesity caused an increase in circulating concentration of SHBG, which was associated with a decrease of liver fat content (Stefan et…”
Background
High Glucose Induces Transactivation of the .ALPHA.2-HS Glycoprotein Gene Through the ERK1/2 Signaling Pathway
Takata, H., Ikeda, Y., Suehiro, T., Ishibashi, A., Inoue, M., Kumon, Y., & Terada, Y. (2009) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.no950 · Cited by 66 · see citing works
Low serum sex hormone‐binding globulin is associated with nonalcoholic fatty liver disease in type 2 diabetic patients
Hua, X., Sun, Y., Zhong, Y., Feng, W., Huang, H., Wang, W., Zhang, T., & Hu, Y. (2013) · Clinical Endocrinology · doi:10.1111/cen.12360 · Cited by 65 · cited 1× · see citing works
“Similarly, the association of low concentration of this hepatokine with NAFLD was also demonstrated in type 2 diabetic patients (Hua et al., 2014).”
Background
Serum fetuin A/ α 2HS-glycoprotein levels in patients with non-alcoholic fatty liver disease: relation with liver fibrosis
Yilmaz, Y. N., Yönal, O., Kurt, R., Arı, F., Oral, A. Y., Çelikel, Ç., KORKMAZ, Ş., Ulukaya, E., Ozdogan, O. C., İmeryüz, N., et al. (2010) · Annals of Clinical Biochemistry International Journal of Laboratory Medicine · doi:10.1258/acb.2010.010169 · Cited by 64 · cited 3× · see citing works
“It should be emphasized that NAFLD was diagnosed on the basis of different diagnostic criteria (ultrasound, MRI and liver biopsy) ( Li et al., 2010; Yilmaz et al., 2010; Reinehr et al., 2012; Giannini et al., 2013).”
BackgroundResult
Nonalcoholic fatty liver disease and atherosclerosis
Gaudio, E., Nobili, V., Franchitto, A., Onori, P., & Carpino, G. (2012) · Internal and Emergency Medicine · doi:10.1007/s11739-012-0826-5 · Cited by 62 · cited 1× · see citing works
“Therefore, NAFLD is considered as a specific manifestation of the metabolic syndrome (Targher et al., 2010; Pacifico et al., 2011; Gaudio et al., 2012).”
Background
Serum sex hormone-binding globulin levels are independently associated with nonalcoholic fatty liver disease in people with type 2 diabetes
Shin, J. Y., Kim, S., Lee, M. Y., Kim, H. S., Ye, B. I., Shin, Y. G., Baik, S. K., & Chung, C. H. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2011.07.029 · Cited by 59 · cited 2× · see citing works
“…relationship between SHBG and intrahepatic fat content was confirmed in different groups of patients where liver steatosis was assessed using ultrasound (Shin et al., 2011; Fletcher-Mors et al., 2014), MRI (Bonnet et al., 2013) or computed tomography (Kavanagh et al., 2013; Lazo et al., 2015).”
Background
Adipokines and Redox Signaling: Impact on Fatty Liver Disease
Parola, M., & Marra, F. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2010.3848 · Cited by 59 · see citing works
Sex steroids and sex hormone-binding globulin in postmenopausal women with nonalcoholic fatty liver disease
Polyzos, S., Kountouras, J., Tsatsoulis, A., Zafeiriadou, E., Katsiki, E., Patsiaoura, K., Zavos, C., Anastasiadou, V., & Slavakis, A. (2013) · HORMONES · doi:10.1007/bf03401306 · Cited by 59 · cited 1× · see citing works
“In postmenopausal women with biopsy-proven NAFLD (Polyzos et al., 2013), there was lower concentration of this hepatokine detected compared to the control group and it was found that the serum concentration of SHBG was associated with NAFLD regardless of age, BMI and waist circumference.”
Background
Increased serum leukocyte cell-derived chemotaxin 2 (LECT2) levels in obesity and fatty liver
Okumura, A. (2013) · BioScience Trends · doi:10.5582/bst.2013.v7.6.276 · Cited by 57 · cited 2× · see citing works
“Okumura et al. (2013) reported that serum LECT2 level was significantly higher in patients with obesity and NAFLD.”
Background
Liver Transplantation in Nonalcoholic Steatohepatitis Is Associated with High Mortality and Post-Transplant Complications: A Single-Center Experience
Heuer, M., Kaiser, G. M., Kahraman, A., Banysch, M., Saner, F. H., Máthé, Z., Gerken, G., Paul, A., Canbay, A. E., & Treckmann, J. W. (2012) · Digestion · doi:10.1159/000339344 · Cited by 56 · cited 2× · see citing works
“In some cases, patients with NAFLD and advanced liver cirrhosis require liver transplantation (Burke et al., 2004; Heuer et al., 2012).”
Background
Fetuin-A mRNA expression is elevated in NASH compared with NAFL patients
Kahraman, A., Sowa, J., Schlattjan, M., Sydor, S., Pronadl, M., Wree, A., Beilfuss, A., Kılıçarslan, A., Altınbaş, A., Bechmann, L. P., et al. (2013) · Clinical Science · doi:10.1042/cs20120542 · Cited by 56 · cited 3× · see citing works
“It was demonstrated that fetuin-A mRNA expression was higher in NASH compared to patients with simple fatty liver (Kahraman et al., 2013).”
BackgroundResult
Serum levels of angiopoietin-related growth factor are increased in metabolic syndrome
Namkung, J., Koh, S. B., Kong, I. D., Choi, J.-W., & Yeh, B.-I. (2010) · Metabolism · doi:10.1016/j.metabol.2010.05.013 · Cited by 54 · cited 3× · see citing works
“Namkung et al. (2011) suggested that the function of AGF may be different in humans than in animals.”
Background
The effects of fibroblast growth factor-21 knockdown and over-expression on its signaling pathway and glucose–lipid metabolism in vitro
Li, K., Li, L., Yang, M., Liu, H., Boden, G. H., & Yang, G. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.07.026 · Cited by 54 · cited 2× · see citing works
“FGF-21 directly regulates lipid metabolism and reduces hepatic lipid accumulation in an insulin-independent manner (Zhang et al., 2011; Li et al., 2012; Lee et al., 2014).”
BackgroundInfluential
Modulating fibroblast growth factor 21 in hyperphagic OLETF rats with daily exercise and caloric restriction
Fletcher, J. A., Meers, G. M.-E., Laughlin, M. H., Ibdah, J. A., Thyfault, J. P., & Rector, R. S. (2012) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/h2012-091 · Cited by 53 · cited 1× · see citing works
“It was demonstrated by studying OLEFT rats that lifestyle modification (chronic exercise and caloric restriction) reduces hepatic expression of FGF-21 mRNA and circulating FGF-21 concentrations, which may indicate that such therapy alleviate FGF-21 resistance (Fletcher et al., 2012).”
Background
Exendin-4 regulates lipid metabolism and fibroblast growth factor 21 in hepatic steatosis
Lee, J., Hong, S., Park, S. E., Rhee, E., Park, C., Oh, K.-W., Park, S. W., & Lee, W. (2014) · Metabolism · doi:10.1016/j.metabol.2014.04.011 · Cited by 53 · cited 2× · see citing works
“FGF-21 directly regulates lipid metabolism and reduces hepatic lipid accumulation in an insulin-independent manner (Zhang et al., 2011; Li et al., 2012; Lee et al., 2014).”
BackgroundInfluential
Serum levels of angiopoietin-related growth factor in diabetes mellitus and chronic hemodialysis
Ebert, T., Bachmann, A., Lössner, U., Kratzsch, J., Blüher, M., Stümvoll, M., & Faßhauer, M. (2009) · Metabolism · doi:10.1016/j.metabol.2008.11.016 · Cited by 51 · cited 1× · see citing works
“However, Ebert et al. (2009) showed that serum AGF concentration is significantly increased in diabetic compared with non-diabetic patients.”
Background
Liver fat and SHBG affect insulin resistance in midlife women: The Study of Women's Health Across the Nation (SWAN)
Kavanagh, K., Espeland, M. A., Sutton‐Tyrrell, K., Barinas‐Mitchell, E., Khoudary, S. R. E., & Wildman, R. P. (2013) · Obesity · doi:10.1002/oby.20077 · Cited by 44 · cited 2× · see citing works
“…relationship between SHBG and intrahepatic fat content was confirmed in different groups of patients where liver steatosis was assessed using ultrasound (Shin et al., 2011; Fletcher-Mors et al., 2014), MRI (Bonnet et al., 2013) or computed tomography (Kavanagh et al., 2013; Lazo et al., 2015).”
Background
Angiopoietin-Related Growth Factor Suppresses Gluconeogenesis through the Akt/Forkhead Box Class O1-Dependent Pathway in Hepatocytes
Kitazawa, M., Ohizumi, Y., Oike, Y., Hishinuma, T., & Hashimoto, S. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.127530 · Cited by 44 · cited 17× · see citing works
“Namkung et al. (2011) suggested that the function of AGF may be different in humans than in animals.”
BackgroundInfluential
Associations of Fatty Liver Disease and Other Factors Affecting Serum SHBG Concentrations: A Population Based Study on 1657 Subjects
Flechtner-Mors, M., Schick, A., Oeztuerk, S., Haenle, M., Wilhelm, M., Koenig, W., Imhof, A., Boehm, B. O., Graeter, T., Mason, R., et al. (2013) · Hormone and Metabolic Research · doi:10.1055/s-0033-1354369 · Cited by 42 · cited 2× · see citing works
“In our preliminary study serum FGF-21 level was significantly higher in children with NAFLD (diagnosed in ultrasound and 1HMRS) compared to the controls and to the non-hepatopathic obese patients (Lebensztejn et al., 2016).”
Result
Visceral obesity modulates the impact of apolipoprotein C3 gene variants on liver fat content
Peter, A., Kantartzis, K., Machicao, F. E., Machann, J., Wagner, S., Templin, S., Königsrainer, I., Königsrainer, A., Schick, F., Fritsche, A., et al. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.154 · Cited by 36 · cited 1× · see citing works
“Moreover, APOC3 mRNA which is increased in fatty liver is regulated by single nucleotide polymorphisms in APOC3 and its influence depends on visceral obesity (Peter et al., 2012).”
Background
Serum Fetuin-A, Cardiovascular Risk Factors, and Six-Year Follow-up Outcome in Patients With Coronary Heart Disease
Roos, M., von Eynatten, M., Heemann, U. W., Rothenbacher, D., Brenner, H., & Breitling, L. P. (2010) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2010.01.342 · Cited by 35 · cited 1× · see citing works
“It is also considered as a biomarker for neurodegenerative diseases as well as indicator of insulin resistance, cardiovascular risk, endothelial dysfunction and subclinical atherosclerosis (Stefan et al., 2006; Roos et al., 2010; Mori et al., 2011; Mori et al., 2012; Dogru et al., 2013).”
Background
Apolipoprotein C3 Gene Variants in Nonalcoholic Fatty Liver Disease
Richart, C., Auguet, T., & Terra, X. (2010) · New England Journal of Medicine · doi:10.1056/nejmc1005265 · Cited by 29 · cited 1× · see citing works
“The consequence of this is the inhibition of lipoprotein lipase activity and impaired chylomicrons clearance (Petersen et al., 2010).”
Background
Relationship Between Serum Levels of Angiopoietin-Related Growth Factor and Metabolic Risk Factors
Ebert, T., Kralisch, S., Loessner, U., et al. (2014) · Hormone and Metabolic Research · doi:10.1055/s-0034-1382078 · Cited by 28 · cited 1×
“In the further study conducted by these authors, in a large, well- metabolically characterized cohort (Ebert et al., 2014), patients with type 2 diabetes had significantly higher serum AGF concentration in comparison to controls.”
Result
Serum fetuin A concentration is elevated in children with non-alcoholic fatty liver disease
Lebensztejn, D. M., Białokoz‐Kalinowska, I., Kłusek-Oksiuta, M., Tarasów, E., Wojtkowska, M., & Kaczmarski, M. G. (2014) · Advances in Medical Sciences · doi:10.1016/j.advms.2013.08.003 · Cited by 25 · cited 4× · see citing works
“In our study (Lebensztejn et al., 2014) the correlation of this glycoprotein with HOMA-IR and lipid profile parameters in patients with NAFLD was not confirmed.”
BackgroundInfluentialSelf-citation
Human selenoprotein P gene maps to 5q31.
Hill, K., Dasouki, M. J., Phillips, J. A., et al. (1996) · Genomics · doi:10.1006/geno.1996.0505 · Cited by 18 · cited 2×
“This glycoprotein was discovered in 1944 in bovine calves (Pedersen, 1944).”
Background
The Single Nucleotide Polymorphism rs499765 Is Associated with Fibroblast Growth Factor 21 and Nonalcoholic Fatty Liver Disease in a Chinese Population with Normal Glucose Tolerance
Jiang, S., Zhang, R., Li, H., Fang, Q., Jiang, F., Hou, X., Hu, C., & Jia, W. (2014) · Lifestyle Genomics · doi:10.1159/000367943 · Cited by 16 · cited 2× · see citing works
“Moreover, Jiang et al. (2014) confirmed that the single nucleotide polymorphism rs499765 is associated with FGF-21 and NAFLD in non-diabetic population.”
Background

Flagged first, then by citations

9 of the 122 references couldn’t be matched to a known paper.

Sorted by citations

Mechanisms and disease consequences of nonalcoholic fatty liver disease
Loomba, R., Friedman, S. L., & Shulman, G. I. (2021) · Cell · doi:10.1016/j.cell.2021.04.015 · Cited by 2,002 · see citing works
Triggering and resolution of inflammation in NASH
Schuster, S., Cabrera, D., Arrese, M., & Feldstein, A. E. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0009-6 · Cited by 943 · see citing works
Impaired adipogenesis and dysfunctional adipose tissue in human hypertrophic obesity
Hammarstedt, A., Gogg, S., Hedjazifar, S., Nerstedt, A., & Smith, U. (2018) · Physiological Reviews · doi:10.1152/physrev.00034.2017 · Cited by 462 · see citing works
Extracellular Matrix Remodeling of Adipose Tissue in Obesity and Metabolic Diseases
Ruiz‐Ojeda, F. J., Méndez-Gutiérrez, A., Aguilera, C. M., & Plaza‐Díaz, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194888 · Cited by 305 · see citing works
Sweet Sixteenth for ChREBP: Established Roles and Future Goals
Abdul-Wahed, A., Guilmeau, S., & Postic, C. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.07.004 · Cited by 231 · see citing works
“This was named the glucose-sensing module (GSM), also known as mondo conserved region (MCR), composed of a low-glucose inhibitory domain (LID) and a transactivation domain called glucose-response activation conserved element (GRACE) (Singh and Irwin, 2016) (Li et al., 2006) (Figure 1).”
Background
Adipokines, Myokines, and Hepatokines: Crosstalk and Metabolic Repercussions
de Oliveira dos Santos, A. R., de Oliveira Zanuso, B., Miola, V. F. B., Barbalho, S. M., Santos Bueno, P. C., Flato, U. A. P., Detregiachi, C. R. P., Buchaim, D. V., Buchaim, R. L., Tofano, R. J., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052639 · Cited by 189 · see citing works
NAFLD, and cardiovascular and cardiac diseases: Factors influencing risk, prediction and treatment
Targher, G., Corey, K. E., & Byrne, C. D. (2020) · Diabetes & Metabolism · doi:10.1016/j.diabet.2020.101215 · Cited by 170 · see citing works
New insight into inter-organ crosstalk contributing to the pathogenesis of non-alcoholic fatty liver disease (NAFLD)
Zhang, X., Ji, X., Wang, Q., & Li, J. Z. (2017) · Protein & Cell · doi:10.1007/s13238-017-0436-0 · Cited by 131 · see citing works
Non-alcoholic fatty liver disease in the first trimester and subsequent development of gestational diabetes mellitus
Lee, S. M., Kwak, S. H., Koo, J. N., Oh, I. H., Kwon, J. E., Kim, B. J., Kim, S. M., Kim, S. Y., Kim, G. M., Joo, S. K., et al. (2018) · Diabetologia · doi:10.1007/s00125-018-4779-8 · Cited by 121 · see citing works
Pathogenesis of Nonalcoholic Steatohepatitis: Interactions between Liver Parenchymal and Nonparenchymal Cells
Magee, N. S., Zou, A., & Zhang, Y. (2016) · BioMed Research International · doi:10.1155/2016/5170402 · Cited by 108 · see citing works
“For example, inflammation, which occurs in NASH patients and in animal models of human NASH, is induced by various mediators including endotoxins, adipokines, inflammatory cytokines, chemokines, and other inflammatory mediators [14].”
Background
Periodontitis changes renal structures by oxidative stress and lipid peroxidation
França, L. F. D. C., Vasconcelos, A. C. C. G., da Silva, F. R. P., Alves, E. H. P., Carvalho, J. D. S., Lenardo, D. D., de Souza, L. K. M., Barbosa, A. L. D. R., Medeiros, J. V. R., de Oliveira, J. S., et al. (2017) · Journal Of Clinical Periodontology · doi:10.1111/jcpe.12729 · Cited by 91 · see citing works
Melatonin improves insulin resistance and hepatic steatosis through attenuation of alpha‐2‐ HS ‐glycoprotein
Heo, J., Yoon, D. W., Yu, J. H., Kim, N. H., Yoo, H. J., Seo, J. A., Kim, S. G., Choi, K. M., Baik, S. H., Choi, D. S., et al. (2018) · Journal of Pineal Research · doi:10.1111/jpi.12493 · Cited by 80 · see citing works
Obesity, non-alcoholic fatty liver disease and hepatocellular carcinoma: current status and therapeutic targets
Chen, Y.-S., Wang, W., Morgan, M., Robson, T., & Annett, S. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1148934 · Cited by 63 · see citing works
“Hepatokines may be considered biomarkers of ectopic fat accumulation in the liver and markers of the disease progression, some of them may be the target for the prevention and treatment of IR and HCC (113, 115).”
Background
Sex Differences in Nonalcoholic Fatty Liver Disease: Estrogen Influence on the Liver–Adipose Tissue Crosstalk
Morán-Costoya, A., Proenza, A. M., Gianotti, M., Lladó, I., & Valle, A. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0044 · Cited by 58 · see citing works
“The Hepatokines Fibroblast Growth Factor 21, Retinol-Binding Protein 4, and Angiopoietin-like Protein 3 The liver has been shown to affect the lipids and glucose metabolism by hepatokines released into the blood, and NAFLD seems to be associated with altered hepatokines production (107).”
Multiple organs involved in the pathogenesis of non-alcoholic fatty liver disease
Li, X., & Wang, H. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-00507-y · Cited by 46 · see citing works
Protection against nonalcoholic steatohepatitis through targeting IL-18 and IL-1alpha by luteolin
Abu‐Elsaad, N., & El-Karef, A. (2019) · Pharmacological Reports · doi:10.1016/j.pharep.2019.03.009 · Cited by 54 · see citing works
A systematic review of the present and future of non-alcoholic fatty liver disease
Lucas, C., Lucas, G., Lucas, N., Krzowska-Firych, J., & Tomasiewicz, K. (2018) · Clinical and Experimental Hepatology · doi:10.5114/ceh.2018.78120 · Cited by 52 · see citing works
“Fetuin-A is a biomarker of NAFLD, and is increased in NAFLD patients, this hepatokine suppresses the autophosphorylation of insulin receptors in the skeletal muscles and liver, as well as promoting inflammatory cytokines in monocytes and adipocytes whilst simultaneously activating Toll-like receptors (TLRs) 4 [11].”
Background
Non-Alcoholic Steatohepatitis (NASH) and Organokines: What Is Now and What Will Be in the Future
dos Santos, J. P. M., de Maio, M. C., Lemes, M. A., Laurindo, L. F., Haber, J. F. D. S., Bechara, M. D., do Prado, P. S., Rauen, E. C., Costa, F., Pereira, B. C. D. A., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23010498 · Cited by 47 · see citing works
Role of hepatokines in non-alcoholic fatty liver disease
Ke, Y., Xu, C., Lin, J., & Li, Y. (2019) · Journal of Translational Internal Medicine · doi:10.2478/jtim-2019-0029 · Cited by 46 · see citing works
“In the recent decades, accumulating evidence revealed that liver may modulate the processes of NAFLD and other metabolic co-morbidities by secreting hepatokines, including fetuin-A, angiopoietin-related growth factor (AGF), fibrosis growth factor 21 (FGF 21), insulin-like growth factors (IGF), selenoprotein P (SeP), l…”
Background
NADPH Oxidases Connecting Fatty Liver Disease, Insulin Resistance and Type 2 Diabetes: Current Knowledge and Therapeutic Outlook
Nascè, A., Gariani, K., Jornayvaz, F. R., & Szántó, I. (2022) · Antioxidants · doi:10.3390/antiox11061131 · Cited by 46 · see citing works
MANAGEMENT OF ENDOCRINE DISEASE: Non-alcoholic fatty liver disease: a multidisciplinary approach towards a cardiometabolic liver disease
Ruissen, M. M., Mak, A. L., Beuers, U. H., Tushuizen, M. E., & Holleboom, A. G. (2020) · European Journal of Endocrinology · doi:10.1530/eje-20-0065 · Cited by 43 · see citing works
Baicalein Enhances the Effect of Acarbose on the Improvement of Nonalcoholic Fatty Liver Disease Associated with Prediabetes via the Inhibition of De Novo Lipogenesis
Xing, Y., Ren, X., Li, X., Sui, L., Shi, X., Sun, Y., Quan, C., Xiu, Z., & Dong, Y. (2021) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.1c04194 · Cited by 43 · see citing works
Targeting NFATc4 attenuates non-alcoholic steatohepatitis in mice
Du, M., Wang, X., Yuan, L., Liu, B., Mao, X., Huang, D., Yang, L., Huang, K., Zhang, F., Wang, Y., et al. (2020) · Journal of Hepatology · doi:10.1016/j.jhep.2020.07.030 · Cited by 41 · see citing works
Organ–Organ Crosstalk and Alcoholic Liver Disease
Poole, L. G., Dolin, C. E., & Arteel, G. E. (2017) · Biomolecules · doi:10.3390/biom7030062 · Cited by 42 · see citing works
“, fibroblast growth factor 21 (FGF21); [22,23]).”
Update on pathogenesis, diagnostics and therapy of nonalcoholic fatty liver disease in children
Flisiak‐Jackiewicz, M., & Lebensztejn, D. M. (2019) · Clinical and Experimental Hepatology · doi:10.5114/ceh.2019.83152 · Cited by 40 · see citing works
“[31] demonstrated that serum fetuin A concentration was significantly higher in children with NAFLD in comparison to the controls.”
ResultSelf-citation
Transabdominal ultrasonography of the pancreas is superior to that of the liver for detection of ectopic fat deposits resulting from metabolic syndrome
Li, S., Su, L., Lv, G., et al. (2017) · Medicine · doi:10.1097/md.0000000000008060 · Cited by 37 · see citing works
The effect of pomegranate extract on anthropometric indices, serum lipids, glycemic indicators, and blood pressure in patients with nonalcoholic fatty liver disease: A randomized double‐blind clinical trial
Goodarzi, R., Jafarirad, S., Mohammadtaghvaei, N., et al. (2021) · Phytotherapy Research · doi:10.1002/ptr.7249 · Cited by 35 · see citing works
Predictive Value of Adiposity Level, Metabolic Syndrome, and Insulin Resistance for the Risk of Nonalcoholic Fatty Liver Disease Diagnosis in Obese Children
Prokopowicz, Z., Małecka‐Tendera, E., & Matusik, P. (2018) · Canadian Journal of Gastroenterology and Hepatology · doi:10.1155/2018/9465784 · Cited by 34 · see citing works
“The pathogenesis of NAFLD and its progression are complex process, called multiplehit theory combining environmental (dietary habits, physical activity [3, 4]), molecular (lipotoxicity [5]), endoplasmic reticulum stress [6], mitochondrial dysfunction [7], organokines effect [8, 9], genetic (polymorphism involved in th…”
Background
Loss of liver-specific and sexually dimorphic gene expression by aryl hydrocarbon receptor activation in C57BL/6 mice
Nault, R., Fader, K. A., Harkema, J. R., & Zacharewski, T. R. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184842 · Cited by 31 · see citing works
Pediatric non-alcoholic fatty liver disease: current perspectives on diagnosis and management
Sessa, A. D., Cirillo, G., Guarino, S., et al. (2019) · Pediatric Health Medicine and Therapeutics · doi:10.2147/phmt.s188989 · Cited by 30 · see citing works
“To date, evidence submit your manuscript | www.dovepress.com DovePress Pediatric Health, Medicine and Therapeutics 2019:1090 supports MRI, MR Spectroscopy, proton MR spectroscopy (1H-MRS) and, in particular, proton density fat fraction (PDFF) as the most accurate noninvasive imaging tools for NAFLD detection, even in…”
BackgroundInfluential
Implication of the hepatokine, fibrinogen-like protein 1 in liver diseases, metabolic disorders and cancer: The need to harness its full potential
Liu, X.-H., Qi, L., Alolga, R. N., & Liu, Q. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.66834 · Cited by 28 · see citing works
“Hepatocytes secrete ~560 hepatokines, many of which affect metabolism both locally and in distant organs and are linked to the pathogenesis of metabolic diseases [20, 21].”
Background
SHBG as a Marker of NAFLD and Metabolic Impairments in Women Referred for Oligomenorrhea and/or Hirsutism and in Women With Sexual Dysfunction
Stasi, V. D., Maseroli, E., Rastrelli, G., Scavello, I., Cipriani, S., Todisco, T., Marchiani, S., Sorbi, F., Fambrini, M., Petraglia, F., et al. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.641446 · Cited by 28 · see citing works
“For this reason, in a clinical setting, having a single, rapid, and low cost marker, such as SHBG, can be the first “alarm bell” to deepen liver conditions in these patients (55, 68).”
Background
Long Non-Coding RNAs Involved in Progression of Non-Alcoholic Fatty Liver Disease to Steatohepatitis
Atanasovska, B., Rensen, S. S., Marsman, G., Shiri‐Sverdlov, R., Withoff, S., Kuipers, F., Wijmenga, C., van de Sluis, B., & Fu, J. (2021) · Cells · doi:10.3390/cells10081883 · Cited by 28 · see citing works
Non-Alcoholic Fatty Liver Disease in HIV/HBV Patients – a Metabolic Imbalance Aggravated by Antiretroviral Therapy and Perpetuated by the Hepatokine/Adipokine Axis Breakdown
Iacob, S. A., & Iacob, D. G. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.814209 · Cited by 28 · see citing works
Liver inflammation at the time of spinal cord injury enhances intraspinal pathology, liver injury, metabolic syndrome and locomotor deficits
Goodus, M. T., Carson, K. E., Sauerbeck, A. D., Dey, P., Alfredo, A. N., Popovich, P. G., Bruno, R. S., & McTigue, D. M. (2021) · Experimental Neurology · doi:10.1016/j.expneurol.2021.113725 · Cited by 26 · see citing works
Serum fetuin A level is associated with nonalcoholic fatty liver disease in Chinese population
Cui, Z., Xuan, R., & Yang, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.22361 · Cited by 25 · see citing works
“In previous basic scientific research, Fetuin A was demonstrated to induce IR and activated inflammatory response in NAFLD, indicating an adverse role in NAFLD [22].”
Background
Liver-lung axes in alcohol-related liver disease
Arteel, G. E. (2020) · Clinical and Molecular Hepatology · doi:10.3350/cmh.2020.0174 · Cited by 25 · see citing works
“, FGF21).(48,49) The net effect of these interactions is to generate an organ that rapidly responds to endocrine signals, as well as rapidly produces endocrine signals in response to stimuli.”
Background
Can hepatokines be regarded as novel non-invasive serum biomarkers of intrahepatic lipid content in obese children?
Flisiak‐Jackiewicz, M., Bobrus‐Chociej, A., Wasilewska, N., Tarasów, E., Wojtkowska, M., & Lebensztejn, D. M. (2019) · Advances in Medical Sciences · doi:10.1016/j.advms.2019.02.005 · Cited by 23 · see citing works
Self-citation
Leukocyte cell‐derived chemotaxin 2 promotes the development of nonalcoholic fatty liver disease through STAT‐1 pathway in mice
Wang, J., Chen, Y., Pan, R., Wu, C., Chen, S., Li, L., Li, Y., Yu, C., Meng, Z., & Xu, C. (2021) · Liver International · doi:10.1111/liv.14816 · Cited by 23 · see citing works
Noninvasive biomarkers in pediatric nonalcoholic fatty liver disease
Jayasekera, D. W., & Hartmann, P. (2023) · World Journal of Hepatology · doi:10.4254/wjh.v15.i5.609 · Cited by 22 · see citing works
The implication of hepatokines in metabolic syndrome
Esfahani, M., Baranchi, M., & Goodarzi, M. T. (2019) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2019.06.027 · Cited by 21 · see citing works
Fetuin-A – Alpha2-Heremans-Schmid Glycoprotein: From Structure to a Novel Marker of Chronic Diseases Part 1. Fetuin-A as a Calcium Chaperone and Inflammatory Marker
Komsa‐Penkova, R., Golemanov, G. M., Radionova, Z. V., Tonchev, P., Iliev, S. D., & Penkov, V. P. (2017) · Journal of Biomedical and Clinical Research · doi:10.1515/jbcr-2017-0015 · Cited by 20 · see citing works
The endocrine role of hepatokines: implications for human health and disease
Iglesias, P. (2025) · Frontiers in Endocrinology · doi:10.3389/fendo.2025.1663353 · Cited by 22 · see citing works
“On the other hand, certain hepatokines have been involved in the pathophysiology and progression of NAFLD and its advanced form, NASH.”
Influential
Deletion of Mcpip1 in Mcpip1fl/flAlbCre mice recapitulates the phenotype of human primary biliary cholangitis
Kotlinowski, J., Hutsch, T., Czyżyńska-Cichoń, I., Wadowska, M., Pydyn, N., Jasztal, A., Kij, A., Dobosz, E., Lech, M., Miękus, K., et al. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166086 · Cited by 19 · see citing works
Management of Diabetes Mellitus in Patients with Chronic Liver Diseases
Zhao, Y., Xing, H., Wang, X., Ou, W., Zhao, H., Li, B., Li, Y., Duan, Y., Zhuang, L., Li, W., et al. (2019) · Journal of Diabetes Research · doi:10.1155/2019/6430486 · Cited by 19 · see citing works
“In addition, the delivery of fetuin-A, fetuin-B, and selenoprotein P (SeP) into the blood has autocrine, paracrine and endocrine activities, which promote the development of atherosclerosis by regulating endothelial dysfunction and infiltrating inflammatory cells of the vessel wall, causing multiple metabolic disorder…”
Background
Engineered Probiotic and Prebiotic Nutraceutical Supplementations in Combating Non-communicable Disorders: A Review
Kerry, R. G., Das, G., Golla, U., Rodríguez-Torres, M. D. P., Shin, H., & Patra, J. K. (2020) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201021666201013153142 · Cited by 17 · see citing works
Carbonic anhydrase 3 increases during liver adipogenesis even in pre‐obesity, and its inhibitors reduce liver adipose accumulation
Yamamoto, H., Uramaru, N., Kawashima, A., et al. (2022) · FEBS Open Bio · doi:10.1002/2211-5463.13376 · Cited by 16 · see citing works
Antilipidemic and Hepatoprotective Effects of Ethanol Extract of Justicia spicigera in Streptozotocin Diabetic Rats
Murillo‐Villicaña, M., Noriega‐Cisneros, R., Peña‐Montes, D. J., Huerta‐Cervantes, M., Aguilera‐Méndez, A., Cortés‐Rojo, C., Salgado‐Garciglia, R., Montoya-Pérez, R. D. C., Riveros‐Rosas, H., & Saavedra‐Molina, A. (2022) · Nutrients · doi:10.3390/nu14091946 · Cited by 17 · see citing works
Crosstalk between the liver and kidney in diabetic nephropathy
Yang, M., Luo, S., Yang, J., Chen, W., He, L., Liu, D., Zhao, L., & Wang, X. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175219 · Cited by 17 · see citing works
Cardiac Hepatopathy: New Perspectives on Old Problems through a Prism of Endogenous Metabolic Regulations by Hepatokines
Berezin, A. A., Obradovic, Z., Berezina, T. A., Boxhammer, E., Lichtenauer, M., & Berezin, A. Е. (2023) · Antioxidants · doi:10.3390/antiox12020516 · Cited by 17 · see citing works
Hepatokine Profile in Adolescents with Polycystic Ovary Syndrome: A Case–Control Study
Giannouli, A., Stefanaki, C., Kouskoutis, C., Konidari, M., Mani, I., Konidari, K., Markantonis, S. L., Mantzou, A., Dourakis, S. P., Deligeoroglou, E., et al. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12175744 · Cited by 15 · see citing works
Higher Serum Selenoprotein P Level as a Novel Inductor of Metabolic Complications in Psoriasis
Baran, A. M., Nowowiejska, J., Krahel, J. A., Kaminski, T. W., Maciaszek, M., & Flisiak, I. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21134594 · Cited by 13 · see citing works
“NAFLD, nowadays reported as the main cause of chronic liver disease in developed countries, affects up to half of the persons with psoriasis [24].”
Background
Estimation of gamma-glutamyl transferase as a suitable simple biomarker of the cardiovascular risk in children with non-alcoholic fatty liver disease
Bobrus‐Chociej, A., Flisiak‐Jackiewicz, M., Daniluk, U., et al. (2018) · Acta Biochimica Polonica · doi:10.18388/abp.2018_2611 · Cited by 12 · see citing works
Self-citation
The role of chemerin in the pathogenesis of cholelithiasis in children and adolescents
Zdanowicz, K., Ryzko, J., Bobrus‐Chociej, A., et al. (2020) · Journal of Paediatrics and Child Health · doi:10.1111/jpc.15223 · Cited by 12 · see citing works
Self-citation
Contribution of organokines in the development of NAFLD/NASH associated hepatocellular carcinoma
Vachher, M., Bansal, S., Kumar, B., Yadav, S., Arora, T. K., Wali, N. M., & Burman, A. (2022) · Journal of Cellular Biochemistry · doi:10.1002/jcb.30252 · Cited by 11 · see citing works
Binge drinking leads to an oxidative and metabolic imbalance in skeletal muscle during adolescence in rats: endocrine repercussion
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Authors: Lebensztejn, D. M., Flisiak-Jackiewicz, M., Białokoz-Kalinowska, I., Bobrus-Chociej, A., & Kowalska, I.
Affiliations: Medical University of Białystok (PL)
Department of Pediatrics, Gastroenterology and Allergology, Medical University of Bialystok, Poland
Medical Institute, Lomza State University of Applied Sciences, Poland
ORCID: Lebensztejn, Dariusz M.
Kowalska, Irina
Venue: Acta Biochimica Polonica
Publisher: Frontiers Media SA
Published: 2016
Volume: 63
Issue: 3
Pages: 459-467
ISSN: 0001-527X (ISSN-L)
1734-154X
DOI: 10.18388/abp.2016_1252
OpenAlex: W4253038549
Cited by: 90
References: 122
Citations by year: 2026: 2 · 2025: 2 · 2024: 4 · 2023: 11 · 2022: 13 · 2021: 17 · 2020: 9 · 2019: 13 · 2018: 9 · 2017: 9 · 2016: 1
FWCI: 9.94
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by-sa
Locations: Acta Biochimica Polonica (publishedVersion, cc-by-sa)
Acta Biochimica Polonica (publishedVersion, cc-by)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
Health Sciences › Medicine › Epidemiology › Adipokines, Inflammation, and Metabolic Diseases
Health Sciences › Medicine › Hepatology › Liver physiology and pathology
Keywords: hepatokines, non-alcoholic fatty liver disease, nonalcoholic steatohepatitis, metabolic syndrome, fetuin-A, FGF21, selenoprotein P, sex hormone-binding globulin, LECT2, insulin resistance, visceral obesity, dyslipidemia, liver fibrosis
MeSH terms: Animals, Fibroblast Growth Factors, Humans, Liver, Sex Hormone-Binding Globulin, Signal Transduction, Intercellular Signaling Peptides and Proteins, Selenoprotein P, alpha-2-HS-Glycoprotein, Non-alcoholic Fatty Liver Disease

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Hepatokines and non-alcoholic fatty liver disease

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