Maternal obesity programs offspring nonalcoholic fatty liver disease by innate immune dysfunction in mice
Open accessAbstract
The global prevalence of obesity-induced liver disease (nonalcoholic fatty liver disease; NAFLD) is rising. Suggested causes include a role for in utero influences of maternal obesity compounded by the availability of energy-dense foods throughout postnatal life. Using a physiologically relevant model, we investigated the role of the innate immune system in liver injury induced by maternal obesity followed by a postnatal obesogenic diet. Female C57BL/6J mice were fed a standard or obesogenic diet before and throughout pregnancy and during lactation. Female offspring were weaned onto a standard or obesogenic diet at 3 weeks postpartum. Biochemical and histological indicators of dysmetabolism, NAFLD and fibrosis, analysis of profibrotic pathways, liver innate immune cells, and reactive oxygen species (ROS) were investigated at 3, 6, and 12 months. Female offspring exposed to a postweaning obesogenic diet (OffCon-OD) demonstrated evidence of liver injury, which was exacerbated by previous exposure to maternal obesity (OffOb-OD), as demonstrated by raised alanine aminotransferase, hepatic triglycerides, and hepatic expression of interleukin (IL)-6, tumor necrosis factor alpha, transforming growth factor beta, alpha smooth muscle actin, and collagen (P < 0.01). Histological evidence of hepatosteatosis and a more-robust NAFLD phenotype with hepatic fibrosis was observed at 12 months in OffOb-OD. A role for the innate immune system was indicated by increased Kupffer cell numbers with impaired phagocytic function and raised ROS synthesis (P < 0.01), together with reduced natural killer T cells and raised interleukin (IL)-12 and IL-18. Conclusion: Maternal obesity in the context of a postnatal hypercalorific obesogenic diet aggressively programs offspring NAFLD associated with innate immune dysfunction, resulting in a comprehensive phenotype that accurately reflects the human disease. (HEPATOLOGY 2013)
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Maternal obesity induced hepatic steatosis in the offspring.
“a number of studies showed that maternal obesity induced greater adiposity and obesity [95,96,97,98] as well as hepatic steatosis [95,96,99] in the offspring.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [96]
The Results report that maternal obesity exacerbated hepatic fat accumulation in offspring fed a postweaning obesogenic diet. The Discussion also says offspring of obese dams weaned onto standard chow had similar hepatic triglyceride content and histological steatosis to controls. The claim omits this important postnatal-diet qualification. (LLM, conf=0.87)
Experimental — accuracy not yet measuredMaternal obesity induced greater adiposity and obesity in the offspring.
“a number of studies showed that maternal obesity induced greater adiposity and obesity [95,96,97,98] as well as hepatic steatosis [95,96,99] in the offspring.”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [96]
Several studies have reported hyperlipidemia in offspring of maternal obesity, including elevated free fatty acids, plasma triacylglycerol and reduced total and HDL cholesterol, though one study did not observe alterations in plasma lipids.
“Several of these studies have reported hyperlipidemia [96,100], including elevated free fatty acids, plasma triacylglycerol and reduced total and HDL cholesterol in the offspring, though one study did not observe alterations in plasma lipids [101].”
From Recent Experimental Studies of Maternal Obesity, Diabetes during Pregnancy and the Developmental Origins of Cardiovascular Disease (2022) · cites this paper as [96]
The citation to this paper is attached to the assertion that one study found no alterations in plasma lipids. The Materials and Methods section (page unavailable) says plasma was assayed for ALT, while triglycerides were measured in liver tissue. The Results and Discussion discuss hepatic triglycerides, not unchanged plasma lipids; searches for plasma lipid and cholesterol findings found no supporting passage. (LLM, conf=0.76)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A SIMPLE METHOD FOR THE ISOLATION AND PURIFICATION OF TOTAL LIPIDES FROM ANIMAL TISSUES
Folch, J., Lees, M., & Stanley, G. H. S. (1957) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)64849-5 · Cited by 65,189 · see citing works
Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010.
Flegal, K., Carroll, M., Kit, B., & Ogden, C. (2012) · Journal of the American Medical Association (JAMA) · doi:10.1001/jama.2012.39 · Cited by 5,523 · see citing works
Nonalcoholic Fatty Liver Disease
Angulo, P. (2002) · New England Journal of Medicine · doi:10.1056/nejmra011775 · Cited by 5,228 · see citing works
Steatohepatitis: A tale of two “hits”?
Day, C. P., & James, O. F. W. (1998) · Gastroenterology · doi:10.1016/s0016-5085(98)70599-2 · Cited by 4,285 · see citing works
Targher, G., Bertolini, L., Padovani, R., Rodella, S., Tessari, R., Zenari, L., Day, C. P., & Arcaro, G. (2007) · Diabetes Care · doi:10.2337/dc06-2247 · Cited by 990 · see citing works
Li, Z., Yang, S., Lin, H., Huang, J., Watkins, P. A., Moser, A. B., Desimone, C., Song, X.-Y., & Diehl, A. M. (2003) · Hepatology · doi:10.1053/jhep.2003.50048 · Cited by 930 · see citing works
Samuelsson, A.-M., Matthews, P. A., Argenton, M., Christie, M. R., McConnell, J. M., Jansen, E. H. J. M., Piersma, A. H., Ozanne, S. E., Twinn, D. F., Remacle, C., et al. (2008) · Hypertension · doi:10.1161/hypertensionaha.107.101477 · Cited by 923 · see citing works
Self-citationGut microbiome, obesity, and metabolic dysfunction
Tilg, H., & Kaser, A. (2011) · Journal of Clinical Investigation · doi:10.1172/jci58109 · Cited by 860 · see citing works
Rivera, C. A., Adegboyega, P., van Rooijen, N., Tagalicud, A., Allman, M., & Wallace, M. (2007) · Journal of Hepatology · doi:10.1016/j.jhep.2007.04.019 · Cited by 693 · see citing works
Perinatal risk factors for childhood obesity and metabolic dysregulation
Catalano, P. M., Farrell, K., Thomas, A., Huston-Presley, L., Mencin, P., de Mouzon, S. H., & Amini, S. B. (2009) · The American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.27416 · Cited by 553 · see citing works
The fetal and infant origins of disease
Barker, D. J. P. (1995) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.1995.tb01730.x · Cited by 530 · see citing works
Lipopolysaccharides in liver injury: molecular mechanisms of Kupffer cell activation
Su, G. L. (2002) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00550.2001 · Cited by 481 · see citing works
Kupffer cells in non-alcoholic fatty liver disease: The emerging view
Baffy, G. (2009) · Journal of Hepatology · doi:10.1016/j.jhep.2009.03.008 · Cited by 472 · see citing works
Bruce, K. D., Cagampang, F. R., Argenton, M., Zhang, J., Ethirajan, P. L., Burdge, G. C., Bateman, A. C., Clough, G. F., Poston, L., Hanson, M. A., et al. (2009) · Hepatology · doi:10.1002/hep.23205 · Cited by 449 · see citing works
Self-citationInnate and adaptive lymphoid cells in the human liver
Doherty, D. G., & O’Farrelly, C. (2000) · Immunological Reviews · doi:10.1034/j.1600-0528.2002.017416.x · Cited by 404 · see citing works
Oben, J. A., Mouralidarane, A., Samuelsson, A.-M., Matthews, P. J., Morgan, M. L., Mckee, C., Soeda, J., Fernandez-Twinn, D. S., Martin-Gronert, M. S., Ozanne, S. E., et al. (2010) · Journal of Hepatology · doi:10.1016/j.jhep.2009.12.042 · Cited by 314 · cited 5× · see citing works
“NAFLD in tandem with reduced hepatic insulin signalling and raised sympathetic tone.(3,16) We now demonstrate, using a more physiologically relevant and translational model, that the maternal and postnatal environments interact to exacerbate the progression of NAFLD.”
BackgroundMethodResultInfluentialSelf-citationDietary Factors Alter Hepatic Innate Immune System in Mice With Nonalcoholic Ratty Liver Disease * #
Li, Z., Soloski, M. J., & Diehl, A. M. (2005) · Hepatology · doi:10.1002/hep.20826 · Cited by 294 · see citing works
Maternal obesity, gestational weight gain and diet as determinants of offspring long term health.
Poston, L. (2012) · Best practice & research. Clinical endocrinology & metabolism · doi:10.1016/j.beem.2012.03.010 · Cited by 218 · see citing works
Self-citationGuebre‐Xabier, M., Yang, S., Lin, H. Z., Schwenk, R., Krzych, U., & Diehl, A. M. (2000) · Hepatology · doi:10.1002/hep.510310313 · Cited by 192 · see citing works
Non‐alcoholic steatohepatitis: Definitions and pathogenesis
Day, C., & SAKSENA, S. (2002) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.17.s3.31.x · Cited by 183 · see citing works
Kupffer Cell and Interleukin-12–Dependent Loss of Natural Killer T Cells in Hepatosteatosis
Kremer, M., Thomas, E., Milton, R. J., Perry, A. W., van Rooijen, N., Wheeler, M. D., Zacks, S., Fried, M., Rippe, R. A., & Hines, I. N. (2009) · Hepatology · doi:10.1002/hep.23292 · Cited by 156 · see citing works
Endotoxin and Kupffer cell activation in alcoholic liver disease.
Wheeler, M. D. (2003) · Europe PMC (PubMed Central) · Cited by 155 · see citing works
Bayol, S. A., Simbi, B. H., Fowkes, R. C., & Stickland, N. C. (2010) · Endocrinology · doi:10.1210/en.2009-1192 · Cited by 127 · see citing works
Wei, Y., Clark, S. E., Morris, E. M., Thyfault, J. P., Uptergrove, G. M., Whaley‐Connell, A. T., Ferrario, C. M., Sowers, J. R., & Ibdah, J. A. (2008) · Journal of Hepatology · doi:10.1016/j.jhep.2008.03.018 · Cited by 120 · see citing works
Critical role of Kupffer cells in the management of diet-induced diabetes and obesity
Neyrinck, A. M., Cani, P. D., Dewulf, E. M., Backer, F. D., Bindels, L. B., & Delzenne, N. M. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.05.070 · Cited by 113 · see citing works
Maternal over-nutrition and offspring obesity predisposition: targets for preventative interventions
Rooney, K. B., & Ozanne, S. E. (2011) · International Journal of Obesity · doi:10.1038/ijo.2011.96 · Cited by 103 · see citing works
Roles of liver innate immune cells in nonalcoholic fatty liver disease
Zhan, Y.-T. (2010) · World Journal of Gastroenterology · doi:10.3748/wjg.v16.i37.4652 · Cited by 97 · see citing works
Reactive oxygen species are essential mediators in antigen presentation by Kupffer cells
Maemura, K., Zheng, Q., Wada, T., Ozaki, M., Takao, S., Aikou, T., Bulkley, G. B., Klein, A. S., & Sun, Z. (2005) · Immunology and Cell Biology · doi:10.1111/j.1440-1711.2005.01323.x · Cited by 90 · see citing works
Pot, G. K., Prynne, C. J., Roberts, C., Olson, A. D., Nicholson, S. K., Whitton, C., Teucher, B., Bates, B., Henderson, H., Pigott, S., et al. (2011) · British Journal Of Nutrition · doi:10.1017/s0007114511002911 · Cited by 83 · see citing works
Asanuma, T., Ono, M., Kubota, K., Hirose, A., Hayashi, Y., Saibara, T., Inanami, O., Ogawa, Y., Enzan, H., Onishi, S., et al. (2009) · Gut · doi:10.1136/gut.2009.176651 · Cited by 72 · see citing works
Self-citationFostering in mice induces cardiovascular and metabolic dysfunction in adulthood
Matthews, P. A., Samuelsson, A., Seed, P. T., Pombo, J., Oben, J. A., Poston, L., & Taylor, P. D. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.212324 · Cited by 53 · see citing works
Self-citationElinav, E., Abd-Elnabi, A., Pappo, O., Bernstein, I., Klein, A., Engelhardt, D., Rabbani, E., & Ilan, Y. (2005) · Journal of Hepatology · doi:10.1016/j.jhep.2005.08.013 · Cited by 44 · see citing works
Practical management of the increasing burden of non-alcoholic fatty liver disease
Mouralidarane, A., Lin, C.-I., Suleyman, N., Soeda, J., & Oben, J. (2010) · Frontline Gastroenterology · doi:10.1136/fg.2009.000935 · Cited by 8 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Asanuma T, Ono M, Kubota K, Hirose A, Hayashi Y, Saibara T, et al. Super paramagnetic iron oxide MRI shows defective Kupffer cell uptake function in non-alcoholic fatty liver disease. Gut 2010;59: 258-266.
Cited by
Sorted by citations
The Role of the Immune System in Metabolic Health and Disease
Zmora, N., Bashiardes, S., Levy, M., & Elinav, E. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.02.006 · Cited by 323 · see citing works
The gut microbiota in infants of obese mothers increases inflammation and susceptibility to NAFLD
Soderborg, T. K., Clark, S. E., Mulligan, C. E., Janssen, R. C., Babcock, L. R., Ir, D., Young, B. E., Krebs, N. F., Lemas, D. J., Johnson, L. K., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06929-0 · Cited by 291 · see citing works
Endocrine-disrupting chemicals and fatty liver disease
Foulds, C., Treviño, L., York, B., & Walker, C. (2017) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2017.42 · Cited by 217 · see citing works
Zhang, X., Zhang, J.-H., Chen, X.-Y., Hu, Q., Wang, M., Jin, R., Zhang, Q., Wang, W., Wang, R., Kang, L.-L., et al. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2014.5868 · Cited by 239 · see citing works
Developmental origins of NAFLD: a womb with a clue
Wesolowski, S. R., Kasmi, K. C. E., Jonscher, K. R., & Friedman, J. E. (2016) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2016.160 · Cited by 231 · see citing works
Wankhade, U., Zhong, Y., Kang, P., Alfaro, M. P., Chintapalli, S., Thakali, K. M., & Shankar, K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0175675 · Cited by 167 · see citing works
A Guide to Non-Alcoholic Fatty Liver Disease in Childhood and Adolescence
Temple, J., Cordero, P., Li, J., Nguyen, V., & Oben, J. A. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17060947 · Cited by 171 · see citing works
Self-citationProgress and challenges in the prevention and control of nonalcoholic fatty liver disease
Cai, J., Zhang, X., & Li, H. (2018) · Medicinal Research Reviews · doi:10.1002/med.21515 · Cited by 159 · see citing works
Nonalcoholic Fatty Liver Disease in Children
Mann, J. P., Valenti, L. V. C., Scorletti, E., Byrne, C. D., & Nobili, V. (2018) · Seminars in Liver Disease · doi:10.1055/s-0038-1627456 · Cited by 161 · see citing works
Ullah, R., Rauf, N., Nabi, G., Ullah, H., Shen, Y., Zhou, Y., & Fu, J. (2019) · International Journal of Biological Sciences · doi:10.7150/ijbs.30121 · Cited by 157 · see citing works
Developmental origins of nonalcoholic fatty liver disease
Brumbaugh, D. E., & Friedman, J. E. (2013) · Pediatric Research · doi:10.1038/pr.2013.193 · Cited by 145 · see citing works
Alfaradhi, M. Z., Fernandez-Twinn, D. S., Martin-Gronert, M. S., Musial, B., Fowden, A., & Ozanne, S. E. (2014) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00049.2014 · Cited by 136 · see citing works
Maternal cholestasis during pregnancy programs metabolic disease in offspring
Papacleovoulou, G., Abu‐Hayyeh, S., Nikolopoulou, E., Briz, Ó., Owen, B. M., Nikolova, V., Ovadia, C., Huang, X. B., Vääräsmäki, M., Baumann, M. U., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci68927 · Cited by 129 · see citing works
Ayonrinde, O. T., Oddy, W. H., Adams, L. A., Mori, T. A., Beilin, L. J., de Klerk, N. H., & Olynyk, J. K. (2017) · Journal of Hepatology · doi:10.1016/j.jhep.2017.03.029 · Cited by 129 · see citing works
Afrin, R., Arumugam, S., Rahman, M. A., Wahed, M. I. I., Karuppagounder, V., Harima, M., Suzuki, H., Miyashita, S., Suzuki, K., Yoneyama, H., et al. (2017) · International Immunopharmacology · doi:10.1016/j.intimp.2017.01.016 · Cited by 122 · see citing works
Keleher, M. R., Zaidi, R., Shah, S., Oakley, M. E., Pavlatos, C., Idrissi, S. E., Xing, X., Li, D., Wang, T., & Cheverud, J. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0192606 · Cited by 122 · see citing works
Thorn, S. R., Baquero, K. C., Newsom, S., Kasmi, K. E., Bergman, B., Shulman, G., Grove, K., & Friedman, J. (2014) · Diabetes · doi:10.2337/db14-0276 · Cited by 109 · see citing works
Maternal obesity increases the risk and severity of NAFLD in offspring
Hagström, H., Simon, T. G., Roelstraete, B., Stephansson, O., Söderling, J. K., & Ludvigsson, J. F. (2021) · Journal of Hepatology · doi:10.1016/j.jhep.2021.06.045 · Cited by 118 · see citing works
Heerwagen, M. J. R., Stewart, M. S., de la Houssaye, B. A., Janssen, R. C., & Friedman, J. E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067791 · Cited by 111 · see citing works
García‐Martínez, R., Andreola, F., Mehta, G., Poulton, K., Oria, M., Jover‐Cobos, M., Soeda, J., Macnaughtan, J., Chiara, F. D., Habtesion, A., et al. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.10.031 · Cited by 106 · see citing works
Self-citationThe Obese Liver Environment Mediates Conversion of NK Cells to a Less Cytotoxic ILC1-Like Phenotype
Cuff, A. O., Sillito, F., Dertschnig, S., Hall, A., Luong, T., Chakraverty, R., & Male, V. (2019) · bioRxiv · doi:10.3389/fimmu.2019.02180 · Cited by 90 · see citing works
Wallace, J. G., Bellissimo, C. J., Yeo, E., Xia, Y. F., Petrik, J., Surette, M. G., Bowdish, D. M. E., & Sloboda, D. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-54098-x · Cited by 99 · see citing works
DNA Methylation in Nonalcoholic Fatty Liver Disease
Hyun, J., & Jung, Y. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218138 · Cited by 99 · see citing works
Jovicic, N. U., Jeftic, I. D., Jovanović, I., Radosavljevic, G. D., Arsenijević, N., Lukić, M. L., & Pejnovic, N. N. (2015) · PLoS ONE · doi:10.1371/journal.pone.0134089 · Cited by 97 · see citing works
Wankhade, U. D., Zhong, Y., Kang, P., Alfaro, M., Chintapalli, S. V., Piccolo, B. D., Mercer, K. E., Andres, A., Thakali, K. M., & Shankar, K. (2018) · Scientific Reports · doi:10.1038/s41598-018-34453-0 · Cited by 95 · see citing works
Lomas‐Soria, C., Reyes‐Castro, L. A., Rodríguez-González, G. L., Ibáñez, C. A., Bautista, C. J., Cox, L. A., Nathanielsz, P. W., & Zambrano, E. (2018) · The Journal of Physiology · doi:10.1113/jp276372 · Cited by 94 · see citing works
Maternal western diet primes non‐alcoholic fatty liver disease in adult mouse offspring
Pruis, M., Lendvai, Á., Bloks, V., Zwier, M., Baller, J., de Bruin, A., Groen, A. K., & Plösch, T. (2014) · Acta Physiologica · doi:10.1111/apha.12197 · Cited by 98 · see citing works
Kereliuk, S., Brawerman, G., & Dolinsky, V. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18071451 · Cited by 90 · see citing works
The effect of maternal Inflammation on foetal programming of metabolic disease
Ingvorsen, C., Brix, S., Ozanne, S. E., & Hellgren, L. (2015) · Acta Physiologica · doi:10.1111/apha.12533 · Cited by 80 · see citing works
Li, M.-L., Reynolds, C., Segovia, S., Gray, C., & Vickers, M. (2015) · BioMed Research International · doi:10.1155/2015/437107 · Cited by 74 · see citing works
Jonscher, K. R., Stewart, M. S., Alfonso-García, A., DeFelice, B. C., Wang, X.-X. X., Luo, Y., Levi, M., Heerwagen, M. J. R., Janssen, R., Houssaye, B. A., et al. (2017) · The FASEB Journal · doi:10.1096/fj.201600906r · Cited by 59 · see citing works
Patel, S., Lawlor, D., Callaway, M., Macdonald-Wallis, C., Sattar, N., & Fraser, A. (2016) · BMC Pediatrics · doi:10.1186/s12887-016-0585-y · Cited by 58 · see citing works
Non‐alcoholic fatty liver disease: the role of nuclear receptors and circadian rhythmicity
Mazzoccoli, G., Vinciguerra, M., Oben, J. A., Tarquini, R., & Cosmo, S. D. (2014) · Liver International · doi:10.1111/liv.12534 · Cited by 65 · see citing works
Self-citationMitochondrial role in the neonatal predisposition to developing nonalcoholic fatty liver disease
Baker, P. R., & Friedman, J. E. (2018) · Journal of Clinical Investigation · doi:10.1172/jci120846 · Cited by 61 · see citing works
Friedman, J. E., Dobrinskikh, E., Garcia, A. A., Fast, A., Janssen, R. C., Soderborg, T. K., Anderson, A. L., Reisz, J. A., D’Alessandro, A., Frank, D. N., et al. (2018) · Hepatology Communications · doi:10.1002/hep4.1139 · Cited by 59 · see citing works
Paul, H., Collins, K., Nicolucci, A. C., Urbanski, S., Hart, D. A., Vogel, H. J., & Reimer, R. A. (2019) · The FASEB Journal · doi:10.1096/fj.201801551r · Cited by 49 · see citing works
Pediatric Non-Alcoholic Fatty Liver Disease: Nutritional Origins and Potential Molecular Mechanisms
Mandala, A., Janssen, R., Palle, S. K., Short, K., & Friedman, J. (2020) · Nutrients · doi:10.3390/nu12103166 · Cited by 51 · see citing works
Perinatal exposure to maternal obesity: Lasting cardiometabolic impact on offspring
Kışlal, S., Shook, L. L., & Edlow, A. G. (2020) · Prenatal Diagnosis · doi:10.1002/pd.5784 · Cited by 59 · see citing works
Mouralidarane, A., Soeda, J., Sugden, D., Bocianowska‐Zbrog, A., Carter, R. M., Ray, S., Saraswati, R., Cordero, P., Novelli, M. R., Fusai, G., et al. (2015) · International Journal of Obesity · doi:10.1038/ijo.2015.85 · Cited by 55 · see citing works
Self-citationMcKee, C. M., Sigala, B., Soeda, J., Mouralidarane, A., Morgan, M. L., Mazzoccoli, G., Rappa, F., Cappello, F., Cabibi, D., Pazienza, V., et al. (2015) · Scientific Reports · doi:10.1038/srep08812 · Cited by 54 · see citing works
Self-citationThe Role of Vitamins in the Pathogenesis of Non-alcoholic Fatty Liver Disease
Li, J.-W., Cordero, P., Nguyen, V., & Oben, J. (2016) · Integrative Medicine Insights · doi:10.4137/imi.s31451 · Cited by 50 · see citing works
Self-citationNash, M. J., Dobrinskikh, E., Soderborg, T. K., Janssen, R. C., Takahashi, D. L., Dean, T. A., Varlamov, O., Hennebold, J. D., GANNON, M. A., Aagaard, K. M., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112393 · Cited by 52 · see citing works
Pereira, T. J., Gruber, B. L. M., Kereliuk, S. M., & Dolinsky, V. W. (2014) · Biochemistry and Cell Biology · doi:10.1139/bcb-2014-0141 · Cited by 51 · see citing works
Wesolowski, S. R., Mulligan, C., Janssen, R., Baker, P. R., Bergman, B., D'Alessandro, A., Nemkov, T., Maclean, K., Jiang, H., Dean, T., et al. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.09.008 · Cited by 45 · see citing works
Developmental Programming of NAFLD by Parental Obesity
Thompson, M. D. (2020) · Hepatology Communications · doi:10.1002/hep4.1578 · Cited by 47 · see citing works
Querter, I., Pauwels, N., Bruyne, R. D., Dupont, E., Verhelst, X., Devisscher, L., Vlierberghe, H. V., Geerts, A. M., & Lefere, S. (2021) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2021.04.014 · Cited by 47 · see citing works
Monks, J., Orlicky, D. J., Stefanski, A. L., Libby, A. E., Bales, E. S., Rudolph, M. C., Johnson, G. C., Sherk, V. D., Jackman, M. R., Williamson, K. M., et al. (2018) · Nutrition and Diabetes · doi:10.1038/s41387-018-0027-z · Cited by 44 · see citing works
Enhanced Steatosis and Fibrosis in Liver of Adult Offspring Exposed to Maternal High-Fat Diet
Thompson, M. D., Cismowski, M., Trask, A., Lallier, S. W., Graf, A. E., Rogers, L., Lucchesi, P., & Brigstock, D. (2016) · Gene Expression · doi:10.3727/105221616x692135 · Cited by 41 · see citing works
Impact of pregravid obesity on maternal and fetal immunity: Fertile grounds for reprogramming
Sureshchandra, S., Marshall, N., & Messaoudi, I. (2019) · Journal of Leukocyte Biology · doi:10.1002/jlb.3ri0619-181r · Cited by 38 · see citing works
Developmental Programming of Pediatric Non-Alcoholic Fatty Liver Disease: Redefining the ‘First-Hit’
Stewart, M. S., Heerwagen, M. J. R., & Friedman, J. (2013) · Clinical obstetrics and gynecology · doi:10.1097/grf.0b013e3182a09760 · Cited by 47 · see citing works
Miranda, R. A., de Almeida, M. M., Dias-Rocha, C. P., Fassarella, L. B., Souza, L. L., Souza, A. F. P., de Andrade, C. B. V., Fortunato, R. S., Pazos-Moura, C. C., & Trevenzoli, I. H. (2018) · Scientific Reports · doi:10.1038/s41598-018-32906-0 · Cited by 38 · see citing works
Nelson, B. N., & Friedman, J. E. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115951 · Cited by 36 · see citing works
Kereliuk, S. M., & Dolinsky, V. W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084467 · Cited by 34 · see citing works
“Using this approach, a number of studies showed that maternal obesity induced greater adiposity and obesity [95–98] as well as hepatic steatosis [95,96,99] in the offspring.”
BackgroundEarly life programming and the risk of non-alcoholic fatty liver disease
Lynch, C., Chan, C. S., & Drake, A. J. (2017) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174416000805 · Cited by 33 · see citing works
Thompson, M. D., Derse, A., Ferey, J. L. A., Reid, M., Xie, Y., Christ, M., Chatterjee, D., Nguyen, C., Harasymowicz, N. S., Guilak, F., et al. (2019) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00474.2018 · Cited by 32 · see citing works
Nutritional, pharmacological, and environmental programming of NAFLD in early life
Galvan-Martinez, D. H., Bosquez-Mendoza, V. M., Ruíz‐Noa, Y., Ibarra‐Reynoso, L. D. R., Barbosa‐Sabanero, G., & Lazo-de-la-Vega-Monroy, M.-L. (2022) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00168.2022 · Cited by 31 · see citing works
Manna, L. B., Papacleovoulou, G., Flaviani, F., Pataia, V., Qadri, A., Abu‐Hayyeh, S., McIlvride, S., Jansen, E. H. J. M., Dixon, P. H., Chambers, J. J. G., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-67301-1 · Cited by 30 · see citing works
Soeda, J., Cordero, P., Li, J.-W., Mouralidarane, A., Asilmaz, E., Ray, S., Nguyen, V., Carter, R., Novelli, M., Vinciguerra, M., et al. (2016) · International Journal of Food Science and Nutrition · doi:10.1080/09637486.2016.1261086 · Cited by 28 · see citing works
Self-citationCao, B., Liu, C., Zhang, Q., & Dong, Y. (2020) · Frontiers in Nutrition · doi:10.3389/fnut.2020.581723 · Cited by 29 · see citing works
Chen, H.-C., Chen, Y.-Z., Wang, C.-H., & Lin, F.-J. (2019) · Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.108319 · Cited by 23 · see citing works
Sarcopenic obesity and therapeutic outcomes in gastrointestinal surgical oncology: A meta-analysis
Wang, P., Wang, S., Ma, Y., Li, H., Liu, Z., Lin, G., Li, X., Yang, F., & Qiu, M. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.921817 · Cited by 27 · see citing works
Diabetic pregnancy activates the innate immune response through TLR5 or TLR1/2 on neonatal monocyte
Yanai, S., Tokuhara, D., Tachibana, D., Saito, M., Sakashita, Y., Shintaku, H., & Koyama, M. (2016) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2016.06.007 · Cited by 26 · see citing works
Zeng, J., Shen, F., Zou, Z.-Y., Yang, R.-X., Jin, Q.-F., Yang, J., Chen, G.-Y., & Fan, J.-G. (2022) · World Journal of Gastroenterology · doi:10.3748/wjg.v28.i16.1681 · Cited by 25 · see citing works
Wu, J., Zheng, L., Mo, J., Yao, X., Fan, C., & Bao, Y. (2020) · BioMed Research International · doi:10.1155/2020/9329427 · Cited by 24 · see citing works
Nonalcoholic fatty liver disease and bariatric surgery in adolescents
Holterman, A., Gurria, J. P., Tanpure, S., & DiSomma, N. M. (2013) · Seminars in Pediatric Surgery · doi:10.1053/j.sempedsurg.2013.10.016 · Cited by 23 · see citing works
Maragkoudaki, X., Naylor, M., Papacleovoulou, G., Stolarczyk, E., Rees, D., Pombo, J., Abu‐Hayyeh, S., Czajka, A., Howard, J. K., Malik, A. N., et al. (2020) · International Journal of Obesity · doi:10.1038/s41366-020-00682-5 · Cited by 25 · see citing works
Self-citationAbeysekera, K. W. M., Orr, J. G., Madley‐Dowd, P., Fernandes, G., Zuccolo, L., Gordon, F. H., Lawlor, D. A., Heron, J., & Hickman, M. (2021) · The Lancet Regional Health - Europe · doi:10.1016/j.lanepe.2021.100206 · Cited by 22 · see citing works
Ambrosetti, V., Guerra, M., Ramirez, L., Reyes, A., Álvarez, D., Olguín, S., Gonzalez‐Mañán, D., Fernandois, D., Sotomayor‐Zárate, R., & Cruz, G. (2016) · Endocrine · doi:10.1007/s12020-016-0858-0 · Cited by 20 · see citing works
Paternal hyperglycemia in rats exacerbates the development of obesity in offspring
Shi, X., Li, X., Hou, Y., Cao, X., Zhang, Y., Wang, H., Wang, H., Peng, C. X., Li, J., Li, Q., et al. (2017) · Journal of Endocrinology · doi:10.1530/joe-17-0082 · Cited by 20 · see citing works
Leca, B. M., Lagojda, L., Kite, C., Karteris, E., Kassi, E. N., Randeva, H. S., & Kyrou, I. (2024) · Expert Review of Endocrinology & Metabolism · doi:10.1080/17446651.2024.2365791 · Cited by 19 · see citing works
Glucocorticoids and intrauterine programming of nonalcoholic fatty liver disease
Chen, Z., Xia, L., Shen, L., Xu, D., Guo, Y., & Wang, H. (2023) · Metabolism · doi:10.1016/j.metabol.2023.155713 · Cited by 18 · see citing works
Nonalcoholic Fatty Liver Disease
Fitzpatrick, E. (2021) · Springer eBooks · doi:10.1007/978-3-030-80068-0_69 · Cited by 18 · see citing works
Moeckli, B., Delaune, V., Prados, J., Tihy, M., Peloso, A., Oldani, G., Delmi, T., Slits, F., Gex, Q., Rubbia‐Brandt, L., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10020294 · Cited by 18 · see citing works
Chae, S. A., Son, J. S., Zhao, L., Gao, Y., Liu, X., de Avila, J. M., Zhu, M. J., & Du, . (2022) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00023.2022 · Cited by 18 · see citing works
Maternal Fructose Intake, Programmed Mitochondrial Function and Predisposition to Adult Disease
Smith, E. V. L., Dyson, R. M., Weth, F. R., Berry, M. J., & Gray, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012215 · Cited by 18 · see citing works
Lie, S., Morrison, J. L., Williams-Wyss, O., Suter, C. M., Humphreys, D. T., Ozanne, S. E., Zhang, S., MacLaughlin, S. M., Kleemann, D. O., Walker, S. K., et al. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00600.2014 · Cited by 18 · see citing works
Li, Q., Pereira, T. J., Moyce, B. L., Mahood, T. H., Doucette, C. A., Rempel, J., & Dolinsky, V. W. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.08.004 · Cited by 18 · see citing works
Lipotoxicity and the role of maternal nutrition
Pruis, M., van Ewijk, P. A., Schrauwen-Hinderling, V. B., & Plösch, T. (2014) · Acta Physiologica · doi:10.1111/apha.12171 · Cited by 18 · see citing works
Savva, C., Helguero, L. A., Gonzalez-Granillo, M. A., Melo, T., Couto, D., Angelin, B., Domingues, M. R., Li, X., Kutter, C., & Korach-André, M. (2022) · Communications Biology · doi:10.1038/s42003-022-04022-3 · Cited by 16 · see citing works
A high-fat maternal diet decreases adiponectin receptor-1 expression in offspring
Hou, M., Chu, Z., Liu, T., Lv, H., Sun, L. V., Wang, B., Huang, J., & Yan, W. (2014) · The Journal of Maternal-Fetal & Neonatal Medicine · doi:10.3109/14767058.2014.914489 · Cited by 16 · see citing works
Maternal Early‐Pregnancy Glucose Concentrations and Liver Fat Among School‐Age Children
Geurtsen, M. L., Wahab, R. J., Felix, J. F., Gaillard, R., & Jaddoe, V. W. V. (2021) · Hepatology · doi:10.1002/hep.31910 · Cited by 17 · see citing works
Kasch, J., Schumann, S., Schreiber, S., Klaus, S., & Kanzleiter, I. (2017) · PLoS ONE · doi:10.1371/journal.pone.0173076 · Cited by 16 · see citing works
Hinrichs, H., Faerber, A., Young, M., Ballentine, S. J., & Thompson, M. D. (2023) · Endocrinology · doi:10.1210/endocr/bqad010 · Cited by 15 · see citing works
Sugino, K. Y., Janssen, R. C., McMahan, R. H., Zimmerman, C., Friedman, J. E., & Jonscher, K. R. (2024) · Nutrients · doi:10.3390/nu16121808 · Cited by 15 · see citing works
Thompson, M. D., Kang, J., Faerber, A., Hinrichs, H., Özler, O., Cowen, J., Xie, Y., Tarr, P. I., & Davidson, N. O. (2022) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00247.2021 · Cited by 15 · see citing works
Developmental Origins of Nonalcoholic Fatty Liver Disease (NAFLD).
Itoh, H., & Kanayama, N. (2018) · Advances in Experimental Medicine and Biology · doi:10.1007/978-981-10-5526-3_4 · Cited by 10 · see citing works
Gong, H., Yuan, Q., Du, ., & Mao, X. (2023) · Food & Function · doi:10.1039/d2fo04026c · Cited by 14 · see citing works
Histone variants and lipid metabolism
Borghesan, M., Mazzoccoli, G., Sheedfar, F., Oben, J. A., Pazienza, V., & Vinciguerra, M. (2014) · Biochemical Society Transactions · doi:10.1042/bst20140119 · Cited by 14 · see citing works
Self-citationRodrigo, N., Saad, S., Pollock, C. A., & Glastras, S. J. (2022) · Nutrients · doi:10.3390/nu14102154 · Cited by 13 · see citing works
Shashikadze, B., Valla, L., Lombardo, S. D., Prehn, C. P., Haid, M., Riols, F., Stöckl, J. B., Elkhateib, R., Renner, S., Rathkolb, B., et al. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101768 · Cited by 13 · see citing works
Boone‐Heinonen, J., Messer, L. C., Fortmann, S. P., Wallack, L., & Thornburg, K. L. R. (2015) · Preventive Medicine · doi:10.1016/j.ypmed.2015.10.012 · Cited by 13 · see citing works
Moeckli, B., Delaune, V., Gilbert, B. T. P., Peloso, A., Oldani, G., Hajji, S. E., Slits, F., Ribeiro, J. R., Mercier, R., Gleyzolle, A., et al. (2024) · JHEP Reports · doi:10.1016/j.jhepr.2024.101056 · Cited by 12 · see citing works
Cordero, P., Li, J.-W., Nguyen, V., Pombo, J., Maicas, N., Novelli, M., Taylor, P., Samuelsson, A., Vinciguerra, M., & Oben, J. (2017) · Nutrients · doi:10.3390/nu9091041 · Cited by 11 · see citing works
Self-citationInfluence of Early-Life Environmental Exposures on Immune Function Across the Life Span
Boulé, L. A., & Lawrence, B. P. (2016) · Springer eBooks · doi:10.1007/978-3-7091-1890-0_2 · Cited by 12 · see citing works
Ye, J., Shi, R., Wu, X., Fan, H., Zhao, Y., Hu, X., Wang, L., Bo, X., Li, D., Ge, Y., et al. (2025) · Gut Microbes · doi:10.1080/19490976.2025.2452241 · Cited by 11 · see citing works
Nairz, J., Messner, A., Zollner-Kiechl, S., Winder, B., Hochmayr, C., Egger, A., Griesmacher, A., Geiger, R., Griesmaier, E., Pechlaner, R., et al. (2024) · PLoS ONE · doi:10.1371/journal.pone.0298800 · Cited by 11 · see citing works
Liang, Y., Liu, D., Li, Y., Hou, H., Li, P., Ma, X., Li, P., Zhan, J., & Wang, P. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.168624 · Cited by 10 · see citing works
Prenatal metformin treatment improves ovarian function in offspring of obese rats.
Álvarez, D., Ceballo, K., Olguín, S., Martínez-Pinto, J., Maliqueo, M., Fernandois, D., Sotomayor-Zárate, R., & Cruz, G. (2018) · Journal of Endocrinology · doi:10.1530/joe-18-0352 · Cited by 9 · see citing works
Non-alcoholic fatty liver disease: more than just ectopic fat accumulation
Francisco Barrera, M., & George, J. (2013) · Drug Discovery Today Disease Mechanisms · doi:10.1016/j.ddmec.2013.06.002 · Cited by 8 · see citing works
Han, S., Zhu, F. Y., Huang, X., Yan, P., Xu, K., Shen, F., Sun, J., Yang, Z., Jin, G., & Teng, Y. (2021) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2021.10148 · Cited by 8 · see citing works
- Authors
- Mouralidarane, A., Soeda, J., Visconti-Pugmire, C., Samuelsson, A.-M., Pombo, J., Maragkoudaki, X., Butt, A., Saraswati, R., Novelli, M., Fusai, G., Poston, L., Taylor, P. D., & Oben, J. A.
- Affiliations
- King's College London (GB)
- The Royal Free Hospital (GB)
- University College London (GB)
- National Health Service (GB)
- Corresponding author
- Oben, Jude A.
- Venue
- Hepatology
- Published
- 2013-07
- Volume
- 58
- Issue
- 1
- Pages
- 128-138
- ISSN
- 0270-9139 (ISSN-L)
- OpenAlex
- W1969470394
- Cited by
- 145
- References
- 33
- Citations by year
- 2026: 1 · 2025: 10 · 2024: 8 · 2023: 9 · 2022: 14 · 2021: 7 · 2020: 10 · 2019: 10 · 2018: 16 · 2017: 12 · 2016: 15 · 2015: 13 · 2014: 10 · 2013: 10
- FWCI
- 11.62
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hepatology (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Funders
- Wellcome Trust
- British Heart Foundation (FS/10/003/28163)
- Biotechnology and Biological Sciences Research Council (BB/H008845/1)
- Topics
- Health Sciences › Medicine › Epidemiology › Liver Disease Diagnosis and Treatment
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- maternal obesity, non-alcoholic fatty liver disease, offspring programming, innate immune dysregulation, obesogenic diet, Kupffer cells, NKT cells, reactive oxygen species, liver fibrosis, hepatic steatosis, IL-12, IL-18, postnatal diet, liver injury
- MeSH terms
- Animals, Dietary Fats, Fatty Liver, Female, Immunity, Innate, Liver, Liver Diseases, Mice, Inbred C57BL, Obesity, Pregnancy, Prenatal Exposure Delayed Effects, Mice, Non-alcoholic Fatty Liver Disease
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review