Natriuretic Peptides/cGMP/cGMP-Dependent Protein Kinase Cascades Promote Muscle Mitochondrial Biogenesis and Prevent Obesity
Open accessAbstract
OBJECTIVE: Natriuretic peptides (NPs) have been characterized as vascular hormones that regulate vascular tone via guanylyl cyclase (GC), cyclic GMP (cGMP), and cGMP-dependent protein kinase (cGK). Recent clinical studies have shown that plasma NP levels were lower in subjects with the metabolic syndrome. The present study was conducted to elucidate the roles for NP/cGK cascades in energy metabolism. RESEARCH DESIGN AND METHODS: We used three types of genetically engineered mice: brain NP (BNP) transgenic (BNP-Tg), cGK-Tg, and guanylyl cyclase-A (GCA) heterozygous knockout (GCA+/−) mice and analyzed the metabolic consequences of chronic activation of NP/cGK cascades in vivo. We also examined the effect of NPs in cultured myocytes. RESULTS: BNP-Tg mice fed on high-fat diet were protected against diet-induced obesity and insulin resistance, and cGK-Tg mice had reduced body weight even on standard diet; surprisingly, giant mitochondria were densely packed in the skeletal muscle. Both mice showed an increase in muscle mitochondrial content and fat oxidation through upregulation of peroxisome proliferator–activated receptor (PPAR)-γ coactivator (PGC)-1α and PPARδ. The functional NP receptors, GCA and guanylyl cyclase-B, were downregulated by feeding a high-fat diet, while GCA+/− mice showed increases in body weight and glucose intolerance when fed a high-fat diet. NPs directly increased the expression of PGC-1α and PPARδ and mitochondrial content in cultured myocytes. CONCLUSIONS: The findings together suggest that NP/cGK cascades can promote muscle mitochondrial biogenesis and fat oxidation, as to prevent obesity and glucose intolerance. The vascular hormone, NP, would contribute to coordinated regulation of oxygen supply and consumption.
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Transgenic mice that overexpressed brain natriuretic peptide were protected against diet-induced obesity and insulin resistance.
“Consistent with this hypothesis, transgenic mice that overexpressed BNP were protected against diet-induced obesity and insulin resistance98.”
From Obesity, kidney dysfunction and hypertension: mechanistic links (2019) · cites this paper as [98]
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BackgroundResultInfluentialIncreased cGMP promotes healthy expansion and browning of white adipose tissue
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“Transgenic mice over-expressing BNP and components of the BNP downstream signalling cascade were protected from diet-induced insulin resistance and obesity compared to wild-type mice, by up-regulation of mitochondrial biogenesis and fat oxidation [28].”
BackgroundHigher Natriuretic Peptide Levels Associate With a Favorable Adipose Tissue Distribution Profile
Neeland, I. J., Winders, B. R., Ayers, C. R., Das, S. R., Chang, A. Y., Berry, J. D., Khera, A., McGuire, D. K., Vega, G. L., de Lemos, J. A., et al. (2013) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2013.03.038 · Cited by 118 · see citing works
“Atrial natriuretic and B-type natriuretic peptides (BNPs) bind to NPR-A receptors on adipose tissue and stimulate lipolysis (6), promote browning of adipocytes (7), regulate body fat distribution by activation of peroxisome proliferator-activated receptor gamma gene expression (8), and enhance adiponectin secretion fr…”
BackgroundWu, W., Shi, F., Liu, D., Ceddia, R. P., Gaffin, R. D., Wei, W., Fang, H., Lewandowski, E. D., & Collins, S. (2017) · Science Signaling · doi:10.1126/scisignal.aam6870 · Cited by 118 · see citing works
NH2-Terminal Pro–Brain Natriuretic Peptide and Risk of Diabetes
Lazo, M., Young, J. H., Brancati, F. L., Coresh, J., Whelton, S. P., Ndumele, C. E., Hoogeveen, R. C., Ballantyne, C. M., & Selvin, E. (2013) · Diabetes · doi:10.2337/db13-0478 · Cited by 107 · see citing works
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Stimulation of soluble guanylyl cyclase protects against obesity by recruiting brown adipose tissue
Hoffmann, L. S., Etzrodt, J., Willkomm, L., Sanyal, A., Scheja, L., Fischer, A. W., Stasch, J., Bloch, W., Friebe, A., Heeren, J., et al. (2015) · Nature Communications · doi:10.1038/ncomms8235 · Cited by 102 · see citing works
“The results of our study show that pharmacological sGC stimulation protects against DIO and induces weight loss in already established obesity.”
InfluentialCannone, V., Boerrigter, G., Cataliotti, A., Costello‐Boerrigter, L. C., Olson, T. M., McKie, P. M., Heublein, D. M., Lahr, B. D., Bailey, K. R., Averna, M. R., et al. (2011) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2011.05.011 · Cited by 103 · see citing works
“demonstrated in a mouse model that BNP overexpression prevented the development of obesity in response to a high fat diet (14).”
BackgroundInfluentialThe natriuretic peptides and cardiometabolic health
Gupta, D., & Wang, T. J. (2015) · Circulation Journal · doi:10.1253/circj.cj-15-0589 · Cited by 85 · see citing works
Pivovarova‐Ramich, O., Gögebakan, Ö., Klöting, N., Sparwaßer, A., Weickert, M. O., Haddad, I., Nikiforova, V. J., Bergmann, A., Kruse, M., Seltmann, A., et al. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-2839 · Cited by 91 · see citing works
“NP activate two membrane-bound guanylyl cyclase receptors [NP receptor A (NPRA) and NP receptor B (NPRB)], leading to an increase in intracellular cGMP and thus affecting the activity of cGMP-regulated enzymes and ion channels (3, 4).”
InfluentialKovacova, Z., Tharp, W. G., Liu, D., Wei, W., Xie, H., Collins, S., & Pratley, R. E. (2016) · Obesity · doi:10.1002/oby.21418 · Cited by 85 · see citing works
Atrial Natriuretic Peptide and Adiponectin Interactions in Man
Birkenfeld, A. L., Boschmann, M., Engeli, S., Moro, C., Arafat, A. M., Luft, F. C., & Jordan, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043238 · Cited by 90 · see citing works
“In contrast, augmented natriuretic peptide availability improves insulin sensitivity in mice [4].”
Unexpectedly Low Natriuretic Peptide Levels in Patients With Heart Failure
Bachmann, K. N., Gupta, D. K., Xu, M., Brittain, E. L., Farber‐Eger, E. H., Arora, P. K., Collins, S., Wells, Q. S., & Wang, T. J. (2021) · JACC Heart Failure · doi:10.1016/j.jchf.2020.10.008 · Cited by 87 · see citing works
Defective Natriuretic Peptide Receptor Signaling in Skeletal Muscle Links Obesity to Type 2 Diabetes
Coué, M., Badin, P.-M., Vila, I. K., Laurens, C., Louche, K., Marqués, M.-A., Bourlier, V., Mouisel, É., Tavernier, G., Rustan, A. C., et al. (2015) · Diabetes · doi:10.2337/db15-0305 · Cited by 87 · see citing works
The Role of the Skeletal Muscle Secretome in Mediating Endurance and Resistance Training Adaptations
Leuchtmann, A. B., Adak, V., Dilbaz, S., & Handschin, C. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.709807 · Cited by 84 · see citing works
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“Transgenic mice overexpressing BNP or PKG increased the mitochondrial muscle content and fat oxidation through upregulation of PGC-1α and PPARδ, preventing obesity and glucose intolerance; moreover, treatment of myotubes with ANP and BNP stimulates mitochondrial biogenesis and mitochondrial respiration [171].”
BackgroundKou, G., Li, Z., Wu, C., Liu, Y., Hu, Y., Guo, L., Xu, X., & Zhou, Z. (2018) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.8b04124 · Cited by 78 · see citing works
Muraki, A., Miyashita, K., Mitsuishi, M., Tamaki, M., Tanaka, K., & Itoh, H. (2012) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01362.2011 · Cited by 80 · see citing works
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Natriuretic peptide control of energy balance and glucose homeostasis
Coué, M., & Moro, C. (2015) · Biochimie · doi:10.1016/j.biochi.2015.05.017 · Cited by 75 · see citing works
The Natriuretic Peptides and Fat Metabolism
Wang, T. J. (2012) · New England Journal of Medicine · doi:10.1056/nejmcibr1204796 · Cited by 73 · see citing works
Diabetes-Related Heart Failure
Bando, Y., & Murohara, T. (2014) · Circulation Journal · doi:10.1253/circj.cj-13-1564 · Cited by 71 · see citing works
Plante, É., Ménaouar, A., Danalache, B. A., Broderick, T. L., Jankowski, M., & Gutkowska, J. (2014) · Diabetologia · doi:10.1007/s00125-014-3201-4 · Cited by 71 · see citing works
“It has been shown that BNP is a protective agent against the development of type 2 diabetes in humans [13] and against diet-induced obesity and insulin resistance in mice [14].”
BackgroundThe foraging Gene and Its Behavioral Effects: Pleiotropy and Plasticity
Anreiter, I., & Sokolowski, M. B. (2019) · Annual Review of Genetics · doi:10.1146/annurev-genet-112618-043536 · Cited by 66 · see citing works
Jordan, J., Birkenfeld, A. L., Melander, O., & Moro, C. (2018) · Hypertension · doi:10.1161/hypertensionaha.118.11081 · Cited by 68 · see citing works
“Elevated oxygen consumption and fat oxidation through increased muscular mitochondrial respiration were likely involved.(53) Ubiquitous cGK-I overexpression elicited a similar response.”
BackgroundCardiac Natriuretic Peptides, Hypertension and Cardiovascular Risk
Sarzani, R., Spannella, F., Giulietti, F., Balietti, P., Cocci, G., & Bordicchia, M. (2017) · High Blood Pressure & Cardiovascular Prevention · doi:10.1007/s40292-017-0196-1 · Cited by 69 · see citing works
“brown adipose tissue, and at the same time enhance this process, by inducing mitochondrial biogenesis, oxygen consumption and thermogenesis [40, 41].”
BackgroundB-Type Natriuretic Peptide Modulates Ghrelin, Hunger, and Satiety in Healthy Men
Vila, G., Grimm, G., Resl, M., Heinisch, B. B., Einwallner, E., Esterbauer, H., Dieplinger, B., Mueller, T., Luger, A., & Clodi, M. (2012) · Diabetes · doi:10.2337/db11-1466 · Cited by 66 · see citing works
“BNP transgenic mice are protected against diet-induced obesity and insulin resistance (10).”
BackgroundRe Cecconi, A. D., Forti, M., Chiappa, M., Zhu, Z., Zingman, L. V., Cervo, L., Beltrame, L., Marchini, S., & Piccirillo, R. (2019) · Cancers · doi:10.3390/cancers11101541 · Cited by 66 · see citing works
“, cGMP) production following stimulation by natriuretic peptides in muscles, as in myocytes, results in increased oxidative metabolism of muscle, in other words, more lipid utilization and mitochondria biogenesis [65,66].”
BackgroundNeinast, M. D., Frank, A. P., Zechner, J. F., Li, Q., Vishvanath, L., Palmer, B. F., Aguirre, V., Gupta, R. K., & Clegg, D. J. (2015) · Molecular Metabolism · doi:10.1016/j.molmet.2015.02.006 · Cited by 64 · see citing works
Peripheral signalling involved in energy homeostasis control
Lancha, A., Frühbeck, G., & Gómez‐Ambrosi, J. (2012) · Nutrition Research Reviews · doi:10.1017/s0954422412000145 · Cited by 65 · see citing works
“oxidation, preventing the development of obesity and insulin resistance in mice((428)).”
BackgroundGupta, D. K., Daniels, L. B., Cheng, S. C., deFilippi, C. R., Criqui, M. H., Maisel, A. S., Lima, J. A. C., Bahrami, H., Greenland, P., Cushman, M., et al. (2017) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2017.06.030 · Cited by 63 · see citing works
Davidson, E. P., Coppey, L. J., Holmes, A. J., Dake, B. L., & Yorek, M. A. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.07.016 · Cited by 59 · see citing works
Feeding-Related Traits Are Affected by Dosage of theforagingGene inDrosophila melanogaster
Allen, A. M., Anreiter, I., Neville, M. C., & Sokolowski, M. B. (2016) · Genetics · doi:10.1534/genetics.116.197939 · Cited by 58 · see citing works
Cannone, V., Cefalu, A. B., Noto, D., Scott, C. G., Bailey, K. R., Cavera, G., Pagano, M., Sapienza, M., Averna, M. R., & Burnett, J. C. J. (2013) · Diabetes Care · doi:10.2337/dc12-2337 · Cited by 57 · see citing works
“Genetically engineered mice that are exposed throughout life to a plasma BNP concentration that is 100 times higher than the physiological concentration are protected from obesity and insulin resistance when fed with a high-fat diet (32).”
BackgroundSanchez, O. A., Duprez, D. A., Bahrami, H., Daniels, L. B., Folsom, A. R., Lima, J. A. C., Maisel, A. S., Peralta, C. A., & Jacobs, D. R. (2013) · Metabolism · doi:10.1016/j.metabol.2013.11.017 · Cited by 56 · see citing works
“In addition, low levels of BNP can also affect BMI through its effects on mitochondrial genesis [36].”
BackgroundRelation of Visceral Adiposity to Circulating Natriuretic Peptides in Ambulatory Individuals
Cheng, S. C., Fox, C. S., Larson, M. G., Massaro, J. M., McCabe, E. L., Khan, A. M., Levy, D. A., Hoffmann, U., O’Donnell, C. J., Miller, K. K., et al. (2011) · The American Journal of Cardiology · doi:10.1016/j.amjcard.2011.05.033 · Cited by 56 · see citing works
Interplay between Obesity-Induced Inflammation and cGMP Signaling in White Adipose Tissue
Sanyal, A., Naumann, J., Hoffmann, L. S., Chabowska-Kita, A., Ehrlund, A., Schlitzer, A., Arner, P., Blüher, M., & Pfeifer, A. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.028 · Cited by 55 · see citing works
“, 1991; McDonald and Murad, 1996; Poulos, 2006); and membrane-bound particulate GC (pGC), upon extracellular natriuretic peptide activation (Miyashita et al., 2009; Waldman et al., 1984).”
BackgroundNatriuretic peptides promote glucose uptake in a cGMP-dependent manner in human adipocytes
Coué, M., Barquissau, V., Morigny, P., Louche, K., Lefort, C., Mairal, A., Carpéné, C., Viguerie, N., Arner, P., Langin, D., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-19619-0 · Cited by 53 · see citing works
The Importance of Natriuretic Peptides in Cardiometabolic Diseases
Vinnakota, S., & Chen, H. H. (2020) · Journal of the Endocrine Society · doi:10.1210/jendso/bvaa052 · Cited by 54 · see citing works
“Multiple hypotheses have been put forward to explain this, including increased NPR-C–mediated clearance [58] as well as decreased synthesis [59].”
BackgroundPandey, K. N. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.693099 · Cited by 56 · see citing works
Davidson, E. P., Coppey, L. J., Holmes, A. J., & Yorek, M. A. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.12.003 · Cited by 52 · see citing works
Cannone, V., Huntley, B. K., Olson, T. M., Heublein, D. M., Scott, C. G., Bailey, K. R., Redfield, M. M., Rodeheffer, R. J., & Burnett, J. C. J. (2013) · Hypertension · doi:10.1161/hypertensionaha.113.01344 · Cited by 52 · see citing works
“Evaluating the metabolic phenotype associated with rs5065 genotypes was relevant because natriuretic peptides have lipolytic actions(3) and protect against obesity, as shown in mouse models.(22) Furthermore, we have reported that the ANP genetic variant rs5068 that is associated with increased circulating ANP and BNP…”
BackgroundLazo, M., Rubin, J., Clark, J. M., Coresh, J., Schneider, A. L. C., Ndumele, C. E., Hoogeveen, R. C., Ballantyne, C. M., & Selvin, E. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.11.024 · Cited by 52 · see citing works
Ashmore, T., Roberts, L. D., Morash, A. J., Kotwica, A. O., Finnerty, J., West, J. A., Murfitt, S. A., Fernandez, B. O., Branco, C. M., Cowburn, A. S., et al. (2015) · BMC Biology · doi:10.1186/s12915-015-0221-6 · Cited by 51 · see citing works
“In muscle, cGMP stimulated mitochondrial biogenesis and FA oxidation [16], whilst in white adipose tissue (WAT), cGMP, acting via cGMP-dependent protein kinases (PKGs) promoted the browning response characterised by increased mitochondrial density and uncoupling protein 1 (UCP1) expression [17, 18].”
Reciprocal regulation of natriuretic peptide receptors by insulin in adipose cells
Nakatsuji, H., Maeda, N., Hibuse, T., Hiuge, A., Hirata, A., Kuroda, Y., Kishida, K., Kihara, S., Funahashi, T., & Shimomura, I. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.01.008 · Cited by 51 · see citing works
“Other group recently demonstrated similar results that NPR-3 mRNA level of WAT was increased when mice were fed with high-fat diet [16].”
ResultCeddia, R. P., & Collins, S. (2020) · Clinical Science · doi:10.1042/cs20190579 · Cited by 51 · see citing works
Chang, P., Zhang, X., Zhang, J., Wang, J., Wang, X., Li, M., Wang, R., Yu, J., & Fu, F. (2023) · Redox Biology · doi:10.1016/j.redox.2023.102702 · Cited by 49 · see citing works
“BNP has been shown to protect mitochondria in previous studies [49, 50], while the direct link between the mitochondria and BNP signaling pathway is still largely unknown.”
BackgroundHeinisch, B. B., Vila, G., Resl, M., Riedl, M., Dieplinger, B., Mueller, T., Luger, A., Pacini, G., & Clodi, M. (2011) · Diabetologia · doi:10.1007/s00125-011-2392-1 · Cited by 49 · see citing works
“Data from rodent studies introduce further evidence on the anti-diabetogenic effects of BNP, as chronic overexpression of BNP protects mice against diet-induced obesity and accompanying insulin resistance [28].”
BackgroundTargeting cardiac natriuretic peptides in the therapy of diabetes and obesity
Moro, C. (2016) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2016.1254198 · Cited by 49 · see citing works
“This is also associated with an elevated rate of oxygen consumption and fat oxidation, possibly due to increased mitochondrial respiration in white/ brown adipocytes and skeletal muscle cells [43].”
BackgroundInfluentialHamasaki, H., Kawashima, Y., & Yanai, H. (2016) · Frontiers in Endocrinology · doi:10.3389/fendo.2016.00147 · Cited by 49 · see citing works
“BNP stimulates lipolysis (45) and promotes muscle mitochondrial biogenesis and fat oxidation through upregulation of peroxisome proliferator-activated receptor-γ coactivator-1α (PGC-1α) (46) and increases adiponectin secretion (47), thereby improving insulin resistance.”
BackgroundKimura, H., Nagoshi, T., Yoshii, A., Kashiwagi, Y., Tanaka, Y., Ito, K., Yoshino, T., Tanaka, T. D., & Yoshimura, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-13563-1 · Cited by 49 · see citing works
Bordicchia, M., Ceresiani, M., Pavani, M., Minardi, D., Polito, M., Wabitsch, M., Cannone, V., Burnett, J. C. J., Dessı̀-Fulgheri, P., & Sarzani, R. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00499.2015 · Cited by 48 · see citing works
“Indeed, recent studies reported also a link between obesity/ type 2 diabetes and NP receptor mRNA levels in both muscle and subcutaneous adipose tissue, suggesting that NPRA and NPRC expression is impaired in obesity not only in adipose but also in skeletal muscle (24, 21, 10, 28).”
BackgroundKimura, H., Nagoshi, T., Oi, Y., Yoshii, A., Tanaka, Y., Takahashi, H., Kashiwagi, Y., Tanaka, T. D., & Yoshimura, M. (2021) · Scientific Reports · doi:10.1038/s41598-021-96970-9 · Cited by 48 · see citing works
Werbner, B., Tavakoli‐Rouzbehani, O. M., Fatahian, A. N., & Boudina, S. (2023) · The Journal of Cardiovascular Aging · doi:10.20517/jca.2022.42 · Cited by 44 · see citing works
Mitochondrial dysfunction in cognitive neurodevelopmental disorders: Cause or effect?
Anitha, A., Thanseem, I., Iype, M., & Thomas, S. V. (2023) · Mitochondrion · doi:10.1016/j.mito.2023.01.002 · Cited by 46 · see citing works
Moon, Y., Balke, J. E., Madorma, D., Siegel, M. P., Knowels, G. M., Brouckaert, P., Buys, E. S., Marcinek, D. J., & Percival, J. M. (2016) · Antioxidants and Redox Signaling · doi:10.1089/ars.2016.6630 · Cited by 46 · see citing works
“Recent evidence suggests that decreased NO-cGMP signaling in tissues including skeletal muscle is a pathogenic feature of obesity (31,39,48,49,51).”
BackgroundInfluentialScirica, B. M. (2016) · Clinical Chemistry · doi:10.1373/clinchem.2016.255539 · Cited by 47 · see citing works
Myocardial metabolism in heart failure: Purinergic signalling and other metabolic concepts
Birkenfeld, A. L., Jordan, J., Dworak, M., Merkel, T., & Burnstock, G. (2018) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2018.08.015 · Cited by 45 · see citing works
Haufe, S., Kaminski, J., Utz, W., Haas, V., Mähler, A., Daniels, M. A., Birkenfeld, A. L., Lichtinghagen, R., Luft, F. C., Schulz-Menger, J., et al. (2015) · Journal of Hypertension · doi:10.1097/hjh.0000000000000573 · Cited by 41 · see citing works
“Weight loss reduced adipose NPR-C expression in rodents [5,17].”
BackgroundBalke, J. E., Zhang, L., & Percival, J. M. (2018) · Nitric Oxide · doi:10.1016/j.niox.2018.11.004 · Cited by 44 · see citing works
Pandey, K. N. (2018) · Physiological Genomics · doi:10.1152/physiolgenomics.00083.2018 · Cited by 42 · see citing works
“The ANP/NPRA system has been shown to enhance the browning of white adipocytes in humans, which is considered physiologically beneficial (48, 133).”
BackgroundmiR-146a regulates insulin sensitivity via NPR3
Roos, J., Dahlhaus, M., Funcke, J., Kustermann, M., Strauß, G., Halbgebauer, D., Boldrin, E., Holzmann, K., Möller, P., Trojanowski, B. M., et al. (2020) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-020-03699-1 · Cited by 44 · see citing works
Regulation of metabolism by cGMP
Pfeifer, A., Kilić, A., & Hoffmann, L. S. (2013) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2013.06.001 · Cited by 43 · see citing works
Maimaitiyiming, H., Li, Y., Cui, W., Tong, X., Norman‐Burgdolf, H., Qi, X., & Wang, S. (2013) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00192.2013 · Cited by 43 · see citing works
“One mechanism of this PKG-mediated mitochondria protection may be the stimulatory effect of PKG on mitochondria biogenesis by regulating PGC1- expression (21, 35, 38).”
BackgroundThe Atrial Natriuretic Peptide and Guanylyl Cyclase-A System Modulates Pancreatic β-Cell Function
Ropero, A. B., Soriano, S., Tudurí, E., Marroquí, L., Téllez, N., Gaßner, B., Juan-Picó, P., Montanya, E., Quesada, I., Kühn, M., et al. (2010) · Endocrinology · doi:10.1210/en.2010-0119 · Cited by 42 · see citing works
“In fact, GC-A / mice fed with high-fat diet developed glucose intolerance,whereas theoverexpression of BNP protected mice from developing high-fat diet-dependent insulin resistance (4).”
BackgroundNatriuretic peptides in the control of lipid metabolism and insulin sensitivity
Verboven, K., Hansen, D., Jocken, J., & Blaak, E. (2017) · Obesity Reviews · doi:10.1111/obr.12598 · Cited by 34 · see citing works
“Taken together, in vitro studies have shown that the NP system is able to induce a thermogenic process in the AT and to induce BAT activation.”
BackgroundInfluentialRole of cAMP and cGMP Signaling in Brown Fat
Reverte-Salisa, L., Sanyal, A., & Pfeifer, A. (2018) · Handbook of experimental pharmacology · doi:10.1007/164_2018_117 · Cited by 42 · see citing works
Endocrine functions of the heart: from bench to bedside
Volpe, M., Gallo, G., & Rubattu, S. D. (2022) · European Heart Journal · doi:10.1093/eurheartj/ehac759 · Cited by 42 · see citing works
Everett, B. M., Cook, N. R., Chasman, D. I., Magnone, M. C., Bobadilla, M., Rifai, N., Ridker, P. M., & Pradhan, A. D. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.194167 · Cited by 41 · see citing works
“(30), transgenic mice that expressed BNP at levels 100 times normal were leaner, were resistant to the effects of a high-fat diet on weight gain and insulin resistance, and had lower total body fat and increased oxygen consumption.”
Ramos, H. R., Birkenfeld, A. L., & de Bold, A. J. (2015) · Endocrine Connections · doi:10.1530/ec-15-0018 · Cited by 38 · see citing works
Singh, S., Pandey, A., & Neeland, I. J. (2020) · Progress in Cardiovascular Diseases · doi:10.1016/j.pcad.2020.09.006 · Cited by 41 · see citing works
Effect of Phosphodiesterase Inhibition on Insulin Resistance in Obese Individuals
Ho, J. E., Arora, P., Walford, G. A., Ghorbani, A., Guanaga, D. P., Dhakal, B. P., Nathan, D. I., Buys, E. S., Florez, J. C., Newton‐Cheh, C., et al. (2014) · Journal of the American Heart Association · doi:10.1161/jaha.114.001001 · Cited by 39 · see citing works
Shero, J. A., Lindholm, M. E., Sandri, M. F., & Stanford, K. I. (2025) · Circulation Research · doi:10.1161/circresaha.124.325614 · Cited by 43 · see citing works
Lutz, S. Z., Hennige, A. M., Feil, S. C., Peter, A., Gerling, A., Machann, J., Kröber, S. M., Rath, M., Schürmann, A., Weigert, C., et al. (2011) · Diabetes · doi:10.2337/db10-0760 · Cited by 39 · see citing works
Shan, S., Qiao, Q., Yin, R., Zhang, L., Shi, J., Zhao, W., Zhou, J., & Li, Z. (2023) · Journal of Agricultural and Food Chemistry · doi:10.1021/acs.jafc.2c05764 · Cited by 36 · see citing works
Duranti, G., Ceci, R., Sgrò, P., Sabatini, S., & Luigi, L. D. (2017) · Cell Stress and Chaperones · doi:10.1007/s12192-017-0778-9 · Cited by 36 · see citing works
“2003) through mitochondrial biogenesis and fatty acid (FA) oxidation stimulation (Miyashita et al. 2009).”
Background
- Authors
- Miyashita, K., Itoh, H., Tsujimoto, H., Tamura, N., Fukunaga, Y., Sone, M., Yamahara, K., Taura, D., Inuzuka, M., Sonoyama, T., & Nakao, K.
- Affiliations
- Keio University (JP)
- Kyoto University (JP)
- Corresponding author
- Itoh, Hiroshi
- ORCID
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2009-08-18
- Volume
- 58
- Issue
- 12
- Pages
- 2880-2892
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- PMC
- PMC2780866
- OpenAlex
- W2112688747
- Cited by
- 288
- References
- 40
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 14 · 2023: 19 · 2022: 16 · 2021: 19 · 2020: 17 · 2019: 19 · 2018: 17 · 2017: 20 · 2016: 20 · 2015: 26 · 2014: 19 · 2013: 18 · 2012: 24
- FWCI
- 11.75
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Diabetes (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Funders
- Smoking Research Foundation
- Topics
- Health Sciences › Medicine › Physiology › Adipose Tissue and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- natriuretic peptides, brain natriuretic peptide, cGMP-dependent protein kinase, guanylyl cyclase-A, guanylyl cyclase B, obesity prevention, insulin resistance, impaired glucose tolerance, PGC-1α, PPARδ, fat oxidation, high-fat diet, energy metabolism, metabolic syndrome
- MeSH terms
- Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1-alpha, Animals, Blood Glucose, Cells, Cultured, Dietary Fats, Genetic Engineering, Cyclic GMP, Insulin Resistance, Mitochondria, Molecular Sequence Data, Obesity, Oxygen Consumption, Protein Kinases, Transcription Factors, Lipid Peroxidation, Trans-Activators, Down-Regulation, Up-Regulation, Receptors, Atrial Natriuretic Factor, Glucose Intolerance, Mice, Knockout, Muscle, Skeletal, Natriuretic Peptide, Brain, Muscle Cells, Natriuretic Peptides, PPAR delta, PPAR gamma, Mice
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 ›
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