Influence of Adipokines on Metabolic Dysfunction and Aging
Abstract
:1. Introduction
2. Adipokines in the Regulation of Health and Diseases
2.1. Adiponectin
2.2. Fiboblast Growth Factor 21 (Fgf21)
2.3. Adipsin
2.4. Apelin
2.5. Omentin
2.6. Annexin
2.7. Neuregulin (Nrg)
2.8. Leptin
2.9. Resistin
2.10. Visfatin/NAMPT
2.11. Chemerin
2.12. Vaspin
2.13. Lipocalin-2
2.14. RBP4
2.15. Fetuin A
3. Age-Related Changes in Adipose Tissue and Adipokines
4. Adipokines Viewed from Caloric Restriction and Centenarian Studies
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Chouchani, E.T.; Kajimura, S. Metabolic adaptation and maladaptation in adipose tissue. Nat. Metab. 2019, 1, 189–200. [Google Scholar] [CrossRef] [PubMed]
- Kawai, T.; Autieri, M.V.; Scalia, R. Adipose tissue inflammation and metabolic dysfunction in obesity. Am. J. Physiol. Cell Physiol. 2021, 320, C375–C391. [Google Scholar] [CrossRef] [PubMed]
- Longo, M.; Zatterale, F.; Naderi, J.; Parrillo, L.; Formisano, P.; Raciti, G.A.; Beguinot, F.; Miele, C. Adipose Tissue Dysfunction as Determinant of Obesity-Associated Metabolic Complications. Int. J. Mol. Sci. 2019, 20, 2358. [Google Scholar] [CrossRef] [PubMed]
- Khan, T.; Muise, E.S.; Iyengar, P.; Wang, Z.V.; Chandalia, M.; Abate, N.; Zhang, B.B.; Bonaldo, P.; Chua, S.; Scherer, P.E. Metabolic dysregulation and adipose tissue fibrosis: Role of collagen VI. Mol. Cell. Biol. 2009, 29, 1575–1591. [Google Scholar] [CrossRef] [PubMed]
- Furukawa, S.; Fujita, T.; Shimabukuro, M.; Iwaki, M.; Yamada, Y.; Nakajima, Y.; Nakayama, O.; Makishima, M.; Matsuda, M.; Shimomura, I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Investig. 2004, 114, 1752–1761. [Google Scholar] [CrossRef] [PubMed]
- Sung, H.K.; Doh, K.O.; Son, J.E.; Park, J.G.; Bae, Y.; Choi, S.; Nelson, S.M.; Cowling, R.; Nagy, K.; Michael, I.P.; et al. Adipose vascular endothelial growth factor regulates metabolic homeostasis through angiogenesis. Cell Metab. 2013, 17, 61–72. [Google Scholar] [CrossRef] [PubMed]
- Lumeng, C.N.; Bodzin, J.L.; Saltiel, A.R. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Investig. 2007, 117, 175–184. [Google Scholar] [CrossRef] [PubMed]
- Frasca, D.; Blomberg, B.B.; Paganelli, R. Aging, Obesity, and Inflammatory Age-Related Diseases. Front. Immunol. 2017, 8, 1745. [Google Scholar] [CrossRef] [PubMed]
- Frasca, D.; Blomberg, B.B. Adipose tissue, immune aging, and cellular senescence. Semin. Immunopathol. 2020, 42, 573–587. [Google Scholar] [CrossRef]
- Abdelaal, M.; le Roux, C.W.; Docherty, N.G. Morbidity and mortality associated with obesity. Ann. Transl. Med. 2017, 5, 161. [Google Scholar] [CrossRef]
- Bhaskaran, K.; Dos-Santos-Silva, I.; Leon, D.A.; Douglas, I.J.; Smeeth, L. Association of BMI with overall and cause-specific mortality: A population-based cohort study of 3.6 million adults in the UK. Lancet Diabetes Endocrinol. 2018, 6, 944–953. [Google Scholar] [CrossRef] [PubMed]
- Dhana, K.; Nano, J.; Ligthart, S.; Peeters, A.; Hofman, A.; Nusselder, W.; Dehghan, A.; Franco, O.H. Obesity and Life Expectancy with and without Diabetes in Adults Aged 55 Years and Older in the Netherlands: A Prospective Cohort Study. PLoS Med. 2016, 13, e1002086. [Google Scholar] [CrossRef]
- Barzilai, N.; She, L.; Liu, B.Q.; Vuguin, P.; Cohen, P.; Wang, J.; Rossetti, L.; Barzilai, N.; She, L.; Liu, B.Q.; et al. Surgical removal of visceral fat reverses hepatic insulin resistance. Diabetes 1999, 48, 94–98. [Google Scholar] [CrossRef] [PubMed]
- Muzumdar, R.; Allison, D.B.; Huffman, D.M.; Ma, X.; Atzmon, G.; Einstein, F.H.; Fishman, S.; Poduval, A.D.; McVei, T.; Keith, S.W.; et al. Visceral adipose tissue modulates mammalian longevity. Aging Cell 2008, 7, 438–440. [Google Scholar] [CrossRef] [PubMed]
- Ou, M.Y.; Zhang, H.; Tan, P.C.; Zhou, S.B.; Li, Q.F. Adipose tissue aging: Mechanisms and therapeutic implications. Cell Death Dis. 2022, 13, 300. [Google Scholar] [CrossRef] [PubMed]
- Zorena, K.; Jachimowicz-Duda, O.; Ślęzak, D.; Robakowska, M.; Mrugacz, M. Adipokines and Obesity. Potential Link to Met abolic Disorders and Chronic Complications. Int. J. Mol. Sci. 2020, 21, 3570. [Google Scholar] [CrossRef] [PubMed]
- López-Otín, C.; Blasco, M.A.; Partridge, L.; Serrano, M.; Kroemer, G. Hallmarks of aging: An expanding universe. Cell 2023, 186, 243–278. [Google Scholar] [CrossRef]
- Li, N.; Zhao, S.; Zhang, Z.; Zhu, Y.; Gliniak, C.M.; Vishvanath, L.; An, Y.A.; Wang, M.Y.; Deng, Y.; Zhu, Q.; et al. Adiponectin preserves metabolic fitness during aging. eLife 2021, 10, e65108. [Google Scholar] [CrossRef]
- Zhang, Y.; Xie, Y.; Berglund, E.D.; Coate, K.C.; He, T.T.; Katafuchi, T.; Xiao, G.; Potthoff, M.J.; Wei, W.; Wan, Y.; et al. The starvation hormone, fibroblast growth factor-21, extends lifespan in mice. eLife 2012, 1, e00065. [Google Scholar] [CrossRef] [PubMed]
- Scherer, P.E.; Williams, S.; Fogliano, M.; Baldini, G.; Lodish, H.F. A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 1995, 270, 26746–26749. [Google Scholar] [CrossRef]
- Ouchi, N.; Kihara, S.; Funahashi, T.; Matsuzawa, Y.; Walsh, K. Obesity, adiponectin and vascular inflammatory disease. Curr. Opin. Lipidol. 2003, 14, 561–566. [Google Scholar] [CrossRef] [PubMed]
- Freitas Lima, L.C.; Braga, V.A.; do Socorro de França Silva, M.; Cruz, J.C.; Sousa Santos, S.H.; de Oliveira Monteiro, M.M.; Balarini, C.M. Adipokines, diabetes and atherosclerosis: An inflammatory association. Front. Physiol. 2015, 6, 304. [Google Scholar] [CrossRef] [PubMed]
- Ouchi, N.; Walsh, K. Adiponectin as an anti-inflammatory factor. Clin. Chim. Acta 2007, 380, 24–30. [Google Scholar] [CrossRef] [PubMed]
- Hajri, T.; Tao, H.; Wattacheril, J.; Marks-Shulman, P.; Abumrad, N.N. Regulation of adiponectin production by insulin: Interactions with tumor necrosis factor-α and interleukin-6. Am. J. Physiol. Endocrinol. Metab. 2011, 300, E350–E360. [Google Scholar] [CrossRef] [PubMed]
- Kumada, M.; Kihara, S.; Ouchi, N.; Kobayashi, H.; Okamoto, Y.; Ohashi, K.; Maeda, K.; Nagaretani, H.; Kishida, K.; Maeda, N.; et al. Adiponectin specifically increased tissue inhibitor of metalloproteinase-1 through interleukin-10 expression in human macrophages. Circulation 2004, 109, 2046–2049. [Google Scholar] [CrossRef]
- Munhoz, A.C.; Serna, J.D.C.; Vilas-Boas, E.A.; Caldeira da Silva, C.C.; Santos, T.G.; Mosele, F.C.; Felisbino, S.L.; Martins, V.R.; Kowaltowski, A.J. Adiponectin reverses β-Cell damage and impaired insulin secretion induced by obesity. Aging Cell 2023, 22, e13827. [Google Scholar] [CrossRef] [PubMed]
- Blüher, M.; Kahn, B.B.; Kahn, C.R. Extended longevity in mice lacking the insulin receptor in adipose tissue. Science 2003, 299, 572–574. [Google Scholar] [CrossRef]
- Bartke, A.; Wright, J.C.; Mattison, J.A.; Ingram, D.K.; Miller, R.A.; Roth, G.S. Extending the lifespan of long-lived mice. Nature 2001, 414, 412. [Google Scholar] [CrossRef]
- Ott, B.; Skurk, T.; Hastreiter, L.; Lagkouvardos, I.; Fischer, S.; Büttner, J.; Kellerer, T.; Clavel, T.; Rychlik, M.; Haller, D.; et al. Effect of caloric restriction on gut permeability, inflammation markers, and fecal microbiota in obese women. Sci. Rep. 2017, 7, 11955. [Google Scholar] [CrossRef]
- Pareja-Galeano, H.; Santos-Lozano, A.; Sanchis-Gomar, F.; Fiuza-Luces, C.; Garatachea, N.; Gálvez, B.G.; Lucia, A.; Emanuele, E. Circulating leptin and adiponectin concentrations in healthy exceptional longevity. Mech. Ageing Dev. 2017, 162, 129–132. [Google Scholar] [CrossRef]
- Arai, Y.; Kamide, K.; Hirose, N. Adipokines and Aging: Findings from Centenarians and the Very Old. Front. Endocrinol. 2019, 10, 142. [Google Scholar] [CrossRef] [PubMed]
- Itoh, N. FGF21 as a Hepatokine, Adipokine, and Myokine in Metabolism and Diseases. Front. Endocrinol. 2014, 5, 107. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, T.; Nakatake, Y.; Konishi, M.; Itoh, N. Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochim. Biophys. Acta 2000, 1492, 203–206. [Google Scholar] [CrossRef] [PubMed]
- Inagaki, T.; Dutchak, P.; Zhao, G.; Ding, X.; Gautron, L.; Parameswara, V.; Li, Y.; Goetz, R.; Mohammadi, M.; Esser, V.; et al. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 2007, 5, 415–425. [Google Scholar] [CrossRef] [PubMed]
- Gimeno, R.E.; Moller, D.E. FGF21-based pharmacotherapy--potential utility for metabolic disorders. Trends Endocrinol. Metab. 2014, 25, 303–311. [Google Scholar] [CrossRef] [PubMed]
- Schlein, C.; Talukdar, S.; Heine, M.; Fischer, A.W.; Krott, L.M.; Nilsson, S.K.; Brenner, M.B.; Heeren, J.; Scheja, L. FGF21 Lowers Plasma Triglycerides by Accelerating Lipoprotein Catabolism in White and Brown Adipose Tissues. Cell Metab. 2016, 23, 441–453. [Google Scholar] [CrossRef] [PubMed]
- Ogawa, Y.; Kurosu, H.; Yamamoto, M.; Nandi, A.; Rosenblatt, K.P.; Goetz, R.; Eliseenkova, A.V.; Mohammadi, M.; Kuro-o, M. BetaKlotho is required for metabolic activity of fibroblast growth factor. Proc. Natl. Acad. Sci. USA 2007, 104, 7432–7437. [Google Scholar] [CrossRef]
- Kharitonenkov, A.; Dunbar, J.D.; Bina, H.A.; Bright, S.; Moyers, J.S.; Zhang, C.; Ding, L.; Micanovic, R.; Mehrbod, S.F.; Knierman, M.D.; et al. FGF-21/FGF-21 receptor interaction and activation is determined by betaKlotho. J. Cell Physiol. 2008, 215, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Inagaki, T.; Lin, V.Y.; Goetz, R.; Mohammadi, M.; Mangelsdorf, D.J.; Kliewer, S.A. Inhibition of growth hormone signaling by the fasting-induced hormone FGF21. Cell Metab. 2008, 8, 77–83. [Google Scholar] [CrossRef]
- Kubicky, R.A.; Wu, S.; Kharitonenkov, A.; De Luca, F. Role of fibroblast growth factor 21 (FGF21) in undernutrition-related attenuation of growth in mice. Endocrinology 2012, 153, 2287–2295. [Google Scholar] [CrossRef]
- Lin, Z.; Tian, H.; Lam, K.S.; Lin, S.; Hoo, R.C.; Konishi, M.; Itoh, N.; Wang, Y.; Bornstein, S.R.; Xu, A.; et al. Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metab. 2013, 17, 779–789. [Google Scholar] [CrossRef] [PubMed]
- Holland, W.L.; Adams, A.C.; Brozinick, J.T.; Bui, H.H.; Miyauchi, Y.; Kusminski, C.M.; Bauer, S.M.; Wade, M.; Singhal, E.; Cheng, C.C.; et al. An FGF21-Adiponectin-Ceramide Axis Controls Energy Expenditure and Insulin Action in Mice. Cell Metab. 2013, 17, 790–797. [Google Scholar] [CrossRef] [PubMed]
- Cook, K.S.; Min, H.Y.; Johnson, D.; Chaplinsky, R.J.; Flier, J.S.; Hunt, C.R.; Spiegelman, B.M. Adipsin: A circulating serine protease homolog secreted by adipose tissue and sciatic nerve. Science 1987, 237, 402–405. [Google Scholar] [CrossRef] [PubMed]
- Flier, J.S.; Cook, K.S.; Usher, P.; Spiegelman, B.M. Severely impaired adipsin expression in genetic and acquired obesity. Science. 1987, 237, 405–408. [Google Scholar] [CrossRef]
- Choy, L.N.; Rosen, B.S.; Spiegelman, B.M. Adipsin and an endogenous pathway of complement from adipose cells. J. Biol. Chem. 1992, 267, 12736–12741. [Google Scholar] [CrossRef] [PubMed]
- Tontonoz, P.; Hu, E.; Spiegelman, B.M. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 1994, 79, 1147–1156. [Google Scholar] [CrossRef] [PubMed]
- Lo, J.C.; Ljubicic, S.; Leibiger, B.; Kern, M.; Leibiger, I.B.; Moede, T.; Kelly, M.E.; Chatterjee Bhowmick, D.; Murano, I.; Cohen, P.; et al. Adipsin is an adipokine that improves β cell function in diabetes. Cell 2014, 158, 41–53. [Google Scholar] [CrossRef] [PubMed]
- Aaron, N.; Kraakman, M.J.; Zhou, Q.; Liu, Q.; Costa, S.; Yang, J.; Liu, L.; Yu, L.; Wang, L.; He, Y.; et al. Adipsin promotes bone marrow adiposity by priming mesenchymal stem cells. eLife 2021, 10, e69209. [Google Scholar] [CrossRef] [PubMed]
- Tatemoto, K.; Hosoya, M.; Habata, Y.; Fujii, R.; Kakegawa, T.; Zou, M.X.; Kawamata, Y.; Fukusumi, S.; Hinuma, S.; Kitada, C.; et al. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun. 1998, 251, 471–476. [Google Scholar] [CrossRef]
- Boucher, J.; Masri, B.; Daviaud, D.; Gesta, S.; Guigné, C.; Mazzucotelli, A.; Castan-Laurell, I.; Tack, I.; Knibiehler, B.; Carpéné, C.; et al. Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 2005, 146, 1764–1771. [Google Scholar] [CrossRef]
- Cirillo, P.; Ziviello, F.; Pellegrino, G.; Conte, S.; Cimmino, G.; Giaquinto, A.; Pacifico, F.; Leonardi, A.; Golino, P.; Trimarco, B. The adipokine apelin-13 induces expression of prothrombotic tissue factor. Thromb. Haemost. 2015, 113, 363–372. [Google Scholar] [CrossRef] [PubMed]
- Castan-Laurell, I.; Masri, B.; Valet, P. The apelin/APJ system as a therapeutic target in metabolic diseases. Expert Opin. Ther. Targets 2019, 23, 215–225. [Google Scholar] [CrossRef] [PubMed]
- Hu, G.; Wang, Z.; Zhang, R.; Sun, W.; Chen, X. The Role of Apelin/Apelin Receptor in Energy Metabolism and Water Homeostasis: A Comprehensive Narrative Review. Front. Physiol. 2021, 12, 632886. [Google Scholar] [CrossRef] [PubMed]
- Li, L.; Yang, G.; Li, Q.; Tang, Y.; Yang, M.; Yang, H.; Li, K. Changes and relations of circulating visfatin, apelin, and resistin levels in normal, impaired glucose tolerance, and type 2 diabetic subjects. Exp. Clin. Endocrinol. Diabetes 2006, 114, 544–548. [Google Scholar] [CrossRef] [PubMed]
- Soriguer, F.; Garrido-Sanchez, L.; Garcia-Serrano, S.; Garcia-Almeida, J.M.; Garcia-Arnes, J.; Tinahones, F.J.; Garcia-Fuentes, E. Apelin levels are increased in morbidly obese subjects with type 2 diabetes mellitus. Obes. Surg. 2009, 19, 1574–1580. [Google Scholar] [CrossRef] [PubMed]
- Attané, C.; Foussal, C.; Le Gonidec, S.; Benani, A.; Daviaud, D.; Wanecq, E.; Guzmán-Ruiz, R.; Dray, C.; Bezaire, V.; Rancoule, C.; et al. Apelin treatment increases complete Fatty Acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes 2012, 61, 310–320. [Google Scholar] [CrossRef] [PubMed]
- Li, M.; Fang, H.; Hu, J. Apelin-13 ameliorates metabolic and cardiovascular disorders in a rat model of type 2 diabetes with a high-fat diet. Mol. Med. Rep. 2018, 18, 5784–5790. [Google Scholar] [CrossRef] [PubMed]
- Maguire, J.J.; Kleinz, M.J.; Pitkin, S.L.; Davenport, A.P. [Pyr1]apelin-13 identified as the predominant apelin isoform in the human heart: Vasoactive mechanisms and inotropic action in disease. Hypertension 2009, 54, 598–604. [Google Scholar] [CrossRef] [PubMed]
- Yu, X.H.; Tang, Z.B.; Liu, L.J.; Qian, H.; Tang, S.L.; Zhang, D.W.; Tian, G.P.; Tang, C.K. Apelin and its receptor APJ in cardiovascular diseases. Clin. Chim. Acta 2014, 428, 1–8. [Google Scholar] [CrossRef]
- Chong, K.S.; Gardner, R.S.; Morton, J.J.; Ashley, E.A.; McDonagh, T.A. Plasma concentrations of the novel peptide apelin are decreased in patients with chronic heart failure. Eur. J. Heart Fail. 2006, 8, 355–360. [Google Scholar] [CrossRef]
- Zhou, Q.; Chen, L.; Tang, M.; Guo, Y.; Li, L. Apelin/APJ system: A novel promising target for anti-aging intervention. Clin. Chim. Acta 2018, 487, 233–240. [Google Scholar] [CrossRef] [PubMed]
- Yue, P.; Jin, H.; Aillaud, M.; Deng, A.C.; Azuma, J.; Asagami, T.; Kundu, R.K.; Reaven, G.M.; Quertermous, T.; Tsao, P.S. Apelin is necessary for the maintenance of insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 2010, 298, E59–E67. [Google Scholar] [CrossRef] [PubMed]
- Yang, R.Z.; Lee, M.J.; Hu, H.; Pray, J.; Wu, H.B.; Hansen, B.C.; Shuldiner, A.R.; Fried, S.K.; McLenithan, J.C.; Gong, D.W. Identification of omentin as a novel depot-specific adipokine in human adipose tissue: Possible role in modulating insulin action. Am. J. Physiol. Endocrinol. Metab. 2006, 290, E1253–E2361. [Google Scholar] [CrossRef] [PubMed]
- Pan, H.Y.; Guo, L.; Li, Q. Changes of serum omentin-1 levels in normal subjects and in patients with impaired glucose regulation and with newly diagnosed and untreated type 2 diabetes. Diabetes Res. Clin. Pract. 2010, 88, 29–33. [Google Scholar] [CrossRef]
- de Souza Batista, C.M.; Yang, R.Z.; Lee, M.J.; Glynn, N.M.; Yu, D.Z.; Pray, J.; Ndubuizu, K.; Patil, S.; Schwartz, A.; Kligman, M.; et al. Omentin plasma levels and gene expression are decreased in obesity. Diabetes 2007, 56, 1655–1661. [Google Scholar] [CrossRef] [PubMed]
- Tan, B.K.; Adya, R.; Farhatullah, S.; Lewandowski, K.C.; O’Hare, P.; Lehnert, H.; Randeva, H.S. Omentin-1, a novel adipokine, is decreased in overweight insulin-resistant women with polycystic ovary syndrome: Ex vivo and in vivo regulation of omentin-1 by insulin and glucose. Diabetes 2008, 57, 801–808. [Google Scholar] [CrossRef] [PubMed]
- Yamawaki, H.; Kuramoto, J.; Kameshima, S.; Usui, T.; Okada, M.; Hara, Y. Omentin, a novel adipocytokine inhibits TNF-induced vascular inflammation in human endothelial cells. Biochem. Biophys. Res. Commun. 2011, 408, 339–343. [Google Scholar] [CrossRef]
- Lin, X.; Sun, Y.; Yang, S.; Yu, M.; Pan, L.; Yang, J.; Yang, J.; Shao, Q.; Liu, J.; Liu, Y.; et al. Omentin-1 Modulates Macrophage Function via Integrin Receptors αvβ3 and αvβ5 and Reverses Plaque Vulnerability in Animal Models of Atherosclerosis. Front. Cardiovasc. Med. 2021, 8, 757926. [Google Scholar] [CrossRef]
- Shibata, R.; Takahashi, R.; Kataoka, Y.; Ohashi, K.; Ikeda, N.; Kihara, S.; Murohara, T.; Ouchi, N. Association of a fat-derived plasma protein omentin with carotid artery intima-media thickness in apparently healthy men. Hypertens. Res. 2011, 34, 1309–1312. [Google Scholar] [CrossRef]
- Shibata, R.; Ouchi, N.; Kikuchi, R.; Takahashi, R.; Takeshita, K.; Kataoka, Y.; Ohashi, K.; Ikeda, N.; Kihara, S.; Murohara, T. Circulating omentin is associated with coronary artery disease in men. Atherosclerosis 2011, 219, 811–814. [Google Scholar] [CrossRef]
- Gerke, V.; Creutz, C.E.; Moss, S.E. Annexins: Linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell. Biol. 2005, 6, 449–461. [Google Scholar] [CrossRef] [PubMed]
- Moss, S.E.; Morgan, R.O. The annexins. Genome Biol. 2004, 5, 219. [Google Scholar] [CrossRef] [PubMed]
- Akasheh, R.T.; Pini, M.; Pang, J.; Fantuzzi, G. Increased adiposity in annexin A1-deficient mice. PLoS ONE 2013, 8, e82608. [Google Scholar] [CrossRef] [PubMed]
- Aguilera, C.M.; Gomez-Llorente, C.; Tofe, I.; Gil-Campos, M.; Cañete, R.; Gil, Á. Genome-wide expression in visceral adipose tissue from obese prepubertal children. Int. J. Mol. Sci. 2015, 16, 7723–7737. [Google Scholar] [CrossRef] [PubMed]
- Perretti, M.; D’Acquisto, F. Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 2009, 9, 62–70. [Google Scholar] [CrossRef] [PubMed]
- Locatelli, I.; Sutti, S.; Jindal, A.; Vacchiano, M.; Bozzola, C.; Reutelingsperger, C.; Kusters, D.; Bena, S.; Parola, M.; Paternostro, C.; et al. Endogenous annexin A1 is a novel protective determinant in nonalcoholic steatohepatitis in mice. Hepatology 2014, 60, 531–544. [Google Scholar] [CrossRef]
- Grewal, T.; Enrich, C.; Rentero, C.; Buechler, C. Annexins in Adipose Tissue: Novel Players in Obesity. Int. J. Mol. Sci. 2019, 20, 3449. [Google Scholar] [CrossRef] [PubMed]
- You, Q.; Ke, Y.; Chen, X.; Yan, W.; Li, D.; Chen, L.; Wang, R.; Yu, J.; Hong, H. Loss of Endothelial Annexin A1 Aggravates Inflammation-Induched Vascular Aging. Adv. Sci. 2024, e2307040. [Google Scholar] [CrossRef]
- Falls, D.L. Neuregulins: Functions, forms, and signaling strategies. Exp. Cell Res. 2003, 284, 14–30. [Google Scholar] [CrossRef]
- Meyer, D.; Yamaai, T.; Garratt, A.; Riethmacher-Sonnenberg, E.; Kane, D.; Theill, L.E.; Birchmeier, C. Isoform-specific expression and function of neuregulin. Development 1997, 124, 3575–3586. [Google Scholar] [CrossRef]
- Caillaud, K.; Boisseau, N.; Ennequin, G.; Chavanelle, V.; Etienne, M.; Li, X.; Denis, P.; Dardevet, D.; Lacampagne, A.; Sirvent, P. Neuregulin 1 improves glucose tolerance in adult and old rats. Diabetes Metab. 2016, 42, 96–104. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.X.; Zhao, X.Y.; Meng, Z.X.; Kern, M.; Dietrich, A.; Chen, Z.; Cozacov, Z.; Zhou, D.; Okunade, A.L.; Su, X.; et al. The brown fat-enriched secreted factor Nrg4 preserves metabolic homeostasis through attenuation of hepatic lipogenesis. Nat. Med. 2014, 20, 1436–1443. [Google Scholar] [CrossRef] [PubMed]
- 83 Csongrádi, É.; Káplár, M.; Nagy, B., Jr.; Koch, C.A.; Juhász, A.; Bajnok, L.; Varga, Z.; Seres, I.; Karányi, Z.; Magyar, M.T.; et al. Adipokines as atherothrombotic risk factors in obese subjects: Associations with haemostatic markers and common carotid wall thickness. Nutr. Metab. Cardiovasc. Dis. 2017, 27, 571–580. [Google Scholar] [CrossRef] [PubMed]
- Jung, C.H.; Kim, B.Y.; Mok, J.O.; Kang, S.K.; Kim, C.H. Association between serum adipocytokine levels and microangiopathies in patients with type 2 diabetes mellitus. J. Diabetes Investig. 2014, 5, 333–339. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Proenca, R.; Maffei, M.; Barone, M.; Leopold, L.; Friedman, J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372, 425–432. [Google Scholar] [CrossRef] [PubMed]
- Flehmig, G.; Scholz, M.; Klöting, N.; Fasshauer, M.; Tönjes, A.; Stumvoll, M.; Youn, B.S.; Blüher, M. Identification of adipokine clusters related to parameters of fat mass, insulin sensitivity and inflammation. PLoS ONE 2014, 9, e99785. [Google Scholar] [CrossRef]
- Chandra, A.; Neeland, I.J.; Berry, J.D.; Ayers, C.R.; Rohatgi, A.; Das, S.R.; Khera, A.; McGuire, D.K.; de Lemos, J.A.; Turer, A.T. The relationship of body mass and fat distribution with incident hypertension: Observations from the Dallas Heart Study. J. Am. Coll. Cardiol. 2014, 64, 997–1002. [Google Scholar] [CrossRef] [PubMed]
- Guan, X.M.; Yu, H.; Van der Ploeg, L.H. Evidence of altered hypothalamic pro-opiomelanocortin/neuropeptide Y mRNA expression in tubby mice. Brain Res. Mol. Brain Res. 1998, 59, 273–279. [Google Scholar] [CrossRef]
- Ge, T.T.; Yao, X.X.; Zhao, F.L.; Zou, X.H.; Yang, W.; Cui, R.J.; Li, B.J. Role of leptin in the regulation of food intake in fasted mice. J. Cell. Mol. Med. 2020, 24, 4524–4532. [Google Scholar] [CrossRef]
- Shimabukuro, M.; Koyama, K.; Chen, G.; Wang, M.Y.; Trieu, F.; Lee, Y.; Newgard, C.B.; Unger, R.H. Direct antidiabetic effect of leptin through triglyceride depletion of tissues. Proc. Natl. Acad. Sci. USA 1997, 94, 4637–4641. [Google Scholar] [CrossRef]
- Savage, D.B.; O’Rahilly, S. Leptin: A novel therapeutic role in lipodystrophy. J. Clin. Investig. 2002, 109, 1285–1286. [Google Scholar] [CrossRef] [PubMed]
- Frühbeck, G.; Catalán, V.; Rodríguez, A.; Gómez-Ambrosi, J. Adiponectin-leptin ratio: A promising index to estimate adipose tissue dysfunction. Relation with obesity-associated cardiometabolic risk. Adipocyte 2018, 7, 57–62. [Google Scholar] [CrossRef] [PubMed]
- Blüher, M.; Mantzoros, C.S. From leptin to other adipokines in health and disease: Facts and expectations at the beginning of the 21st century. Metabolism 2015, 64, 131–145. [Google Scholar] [CrossRef] [PubMed]
- Mantzoros, C.S.; Magkos, F.; Brinkoetter, M.; Sienkiewicz, E.; Dardeno, T.A.; Kim, S.Y.; Hamnvik, O.P.; Koniaris, A. Leptin in human physiology and pathophysiology. Am. J. Physiol. Endocrinol. Metab. 2011, 301, E567–E584. [Google Scholar] [CrossRef] [PubMed]
- Parhami, F.; Tintut, Y.; Ballard, A.; Fogelman, A.M.; Demer, L.L. Leptin enhances the calcification of vascular cells: Artery wall as a target of leptin. Circ. Res. 2001, 88, 954–960. [Google Scholar] [CrossRef]
- Steppan, C.M.; Bailey, S.T.; Bhat, S.; Brown, E.J.; Banerjee, R.R.; Wright, C.M.; Patel, H.R.; Ahima, R.S.; Lazar, M.A. The hormone resistin links obesity to diabetes. Nature 2001, 409, 307–312. [Google Scholar] [CrossRef]
- Lehrke, M.; Reilly, M.P.; Millington, S.C.; Iqbal, N.; Rader, D.J.; Lazar, M.A. An inflammatory cascade leading to hyperresistinemia in humans. PLoS Med. 2004, 1, e45. [Google Scholar] [CrossRef]
- Silswal, N.; Singh, A.K.; Aruna, B.; Mukhopadhyay, S.; Ghosh, S.; Ehtesham, N.Z. Human resistin stimulates the pro-inflammatory cytokines TNF-alpha and IL-12 in macrophages by NF-kappaB-dependent pathway. Biochem. Biophys. Res. Commun. 2005, 334, 1092–1101. [Google Scholar] [CrossRef] [PubMed]
- Fain, J.N.; Cheema, P.S.; Bahouth, S.W.; Hiler, M.L. Resistin release by human adipose tissue explants in primary culture. Biochem. Biophys. Res. Commun. 2003, 300, 674–678. [Google Scholar] [CrossRef]
- Patel, L.; Buckels, A.C.; Kinghorn, I.J.; Murdock, P.R.; Holbrook, J.D.; Plumpton, C.; Macphee, C.H.; Smith, S.A. Resistin is expressed in human macrophages and directly regulated by PPAR gamma activators. Biochem. Biophys. Res. Commun. 2003, 300, 472–476. [Google Scholar] [CrossRef]
- Ghosh, S.; Singh, A.K.; Aruna, B.; Mukhopadhyay, S.; Ehtesham, N.Z. The genomic organization of mouse resistin reveals major differences from the human resistin: Functional implications. Gene 2003, 305, 27–34. [Google Scholar] [CrossRef] [PubMed]
- Filková, M.; Haluzík, M.; Gay, S.; Senolt, L. The role of resistin as a regulator of inflammation: Implications for various human pathologies. Clin. Immunol. 2009, 133, 157–170. [Google Scholar] [CrossRef] [PubMed]
- Gnacińska, M.; Małgorzewicz, S.; Stojek, M.; Łysiak-Szydłowska, W.; Sworczak, K. Role of adipokines in complications related to obesity: A review. Adv. Med. Sci. 2009, 54, 150–157. [Google Scholar] [CrossRef] [PubMed]
- Cardoso, A.L.; Fernandes, A.; Aguilar-Pimentel, J.A.; de Angelis, M.H.; Guedes, J.R.; Brito, M.A.; Ortolano, S.; Pani, G.; Athanasopoulou, S.; Gonos, E.S.; et al. Towards frailty biomarkers: Candidates from genes and pathways regulated in aging and age-related diseases. Ageing Res. Rev. 2018, 47, 214–277. [Google Scholar] [CrossRef]
- Parkkila, K.; Kiviniemi, A.; Tulppo, M.; Perkiömäki, J.; Kesäniemi, Y.A.; Ukkola, O. Resistin is a risk factor for all-cause mortality in elderly Finnish population: A prospective study in the OPERA cohort. PLoS ONE 2021, 16, e0248015. [Google Scholar] [CrossRef] [PubMed]
- Yu, A.; Zheng, Y.; Zhang, R.; Huang, J.; Zhu, Z.; Zhou, R.; Jin, D.; Yang, Z. Resistin impairs SIRT1 function and induces senescence-associated phenotype in hepatocytes. Mol. Cell. Endocrinol. 2013, 377, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Ruderman, N.B.; Xu, X.J.; Nelson, L.; Cacicedo, J.M.; Saha, A.K.; Lan, F.; Ido, Y. AMPK and SIRT1: A long-standing partnership? Am. J. Physiol. Endocrinol. Metab. 2010, 298, E751–E760. [Google Scholar] [CrossRef] [PubMed]
- Samal, B.; Sun, Y.; Stearns, G.; Xie, C.; Suggs, S.; McNiece, I. Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol. Cell. Biol. 1994, 14, 1431–1437. [Google Scholar] [CrossRef] [PubMed]
- Fukuhara, A.; Matsuda, M.; Nishizawa, M.; Segawa, K.; Tanaka, M.; Kishimoto, K.; Matsuki, Y.; Murakami, M.; Ichisaka, T.; Murakami, H.; et al. Visfatin: A protein secreted by visceral fat that mimics the effects of insulin. Science 2005, 307, 426–430. [Google Scholar] [CrossRef]
- Chang, Y.H.; Chang, D.M.; Lin, K.C.; Shin, S.J.; Lee, Y.J. Visfatin in overweight/obesity, type 2 diabetes mellitus, insulin resistance, metabolic syndrome and cardiovascular diseases: A meta-analysis and systemic review. Diabetes Metab. Res. Rev. 2011, 27, 515–527. [Google Scholar] [CrossRef]
- Lin, Y.T.; Chen, L.K.; Jian, D.Y.; Hsu, T.C.; Huang, W.C.; Kuan, T.T.; Wu, S.Y.; Kwok, C.F.; Ho, L.T.; Juan, C.C. Visfatin Promotes Monocyte Adhesion by Upregulating ICAM-1 and VCAM-1 Expression in Endothelial Cells via Activation of p38-PI3K-Akt Signaling and Subsequent ROS Production and IKK/NF-κB Activation. Cell Physiol. Biochem. 2019, 52, 1398–1411. [Google Scholar] [CrossRef] [PubMed]
- Araki, T.; Sasaki, Y.; Milbrandt, J. Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 2004, 305, 1010–1013. [Google Scholar] [CrossRef]
- Pillai, J.B.; Isbatan, A.; Imai, S.; Gupta, M.P. Poly(ADP-ribose) polymerase-1-dependent cardiac myocyte cell death during heart failure is mediated by NAD+ depletion and reduced Sir2alpha deacetylase activity. J. Biol. Chem. 2005, 280, 43121–43130. [Google Scholar] [CrossRef]
- Nielsen, K.N.; Peics, J.; Ma, T.; Karavaeva, I.; Dall, M.; Chubanava, S.; Basse, A.L.; Dmytriyeva, O.; Treebak, J.T.; Gerhart-Hines, Z. NAMPT-mediated NAD+ biosynthesis is indispensable for adipose tissue plasticity and development of obesity. Mol. Metab. 2018, 11, 178–188. [Google Scholar] [CrossRef]
- Yoshida, M.; Satoh, A.; Lin, J.B.; Mills, K.F.; Sasaki, Y.; Rensing, N.; Wong, M.; Apte, R.S.; Imai, S.I. Extracellular Vesicle-Contained eNAMPT Delays Aging and Extends Lifespan in Mice. Cell Metab. 2019, 30, 329–342.e5. [Google Scholar] [CrossRef] [PubMed]
- Ernst, M.C.; Sinal, C.J. Chemerin: At the crossroads of inflammation and obesity. Trends Endocrinol. Metab. 2010, 21, 660–667. [Google Scholar] [CrossRef]
- Muruganandan, S.; Roman, A.A.; Sinal, C.J. Role of chemerin/CMKLR1 signaling in adipogenesis and osteoblastogenesis of bone marrow stem cells. J. Bone Miner. Res. 2010, 25, 222–234. [Google Scholar] [CrossRef]
- Muruganandan, S.; Parlee, S.D.; Rourke, J.L.; Ernst, M.C.; Goralski, K.B.; Sinal, C.J. Chemerin, a novel peroxisome proliferator-activated receptor gamma (PPARgamma) target gene that promotes mesenchymal stem cell adipogenesis. J. Biol. Chem. 2011, 286, 23982–23995. [Google Scholar] [CrossRef] [PubMed]
- Wittamer, V.; Franssen, J.D.; Vulcano, M.; Mirjolet, J.F.; Le Poul, E.; Migeotte, I.; Brézillon, S.; Tyldesley, R.; Blanpain, C.; Detheux, M.; et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J. Exp. Med. 2003, 198, 977–985. [Google Scholar] [CrossRef]
- Goralski, K.B.; McCarthy, T.C.; Hanniman, E.A.; Zabel, B.A.; Butcher, E.C.; Parlee, S.D.; Muruganandan, S.; Sinal, C.J. Chemerin, a novel adipokine that regulates adipogenesis and adipocyte metabolism. J. Biol. Chem. 2007, 282, 28175–28188. [Google Scholar] [CrossRef]
- Du, X.Y.; Zabel, B.A.; Myles, T.; Allen, S.J.; Handel, T.M.; Lee, P.P.; Butcher, E.C.; Leung, L.L. Regulation of chemerin bioactivity by plasma carboxypeptidase N, carboxypeptidase B (activated thrombin-activable fibrinolysis inhibitor), and platelets. J. Biol. Chem. 2009, 284, 751–758. [Google Scholar] [CrossRef] [PubMed]
- Ernst, M.C.; Issa, M.; Goralski, K.B.; Sinal, C.J. Chemerin exacerbates glucose intolerance in mouse models of obesity and diabetes. Endocrinology 2010, 151, 1998–2007. [Google Scholar] [CrossRef] [PubMed]
- Yun, H.; Dumbell, R.; Hanna, K.; Bowen, J.; McLean, S.L.; Kantamneni, S.; Pors, K.; Wu, Q.F.; Helfer, G. The Chemerin-CMKLR1 Axis is Functionally important for Central Regulation of Energy Homeostasis. Front. Physiol. 2022, 13, 897105. [Google Scholar] [CrossRef] [PubMed]
- Bozaoglu, K.; Curran, J.E.; Stocker, C.J.; Zaibi, M.S.; Segal, D.; Konstantopoulos, N.; Morrison, S.; Carless, M.; Dyer, T.D.; Cole, S.A.; et al. Chemerin, a novel adipokine in the regulation of angiogenesis. J. Clin. Endocrinol. Metab. 2010, 95, 2476–2485. [Google Scholar] [CrossRef] [PubMed]
- Buechler, C.; Feder, S.; Haberl, E.M.; Aslanidis, C. Chemerin Isoforms and Activity in Obesity. Int. J. Mol. Sci. 2019, 20, 1128. [Google Scholar] [CrossRef] [PubMed]
- Wittamer, V.; Bondue, B.; Guillabert, A.; Vassart, G.; Parmentier, M.; Communi, D. Neutrophil-mediated maturation of chemerin: A link between innate and adaptive immunity. J. Immunol. 2005, 175, 487–493. [Google Scholar] [CrossRef]
- Sanchis-Gomar, F.; Pareja-Galeano, H.; Santos-Lozano, A.; Garatachea, N.; Fiuza-Luces, C.; Venturini, L.; Ricevuti, G.; Lucia, A.; Emanuele, E. A preliminary candidate approach identifies the combination of chemerin, fetuin-A, and fibroblast growth factors 19 and 21 as a potential biomarker panel of successful aging. AGE 2015, 37, 42. [Google Scholar] [CrossRef] [PubMed]
- Stefanov, T.; Blüher, M.; Vekova, A.; Bonova, I.; Tzvetkov, S.; Kurktschiev, D.; Temelkova-Kurktschiev, T. Circulating chemerin decreases in response to a combined strength and endurance training. Endocrine 2014, 45, 382–391. [Google Scholar] [CrossRef] [PubMed]
- Hida, K.; Wada, J.; Eguchi, J.; Zhang, H.; Baba, M.; Seida, A.; Hashimoto, I.; Okada, T.; Yasuhara, A.; Nakatsuka, A.; et al. Visceral adipose tissue-derived serine protease inhibitor: A unique insulin-sensitizing adipocytokine in obesity. Proc. Natl. Acad. Sci. USA 2005, 202, 10610–10615. [Google Scholar] [CrossRef]
- Feng, R.; Li, Y.; Wang, C.; Luo, C.; Liu, L.; Chuo, F.; Li, Q.; Sun, C. Higher vaspin levels in subjects with obesity and type 2 diabetes mellitus: A meta-analysis. Diabetes Res. Clin. Pract. 2014, 106, 88–94. [Google Scholar] [CrossRef]
- Youn, B.S.; Klöting, N.; Kratzsch, J.; Lee, N.; Park, J.W.; Song, E.S.; Ruschke, K.; Oberbach, A.; Fasshauer, M.; Stumvoll, M.; et al. Serum vaspin concentrations in human obesity and type 2 diabetes. Diabetes 2008, 57, 372–377. [Google Scholar] [CrossRef] [PubMed]
- Kurowska, P.; Mlyczyńska, E.; Dawid, M.; Jurek, M.; Klimczyk, D.; Dupont, J.; Rak, A. Review: Vaspin (SERPINA12) Expression and Function in Endocrine Cells. Cells 2021, 10, 1710. [Google Scholar] [CrossRef] [PubMed]
- Liu, P.; Li, G.; Wu, J.; Zhou, X.; Wang, L.; Han, W.; Lv, Y.; Sun, C. Vaspin promotes 3T3-L1 preadipocyte differentiation. Exp. Biol. Med. 2015, 240, 1520–1527. [Google Scholar] [CrossRef] [PubMed]
- Nicholson, T.; Church, C.; Tsintzas, K.; Jones, R.; Breen, L.; Davis, E.T.; Baker, D.J.; Jones, S.W. Vaspin promotes insulin sensitivity of elderly muscle and is upregulated in obesity. J. Endocrinol. 2019, 241, 31–43. [Google Scholar] [CrossRef] [PubMed]
- Heneka, M.T.; Carson, M.J.; El Khoury, J.; Landreth, G.E.; Brosseron, F.; Feinstein, D.L.; Jacobs, A.H.; Wyss-Coray, T.; Vitorica, J.; Ransohoff, R.M.; et al. Neuroinflammation in Alzheimer’s disease. Lancet Neurol. 2015, 14, 388–405. [Google Scholar] [CrossRef] [PubMed]
- Flo, T.H.; Smith, K.D.; Sato, S.; Rodriguez, D.J.; Holmes, M.A.; Strong, R.K.; Akira, S.; Aderem, A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004, 432, 917–921. [Google Scholar] [CrossRef] [PubMed]
- Yan, Q.W.; Yang, Q.; Mody, N.; Graham, T.E.; Hsu, C.H.; Xu, Z.; Houstis, N.E.; Kahn, B.B.; Rosen, E.D. The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 2007, 56, 2533–2540. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Lam, K.S.; Kraegen, E.W.; Sweeney, G.; Zhang, J.; Tso, A.W.; Chow, W.S.; Wat, N.M.; Xu, J.Y.; Hoo, R.L.; et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin. Chem. 2007, 53, 34–41. [Google Scholar] [CrossRef] [PubMed]
- Guo, H.; Jin, D.; Zhang, Y.; Wright, W.; Bazuine, M.; Brockman, D.A.; Bernlohr, D.A.; Chen, X. Lipocalin-2 deficiency impairs thermogenesis and potentiates diet-induced insulin resistance in mice. Diabetes 2010, 59, 1376–1385. [Google Scholar] [CrossRef]
- Guo, H.; Bazuine, M.; Jin, D.; Huang, M.M.; Cushman, S.W.; Chen, X. Evidence for the regulatory role of lipocalin 2 in high-fat diet-induced adipose tissue remodeling in male mice. Endocrinology 2013, 154, 3525–3538. [Google Scholar] [CrossRef]
- Jin, D.; Guo, H.; Bu, S.Y.; Zhang, Y.; Hannaford, J.; Mashek, D.G.; Chen, X. Lipocalin 2 is a selective modulator of peroxisome proliferator-activated receptor-gamma activation and function in lipid homeostasis and energy expenditure. FASEB J. 2011, 25, 754–764. [Google Scholar] [CrossRef] [PubMed]
- Law, I.K.; Xu, A.; Lam, K.S.; Berger, T.; Mak, T.W.; Vanhoutte, P.M.; Liu, J.T.; Sweeney, G.; Zhou, M.; Yang, B.; et al. Lipocalin-2 deficiency attenuates insulin resistance associated with aging and obesity. Diabetes 2010, 59, 872–882. [Google Scholar] [CrossRef]
- Zhang, J.; Wu, Y.; Zhang, Y.; Leroith, D.; Bernlohr, D.A.; Chen, X. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol. Endocrinol. 2008, 22, 1416–1426. [Google Scholar] [CrossRef] [PubMed]
- Guo, H.; Foncea, R.; O’Byrne, S.M.; Jiang, H.; Zhang, Y.; Deis, J.A.; Blaner, W.S.; Bernlohr, D.A.; Chen, X. Lipocalin 2, a Regulator of Retinoid Homeostasis and Retinoid-mediated Thermogenic Activation in Adipose Tissue. J. Biol. Chem. 2016, 291, 11216–11229. [Google Scholar] [CrossRef] [PubMed]
- Mosialou, I.; Shikhel, S.; Liu, J.M.; Maurizi, A.; Luo, N.; He, Z.; Huang, Y.; Zong, H.; Friedman, R.A.; Barasch, J.; et al. MC4R-dependent suppression of appetite by bone-derived lipocalin 2. Nature. 2017, 543, 385–390. [Google Scholar] [CrossRef] [PubMed]
- Dekens, D.W.; Eisel, U.L.M.; Gouweleeuw, L.; Schoemaker, R.G.; De Deyn, P.P.; Naudé, P.J.W. Lipocalin 2 as a link between ageing, risk factor conditions and age-related brain diseases. Ageing Res. Rev. 2021, 70, 101414. [Google Scholar] [CrossRef]
- Flower, D.R.; North, A.C.; Sansom, C.E. The lipocalin protein family: Structural and sequence overview. Biochim. Biophys. Acta 2000, 1482, 9–24. [Google Scholar] [CrossRef]
- O’Byrne, S.M.; Blaner, W.S. Retinol and retinyl esters: Biochemistry and physiology. J. Lipid Res. 2013, 54, 1731–1743. [Google Scholar] [CrossRef]
- Quadro, L.; Blaner, W.S.; Salchow, D.J.; Vogel, S.; Piantedosi, R.; Gouras, P.; Freeman, S.; Cosma, M.P.; Colantuoni, V.; Gottesman, M.E. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J. 1999, 18, 4633–4644. [Google Scholar] [CrossRef]
- Blaner, W.S. Vitamin A signaling and homeostasis in obesity, diabetes, and metabolic disorders. Pharmacol. Ther. 2019, 197, 153–178. [Google Scholar] [CrossRef]
- Lee, S.A.; Yuen, J.J.; Jiang, H.; Kahn, B.B.; Blaner, W.S. Adipocyte-specific overexpression of retinol-binding protein 4 causes hepatic steatosis in mice. Hepatology 2016, 64, 1534–1546. [Google Scholar] [CrossRef] [PubMed]
- Yang, Q.; Graham, T.E.; Mody, N.; Preitner, F.; Peroni, O.D.; Zabolotny, J.M.; Kotani, K.; Quadro, L.; Kahn, B.B. Serum retinol binding protein 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 2005, 436, 356–362. [Google Scholar] [CrossRef] [PubMed]
- Moraes-Vieira, P.M.; Yore, M.M.; Dwyer, P.M.; Syed, I.; Aryal, P.; Kahn, B.B. RBP4 activates antigen-presenting cells, leading to adipose tissue inflammation and systemic insulin resistance. Cell Metab. 2014, 19, 512–526. [Google Scholar] [CrossRef] [PubMed]
- Moraes-Vieira, P.M.; Yore, M.M.; Sontheimer-Phelps, A.; Castoldi, A.; Norseen, J.; Aryal, P.; Simonyté Sjödin, K.; Kahn, B.B. Retinol binding protein 4 primes the NLRP3 inflammasome by signaling through Toll-like receptors 2 and 4. Proc. Natl. Acad. Sci. USA 2020, 117, 31309–31318. [Google Scholar] [CrossRef] [PubMed]
- McInnes, K.J.; Smith, L.B.; Hunger, N.I.; Saunders, P.T.; Andrew, R.; Walker, B.R. Deletion of the androgen receptor in adipose tissue in male mice elevates retinol binding protein 4 and reveals independent effects on visceral fat mass and on glucose homeostasis. Diabetes 2012, 61, 1072–1081. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Shen, T.; Li, Q.; Chen, X.; Li, Y.; Li, D.; Chen, G.; Ling, W.; Chen, Y.M. Retinol Binding Protein-4 Levels and Non-alcoholic Fatty Liver Disease: A community-based cross-sectional study. Sci. Rep. 2017, 7, 45100. [Google Scholar] [CrossRef]
- Liu, Y.; Mu, D.; Chen, H.; Li, D.; Song, J.; Zhong, Y.; Xia, M. Retinol-Binding Protein 4 Induces Hepatic Mitochondrial Dysfunction and Promotes Hepatic Steatosis. J. Clin. Endocrinol. Metab. 2016, 101, 4338–4348. [Google Scholar] [CrossRef]
- Trepanowski, J.F.; Mey, J.; Varady, K.A. Fetuin-A: A novel link between obesity and related complications. Int. J. Obes. 2015, 39, 734–741. [Google Scholar] [CrossRef] [PubMed]
- Chekol Abebe, E.; Tilahun Muche, Z.; Behaile T/Mariam, A.; Mengie Ayele, T.; Mekonnen Agidew, M.; Teshome Azezew, M.; Abebe Zewde, E.; Asmamaw Dejenie, T.; Asmamaw Mengstie, M. The structure, biosynthesis, and biological roles of fetuin-A: A review. Front. Cell Dev. Biol. 2022, 10, 945287. [Google Scholar] [CrossRef]
- Auberger, P.; Falquerho, L.; Contreres, J.O.; Pages, G.; Le Cam, G.; Rossi, B.; Le Cam, A. Characterization of a natural inhibitor of the insulin receptor tyrosine kinase: cDNA cloning, purification, and anti-mitogenic activity. Cell 1989, 58, 631–640. [Google Scholar] [CrossRef]
- Goustin, A.S.; Derar, N.; Abou-Samra, A.B. Ahsg-fetuin blocks the metabolic arm of insulin action through its interaction with the 95-kD β-subunit of the insulin receptor. Cell Signal. 2013, 25, 981–988. [Google Scholar] [CrossRef] [PubMed]
- Dogru, T.; Kirik, A.; Gurel, H.; Rizvi, A.A.; Rizzo, M.; Sonmez, A. The Evolving Role of Fetuin-A in Nonalcoholic Fatty Liver Disease: An Overview from Liver to the Heart. Int. J. Mol. Sci. 2021, 22, 6627. [Google Scholar] [CrossRef]
- Reinehr, T. Inflammatory markers in children and adolescents with type 2 diabetes mellitus. Clin. Chim. Acta 2019, 496, 100–107. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Z.; Sun, M.; Jin, H.; Chen, H.; Ju, H. Fetuin-a to adiponectin ratio is a sensitive indicator for evaluating metabolic syndrome in the elderly. Lipids Health Dis. 2020, 19, 61. [Google Scholar] [CrossRef]
- Reynolds, J.L.; Skepper, J.N.; McNair, R.; Kasama, T.; Gupta, K.; Weissberg, P.L.; Jahnen-Dechent, W.; Shanahan, C.M. Multifunctional roles for serum protein fetuin-a in inhibition of human vascular smooth muscle cell calcification. J. Am. Soc. Nephrol. 2005, 16, 2920–2930. [Google Scholar] [CrossRef]
- Das, S.; Chattopadhyay, D.; Chatterjee, S.K.; Mondal, S.A.; Majumdar, S.S.; Mukhopadhyay, S.; Saha, N.; Velayutham, R.; Bhattacharya, S.; Mukherjee, S. Increase in PPARγ inhibitory phosphorylation by Fetuin-A through the activation of Ras-MEK-ERK pathway causes insulin resistance. Biochim. Biophys. Acta Mol. Basis Dis. 2021, 1867, 166050. [Google Scholar] [CrossRef]
- Sardana, O.; Goyal, R.; Bedi, O. Molecular and pathobiological involvement of fetuin-A in the pathogenesis of NAFLD. Inflammopharmacology 2021, 29, 1061–1074. [Google Scholar] [CrossRef] [PubMed]
- Hotamisligil, G.S.; Johnson, R.S.; Distel, R.J.; Ellis, R.; Papaioannou, V.E.; Spiegelman, B.M. Uncoupling of obesity from insulin resistance through a targeted mutation in aP2, the adipocyte fatty acid binding protein. Science 1996, 274, 1377–1379. [Google Scholar] [CrossRef]
- Bonen, A.; Campbell, S.E.; Benton, C.R.; Chabowski, A.; Coort, S.L.; Han, X.X.; Koonen, D.P.; Glatz, J.F.; Luiken, J.J. Regulation of fatty acid transport by fatty acid translocase/CD36. Proc. Nutr. Soc. 2004, 63, 245–249. [Google Scholar] [CrossRef]
- Elsas, J.; Sellhaus, B.; Herrmann, M.; Kinkeldey, A.; Weis, J.; Jahnen-Dechent, W.; Häusler, M. Fetuin-a in the developing brain. Dev. Neurobiol. 2013, 73, 354–369. [Google Scholar] [CrossRef]
- Li, W.; Zhu, S.; Li, J.; Huang, Y.; Zhou, R.; Fan, X.; Yang, H.; Gong, X.; Eissa, N.T.; Jahnen-Dechent, W.; et al. A hepatic protein, fetuin-A, occupies a protective role in lethal systemic inflammation. PLoS ONE 2011, 6, e16945. [Google Scholar] [CrossRef] [PubMed]
- Kuk, J.L.; Saunders, T.J.; Davidson, L.E.; Ross, R. Age-related changes in total and regional fat distribution. Ageing Res. Rev. 2009, 8, 339–348. [Google Scholar] [CrossRef] [PubMed]
- Sawaki, D.; Czibik, G.; Pini, M.; Ternacle, J.; Suffee, N.; Mercedes, R.; Marcelin, G.; Surenaud, M.; Marcos, E.; Gual, P.; et al. Visceral Adipose Tissue Drives Cardiac Aging Through Modulation of Fibroblast Senescence by Osteopontin Production. Circulation 2018, 138, 809–822. [Google Scholar] [CrossRef] [PubMed]
- Shin, J.A.; Jeong, S.I.; Kim, M.; Yoon, J.C.; Kim, H.S.; Park, E.M. Visceral adipose tissue inflammation is associated with age-related brain changes and ischemic brain damage in aged mice. Brain Behav. Immun. 2015, 50, 221–231. [Google Scholar] [CrossRef] [PubMed]
- Sánchez-Rodríguez, M.; García-Sánchez, A.; Retana-Ugalde, R.; Mendoza-Núñez, V.M. Serum leptin levels and blood pressure in the overweight elderly. Arch. Med. Res. 2000, 31, 425–428. [Google Scholar] [CrossRef]
- Milek, M.; Moulla, Y.; Kern, M.; Stroh, C.; Dietrich, A.; Schön, M.R.; Gärtner, D.; Lohmann, T.; Dressler, M.; Kovacs, P.; et al. Adipsin Serum Concentrations and Adipose Tissue Expression in People with Obesity and Type 2 Diabetes. Int. J. Mol. Sci. 2022, 23, 2222. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Wen, J.; Lu, Y.; Ji, H.; Zhuang, J.; Su, Y.; Liu, B.; Li, H.; Xu, Y. Impact of age on plasma vaspin concentration in a group of normal Chinese people. J. Endocrinol. Investig. 2017, 40, 143–151. [Google Scholar] [CrossRef] [PubMed]
- Acquarone, E.; Monacelli, F.; Borghi, R.; Nencioni, A.; Odetti, P. Resistin: A reappraisal. Mech. Ageing Dev. 2019, 178, 46–63. [Google Scholar] [CrossRef]
- Schmid, A.; Bala, M.; Leszczak, S.; Ober, I.; Buechler, C.; Karrasch, T. Pro-inflammatory chemokines CCL2, chemerin, IP-10 and RANTES in human serum during an oral lipid tolerance test. Cytokine 2016, 80, 56–63. [Google Scholar] [CrossRef]
- Nakanishi, K.; Ishibashi, C.; Ide, S.; Yamamoto, R.; Nishida, M.; Nagatomo, I.; Moriyama, T.; Yamauchi-Takihara, K. Serum FGF21 levels are altered by various factors including lifestyle behaviors in male subjects. Sci. Rep. 2021, 11, 22632. [Google Scholar] [CrossRef]
- Olszanecka-Glinianowicz, M.; Owczarek, A.; Bożentowicz-Wikarek, M.; Brzozowska, A.; Mossakowska, M.; Zdrojewski, T.; Grodzicki, T.; Więcek, A.; Chudek, J. Relationship between circulating visfatin/NAMPT, nutritional status and insulin resistance in an elderly population—Results from the PolSenior substudy. Metabolism 2014, 63, 1409–1418. [Google Scholar] [CrossRef] [PubMed]
- Mattison, J.A.; Colman, R.J.; Beasley, T.M.; Allison, D.B.; Kemnitz, J.W.; Roth, G.S.; Ingram, I.K.; Weindruch, R.; de Cabo, R.; Anderson, R.M. Caloric restriction improves health and survival of rhesus monkeys. Nat. Commun. 2017, 8, 14063. [Google Scholar] [CrossRef] [PubMed]
- Lin, S.J.; Kaeberlein, M.; Andalis, A.A.; Sturtz, L.A.; Defossez, P.A.; Culotta, V.C.; Fink, G.R.; Guarente, L. Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 2002, 418, 344–348. [Google Scholar] [CrossRef] [PubMed]
- Longo, V.D.; Anderson, R.M. Nutrition, longevity and disease: From molecular mechanisms to interventions. Cell 2022, 185, 1455–1470. [Google Scholar] [CrossRef] [PubMed]
- Most, J.; Tosti, V.; Redman, L.M.; Fontana, L. Calorie restriction in humans: An update. Ageing Res. Rev. 2017, 39, 36–45. [Google Scholar] [CrossRef] [PubMed]
- Kraus, W.E.; Bhapkar, M.; Huffman, K.M.; Pieper, C.F.; Krupa Das, S.; Redman, L.M.; Villareal, D.T.; Rochon, J.; Roberts, S.B.; Ravussin, E.; et al. 2 years of calorie restriction and cardiometabolic risk (CALERIE): Exploratory outcomes of a multicentre, phase 2, randomised controlled trial. Lancet Diabetes Endocrinol. 2019, 7, 673–683. [Google Scholar] [CrossRef] [PubMed]
- Dakic, T.; Jevdjovic, T.; Vujovic, P.; Mladenovic, A. The Less We Eat, the Longer We Live: Can Caloric Restriction Help Us Become Centenarians? Int. J. Mol. Sci. 2022, 23, 6546. [Google Scholar] [CrossRef]
- Yu, D.; Tomasiewicz, J.L.; Yang, S.E.; Miller, B.R.; Wakai, M.H.; Sherman, D.S.; Cummings, N.E.; Baar, E.L.; Brinkman, J.A.; Syed, F.A.; et al. Calorie-Restriction-Induced Insulin Sensitivity Is Mediated by Adipose mTORC2 and Not Required for Lifespan Extension. Cell Rep. 2019, 29, 236–248.e3. [Google Scholar] [CrossRef] [PubMed]
- Chiba, T.; Yamaza, H.; Shimokawa, I. Role of insulin and growth hormone/insulin-like growth factor-I signaling in lifespan extension: Rodent longevity models for studying aging and calorie restriction. Curr. Genom. 2007, 8, 423–428. [Google Scholar] [CrossRef]
- Hall, K.D.; Bemis, T.; Brychta, R.; Chen, K.Y.; Courville, A.; Crayner, E.J.; Goodwin, S.; Guo, J.; Howard, L.; Knuth, N.D.; et al. Calorie for Calorie, Dietary Fat Restriction Results in More Body Fat Loss than Carbohydrate Restriction in People with Obesity. Cell Metab. 2015, 22, 427–436. [Google Scholar] [CrossRef]
- Weiss, E.P.; Racette, S.B.; Villareal, D.T.; Fontana, L.; Steger-May, K.; Schechtman, K.B.; Klein, S.; Holloszy, J.O.; Washington University School of Medicine CALERIE Group. Improvements in glucose tolerance and insulin action induced by increasing energy expenditure or decreasing energy intake: A randomized controlled trial. Am. J. Clin. Nutr. 2006, 84, 1033–1042. [Google Scholar] [CrossRef] [PubMed]
- Tam, C.S.; Covington, J.D.; Ravussin, E.; Redman, L.M. Little evidence of systemic and adipose tissue inflammation in overweight individuals. Front. Genet. 2012, 3, 58. [Google Scholar] [CrossRef] [PubMed]
- Angelino, D.; Pietrangeli, F.; Serafini, M. Early Dinner Time and Caloric Restriction Lapse Contribute to the Longevity of Nonagenarians and Centenarians of the Italian Abruzzo Region: A Cross-Sectional Study. Front. Nutr. 2022, 9, 863106. [Google Scholar] [CrossRef] [PubMed]
Adipokines | Roles |
---|---|
Adiponectin | Improves glucose homeostasis; has antidiabetic, anti-inflammatory, and antiatherogenic effects |
FGF21 | Improves age-related tissue dysfunctions; extends lifespan; |
positively associated with longevity | |
Adipsin | Improves glucose tolerance and beta-cell functions; |
stimulates triacylglycerol synthesis and storage in adipose tissue; | |
positively associated with longevity; increases cell survival and SIRT1 activity and has neuroprotective effects | |
Apelin | Regulates food intake; improves glucose disposal |
Omentin | Improves insulin sensitivity; has an anti-inflammatory effect |
Annexin | Regulates inflammation, lipolysis, lipogenesis, and adiposity |
Neuregulin | Regulates cell proliferation, survival, migration, and differentiation; |
reduces hepatic glucose production and lipogenesis; | |
stimulates thermogenesis in brown adipose tissue | |
Leptin | Regulates appetite and energy expenditure; |
negatively associated with longevity | |
Resistin | Positively associated with obesity and insulin resistance; accelerates inflammation; |
positively correlated with cellular senescence and aging | |
Visfatin | Stimulates triacylglycerol synthesis and storage in adipose tissue; |
positively associated with longevity; increases cell survival and SIRT1 activity and has neuroprotective effects | |
Chemerin | Regulates cell proliferation, differentiation, and energy metabolism; |
negatively associated with longevity | |
Vaspin | Regulates insulin sensitivity, adipocyte differentiation, and angiogenesis; inhibits inflammation |
Lipocalin-2 | Regulates dyslipidemia and insulin resistance; inhibits inflammation |
RBP4 | Positively associated with obesity and insulin resistance; |
impairs mitochondrial fatty acid β-oxidation | |
Fetuin A | Positively associated with insulin resistance and inflammation |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Park, S.; Shimokawa, I. Influence of Adipokines on Metabolic Dysfunction and Aging. Biomedicines 2024, 12, 873. https://doi.org/10.3390/biomedicines12040873
Park S, Shimokawa I. Influence of Adipokines on Metabolic Dysfunction and Aging. Biomedicines. 2024; 12(4):873. https://doi.org/10.3390/biomedicines12040873
Chicago/Turabian StylePark, Seongjoon, and Isao Shimokawa. 2024. "Influence of Adipokines on Metabolic Dysfunction and Aging" Biomedicines 12, no. 4: 873. https://doi.org/10.3390/biomedicines12040873