Divergent roles for Adiponectin receptor 1 (adipor1) and AdipoR2 in mediating revascularization and metabolic dysfunction in vivo

Journal of Biological Chemistry

Volumn 289, Issue 23, 2014, Pages 16200-16213

  Parker Duffen, Jennifer L ^a   Nakamura, Kazuto ^a   Silver, Marcy ^a   Zuriaga, Maria A ^a   Maclauchlan, Susan ^a   Aprahamian, Tamar R ^a   Walsh, Kenneth ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOLISM; NUTRITION;

ANTI-INFLAMMATORIES; CARDIOVASCULAR TISSUES; DIET-INDUCED OBESITY; ISCHEMIA MODEL; ISCHEMIC SURGERY; METABOLIC FUNCTION; OVER-EXPRESSION; REVASCULARIZATION;

MAMMALS;

ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD FLOW; CONTROLLED STUDY; DISEASE SEVERITY; HOMEOSTASIS; IN VIVO STUDY; LIMB ISCHEMIA; METABOLIC DISORDER; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPERFUSION; TISSUE REGENERATION; WEIGHT GAIN; WILD TYPE;

ADIPONECTIN; ADIPOR1; ADIPOR2; ANGIOGENESIS; METABOLISM; RECEPTOR; VASCULAR BIOLOGY;

ANIMALS; EXTREMITIES; METABOLIC DISEASES; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, ADIPONECTIN;

EID: 84902146471     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.548115     Document Type: Article

References (56)

1. Ouchi, N., Parker, J. L., Lugus, J. J., and Walsh, K. (2011) Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11, 85-97
2. Ouchi, N., Kihara, S., Funahashi, T., Matsuzawa, Y., and Walsh, K. (2003) Obesity, adiponectin, and vascular inflammatory disease. Curr. Opin. Lipidol. 14, 561-566
3. Hu, E., Liang, P., and Spiegelman, B. M. (1996) AdipoQ is a novel adiposespecific gene dysregulated in obesity. J. Biol. Chem. 271, 10697-10703
4. Maeda, N., Shimomura, I., Kishida, K., Nishizawa, H., Matsuda, M., Nagaretani, H., Furuyama, N., Kondo, H., Takahashi, M., Arita, Y., Komuro, R., Ouchi, N., Kihara, S., Tochino, Y., Okutomi, K., Horie, M., Takeda, S., Aoyama, T., Funahashi, T., and Matsuzawa, Y. (2002) Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 8, 731-737
5. Kubota, N., Terauchi, Y., Yamauchi, T., Kubota, T., Moroi, M., Matsui, J., Eto, K., Yamashita, T., Kamon, J., Satoh, H., Yano, W., Froguel, P., Nagai, R., Kimura, S., Kadowaki, T., and Noda, T. (2002) Disruption of adiponectin causes insulin resistance and neointimal formation. J. Biol. Chem. 277, 25863-25866
6. Nawrocki, A. R., Rajala, M. W., Tomas, E., Pajvani, U. B., Saha, A. K., Trumbauer, M. E., Pang, Z., Chen, A. S., Ruderman, N. B., Chen, H., Rossetti, L., and Scherer, P. E. (2006) Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor β agonists. J. Biol. Chem. 281, 2654-2660
7. Ma, K., Cabrero, A., Saha, P. K., Kojima, H., Li, L., Chang, B. H., Paul, A., and Chan, L. (2002) Increased β-oxidation but no insulin resistance or glucose intolerance in mice lacking adiponectin. J. Biol. Chem. 277, 34658-34661
8. Kim, J. Y., van de Wall, E., Laplante, M., Azzara, A., Trujillo, M. E., Hofmann, S. M., Schraw, T., Durand, J. L., Li, H., Li, G., Jelicks, L. A., Mehler, M. F., Hui, D. Y., Deshaies, Y., Shulman, G. I., Schwartz, G. J., and Scherer, P. E. (2007) Obesity-associated improvements in metabolic profile through expansion of adipose tissue. J. Clin. Invest. 117, 2621-2637
9. Aprahamian, T. R. (2013) Elevated adiponectin expression promotes adipose tissue vascularity under conditions of diet-induced obesity. Metabolism 62, 1730-1738
10. Yang, W. S., Jeng, C. Y., Wu, T. J., Tanaka, S., Funahashi, T., Matsuzawa, Y., Wang, J. P., Chen, C. L., Tai, T. Y., and Chuang, L. M. (2002) Synthetic peroxisome proliferator-activated receptor-β agonist, rosiglitazone, increases plasma levels of adiponectin in type 2 diabetic patients. Diabetes Care 25, 376-380
11. Yamauchi, T., Kamon, J., Ito, Y., Tsuchida, A., Yokomizo, T., Kita, S., Sugiyama, T., Miyagishi, M., Hara, K., Tsunoda, M., Murakami, K., Ohteki, T., Uchida, S., Takekawa, S., Waki, H., Tsuno, N. H., Shibata, Y., Terauchi, Y., Froguel, P., Tobe, K., Koyasu, S., Taira, K., Kitamura, T., Shimizu, T., Nagai, R., and Kadowaki, T. (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423, 762-769
12. Lee, M. H., Klein, R. L., El-Shewy, H. M., Luttrell, D. K., and Luttrell, L. M. (2008) The adiponectin receptors AdipoR1 and AdipoR2 activate ERK1/2 through a Src/Ras-dependent pathway and stimulate cell growth. Biochemistry 47, 11682-11692
13. Cheng, K. K., Lam, K. S., Wang, Y., Huang, Y., Carling, D., Wu, D., Wong, C., and Xu, A. (2007) Adiponectin-induced endothelial nitric oxide synthase activation and nitric oxide production are mediated by APPL1 in endothelial cells. Diabetes 56, 1387-1394
14. Adya, R., Tan, B. K., Chen, J., and Randeva, H. S. (2012) Protective actions of globular and full-length adiponectin on human endothelial cells: novel insights into adiponectin-induced angiogenesis. J. Vasc. Res. 49, 534-543
15. Zhang, P., Wang, Y., Fan, Y., Tang, Z., and Wang, N. (2009) Overexpression of adiponectin receptors potentiates the antiinflammatory action of subeffective dose of globular adiponectin in vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 29, 67-74
16. Fasshauer, M., Klein, J., Kralisch, S., Klier, M., Lössner, U., Blüher, M., and Paschke, R. (2004) Growth hormone is a positive regulator of adiponectin receptor 2 in 3T3-L1 adipocytes. FEBS Lett. 558, 27-32
17. Parker-Duffen, J. L., Nakamura, K., Silver, M., Kikuchi, R., Tigges, U., Yoshida, S., Denzel, M. S., Ranscht, B., and Walsh, K. (2013) T-cadherin is essential for adiponectin-mediated revascularization. J. Biol. Chem. 288, 24886-24897
18. Yamauchi, T., Nio, Y., Maki, T., Kobayashi, M., Takazawa, T., Iwabu, M., Okada-Iwabu, M., Kawamoto, S., Kubota, N., Kubota, T., Ito, Y., Kamon, J., Tsuchida, A., Kumagai, K., Kozono, H., Hada, Y., Ogata, H., Tokuyama, K., Tsunoda, M., Ide, T., Murakami, K., Awazawa, M., Takamoto, I., Froguel, P., Hara, K., Tobe, K., Nagai, R., Ueki, K., and Kadowaki, T. (2007) Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13, 332-339
19. Iwabu, M., Yamauchi, T., Okada-Iwabu, M., Sato, K., Nakagawa, T., Funata, M., Yamaguchi, M., Namiki, S., Nakayama, R., Tabata, M., Ogata, H., Kubota, N., Takamoto, I., Hayashi, Y. K., Yamauchi, N., Waki, H., Fukayama, M., Nishino, I., Tokuyama, K., Ueki, K., Oike, Y., Ishii, S., Hirose, K., Shimizu, T., Touhara, K., and Kadowaki, T. (2010) Adiponectin and AdipoR1 regulate PGC-1β and mitochondria by Ca2β and AMPK/SIRT1. Nature 464, 1313-1319
20. Patel, S. A., Hoehn, K. L., Lawrence, R. T., Sawbridge, L., Talbot, N. A., Tomsig, J. L., Turner, N., Cooney, G. J., Whitehead, J. P., Kraegen, E. W., and Cleasby, M. E. (2012) Overexpression of the adiponectin receptor AdipoR1 in rat skeletal muscle amplifies local insulin sensitivity. Endocrinology 153, 5231-5246
21. Luo, N., Chung, B. H., Wang, X., Klein, R. L., Tang, C. K., Garvey, W. T., and Fu, Y. (2013) Enhanced adiponectin actions by overexpression of adiponectin receptor 1 in macrophages. Atherosclerosis 228, 124-135
22. Bjursell, M., Ahnmark, A., Bohlooly-Y, M., William-Olsson, L., Rhedin, M., Peng, X. R., Ploj, K., Gerdin, A. K., Arnerup, G., Elmgren, A., Berg, A. L., Oscarsson, J., and Lindén, D. (2007) Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes 56, 583-593
23. Liu, Y., Michael, M. D., Kash, S., Bensch, W. R., Monia, B. P., Murray, S. F., Otto, K. A., Syed, S. K., Bhanot, S., Sloop, K. W., Sullivan, J. M., and Reifel-Miller, A. (2007) Deficiency of adiponectin receptor 2 reduces dietinduced insulin resistance but promotes type 2 diabetes. Endocrinology 148, 683-692
24. Pischon, T., Girman, C. J., Hotamisligil, G. S., Rifai, N., Hu, F. B., and Rimm, E. B. (2004) Plasma adiponectin levels and risk of myocardial infarction in men. JAMA 291, 1730-1737
25. Ho, D. Y., Cook, N. R., Britton, K. A., Kim, E., Creager, M. A., Ridker, P. M., and Pradhan, A. D. (2011) High-molecular-weight and total adiponectin levels and incident symptomatic peripheral artery disease in women: a prospective investigation. Circulation 124, 2303-2311
26. Ouchi, N., Ohishi, M., Kihara, S., Funahashi, T., Nakamura, T., Nagaretani, H., Kumada, M., Ohashi, K., Okamoto, Y., Nishizawa, H., Kishida, K., Maeda, N., Nagasawa, A., Kobayashi, H., Hiraoka, H., Komai, N., Kaibe, M., Rakugi, H., Ogihara, T., and Matsuzawa, Y. (2003) Association of hypoadiponectinemia with impaired vasoreactivity. Hypertension 42, 231-234
27. Shibata, R., Izumiya, Y., Sato, K., Papanicolaou, K., Kihara, S., Colucci, W. S., Sam, F., Ouchi, N., and Walsh, K. (2007) Adiponectin protects against the development of systolic dysfunction following myocardial infarction. J. Mol. Cell Cardiol. 42, 1065-1074
28. Shibata, R., Ouchi, N., Ito, M., Kihara, S., Shiojima, I., Pimentel, D. R., Kumada, M., Sato, K., Schiekofer, S., Ohashi, K., Funahashi, T., Colucci, W. S., and Walsh, K. (2004) Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat. Med. 10, 1384-1389
29. Shibata, R., Ouchi, N., Kihara, S., Sato, K., Funahashi, T., and Walsh, K. (2004) Adiponectin stimulates angiogenesis in response to tissue ischemia through stimulation of amp-activated protein kinase signaling. J. Biol. Chem. 279, 28670-28674
30. Ohashi, K., Ouchi, N., Sato, K., Higuchi, A., Ishikawa, T. O., Herschman, H. R., Kihara, S., and Walsh, K. (2009) Adiponectin promotes revascularization of ischemic muscle through a cyclooxygenase 2-dependent mechanism. Mol. Cell. Biol. 29, 3487-3499
31. Kondo, M., Shibata, R., Miura, R., Shimano, M., Kondo, K., Li, P., Ohashi, T., Kihara, S., Maeda, N., Walsh, K., Ouchi, N., and Murohara, T. (2009) Caloric restriction stimulates revascularization in response to ischemia via adiponectin-mediated activation of endothelial nitric-oxide synthase. J. Biol. Chem. 284, 1718-1724
32. Higuchi, A., Ohashi, K., Kihara, S., Walsh, K., and Ouchi, N. (2009) Adiponectin suppresses pathological microvessel formation in retina through modulation of tumor necrosis factor-β expression. Circ. Res. 104, 1058-1065
33. Higuchi, A., Ohashi, K., Shibata, R., Sono-Romanelli, S., Walsh, K., and Ouchi, N. (2010) Thiazolidinediones reduce pathological neovascularization in ischemic retina via an adiponectin-dependent mechanism. Arterioscler. Thromb. Vasc. Biol. 30, 46-53
34. Kobayashi, H., Ouchi, N., Kihara, S., Walsh, K., Kumada, M., Abe, Y., Funahashi, T., and Matsuzawa, Y. (2004) Selective suppression of endothelial cell apoptosis by the high molecular weight form of adiponectin. Circ. Res. 94, e27-31
35. Ouchi, N., Kobayashi, H., Kihara, S., Kumada, M., Sato, K., Inoue, T., Funahashi, T., and Walsh, K. (2004) Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J. Biol. Chem. 279, 1304-1309
36. Shibata, R., Skurk, C., Ouchi, N., Galasso, G., Kondo, K., Ohashi, T., Shimano, M., Kihara, S., Murohara, T., and Walsh, K. (2008) Adiponectin promotes endothelial progenitor cell number and function. FEBS Lett. 582, 1607-1612
37. Wong, W. T., Tian, X. Y., Xu, A., Yu, J., Lau, C. W., Hoo, R. L., Wang, Y., Lee, V. W., Lam, K. S., Vanhoutte, P. M., and Huang, Y. (2011) Adiponectin is required for PPARβ-mediated improvement of endothelial function in diabetic mice. Cell Metab. 14, 104-115
38. Aprahamian, T., Bonegio, R. G., Richez, C., Yasuda, K., Chiang, L. K., Sato, K., Walsh, K., and Rifkin, I. R. (2009) The peroxisome proliferator-activated receptor β agonist rosiglitazone ameliorates murine lupus by induction of adiponectin. J. Immunol. 182, 340-346
39. Zbinden, S., Clavijo, L. C., Kantor, B., Morsli, H., Cortes, G. A., Andrews, J. A., Jang, G. J., Burnett, M. S., and Epstein, S. E. (2007) Interanimal variability in preexisting collaterals is a major factor determining outcome in experimental angiogenesis trials. Am. J. Physiol. Heart Circ. Physiol. 292, H1891-H1897
40. Zhang, G., Gao, X., Song, Y. K., Vollmer, R., Stolz, D. B., Gasiorowski, J. Z., Dean, D. A., and Liu, D. (2004) Hydroporation as the mechanism of hydrodynamic delivery. Gene Ther. 11, 675-682
41. Liu, F., Song, Y., and Liu, D. (1999) Hydrodynamics-based transfection in animals by systemic administration of plasmid DNA. Gene Ther. 6, 1258-1266
42. Denzel, M. S., Scimia, M. C., Zumstein, P. M., Walsh, K., Ruiz-Lozano, P., and Ranscht, B. (2010) T-cadherin is critical for adiponectin-mediated cardioprotection in mice. J. Clin. Invest. 120, 4342-4352
43. Holland, W. L., Miller, R. A., Wang, Z. V., Sun, K., Barth, B. M., Bui, H. H., Davis, K. E., Bikman, B. T., Halberg, N., Rutkowski, J. M., Wade, M. R., Tenorio, V. M., Kuo, M. S., Brozinick, J. T., Zhang, B. B., Birnbaum, M. J., Summers, S. A., and Scherer, P. E. (2011) Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat. Med. 17, 55-63
44. Ye, R., and Scherer, P. E. (2013) Adiponectin, driver or passenger on the road to insulin sensitivity? Mol. Metab. 2, 133-141
45. Ding, M., Carrão, A. C., Wagner, R. J., Xie, Y., Jin, Y., Rzucidlo, E. M., Yu, J., Li, W., Tellides, G., Hwa, J., Aprahamian, T. R., and Martin, K. A. (2012) Vascular smooth muscle cell-derived adiponectin: a paracrine regulator of contractile phenotype. J. Mol. Cell Cardiol. 52, 474-484
46. Ohashi, K., Parker, J. L., Ouchi, N., Higuchi, A., Vita, J. A., Gokce, N., Pedersen, A. A., Kalthoff, C., Tullin, S., Sams, A., Summer, R., and Walsh, K. (2010) Adiponectin promotes macrophage polarization toward an antiinflammatory phenotype. J. Biol. Chem. 285, 6153-6160
47. Satoh, H., Nguyen, M. T., Trujillo, M., Imamura, T., Usui, I., Scherer, P. E., and Olefsky, J. M. (2005) Adenovirus-mediated adiponectin expression augments skeletal muscle insulin sensitivity in male Wistar rats. Diabetes 54, 1304-1313
48. Rizvi, Y. Q., Mehta, C. S., and Oyekan, A. (2013) Interactions of PPAR-β and adenosine receptors in hypoxia-induced angiogenesis. Vascul. Pharmacol. 59, 144-151
49. Nagata, D., Mogi, M., and Walsh, K. (2003) AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J. Biol. Chem. 278, 31000-31006
50. Ouchi, N., Shibata, R., and Walsh, K. (2005) AMP-activated protein kinase signaling stimulates VEGF expression and angiogenesis in skeletal muscle. Circ. Res. 96, 838-846
51. Wang, Y., Wang, X., Lau, W. B., Yuan, Y., Booth, D., Li, J. J., Scalia, R., Preston, K., Gao, E., Koch, W., and Ma, X. L. (2014) Adiponectin inhibits tumor necrosis factor-β-induced vascular inflammatory response via caveolin-mediated ceramidase recruitment and activation. Circ. Res. 114, 792-805
52. Wang, Y., Wang, X., Jasmin, J. F., Lau, W. B., Li, R., Yuan, Y., Yi, W., Chuprun, K., Lisanti, M. P., Koch, W. J., Gao, E., and Ma, X. L. (2012) Essential role of caveolin-3 in adiponectin signalsome formation and adiponectin cardioprotection. Arterioscler. Thromb. Vasc. Biol. 32, 934-942
53. Zheng, Q., Yuan, Y., Yi, W., Lau, W. B., Wang, Y., Wang, X., Sun, Y., Lopez, B. L., Christopher, T. A., Peterson, J. M., Wong, G. W., Yu, S., Yi, D., and Ma, X. L. (2011) C1q/TNF-related proteins, a family of novel adipokines, induce vascular relaxation through the adiponectin receptor-1/AMPK/eNOS/nitric oxide signaling pathway. Arterioscler. Thromb. Vasc. Biol. 31, 2616-2623
54. Dormandy, J. A., Charbonnel, B., Eckland, D. J., Erdmann, E., Massi-Benedetti, M., Moules, I. K., Skene, A. M., Tan, M. H., Lefèbvre, P. J., Murray, G. D., Standl, E., Wilcox, R. G., Wilhelmsen, L., Betteridge, J., Birkeland, K., Golay, A., Heine, R. J., Korányi, L., Laakso, M., Mokán, M., Norkus, A., Pirags, V., Podar, T., Scheen, A., Scherbaum, W., Schernthaner, G., Schmitz, O., Skrha, J., Smith, U., Taton, J., and PROactive investigators (2005) Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet 366, 1279-1289
55. Lincoff, A. M., Wolski, K., Nicholls, S. J., and Nissen, S. E. (2007) Pioglitazone and risk of cardiovascular events in patients with type 2 diabetes mellitus: a meta-analysis of randomized trials. JAMA 298, 1180-1188
56. Singh, S., Loke, Y. K., and Furberg, C. D. (2007) Long-term risk of cardiovascular events with rosiglitazone: a meta-analysis. JAMA 298, 1189-1195