Inhibition of endothelial p53 improves metabolic abnormalities related to dietary obesity

Cell Reports

Volumn 7, Issue 5, 2014, Pages 1691-1703

  Yokoyama, Masataka ^a   Okada, Sho ^a   Nakagomi, Atsushi ^a   Moriya, Junji ^a   Shimizu, Ippei ^b   Nojima, Aika ^a   Yoshida, Yohko ^b   Ichimiya, Harumi ^c   Kamimura, Naomi ^c   Kobayashi, Yoshio ^a   Ohta, Shigeo ^c   Fruttiger, Marcus ^d   Lozano, Guillermina ^e   Minamino, Tohru ^b,f  

^a CHIBA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^c NIPPON MEDICAL SCHOOL   (Japan)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE TRANSPORTER 1; NITRIC OXIDE SYNTHASE; PROTEIN P53; ENDOTHELIAL NITRIC OXIDE SYNTHASE; PPARGC1A PROTEIN, MOUSE; TRANSCRIPTION FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOGENESIS; CALORIC INTAKE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GLUCOSE HOMEOSTASIS; HUMAN; HUMAN CELL; INSULIN SENSITIVITY; LIPID STORAGE; METABOLIC DISORDER; MITOCHONDRION; MOUSE; NONHUMAN; OBESITY; OXYGEN CONSUMPTION; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS INHIBITION; SKELETAL MUSCLE; UPREGULATION; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; GENETICS; INSULIN RESISTANCE; LIPID DIET; LIPID METABOLISM; METABOLISM; MITOCHONDRIAL DYNAMICS; UMBILICAL VEIN ENDOTHELIAL CELL; DISEASE ASSOCIATION; ENZYME INACTIVATION; ENZYME PHOSPHORYLATION; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; METABOLIC INHIBITION; METABOLIC REGULATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

ANIMALS; DIET, HIGH-FAT; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INSULIN RESISTANCE; LIPID METABOLISM; MICE; MICE, INBRED C57BL; MITOCHONDRIAL TURNOVER; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE TYPE III; OBESITY; OXYGEN CONSUMPTION; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

MUS;

EID: 84902304773     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.04.046     Document Type: Article

References (63)

1. Aguilar V., Alliouachene S., Sotiropoulos A., Sobering A., Athea Y., Djouadi F., Miraux S., Thiaudière E., Foretz M., Viollet B., et al. S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab. 2007, 5:476-487.
2. Alpert E., Gruzman A., Riahi Y., Blejter R., Aharoni P., Weisinger G., Eckel J., Kaiser N., Sasson S. Delayed autoregulation of glucose transport in vascular endothelial cells. Diabetologia 2005, 48:752-755.
3. Arany Z. PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr. Opin. Genet. Dev. 2008, 18:426-434.
4. Arany Z., Foo S.Y., Ma Y., Ruas J.L., Bommi-Reddy A., Girnun G., Cooper M., Laznik D., Chinsomboon J., Rangwala S.M., et al. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 2008, 451:1008-1012.
5. Barber P.A., Hoyte L., Colbourne F., Buchan A.M. Temperature-regulated model of focal ischemia in the mouse: a study with histopathological and behavioral outcomes. Stroke 2004, 35:1720-1725.
6. Beckman J.A., Creager M.A., Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 2002, 287:2570-2581.
7. Benedito R., Roca C., Sörensen I., Adams S., Gossler A., Fruttiger M., Adams R.H. The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 2009, 137:1124-1135.
8. Brodsky S.V., Gealekman O., Chen J., Zhang F., Togashi N., Crabtree M., Gross S.S., Nasjletti A., Goligorsky M.S. Prevention and reversal of premature endothelial cell senescence and vasculopathy in obesity-induced diabetes by ebselen. Circ. Res. 2004, 94:377-384.
9. Butler A.A., Kozak L.P. A recurring problem with the analysis of energy expenditure in genetic models expressing lean and obese phenotypes. Diabetes 2010, 59:323-329.
10. Calvo J.A., Daniels T.G., Wang X., Paul A., Lin J., Spiegelman B.M., Stevenson S.C., Rangwala S.M. Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake. J.Appl. Physiol. 2008, 104:1304-1312.
11. Cantley L.C., Neel B.G. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc. Natl. Acad. Sci. USA 1999, 96:4240-4245.
12. Cao Y. Angiogenesis and vascular functions in modulation of obesity, adipose metabolism, and insulin sensitivity. Cell Metab. 2013, 18:478-489.
13. Chang S., Multani A.S., Cabrera N.G., Naylor M.L., Laud P., Lombard D., Pathak S., Guarente L., DePinho R.A. Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat. Genet. 2004, 36:877-882.
14. Chen J., Goligorsky M.S. Premature senescence of endothelial cells: Methusaleh's dilemma. Am. J. Physiol. Heart Circ. Physiol. 2006, 290:H1729-H1739.
15. Clark M.G. Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E732-E750.
16. Clark M.G., Wallis M.G., Barrett E.J., Vincent M.A., Richards S.M., Clerk L.H., Rattigan S. Blood flow and muscle metabolism: a focus on insulin action. Am. J. Physiol. Endocrinol. Metab. 2003, 284:E241-E258.
17. Claxton S., Kostourou V., Jadeja S., Chambon P., Hodivala-Dilke K., Fruttiger M. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis 2008, 46:74-80.
18. Cousin S.P., Hügl S.R., Wrede C.E., Kajio H., Myers M.G., Rhodes C.J. Free fatty acid-induced inhibition of glucose and insulin-like growth factor I-induced deoxyribonucleic acid synthesis in the pancreatic beta-cell line INS-1. Endocrinology 2001, 142:229-240.
19. Czernichow S., Greenfield J.R., Galan P., Bastard J.P., Charnaux N., Samaras K., Safar M.E., Blacher J., Hercberg S., Levy B.I. Microvascular dysfunction in healthy insulin-sensitive overweight individuals. J.Hypertens. 2010, 28:325-332.
20. Gordon S. Macrophage heterogeneity and tissue lipids. J.Clin. Invest. 2007, 117:89-93.
21. Grier J.D., Xiong S., Elizondo-Fraire A.C., Parant J.M., Lozano G. Tissue-specific differences of p53 inhibition by Mdm2 and Mdm4. Mol. Cell. Biol. 2006, 26:192-198.
22. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
23. Huang Y., Lei L., Liu D., Jovin I., Russell R., Johnson R.S., Di Lorenzo A., Giordano F.J. Normal glucose uptake in the brain and heart requires an endothelial cell-specific HIF-1α-dependent function. Proc. Natl. Acad. Sci. USA 2012, 109:17478-17483.
24. Iwabu M., Yamauchi T., Okada-Iwabu M., Sato K., Nakagawa T., Funata M., Yamaguchi M., Namiki S., Nakayama R., Tabata M., et al. Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature 2010, 464:1313-1319.
25. Jonk A.M., Houben A.J., de Jongh R.T., Serné E.H., Schaper N.C., Stehouwer C.D. Microvascular dysfunction in obesity: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Physiology (Bethesda) 2007, 22:252-260.
26. Kawase T., Ohki R., Shibata T., Tsutsumi S., Kamimura N., Inazawa J., Ohta T., Ichikawa H., Aburatani H., Tashiro F., Taya Y. PH domain-only protein PHLDA3 is a p53-regulated repressor of Akt. Cell 2009, 136:535-550.
27. Kim Y.B., Peroni O.D., Aschenbach W.G., Minokoshi Y., Kotani K., Zisman A., Kahn C.R., Goodyear L.J., Kahn B.B. Muscle-specific deletion of the Glut4 glucose transporter alters multiple regulatory steps in glycogen metabolism. Mol. Cell. Biol. 2005, 25:9713-9723.
28. Kim C.S., Jung S.B., Naqvi A., Hoffman T.A., DeRicco J., Yamamori T., Cole M.P., Jeon B.H., Irani K. p53 impairs endothelium-dependent vasomotor function through transcriptional upregulation of p66shc. Circ. Res. 2008, 103:1441-1450.
29. Kubota T., Kubota N., Kumagai H., Yamaguchi S., Kozono H., Takahashi T., Inoue M., Itoh S., Takamoto I., Sasako T., et al. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab. 2011, 13:294-307.
30. Kukreja R.C., Xi L. eNOS phosphorylation: a pivotal molecular switch in vasodilation and cardioprotection?. J.Mol. Cell. Cardiol. 2007, 42:280-282.
31. Kumar A., Kim C.S., Hoffman T.A., Naqvi A., Dericco J., Jung S.B., Lin Z., Jain M.K., Irani K. p53 impairs endothelial function by transcriptionally repressing Kruppel-Like Factor 2. Arterioscler. Thromb. Vasc. Biol. 2011, 31:133-141.
32. Kunieda T., Minamino T., Nishi J., Tateno K., Oyama T., Katsuno T., Miyauchi H., Orimo M., Okada S., Takamura M., et al. Angiotensin II induces premature senescence of vascular smooth muscle cells and accelerates the development of atherosclerosis via a p21-dependent pathway. Circulation 2006, 114:953-960.
33. Laakso M., Edelman S.V., Brechtel G., Baron A.D. Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man. A novel mechanism for insulin resistance. J.Clin. Invest. 1990, 85:1844-1852.
34. Leone T.C., Lehman J.J., Finck B.N., Schaeffer P.J., Wende A.R., Boudina S., Courtois M., Wozniak D.F., Sambandam N., Bernal-Mizrachi C., et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 2005, 3:e101.
35. Lin J., Wu H., Tarr P.T., Zhang C.Y., Wu Z., Boss O., Michael L.F., Puigserver P., Isotani E., Olson E.N., et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002, 418:797-801.
36. Maeda N., Shimomura I., Kishida K., Nishizawa H., Matsuda M., Nagaretani H., Furuyama N., Kondo H., Takahashi M., Arita Y., et al. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nat. Med. 2002, 8:731-737.
37. Marino S., Vooijs M., van Der Gulden H., Jonkers J., Berns A. Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 2000, 14:994-1004.
38. McTernan P.G., Fisher F.M., Valsamakis G., Chetty R., Harte A., McTernan C.L., Clark P.M., Smith S.A., Barnett A.H., Kumar S. Resistin and type 2 diabetes: regulation of resistin expression by insulin and rosiglitazone and the effects of recombinant resistin on lipid and glucose metabolism in human differentiated adipocytes. J.Clin. Endocrinol. Metab. 2003, 88:6098-6106.
39. Michael L.F., Wu Z., Cheatham R.B., Puigserver P., Adelmant G., Lehman J.J., Kelly D.P., Spiegelman B.M. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl. Acad. Sci. USA 2001, 98:3820-3825.
40. Minamino T., Komuro I. Vascular cell senescence: contribution to atherosclerosis. Circ. Res. 2007, 100:15-26.
41. Minamino T., Komuro I. Vascular aging: insights from studies on cellular senescence, stem cell aging, and progeroid syndromes. Nat. Clin. Pract. Cardiovasc. Med. 2008, 5:637-648.
42. Minamino T., Orimo M., Shimizu I., Kunieda T., Yokoyama M., Ito T., Nojima A., Nabetani A., Oike Y., Matsubara H., et al. A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat. Med. 2009, 15:1082-1087.
43. Miura S., Kai Y., Ono M., Ezaki O. Overexpression of peroxisome proliferator-activated receptor gamma coactivator-1alpha down-regulates GLUT4 mRNA in skeletal muscles. J.Biol. Chem. 2003, 278:31385-31390.
44. Miyauchi H., Minamino T., Tateno K., Kunieda T., Toko H., Komuro I. Akt negatively regulates the invitro lifespan of human endothelial cells via a p53/p21-dependent pathway. EMBO J. 2004, 23:212-220.
45. Montooth K.L., Marden J.H., Clark A.G. Mapping determinants of variation in energy metabolism, respiration and flight in Drosophila. Genetics 2003, 165:623-635.
46. Mootha V.K., Lindgren C.M., Eriksson K.F., Subramanian A., Sihag S., Lehar J., Puigserver P., Carlsson E., Ridderstråle M., Laurila E., et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 2003, 34:267-273.
47. Mortensen K., Skouv J., Hougaard D.M., Larsson L.I. Endogenous endothelial cell nitric-oxide synthase modulates apoptosis in cultured breast cancer cells and is transcriptionally regulated by p53. J.Biol. Chem. 1999, 274:37679-37684.
48. Muris D.M., Houben A.J., Schram M.T., Stehouwer C.D. Microvascular dysfunction is associated with a higher incidence of type 2 diabetes mellitus: a systematic review and meta-analysis. Arterioscler. Thromb. Vasc. Biol. 2012, 32:3082-3094.
49. Narkar V.A., Downes M., Yu R.T., Embler E., Wang Y.X., Banayo E., Mihaylova M.M., Nelson M.C., Zou Y., Juguilon H., et al. AMPK and PPARdelta agonists are exercise mimetics. Cell 2008, 134:405-415.
50. Oike Y., Akao M., Yasunaga K., Yamauchi T., Morisada T., Ito Y., Urano T., Kimura Y., Kubota Y., Maekawa H., et al. Angiopoietin-related growth factor antagonizes obesity and insulin resistance. Nat. Med. 2005, 11:400-408.
51. Orimo M., Minamino T., Miyauchi H., Tateno K., Okada S., Moriya J., Komuro I. Protective role of SIRT1 in diabetic vascular dysfunction. Arterioscler. Thromb. Vasc. Biol. 2009, 29:889-894.
52. Patti M.E., Butte A.J., Crunkhorn S., Cusi K., Berria R., Kashyap S., Miyazaki Y., Kohane I., Costello M., Saccone R., et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc. Natl. Acad. Sci. USA 2003, 100:8466-8471.
53. Plutzky J. Macrovascular effects and safety issues of therapies for type 2 diabetes. Am. J. Cardiol. 2011, 108(Suppl):25B-32B.
54. Puigserver P., Wu Z., Park C.W., Graves R., Wright M., Spiegelman B.M. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 1998, 92:829-839.
55. Rajah T.T., Olson A.L., Grammas P. Differential glucose uptake in retina- and brain-derived endothelial cells. Microvasc. Res. 2001, 62:236-242.
56. Russell S.J., Kahn C.R. Endocrine regulation of ageing. Nat. Rev. Mol. Cell Biol. 2007, 8:681-691.
57. Sano M., Minamino T., Toko H., Miyauchi H., Orimo M., Qin Y., Akazawa H., Tateno K., Kayama Y., Harada M., et al. p53-induced inhibition ofHif-1 causes cardiac dysfunction during pressure overload. Nature 2007, 446:444-448.
58. Serrano M., Blasco M.A. Putting the stress on senescence. Curr. Opin. Cell Biol. 2001, 13:748-753.
59. Stambolic V., MacPherson D., Sas D., Lin Y., Snow B., Jang Y., Benchimol S., Mak T.W. Regulation of PTEN transcription by p53. Mol. Cell 2001, 8:317-325.
60. Stewart S.A., Weinberg R.A. Telomeres: cancer to human aging. Annu. Rev. Cell Dev. Biol. 2006, 22:531-557.
61. Tang Y., Harrington A., Yang X., Friesel R.E., Liaw L. The contribution of the Tie2+ lineage to primitive and definitive hematopoietic cells. Genesis 2010, 48:563-567.
62. Vicent D., Ilany J., Kondo T., Naruse K., Fisher S.J., Kisanuki Y.Y., Bursell S., Yanagisawa M., King G.L., Kahn C.R. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J.Clin. Invest. 2003, 111:1373-1380.
63. Wade M., Wang Y.V., Wahl G.M. The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol. 2010, 20:299-309.