Cellular senescence in type 2 diabetes: A therapeutic opportunity

Diabetes

Volumn 64, Issue 7, 2015, Pages 2289-2298

  Palmer, Allyson K ^a   Tchkonia, Tamara ^a   LeBrasseur, Nathan K ^a   Chini, Eduardo N ^a   Xu, Ming ^a   Kirkland, James L ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; GLUCOSE; GROWTH HORMONE; SOMATOMEDIN C; IGFBP3 PROTEIN, HUMAN; SOMATOMEDIN BINDING PROTEIN 3;

ADIPOSE TISSUE; ARTICLE; CELL AGING; DIABETIC NEPHROPATHY; DIABETIC RETINOPATHY; HUMAN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SENESCENCE; ANIMAL; COMPLICATION; DIABETES MELLITUS, TYPE 2; INSULIN RESISTANCE; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR MICROENVIRONMENT;

ADIPOSE TISSUE; ANIMALS; CELL AGING; CELLULAR MICROENVIRONMENT; CERAMIDES; DIABETES MELLITUS, TYPE 2; HUMANS; INSULIN RESISTANCE; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 3; INSULIN-LIKE GROWTH FACTOR I; INSULIN-SECRETING CELLS;

EID: 84962079683     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-1820     Document Type: Article

References (94)

1. Centers for Disease Control and Prevention. National Diabetes Statistics Report: Estimates of Diabetes and its Burden in the United States, 2014. Atlanta, GA, U.S. Department of Health and Human Services, 2014
2. Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA 2014;311:806-814
3. Kannel WB, McGee DL. Diabetes and glucose tolerance as risk factors for cardiovascular disease: The Framingham Study. Diabetes Care 1979;2:120-126
4. Anderson RJ, Freedland KE, Clouse RE, Lustman PJ. The prevalence of comorbid depression in adults with diabetes: A meta-analysis. Diabetes Care 2001;24:1069-1078
5. Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: Epidemiology, pathophysiology, and management. JAMA 2002;287:2570-2581
6. Brem H, Tomic-Canic M. Cellular and molecular basis of wound healing in diabetes. J Clin Invest 2007;117:1219-1222
7. Baker DJ, Wijshake T, Tchkonia T, et al. Clearance of p16Ink4a-positive senescent cells delays ageing-associated disorders. Nature 2011;479:232-236
8. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013;153:1194-1217
9. Kirkland JL, Tchkonia T. Clinical strategies and animal models for developing senolytic agents. Exp Gerontol. 28 October 2015 [Epub ahead of print]. DOI: 10.1016/j.exger.2014.10.012
10. Muñoz-Espín D, Serrano M. Cellular senescence: From physiology to pathology. Nat Rev Mol Cell Biol 2014;15:482-496
11. Campisi J, d'Adda di Fagagna F. Cellular senescence: When bad things happen to good cells. Nat Rev Mol Cell Biol 2007;8:729-740
12. Coppé JP, Patil CK, Rodier F, et al. Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 2008;6:2853-2868
13. Kuilman T, Peeper DS. Senescence-messaging secretome: SMS-ing cellular stress. Nat Rev Cancer 2009;9:81-94
14. Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract 2014;105:141-150
15. Dandona P, Aljada A, Bandyopadhyay A. Inflammation: The link between insulin resistance, obesity and diabetes. Trends Immunol 2004;25:4-7
16. Campisi J. Senescent cells, tumor suppression, and organismal aging: Good citizens, bad neighbors. Cell 2005;120:513-522
17. Zhu Y, Armstrong JL, Tchkonia T, Kirkland JL. Cellular senescence and the senescent secretory phenotype in age-related chronic diseases. Curr Opin Clin Nutr Metab Care 2014;17:324-328
18. Tchkonia T, Zhu Y, Van Deursen J, Campisi J, Kirkland JL. Cellular senescence and the senescent secretory phenotype: Therapeutic opportunities. J Clin Invest 2013;123:966-972
19. Nelson G, Wordsworth J, Wang C, et al. A senescent cell bystander effect: Senescence-induced senescence. Aging Cell 2012;11:345-349
20. Tchkonia T, Morbeck DE, Von Zglinicki T, et al. Fat tissue, aging, and cellular senescence. Aging Cell 2010;9:667-684
21. Melk A, Schmidt BMW, Vongwiwatana A, Rayner DC, Halloran PF. Increased expression of senescence-associated cell cycle inhibitor p16INK4a in deteriorating renal transplants and diseased native kidney. Am J Transplant 2005;5: 1375-1382
22. Waaijer ME, Parish WE, Strongitharm BH, et al. The number of p16INK4a positive cells in human skin reflects biological age. Aging Cell 2012;11:722-725
23. Minamino T, Orimo M, Shimizu I, et al. A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat Med 2009;15:1082-1087
24. Minamino T, Komuro I. Vascular cell senescence: Contribution to atherosclerosis. Circ Res 2007;100:15-26
25. Westhoff JH, Hilgers KF, Steinbach MP, et al. Hypertension induces somatic cellular senescence in rats and humans by induction of cell cycle inhibitor p16INK4a. Hypertension 2008;52:123-129
26. Kirkland JL. Translating advances from the basic biology of aging into clinical application. Exp Gerontol 2013;48:1-5
27. Stout MB, Tchkonia T, Pirtskhalava T, et al. Growth hormone action predicts age-related white adipose tissue dysfunction and senescent cell burden in mice. Aging (Albany, NY Online) 2014;6:575-586
28. Tran D, Bergholz J, Zhang H, et al. Insulin-like growth factor-1 regulates the SIRT1-p53 pathway in cellular senescence. Aging Cell 2014;13:669-678
29. Tabibian JH, O'Hara SP, Splinter PL, Trussoni CE, LaRusso NF. Cholangiocyte senescence by way of N-ras activation is a characteristic of primary sclerosing cholangitis. Hepatology 2014;59:2263-2275
30. Van Deursen JM. The role of senescent cells in ageing. Nature 2014;509: 439-446
31. Freund A, Orjalo AV, Desprez PY, Campisi J. Inflammatory networks during cellular senescence: Causes and consequences. Trends Mol Med 2010;16:238-246
32. Muñoz-Espín D, Cañamero M, Maraver A, et al. Programmed cell senescence during mammalian embryonic development. Cell 2013;155:1104-1118
33. Meuter A, Rogmann LM, Winterhoff BJ, Tchkonia T, Kirkland JL, Morbeck DE. Markers of cellular senescence are elevated in murine blastocysts cultured in vitro: Molecular consequences of culture in atmospheric oxygen. J Assist Reprod Genet 2014;31:1259-1267
34. Demaria M, Ohtani N, Youssef SA, et al. An essential role for senescent cells in optimal wound healing through secretion of PDGF-AA. Dev Cell 2014;31:722-733
35. Yokoi T, Fukuo K, Yasuda O, et al. Apoptosis signal-regulating kinase 1 mediates cellular senescence induced by high glucose in endothelial cells. Diabetes 2006;55:1660-1665
36. Cramer C, Freisinger E, Jones RK, et al. Persistent high glucose concentrations alter the regenerative potential of mesenchymal stem cells. Stem Cells Dev 2010;19:1875-1884
37. Blazer S, Khankin E, Segev Y, et al. High glucose-induced replicative senescence: Point of no return and effect of telomerase. Biochem Biophys Res Commun 2002;296:93-101
38. Ksiazek K, Passos JF, Olijslagers S, Von Zglinicki T. Mitochondrial dysfunction is a possible cause of accelerated senescence of mesothelial cells exposed to high glucose. Biochem Biophys Res Commun 2008;366:793-799
39. Peppa M, Uribarri J, Vlassara H. Glucose, advanced glycation end products, and diabetes complications: What is new and what works. Clinical Diabetes 2003;21:186-187
40. Liu J, Huang K, Cai GY, et al. Receptor for advanced glycation end-products promotes premature senescence of proximal tubular epithelial cells via activation of endoplasmic reticulum stress-dependent p21 signaling. Cell Signal 2014;26: 110-121
41. Kim KS, Seu YB, Baek SH, et al. Induction of cellular senescence by insulinlike growth factor binding protein-5 through a p53-dependent mechanism. Mol Biol Cell 2007;18:4543-4552
42. Elzi DJ, Lai Y, Song M, Hakala K, Weintraub ST, Shiio Y. Plasminogen activator inhibitor 1-insulin-like growth factor binding protein 3 cascade regulates stress-induced senescence. Proc Natl Acad Sci U S A 2012;109:12052-12057
43. Frystyk J. Free insulin-like growth factors-measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res 2004;14:337-375
44. Minamino T, Miyauchi H, Tateno K, Kunieda T, Komuro I. Akt-induced cellular senescence: Implication for human disease. Cell Cycle 2004;3:449-451
45. Chan SS, Twigg SM, Firth SM, Baxter RC. Insulin-like growth factor binding protein-3 leads to insulin resistance in adipocytes. J Clin Endocrinol Metab 2005; 90:6588-6595
46. Silha JV, Gui Y, Murphy LJ. Impaired glucose homeostasis in insulin-like growth factor-binding protein-3-transgenic mice. Am J Physiol Endocrinol Metab 2002;283:E937-E945
47. Galadari S, Rahman A, Pallichankandy S, Galadari A, Thayyullathil F. Role of ceramide in diabetes mellitus: Evidence and mechanisms. Lipids Health Dis 2013;12:98
48. Mouton RE, Venable ME. Ceramide induces expression of the senescence histochemical marker, beta-galactosidase, in human fibroblasts. Mech Ageing Dev 2000;113:169-181
49. Ford JH. Saturated fatty acid metabolism is key link between cell division, cancer, and senescence in cellular and whole organism aging. Age (Dordr) 2010; 32:231-237
50. Zuellig RA, Hornemann T, Othman A, et al. Deoxysphingolipids, novel biomarkers for type 2 diabetes, are cytotoxic for insulin-producing cells. Diabetes 2014;63:1326-1339
51. Yang G, Badeanlou L, Bielawski J, Roberts AJ, Hannun YA, Samad F. Central role of ceramide biosynthesis in body weight regulation, energy metabolism, and the metabolic syndrome. Am J Physiol Endocrinol Metab 2009; 297:E211-E224
52. Xu H, Barnes GT, Yang Q, et al. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 2003; 112:1821-1830
53. Kim CS, Park HS, Kawada T, et al. Circulating levels of MCP-1 and IL-8 are elevated in human obese subjects and associated with obesity-related parameters. Int J Obes (Lond) 2006;30:1347-1355
54. Utsal L, Tillmann V, Zilmer M, et al. Elevated serum IL-6, IL-8, MCP-1, CRP, and IFN-g levels in 10-to 11-year-old boys with increased BMI. Horm Res Paediatr 2012;78:31-39
55. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA 2001;286: 327-334
56. Spranger J, Kroke A, Möhlig M, et al. Inflammatory cytokines and the risk to develop type 2 diabetes: Results of the prospective population-based European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam Study. Diabetes 2003;52:812-817
57. Schneider DJ, Sobel BE. PAI-1 and diabetes: A journey from the bench to the bedside. Diabetes Care 2012;35:1961-1967
58. Davalos AR, Kawahara M, Malhotra GK, et al. p53-Dependent release of Alarmin HMGB1 is a central mediator of senescent phenotypes. J Cell Biol 2013; 201:613-629
59. Stern DM, Yan SD, Yan SF, Schmidt AM. Receptor for advanced glycation endproducts (RAGE) and the complications of diabetes. Ageing Res Rev 2002;1: 1-15
60. Hamm JK, el Jack AK, Pilch PF, Farmer SR. Role of PPAR gamma in regulating adipocyte differentiation and insulin-responsive glucose uptake. Ann N Y Acad Sci 1999;892:134-145
61. Young AR, Narita M, Ferreira M, et al. Autophagy mediates the mitotic senescence transition. Genes Dev 2009;23:798-803
62. Tchkonia T, Corkey BE, Kirkland JL. Current views of the fat cell as an endocrine cell: Lipotoxicity. In Overweight and the Metabolic Syndrome: From Bench to Bedside (Endocrine Updates). Bray GA, Ryan DH, Eds. New York, Springer, 2006, p. 105-118
63. Sone H, Kagawa Y. Pancreatic beta cell senescence contributes to the pathogenesis of type 2 diabetes in high-fat diet-induced diabetic mice. Diabetologia 2005;48:58-67
64. Uchida T, Nakamura T, Hashimoto N, et al. Deletion of Cdkn1b ameliorates hyperglycemia by maintaining compensatory hyperinsulinemia in diabetic mice. Nat Med 2005;11:175-182
65. Tavana O, Puebla-Osorio N, Sang M, Zhu C. Absence of p53-dependent apoptosis combined with nonhomologous end-joining deficiency leads to a severe diabetic phenotype in mice. Diabetes 2010;59:135-142
66. Zhu Y, Tchkonia T, Pirtskhalava T, et al. The Achilles' heel of senescent cells: From transcriptome to senolytic drugs. Aging Cell. 9 March 2015 [Epub ahead of print]. DOI: 10.1111/acel.12344
67. Verzola D, Gandolfo MT, Gaetani G, et al. Accelerated senescence in the kidneys of patients with type 2 diabetic nephropathy. Am J Physiol Renal Physiol 2008;295:F1563-F1573
68. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005;433:760-764
69. Golde TE, Miller VM. Proteinopathy-induced neuronal senescence: A hypothesis for brain failure in Alzheimer's and other neurodegenerative diseases. Alzheimers Res Ther 2009;1:5
70. Chinta SJ, Lieu CA, Demaria M, Laberge RM, Campisi J, Andersen JK. Environmental stress, ageing and glial cell senescence: A novel mechanistic link to Parkinson's disease? J Intern Med 2013;273:429-436
71. Jurk D, Wang C, Miwa S, et al. Postmitotic neurons develop a p21-dependent senescence-like phenotype driven by a DNA damage response. Aging Cell 2012;11:996-1004
72. Kiliaan AJ, Arnoldussen IA, Gustafson DR. Adipokines: A link between obesity and dementia? Lancet Neurol 2014;13:913-923
73. Banks WA, Kastin AJ, Broadwell RD. Passage of cytokines across the bloodbrain barrier. Neuroimmunomodulation 1995;2:241-248
74. Rota M, LeCapitaine N, Hosoda T, et al. Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66shc gene. Circ Res 2006;99:42-52
75. Kortlever RM, Higgins PJ, Bernards R. Plasminogen activator inhibitor-1 is a critical downstream target of p53 in the induction of replicative senescence. Nat Cell Biol 2006;8:877-884
76. Wan YZ, Gao P, Zhou S, et al. SIRT1-mediated epigenetic downregulation of plasminogen activator inhibitor-1 prevents vascular endothelial replicative senescence. Aging Cell 2014;13:890-899
77. Eren M, Boe AE, Murphy SB, et al. PAI-1-regulated extracellular proteolysis governs senescence and survival in Klotho mice. Proc Natl Acad Sci U S A 2014; 111:7090-7095
78. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: Possible role in insulin resistance. Science 2003;300:1140-1142
79. Passos JF, Nelson G, Wang C, et al. Feedback between p21 and reactive oxygen production is necessary for cell senescence. Mol Syst Biol 2010;6: 347
80. Aw D, Silva AB, Palmer DB. Immunosenescence: Emerging challenges for an ageing population. Immunology 2007;120:435-446
81. Ghesquière B, Wong BW, Kuchnio A, Carmeliet P. Metabolism of stromal and immune cells in health and disease. Nature 2014;511:167-176
82. Chiu BC, Martin BE, Stolberg VR, Chensue SW. The host environment is responsible for aging-related functional NK cell deficiency. J Immunol 2013;191: 4688-4698
83. Xue W, Zender L, Miething C, et al. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 2007;445: 656-660
84. Lutz CT, Quinn LS. Sarcopenia, obesity, and natural killer cell immune senescence in aging: Altered cytokine levels as a common mechanism. Aging (Albany, NY Online) 2012;4:535-546
85. Sebastian C, Lloberas J, Celada A. Molecular and cellular aspects of macrophage aging. In Handbook on Immunosenescence. Fulop T, Ed. New York, Springer, 2009, p. 919-945
86. Harrison DE, Strong R, Allison DB, et al. Acarbose, 17-a-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell 2014;13:273-282
87. Martin-Montalvo A, Mercken EM, Mitchell SJ, et al. Metformin improves healthspan and lifespan in mice. Nat Commun 2013;4:2192
88. Yin M, Zhou J, Gorak EJ, Quddus F. Metformin is associated with survival benefit in cancer patients with concurrent type 2 diabetes: A systematic review and meta-analysis. Oncologist 2013;18:1248-1255
89. Bannister CA, Holden SE, Jenkins-Jones S, et al. Can people with type 2 diabetes live longer than those without? A comparison of mortality in people initiated with metformin or sulphonylurea monotherapy and matched, nondiabetic controls. Diabetes Obes Metab 2014;16:1165-1173
90. Noto H, Goto A, Tsujimoto T, Noda M. Cancer risk in diabetic patients treated with metformin: A systematic review and meta-analysis. PLoS One 2012; 7:e33411
91. Moiseeva O, Deschênes-Simard X, St-Germain E, et al. Metformin inhibits the senescence-associated secretory phenotype by interfering with IKK/NF-kB activation. Aging Cell 2013;12:489-498
92. Leng S, Chaves P, Koenig K, Walston J. Serum interleukin-6 and hemoglobin as physiological correlates in the geriatric syndrome of frailty: A pilot study. J Am Geriatr Soc 2002;50:1268-1271
93. Dörr JR, Yu Y, Milanovic M, et al. Synthetic lethal metabolic targeting of cellular senescence in cancer therapy. Nature 2013;501:421-425
94. Stolar M. Glycemic control and complications in type 2 diabetes mellitus. Am J Med 2010;123(Suppl.):S3-S11