Home LiteratureArticle Details
PMID: 19718037 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A crucial role for adipose tissue p53 in the regulation of insulin resistance.

Nature medicine ·Vol. 15 ·No. 9 ·2009-09-00 ·Pages 1082-7

Minamino T, Orimo M, Shimizu I, Kunieda T, Yokoyama M, Ito T, Nojima A, Nabetani A, Oike Y, Matsubara H, Ishikawa F, Komuro I

Abstract

Various stimuli, such as telomere dysfunction and oxidative stress, can induce irreversible cell growth arrest, which is termed 'cellular senescence'. This response is controlled by tumor suppressor proteins such as p53 and pRb. There is also evidence that senescent cells promote changes related to aging or age-related diseases. Here we show that p53 expression in adipose tissue is crucially involved in the development of insulin resistance, which underlies age-related cardiovascular and metabolic disorders. We found that excessive calorie intake led to the accumulation of oxidative stress in the adipose tissue of mice with type 2 diabetes-like disease and promoted senescence-like changes, such as increased activity of senescence-associated beta-galactosidase, increased expression of p53 and increased production of proinflammatory cytokines. Inhibition of p53 activity in adipose tissue markedly ameliorated these senescence-like changes, decreased the expression of proinflammatory cytokines and improved insulin resistance in mice with type 2 diabetes-like disease. Conversely, upregulation of p53 in adipose tissue caused an inflammatory response that led to insulin resistance. Adipose tissue from individuals with diabetes also showed senescence-like features. Our results show a previously unappreciated role of adipose tissue p53 expression in the regulation of insulin resistance and suggest that cellular aging signals in adipose tissue could be a new target for the treatment of diabetes (pages 996-967).

MeSH Terms
Adipose Tissue/metabolism Aging/genetics,metabolism Animals Cyclin-Dependent Kinase Inhibitor p21/genetics,metabolism Diabetes Mellitus, Type 2/genetics,metabolism Energy Intake Genes, p53 Insulin Resistance/genetics,physiology Mice Mice, Mutant Strains Mice, Transgenic Oxidative Stress RNA, Messenger/genetics,metabolism Signal Transduction Tumor Suppressor Protein p53/deficiency,genetics,metabolism
Chemicals
Cdkn1a protein, mouse Cyclin-Dependent Kinase Inhibitor p21 RNA, Messenger Tumor Suppressor Protein p53
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Minamino Tohru
Department of Cardiovascular Science and Medicine, Chiba University Graduate School of Medicine, Chuo-ku, Chiba, Japan.
Orimo Masayuki
Shimizu Ippei
Kunieda Takeshige
Yokoyama Masataka
Ito Takashi
Nojima Aika
Nabetani Akira
Oike Yuichi
Matsubara Hisahiro
Ishikawa Fuyuki
Komuro Issei
References (31)
31 references, click to expand
  1. Telomere length regulation.
    Annu Rev Biochem. 1996;65:337-65 PMID: 8811183
  2. Extended longevity in mice lacking the insulin receptor in adipose tissue.
    Science. 2003 Jan 24;299(5606):572-4 PMID: 12543978
  3. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2.
    Science. 1999 Feb 26;283(5406):1321-5 PMID: 10037601
  4. A biomarker that identifies senescent human cells in culture and in aging skin in vivo.
    Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9363-7 PMID: 7568133
  5. Cellular senescence in aging primates.
    Science. 2006 Mar 3;311(5765):1257 PMID: 16456035
  6. Obesity is associated with macrophage accumulation in adipose tissue.
    J Clin Invest. 2003 Dec;112(12):1796-808 PMID: 14679176
  7. Telomeres: cancer to human aging.
    Annu Rev Cell Dev Biol. 2006;22:531-57 PMID: 16824017
  8. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors.
    Cell. 2005 Feb 25;120(4):513-22 PMID: 15734683
  9. The fatty acid-binding protein, aP2, coordinates macrophage cholesterol trafficking and inflammatory activity. Macrophage expression of aP2 impacts peroxisome proliferator-activated receptor gamma and IkappaB kinase activities.
    J Biol Chem. 2005 Apr 1;280(13):12888-95 PMID: 15684432
  10. The plasticity of aging: insights from long-lived mutants.
    Cell. 2005 Feb 25;120(4):449-60 PMID: 15734678
  11. Transcriptional activation of cyclooxygenase-2 by tumor suppressor p53 requires nuclear factor-kappaB.
    Oncogene. 2006 Sep 21;25(42):5708-18 PMID: 16682957
  12. Putting the stress on senescence.
    Curr Opin Cell Biol. 2001 Dec;13(6):748-53 PMID: 11698192
  13. Presence of telomeric G-strand tails in the telomerase catalytic subunit TERT knockout mice.
    Genes Cells. 1999 Oct;4(10):563-72 PMID: 10583505
  14. Vascular aging: insights from studies on cellular senescence, stem cell aging, and progeroid syndromes.
    Nat Clin Pract Cardiovasc Med. 2008 Oct;5(10):637-48 PMID: 18762784
  15. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis.
    Cell. 1999 May 14;97(4):527-38 PMID: 10338216
  16. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance.
    Science. 1993 Jan 1;259(5091):87-91 PMID: 7678183
  17. Long-lived Drosophila with overexpressed dFOXO in adult fat body.
    Science. 2004 Jul 16;305(5682):361 PMID: 15192154
  18. Senescence and immortalization: role of telomeres and telomerase.
    Carcinogenesis. 2005 May;26(5):867-74 PMID: 15471900
  19. Lack of macrophage fatty-acid-binding protein aP2 protects mice deficient in apolipoprotein E against atherosclerosis.
    Nat Med. 2001 Jun;7(6):699-705 PMID: 11385507
  20. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA.
    Cell. 1997 Oct 3;91(1):25-34 PMID: 9335332
  21. 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 Apr 15;14(8):994-1004 PMID: 10783170
  22. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance.
    Dev Cell. 2002 Jul;3(1):25-38 PMID: 12110165
  23. Rise in insulin resistance is associated with escalated telomere attrition.
    Circulation. 2005 May 3;111(17):2171-7 PMID: 15851602
  24. Role of NF-kappaB in p53-mediated programmed cell death.
    Nature. 2000 Apr 20;404(6780):892-7 PMID: 10786798
  25. Drosophila dFOXO controls lifespan and regulates insulin signalling in brain and fat body.
    Nature. 2004 Jun 3;429(6991):562-6 PMID: 15175753
  26. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance.
    J Biol Chem. 2006 Sep 8;281(36):26602-14 PMID: 16809344
  27. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30.
    Nat Med. 2002 Jul;8(7):731-7 PMID: 12068289
  28. Tissue-specific activities of C. elegans DAF-16 in the regulation of lifespan.
    Cell. 2003 Nov 14;115(4):489-502 PMID: 14622602
  29. Increased oxidative stress in obesity and its impact on metabolic syndrome.
    J Clin Invest. 2004 Dec;114(12):1752-61 PMID: 15599400
  30. Essential role of mouse telomerase in highly proliferative organs.
    Nature. 1998 Apr 9;392(6676):569-74 PMID: 9560153
  31. Vascular cell senescence: contribution to atherosclerosis.
    Circ Res. 2007 Jan 5;100(1):15-26 PMID: 17204661
Article Info
Journal
Nature medicine
Abbr.
Nat Med
ISSN
1546-170X
Published
2009-09-00
Epub
2009-00-30
Pages
1082-7
Language
English
Region
United States
NLM ID
9502015
Subset
IM
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com