Journal of Molecular and Cellular Cardiology
Volume 47, Issue 6 , Pages 798-809 , December 2009

Angiotensin II type 1 receptor-associated protein prevents vascular smooth muscle cell senescence via inactivation of calcineurin/nuclear factor of activated T cells pathway

  • Li-Juan Min

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Masaki Mogi

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Kouichi Tamura

      Affiliations

    • Department of Medical Science and Cardiorenal Medicine, Yokohama City University Graduate School of Medicine, Yokohama, Japan
    • ,
  • Jun Iwanami

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Akiko Sakata

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Teppei Fujita

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Kana Tsukuda

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Fei Jing

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Masaru Iwai

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • ,
  • Masatsugu Horiuchi

      Affiliations

    • Department of Molecular Cardiovascular Biology and Pharmacology, Graduate School of Medicine, Ehime University, Tohon, Ehime 791-0295, Japan
    • Corresponding Author InformationCorresponding author. Tel: +81 89 960 5248; fax: +81 89 960 5251.

Received 15 May 2009 ,Revised 28 August 2009 ,Accepted 9 September 2009.

References 

  1. de Gasparo M, Catt KJ, Inagami T, Wright JW, Unger T. International union of pharmacology. XXIII. The angiotensin II receptors. Pharmacol. Rev. 2000;52:415–472
  2. Carey RM, Siragy HM. Newly recognized components of the renin–angiotensin system: potential roles in cardiovascular and renal regulation. Endocr. Rev. 2003;24:261–271
  3. Bockaert J, Marin P, Dumuis A, Fagni L. The ‘magic tail’ of G protein-coupled receptors: an anchorage for functional protein networks. FEBS Lett. 2003;546:65–72
  4. Daviet L, Lehtonen JY, Tamura K, Griese DP, Horiuchi M, Dzau VJ. Cloning and characterization of ATRAP, a novel protein that interacts with the angiotensin II type 1 receptor. J. Biol. Chem. 1999;274:17058–17062
  5. Tamura K, Tanaka Y, Tsurumi Y, Azuma K, Shigenaga A, Wakui H, et al. The role of angiotensin AT1 receptor-associated protein in renin–angiotensin system regulation and function. Curr. Hypertens Rep. 2007;9:121–127
  6. Azuma K, Tamura K, Shigenaga A, Wakui H, Masuda S, Tsurumi-Ikeya Y, et al. Novel regulatory effect of angiotensin II type 1 receptor-interacting molecule on vascular smooth muscle cells. Hypertension. 2007;50:926–932
  7. Cui T, Nakagami H, Iwai M, Takeda Y, Shiuchi T, Tamura K, et al. ATRAP, novel AT1 receptor associated protein, enhances internalization of AT1 receptor and inhibits vascular smooth muscle cell growth. Biochem. Biophys. Res. Commun. 2000;279:938–941
  8. Hunyady L, Catt KJ, Clark AJ, Gaborik Z. Mechanisms and functions of AT(1) angiotensin receptor internalization. Regul. Pept. 2000;91:29–44
  9. Olivares-Reyes JA, Smith RD, Hunyady L, Shah BH, Catt KJ. Agonist-induced signaling, desensitization, and internalization of a phosphorylation-deficient AT1A angiotensin receptor. J. Biol. Chem. 2001;276:37761–37768
  10. Suzuki E, Nishimatsu H, Satonaka H, Walsh K, Goto A, Omata M, et al. Angiotensin II induces myocyte enhancer factor 2- and calcineurin/nuclear factor of activated T cell-dependent transcriptional activation in vascular myocytes. Circ. Res. 2002;90:1004–1011
  11. Nilsson J, Nilsson LM, Chen YW, Molkentin JD, Erlinge D, Gomez MF. High glucose activates nuclear factor of activated T cells in native vascular smooth muscle. Arterioscler. Thromb Vasc. Biol. 2006;26:794–800
  12. Huang C, Mattjus P, Ma WY, Rincon M, Chen NY, Brown RE, et al. Involvement of nuclear factor of activated T cells activation in UV response. Evidence from cell culture and transgenic mice. J. Biol. Chem. 2000;275:9143–9149
  13. Horsley V, Pavlath GK. NFAT: ubiquitous regulator of cell differentiation and adaptation. J. Cell Biol. 2002;156:771–774
  14. Dostal DE. The cardiac renin–angiotensin system: novel signaling mechanisms related to cardiac growth and function. Regul. Pept. 2000;91:1–11
  15. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell. 1998;93:215–228
  16. Guo S, Lopez-Ilasaca M, Dzau VJ. Identification of calcium-modulating cyclophilin ligand (CAML) as transducer of angiotensin II-mediated nuclear factor of activated T cells (NFAT) activation. J. Biol. Chem. 2005;280:12536–12541
  17. Kunieda T, Minamino T, Nishi J, Tateno K, Oyama T, Katsuno T, 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
  18. Min LJ, Mogi M, Iwanami J, Li JM, Sakata A, Fujita T, et al. Cross-talk between aldosterone and angiotensin II in vascular smooth muscle cell senescence. Cardiovasc. Res. 2007;76:506–516
  19. Basso N, Paglia N, Stella I, de Cavanagh EM, Ferder L, del Rosario Lores Arnaiz M, et al. Protective effect of the inhibition of the renin–angiotensin system on aging. Regul. Pept. 2005;128:247–252
  20. Imanishi T, Hano T, Nishio I. Angiotensin II accelerates endothelial progenitor cell senescence through induction of oxidative stress. J. Hypertens. 2005;23:97–104
  21. Chen Y, Kelm RJ, Budd RC, Sobel BE, Schneider DJ. Inhibition of apoptosis and caspase-3 in vascular smooth muscle cells by plasminogen activator inhibitor type-1. J. Cell Biochem. 2004;92:178–188
  22. Min LJ, Mogi M, Iwanami J, Li JM, Sakata A, Fujita T, et al. Angiotensin II type 2 receptor deletion enhances vascular senescence by methyl methanesulfonate sensitive 2 inhibition. Hypertension. 2008;51:1339–1344
  23. Tsurumi Y, Tamura K, Tanaka Y, Koide Y, Sakai M, Yabana M, et al. Interacting molecule of AT1 receptor, ATRAP, is colocalized with AT1 receptor in the mouse renal tubules. Kidney Int. 2006;69:488–494
  24. Min LJ, Mogi M, Li JM, Iwanami J, Iwai M, Horiuchi M. Aldosterone and angiotensin II synergistically induce mitogenic response in vascular smooth muscle cells. Circ. Res. 2005;97:434–442
  25. Luo Q, Kang Q, Si W, Jiang W, Park JK, Peng Y, et al. Connective tissue growth factor (CTGF) is regulated by Wnt and bone morphogenetic proteins signaling in osteoblast differentiation of mesenchymal stem cells. J. Biol. Chem. 2004;279:55958–55968
  26. Oshita A, Iwai M, Chen R, Ide A, Okumura M, Fukunaga S, et al. Attenuation of inflammatory vascular remodeling by angiotensin II type 1 receptor-associated protein. Hypertension. 2006;48:671–676
  27. Chainiaux F, Magalhaes JP, Eliaers F, Remacle J, Toussaint O. UVB-induced premature senescence of human diploid skin fibroblasts. Int. J. Biochem. Cell. Biol. 2002;34:1331–1339
  28. Tanaka Y, Tamura K, Koide Y, Sakai M, Tsurumi Y, Noda Y, et al. The novel angiotensin II type 1 receptor (AT1R)-associated protein ATRAP downregulates AT1R and ameliorates cardiomyocyte hypertrophy. FEBS Lett. 2005;579:1579–1586
  29. Miura S, Saku K, Karnik SS. Molecular analysis of the structure and function of the angiotensin II type 1 receptor. Hypertens Res. 2003;26:937–943
  30. Lopez-Ilasaca M, Liu X, Tamura K, Dzau VJ. The angiotensin II type I receptor-associated protein, ATRAP, is a transmembrane protein and a modulator of angiotensin II signaling. Mol. Biol. Cell. 2003;14:5038–5050
  31. Itahana K, Dimri GP, Hara E, Itahana Y, Zou Y, Desprez PY, et al. A role for p53 in maintaining and establishing the quiescence growth arrest in human cells. J. Biol. Chem. 2002;277:18206–18214
  32. Ferbeyre G, de Stanchina E, Lin AW, Querido E, McCurrach ME, Hannon GJ, et al. Oncogenic ras and p53 cooperate to induce cellular senescence. Mol. Cell Biol. 2002;22:3497–3508
  33. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, et al. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 2004;94:110–8.
  34. Santini MP, Talora C, Seki T, Bolgan L, Dotto GP. Cross talk among calcineurin, Sp1/Sp3, and NFAT in control of p21(WAF1/CIP1) expression in keratinocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 2001;98:9575–9580
  35. Rivera A, Maxwell SA. The p53-induced gene-6 (proline oxidase) mediates apoptosis through a calcineurin-dependent pathway. J. Biol. Chem. 2005;280:29346–29354
  36. Zhang LH, Youn HD, Liu JO. Inhibition of cell cycle progression by the novel cyclophilin ligand sanglifehrin A is mediated through the NFkappa B-dependent activation of p53. J. Biol. Chem. 2001;276:43534–43540
  37. Conchon S, Barrault MB, Miserey S, Corvol P, Clauser E. The C-terminal third intracellular loop of the rat AT1A angiotensin receptor plays a key role in G protein coupling specificity and transduction of the mitogenic signal. J. Biol. Chem. 1997;272:25566–25572

PII: S0022-2828(09)00382-4

doi: 10.1016/j.yjmcc.2009.09.006

Journal of Molecular and Cellular Cardiology
Volume 47, Issue 6 , Pages 798-809 , December 2009

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