Expression of caveolin-3 as positive intracellular signaling regulator on the development of hypertrophy in cardiac tissues

  • Kim, Joo-Heon (Institute of Animal Medicine, College of Veterinary Medicine, Gyeongsang National University) ;
  • Han, Jin (Cardiovascular & Metabolic Disease Center, College of Medicine, Inje University) ;
  • Kim, Yong-Kwon (College of Biomedical Science and Engineering, Inje University) ;
  • Yang, Young-Ae (College of Biomedical Science and Engineering, Inje University) ;
  • Hong, Yonggeun (Cardiovascular & Metabolic Disease Center, College of Medicine, Inje University)
  • Accepted : 2005.11.28
  • Published : 2005.12.29

Abstract

We have examined distribution and expression of caveolin-3 (cav-3), one of three caveolin isoforms from 16-wks-old spontaneously hypertensive rats (SHR) compared with age-matched control wistar-kyoto (WKY) rats. The expression of cav-3 was increased, whereas expression of PKB/Akt and calcineurin (Cn) was not changed in cardiac tissues of SHR compared to WKY rats. Interestingly, expression of cav-3, PKB/Akt and Cn were decreased in plasma membrane fraction in SHR compared to WKY rats. In H9c2 cardiomyoblast cells treated with phenylephrine ($50{\mu}M$, 48hr) or isoproterenol ($10{\mu}M$, 48hr), the expression of cav-3 was markedly enhanced compared to nontreated cells. Upon immunofluorescence analysis, cav-3 was localized in plasma membrane of control H9c2 cells. However phenylephrine or isoproterenol treatment caused translocation of cav-3 to perinuclear region. These results suggest that cav-3 plays as positive regulators in the development of hypertrophy in cardiac tissues of SHR rats.

Keywords

References

  1. Anderson RGW. The caveolae membrane system. Annu Rev Biochem 1998, 67, 199-225 https://doi.org/10.1146/annurev.biochem.67.1.199
  2. Baumann CA, Ribon V, Kanzaki M, Thurmound DC, Mora S, Shigematsu S, Bickel PE, Pessin JE, Saltiel AR. CAP defines a second signaling pathway required for insulin-stimulated glucosetransport. Nature 2000, 407, 202-207 https://doi.org/10.1038/35025089
  3. Boheler KR, Schwartzk M. Gene expression in cardiac hypertrophy. Trends Cardiovasc Med 1992, 5, 176-182
  4. Colombo F, Noel J, Mayers P, Mericier I, Calderone A. Beta-adrenergic stimulation of rat cardiac fibroblasts promotes protein synthesis via the activation of phosphatidylinositol 3-kinase. J Mol Cell Cardiol 2001, 33, 1091-1106 https://doi.org/10.1006/jmcc.2001.1381
  5. De Windt LJ, Lim HW, Bueno OF, Liang Q, Delling U, Braz JC, Glascock, Limball TF, del Monte F, Hajjar RJ, Molkentin JD. Targeted inhibition of calcineurin attenuates cardiac hypertrophy in vivo. Proc Natl Acad Sci USA 2001, 98, 3322-3327
  6. Engelman JA, Chu C, Lin A, Jo H, Ikezu T, Okamoto T, Kohtz DS, Lisanti MP. Caveolinmediated regulation of signaling along the p42/44 MAP kinase cascade in vivo; a role for the caveolinscaffolding domain, FEBS Lett 1998, 428, 205-211 https://doi.org/10.1016/S0014-5793(98)00470-0
  7. Engelman JA, Zhang XL, Razani B, Pestell RG, Lisanti MP. p42/44 MAP kinase-dependent and - independent signaling pathways regulate caveolin-1 gene expression. Activation of ras-MAP kinase and protein kinase a signaling cascade transcriptionally down-regulates caveolin-1 promoter activity. J Biol Chem 1999, 274, 32333-32341 https://doi.org/10.1074/jbc.274.45.32333
  8. Fujimoto TKH, Nomura RUT. Isoforms of caveolin-1 and caveolar structure. J Cell Sci 2000, 113, 3509-3517
  9. Fujta T, Yoya Y, Iwatsubo K, Ouda T, Kimura K, Umemura S, Ishikawa Y. Accumulation of molecules involved in a1-adrenergic signal within caveolae: caveolin expression and the development of cardiac hypertrophy. Cardiovascular Res 2001, 51, 709-716 https://doi.org/10.1016/S0008-6363(01)00348-0
  10. Galbiati F, Volonte D, Engelman JA, Scherer PE, Lisanti MP. Targeted down-regulation of caveolin-3 is sufficient to inhibit myotube formation in differentiating C2C12 myoblasts. Transient activationof p38 mitogenactivated protein kinase is required for induction of caveolin-3 expression and subsequent myotube formation. J Biol Chem 1999, 274, 30315-30321 https://doi.org/10.1074/jbc.274.42.30315
  11. Gerdes J Li L, Schlueter C, Duchrow M, Wohlenberg C, Gerlach C, Stahmer I. Immunobiological and molecular biological characterization of the cell proliferation-associated nuclear antigen that is defined by monoclonal antibody Ki-67. Am J Pathol 1991, 138, 867-873
  12. Gustavsson J, Parpal S, Kalrlsson M, Ramising C, Thorn H, Borg M, Lindroth M, Peterson HK, Magnusson KE, Stralfors P. Localization of the insulin receptor in caveolae of adipocyte plasma membrane. FASEB J 1999, 13, 1961-1971
  13. Hong SH, Ondrey FG, Avis IM, Chen Z, Loukinova E, Cavanaugh PF Jr, Waes C, Mulshine JL. Cyclooxygenase regulates human oropharyngeal carcinomas via the proinflammatory cytokine IL-6: a general role for inflammation? FASEB J 2000, 14, 1499-1507 https://doi.org/10.1096/fj.14.11.1499
  14. Hong Y, Cho JH, Kim JH. Involvement of calcineurin and Akt/PKB in development of hereditary hypertension. Korean J Vet Res 2004, 44, 7-13
  15. Karpen JW, Rich TC. The fourth dimension in cellular signaling. Science 2001, 293, 2204-2205 https://doi.org/10.1126/science.293.5538.2204
  16. Kurzchalia TV, Parton RG. Membrane microdomains and caveolae. Curr Opin Cell Biol 1999, 11, 424-431 https://doi.org/10.1016/S0955-0674(99)80061-1
  17. MacLellan WR, Schneider MD. Genetic dissection of cardiac growth control pathways. Annu Rev Physiol 2000, 62, 289-319 https://doi.org/10.1146/annurev.physiol.62.1.289
  18. Marian AJ, Roberts R. Recent advances in the molecular genetics of hypertrophic cardiomyopathy. Circulation 1995, 92, 1336-1347 https://doi.org/10.1161/01.CIR.92.5.1336
  19. Marian AJ, Roberts R. Familial hypertrophic cardiomyopathy: a paradigm of the cardiac hypertrophic response to injury. Ann Med 1998, Suppl 1, 24-32
  20. Molkentin JD, Dorn II GW. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu Rev Physiol 2001, 63, 391-426 https://doi.org/10.1146/annurev.physiol.63.1.391
  21. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 1998, 93, 215-228 https://doi.org/10.1016/S0092-8674(00)81573-1
  22. Nicol RL, Frey N, Pearson G, Cobb M, Richardson J, Olson EN. Activated MEK5 induces serial assembly of sarcomeres and eccentric cardiac hypertrophy. EMBO J 2001, 20, 2757-2767 https://doi.org/10.1093/emboj/20.11.2757
  23. Okamoto T, Schlegel A, Scherer PE, Lisanti MP. Caveolins a family of scaffolding proteins for organizing preassembled signaling complexes at the plasma membrane. J Biol Chem 1998, 273, 5419-5422 https://doi.org/10.1074/jbc.273.10.5419
  24. Ostrom RS, Gregorian C, Drenan RM, Xiang Y, Regan JW, Insel PA. Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem 2001, 276, 42063-42069 https://doi.org/10.1074/jbc.M105348200
  25. Palade GE. An electron microscope study of the mitochondrial structure. J Histochem Cytochem 1953, 1, 188-211 https://doi.org/10.1177/1.4.188
  26. Pfeffer MA, Frohlich ED, Pfeffer JM, Yunice A, Nordquist JA. Pathophysiological implications of the increased cardiac output of young spontaneously hypertensive rats. Circ Res 1974, 34/35, I235-I242
  27. Razani B, Schlegel A, Lisanti MP. Caveolin proteins in signaling, oncogenic transformation and muscular dystrophy. J Cell Sci 2000, 113, 2103-2109
  28. Schlegel A, Lisanti MP. Caveolae and their coat proteins, the caveolins: from electron microscopic novelty to biological launching pad. J Cell Physiol 2001, 186, 329-337 https://doi.org/10.1002/1097-4652(2001)9999:9999<000::AID-JCP1045>3.0.CO;2-0
  29. Smart EJ, Graft GA, McNiven MA, Sessa WC, Engelman JA, Scherer PE, Okamoto T, Lisanti MP. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 1999, 19, 7289-7304 https://doi.org/10.1128/MCB.19.11.7289
  30. Smart EJ, Ying YS, Mineo C, Anderson RGW. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc Natl Acad Sci USA 1995, 92, 10104-10108
  31. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP. Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the arcolemma and co-fractionates with dystrophin and dystrophin associated glycoproteins. J Biol Chem 1996, 271, 15160-15165 https://doi.org/10.1074/jbc.271.25.15160
  32. Sussman MM, Lim HW, Gude N, Taigen T, Olson EN, Robbins J, Colbert MC, Gualberto A, Wieezorek DF, Molkentin JD. Prevention of cardiac hypertrophy in mice by calcineurin inhibition. Science 1998, 281, 1690-1693 https://doi.org/10.1126/science.281.5383.1690
  33. Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF, Lisanti MP. Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem 1996, 271, 2255- 2261 https://doi.org/10.1074/jbc.271.4.2255
  34. Tang Z, Okamoto T, Boontrakulpoontawee P, Katada T, Otsuka AJ, Lisanti MP. Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegans. Implication for the molecular evolution of mammalian caveolin genes. J Biol Chem 1997, 272, 2437-2445 https://doi.org/10.1074/jbc.272.4.2437
  35. Taylor JM, Rovin JD, Parsons T. A role for focal adhesion kinase in phenylephrine-induced hypertrophy of rat ventricular cardiomyocytes. J Biol Chem 2000, 275, 19250-19257 https://doi.org/10.1074/jbc.M909099199
  36. Toya Y, Schwencke C, Couet J, Lisanti MP, Ishikawa Y. Inhibition of adenyl cyclase by caveolin peptides. Endocrinology 1998, 139, 15693-15701
  37. Uehara K, Miyoshi M. Tubular invaginations with caveolae and coated pits in the sinus endothelial cells of the rat spleen. Histochem Cell Biol 1999, 112, 351-358 https://doi.org/10.1007/s004180050416
  38. Watanabe T, Pakala R, Katagiri T, Benedict CR. Angiotensin II and serotonin potentiate endothelin-1-induced vascular smooth muscle cell proliferation. J Hypertension 2001, 19, 731-739 https://doi.org/10.1097/00004872-200104000-00010
  39. Yamada E. The fine structure of the gall bladder of the mouse. J Biophys Biochem Cytol 1955, 1, 445-458 https://doi.org/10.1083/jcb.1.5.445
  40. Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 2004, 18, 1272-1282 https://doi.org/10.1101/gad.1199904
  41. Zou Y, Komuro I, Yamazaki T, Kudoh S, Uozumi H, Kadowaki T, Yazaki Y. Both Gs and Gi proteins are critically involved cardiomyocyte. J Biol Chem 1999, 274, 9760-9770 https://doi.org/10.1074/jbc.274.14.9760