Caveolin-2 is a negative regulator of anti-proliferative function and signaling of transforming growth factor-β in endothelial cells

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 5, 2011, Pages

  Xie, Leike ^a   Vo Ransdell, Chi ^a   Abel, Britain ^a   Willoughby, Cara ^a   Jang, Sungchan ^a   Sowa, Grzegorz ^a  

^a University of Missouri   (United States)

Author keywords

Activin receptor like kinase 5; Caveolin 1; Collagen type 1; Plasminogen activator inhibitor 1; Smad2 3

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; BROXURIDINE; CAVEOLIN 2; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INHIBITION KINETICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA ISOLATION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE;

ANIMALS; CAVEOLIN 2; CELL PROLIFERATION; CELLS, CULTURED; COLLAGEN TYPE I; ENDOTHELIAL CELLS; LUNG; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHOSPHORYLATION; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

EID: 80054881030     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00486.2010     Document Type: Article

References (57)

1. Aprelikova O, Xiong Y, Liu ET. Both p16 and p21 families of cyclindependent kinase (CDK) inhibitors block the phosphorylation of cyclindependent kinases by the CDK-activating kinase. J Biol Chem 270: 18195-18197, 1995.
2. Bohnsack BL, Hirschi KK. Red light, green light: signals that control endothelial cell proliferation during embryonic vascular development. Cell Cycle 3: 1506-1511, 2004.
3. Byfield SD, Roberts AB. Lateral signaling enhances TGF-β response complexity. Trends Cell Biol 14: 107-111, 2004.
4. Chan YG, Cardwell MM, Hermanas TM, Uchiyama T, Martinez JJ. Rickettsial outer-membrane protein B (rOmpB) mediates bacterial invasion through Ku70 in an actin, c-Cbl, clathrin and caveolin 2-dependent manner. Cell Microbiol 11: 629-644, 2009.
5. Das K, Lewis RY, Scherer PE, Lisanti MP. The membrane-spanning domains of caveolins-1 and -2 mediate the formation of caveolin heterooligomers. Implications for the assembly of caveolae membranes in vivo. J Biol Chem 274: 18721-18728, 1999.
6. Del Galdo F, Lisanti MP, Jimenez SA. Caveolin-1, transforming growth factor-β receptor internalization, and the pathogenesis of systemic sclerosis. Curr Opin Rheumatol 20: 713-719, 2008.
7. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293: 2449-2452., 2001.
8. Fujimoto T, Kogo H, Nomura R, Une T. Isoforms of caveolin-1 and caveolar structure. J Cell Sci 113: 3509-3517, 2000.
9. Goumans MJ, Lebrin F, Valdimarsdottir G. Controlling the angiogenic switch: a balance between two distinct TGF-β receptor signaling pathways. Trends Cardiovasc Med 13: 301-307, 2003.
10. Goumans MJ, Valdimarsdottir G, Itoh S, Lebrin F, Larsson J, Mummery C, Karlsson S, ten Dijke P. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFβ/ALK5 signaling. Mol Cell 12: 817-828, 2003.
11. Goumans MJ, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-β type I receptors. EMBO J 21: 1743-1753, 2002.
12. Hannan RL, Kourembanas S, Flanders KC, Rogelj SJ, Roberts AB, Faller DV, Klagsbrun M. Endothelial cells synthesize basic fibroblast growth factor and transforming growth factor β. Growth Factors 1: 7-17, 1988.
13. Harrison CA, Gray PC, Vale WW, Robertson DM. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol Metab 16: 73-78, 2005.
14. Hirai R, Kaji K. Transforming growth factor β 1-specific binding proteins on human vascular endothelial cells. Exp Cell Res 201: 119-125, 1992.
15. Igarashi J, Shoji K, Hashimoto T, Moriue T, Yoneda K, Takamura T, Yamashita T, Kubota Y, Kosaka H. Transforming growth factor-β1 downregulates caveolin-1 expression and enhances sphingosine 1-phosphate signaling in cultured vascular endothelial cells. Am J Physiol Cell Physiol 297: C1263-C1274, 2009.
16. Itoh S, Itoh F, Goumans MJ, Ten Dijke P. Signaling of transforming growth factor-β family members through Smad proteins. Eur J Biochem 267: 6954-6967, 2000.
17. Kang JS, Liu C, Derynck R. New regulatory mechanisms of TGF-β receptor function. Trends Cell Biol 19: 385-394, 2009.
18. Kim S, Lee Y, Seo JE, Cho KH, Chung JH. Caveolin-1 increases basal and TGF-β1-induced expression of type I procollagen through PI-3 kinase/Akt/mTOR pathway in human dermal fibroblasts. Cell Signal 20: 1313-1319, 2008.
19. Kim S, Pak Y. Caveolin-2 regulation of the cell cycle in response to insulin in Hirc-B fibroblast cells. Biochem Biophys Res Commun 330: 88-96, 2005.
20. Krajewska WM, Maslowska I. Caveolins: structure and function in signal transduction. Cell Mol Biol Lett 9: 195-220, 2004.
21. Kwon H, Jeong K, Hwang EM, Park JY, Hong SG, Choi WS, Pak Y. Caveolin-2 regulation of STAT3 transcriptional activation in response to insulin. Biochim Biophys Acta 1793: 1325-1333, 2009.
22. Kwon H, Jeong K, Pak Y. Identification of pY19-Caveolin-2 as a positive regulator of insulin-stimulated actin cytoskeleton-dependent mitogenesis. J Cell Mol Med, 2008.
23. Lahtinen U, Honsho M, Parton RG, Simons K, Verkade P. Involvement of caveolin-2 in caveolar biogenesis in MDCK cells. FEBS Lett 538: 85-88, 2003.
24. Lee EK, Lee YS, Han IO, Park SH. Expression of Caveolin-1 reduces cellular responses to TGF-β1 through down-regulating the expression of TGF-β type II receptor gene in NIH3T3 fibroblast cells. Biochem Biophys Res Commun 359: 385-390, 2007.
25. Lee H, Park DS, Wang XB, Scherer PE, Schwartz PE, Lisanti MP. Src-induced phosphorylation of caveolin-2 on tyrosine 19. Phosphocaveolin-2 (Tyr(P)19) is localized near focal adhesions, remains associated with lipid rafts/caveolae, but no longer forms a high molecular mass hetero-oligomer with caveolin-1. J Biol Chem 277: 34556-34567, 2002.
26. Massague J, Wotton D. Transcriptional control by the TGF-β/Smad signaling system. EMBO J 19: 1745-1754, 2000.
27. Mora R, Bonilha VL, Marmorstein A, Scherer PE, Brown D, Lisanti MP, Rodriguez-Boulan E. Caveolin-2 localizes to the golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J Biol Chem 274: 25708-25717, 1999.
28. Moustakas A, Souchelnytskyi S, Heldin CH. Smad regulation in TGF-β signal transduction. J Cell Sci 114: 4359-4369, 2001.
29. Myoken Y, Kan M, Sato GH, McKeehan WL, Sato JD. Bifunctional effects of transforming growth factor-β (TGF-β) on endothelial cell growth correlate with phenotypes of TGF-β binding sites. Exp Cell Res 191: 299-304, 1990.
30. Neganova I, Lako M. G1 to S phase cell cycle transition in somatic and embryonic stem cells. J Anat 213: 30-44, 2008.
31. OConnor PM. Mammalian G1 and G2 phase checkpoints. Cancer Surv 29: 151-182, 1997.
32. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, Li E. Activin receptor-like kinase 1 modulates transforming growth factor-β 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 97: 2626-2631, 2000.
33. Ota T, Fujii M, Sugizaki T, Ishii M, Miyazawa K, Aburatani H, Miyazono K. Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-β in human umbilical vein endothelial cells. J Cell Physiol 193: 299-318, 2002.
34. Parat MO. The biology of caveolae: achievements and perspectives. Int Rev Cell Mol Biol 273: 117-162, 2009.
35. Parker S, Walker DS, Ly S, Baylis HA. Caveolin-2 is required for apical lipid trafficking and suppresses basolateral recycling defects in the intestine of Caenorhabditis elegans. Mol Biol Cell 20: 1763-1771, 2009.
36. Parolini I, Sargiacomo M, Galbiati F, Rizzo G, Grignani F, Engelman JA, Okamoto T, Ikezu T, Scherer PE, Mora R, Rodriguez-Boulan E, Peschle C, Lisanti MP. Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane. Retention of caveolin-2 at the level of the golgi complex. J Biol Chem 274: 25718-25725, 1999.
37. Pece-Barbara N, Vera S, Kathirkamathamby K, Liebner S, Di Guglielmo GM, Dejana E, Wrana JL, Letarte M. Endoglin null endothelial cells proliferate faster and are more responsive to transforming growth factor β1 with higher affinity receptors and an activated Alk1 pathway. J Biol Chem 280: 27800-27808, 2005.
38. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138, 2001.
39. Razani B, Wang XB, Engelman JA, Battista M, Lagaud G, Zhang XL, Kneitz B, Hou H Jr, Christ GJ, Edelmann W, Lisanti MP. Caveolin- 2-deficient mice show evidence of severe pulmonary dysfunction without disruption of caveolae. Mol Cell Biol 22: 2329-2344, 2002.
40. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, Lisanti MP. Caveolin-1 regulates transforming growth factor (TGF)- β/SMAD signaling through an interaction with the TGF-β type I receptor. J Biol Chem 276: 6727-6738, 2001.
41. Santibanez JF, Blanco FJ, Garrido-Martin EM, Sanz-Rodriguez F, del Pozo MA, Bernabeu C. Caveolin-1 interacts and cooperates with the transforming growth factor-β type I receptor ALK1 in endothelial caveolae. Cardiovasc Res 77: 791-799, 2008.
42. Schubert W, Sotgia F, Cohen AW, Capozza F, Bonuccelli G, Bruno C, Minetti C, Bonilla E, Dimauro S, Lisanti MP. Caveolin-1(-/-)- and caveolin-2(-/-)-deficient mice both display numerous skeletal muscle ab-normalities, with tubular aggregate formation. Am J Pathol 170: 316-333, 2007.
43. Sherr CJ, Roberts JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512, 1999.
44. Sherr CJ, Roberts JM. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9: 1149-1163, 1995.
45. Shmuel M, Nodel-Berner E, Hyman T, Rouvinski A, Altschuler Y. Caveolin 2 regulates endocytosis and trafficking of the M1 muscarinic receptor in MDCK epithelial cells. Mol Biol Cell 18: 1570-1585, 2007.
46. Sowa G, Pypaert M, Fulton D, Sessa WC. The phosphorylation of caveolin-2 on serines 23 and 36 modulates caveolin-1-dependent caveolae formation. Proc Natl Acad Sci USA 100: 6511-6516, 2003.
47. Sowa G, Xie L, Xu L, Sessa WC. Serine 23 and 36 phosphorylation of caveolin-2 is differentially regulated by targeting to lipid raft/caveolae and in mitotic endothelial cells. Biochemistry 47: 101-111, 2008.
48. ten Dijke P, Hill CS. New insights into TGF-β-Smad signalling. Trends Biochem Sci 29: 265-273, 2004.
49. Toyoshima H, Hunter T. P27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 78: 67-74, 1994.
50. Trimarchi JM, Lees JA. Sibling rivalry in the E2F family. Nat Rev Mol Cell Biol 3: 11-20, 2002.
51. Wang XB, Lee H, Capozza F, Marmon S, Sotgia F, Brooks JW, Campos-Gonzalez R, Lisanti MP. Tyrosine phosphorylation of caveolin-2 at residue 27: differences in the spatial and temporal behavior of phospho-Cav-2 (pY19 and pY27). Biochemistry 43: 13694-13706, 2004.
52. Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F, Ifedigbo E, Xu X, Oury TD, Kaminski N, Choi AM. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 203: 2895-2906, 2006.
53. Williams TM, Lisanti MP. The Caveolin genes: from cell biology to medicine. Ann Med 36: 584-595, 2004.
54. Wu X, Ma J, Han JD, Wang N, Chen YG. Distinct regulation of gene expression in human endothelial cells by TGF-β and its receptors. Microvasc Res 71: 12-19, 2006.
55. Xie L, Frank PG, Lisanti MP, Sowa G. Endothelial cells isolated from caveolin-2 knockout mice display higher proliferation rate and cell cycle progression relative to their wild-type counterparts. Am J Physiol Cell Physiol 298: C693-C701, 2010.
56. Zaas DW, Duncan MJ, Li G, Wright JR, Abraham SN. Pseudomonas invasion of type I pneumocytes is dependent on the expression and phosphorylation of caveolin-2. J Biol Chem 280: 4864-4872, 2005.
57. Zaas DW, Swan ZD, Brown BJ, Li G, Randell SH, Degan S, Sunday ME, Wright JR, Abraham SN. Counteracting signaling activities in lipid rafts associated with the invasion of lung epithelial cells by Pseudomonas aeruginosa. J Biol Chem 284: 9955-9964, 2009.