MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes

Journal of Cell Biology

Volumn 185, Issue 7, 2009, Pages 1259-1273

  Bastiani, Michele ^a   Liu, Libin ^c   Hill, Michelle M ^a   Jedrychowski, Mark P ^c   Nixon, Susan J ^a   Lo, Harriet P ^a   Abankwa, Daniel ^a   Luetterforst, Robert ^a   Fernandez Rojo, Manuel ^a   Breen, Michael R ^c   Gygi, Steven P ^d   Vinten, Jorgen ^e   Walser, Piers J ^a   North, Kathryn N ^b   Hancock, John F ^a   Pilch, Paul F ^c   Parton, Robert G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b CHILDREN S HOSPITAL AT WESTMEAD   (Australia)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN; CAVIN 1; CAVIN 2; CAVIN 3; CAVIN 4; CYTOPLASM PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; CAVEOLA; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; MUSCLE DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

3T3-L1 CELLS; AMINO ACID SEQUENCE; ANIMALS; CAVEOLAE; CAVEOLINS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; MUSCLE PROTEINS; MUSCULAR DISEASES; PHYLOGENY; PROTEIN ISOFORMS; RECOMBINANT FUSION PROTEINS; SARCOLEMMA; SEQUENCE ALIGNMENT;

EID: 67649583182     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200903053     Document Type: Article

References (57)

1. Aboulaich, N., J.P. Vainonen, P. Stralfors, and A.V. Vener. 2004. Vectorial proteomics reveal targeting, phosphorylation and specific fragmentation of polymerase I and transcript release factor (PTRF) at the surface of caveolae in human adipocytes. Biochem. J. 383:237-248. (Pubitemid 39446684)
2. Birnbaum, M.J. 1989. Identification of a novel gene encoding an insulin-responsive glucose transporter protein. Cell. 57:305-315. (Pubitemid 19112369)
3. Burgener, R., M. Wolf, T. Ganz, and M. Baggiolini. 1990. Purification and characterization of a major phosphatidylserine-binding phosphoprotein from human platelets. Biochem. J. 269:729-734. (Pubitemid 20236084)
4. Capozza, F., T.P. Combs, A.W. Cohen, Y.R. Cho, S.Y. Park, W. Schubert, T.M. Williams, D.L. Brasaemle, L.A. Jelicks, P.E. Scherer, et al. 2005. Caveolin-3 knockout mice show increased adiposity and whole body insulin resistance, with ligand-induced insulin receptor instability in skeletal muscle. Am. J. Physiol. Cell Physiol. 288:C1317-C1331. (Pubitemid 40991069)
5. Carlton, J.G., and P.J. Cullen. 2005. Coincidence detection in phosphoinositide signaling. Trends Cell Biol. 15:540-547. (Pubitemid 41398187)
6. Carninci, P., T. Kasukawa, S. Katayama, J. Gough, M.C. Frith, N. Maeda, R. Oyama, T. Ravasi, B. Lenhard, C. Wells, et al. 2005. The transcriptional landscape of the mammalian genome. Science. 309:1559-1563.
7. Carozzi, A.J., E. Ikonen, M.R. Lindsay, and R.G. Parton. 2000. Role of cholesterol in developing T-tubules: analogous mechanisms for T-tubule and caveolae biogenesis. Traffic. 1:326-341.
8. Cheng, Z.J., R.D. Singh, D.L. Marks, and R.E. Pagano. 2006. Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids. Mol. Membr. Biol. 23:101-110.
9. Cohen, A.W., B. Razani, W. Schubert, T.M. Williams, X.B. Wang, P. Iyengar, D.L. Brasaemle, P.E. Scherer, and M.P. Lisanti. 2004. Role of caveolin-1 in the modulation of lipolysis and lipid droplet formation. Diabetes. 53:1261-1270. (Pubitemid 38569012)
10. Drab, M., P. Verkade, M. Elger, M. Kasper, M. Lohn, B. Lauterbach, J. Menne, C. Lindschau, F. Mende, F.C. Luft, et al. 2001. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science. 293:2449-2452. (Pubitemid 32917325)
11. Fernandez, M.A., C. Albor, M. Ingelmo-Torres, S.J. Nixon, C. Ferguson, T. Kurzchalia, F. Tebar, C. Enrich, R.G. Parton, and A. Pol. 2006. Caveolin-1 is essential for liver regeneration. Science. 313:1628-1632. (Pubitemid 44414035)
12. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1995. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc. Natl. Acad. Sci. USA. 92:8655-8659.
13. Garg, A., and A.K. Agarwal. 2008. Caveolin-1: a new locus for human lipodystrophy. J. Clin. Endocrinol. Metab. 93:1183-1185.
14. Green, H., and O. Kehinde. 1976. Spontaneous heritable changes leading to increased adipose conversion in 3T3 cells. Cell. 7:105-113.
15. Gustincich, S., and C. Schneider. 1993. Serum deprivation response gene is induced by serum starvation but not by contact inhibition. Cell Growth Differ. 4:753-760.
16. Gustincich, S., P. Vatta, S. Goruppi, M. Wolf, S. Saccone, G. Della Valle, M. Baggiolini, and C. Schneider. 1999. The human serum deprivation response gene (SDPR) maps to 2q32-q33 and codes for a phosphatidylserine-binding protein. Genomics. 57:120-129. (Pubitemid 29187944)
17. Hernandez-Deviez, D.J., S. Martin, S.H. Laval, H.P. Lo, S.T. Cooper, K.N. North, K. Bushby, and R.G. Parton. 2006. Aberrant dysferlin trafficking in cells lacking caveolin or expressing dystrophy mutants of caveolin-3. Hum. Mol. Genet. 15:129-142. (Pubitemid 43020111)
18. Hill, M.M., M. Bastiani, R. Luetterforst, M. Kirkham, A. Kirkham, S.J. Nixon, P. Walser, D. Abankwa, V.M. Oorschot, S. Martin, et al. 2008. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell. 132:113-124.
19. Honing, S., D. Ricotta, M. Krauss, K. Spate, B. Spolaore, A. Motley, M. Robinson, C. Robinson, V. Haucke, and D.J. Owen. 2005. Phosphatidylinositol-(4, 5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol. Cell. 18:519-531. (Pubitemid 40726229)
20. Izumi, Y., S. Hirai, Y. Tamai, A. Fujise-Matsuoka, Y. Nishimura, and S. Ohno. 1997. A protein kinase Cdelta-binding protein SRBC whose expression is induced by serum starvation. J. Biol. Chem. 272:7381-7389. (Pubitemid 27166449)
21. James, D.E., R. Brown, J. Navarro, and P.F. Pilch. 1988. Insulin-regulatable tissues express a unique insulin-sensitive glucose transport protein. Nature. 333:183-185. (Pubitemid 18124905)
22. Jansa, P., S.W. Mason, U. Hoffmann-Rohrer, and I. Grummt. 1998. Cloning and functional characterization of PTRF, a novel protein which induces dissociation of paused ternary transcription complexes. EMBO J. 17:2855-2864. (Pubitemid 28227132)
23. Jansa, P., C. Burek, E.E. Sander, and I. Grummt. 2001. The transcript release factor PTRF augments ribosomal gene transcription by facilitating reinitiation of RNA polymerase I. Nucleic Acids Res. 29:423-429. (Pubitemid 32060929)
24. Kandror, K.V., J.M. Stephens, and P.F. Pilch. 1995. Expression and compartmentalization of caveolin in adipose cells: coordinate regulation with and structural segregation from GLUT4. J. Cell Biol. 129:999-1006.
25. Kim, C.A., M. Delepine, E. Boutet, H. El Mourabit, S. Le Lay, M. Meier, M. Nemani, E. Bridel, C.C. Leite, D.R. Bertola, et al. 2008. Association of a homozygous nonsense caveolin-1 mutation with Berardinelli-Seip congenital lipodystrophy. J. Clin. Endocrinol. Metab. 93:1129-1134. (Pubitemid 351540679)
26. Kirkham, M., S.J. Nixon, M.T. Howes, L. Abi-Rached, D.E. Wakeham, M. Hanzal-Bayer, C. Ferguson, M.M. Hill, M. Fernandez-Rojo, D.A. Brown, et al. 2008. Evolutionary analysis and molecular dissection of caveola biogenesis. J. Cell Sci. 121:2075-2086. (Pubitemid 352015205)
27. Le Lay, S., E. Hajduch, M.R. Lindsay, X. Le Liepvre, C. Thiele, P. Ferre, R.G. Parton, T. Kurzchalia, K. Simons, and I. Dugail. 2006. Cholesterol-induced caveolin targeting to lipid droplets in adipocytes: a role for caveolar endocytosis. Traffic. 7:549-561. (Pubitemid 44026753)
28. Lee, S.W., C.L. Reimer, P. Oh, D.B. Campbell, and J.E. Schnitzer. 1998. Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene. 16:1391-1397. (Pubitemid 28151846)
29. Liu, L., and P.F. Pilch. 2008. A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J. Biol. Chem. 283:4314-4322.
30. Liu, L., D. Brown, M. McKee, N.K. Lebrasseur, D. Yang, K.H. Albrecht, K. Ravid, and P.F. Pilch. 2008. Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab. 8:310-317.
31. Mason, S.W., E.E. Sander, and I. Grummt. 1997. Identification of a transcript release activity acting on ternary transcription complexes containing murine RNA polymerase I. EMBO J. 16:163-172. (Pubitemid 27032859)
32. Mineo, C., G.L. James, E.J. Smart, and R.G. Anderson. 1996. Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J. Biol. Chem. 271:11930-11935. (Pubitemid 26157268)
33. Mineo, C., Y.S. Ying, C. Chapline, S. Jaken, and R.G. Anderson. 1998. Targeting of protein kinase Cα to caveolae. J. Cell Biol. 141:601-610. (Pubitemid 28217907)
34. Monier, S., D.J. Dietzen, W.R. Hastings, D.M. Lublin, and T.V. Kurzchalia. 1996. Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett. 388:143-149. (Pubitemid 26226349)
35. Ogata, T., T. Ueyama, K. Isodono, M. Tagawa, N. Takehara, T. Kawashima, K. Harada, T. Takahashi, T. Shioi, H. Matsubara, and H. Oh. 2008. MURC, a muscle-restricted coiled-coil protein that modulates the Rho/ROCK pathway, induces cardiac dysfunction and conduction disturbance. Mol. Cell. Biol. 28:3424-3436.
36. Parton, R.G., and K. Simons. 2007. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 8:185-194. (Pubitemid 46310548)
37. Parton, R.G., M. Way, N. Zorzi, and E. Stang. 1997. Caveolin-3 associates with developing T-tubules during muscle differentiation. J. Cell Biol. 136:137-154. (Pubitemid 27044810)
38. Pelkmans, L., and M. Zerial. 2005. Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature. 436:128-133. (Pubitemid 40966198)
39. Pelkmans, L., T. Burli, M. Zerial, and A. Helenius. 2004. Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell. 118:767-780. (Pubitemid 39221735)
40. Pilch, P.F., R.P. Souto, L. Liu, M.P. Jedrychowski, E.A. Berg, C.E. Costello, and S.P. Gygi. 2007. Cellular spelunking: exploring adipocyte caveolae. J. Lipid Res. 48:2103-2111. (Pubitemid 47529553)
41. Pol, A., S. Martin, M.A. Fernandez, M. Ingelmo-Torres, C. Ferguson, C. Enrich, and R.G. Parton. 2005. Cholesterol and fatty acids regulate dynamic caveolin trafficking through the Golgi complex and between the cell surface and lipid bodies. Mol. Biol. Cell. 16:2091-2105. (Pubitemid 40471974)
42. Razani, B., T.P. Combs, X.B. Wang, P.G. Frank, D.S. Park, R.G. Russell, M. Li, B. Tang, L.A. Jelicks, P.E. Scherer, and M.P. Lisanti. 2002. Caveolin-1- deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J. Biol. Chem. 277:8635-8647. (Pubitemid 34968330)
43. Scherer, P.E., M.P. Lisanti, G. Baldini, M. Sargiacomo, C.C. Mastick, and H.F. Lodish. 1994. Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J. Cell Biol. 127:1233-1243. (Pubitemid 24362559)
44. Souto, R.P., G. Vallega, J. Wharton, J. Vinten, J. Tranum-Jensen, and P.F. Pilch. 2003. Immunopurification and characterization of rat adipocyte caveolae suggest their dissociation from insulin signaling. J. Biol. Chem. 278:18321-18329. (Pubitemid 36799452)
45. Tagawa, A., A. Mezzacasa, A. Hayer, A. Longatti, L. Pelkmans, and A. Helenius. 2005. Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J. Cell Biol. 170:769-779. (Pubitemid 41242109)
46. Tagawa, M., T. Ueyama, T. Ogata, N. Takehara, N. Nakajima, K. Isodono, S. Asada, T. Takahashi, H. Matsubara, and H. Oh. 2008. MURC, a muscle-restricted coiled-coil protein, is involved in the regulation of skeletal myogenesis. Am. J. Physiol. Cell Physiol. 295:C490-C498.
47. Tahir, S.A., G. Yang, A.A. Goltsov, M. Watanabe, K. Tabata, J. Addai, M.A. Fattah el, D. Kadmon, and T.C. Thompson. 2008. Tumor cell-secreted caveolin-1 has proangiogenic activities in prostate cancer. Cancer Res. 68:731-739.
48. Thisse, B., and C. Thisse. 2004. Fast Release Clones: A High Throughput Expression Analysis. ZFIN Direct Data Submission. Available at: http://zfin.org (accessed August 25, 2008).
49. Vinten, J., M. Voldstedlund, H. Clausen, K. Christiansen, J. Carlsen, and J. Tranum-Jensen. 2001. A 60-kDa protein abundant in adipocyte caveolae. Cell Tissue Res. 305:99-106. (Pubitemid 32681872)
50. Vinten, J., A.H. Johnsen, P. Roepstorff, J. Harpoth, and J. Tranum-Jensen. 2005. Identification of a major protein on the cytosolic face of caveolae. Biochim. Biophys. Acta. 1717:34-40. (Pubitemid 41642663)
51. Voldstedlund, M., J. Vinten, and J. Tranum-Jensen. 2001. cav-p60 expression in rat muscle tissues. Distribution of caveolar proteins. Cell Tissue Res. 306:265-276. (Pubitemid 32972385)
52. Voldstedlund, M., L. Thuneberg, J. Tranum-Jensen, J. Vinten, and E.I. Christensen. 2003. Caveolae, caveolin and cav-p60 in smooth muscle and renin-producing cells in the rat kidney. Acta Physiol. Scand. 179:179-188. (Pubitemid 37249253)
53. Wanaski, S.P., B.K. Ng, and M. Glaser. 2003. Caveolin scaffolding region and the membrane binding region of SRC form lateral membrane domains. Biochemistry. 42:42-56. (Pubitemid 36083850)
54. Way, M., and R.G. Parton. 1995. M-caveolin, a muscle-specific caveolin-related protein. FEBS Lett. 376:108-112. (Pubitemid 126334510)
55. Woodman, S.E., F. Sotgia, F. Galbiati, C. Minetti, and M.P. Lisanti. 2004. Caveolinopathies: mutations in caveolin-3 cause four distinct autosomal dominant muscle diseases. Neurology. 62:538-543. (Pubitemid 38252792)
56. Xu, X.L., L.C. Wu, F. Du, A. Davis, M. Peyton, Y. Tomizawa, A. Maitra, G. Tomlinson, A.F. Gazdar, B.E. Weissman, et al. 2001. Inactivation of human SRBC, located within the 11p15.5-p15.4 tumor suppressor region, in breast and lung cancers. Cancer Res. 61:7943-7949. (Pubitemid 33049385)
57. Yao, Q., J. Chen, H. Cao, J.D. Orth, J.M. McCaffery, R.V. Stan, and M.A. McNiven. 2005. Caveolin-1 interacts directly with dynamin-2. J. Mol. Biol. 348:491-501. (Pubitemid 40462111)