Muscle-specific interaction of caveolin isoforms: Differential complex formation between caveolins in fibroblastic vs. muscle cells

American Journal of Physiology - Cell Physiology

Volumn 288, Issue 3 57-3, 2005, Pages

  Capozza, Franco ^a,b   Cohen, Alex W ^a,b   Cheung, Michelle W C ^a,b   Sotgia, Federica ^a,b   Schubert, William ^a,b   Battista, Michela ^a,b   Lee, Hyangkyu ^a,b   Frank, Philippe G ^a,b   Lisanti, Michael P ^a,b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b ALBERT EINSTEIN CANCER CENTER   (United States)

Author keywords

Caveolae; Caveolin 1; Caveolin 2; Caveolin 3

Indexed keywords

CAVEOLIN 1; CAVEOLIN 2; CAVEOLIN 3; ISOPROTEIN; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL TYPE; CONTROLLED STUDY; EPITHELIUM CELL; FIBROBLAST; GENETIC TRANSFECTION; HYPOPHYSIS CELL; IMMUNOPRECIPITATION; MOUSE; MUSCLE CELL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE; SMOOTH MUSCLE FIBER; TISSUE DISTRIBUTION;

ANIMALS; CAVEOLAE; CAVEOLINS; CELL LINE; DETERGENTS; FIBROBLASTS; MACROMOLECULAR SUBSTANCES; MICE; MICE, KNOCKOUT; MUSCLES; MYOBLASTS; OCTOXYNOL; PROTEIN ISOFORMS; RETROVIRIDAE;

EID: 13644265469     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00232.2004     Document Type: Article

References (54)

1. Bickel PE, Scherer PE, Schnitzer JE, Oh P, Lisanti MP, and Lodish HF. Flotillin and epidermal surface antigen define a new family of caveolae-associated integral membrane proteins. J Biol Chem 272: 13793-13802, 1997.
2. Das K, Lewis RY, Scherer PE, and Lisanti MP. The membrane-spanning domains of caveolins-1 and -2 mediate the formation of caveolin hetero-oligomers. Implications for the assembly of caveolae membranes in vivo. J Biol Chem 274: 18721-18728, 1999.
3. Dietzen DJ, Hastings WR, and Lublin DM. Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J Biol Chem 270: 6838-6842, 1995.
4. Fra AM, Masserini M, Palestini P, Sonnino S, and Simons K. A photo-reactive derivative of ganglioside GM1 specifically cross-links VIP21-caveolin on the cell surface. FEBS Lett 375: 11-14, 1995.
5. Fra AM, Williamson E, Simons K, and Parton RG. De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci USA 92: 8655-8659, 1995.
6. Frank PG, Marcel YL, Connelly MA, Lublin DM, Franklin V, Williams DL, and Lisanti MP. Stabilization of caveolin-1 by cellular cholesterol and scavenger receptor class B type I. Biochemistry 41: 11931-11940, 2002.
7. Galbiati F, Volonte D, Engelman JA, Scherer PE, and Lisanti MP. Targeted down-regulation of caveolin-3 is sufficient to inhibit myotube formation in differentiating C2C12 myoblasts. Transient activation of p38 mitogen-activated protein kinase is required for induction of caveolin-3 expression and subsequent myotube formation. J Biol Chem 274: 30315-30321, 1999.
8. Galbiati F, Volonte D, Engelman JA, Watanabe G, Burk R, Pestell RG, and Lisanti MP. Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 17: 6633-6648, 1998.
9. Galbiati F, Volonte D, Goltz JS, Steele Z, Sen J, Jurcsak J, Stein D, Stevens L, and Lisanti MP. Identification, sequence and developmental expression of invertebrate flotillins from Drosophila melanogaster. Gene 210: 229-237, 1998.
10. 1 arrest via a p53/p21(WAF1/Cip1)- dependent mechanism. Mol Biol Cell 12: 2229-2244, 2001.
11. Galbiati F, Volonte D, Minetti C, Chu JB, and Lisanti MP. Phenotypic behavior of caveolin-3 mutations that cause autosomal dominant limb girdle muscular dystrophy (LGMD-1C). Retention of LGMD-1C caveolin-3 mutants within the Golgi complex. J Biol Chem 274: 25632-25641, 1999.
12. Grignani F, Kinsella T, Mencarelli A, Valtieri M, Riganelli D, Lanfrancone L, Peschle C, Nolan GP, and Pelicci PG. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res 58: 14-19, 1998.
13. Hagiwara Y, Nishina Y, Yorifuji H, and Kikuchi T. Immunolocalization of caveolin-1 and caveolin-3 in monkey skeletal, cardiac and uterine smooth muscles. Cell Struct Funct 27: 375-382, 2002.
14. Kinsella TM and Nolan GP. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum Gene Ther 7: 1405-1413, 1996.
15. Koleske AJ, Baltimore D, and Lisanti MP. Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 92: 1381-1385, 1995.
16. Li S, Galbiati F, Volonte D, Sargiacomo M, Engelman JA, Das K, Scherer PE, and Lisanti MP. Mutational analysis of caveolin-induced vesicle formation. Expression of caveolin-1 recruits caveolin-2 to caveolae membranes. FEBS Lett 434: 127-134, 1998.
17. Li S, Song KS, Koh SS, Kikuchi A, and Lisanti MP. Baculovirus-based expression of mammalian caveolin in Sf21 insect cells. A model system for the biochemical and morphological study of caveolae biogenesis. J Biol Chem 271: 28647-28654, 1996.
18. Li S, Song KS, and Lisanti MP. Expression and characterization of recombinant caveolin. Purification by polyhistidine tagging and cholesterol-dependent incorporation into defined lipid membranes. J Biol Chem 271: 568-573, 1996.
19. Lisanti MP, Scherer PE, Vidugiriene J, Tang Z, Hermanowski-Vosatka A, Tu YH, Cook RF, and Sargiacomo M. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J Cell Biol 126: 111-126, 1994.
20. Monier S, Dietzen DJ, Hastings WR, Lublin DM, and Kurzchalia TV. Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett 388: 143-149, 1996.
21. Morgenstern JP and Land H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 18: 3587-3596, 1990.
22. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, and Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA 92: 10339-10343, 1995.
23. Nystrom FH, Chen H, Cong LN, Li Y, and Quon MJ. Caveolin-1 interacts with the insulin receptor and can differentially modulate insulin signaling in transfected Cos-7 cells and rat adipose cells. Mol Endocrinol 13: 2013-2024, 1999.
24. Palade GE and Bruns RR. Structural modification of plasmalemma vesicles. J Cell Biol 37: 633-649, 1968.
25. 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, and 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.
26. Parton RG, Way M, Zorzi N, and Stang E. Caveolin-3 associates with developing T-tubules during muscle differentiation. J Cell Biol 136: 137-154, 1997.
27. Razani B, Combs TP, Wang XB, Frank PG, Park DS, Russell MG, Li M, Tang B, Jelicks LA, Scherer PE, and Lisanti MP. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem 277: 8635-8647, 2002.
28. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell MG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, and Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138, 2001.
29. Razani B and Lisanti MP. Caveolin-deficient mice: insights into caveolar function and human disease. J Clin Invest 108: 1553-1561, 2001.
30. Razani B, Rubin CS, and Lisanti MP. Regulation of cAMP-mediated signal transduction via interaction of caveolins with the catalytic subunit of protein kinase A. J Biol Chem 274: 26353-26360, 1999.
31. Razani B, Zhang XL, Bitzer M, von Gersdorff G, Bottinger EP, and 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.
32. Rothberg KG, Heuser JE, Donzell WC, Ying Y, Glenney JR, and Anderson RGW. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682, 1992.
33. Rybin VO, Grabham PW, Elouardighi H, and Steinberg SF. Caveolae-associated proteins in cardiomyocytes: caveolin-2 expression and interactions with caveolin-3. Am J Physiol Heart Circ Physiol 285: H325-H332, 2003.
34. Sargiacomo M, Scherer PE, Tang Z, Kubler E, Song KS, Sanders MC, and Lisanti MP. Oligomeric structure of caveolin: implications for caveolae membrane organization. Proc Natl Acad Sci USA 92: 9407-9411, 1995.
35. Sargiacomo M, Sudol M, Tang Z, and Lisanti MP. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol 122: 789-807, 1993.
36. Scherer PE, Lewis RY, Volonte D, Engelman JA, Galbiati F, Couet J, Kohtz DS, van Donselaar E, Peters P, and Lisanti MP. Cell-type and tissue-specific expression of caveolin-2. Caveolins 1 and 2 co-localize and form a stable hetero-oligomeric complex in vivo. J Biol Chem 272: 29337-29346, 1997.
37. Scherer PE, Okamoto T, Chun M, Nishimoto I, Lodish HF, and Lisanti MP. Identification, sequence, and expression of caveolin-2 defines a caveolin gene family. Proc Natl Acad Sci USA 93: 131-135, 1996.
38. Scherer PE, Tang Z, Chun M, Sargiacomo M, Lodish HF, and Lisanti MP. Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution. Identification and epitope mapping of an isoform-specific monoclonal antibody probe. J Biol Chem 270: 16395-16401, 1995.
39. Schlegel A and Lisanti MP. A molecular dissection of caveolin-1 membrane attachment and oligomerization. Two separate regions of the caveolin-1 C-terminal domain mediate membrane binding and oligomer/oligomer interactions in vivo. J Biol Chem 275: 21605-21617, 2000.
40. Schlegel A, Schwab RB, Scherer PE, and Lisanti MP. A role for the caveolin scaffolding domain in mediating the membrane attachment of caveolin-1. The caveolin scaffolding domain is both necessary and sufficient for membrane binding in vitro. J Biol Chem 274: 22660-22667, 1999.
41. Schlegel A, Wang C, Pestell RG, and Lisanti MP. Ligand-independent activation of oestrogen receptor alpha by caveolin-1. Biochem J 359: 203-210, 2001.
42. Schnitzer JE, Oh P, Pinney E, and Allard J. Filipin-sensitive caveolae-mediated transport in endothelium: reduced transcytosis, scavenger endocytosis, and capillary permeability of select macromolecules. J Cell Biol 127: 1217-1232, 1994.
43. Segal SS, Brett SE, and Sessa WC. Codistribution of NOS and caveolin throughout peripheral vasculature and skeletal muscle of hamsters. Am J Physiol Heart Circ Physiol 277: H1167-H1177, 1999.
44. Simons K and Ikonen E. How cells handle cholesterol. Science 290: 1721-1726, 2000.
45. Smart EJ, Graf GA, McNiven MA, Sessa WC, Engelman JA, Scherer PE, Okamoto T, and Lisanti MP. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol 19: 7289-7304, 1999.
46. Smart EJ, Ying Y, Donzell WC, and Anderson RG. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J Biol Chem 271: 29427-29435, 1996.
47. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, and Lisanti MP. Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem 271: 15160-15165, 1996.
48. Song KS, Tang Z, Li S, and Lisanti MP. Mutational analysis of the properties of caveolin-1. A novel role for the C-terminal domain in mediating homotypic caveolin-caveolin interactions. J Biol Chem 272: 4398-4403, 1997.
49. Sotgia F, Razani B, Bonuccelli G, Schubert W, Battista M, Lee H, Capozza F, Schubert AL, Minetti C, Buckley JT, and Lisanti MP. Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol Cell Biol 22: 3905-3926, 2002.
50. Tang Z, Scherer PE, Okamoto T, Song K, Chu C, Kohtz DS, Nishimoto I, Lodish HF, and Lisanti MP. Molecular cloning of caveolin-3, a novel member of the caveolin gene family expressed predominantly in muscle. J Biol Chem 271: 2255-2261, 1996.
51. Toya Y, Schwencke C, Couet J, Lisanti MP, and Ishikawa Y. Inhibition of adenylyl cyclase by caveolin peptides. Endocrinology 139: 2025-2031, 1998.
52. Volonte D, Galbiati F, Li S, Nishiyama K, Okamoto T, and Lisanti MP. Flotillins/cavatellins are differentially expressed in cells and tissues and form a hetero-oligomeric complex with caveolins in vivo. Characterization and epitope-mapping of a novel flotillin-1 monoclonal antibody probe. J Biol Chem 274: 12702-12709, 1999.
53. Woodman SE, Cheung MW, Tarr M, North AC, Schubert W, Lagaud G, Marks CB, Russell RG, Hassan GS, Factor SM, Christ GJ, and Lisanti MP. Urogenital alterations in aged male caveolin-1 knockout mice. J Urol 171: 950-957, 2004.
54. Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol 1: 445-458, 1955.