Altered localization of h-ras in caveolin-1-null cells is palmitoylation-independent

Journal of Cell Communication and Signaling

Volumn 1, Issue 3-4, 2007, Pages 195-204

  Baran, Joanne ^a   Mundy, Dorothy I ^b   Vasanji, Amit ^a   Parat, Marie Odile ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Palmitate; Post translational modification

Indexed keywords

MUS;

EID: 59649083930     PISSN: 18739601     EISSN: 1873961X     Source Type: Journal    
DOI: 10.1007/s12079-008-0017-3     Document Type: Article

References (46)

1. Anderson RG, Kamen BA, Rothberg KG, Lacey SW (1992) Potocytosis: sequestration and transport of small molecules by caveolae. Science 255:410–411
2. Apolloni A, Prior IA, Lindsay M, Parton RG, Hancock JF (2000) H-ras but not K-ras traffics to the plasma membrane through the exocytic pathway. Mol Cell Biol 20:2475–2487
3. Bivona TG, Philips MR (2003) Ras pathway signaling on endomem-branes. Curr Opin Cell Biol 15:136–142
4. Camp LA, Hofmann SL (1993) Purification and properties of a palmitoyl-protein thioesterase that cleaves palmitate from H-Ras. J Biol Chem 268:22566–22574
5. Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL, Cox AD, Philips MR (2002) Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol 4:343–350
6. Choy E, Chiu VK, Silletti J, Feoktistov M, Morimoto T, Michaelson D, Ivanov IE, Philips MR (1999) Endomembrane trafficking of ras: the CAAX motif targets proteins to the ER and Golgi. Cell 98:69–80
7. Das AK, Dasgupta B, Bhattacharya R, Basu J (1997) Purification and biochemical characterization of a protein-palmitoyl acyltransferase from human erythrocytes. J Biol Chem 272:11021–11025
8. del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande-Garcia A, Anderson RG, Schwartz MA (2005) Phospho-caveolin-1 mediates integrin-regulated membrane domain inter-nalization. Nat Cell Biol 7:901–908
9. Dietzen DJ, Hastings WR, Lublin DM (1995) Caveolin is palmitoylated on multiple cysteine residues. Palmitoylation is not necessary for localization of caveolin to caveolae. J Biol Chem 270:6838–6842
10. Drab M et al (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293:2449–2452
11. Duncan JA, Gilman AG (1998) A cytoplasmic acyl-protein thioesterase that removes palmitate from G protein alpha subunits and p21 (RAS). J Biol Chem 273:15830–15837
12. Dunphy JT, Greentree WK, Manahan CL, Linder ME (1996) G-protein palmitoyltransferase activity is enriched in plasma membranes. J Biol Chem 271:7154–7159
13. Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, Lisanti MP (1997) Recombinant expression of caveolin-1 in oncogeni-cally transformed cells abrogates anchorage-independent growth. J Biol Chem 272:16374–16381
14. Engelman JA, Zhang XL, Razani B, Pestell RG, Lisanti MP (1999) p42/44 MAP Kinase-dependent and -independent Signaling Pathways Regulate Caveolin-1 Gene Expression. Activation of ras-map kinase and protein kinase a signaling cascades transcrip-tionally down-regulates caveolin-1 promoter activity. J Biol Chem 274:32333–32341
15. Fra AM, Williamson E, Simons K, Parton RG (1995) De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci U S A 92:8655–8659
16. Galbiati F, Volonte D, Meani D, Milligan G, Lublin DM, Lisanti MP, Parenti M (1999) The dually acylated NH2-terminal domain of Gi1alpha is sufficient to target a green fluorescent protein reporter to caveolin-enriched plasma membrane domains. Palmitoylation of caveolin-1 is required for the recognition of dually acylated g-protein alpha subunits in vivo. J Biol Chem 274:5843–5850
17. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC (1997) Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 272:25437–25440
18. Hancock JF (2003) Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4:373–384
19. Hancock JF, Paterson H, Marshall CJ (1990) A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane. Cell 63:133–139
20. Koleske AJ, Baltimore D, Lisanti MP (1995) Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci U S A 92:1381–1385
21. Lee H, Woodman SE, Engelman JA, Volonte D, Galbiati F, Kaufman HL, Lublin DM, Lisanti MP (2001) Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase. Targeting of dually acylated molecules (GPI-linked, trans-membrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (Tyr-14). J Biol Chem 276:35150–35158
22. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE, Hansen SH, Nishimoto I, Lisanti MP (1995) Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem 270:15693–15701
23. Li S, Couet J, Lisanti MP (1996) Src tyrosine kinases, Galpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 271:29182–29190
24. Lobo S, Greentree WK, Linder ME, Deschenes RJ (2002) Identification of a Ras palmitoyltransferase in Saccharomyces cerevisiae. J Biol Chem 277:41268–41273
25. Matallanas D, Sanz-Moreno V, Arozarena I, Calvo F, gudo-Ibanez L, Santos E, Berciano MT, Crespo P (2006) Distinct utilization of effectors and biological outcomes resulting from site-specific Ras activation: Ras functions in lipid rafts and Golgi complex are dispensable for proliferation and transformation. Mol Cell Biol 26:100–116
26. Michaelson D, Ahearn I, Bergo M, Young S, Philips M (2002) Membrane trafficking of heterotrimeric G proteins via the endoplasmic reticulum and Golgi. Mol Biol Cell 13:3294–3302
27. Mineo C, Anderson RG (2001) Potocytosis. Histochem Cell Biol 116:109–118
28. Mineo C, James GL, Smart EJ, Anderson RG (1996) Localization of epidermal growth factor-stimulated Ras/Raf-1 interaction to caveolae membrane. J Biol Chem 271:11930–11935
29. Monier S, Dietzen DJ, Hastings WR, Lublin DM, Kurzchalia TV (1996) Oligomerization of VIP21-caveolin in vitro is stabilized by long chain fatty acylation or cholesterol. FEBS Lett 388:143–149
30. Parat MO, Fox PL (2001) Palmitoylation of caveolin-1 in endothelial cells is post-translational but irreversible. J Biol Chem 276:15776–15782
31. Paz A, Haklai R, Elad-Sfadia G, Ballan E, Kloog Y (2001) Galectin-1 binds oncogenic H-Ras to mediate Ras membrane anchorage and cell transformation. Oncogene 20:7486–7493
32. Prior IA, Harding A, Yan J, Sluimer J, Parton RG, Hancock JF (2001) GTP-dependent segregation of H-ras from lipid rafts is required for biological activity. Nat Cell Biol 3:368–375
33. Quatela SE, Philips MR (2006) Ras signaling on the Golgi. Curr Opin Cell Biol 18:162–167
34. Razani B et al (2001) Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276:38121–38138
35. Resh MD (2006) Palmitoylation of ligands, receptors, and intracellular signaling molecules. Sci STKE 2006: re14
36. Roy S, Luetterforst R, Harding A, Apolloni A, Etheridge M, Stang E, Rolls B, Hancock JF, Parton RG (1999) Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat Cell Biol 1:98–105
37. Schlegel A, Pestell RG, Lisanti MP (2000) Caveolins in cholesterol trafficking and signal transduction: implications for human disease. Front Biosci 5:929–937
38. Smotrys JE, Linder ME (2004) Palmitoylation of intracellular signaling proteins: regulation and function. Annu Rev Biochem 73:559–587
39. Song SK, Li Shengwen, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP (1996) Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae micro-domains. Detergent-free purification of caveolae microdomains. J Biol Chem 271:9690–9697
40. Sotgia F et al (2002) Intracellular retention of glycosylphosphatidyl inositol-linked proteins in caveolin-deficient cells. Mol Cell Biol 22:3905–3926
41. Swarthout JT, Lobo S, Farh L, Croke MR, Greentree WK, Deschenes RJ, Linder ME (2005) DHHC9 and GCP16 constitute a human protein fatty acyltransferase with specificity for H- and N-Ras. J Biol Chem 280:31141–31148
42. Uittenbogaard A, Smart EJ (2000) Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J Biol Chem 275:25595–25599
43. White MA, Anderson RG (2005) Signaling networks in living cells. Annu Rev Pharmacol Toxicol 45:587–603
44. Yeh DC, Duncan JA, Yamashita S, Michel T (1999) Depalmitoylation of endothelial nitric-oxide synthase by acyl-protein thioesterase 1 Is potentiated by Ca (2+)-calmodulin. J Biol Chem 274:33148–33154
45. Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, Lin MI, Drab M, Kurzchalia TV, Stan RV, Sessa WC (2006) Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Invest 116:1284–1291
46. Zheng H, McKay J, Buss JE (2007) H-Ras does not need COP-I or COP-II-dependent vesicular transport to reach the plasma membrane. J Biol Chem 282:25760–25768