A novel domain of caveolin-2 that controls nuclear targeting: Regulation of insulin-specific ERK activation and nuclear translocation by caveolin-2

Journal of Cellular and Molecular Medicine

Volumn 15, Issue 4, 2011, Pages 888-908

  Kwon, Hayeong ^a   Jeong, Kyuho ^a   Hwang, Eun Mi ^a   Park, Jae Yong ^a   Pak, Yunbae ^a  

^a Gyeongsang National University   (South Korea)

Author keywords

Caveolin 2; IGF 1; Insulin; Lamin A C; Nuclear translocation; Phospho ERK

Indexed keywords

CAVEOLIN 2; INSULIN; INSULIN RECEPTOR; LAMIN; MITOGEN ACTIVATED PROTEIN KINASE; MUTANT PROTEIN; SIGNAL PEPTIDE; SOMATOMEDIN C;

ANIMAL; ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL STRAIN COS1; CELL STRAIN HEK293; CERCOPITHECUS; CHEMISTRY; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; GENE DELETION; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; RAT; STRUCTURE ACTIVITY RELATION;

ANIMALS; CAVEOLIN 2; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; COS CELLS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEK293 CELLS; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; LAMINS; MUTANT PROTEINS; NUCLEAR ENVELOPE; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RATS; RECEPTOR, INSULIN; SEQUENCE DELETION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79954995335     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2010.01079.x     Document Type: Article

References (57)

1. Fra AM, Williamson E, Simons K, et al De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. Proc Natl Acad Sci USA. 1995; 92: 8655-9.
2. Liu P, Rudick M, Anderson RG. Multiple functions of caveolin-1. J Biol Chem. 2002; 277: 41295-98.
3. Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev. 2002; 54: 431-67.
4. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol. 2007; 8: 185-94.
5. Head BP, Insel PA. Do caveolins regulate cells by actions outside of caveolae Trends Cell Biol. 2007; 17: 51-7.
6. Goetz JG, Lajoie P, Wiseman SM, et al Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev. 2008; 27: 715-35.
7. Lajoie P, Goetz JG, Dennis JW, et al Lattices, rafts, and scaffolds: domain regulation of receptor signaling at the plasma membrane. J Cell Biol. 2009; 185: 381-5.
8. Feng Y, Venema VJ, Venema RC, et al VEGF induces nuclear translocation of Flk-1/KDR, endothelial nitric oxide synthase, and caveolin-1 in vascular endothelial cells. Biochem Biophys Res Commun. 1999; 256: 192-7.
9. Gaus K, Le Lay S, Balasubramanian N, et al Integrin-mediated adhesion regulates membrane order. J Cell Biol. 2006; 174: 725-34.
10. Sanna E, Miotti S, Mazzi M, et al Binding of nuclear caveolin-1 to promoter elements of growth-associated genes in ovarian carcinoma cells. Exp Cell Res. 2007; 313: 1307-17.
11. Razani B, Wang XB, Engelman JA, et al Caveolin-2-deficient mice show evidence of severe pulmonary dysfunction without disruption of caveolae. Mol Cell Biol. 2002; 22: 2329-44.
12. Lahtinen U, Honsho M, Parton RG, et al Involvement of caveolin-2 in caveolar biogenesis in MDCK cells. FEBS Lett. 2003; 538: 85-8.
13. Kim S, Pak Y. Caveolin-2 regulation of the cell cycle in response to insulin in Hirc-B fibroblast cells. Biochem Biophys Res Commun. 2005; 330: 88-96.
14. 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. 2009; 13: 1549-64.
15. Kwon H, Jeong K, Hwang EM, et al Caveolin-2 regulation of STAT3 transcriptional activation in response to insulin. Biochim Biophys Acta. 2009; 1793: 1325-33.
16. Zehorai E, Yao Z, Plotnikov A, et al The subcellular localization of MEK and ERK-A novel nuclear translocation signal (NTS) paves a way to the nucleus. Mol Cell Endocrinol. 2010; 314: 213-20.
17. González JM, Navarro-Puche A, Casar B, et al Fast regulation of AP-1 activity through interaction of lamin A/C, ERK1/2, and c-Fos at the nuclear envelope. J Cell Biol. 2008; 183: 653-66.
18. Taniura H, Glass C, Gerace L. A chromatin binding site in the tail domain of nuclear lamins that interacts with core histones. J Cell Biol. 1995; 131: 33-44.
19. Mariappan I, Parnaik VK. Sequestration of pRb by cyclin D3 causes intranuclear reorganization of lamin A/C during muscle cell differentiation. Mol Biol Cell. 2005; 16: 1948-60.
20. Liu JP, Baker J, Perkins AS, et al Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell. 1993; 75: 59-72.
21. Jhun BH, Meinkoth JL, Leitner JW, et al Insulin and insulin-like growth factor-I signal transduction requires p21ras. J Biol Chem. 1994; 269: 5699-704.
22. LeRoith D, Werner H, Beitner-Johnson D, et al Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev. 1995; 16: 143-63.
23. Di Cola G, Cool MH, Accili D. Hypoglycemic effect of insulin-like growth factor-1 in mice lacking insulin receptors. J Clin Invest. 1997; 99: 2538-44.
24. El-Shewy HM, Lee MH, Obeid LM, et al The insulin-like growth factor type 1 and insulin-like growth factor type 2/mannose-6-phosphate receptors independently regulate ERK1/2 activity in HEK293 cells. J Biol Chem. 2007; 282: 26150-7.
25. Ullrich A, Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell. 1990; 61: 203-12.
26. Baserga R, Hongo A, Rubini M, et al The IGF-I receptor in cell growth, transformation and apoptosis. Biochim Biophys Acta. 1997; 1332: F105-26.
27. Dupont J, Fernandez AM, Glackin CA, et al Insulin-like growth factor 1 (IGF-1)-induced twist expression is involved in the anti-apoptotic effects of the IGF-1 receptor. J Biol Chem. 2001; 276: 26699-707.
28. Dupont J, Khan J, Qu BH, et al Insulin and IGF-1 induce different patterns of gene expression in mouse fibroblast NIH-3T3 cells: identification by cDNA microarray analysis. Endocrinology. 2001; 142: 4969-75.
29. Myers MG Jr, Sun XJ, Cheatham B, et al IRS-1 is a common element in insulin and insulin-like growth factor-I signaling to the phosphatidylinositol 3'-kinase. Endocrinology. 1993; 132: 1421-30.
30. Sun XJ, Wang LM, Zhang Y, et al Role of IRS-2 in insulin and cytokine signalling. Nature. 1995; 377:173-7.
31. Lehr S, Kotzka J, Herkner A, et al Identification of major tyrosine phosphorylation sites in the human insulin receptor substrate Gab-1 by insulin receptor kinase in vitro. Biochemistry. 2000; 39: 10898-907.
32. Pronk GJ, McGlade J, Pelicci G, et al Insulin-induced phosphorylation of the 46- and 52-kDa Shc proteins. J Biol Chem. 1993; 268: 5748-53.
33. Pandini G, Frasca F, Mineo R, et al Insulin/insulin-like growth factor I hybrid receptors have different biological characteristics depending on the insulin receptor isoform involved. J Biol Chem. 2002; 277: 39684-95.
34. Al-Khalili L, Kotova O, Tsuchida H, et al ERK1/2 mediates insulin stimulation of Na(+), K(+)-ATPase by phosphorylation of the alpha-subunit in human skeletal muscle cells. J Biol Chem. 2004; 279: 25211-8.
35. Vanhaesebroeck B, Alessi DR. The PI3K-PDK1 connection: more than just a road to PKB. Biochem J. 2000; 346: 561-76.
36. Vial C, Evans RJ. Disruption of lipid rafts inhibits P2×1 receptor-mediated currents and arterial vasoconstriction. J Biol Chem. 2005; 280: 30705-11.
37. Torres VA, Tapia JC, RodrÌguez DA, et al Caveolin-1 controls cell proliferation and cell death by suppressing expression of the inhibitor of apoptosis protein survivin. J Cell Sci. 2006; 119: 1812-23.
38. Labrecque L, Nyalendo C, Langlois S, et al Src-mediated tyrosine phosphorylation of caveolin-1 induces its association with membrane type 1 matrix metalloproteinase. J Biol Chem. 2004; 279: 52132-40.
39. Pak Y, Paule CR, Bao YD, et al Insulin stimulates the biosynthesis of chiro-inositol-containing phospholipids in a rat fibroblast line expressing the human insulin receptor. Proc Natl Acad Sci USA. 1993; 90: 7759-63.
40. Stumpo DJ, Blackshear PJ. Cellular expression of mutant insulin receptors interferes with the rapid transcriptional response to both insulin and insulin-like growth factor I. J Biol Chem. 1991; 266: 455-60.
41. Girard M, McPherson PS. RME-8 regulates trafficking of the epidermal growth factor receptor. FEBS Lett. 2008; 582: 961-6.
42. Roudabush FL, Pierce KL, Maudsley S. et al Transactivation of the EGF receptor mediates IGF-1-stimulated shc phosphorylation and ERK1/2 activation in COS-7 cells. J Biol Chem. 2000; 275: 22583-9.
43. Sasaoka T, Rose DW, Jhun BH, et al Evidence for a functional role of Shc proteins in mitogenic signaling induced by insulin, insulin-like growth factor-1, and epidermal growth factor. J Biol Chem. 1994; 269: 13689-94.
44. Dalle S, Ricketts W, Imamura T, et al Insulin and insulin-like growth factor I receptors utilize different G protein signaling components. J Biol Chem. 2001; 276: 15688-95.
45. Park JY, Hwang EM, Yarishkin O, et al TRPM4b channel suppresses store-operated Ca2+ entry by a novel protein-protein interaction with the TRPC3 channel. Biochem Biophys Res Commun. 2008; 368: 677-83.
46. Behrmann I, Smyczek T, Heinrich PC, et al Janus kinase (Jak) subcellular localization revisited: the exclusive membrane localization of endogenous Janus kinase 1 by cytokine receptor interaction uncovers the Jak.receptor complex to be equivalent to a receptor tyrosine kinase. J Biol Chem. 2004; 279: 35486-93.
47. Sciacca L, Costantino A, Pandini G, et al Insulin receptor activation by IGF-II in breast cancers: evidence for a new autocrine/paracrine mechanism. Oncogene. 1999; 18: 2471-9.
48. Herbert TP, Kilhams GR, Batty IH, et al Distinct signalling pathways mediate insulin and phorbol ester-stimulated eukaryotic initiation factor 4F assembly and protein synthesis in HEK 293 cells. J Biol Chem. 2000; 275: 11249-56.
49. Kwon H, Pak Y. Prolonged tyrosine kinase activation of insulin receptor by pY27-caveolin-2. Biochem Biophys Res Commun. 2010; 391, 49-55.
50. Burack WR, Shaw AS. Live cell imaging of ERK and MEK: simple binding equilibrium explains the regulated nucleocytoplasmic distribution of ERK. J Biol Chem. 2005; 280: 3832-7.
51. Cohen AW, Razani B, Wang XB, et al Caveolin-1-deficient mice show insulin resistance and defective insulin receptor protein expression in adipose tissue. Am J Physiol Cell Physiol. 2003; 285: C222-35.
52. Xie L, Frank PG, Lisanti MP, et al 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. 2010; 298: C693-701.
53. McGinnis S, Madden TL. BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res. 2004; 32: W20-5.
54. Minetti C, Sotgia F, Bruno C, et al Mutations in the caveolin-3 gene cause autosomal dominant limb-girdle muscular dystrophy. Nat Genet. 1998; 18: 365-8.
55. Schlegel A, Arvan P, Lisanti MP. Caveolin-1 binding to endoplasmic reticulum membranes and entry into the regulated secretory pathway are regulated by serine phosphorylation. Protein sorting at the level of the endoplasmic reticulum. J Biol Chem. 2001; 276: 4398-408.
56. Mundy DI, Machleidt T, Ying YS, et al Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton. J Cell Sci. 2002; 115: 4327-39.
57. Pelkmans L, Helenius A. Endocytosis via caveolae. Traffic. 2002; 3: 311-20.