Caveolin-1 mutants P132L and Y14F are dominant negative regulators of invasion, migration and aggregation in H1299 lung cancer cells

Experimental Cell Research

Volumn 316, Issue 10, 2010, Pages 1748-1762

  Shatz, Maria ^a   Lustig, Gila ^a   Reich, Reuven ^b   Liscovitch, Mordechai ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Cancer; Caveolin 1; Cell migration; Focal adhesions; Matrix invasiveness; Survival signaling

Indexed keywords

CAVEOLIN 1; FOCAL ADHESION KINASE; MATRIX METALLOPROTEINASE;

ARTICLE; CANCER CELL; CANCER INVASION; CAVEOLA; CELL AGGREGATION; CELL COUNT; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; GENE INACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LUNG CANCER; LUNG CARCINOGENESIS; MOLECULAR MECHANICS; MUTANT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE;

EID: 77953230423     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.02.006     Document Type: Article

References (70)

1. Liu P., Rudick M., Anderson R.G. Multiple functions of caveolin-1. J. Biol. Chem. 2002, 277:41295-41298.
2. Razani B., Woodman S.E., Lisanti M.P. Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 2002, 54:431-467.
3. Engelman J.A., Chu C., Lin A., Jo H., Ikezu T., Okamoto T., Kohtz D.S., Lisanti M.P. Caveolin-mediated regulation of signaling along the p42/44 MAP kinase cascade in vivo. A role for the caveolin-scaffolding domain. FEBS Lett. 1998, 428:205-211.
4. Galbiati F., Volonte D., Liu J., Capozza F., Frank P.G., Zhu L., Pestell R.G., Lisanti M.P. Caveolin-1 expression negatively regulates cell cycle progression by inducing G(0)/G(1) arrest via a p53/p21(WAF1/Cip1)-dependent mechanism. Mol. Biol. Cell 2001, 12:2229-2244.
5. Capozza F., Williams T.M., Schubert W., McClain S., Bouzahzah B., Sotgia F., Lisanti M.P. Absence of caveolin-1 sensitizes mouse skin to carcinogen-induced epidermal hyperplasia and tumor formation. Am. J. Pathol. 2003, 162:2029-2039.
6. Williams T.M., Cheung M.W., Park D.S., Razani B., Cohen A.W., Muller W.J., Di Vizio D., Chopra N.G., Pestell R.G., Lisanti M.P. Loss of caveolin-1 gene expression accelerates the development of dysplastic mammary lesions in tumor-prone transgenic mice. Mol. Biol. Cell 2003, 14:1027-1042.
7. Hayashi K., Matsuda S., Machida K., Yamamoto T., Fukuda Y., Nimura Y., Hayakawa T., Hamaguchi M. Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res. 2001, 61:2361-2364.
8. Li T., Sotgia F., Vuolo M.A., Li M., Yang W.C., Pestell R.G., Sparano J.A., Lisanti M.P. Caveolin-1 mutations in human breast cancer: functional association with estrogen receptor alpha-positive status. Am. J. Pathol. 2006, 168:1998-2013.
9. Lee H., Park D.S., Razani B., Russell R.G., Pestell R.G., Lisanti M.P. Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am. J. Pathol. 2002, 161:1357-1369.
10. Engelman J.A., Zhang X.L., Lisanti M.P. Genes encoding human caveolin-1 and -2 are co-localized to the D7S522 locus (7q31.1), a known fragile site (FRA7G) that is frequently deleted in human cancers. FEBS Lett. 1998, 436:403-410.
11. Razani B., Schlegel A., Liu J., Lisanti M.P. Caveolin-1, a putative tumour suppressor gene. Biochem. Soc. Trans. 2001, 29:494-499.
12. Liscovitch M., Burgermeister E., Jain N., Ravid D., Shatz M., Tencer L. Caveolin and cancer: a complex relationship. Membrane Microdomain Signaling: Lipid Rafts in Biology and Medicine 2005, 161-190. Humana Press, Totowa, New Jersey. M.P. Mattson (Ed.).
13. Lavie Y., Fiucci G., Liscovitch M. Up-regulation of caveolae and caveolar constituents in multidrug-resistant cancer cells. J. Biol. Chem. 1998, 273:32380-32383.
14. Nasu Y., Timme T.L., Yang G., Bangma C.H., Li L., Ren C., Park S.H., DeLeon M., Wang J., Thompson T.C. Suppression of caveolin expression induces androgen sensitivity in metastatic androgen-insensitive mouse prostate cancer cells. Nat. Med. 1998, 4:1062-1064.
15. Hurlstone A.F., Reid G., Reeves J.R., Fraser J., Strathdee G., Rahilly M., Parkinson E.K., Black D.M. Analysis of the CAVEOLIN-1 gene at human chromosome 7q31.1 in primary tumours and tumour-derived cell lines. Oncogene 1999, 18:1881-1890.
16. Davidson B., Nesland J.M., Goldberg I., Kopolovic J., Gotlieb W.H., Bryne M., Ben-Baruch G., Berner A., Reich R. Caveolin-1 expression in advanced-stage ovarian carcinoma-a clinicopathologic study. Gynecol. Oncol. 2001, 81:166-171.
17. Yang G., Addai J., Ittmann M., Wheeler T.M., Thompson T.C. Elevated caveolin-1 levels in African-American versus white-American prostate cancer. Clin. Cancer Res. 2000, 6:3430-3433.
18. Ho C.C., Huang P.H., Huang H.Y., Chen Y.H., Yang P.C., Hsu S.M. Up-regulated caveolin-1 accentuates the metastasis capability of lung adenocarcinoma by inducing filopodia formation. Am. J. Pathol. 2002, 161:1647-1656.
19. Yoo S.H., Park Y.S., Kim H.R., Sung S.W., Kim J.H., Shim Y.S., Lee S.D., Choi Y.L., Kim M.K., Chung D.H. Expression of caveolin-1 is associated with poor prognosis of patients with squamous cell carcinoma of the lung. Lung cancer (Amsterdam, Netherlands) 2003, 42:195-202.
20. Kato T., Miyamoto M., Kato K., Cho Y., Itoh T., Morikawa T., Okushiba S., Kondo S., Ohbuchi T., Katoh H. Difference of caveolin-1 expression pattern in human lung neoplastic tissue. Atypical adenomatous hyperplasia, adenocarcinoma and squamous cell carcinoma. Cancer Lett. 2004, 214:121-128.
21. Yang C.P., Galbiati F., Volonte D., Horwitz S.B., Lisanti M.P. Upregulation of caveolin-1 and caveolae organelles in Taxol-resistant A549 cells. FEBS Lett. 1998, 439:368-372.
22. Lavie Y., Liscovitch M. Changes in lipid and protein constituents of rafts and caveolae in multidrug resistant cancer cells and their functional consequences. Glycoconj J. 2000, 17:253-259.
23. Pang A., Au W.Y., Kwong Y.L. Caveolin-1 gene is coordinately regulated with the multidrug resistance 1 gene in normal and leukemic bone marrow. Leuk Research 2004, 28:973-977.
24. Li L., Yang G., Ebara S., Satoh T., Nasu Y., Timme T.L., Ren C., Wang J., Tahir S.A., Thompson T.C. Caveolin-1 mediates testosterone-stimulated survival/clonal growth and promotes metastatic activities in prostate cancer cells. Cancer Res. 2001, 61:4386-4392.
25. Sunaga N., Miyajima K., Suzuki M., Sato M., White M.A., Ramirez R.D., Shay J.W., Gazdar A.F., Minna J.D. Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res. 2004, 64:4277-4285.
26. Fiucci G., Ravid D., Reich R., Liscovitch M. Caveolin-1 inhibits anchorage-independent growth, anoikis and invasiveness in MCF-7 human breast cancer cells. Oncogene 2002, 21:2365-2375.
27. Ravid D., Maor S., Werner H., Liscovitch M. Caveolin-1 inhibits cell detachment-induced p53 activation and anoikis by upregulation of insulin-like growth factor-I receptors and signaling. Oncogene 2005, 24:1338-1347.
28. Cordes N., Frick S., Brunner T.B., Pilarsky C., Grutzmann R., Sipos B., Kloppel G., McKenna W.G., Bernhard E.J. Human pancreatic tumor cells are sensitized to ionizing radiation by knockdown of caveolin-1. Oncogene 2007, 26:6851-6862.
29. Li S., Seitz R., Lisanti M.P. Phosphorylation of caveolin by src tyrosine kinases. The alpha-isoform of caveolin is selectively phosphorylated by v-Src in vivo. J. Biol. Chem. 1996, 271:3863-3868.
30. Kimura A., Mora S., Shigematsu S., Pessin J.E., Saltiel A.R. The insulin receptor catalyzes the tyrosine phosphorylation of caveolin-1. J. Biol. Chem. 2002, 277:30153-30158.
31. Maggi D., Biedi C., Segat D., Barbero D., Panetta D., Cordera R. IGF-I induces caveolin 1 tyrosine phosphorylation and translocation in the lipid rafts. Biochem. Biophys. Research Commun. 2002, 295:1085-1089.
32. Swaney J.S., Patel H.H., Yokoyama U., Head B.P., Roth D.M., Insel P.A. Focal adhesions in (myo)fibroblasts scaffold adenylyl cyclase with phosphorylated caveolin. J. Biol. Chem. 2006, 281:17173-17179.
33. Lee H., Volonte D., Galbiati F., Iyengar P., Lublin D.M., Bregman D.B., Wilson M.T., Campos-Gonzalez R., Bouzahzah B., Pestell R.G., Scherer P.E., Lisanti M.P. Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol. Endocrinol. 2000, 14:1750-1775.
34. Tuschl H., Landsteiner H.T., Kovac R. Application of the popliteal lymph node assay in immunotoxicity testing: complementation of the direct popliteal lymph node assay with flow cytometric analyses. Toxicology 2002, 172:35-48.
35. Sigal A., Milo R., Cohen A., Geva-Zatorsky N., Klein Y., Alaluf I., Swerdlin N., Perzov N., Danon T., Liron Y., Raveh T., Carpenter A.E., Lahav G., Alon U. Dynamic proteomics in individual human cells uncovers widespread cell-cycle dependence of nuclear proteins. Nat. Methods 2006, 3:525-531.
36. Ikeda S., Ushio-Fukai M., Zuo L., Tojo T., Dikalov S., Patrushev N.A., Alexander R.W. Novel role of ARF6 in vascular endothelial growth factor-induced signaling and angiogenesis. Circ. Research 2005, 96:467-475.
37. Deryugina E.I., Quigley J.P. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev. 2006, 25:9-34.
38. Yoon S.O., Park S.J., Yun C.H., Chung A.S. Roles of matrix metalloproteinases in tumor metastasis and angiogenesis. J. Biochem. Mol. Biol. 2003, 36:128-137.
39. Cary L.A., Chang J.F., Guan J.L. Stimulation of cell migration by overexpression of focal adhesion kinase and its association with Src and Fyn. J. Cell Sci. 1996, 109(Pt. 7):1787-1794.
40. Vicente-Manzanares M., Webb D.J., Horwitz A.R. Cell migration at a glance. J. Cell Sci. 2005, 118:4917-4919.
41. Volonte D., Galbiati F., Pestell R.G., Lisanti M.P. Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J. Biol. Chem. 2001, 276:8094-8103.
42. del Pozo M.A., Balasubramanian N., Alderson N.B., Kiosses W.B., Grande-Garcia A., Anderson R.G., Schwartz M.A. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 2005, 7:901-908.
43. Jay D., Garcia E.J., de la Luz Ibarra M. In situ determination of a PKA phosphorylation site in the C-terminal region of filamin. Mol. Cell Biochem. 2004, 260:49-53.
44. Woo M.S., Ohta Y., Rabinovitz I., Stossel T.P., Blenis J. Ribosomal S6 kinase (RSK) regulates phosphorylation of filamin A on an important regulatory site. Mol. Cell. Biol. 2004, 24:3025-3035.
45. Kobayashi H., Boelte K.C., Lin P.C. Endothelial cell adhesion molecules and cancer progression. Curr. Med. Chem. 2007, 14:377-386.
46. Mochizuki S., Okada Y. ADAMs in cancer cell proliferation and progression. Cancer Sci. 2007, 98:621-628.
47. Drab M., Verkade P., Elger M., Kasper M., Lohn M., Lauterbach B., Menne J., Lindschau C., Mende F., Luft F.C., Schedl A., Haller H., Kurzchalia T.V. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science (New York, N.Y 2001, 293:2449-2452.
48. Razani B., Engelman J.A., Wang X.B., Schubert W., Zhang X.L., Marks C.B., Macaluso F., Russell R.G., Li M., Pestell R.G., Di Vizio D., Hou H., Kneitz B., Lagaud G., Christ G.J., Edelmann W., Lisanti M.P. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 2001, 276:38121-38138.
49. Wary K.K., Mariotti A., Zurzolo C., Giancotti F.G. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 1998, 94:625-634.
50. Williams T.M., Hassan G.S., Li J., Cohen A.W., Medina F., Frank P.G., Pestell R.G., Di Vizio D., Loda M., Lisanti M.P. Caveolin-1 Promotes Tumor Progression in an Autochthonous Mouse Model of Prostate Cancer: genetic ablation of cav-1 delays advanced prostate tumor development in tramp mice. J. Biol. Chem. 2005, 280:25134-25145.
51. Zhang B., Peng F., Wu D., Ingram A.J., Gao B., Krepinsky J.C. Caveolin-1 phosphorylation is required for stretch-induced EGFR and Akt activation in mesangial cells. Cell Signal 2007, 19:1690-1700.
52. Shajahan A.N., Wang A., Decker M., Minshall R.D., Liu M.C., Clarke R. Caveolin-1 tyrosine phosphorylation enhances paclitaxel-mediated cytotoxicity. J. Biol. Chem. 2007, 282:5934-5943.
53. Shatz M., Liscovitch M. Caveolin-1: a tumor-promoting role in human cancer. Int. J. Radiat. Biol. 2008, 84:177-189.
54. Belanger M.M., Gaudreau M., Roussel E., Couet J. Role of caveolin-1 in etoposide resistance development in A549 lung cancer cells. Cancer Biol. Ther. 2004, 3:954-959.
55. Ho C.C., Kuo S.H., Huang P.H., Huang H.Y., Yang C.H., Yang P.C. Caveolin-1 expression is significantly associated with drug resistance and poor prognosis in advanced non-small cell lung cancer patients treated with gemcitabine-based chemotherapy. Lung cancer (Amsterdam, Netherlands) 2008, 59:105-110.
56. Beardsley A., Fang K., Mertz H., Castranova V., Friend S., Liu J. Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J. Biol. Chem. 2005, 280:3541-3547.
57. Sun X.H., Flynn D.C., Castranova V., Millecchia L.L., Beardsley A.R., Liu J. Identification of a novel domain at the N terminus of caveolin-1 that controls rear polarization of the protein and caveolae formation. J. Biol. Chem. 2007, 282:7232-7241.
58. Grande-Garcia A., Echarri A., de Rooij J., Alderson N.B., Waterman-Storer C.M., Valdivielso J.M., del Pozo M.A. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 2007, 177:683-694.
59. Burridge K. Foot in mouth: do focal adhesions disassemble by endocytosis?. Nat. Cell Biol. 2005, 7:545-547.
60. Ezratty E.J., Partridge M.A., Gundersen G.G. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 2005, 7:581-590.
61. Stahlhut M., van Deurs B. Identification of filamin as a novel ligand for caveolin-1: evidence for the organization of caveolin-1-associated membrane domains by the actin cytoskeleton. Mol. Biol. Cell 2000, 11:325-337.
62. Gingras D., Gauthier F., Lamy S., Desrosiers R.R., Beliveau R. Localization of RhoA GTPase to endothelial caveolae-enriched membrane domains. Biochem. Biophys. Res. Commun. 1998, 247:888-893.
63. Lin M., Divito M.M., Merajver S.D., Boyanapalli M., van Golen K.L. Regulation of pancreatic cancer cell migration and invasion by RhoC GTPase and caveolin-1. Mol. Cancer 2005, 4:21.
64. Wary K.K., Mainiero F., Isakoff S.J., Marcantonio E.E., Giancotti F.G. The adaptor protein Shc couples a class of integrins to the control of cell cycle progression. Cell 1996, 87:733-743.
65. Upla P., Marjomaki V., Kankaanpaa P., Ivaska J., Hyypia T., Van Der Goot F.G., Heino J. Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. Mol. Biol. Cell 2004, 15:625-636.
66. Ning Y., Buranda T., Hudson L.G. Activated epidermal growth factor receptor induces integrin alpha2 internalization via caveolae/raft-dependent endocytic pathway. J. Biol. Chem. 2007, 282:6380-6387.
67. Kirkham M., Fujita A., Chadda R., Nixon S.J., Kurzchalia T.V., Sharma D.K., Pagano R.E., Hancock J.F., Mayor S., Parton R.G. Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles. J. Cell Biol. 2005, 168:465-476.
68. Mege R.M., Gavard J., Lambert M. Regulation of cell-cell junctions by the cytoskeleton. Curr. Opin. Cell Biol. 2006, 18:541-548.
69. Galbiati F., Volonte D., Brown A.M., Weinstein D.E., Ben-Ze'ev A., Pestell R.G., Lisanti M.P. Caveolin-1 expression inhibits Wnt/beta-catenin/Lef-1 signaling by recruiting beta-catenin to caveolae membrane domains. J. Biol. Chem. 2000, 275:23368-23377.
70. Hofmann C., Obermeier F., Artinger M., Hausmann M., Falk W., Schoelmerich J., Rogler G., Grossmann J. Cell-cell contacts prevent anoikis in primary human colonic epithelial cells. Gastroenterology 2007, 132:587-600.