Absence of caveolin-1 sensitizes mouse skin to carcinogen-induced epidermal hyperplasia and tumor formation

American Journal of Pathology

Volumn 162, Issue 6, 2003, Pages 2029-2039

  Capozza, Franco ^a   Williams, Terence M ^a   Schubert, William ^a   McClain, Steve ^a   Bouzahzah, Boumediene ^a   Sotgia, Federica ^a   Lisanti, Michael P ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; CARCINOGEN; CAVEOLIN 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN P42;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CAVEOLA; CELL TRANSFORMATION; CHROMOSOME 7Q; CHROMOSOME FRAGILE SITE; CONTROLLED STUDY; EPIDERMIS HYPERPLASIA; GENE LOCUS; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

EID: 0038751964     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)64335-0     Document Type: Article

References (51)

1. Razani B, Woodman SE, Lisanti MP: Caveolae: from cell biology to animal physiology. Pharmacol Rev 2002, 54:431-467
2. Glenney JR Jr: Tyrosine phosphorylation of a 22-kDa protein is correlated with transformation by Rous sarcoma virus. J Biol Chem 1989, 264:20163-20166
3. Koleske AJ, Baltimore D, Lisanti MP: Reduction of caveolin and caveolae in oncogenically transformed cells. Proc Natl Acad Sci USA 1995, 92:1381-1385
4. Engelman JA, Wycoff CC, Yasuhara S, Song KS, Okamoto T, Lisanti MP: Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 1997, 272:16374-16381
5. Park DS, Razani B, Lasorella A, Schreiber-Agus N, Pestell RG, Iavarone A, Lisanti MP: Evidence that Myc isoforms transcriptionally repress caveolin-1 gene expression via an INR-dependent mechanism. Biochemistry 2001, 40:3354-3362
6. Razani B, Altschuler Y, Zhu L, Pestell RG, Mostov KE, Lisanti MP: Caveolin-1 expression is down-regulated in cells transformed by the human papilloma virus in a p53-dependent manner. Replacement of caveolin-1 expression suppresses HPV-mediated cell transformation. Biochemistry 2000, 39:13916-13924
7. 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
8. Zhang W, Razani B, Altschuler Y, Bouzahzah B, Mostov KE, Pestell RG, Lisanti MP: Caveolin-1 inhibits epidermal growth factor-stimulated lamellipod extension and cell migration in metastatic mammary adenocarcinoma cells (MTLn3): transformation suppressor effects of adenovirus-mediated gene delivery of caveolin-1. J Biol Chem 2000, 275:20717-20725
9. Galbiati F, Volonté D, Engelman JA, Watanabe G, Burk R, Pestell R, Lisanti MP: Targeted down-regulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 1998, 17:6633-6648
10. Lee SW, Reimer CL, Oh P, Campbell DB, Schnitzer JE: Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene 1998, 16:1391-1397
11. Engelman JA, Zhang XL, Galbiati F, Lisanti MP: Chromosomal localization, genomic organization, and developmental expression of the murine caveolin gene family (Cav-1, -2, and -3): Cav-1 and Cav-2 genes map to a known tumor suppressor locus (6-A2/7q31). FEBS Lett 1998, 429:330-336
12. Engelman JA, Zhang XL, Lisanti MP: 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
13. Engelman JA, Zhang XL, Galbiati F, Volonte D, Sotgia F, Pestell RG, Minetti C, Scherer PE, Okamoto T, Lisanti MP: Molecular genetics of the caveolin gene family: implications for human cancers, Diabetes, Alzheimer's disease, and muscular dystrophy. Am J Hum Genetics 1998, 63:1578-1587
14. Jenkins RB, Qian J, Lee HK, Huang H, Hirasawa K, Bostwick DG, Proffitt J, Wilber K, Lieber MM, Liu W, Smith DI: A molecular cytogenetic analysis of 7q31 in prostate cancer. Cancer Res 1998, 58:759-766
15. Kerr J, Leary JA, Hurst T, Shih YC, Antalis TM, Friedlander M, Crawford E, Khoo SK, Ward B, Chenevix-Trench G: Allelic loss on chromosome 7q in ovarian adenocarcinomas: two critical regions and a rearrangement of the PLANH1 locus. Oncogene 1996, 13:1815-1818
16. Shridhar V, Sun QC, Miller OJ, Kalemkerian GP, Petros J, Smith DI: Loss of heterozygosity on the long arm of human chromosome 7 in sporadic renal cell carcinomas. Oncogene 1997, 15:2727-2733
17. Zenklusen JC, Thompson JC, Troncoso P, Kagan J, Conti CJ: Loss of heterozygosity in human primary prostate carcinomas: a possible tumor suppressor gene at 7q31.1. Cancer Res 1994, 54:6370-6373
18. Zenklusen JC, Bieche I, Lidereau R, Conti CJ: (C-A)n microsatellite repeat D7S522 is the most commonly deleted region in human primary breast cancer. Proc Natl Acad Sci USA 1994, 91:12155-12158
19. Huang H, Qian C, Jenkins RB, Smith DI: Fish mapping of YAC clones at human chromosomal band 7q31.2: identification of YACS spanning FRA7G within the common region of LOH in breast and prostate cancer. Genes Chromosomes Cancer 1998, 21:152-159
20. Sager R, Sheng S, Anisowicz A, Sotiropoulou G, Zou Z, Stenman G, Swisshelm K, Chen Z, Hendrix MJC, Pemberton P, Rafidi K, Ryan K: RNA genetics of breast cancer: maspin as a paradigm. Cold Spring Harbor Sym. Quant. Biol. 1994; LIX:537-546
21. Suzuki T, Suzuki Y, Hanada K, Hashimoto A, Redpath JL, Stanbridge EJ, Nishijima M, Kitagawa T: Reduction of caveolin-1 expression in tumorigenic human cell hybrids. J Biochem 1998, 124:383-388
22. Engelman JA, Lee RJ, Karnezis A, Bearss DJ, Webster M, Siegel P, Muller WJ, Windle JJ, Pestell RG, Lisanti MP: Reciprocal regulation of Neu tyrosine kinase activity and caveolin-1 protein expression in vitro and in vivo. Implications for mammary tumorigenesis. J Biol Chem 1998, 273:20448-20455
23. 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
24. Lee H, Park DS, Razani B, Russell RG, Pestell RG, Lisanti MP: 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
25. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV: Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452
26. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP: Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001, 276:38121-38138
27. Park DS, Lee H, Frank PG, Razani B, Nguyen AV, Parlow AF, Russell RG, Hulit J, Pestell RG, Lisanti MP: Caveolin-1-deficient mice show accelerated mammary gland development during pregnancy, premature lactation, and hyperactivation of the Jak-2/STAT5a signaling cascade. Mol Biol Cell 2002, 13:3416-3430
28. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA: Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996, 85:27-37
29. Kupferman ME, Fini ME, Muller WJ, Weber R, Cheng Y, Muschel RJ: Matrix metalloproteinase 9 promoter activity is induced coincident with invasion during tumor progression. Am J Pathol 2000, 157:1777-1783
30. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, Aguirre AJ, Wu EA, Horner JW, DePinho RA: Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 2001, 413:86-91
31. Weinberg WC, Fernandez-Salas E, Morgan DL, Shalizi A, Mirosh E, Stanulis E, Deng C, Hennings H, Yuspa SH: Genetic deletion of p21WAF1 enhances papilloma formation but not malignant conversion in experimental mouse skin carcinogenesis. Cancer Res 1999, 59:2050-2054
32. Gonzalez-Suarez E, Samper E, Flores JM, Blasco MA: Telomerase-deficient mice with short telomeres are resistant to skin tumorigenesis. Nat Genet 2000, 26:114-117
33. Campbell L, Laidler P, Watson RE, Kirby B, Griffiths CE, Gumbleton M: Downregulation and altered spatial pattern of caveolin-1 in chronic plaque psoriasis. Br J Dermatol 2002, 147:701-709
34. Yamamoto H, Ochiya T, Takeshita F, Toriyama-Baba H, Hirai K, Sasaki H, Sakamoto H, Yoshida T, Saito I, Terada M: Enhanced skin carcinogenesis in cyclin D1-conditional transgenic mice: cyclin D1 alters keratinocyte response to calcium-induced terminal differentiation. Cancer Res 2002, 62:1641-1647
35. Gassmann MG, Werner S: Caveolin-1 and -2 expression is differentially regulated in cultured keratinocytes and within the regenerating epidermis of cutaneous wounds. Exp Cell Res 2000, 258:23-32
36. Campbell L, Gumbleton M: Aberrant caveolin-1 expression in psoriasis: a signalling hypothesis. IUBMB Life 2000, 50:361-364
37. Breton S, Lisanti MP, Tyszkowski R, McLaughlin M, Brown D: Basolateral distribution of caveolin-1 in the kidney: absence from H+-ATPase-coated endocytic vesicles in intercalated cells. J Histochem Cytochem 1998, 46:205-214
38. Mora R, Bonilha VL, Marmorstein A, Scherer PE, Brown D, Lisanti MP, Rodriguez-Boulan E: Caveolin-2 localizes to the Golgi complex but redistributes to plasma membrane, caveolae, and rafts when co-expressed with caveolin-1. J Biol Chem 1999, 274:25708-25717
39. Vogel U, Sandvig K, van Deurs B: Expression of caveolin-1 and polarized formation of invaginated caveolae in Caco-2 and MDCK II cells. J Cell Sci 1998, 111:825-832
40. Fuchs E: Keratins and the skin. Annu Rev Cell Dev Biol 1995, 11:123-153
41. Engelman JA, Chu C, Lin A, Jo H, Ikezu T, Okamoto T, Kohtz DS, Lisanti MP: 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
42. Hulit J, Bash T, Fu M, Galbiati F, Albanese C, Sage DR, Schlegel A, Zhurinsky J, Shtutman M, Ben-Ze'ev A, Lisanti MP, Pestell RG: The cyclin D1 gene is transcriptionally repressed by caveolin-1. J Biol Chem 2000, 275:21203-21209
43. Couet J, Sargiacomo M, Lisanti MP: Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem 1997, 272:30429-30438
44. Scheel J, Srinivasan J, Honnert U, Henske A, Kurzchalia TV: Involvement of caveolin-1 in meiotic cell-cycle progression in Caenorhabditis elegans. Nat Cell Biol 1999, 1:127-129
45. Lammie GA, Peters G: Chromosome 11q13 abnormalities in human cancer. Cancer Cells 1991, 3:413-420
46. Bianchi AB, Fischer SM, Robles AI, Rinchk EM, Conti CJ: Overexpression of cyclin D1 in mouse skin carcinogenesis. Oncogene 1993, 8:1127-1133
47. Bizub D, Wood AW, Skalka AM: Mutagenesis of the Ha-ras oncogene in mouse skin tumors induced by polycyclic aromatic hydrocarbons. Proc Natl Acad Sci USA 1986, 83:6048-6052
48. Quintanilla M, Brown K, Ramsden M, Balmain A: Carcinogen-specific mutation and amplification of Ha-ras during mouse skin carcinogenesis. Nature 1986, 322:78-80
49. Filmus J, Robles AI, Shi W, Wong MJ, Colombo LL, Conti C: Induction of cyclin D1 overexpression by activated ras. Oncogene 1994, 9:3627-3633
50. Li WP, Liu P, Pilcher BK, Anderson RG: Cell-specific targeting of caveolin-1 to caveolae, secretory vesicles, cytoplasm or mitochondria. J Cell Sci 2001, 114:1397-1408
51. Woodman SE, Ashton AW, Schubert W, Lee H, Williams TM, Medina FA, Wyckoff JB, Combs TP, Lisanti MP: Caveolin-1 knock-out mice show an impaired angiogenic response to exogenous stimuli. Am J Pathol 2003, 162:2059-2068