Involvement of caveolin-1 in repair of DNA damage through both homologous recombination and non-homologous end joining

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Zhu, Hua ^b   Yue, Jingyin ^b   Pan, Zui ^b   Wu, Hao ^b   Cheng, Yan ^a   Lu, Huimei ^b   Ren, Xingcong ^a   Yao, Ming ^b   Shen, Zhiyuan ^b   Yang, Jin Ming ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; DNA; DNA DEPENDENT PROTEIN KINASE; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; SMALL INTERFERING RNA;

ARTICLE; CANCER CELL CULTURE; CELL NUCLEUS; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME PHOSPHORYLATION; GENE SILENCING; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IONIZING RADIATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; DOUBLE STRANDED DNA BREAK; GENETIC RECOMBINATION; GENETICS; METABOLISM; TUMOR CELL LINE;

ANIMALS; CAVEOLIN 1; CELL LINE, TUMOR; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; GENE SILENCING; HUMANS; RECOMBINATION, GENETIC; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 77957800868     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012055     Document Type: Article

References (56)

1. Bouras T, Lisanti MP, Pestell RG (2004) Caveolin-1 in breast cancer. Cancer Biol Ther 3: 931-941.
2. Burgermeister E, Liscovitch M, Rocken C, Schmid RM, Ebert MP (2008) Caveats of caveolin-1 in cancer progression. Cancer Lett 268: 187-201.
3. Burgermeister E, Xing X, Rocken C, Juhasz M, Chen J, et al. (2007) Differential expression and function of caveolin-1 in human gastric cancer progression. Cancer Res 67: 8519-8526.
4. Carver LA, Schnitzer JE (2003) Caveolae: mining little caves for new cancer targets. Nat Rev Cancer 3: 571-581.
5. Engelman JA, Zhang XL, Lisanti MP (1998) 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 436: 403-410.
6. Sagara Y, Mimori K, Yoshinaga K, Tanaka F, Nishida K, et al. (2004) Clinical significance of Caveolin-1, Caveolin-2 and HER2/neu mRNA expression in human breast cancer. Br J Cancer 91: 959-965.
7. Bender FC, Reymond MA, Bron C, Quest AF (2000) Caveolin-1 levels are down-regulated in human colon tumors, and ectopic expression of caveolin-1 in colon carcinoma cell lines reduces cell tumorigenicity. Cancer Res 60: 5870-5878.
8. Kato T, Miyamoto M, Kato K, Cho Y, Itoh T, et al. (2004) Difference of caveolin-1 expression pattern in human lung neoplastic tissue. Atypical adenomatous hyperplasia, adenocarcinoma and squamous cell carcinoma. Cancer Lett 214: 121-128.
9. Racine C, Belanger M, Hirabayashi H, Boucher M, Chakir J, et al. (1999) Reduction of caveolin 1 gene expression in lung carcinoma cell lines. Biochem Biophys Res Commun 255: 580-586.
10. Sunaga N, Miyajima K, Suzuki M, Sato M, White MA, et al. (2004) Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res 64: 4277-4285.
11. Bagnoli M, Tomassetti A, Figini M, Flati S, Dolo V, et al. (2000) Downmodulation of caveolin-1 expression in human ovarian carcinoma is directly related to alpha-folate receptor overexpression. Oncogene 19: 4754-4763.
12. Wiechen K, Diatchenko L, Agoulnik A, Scharff KM, Schober H, et al. (2001) Caveolin-1 is down-regulated in human ovarian carcinoma and acts as a candidate tumor suppressor gene. Am J Pathol 159: 1635-1643.
13. Wiechen K, Sers C, Agoulnik A, Arlt K, Dietel M, et al. (2001) Down-regulation of caveolin-1, a candidate tumor suppressor gene, in sarcomas. Am J Pathol 158: 833-839.
14. Aldred MA, Ginn-Pease ME, Morrison CD, Popkie AP, Gimm O, et al. (2003) Caveolin-1 and caveolin-2,together with three bone morphogenetic proteinrelated genes, may encode novel tumor suppressors down-regulated in sporadic follicular thyroid carcinogenesis. Cancer Res 63: 2864-2871.
15. Lee SW, Reimer CL, Oh P, Campbell DB, Schnitzer JE (1998) Tumor cell growth inhibition by caveolin re-expression in human breast cancer cells. Oncogene 16: 1391-1397.
16. Wu P, Wang X, Li F, Qi B, Zhu H, et al. (2008) Growth suppression of MCF-7 cancer cell-derived xenografts in nude mice by caveolin-1. Biochem Biophys Res Commun 376: 215-220.
17. Hayashi K, Matsuda S, Machida K, Yamamoto T, Fukuda Y, et al. (2001) Invasion activating caveolin-1 mutation in human scirrhous breast cancers. Cancer Res 61: 2361-2364.
18. Williams TM, Cheung MW, Park DS, Razani B, Cohen AW, et al. (2003) Loss of caveolin-1 gene expression accelerates the development of dysplastic mammary lesions in tumor-prone transgenic mice. Mol Biol Cell 14: 1027-1042.
19. Rajjayabun PH, Garg S, Durkan GC, Charlton R, Robinson MC, et al. (2001) Caveolin-1 expression is associated with high-grade bladder cancer. Urology 58: 811-814.
20. Elsheikh SE, Green AR, Rakha EA, Samaka RM, Ammar AA, et al. (2008) Caveolin 1 and Caveolin 2 are associated with breast cancer basal-like and triple-negative immunophenotype. Br J Cancer 99: 327-334.
21. Pinilla SM, Honrado E, Hardisson D, Benitez J, Palacios J (2006) Caveolin-1 expression is associated with a basal-like phenotype in sporadic and hereditary breast cancer. Breast Cancer Res Treat 99: 85-90.
22. Savage K, Lambros MB, Robertson D, Jones RL, Jones C, et al. (2007) Caveolin 1 is overexpressed and amplified in a subset of basal-like and metaplastic breast carcinomas: a morphologic, ultrastructural, immunohistochemical, and in situ hybridization analysis. Clin Cancer Res 13: 90-101.
23. Patlolla JM, Swamy MV, Raju J, Rao CV (2004) Overexpression of caveolin-1 in experimental colon adenocarcinomas and human colon cancer cell lines. Oncol Rep 11: 957-963.
24. Ando T, Ishiguro H, Kimura M, Mitsui A, Mori Y, et al. (2007) The overexpression of caveolin-1 and caveolin-2 correlates with a poor prognosis and tumor progression in esophageal squamous cell carcinoma. Oncol Rep 18: 601-609.
25. Kato K, Hida Y, Miyamoto M, Hashida H, Shinohara T, et al. (2002) Overexpression of caveolin-1 in esophageal squamous cell carcinoma correlates with lymph node metastasis and pathologic stage. Cancer 94: 929-933.
26. Ho CC, Kuo SH, Huang PH, Huang HY, Yang CH, et al. (2008) 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 59: 105-110.
27. Tanase CP (2008) Caveolin-1: a marker for pancreatic cancer diagnosis. Expert Rev Mol Diagn 8: 395-404.
28. Satoh T, Yang G, Egawa S, Addai J, Frolov A, et al. (2003) Caveolin-1 expression is a predictor of recurrence-free survival in pT2N0 prostate carcinoma diagnosed in Japanese patients. Cancer 97: 1225-1233.
29. Campbell L, Gumbleton M, Griffiths DF (2003) Caveolin-1 overexpression predicts poor disease-free survival of patients with clinically confined renal cell carcinoma. Br J Cancer 89: 1909-1913.
30. Joo HJ, Oh DK, Kim YS, Lee KB, Kim SJ (2004) Increased expression of caveolin-1 and microvessel density correlates with metastasis and poor prognosis in clear cell renal cell carcinoma. BJU Int 93: 291-296.
31. Lavie Y, Fiucci G, Liscovitch M (2001) Upregulation of caveolin in multidrug resistant cancer cells: functional implications. Adv Drug Deliv Rev 49: 317-323.
32. Shatz M, Liscovitch M (2004) Caveolin-1 and cancer multidrug resistance: coordinate regulation of pro-survival proteins? Leuk Res 28: 907-908.
33. Cordes N, Frick S, Brunner TB, Pilarsky C, Grutzmann R, et al. (2007) Human pancreatic tumor cells are sensitized to ionizing radiation by knockdown of caveolin-1. Oncogene 26: 6851-6862.
34. Hehlgans S, Eke I, Storch K, Haase M, Baretton GB, et al. (2009) Caveolin-1 mediated radioresistance of 3D grown pancreatic cancer cells. Radiother Oncol.
35. Lio YC, Schild D, Brenneman MA, Redpath JL, Chen DJ (2004) Human Rad51C deficiency destabilizes XRCC3, impairs recombination, and radiosensitizes S/G2-phase cells. J Biol Chem 279: 42313-42320.
36. Lobrich M, Jeggo PA (2007) The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat Rev Cancer 7: 861-869.
37. Bennardo N, Cheng A, Huang N, Stark JM (2008) Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 4: e1000110.
38. Chen DJ, Nirodi CS (2007) The epidermal growth factor receptor: a role in repair of radiation-induced DNA damage. Clin Cancer Res 13: 6555-6560.
39. Del Pozo MA, Schwartz MA (2007) Rac, membrane heterogeneity, caveolin and regulation of growth by integrins. Trends Cell Biol 17: 246-250.
40. Ravid D, Maor S, Werner H, Liscovitch M (2005) Caveolin-1 inhibits cell detachment-induced p53 activation and anoikis by upregulation of insulin-like growth factor-I receptors and signaling. Oncogene 24: 1338-1347.
41. Glait C, Tencer L, Ravid D, Sarfstein R, Liscovitch M, et al. (2006) Caveolin-1 up-regulates IGF-I receptor gene transcription in breast cancer cells via Sp1- and p53-dependent pathways. Exp Cell Res 312: 3899-3908.
42. Zhu H, Weisleder N, Wu P, Cai C, Chen JW (2008) Caveolae/caveolin-1 are important modulators of store-operated calcium entry in Hs578/T breast cancer cells. J Pharmacol Sci 106: 287-294.
43. Dittmann K, Mayer C, Kehlbach R, Rodemann HP (2008) Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol Cancer 7: 69.
44. Ahn M, Kim H, Kim JT, Lee J, Hyun JW, et al. (2006) Gamma-ray irradiation stimulates the expression of caveolin-1 and GFAP in rat spinal cord: a study of immunoblot and immunohistochemistry. J Vet Sci 7: 309-314.
45. Scully R, Chen J, Ochs RL, Keegan K, Hoekstra M, et al. (1997) Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90: 425-435.
46. Wang Y, Yu J, Zhan Q (2008) BRCA1 regulates caveolin-1 expression and inhibits cell invasiveness. Biochem Biophys Res Commun 370: 201-206.
47. Glait C, Ravid D, Lee SW, Liscovitch M, Werner H (2006) Caveolin-1 controls BRCA1 gene expression and cellular localization in human breast cancer cells. FEBS Lett 580: 5268-5274.
48. Milovanova T, Chatterjee S, Hawkins BJ, Hong N, Sorokina EM, et al. (2008) Caveolae are an essential component of the pathway for endothelial cell signaling associated with abrupt reduction of shear stress. Biochim Biophys Acta 1783: 1866-1875.
49. Ravid D, Maor S, Werner H, Liscovitch M (2006) Caveolin-1 inhibits anoikis and promotes survival signaling in cancer cells. Adv Enzyme Regul 46: 163-175.
50. Patel HH, Tsutsumi YM, Head BP, Niesman IR, Jennings M, et al. (2007) Mechanisms of cardiac protection from ischemia/reperfusion injury: a role for caveolae and caveolin-1. FASEB J 21: 1565-1574.
51. Dasari A, Bartholomew JN, Volonte D, Galbiati F (2006) Oxidative stress induces premature senescence by stimulating caveolin-1 gene transcription through p38 mitogen-activated protein kinase/Sp1-mediated activation of two GC-rich promoter elements. Cancer Res 66: 10805-10814.
52. Frank PG, Lisanti MP (2006) Role of caveolin-1 in the regulation of the vascular shear stress response. J Clin Invest 116: 1222-1225.
53. Li T, Sotgia F, Vuolo MA, Li M, Yang WC, et al. (2006) Caveolin-1 mutations in human breast cancer: functional association with estrogen receptor alphapositive status. Am J Pathol 168: 1998-2013.
54. Zhu H, Wu H, Liu X, Evans BR, Medina DJ, et al. (2008) Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem Pharmacol 76: 582-588.
55. Zhu H, Cai C, Chen J (2004) Suppression of P-glycoprotein gene expression in Hs578T/Dox by the overexpression of caveolin-1. FEBS Lett 576: 369-374.
56. Lu H, Yue J, Meng X, Nickoloff JA, Shen Z (2007) BCCIP regulates homologous recombination by distinct domains and suppresses spontaneous DNA damage. Nucleic Acids Res 35: 7160-7170.