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Published in: Medical Oncology 3/2012

01-09-2012 | Original Paper

Clinicopathological significance and prognostic value of Xeroderma pigmentosum complementary group C (XPC) expression in sporadic breast cancer patients

Authors: Xuefeng Bai, Feng Jin, Yingzi Fu, Zhaojin Yu, Lin Zhao, Jie Ren, Yanlin Li, Xuyang Jiao, Haishan Zhao, Weifan Yao, Xiaoyi Mi, Enhua Wang, Olufunmilayo I. Olopade, Mingyi Zhou, Minjie Wei

Published in: Medical Oncology | Issue 3/2012

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Abstract

Breast cancer is the most common type of cancer among women worldwide, and the incidence of breast cancer is increasing in the developing world. Estrogen exposure is a major risk factor for breast cancer, and estrogen oxidative metabolites have been implicated in chemical carcinogenesis. Xeroderma pigmentosum complementary group C (XPC) plays an important and multifaceted role in cell protection from oxidative DNA damage. Thus, XPC inactivation may be involved in the early stage of breast cancer. The aim of this study was to investigate the expression of XPC protein in sporadic breast cancer tissues and determine whether XPC expression influences breast cancer malignancy and clinical outcome. Fifteen cases of adjacent non-tumor breast tissue, 28 cases of fibroadenomas and 235 cases of breast carcinomas were examined by immunohistochemistry using polyclonal antibody to XPC. Both cytoplasmic and nuclear expression level of XPC were downregulated in breast carcinoma when compared to non-tumor tissues (P < 0.05). The nuclear expression level of XPC was significantly associated with expression of BCL2 (r = 0.231, P = 0.033) and p53 (r = 0.205, P = 0.011), and nuclear expression of XPC was significantly associated with patients’ age (P = 0.024). Neither cytoplasmic nor nuclear expression level of XPC had impact on patients’ survival in the whole samples. However, XPC expression was correlated with adverse survival in HER2-positive, but not HER2-negative, tumors, as demonstrated by Kaplan–Meier analysis. Our results suggested that the XPC protein is involved in the occurrence and progression of breast cancer.
Literature
1.
go back to reference Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev. 2010;19(8):1893–907.PubMedCrossRef Jemal A, Center MM, DeSantis C, Ward EM. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol Biomarkers Prev. 2010;19(8):1893–907.PubMedCrossRef
2.
go back to reference Song M, Lee KM, Kang D. Breast cancer prevention based on gene-environment interaction. Mol Carcinog. 2011;50(4):280–90.PubMedCrossRef Song M, Lee KM, Kang D. Breast cancer prevention based on gene-environment interaction. Mol Carcinog. 2011;50(4):280–90.PubMedCrossRef
3.
go back to reference Henderson BE, Ross R, Bernstein L. Estrogens as a cause of human cancer: the Richard and Hinda Rosenthal Foundation award lecture. Cancer Res. 1988;48(2):246–53.PubMed Henderson BE, Ross R, Bernstein L. Estrogens as a cause of human cancer: the Richard and Hinda Rosenthal Foundation award lecture. Cancer Res. 1988;48(2):246–53.PubMed
4.
go back to reference Bolton JL, Thatcher GR. Potential mechanisms of estrogen quinone carcinogenesis. Chem Res Toxicol. 2008;21(1):93–101.PubMedCrossRef Bolton JL, Thatcher GR. Potential mechanisms of estrogen quinone carcinogenesis. Chem Res Toxicol. 2008;21(1):93–101.PubMedCrossRef
5.
go back to reference Rajapakse N, Butterworth M, Kortenkamp A. Detection of DNA strand breaks and oxidized DNA bases at the single-cell level resulting from exposure to estradiol and hydroxylated metabolites. Environ Mol Mutagen. 2005;45(4):397–404.PubMedCrossRef Rajapakse N, Butterworth M, Kortenkamp A. Detection of DNA strand breaks and oxidized DNA bases at the single-cell level resulting from exposure to estradiol and hydroxylated metabolites. Environ Mol Mutagen. 2005;45(4):397–404.PubMedCrossRef
7.
go back to reference Kim IJ, Ku JL, Kang HC, Park JH, Yoon KA, Shin Y, et al. Mutational analysis of OGG1, MYH, MTH1 in FAP, HNPCC and sporadic colorectal cancer patients: R154H OGG1 polymorphism is associated with sporadic colorectal cancer patients. Hum Genet. 2004;115(6):498–503.PubMedCrossRef Kim IJ, Ku JL, Kang HC, Park JH, Yoon KA, Shin Y, et al. Mutational analysis of OGG1, MYH, MTH1 in FAP, HNPCC and sporadic colorectal cancer patients: R154H OGG1 polymorphism is associated with sporadic colorectal cancer patients. Hum Genet. 2004;115(6):498–503.PubMedCrossRef
8.
go back to reference Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T. Removal of oxygen free-radical-induced 5’, 8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci USA. 2000;97(8):3832–7.PubMedCrossRef Kuraoka I, Bender C, Romieu A, Cadet J, Wood RD, Lindahl T. Removal of oxygen free-radical-induced 5’, 8-purine cyclodeoxynucleosides from DNA by the nucleotide excision-repair pathway in human cells. Proc Natl Acad Sci USA. 2000;97(8):3832–7.PubMedCrossRef
9.
go back to reference Kovacs E, Stucki D, Weber W, Muller H. Impaired DNA-repair synthesis in lymphocytes of breast cancer patients. Eur J Cancer Clin Oncol. 1986;22(7):863–9.PubMedCrossRef Kovacs E, Stucki D, Weber W, Muller H. Impaired DNA-repair synthesis in lymphocytes of breast cancer patients. Eur J Cancer Clin Oncol. 1986;22(7):863–9.PubMedCrossRef
10.
go back to reference Ramos JM, Ruiz A, Colen R, Lopez ID, Grossman L, Matta JL. DNA repair and breast carcinoma susceptibility in women. Cancer. 2004;100(7):1352–7.PubMedCrossRef Ramos JM, Ruiz A, Colen R, Lopez ID, Grossman L, Matta JL. DNA repair and breast carcinoma susceptibility in women. Cancer. 2004;100(7):1352–7.PubMedCrossRef
11.
go back to reference Latimer JJ, Johnson JM, Kelly CM, Miles TD, Beaudry-Rodgers KA, Lalanne NA, et al. Nucleotide excision repair deficiency is intrinsic in sporadic stage I breast cancer. Proc Natl Acad Sci USA. 2010;107(50):21725–30.PubMedCrossRef Latimer JJ, Johnson JM, Kelly CM, Miles TD, Beaudry-Rodgers KA, Lalanne NA, et al. Nucleotide excision repair deficiency is intrinsic in sporadic stage I breast cancer. Proc Natl Acad Sci USA. 2010;107(50):21725–30.PubMedCrossRef
12.
go back to reference Hey T, Lipps G, Sugasawa K, Iwai S, Hanaoka F, Krauss G. The XPC-HR23B complex displays high affinity and specificity for damaged DNA in a true-equilibrium fluorescence assay. Biochemistry. 2002;41(21):6583–7.PubMedCrossRef Hey T, Lipps G, Sugasawa K, Iwai S, Hanaoka F, Krauss G. The XPC-HR23B complex displays high affinity and specificity for damaged DNA in a true-equilibrium fluorescence assay. Biochemistry. 2002;41(21):6583–7.PubMedCrossRef
13.
go back to reference Yang A, Miron S, Mouawad L, Duchambon P, Blouquit Y, Craescu CT. Flexibility and plasticity of human centrin 2 binding to the xeroderma pigmentosum group C protein (XPC) from nuclear excision repair. Biochemistry. 2006;45(11):3653–63.PubMedCrossRef Yang A, Miron S, Mouawad L, Duchambon P, Blouquit Y, Craescu CT. Flexibility and plasticity of human centrin 2 binding to the xeroderma pigmentosum group C protein (XPC) from nuclear excision repair. Biochemistry. 2006;45(11):3653–63.PubMedCrossRef
14.
go back to reference Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001;15(5):507–21.PubMedCrossRef Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001;15(5):507–21.PubMedCrossRef
15.
go back to reference Sugasawa K, Shimizu Y, Iwai S, Hanaoka F. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst). 2002;1(1):95–107.CrossRef Sugasawa K, Shimizu Y, Iwai S, Hanaoka F. A molecular mechanism for DNA damage recognition by the xeroderma pigmentosum group C protein complex. DNA Repair (Amst). 2002;1(1):95–107.CrossRef
16.
go back to reference D’Errico M, Parlanti E, Teson M, de Jesus BM, Degan P, Calcagnile A, et al. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J. 2006;25(18):4305–15.PubMedCrossRef D’Errico M, Parlanti E, Teson M, de Jesus BM, Degan P, Calcagnile A, et al. New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J. 2006;25(18):4305–15.PubMedCrossRef
17.
go back to reference Shimizu Y, Iwai S, Hanaoka F, Sugasawa K. Xeroderma pigmentosum group C protein interacts physically and functionally with thymine DNA glycosylase. EMBO J. 2003;22(1):164–73.PubMedCrossRef Shimizu Y, Iwai S, Hanaoka F, Sugasawa K. Xeroderma pigmentosum group C protein interacts physically and functionally with thymine DNA glycosylase. EMBO J. 2003;22(1):164–73.PubMedCrossRef
18.
go back to reference Shore RE, Zeleniuch-Jacquotte A, Currie D, Mohrenweiser H, Afanasyeva Y, Koenig KL, et al. Polymorphisms in XPC and ERCC2 genes, smoking and breast cancer risk. Int J Cancer. 2008;122(9):2101–5.PubMedCrossRef Shore RE, Zeleniuch-Jacquotte A, Currie D, Mohrenweiser H, Afanasyeva Y, Koenig KL, et al. Polymorphisms in XPC and ERCC2 genes, smoking and breast cancer risk. Int J Cancer. 2008;122(9):2101–5.PubMedCrossRef
19.
go back to reference El-Deiry WS. Transactivation of repair genes by BRCA1. Cancer Biol Ther. 2002;1(5):490–1.PubMed El-Deiry WS. Transactivation of repair genes by BRCA1. Cancer Biol Ther. 2002;1(5):490–1.PubMed
20.
go back to reference Hartman AR, Ford JM. BRCA1 induces DNA damage recognition factors and enhances nucleotide excision repair. Nat Genet. 2002;32(1):180–4.PubMedCrossRef Hartman AR, Ford JM. BRCA1 induces DNA damage recognition factors and enhances nucleotide excision repair. Nat Genet. 2002;32(1):180–4.PubMedCrossRef
21.
go back to reference Yang J, Xu Z, Li J, Zhang R, Zhang G, Ji H, et al. XPC epigenetic silence coupled with p53 alteration has a significant impact on bladder cancer outcome. J Urol. 2010;184(1):336–43.PubMedCrossRef Yang J, Xu Z, Li J, Zhang R, Zhang G, Ji H, et al. XPC epigenetic silence coupled with p53 alteration has a significant impact on bladder cancer outcome. J Urol. 2010;184(1):336–43.PubMedCrossRef
22.
go back to reference Chen Z, Yang J, Wang G, Song B, Li J, Xu Z. Attenuated expression of xeroderma pigmentosum group C is associated with critical events in human bladder cancer carcinogenesis and progression. Cancer Res. 2007;67(10):4578–85.PubMedCrossRef Chen Z, Yang J, Wang G, Song B, Li J, Xu Z. Attenuated expression of xeroderma pigmentosum group C is associated with critical events in human bladder cancer carcinogenesis and progression. Cancer Res. 2007;67(10):4578–85.PubMedCrossRef
23.
go back to reference Wu YH, Cheng YW, Chang JT, Wu TC, Chen CY, Lee H. Reduced XPC messenger RNA level may predict a poor outcome of patients with nonsmall cell lung cancer. Cancer. 2007;110(1):215–23.PubMedCrossRef Wu YH, Cheng YW, Chang JT, Wu TC, Chen CY, Lee H. Reduced XPC messenger RNA level may predict a poor outcome of patients with nonsmall cell lung cancer. Cancer. 2007;110(1):215–23.PubMedCrossRef
24.
go back to reference Fautrel A, Andrieux L, Musso O, Boudjema K, Guillouzo A, Langouet S. Overexpression of the two nucleotide excision repair genes ERCC1 and XPC in human hepatocellular carcinoma. J Hepatol. 2005;43(2):288–93.PubMedCrossRef Fautrel A, Andrieux L, Musso O, Boudjema K, Guillouzo A, Langouet S. Overexpression of the two nucleotide excision repair genes ERCC1 and XPC in human hepatocellular carcinoma. J Hepatol. 2005;43(2):288–93.PubMedCrossRef
25.
go back to reference Rezvani HR, Kim AL, Rossignol R, Ali N, Daly M, Mahfouf W, et al. XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas. J Clin Invest. 2011;121(1):195–211.PubMedCrossRef Rezvani HR, Kim AL, Rossignol R, Ali N, Daly M, Mahfouf W, et al. XPC silencing in normal human keratinocytes triggers metabolic alterations that drive the formation of squamous cell carcinomas. J Clin Invest. 2011;121(1):195–211.PubMedCrossRef
26.
go back to reference Wu YH, Tsai Chang JH, Cheng YW, Wu TC, Chen CY, Lee H. Xeroderma pigmentosum group C gene expression is predominantly regulated by promoter hypermethylation and contributes to p53 mutation in lung cancers. Oncogene. 2007;26(33):4761–73.PubMedCrossRef Wu YH, Tsai Chang JH, Cheng YW, Wu TC, Chen CY, Lee H. Xeroderma pigmentosum group C gene expression is predominantly regulated by promoter hypermethylation and contributes to p53 mutation in lung cancers. Oncogene. 2007;26(33):4761–73.PubMedCrossRef
28.
go back to reference Takebayashi Y, Nakayama K, Kanzaki A, Miyashita H, Ogura O, Mori S, et al. Loss of heterozygosity of nucleotide excision repair factors in sporadic ovarian, colon and lung carcinomas: implication for their roles of carcinogenesis in human solid tumors. Cancer Lett. 2001;174(2):115–25.PubMedCrossRef Takebayashi Y, Nakayama K, Kanzaki A, Miyashita H, Ogura O, Mori S, et al. Loss of heterozygosity of nucleotide excision repair factors in sporadic ovarian, colon and lung carcinomas: implication for their roles of carcinogenesis in human solid tumors. Cancer Lett. 2001;174(2):115–25.PubMedCrossRef
29.
go back to reference Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 1993;75(5):855–62.PubMedCrossRef Wightman B, Ha I, Ruvkun G. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell. 1993;75(5):855–62.PubMedCrossRef
30.
go back to reference Hanova M, Stetina R, Vodickova L, Vaclavikova R, Hlavac P, Smerhovsky Z, et al. Modulation of DNA repair capacity and mRNA expression levels of XRCC1, hOGG1 and XPC genes in styrene-exposed workers. Toxicol Appl Pharmacol. 2010;248(3):194–200.PubMedCrossRef Hanova M, Stetina R, Vodickova L, Vaclavikova R, Hlavac P, Smerhovsky Z, et al. Modulation of DNA repair capacity and mRNA expression levels of XRCC1, hOGG1 and XPC genes in styrene-exposed workers. Toxicol Appl Pharmacol. 2010;248(3):194–200.PubMedCrossRef
31.
go back to reference Sandrini JZ, Trindade GS, Nery LE, Marins LF. Time-course expression of DNA repair-related genes in hepatocytes of zebrafish (Danio rerio) after UV-B exposure. Photochem Photobiol. 2009;85(1):220–6.PubMedCrossRef Sandrini JZ, Trindade GS, Nery LE, Marins LF. Time-course expression of DNA repair-related genes in hepatocytes of zebrafish (Danio rerio) after UV-B exposure. Photochem Photobiol. 2009;85(1):220–6.PubMedCrossRef
32.
go back to reference Adimoolam S, Ford JM. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc Natl Acad Sci USA. 2002;99(20):12985–90.PubMedCrossRef Adimoolam S, Ford JM. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc Natl Acad Sci USA. 2002;99(20):12985–90.PubMedCrossRef
33.
go back to reference Fitch ME, Cross IV, Ford JM. p53 responsive nucleotide excision repair gene products p48 and XPC, but not p53, localize to sites of UV-irradiation-induced DNA damage, in vivo. Carcinogenesis. 2003;24(5):843–50.PubMedCrossRef Fitch ME, Cross IV, Ford JM. p53 responsive nucleotide excision repair gene products p48 and XPC, but not p53, localize to sites of UV-irradiation-induced DNA damage, in vivo. Carcinogenesis. 2003;24(5):843–50.PubMedCrossRef
34.
go back to reference Wang G, Chuang L, Zhang X, Colton S, Dombkowski A, Reiners J, et al. The initiative role of XPC protein in cisplatin DNA damaging treatment-mediated cell cycle regulation. Nucleic Acids Res. 2004;32(7):2231–40.PubMedCrossRef Wang G, Chuang L, Zhang X, Colton S, Dombkowski A, Reiners J, et al. The initiative role of XPC protein in cisplatin DNA damaging treatment-mediated cell cycle regulation. Nucleic Acids Res. 2004;32(7):2231–40.PubMedCrossRef
35.
go back to reference Wang G, Dombkowski A, Chuang L, Xu XX. The involvement of XPC protein in the cisplatin DNA damaging treatment-mediated cellular response. Cell Res. 2004;14(4):303–14.PubMedCrossRef Wang G, Dombkowski A, Chuang L, Xu XX. The involvement of XPC protein in the cisplatin DNA damaging treatment-mediated cellular response. Cell Res. 2004;14(4):303–14.PubMedCrossRef
36.
go back to reference Guillem VM, Cervantes F, Martinez J, Alvarez-Larran A, Collado M, Camos M, et al. XPC genetic polymorphisms correlate with the response to imatinib treatment in patients with chronic phase chronic myeloid leukemia. Am J Hematol. 2010;85(7):482–6.PubMedCrossRef Guillem VM, Cervantes F, Martinez J, Alvarez-Larran A, Collado M, Camos M, et al. XPC genetic polymorphisms correlate with the response to imatinib treatment in patients with chronic phase chronic myeloid leukemia. Am J Hematol. 2010;85(7):482–6.PubMedCrossRef
37.
go back to reference Lai TC, Chow KC, Fang HY, Cho HC, Chen CY, Lin TY, et al. Expression of xeroderma pigmentosum complementation group C protein predicts cisplatin resistance in lung adenocarcinoma patients. Oncol Rep. 2011;25(5):1243–51.PubMed Lai TC, Chow KC, Fang HY, Cho HC, Chen CY, Lin TY, et al. Expression of xeroderma pigmentosum complementation group C protein predicts cisplatin resistance in lung adenocarcinoma patients. Oncol Rep. 2011;25(5):1243–51.PubMed
Metadata
Title
Clinicopathological significance and prognostic value of Xeroderma pigmentosum complementary group C (XPC) expression in sporadic breast cancer patients
Authors
Xuefeng Bai
Feng Jin
Yingzi Fu
Zhaojin Yu
Lin Zhao
Jie Ren
Yanlin Li
Xuyang Jiao
Haishan Zhao
Weifan Yao
Xiaoyi Mi
Enhua Wang
Olufunmilayo I. Olopade
Mingyi Zhou
Minjie Wei
Publication date
01-09-2012
Publisher
Springer US
Published in
Medical Oncology / Issue 3/2012
Print ISSN: 1357-0560
Electronic ISSN: 1559-131X
DOI
https://doi.org/10.1007/s12032-011-0086-7

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