Genetic Evidence for XPC-KRAS Interactions During Lung Cancer Development

Xiaoli Zhang; Nonggao He; Dongsheng Gu; Jeff Wickliffe; James Salazar; Istavan Boldogh; Jingwu Xie

doi:10.1016/j.jgg.2015.09.006

Volume 42 Issue 10

Oct. 2015

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2015 > 42(10): 589-596

PDF( 1309 KB)

Genetic Evidence for XPC-KRAS Interactions During Lung Cancer Development

doi: 10.1016/j.jgg.2015.09.006

a
Department of Pediatrics, Wells Center for Pediatrics Research, Indiana University School of Medicine, Indianapolis, IN 46202, USA
b
University of Texas Medical Branch, School of Medicine Cancer Center, Galveston, TX 77550, USA
c
Department of Global Environmental Health Sciences, Tulane University School of Public Health, New Orleans, LA 70112, USA
d
Biology Department, Galveston College, Galveston, TX 77550, USA
e
Department of Microbiology and Immunology, University of Texas Medical Branch, School of Medicine, Galveston, TX 77550, USA

More Information

Corresponding author: E-mail address: jinxie@iu.edu (Jingwu Xie)
Received Date: 2015-08-11
Accepted Date: 2015-09-17
Rev Recd Date: 2015-09-16

Available Online: 2015-10-17

Publish Date: 2015-10-20

Abstract

Abstract

Lung cancer causes more deaths than breast, colorectal and prostate cancers combined. Despite major advances in targeted therapy in a subset of lung adenocarcinomas, the overall 5-year survival rate for lung cancer worldwide has not significantly changed for the last few decades. DNA repair deficiency is known to contribute to lung cancer development. In fact, human polymorphisms in DNA repair genes such as xeroderma pigmentosum group C (XPC) are highly associated with lung cancer incidence. However, the direct genetic evidence for the role of XPC for lung cancer development is still lacking. Mutations of the Kirsten rat sarcoma viral oncogene homolog (Kras) or its downstream effector genes occur in almost all lung cancer cells, and there are a number of mouse models for lung cancer with these mutations. Using activated Kras, Kras, as a driver for lung cancer development in mice, we showed for the first time that mice with Kras and Xpc knockout had worst outcomes in lung cancer development, and this phenotype was associated with accumulated DNA damage. Using cultured cells, we demonstrated that induced expression of oncogenic KRAS^G12V led to increased levels of reactive oxygen species (ROS) as well as DNA damage, and both can be suppressed by anti-oxidants. Our results suggest that XPC may help repair DNA damage caused by KRAS-mediated production of ROS.
- Lung cancer,
- XPC,
- ROS

The first two authors contributed equally to this work.

FullText(HTML)

References(54)

References

[1]	Adimoolam, S., Ford, J.M. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene Proc. Natl. Acad. Sci. USA, 99 (2002),pp. 12985-12990
[2]	Berenbaum, M.C. A method for testing for synergy with any number of agents J. Infect. Dis., 137 (1978),pp. 122-130
[3]	Berg, R.J., Ruven, H.J., Sands, A.T. et al. Defective global genome repair in XPC mice is associated with skin cancer susceptibility but not with sensitivity to UVB induced erythema and edema J. Invest. Dermatol., 110 (1998),pp. 405-409
[4]	Boldogh, I., Bacsi, A., Choudhury, B.K. et al. ROS generated by pollen NADPH oxidase provide a signal that augments antigen-induced allergic airway inflammation J. Clin. Invest., 115 (2005),pp. 2169-2179
[5]	Boldogh, I., Liebenthal, D., Hughes, T.K. et al. Modulation of 4HNE-mediated signaling by proline-rich peptides from ovine colostrum J. Mol. Neurosci., 20 (2003),pp. 125-134
[6]	Boldogh, I., Roy, G., Lee, M.S. et al. Reduced DNA double strand breaks in chlorambucil resistant cells are related to high DNA-PKcs activity and low oxidative stress Toxicology, 193 (2003),pp. 137-152
[7]	Cheo, D.L., Meira, L.B., Burns, D.K. et al. Cancer Res., 60 (2000),pp. 1580-1584
[8]	Cheo, D.L., Meira, L.B., Hammer, R.E. et al. Curr. Biol., 6 (1996),pp. 1691-1694
[9]	Cheo, D.L., Ruven, H.J., Meira, L.B. et al. Mutat. Res., 374 (1997),pp. 1-9
[10]	Cooper, W.A., Lam, D.C., O'Toole, S.A. et al. Molecular biology of lung cancer J. Thorac. Dis., 5 (2013),pp. S479-S490
[11]	D'Errico, M., Parlanti, E., Teson, M. et al. New functions of XPC in the protection of human skin cells from oxidative damage EMBO J., 25 (2006),pp. 4305-4315
[12]	Dusinska, M., Collins, A.R. The comet assay in human biomonitoring: gene-environment interactions Mutagenesis, 23 (2008),pp. 191-205
[13]	Fan, Q., Gu, D., Liu, H. et al. Defective TGF-beta signaling in bone marrow-derived cells prevents hedgehog-induced skin tumors Cancer Res., 74 (2014),pp. 471-483
[14]	Friedberg, E.C., Bond, J.P., Burns, D.K. et al. Mutat. Res., 459 (2000),pp. 99-108
[15]	Gu, D., Liu, H., Su, G.H. et al. Combining hedgehog signaling inhibition with focal irradiation on reduction of pancreatic cancer metastasis Mol. Cancer Ther., 12 (2013),pp. 1038-1048
[16]	Hastak, K., Adimoolam, S., Trinklein, N.D. et al. Genes Cancer, 3 (2012),pp. 131-140
[17]	Hollander, M.C., Philburn, R.T., Patterson, A.D. et al. Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 13200-13205
[18]	Hu, Z., Wang, Y., Wang, X. et al. Int. J. Cancer, 115 (2005),pp. 478-483
[19]	Jackson, E.L., Willis, N., Mercer, K. et al. Genes Dev., 15 (2001),pp. 3243-3248
[20]	Jin, B., Dong, Y., Zhang, X. et al. PLoS One, 9 (2014),p. e93937
[21]	Johnson, L., Mercer, K., Greenbaum, D. et al. Nature, 410 (2001),pp. 1111-1116
[22]	Krzeszinski, J.Y., Choe, V., Shao, J. et al. XPC promotes MDM2-mediated degradation of the p53 tumor suppressor Mol. Biol. Cell, 25 (2014),pp. 213-221
[23]	Lee, G.Y., Jang, J.S., Lee, S.Y. et al. J. Int. Cancer, 115 (2005),pp. 807-813
[24]	Logan, A., Cocheme, H.M., Li Pun, P.B. et al. Biochim. Biophys. Acta, 1840 (2014),pp. 923-930
[25]	Lu, W., Hu, Y., Chen, G. et al. Novel role of NOX in supporting aerobic glycolysis in cancer cells with mitochondrial dysfunction and as a potential target for cancer therapy PLoS Biol., 10 (2012),p. e1001326
[26]	Matakidou, A., Eisen, T., Fleischmann, C. et al. J. Int. Cancer, 119 (2006),pp. 964-967
[27]	Melis, J.P., Luijten, M., Mullenders, L.H. et al. The role of XPC: implications in cancer and oxidative DNA damage Mutat. Res., 728 (2011),pp. 107-117
[28]	Melis, J.P., van Steeg, H., Luijten, M. Oxidative DNA damage and nucleotide excision repair Antioxid. Redox Signal., 18 (2013),pp. 2409-2419
[29]	Melis, J.P., Wijnhoven, S.W., Beems, R.B. et al. Mouse models for xeroderma pigmentosum group A and group C show divergent cancer phenotypes Cancer Res., 68 (2008),pp. 1347-1353
[30]	Meng, Q., Skopek, T.R., Walker, D.M. et al. Environ. Mol. Mutagen, 32 (1998),pp. 236-243
[31]	Menoni, H., Hoeijmakers, J.H., Vermeulen, W. J. Cell Biol., 199 (2012),pp. 1037-1046
[32]	Ogrunc, M., Di Micco, R., Liontos, M. et al. Oncogene-induced reactive oxygen species fuel hyperproliferation and DNA damage response activation Cell Death Differ., 21 (2014),pp. 998-1012
[33]	Park, M.T., Kim, M.J., Suh, Y. et al. Novel signaling axis for ROS generation during K-Ras-induced cellular transformation Cell Death Differ., 21 (2014),pp. 1185-1197
[34]	Parlanti, E., D'Errico, M., Degan, P. et al. The cross talk between pathways in the repair of 8-oxo-7,8-dihydroguanine in mouse and human cells Free Radic. Biol. Med., 53 (2012),pp. 2171-2177
[35]	Reddel, R.R., Salghetti, S.E., Willey, J.C. et al. Development of tumorigenicity in simian virus 40-immortalized human bronchial epithelial cell lines Cancer Res., 53 (1993),pp. 985-991
[36]	Robert, C., Karaszewska, B., Schachter, J. et al. Improved overall survival in melanoma with combined dabrafenib and trametinib N. Engl. J. Med., 372 (2015),pp. 30-39
[37]	Sengupta, S., Harris, C.C. p53: traffic cop at the crossroads of DNA repair and recombination Nat. Rev. Mol. Cell Biol., 6 (2005),pp. 44-55
[38]	Siegel, R.L., Miller, K.D., Jemal, A. Cancer statistics, 2015 CA Cancer J. Clin., 65 (2015),pp. 5-29
[39]	Thomas, A., Liu, S.V., Subramaniam, D.S. et al. Refining the treatment of NSCLC according to histological and molecular subtypes Nat. Rev. Clin. Oncol., 12 (2015),pp. 511-526
[40]	Thress, K.S., Paweletz, C.P., Felip, E. et al. Nat. Med., 21 (2015),pp. 560-562
[41]	Trachootham, D., Alexandre, J., Huang, P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov., 8 (2009),pp. 579-591
[42]	Tricker, E.M., Xu, C., Uddin, S. et al. Cancer Discov., 5 (2015),pp. 960-971
[43]	Ugurel, S., Loquai, C., Kahler, K. et al. A multicenter DeCOG study on predictors of vemurafenib therapy outcome in melanoma: pretreatment impacts survival Ann. Oncol., 26 (2015),pp. 573-582
[44]	Vogel, U., Overvad, K., Wallin, H. et al. Cancer Lett., 222 (2005),pp. 67-74
[45]	Wang, P., Zhu, C.F., Ma, M.Z. et al. Micro-RNA-155 is induced by K-Ras oncogenic signal and promotes ROS stress in pancreatic cancer Oncotarget, 6 (2015),pp. 21148-21158
[46]	Weber, J.S., D'Angelo, S.P., Minor, D. et al. Lancet Oncol., 16 (2015),pp. 375-384
[47]	Weinberg, F., Hamanaka, R., Wheaton, W.W. et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 8788-8793
[48]	Wickliffe, J.K., Ammenheuser, M.M., Salazar, J.J. et al. A model of sensitivity: 1,3-butadiene increases mutant frequencies and genomic damage in mice lacking a functional microsomal epoxide hydrolase gene Environ. Mol. Mutagen, 42 (2003),pp. 106-110
[49]	Wu, Y.H., Cheng, Y.W., Chang, J.T. et al. Reduced XPC messenger RNA level may predict a poor outcome of patients with nonsmall cell lung cancer Cancer, 110 (2007),pp. 215-223
[50]	Wu, Y.H., Tsai Chang, J.H., Cheng, Y.W. et al. Xeroderma pigmentosum group C gene expression is predominantly regulated by promoter hypermethylation and contributes to p53 mutation in lung cancers Oncogene, 26 (2007),pp. 4761-4773
[51]	Yang, J.C., Sequist, L.V., Geater, S.L. et al. Lancet Oncol., 16 (2015),pp. 830-838
[52]	Yang, J.C., Wu, Y.L., Schuler, M. et al. Lancet Oncol., 16 (2015),pp. 141-151
[53]	Yang, Y., Sharma, R., Sharma, A. et al. Lipid peroxidation and cell cycle signaling: 4-hydroxynonenal, a key molecule in stress mediated signaling Acta Biochim. Pol., 50 (2003),pp. 319-336
[54]	Zhong, H., Yin, H. Role of lipid peroxidation derived 4-hydroxynonenal (4-HNE) in cancer: focusing on mitochondria Redox Biol., 4 (2015),pp. 193-199