p22phox confers resistance to cisplatin, by blocking its entry into the nucleus

Oncotarget

Volumn 6, Issue 6, 2015, Pages 4110-4125

  Hung, Chih Chang ^a,b   Chien, Chen Yu ^c,d,e   Chiang, Wei Fan ^f,g   Lin, Chang Shen ^a   Hour, Tzyh Chyuan ^b   Chen, Hau Ren ^h   Wang, Ling Feng ^b,c   Ko, Jenq Yuh ⁱ   Chang, Chi Hua ^j   Chen, Jeff Yi Fu ^b  

^a KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^c KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

^d KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e KAOHSIUNG MUNICIPAL HSIAO KANG HOSPITAL   (Taiwan)

^f CHI MEI MEDICAL CENTER   (Taiwan)

^g NATIONAL YANG MING UNIVERSITY   (Taiwan)

^h NATIONAL CHUNG CHENG UNIVERSITY   (Taiwan)

ⁱ NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^j CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

more..

Author keywords

Apoptosis; CDDP resistance; Oral squamous cell carcinoma (OSCC); p22phox; PI3K Akt

Indexed keywords

CHECKPOINT KINASE 1; CISPLATIN; PROTEIN KINASE B; PROTEIN P22PHOX; PROTEIN P53; REGULATOR PROTEIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CYBA PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADULT; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL PROTECTION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOPLASM; DRUG RESISTANCE; DRUG SENSITIVITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IC50; MIDDLE AGED; MOUTH SQUAMOUS CELL CARCINOMA; ORAL CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; BIOSYNTHESIS; CARCINOMA, SQUAMOUS CELL; FEMALE; GENE SILENCING; GENETICS; HEAD AND NECK NEOPLASMS; MALE; METABOLISM; MOUTH NEOPLASMS; PATHOLOGY; TUMOR CELL LINE;

ANTINEOPLASTIC AGENTS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL NUCLEUS; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HEAD AND NECK NEOPLASMS; HUMANS; MALE; MIDDLE AGED; MOUTH NEOPLASMS; NADPH OXIDASE; UP-REGULATION;

EID: 84924272625     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2893     Document Type: Article

References (41)

1. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007; 87:245-313.
2. Kawahara T, Ritsick D, Cheng G, Lambeth JD. Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1-and Nox2-dependent reactive oxygen generation. J Biol Chem. 2005; 280:31859-31869.
3. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal. 2006; 18:69-82.
4. Block K, Gorin Y, New DD, Eid A, Chelmicki T, Reed A, Choudhury GG, Parekh DJ, Abboud HE. The NADPH oxidase subunit p22phox inhibits the function of the tumor suppressor protein tuberin. Am J Pathol. 2010; 176:2447-2455.
5. Edderkaoui M, Nitsche C, Zheng L, Pandol SJ, Gukovsky I, Gukovskaya AS. NADPH oxidase activation in pancreatic cancer cells is mediated through Akt-dependent up-regulation of p22phox. J Biol Chem. 2011; 286:7779-7787.
6. Czesnikiewicz-Guzik M, Lorkowska B, Zapala J, Czajka M, Szuta M, Loster B, Guzik TJ, Korbut R. NADPH oxidase and uncoupled nitric oxide synthase are major sources of reactive oxygen species in oral squamous cell carcinoma. Potential implications for immune regulation in high oxidative stress conditions. J Physiol Pharmacol. 2008; 59:139-152.
7. Gonzalez VM, Fuertes MA, Alonso C, Perez JM. Is cisplatin-induced cell death always produced by apoptosis? Mol Pharmacol. 2001; 59:657-663.
8. Specenier PM, Vermorken JB. Current concepts for the management of head and neck cancer: chemotherapy. Oral Oncol. 2009; 45:409-415.
9. Ru P, Steele R, Hsueh EC, Ray RB. Anti-miR-203 upregulates SOCS3 expression in breast cancer cells and enhances cisplatin chemosensitivity. Genes Cancer. 2011; 2:720-727.
10. Azuma M, Harada K, Supriatno , Tamatani T, Motegi K, Ashida Y, Sato M. Potentiation of induction of apoptosis by sequential treatment with cisplatin followed by 5-fluorouracil in human oral cancer cells. Int J Oncol. 2004; 24:1449-1455.
11. Andreadis C, Vahtsevanos K, Sidiras T, Thomaidis I, Antoniadis K, Mouratidou D. 5-Fluorouracil and cisplatin in the treatment of advanced oral cancer. Oral Oncol. 2003; 39:380-385.
12. Aichler M, Motschmann M, Jutting U, Luber B, Becker K, Ott K, Lordick F, Langer R, Feith M, Siewert JR, Walch A. Epidermal growth factor receptor (EGFR) is an independent adverse prognostic factor in esophageal adenocarcinoma patients treated with cisplatin-based neoadjuvant chemotherapy. Oncotarget. 2014; 5:6620-6632.
13. Hiraishi Y, Wada T, Nakatani K, Tojyo I, Matsumoto T, Kiga N, Negoro K, Fujita S. EGFR inhibitor enhances cisplatin sensitivity of oral squamous cell carcinoma cell lines. Pathol Oncol Res. 2008; 14:39-43.
14. Itoh T, Terazawa R, Kojima K, Nakane K, Deguchi T, Ando M, Tsukamasa Y, Ito M, Nozawa Y. Cisplatin induces production of reactive oxygen species via NADPH oxidase activation in human prostate cancer cells. Free Radic Res. 2011; 45:1033-1039.
15. Pak JH, Choi WH, Lee HM, Joo WD, Kim JH, Kim YT, Kim YM, Nam JH. Peroxiredoxin 6 overexpression attenuates cisplatin-induced apoptosis in human ovarian cancer cells. Cancer Invest. 2011; 29:21-28.
16. Villar J, Quadri HS, Song I, Tomita Y, Tirado OM, Notario V. PCPH/ENTPD5 expression confers to prostate cancer cells resistance against cisplatin-induced apoptosis through protein kinase Calpha-mediated Bcl-2 stabilization. Cancer Res. 2009; 69:102-110.
17. Jo H, Lo PK, Li Y, Loison F, Green S, Wang J, Silberstein LE, Ye K, Chen H, Luo HR. Deactivation of Akt by a small molecule inhibitor targeting pleckstrin homology domain and facilitating Akt ubiquitination. Proc Natl Acad Sci U S A. 2011; 108:6486-6491.
18. Weyemi U, Caillou B, Talbot M, Ameziane-El-Hassani R, Lacroix L, Lagent-Chevallier O, Al Ghuzlan A, Roos D, Bidart JM, Virion A, Schlumberger M, Dupuy C. Intracellular expression of reactive oxygen species-generating NADPH oxidase NOX4 in normal and cancer thyroid tissues. Endocrine-related cancer. 2010; 17:27-37.
19. Thompson R, Meuth M, Woll P, Zhu Y, Danson S. Treatment with the Chk1 inhibitor Go6976 enhances cisplatin cytotoxicity in SCLC cells. Int J Oncol. 2012; 40:194-202.
20. Wagner JM, Karnitz LM. Cisplatin-induced DNA damage activates replication checkpoint signaling components that differentially affect tumor cell survival. Mol Pharmacol. 2009; 76:208-214.
21. Xu ZY, Loignon M, Han FY, Panasci L, Aloyz R. Xrcc3 induces cisplatin resistance by stimulation of Rad51-related recombinational repair, S-phase checkpoint activation, and reduced apoptosis. The Journal of pharmacology and experimental therapeutics. 2005; 314:495-505.
22. Downward J. PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol. 2004; 15:177-182.
23. Song G, Ouyang G, Bao S. The activation of Akt/PKB signaling pathway and cell survival. J Cell Mol Med. 2005; 9:59-71.
24. Wang M, Liu ZM, Li XC, Yao YT, Yin ZX. Activation of ERK1/2 and Akt is associated with cisplatin resistance in human lung cancer cells. Journal of chemotherapy (Florence, Italy). 2013; 25:162-169.
25. Wang Y, Chen L, Huang G, He D, He J, Xu W, Zou C, Zong F, Li Y, Chen B, Wu S, Zhao W, Wu J. Klotho sensitizes human lung cancer cell line to cisplatin via PI3k/Akt pathway. PLoS One. 2013; 8:e57391.
26. Zhang LL, Zhang J, Shen L, Xu XM, Yu HG. Overexpression of AKT decreases the chemosensitivity of gastric cancer cells to cisplatin in vitro and in vivo. Molecular medicine reports. 2013; 7:1387-1390.
27. Kim KW, Myers CJ, Jung DK, Lu B. NVP-BEZ-235 enhances radiosensitization via blockade of the PI3K/mTOR pathway in cisplatin-resistant non-small cell lung carcinoma. Genes Cancer. 2014; Jul 5:293-302.
28. Shih RH, Cheng SE, Hsiao LD, Kou YR, Yang CM. Cigarette smoke extract upregulates heme oxygenase-1 via PKC/NADPH oxidase/ROS/PDGFR/PI3K/Akt pathway in mouse brain endothelial cells. Journal of neuroinflammation. 2011; 8:104.
29. Son YO, Wang L, Poyil P, Budhraja A, Hitron JA, Zhang Z, Lee JC, Shi X. Cadmium induces carcinogenesis in BEAS-2B cells through ROS-dependent activation of PI3K/AKT/GSK-3beta/beta-catenin signaling. Toxicol Appl Pharmacol. 2012; 264:153-160.
30. Wang X, Liu JZ, Hu JX, Wu H, Li YL, Chen HL, Bai H, Hai CX. ROS-activated p38 MAPK/ERK-Akt cascade plays a central role in palmitic acid-stimulated hepatocyte proliferation. Free radical biology & medicine. 2011; 51:539-551.
31. Fan L, Song B, Sun G, Ma T, Zhong F, Wei W. Endoplasmic reticulum stress-induced resistance to Doxorubicin is reversed by paeonol treatment in human hepatocellular carcinoma cells. PLoS One. 2013; 8:e62627.
32. Lin Y, Wang Z, Liu L, Chen L. Akt is the downstream target of GRP78 in mediating cisplatin resistance in ER stress-tolerant human lung cancer cells. Lung Cancer. 2011; 71:291-297.
33. Liang XJ, Shen DW, Chen KG, Wincovitch SM, Garfield SH, Gottesman MM. Trafficking and localization of platinum complexes in cisplatin-resistant cell lines monitored by fluorescence-labeled platinum. Journal of cellular physiology. 2005; 202:635-641.
34. Chen HH, Kuo MT. Role of glutathione in the regulation of Cisplatin resistance in cancer chemotherapy. Metal-based drugs. 2010; vol. 2010, Article ID 430939, 7 pages, doi:10.1155/2010/430939.
35. Kasahara K, Fujiwara Y, Nishio K, Ohmori T, Sugimoto Y, Komiya K, Matsuda T, Saijo N. Metallothionein content correlates with the sensitivity of human small cell lung cancer cell lines to cisplatin. Cancer Res. 1991; 51:3237-3242.
36. Kelley SL, Basu A, Teicher BA, Hacker MP, Hamer DH, Lazo JS. Overexpression of metallothionein confers resistance to anticancer drugs. Science (New York, NY). 1988; 241:1813-1815.
37. Pabla N, Huang S, Mi QS, Daniel R, Dong Z. ATR-Chk2 signaling in p53 activation and DNA damage response during cisplatin-induced apoptosis. J Biol Chem. 2008; 283:6572-6583.
38. Shieh SY, Ahn J, Tamai K, Taya Y, Prives C. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes & development. 2000; 14:289-300.
39. Zhao H, Piwnica-Worms H. ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol. 2001; 21:4129-4139.
40. Chiang WF, Hwang TZ, Hour TC, Wang LH, Chiu CC, Chen HR, Wu YJ, Wang CC, Wang LF, Chien CY, Chen JH, Hsu CT, Chen JY. Calreticulin, an endoplasmic reticulum-resident protein, is highly expressed and essential for cell proliferation and migration in oral squamous cell carcinoma. Oral Oncol. 2013; 49:534-541.
41. Chiu CC, Chen BH, Hour TC, Chiang WF, Wu YJ, Chen CY, Chen HR, Chan PT, Liu SY, Chen JY. Betel quid extract promotes oral cancer cell migration by activating a muscarinic M4 receptor-mediated signaling cascade involving SFKs and ERK1/2. Biochem Biophys Res Commun. 2010; 399:60-65.