NOX4 promotes non-small cell lung cancer cell proliferation and metastasis through positive feedback regulation of PI3K/Akt signaling

Oncotarget

Volumn 5, Issue 12, 2014, Pages 4392-4405

  Zhang, Cuixiang ^a,b   Lan, Tian ^c   Hou, Jincai ^a,b   Li, Juan ^c   Fang, Rende ^c   Yang, Zhicheng ^c   Zhang, Min ^c   Liu, Jianxun ^a,b   Liu, Bing ^c  

^a XIYUAN HOSPITAL   (China)

^b Beijing Key Laboratory of Pharmacology of Chinese Materia Medica   (China)

^c GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Metastasis; Non small cell lung cancer; NOX4; PI3K Akt signaling; Proliferation

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; NOX4 PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LUNG CARCINOGENESIS; LUNG METASTASIS; LUNG NON SMALL CELL CANCER; MAJOR CLINICAL STUDY; MALE; METASTASIS POTENTIAL; MOUSE; NONHUMAN; OVERALL SURVIVAL; POSITIVE FEEDBACK; PROTEIN FUNCTION; SURVIVAL PREDICTION; SURVIVAL TIME; TUMOR INVASION; TUMOR VOLUME; UPREGULATION; GENETIC TRANSFECTION; GENETICS; LUNG TUMOR; METABOLISM; MIDDLE AGED; NON SMALL CELL LUNG CANCER; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; LUNG NEOPLASMS; MALE; MIDDLE AGED; NADPH OXIDASE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84905080566     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.2025     Document Type: Article

References (34)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin. 2011; 61: 212-236.
2. Molina JR, Yang P, Cassivi SD, Schild SE, Adjei AA. Non-small cell lung cancer: epidemiology, risk factors, treatment, and survivorship. Mayo Clin Proc. 2008; 83: 584-594.
3. Schiller JH, Harrington D, Belani CP, Langer C, Sandler A, Krook J, Zhu J, Johnson DH. Comparison of four chemotherapy regimens for advanced non-small-cell lung cancer. N Engl J Med. 2002; 346: 92-98.
4. Cheng G, Cao Z, Xu X, van Meir EG, Lambeth JD. Homologs of gp91phox: cloning and tissue expression of Nox3, Nox4, and Nox5. Gene. 2001; 269: 131-140.
5. Altenhofer S, Kleikers PW, Radermacher KA, Scheurer P, Rob Hermans JJ, Schiffers P, Ho H, Wingler K, Schmidt HH. The NOX toolbox: validating the role of NADPH oxidases in physiology and disease. Cell Mol Life Sci. 2012; 69: 2327-2343.
6. Gaggini F, Laleu B, Orchard M, Fioraso-Cartier L, Cagnon L, Houngninou-Molango S, Gradia A, Duboux G, Merlot C, Heitz F, Szyndralewiez C, Page P. Design, synthesis and biological activity of original pyrazolo-pyrido-diazepine,-pyrazine and-oxazine dione derivatives as novel dual Nox4/Nox1 inhibitors. Bioorg Med Chem. 2011; 19: 6989-6999.
7. Bhandarkar SS, Jaconi M, Fried LE, Bonner MY, Lefkove B, Govindarajan B, Perry BN, Parhar R, Mackelfresh J, Sohn A, Stouffs M, Knaus U, Yancopoulos G, Reiss Y, Benest AV, Augustin HG, et al. Fulvene-5 potently inhibits NADPH oxidase 4 and blocks the growth of endothelial tumors in mice. J Clin Invest. 2009; 119: 2359-2365.
8. Brar SS, Corbin Z, Kennedy TP, Hemendinger R, Thornton L, Bommarius B, Arnold RS, Whorton AR, Sturrock AB, Huecksteadt TP, Quinn MT, Krenitsky K, Ardie KG, Lambeth JD, Hoidal JR. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am J Physiol Cell Physiol. 2003; 285: C353-369.
9. Chen J, Liu B, Yuan J, Yang J, Zhang J, An Y, Tie L, Pan Y, Li X. Atorvastatin reduces vascular endothelial growth factor (VEGF) expression in human non-small cell lung carcinomas (NSCLCs) via inhibition of reactive oxygen species (ROS) production. Mol Oncol. 2012; 6: 62-72.
10. Liu F, Gomez Garcia AM, Meyskens FL Jr. NADPH oxidase 1 overexpression enhances invasion via matrix metalloproteinase-2 and epithelial-mesenchymal transition in melanoma cells. J Invest Dermatol. 2012; 132: 2033-2041.
11. Jajoo S, Mukherjea D, Watabe K, Ramkumar V. Adenosine A(3) receptor suppresses prostate cancer metastasis by inhibiting NADPH oxidase activity. Neoplasia. 2009; 11: 1132-1145.
12. Shono T, Yokoyama N, Uesaka T, Kuroda J, Takeya R, Yamasaki T, Amano T, Mizoguchi M, Suzuki SO, Niiro H, Miyamoto K, Akashi K, Iwaki T, Sumimoto H, Sasaki T. Enhanced expression of NADPH oxidase Nox4 in human gliomas and its roles in cell proliferation and survival. Int J Cancer. 2008; 123: 787-792.
13. Vaquero EC, Edderkaoui M, Pandol SJ, Gukovsky I, Gukovskaya AS. Reactive oxygen species produced by NAD(P)H oxidase inhibit apoptosis in pancreatic cancer cells. J Biol Chem. 2004; 279: 34643-34654.
14. Fitzgerald JP, Nayak B, Shanmugasundaram K, Friedrichs W, Sudarshan S, Eid AA, DeNapoli T, Parekh DJ, Gorin Y, Block K. Nox4 mediates renal cell carcinoma cell invasion through hypoxia-induced interleukin 6-and 8-production. PLoS One. 2012; 7: e30712.
15. Goyal P, Weissmann N, Rose F, Grimminger F, Schafers HJ, Seeger W, Hänze J. Identification of novel Nox4 splice variants with impact on ROS levels in A549 cells. Biochem Biophys Res Commun. 2005; 329: 32-39.
16. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, Wu H, Kornblum HI. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell. 2011; 8: 59-71.
17. Mochizuki T, Furuta S, Mitsushita J, Shang WH, Ito M, Yokoo Y, Yamaura M, Ishizone S, Nakayama J, Konagai A, Hirose K, Kiyosawa K, Kamata T. Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene. 2006; 25: 3699-3707.
18. Wu RF, Ma Z, Liu Z, Terada LS. Nox4-derived H2O2 mediates endoplasmic reticulum signaling through local Ras activation. Mol Cell Biol. 2010; 30: 3553-3568.
19. Fresno Vara JA, Casado E, de Castro J, Cejas P, Belda-Iniesta C, González-Barón M. PI3K/Akt signalling pathway and cancer. Cancer Treat Rev. 2004; 30: 193-204.
20. Cappuzzo F, Magrini E, Ceresoli GL, Bartolini S, Rossi E, Ludovini V, Gregorc V, Ligorio C, Cancellieri A, Damiani S, Spreafico A, Paties CT, Lombardo L, Calandri C, Bellezza G, Tonato M, et al. Akt phosphorylation and gefitinib efficacy in patients with advanced non-small-cell lung cancer. J Natl Cancer Inst. 2004; 96: 1133-1141.
21. Dwamena BA, Sonnad SS, Angobaldo JO, Wahl RL. Metastases from non-small cell lung cancer: mediastinal staging in the 1990s--meta-analytic comparison of PET and CT. Radiology. 1999; 213: 530-536.
22. Birim O, Kappetein AP, Stijnen T, Bogers AJ. Meta-analysis of positron emission tomographic and computed tomographic imaging in detecting mediastinal lymph node metastases in nonsmall cell lung cancer. Ann Thorac Surg. 2005; 79: 375-382.
23. Kim YK, Lee KS, Kim BT, Choi JY, Kim H, Kwon OJ, Shim YM, Yi CA, Kim HY, Chung MJ. Mediastinal nodal staging of nonsmall cell lung cancer using integrated 18F-FDG PET/CT in a tuberculosis-endemic country: diagnostic efficacy in 674 patients. Cancer. 2007; 109: 1068-1077.
24. Lee JK, Edderkaoui M, Truong P, Ohno I, Jang KT, Berti A, Pandol SJ, Gukovskaya AS. NADPH oxidase promotes pancreatic cancer cell survival via inhibiting JAK2 dephosphorylation by tyrosine phosphatases. Gastroenterology. 2007; 133: 1637-1648.
25. Gorin Y, Ricono JM, Kim NH, Bhandari B, Choudhury GG, Abboud HE. Nox4 mediates angiotensin II-induced activation of Akt/protein kinase B in mesangial cells. Am J Physiol Renal Physiol. 2003; 285: F219-229.
26. New DD, Block K, Bhandhari B, Gorin Y, Abboud HE. IGF-I increases the expression of fibronectin by Nox4-dependent Akt phosphorylation in renal tubular epithelial cells. Am J Physiol Cell Physiol. 2012; 302: C122-130.
27. Ngkelo A, Meja K, Yeadon M, Adcock I, Kirkham PA. LPS induced inflammatory responses in human peripheral blood mononuclear cells is mediated through NOX4 and Gialpha dependent PI-3kinase signalling. J Inflamm (Lond). 2012; 9: 1.
28. Pattillo CB, Pardue S, Shen X, Fang K, Langston W, Jourd'heuil D, Kavanagh TJ, Patel RP, Kevil CG. ICAM-1 cytoplasmic tail regulates endothelial glutathione synthesis through a NOX4/PI3-kinase-dependent pathway. Free Radic Biol Med. 2010; 49: 1119-1128.
29. Wu KL, Wu CA, Wu CW, Chan SH, Chang AY, Chan JY. Redox-sensitive oxidation and phosphorylation of PTEN contribute to enhanced activation of PI3K/Akt signaling in rostral ventrolateral medulla and neurogenic hypertension in spontaneously hypertensive rats. Antioxid Redox Signal. 2013; 18: 36-50.
30. Zeng SY, Chen X, Chen SR, Li Q, Wang YH, Zou J, Cao WW, Luo JN, Gao H, Liu PQ. Upregulation of Nox4 promotes angiotensin II-induced epidermal growth factor receptor activation and subsequent cardiac hypertrophy by increasing ADAM17 expression. Can J Cardiol. 2013; 29: 1310-1319.
31. Hilenski LL, Clempus RE, Quinn MT, Lambeth JD, Griendling KK. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004; 24: 677-683.
32. Chen K, Kirber MT, Xiao H, Yang Y, Keaney JF Jr. Regulation of ROS signal transduction by NADPH oxidase 4 localization. J Cell Biol. 2008; 181: 1129-1139.
33. Engelman JA. Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat Rev Cancer. 2009; 9: 550-562.
34. Liu B, Wang G, Yang J, Pan X, Yang Z, Zang L. Berberine inhibits human hepatoma cell invasion without cytotoxicity in healthy hepatocytes. PLoS One. 2011; 6: e21416.