NADPH oxidase subunit p22phox-mediated reactive oxygen species contribute to angiogenesis and tumor growth through AKT and ERK1/2 signaling pathways in prostate cancer

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 12, 2013, Pages 3375-3385

  Li, Qi ^a   Fu, Guang Bo ^b   Zheng, Ji Tai ^a   He, Jun ^e   Niu, Xiao Bing ^b   Chen, Qiu Dan ^a   Yin, Yu ^a,c   Qian, Xu ^a   Xu, Qing ^a   Wang, Min ^a   Sun, An Fang ^b   Shu, Yongqian ^d   Rui, Hallgeir ^e   Liu, Ling Zhi ^e   Jiang, Bing Hua ^a,e  

^a Nanjing Medical University   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c ANHUI MEDICAL UNIVERSITY   (China)

^d THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Angiogenesis; P22phox; Prostate cancer; ROS; Tumor growth

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; TUMOR GROWTH;

EID: 84886843534     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.09.018     Document Type: Article

References (53)

1. Gueye S.M., Zeigler-Johnson C.M., Friebel T., Spangler E., Jalloh M., MacBride S., Malkowicz S.B., Rebbeck T.R. Clinical characteristics of prostate cancer in African Americans, American whites, and Senegalese men. Urology 2003, 61:987-992.
2. Singh B.R., Singh B.N., Khan W., Singh H.B., Naqvi A.H. ROS-mediated apoptotic cell death in prostate cancer LNCaP cells induced by biosurfactant stabilized CdS quantum dots. Biomaterials 2012, 33:5753-5767.
3. Xiao D., Powolny A.A., Moura M.B., Kelley E.E., Bommareddy A., Kim S.H., Hahm E.R., Normolle D., Van Houten B., Singh S.V. Phenethyl isothiocyanate inhibits oxidative phosphorylation to trigger reactive oxygen species-mediated death of human prostate cancer cells. J. Biol. Chem. 2010, 285:26558-26569.
4. Dolado I., Swat A., Ajenjo N., De Vita G., Cuadrado A., Nebreda A.R. p38alpha MAP kinase as a sensor of reactive oxygen species in tumorigenesis. Cancer Cell 2007, 11:191-205.
5. He J., Xu Q., Jing Y., Agani F., Qian X., Carpenter R., Li Q., Wang X.R., Peiper S.S., Lu Z., Liu L.Z., Jiang B.H. Reactive oxygen species regulate ERBB2 and ERBB3 expression via miR-199a/125b and DNA methylation. EMBO Rep. 2012, 13:1116-1122.
6. Xia C., Meng Q., Liu L.Z., Rojanasakul Y., Wang X.R., Jiang B.H. Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res. 2007, 67:10823-10830.
7. Arnold R.S., Shi J., Murad E., Whalen A.M., Sun C.Q., Polavarapu R., Parthasarathy S., Petros J.A., Lambeth J.D. Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase NOX1. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5550-5555.
8. Ralph S.J., Rodriguez-Enriquez S., Neuzil J., Saavedra E., Moreno-Sanchez R. The causes of cancer revisited: "mitochondrial malignancy" and ROS-induced oncogenic transformation-why mitochondria are targets for cancer therapy. Mol. Aspects Med. 2010, 31:145-170.
9. Singh K.K. Mitochondria damage checkpoint, aging, and cancer. Ann. N. Y. Acad. Sci. 2006, 1067:182-190.
10. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 2007, 87:245-313.
11. Sakuma S., Negoro M., Kitamura T., Fujimoto Y. Xanthine oxidase-derived reactive oxygen species mediate 4-oxo-2-nonenal-induced hepatocyte cell death. Toxicol. Appl. Pharmacol. 2010, 249:127-131.
12. Drummond G.R., Selemidis S., Griendling K.K., Sobey C.G. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nat. Rev. Drug Discov. 2011, 10:453-471.
13. Block K., Gorin Y. Aiding and abetting roles of NOX oxidases in cellular transformation. Nat. Rev. Cancer 2012, 12:627-637.
14. Datla S.R., Peshavariya H., Dusting G.J., Mahadev K., Goldstein B.J., Jiang F. Important role of NOX4 type NADPH oxidase in angiogenic responses in human microvascular endothelial cells in vitro. Arterioscler. Thromb. Vasc. Biol. 2007, 27:2319-2324.
15. Yamaura M., Mitsushita J., Furuta S., Kiniwa Y., Ashida A., Goto Y., Shang W.H., Kubodera M., Kato M., Takata M., Saida T., Kamata T. NADPH oxidase 4 contributes to transformation phenotype of melanoma cells by regulating G2-M cell cycle progression. Cancer Res. 2009, 69:2647-2654.
16. Brar S.S., Kennedy T.P., Sturrock A.B., Huecksteadt T.P., Quinn M.T., Whorton A.R., Hoidal J.R. An NAD(P)H oxidase regulates growth and transcription in melanoma cells. Am. J. Physiol. Cell Physiol. 2002, 282:C1212-C1224.
17. Arbiser J.L., Petros J., Klafter R., Govindajaran B., McLaughlin E.R., Brown L.F., Cohen C., Moses M., Kilroy S., Arnold R.S., Lambeth J.D. Reactive oxygen generated by NOX1 triggers the angiogenic switch. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:715-720.
18. 2 and plays an integral role in insulin signal transduction. Mol. Cell. Biol. 2004, 24:1844-1854.
19. Mesquita F.S., Dyer S.N., Heinrich D.A., Bulun S.E., Marsh E.E., Nowak R.A. Reactive oxygen species mediate mitogenic growth factor signaling pathways in human leiomyoma smooth muscle cells. Biol. Reprod. 2010, 82:341-351.
20. Lee J.K., Edderkaoui M., Truong P., Ohno I., Jang K.T., Berti A., Pandol S.J., Gukovskaya A.S. NADPH oxidase promotes pancreatic cancer cell survival via inhibiting JAK2 dephosphorylation by tyrosine phosphatases. Gastroenterology 2007, 133:1637-1648.
21. Naughton R., Quiney C., Turner S.D., Cotter T.G. Bcr-Abl-mediated redox regulation of the PI3K/AKT pathway. Leukemia 2009, 23:1432-1440.
22. Block K., Gorin Y., New D.D., Eid A., Chelmicki T., Reed A., Choudhury G.G., Parekh D.J., Abboud H.E. The NADPH oxidase subunit p22phox inhibits the function of the tumor suppressor protein tuberin. Am. J. Pathol. 2010, 176:2447-2455.
23. Caillou B., Talbot M., Weyemi U., Pioche-Durieu C., Al Ghuzlan A., Bidart J.M., Chouaib S., Schlumberger M., Dupuy C. Tumor-associated macrophages (TAMs) form an interconnected cellular supportive network in anaplastic thyroid carcinoma. PLoS One 2011, 6:e22567.
24. Folkman J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 1971, 285:1182-1186.
25. Nicholson B., Theodorescu D. Angiogenesis and prostate cancer tumor growth. J. Cell. Biochem. 2004, 91:125-150.
26. Xu Q., Liu L.Z., Qian X., Chen Q., Jiang Y., Li D., Lai L., Jiang B.H. MiR-145 directly targets p70S6K1 in cancer cells to inhibit tumor growth and angiogenesis. Nucleic Acids Res. 2011.
27. Zhang C., Hao L., Wang L., Xiao Y., Ge H., Zhu Z., Luo Y., Zhang Y. Elevated IGFIR expression regulating VEGF and VEGF-C predicts lymph node metastasis in human colorectal cancer. BMC Cancer 2010, 10:184.
28. Soumaoro L.T., Uetake H., Higuchi T., Takagi Y., Enomoto M., Sugihara K. Cyclooxygenase-2 expression: a significant prognostic indicator for patients with colorectal cancer. Clin. Cancer. Res. 2004, 10:8465-8471.
29. Rajkumar S.V., Leong T., Roche P.C., Fonseca R., Dispenzieri A., Lacy M.Q., Lust J.A., Witzig T.E., Kyle R.A., Gertz M.A., Greipp P.R. Prognostic value of bone marrow angiogenesis in multiple myeloma. Clin. Cancer Res. 2000, 6:3111-3116.
30. Weidner N., Semple J.P., Welch W.R., Folkman J. Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N. Engl. J. Med. 1991, 324:1-8.
31. Zhou Q., Liu L.Z., Fu B., Hu X., Shi X., Fang J., Jiang B.H. Reactive oxygen species regulate insulin-induced VEGF and HIF-1alpha expression through the activation of p70S6K1 in human prostate cancer cells. Carcinogenesis 2007, 28:28-37.
32. Meng Q., Xia C., Fang J., Rojanasakul Y., Jiang B.H. Role of PI3K and AKT specific isoforms in ovarian cancer cell migration, invasion and proliferation through the p70S6K1 pathway. Cell. Signal. 2006, 18:2262-2271.
33. Huynh N., Liu K.H., Baldwin G.S., He H. P21-activated kinase 1 stimulates colon cancer cell growth and migration/invasion via ERK- and AKT-dependent pathways. Biochim. Biophys. Acta 2010, 1803:1106-1113.
34. Meng D., Shi X., Jiang B.H., Fang J. Insulin-like growth factor-I (IGF-I) induces epidermal growth factor receptor transactivation and cell proliferation through reactive oxygen species. Free Radic. Biol. Med. 2007, 42:1651-1660.
35. Shi Y.H., Wang Y.X., Bingle L., Gong L.H., Heng W.J., Li Y., Fang W.G. In vitro study of HIF-1 activation and VEGF release by bFGF in the T47D breast cancer cell line under normoxic conditions: involvement of PI-3K/Akt and MEK1/ERK pathways. J. Pathol. 2005, 205:530-536.
36. Lim S.D., Sun C., Lambeth J.D., Marshall F., Amin M., Chung L., Petros J.A., Arnold R.S. Increased NOX1 and hydrogen peroxide in prostate cancer. Prostate 2005, 62:200-207.
37. Plate K.H., Breier G., Weich H.A., Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992, 359:845-848.
38. Leung D.W., Cachianes G., Kuang W.J., Goeddel D.V., Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 1989, 246:1306-1309.
39. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 1996, 16:4604-4613.
40. Franco R., Schoneveld O., Georgakilas A.G., Panayiotidis M.I. Oxidative stress, DNA methylation and carcinogenesis. Cancer Lett. 2008, 266:6-11.
41. Komatsu D., Kato M., Nakayama J., Miyagawa S., Kamata T. NADPH oxidase 1 plays a critical mediating role in oncogenic Ras-induced vascular endothelial growth factor expression. Oncogene 2008, 27:4724-4732.
42. Nogueira V., Park Y., Chen C.C., Xu P.Z., Chen M.L., Tonic I., Unterman T., Hay N. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 2008, 14:458-470.
43. Kumar B., Koul S., Khandrika L., Meacham R.B., Koul H.K. Oxidative stress is inherent in prostate cancer cells and is required for aggressive phenotype. Cancer Res. 2008, 68:1777-1785.
44. Brown E.J., Albers M.W., Shin T.B., Ichikawa K., Keith C.T., Lane W.S., Schreiber S.L. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 1994, 369:756-758.
45. Dennis P.B., Jaeschke A., Saitoh M., Fowler B., Kozma S.C., Thomas G. Mammalian TOR: a homeostatic ATP sensor. Science 2001, 294:1102-1105.
46. Dufner A., Thomas G. Ribosomal S6 kinase signaling and the control of translation. Exp. Cell Res. 1999, 253:100-109.
47. Calvino E., Estan M.C., Simon G.P., Sancho P., Boyano-Adanez Mdel C., de Blas E., Breard J., Aller P. Increased apoptotic efficacy of lonidamine plus arsenic trioxide combination in human leukemia cells. Reactive oxygen species generation and defensive protein kinase (MEK/ERK, Akt/mTOR) modulation. Biochem. Pharmacol. 2011, 82:1619-1629.
48. Bodine S.C., Stitt T.N., Gonzalez M., Kline W.O., Stover G.L., Bauerlein R., Zlotchenko E., Scrimgeour A., Lawrence J.C., Glass D.J., Yancopoulos G.D. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001, 3:1014-1019.
49. Ma L., Chen Z., Erdjument-Bromage H., Tempst P., Pandolfi P.P. Phosphorylation and functional inactivation of TSC2 by ERK implications for tuberous sclerosis and cancer pathogenesis. Cell 2005, 121:179-193.
50. Maehama T., Dixon J.E. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 1998, 273:13375-13378.
51. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr. Opin. Cell Biol. 1998, 10:262-267.
52. Engelman J.A., Luo J., Cantley L.C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 2006, 7:606-619.
53. Bastola D.R., Pahwa G.S., Lin M.F., Cheng P.W. Downregulation of PTEN/MMAC/TEP1 expression in human prostate cancer cell line DU145 by growth stimuli. Mol. Cell. Biochem. 2002, 236:75-81.