Reactive oxygen species activation of MAPK pathway results in VEGF upregulation as an undesired irradiation response

Journal of Oral Pathology and Medicine

Volumn 42, Issue 8, 2013, Pages 612-619

  Drigotas, Martynas ^a   Affolter, Annette ^a,b   Mann, Wolf J ^a   Brieger, Juergen ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Head and neck squamous cell carcinoma; Irradiation; MAP kinase pathway; Reactive oxygen species; Vascular endothelial growth factor

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; VASCULOTROPIN;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HEAD AND NECK SQUAMOUS CELL CARCINOMA; IMMUNOHISTOCHEMISTRY; INTRACELLULAR MEMBRANE; IRRADIATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIATION DOSE; RADIATION EXPOSURE; RADIATION RESPONSE; STIMULATION; UPREGULATION; WESTERN BLOTTING;

HEAD AND NECK SQUAMOUS CELL CARCINOMA; IRRADIATION; MAP KINASE PATHWAY; REACTIVE OXYGEN SPECIES; VASCULAR ENDOTHELIAL GROWTH FACTOR;

BLOTTING, WESTERN; BUTADIENES; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CYTOPROTECTION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME INHIBITORS; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; HYDROGEN PEROXIDE; IMMUNOHISTOCHEMISTRY; MAP KINASE SIGNALING SYSTEM; NITRILES; RADIATION TOLERANCE; REACTIVE OXYGEN SPECIES; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84883556737     PISSN: 09042512     EISSN: 16000714     Source Type: Journal    
DOI: 10.1111/jop.12056     Document Type: Article

References (48)

1. Balfour A, Rhys Evans PH, Patel SG. Head and neck malignancy: an overview. In: Montgomery PQ, Rhys Evans PH, Gullane PJ, eds. Principles and Practice of Head and Neck Surgery and Oncology, 2nd edn. New York: Informa Healthcare, 2009; 1-13.
2. Grant S, Qiao L, Dent P. Roles of ERBB family receptor tyrosine kinases, and downstream signaling pathways, in the control for cell growth and survival. Front Biosci 2002; 7: 376-89.
3. Schmidt-Ullrich RK, Dent P, Grant S, Mikkelsen RB, Valerie K. Signal transduction and cellular radiation responses. Radiat Res 2000; 153: 245-57.
4. Liou GY, Storz P. Reactive oxygen species in cancer. Free Radic Res 2010; 44: 479-96.
5. Klaunig JE, Kamendulis LM. The role of oxidative stress in carcinogenesis. Annu Rev Pharmacol Toxicol 2004; 44: 239-67.
6. Han D, Williams E, Cadenas E. Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space. Biochem J 2001; 353: 411-6.
7. Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 2002; 9: 387-99.
8. Kamata H, Honda SI, Maeda S, Chang L, Hirata H, Karin M. Reactive oxygen species promote TNFα-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases. Cell 2005; 120: 649-61.
9. Hou N, Torii S, Saito N, Hosaka M, Takeuchi T. Reactive oxygen species-mediated pancreatic β-cell death is regulated by interactions between stress-activated protein kinases, p38 and c-jun N-terminal kinase, and mitogen-activated protein kinase phosphatases. Endocrinology 2008; 149: 1654-65.
10. Zhou JY, Liu Y, Gen SW. The role of mitogen-activated protein kinase phosphatase-1 in oxidative damage-induced cell death. Cancer Res 2006; 66: 4888-94.
11. McCubrey JA, Steelman LS, Chappell WH, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 2007; 1773: 1263-84.
12. Whisler RL, Goyette MA, Grants IS, Newhouse YG. Sublethal levels of oxidant stress stimulate multiple serine/threonine kinases and suppress protein phosphatases in Jurkat T cells. Arch Biochem Biophys 1995; 319: 23-35.
13. Rao RK, Clayton LW. Regulation of protein phosphatase 2A by hydrogen peroxide and glutathionylation. Biochem Biophys Res Commun 2002; 293: 610-6.
14. Lee K, Esselman WJ. Inhibition of PTPs by H(2)O(2) regulates the activation of distinct MAPK pathways. Free Radical Biol Med 2002; 33: 1121-32.
15. Knebel A, Rahmsdorf HJ, Ullrich A, Herrlich P. Dephosphorylation of receptor tyrosine kinases as target of regulation by radiation, oxidants or alkylating agents. EMBO J 1996; 15: 5314-25.
16. Affolter A, Fruth K, Brochhausen C, Schmidtmann I, Mann WJ, Brieger J. Activation of mitogen-activated protein kinase extracellular signal-related kinase in head and neck squamous cell carcinomas after irradiation as part of a rescue mechanism. Head Neck 2011; 33: 1448-57.
17. Affolter A, Drigotas M, Fruth K, et al. Increased radioresistance via G12S K-Ras by compensatory upregulation of MAPK and PI3K pathways in epithelial cancer. Head Neck 2013; 35: 220-8.
18. Brieger J, Schroeder P, Gosepath J, Mann WJ. VEGF-subtype specific protection of SCC and HUVECs from radiation induced cell death. Int J Mol Med 2005; 15: 145-51.
19. Brieger J, Schroeder P, Gosepath J, Mann WJ. Vascular endothelial growth factor and basic fibroblast growth factor are released by squamous cell carcinoma cells after irradiation and increase resistance to subsequent irradiation. Int J Mol Med 2005; 16: 159-64.
20. Welkoborsky HJ, Jacob R, Riazimand SH, Bernauer HS, Mann WJ. Molecular biologic characteristics of seven new cell lines of squamous cell carcinomas of the head and neck and comparison to fresh tumor tissue. Oncol Rep 2003; 65: 60-71.
21. Nichikawa R, Cheng SV, Nagashima R, Huang HJ, Cavenee WK, Matsutani M. Expression if vascular endothelial growth factor in human brain tumors. Acta Neuropathol 1998; 96: 453-62.
22. Plate KH, Breier G, Weich HA, Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992; 359: 845-8.
23. Brown LF, Berse B, Jackman RW, et al. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in adenocarcinomas of the gastrointestinal tract. Cancer Res 1993; 53: 4727-35.
24. Brown LF, Berse B, Jackman RW, et al. Increased expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in kidney and bladder carcinomas. Am J Pathol 1993; 143: 1255-62.
25. Brown LF, Berse B, Jackman RW, et al. Expression of vascular permeability factor (vascular endothelial growth factor) and its receptors in breast cancer. Hum Pathol 1995; 26: 86-91.
26. Brieger J, Weidt EJ, Schirmacher P, Störkel S, Huber C, Decker HJ. Inverse regulation of vascular endothelial growth factor and VHL tumor suppressor gene in sporadic renal cell carcinomas is correlated with vascular growth: an in vivo study on 29 tumors. J Mol Med (Berl) 1999; 77: 505-10.
27. Ferrara N, Houck KA, Jakeman LB, Winer J, Leung DW. The vascular endothelial growth factor family of polypeptides.J Cell Biochem 1991; 47: 211-8.
28. Brieger J, Kattwinkel J, Berres M, Gosepath J, Mann WJ. Impact of vascular endothelial growth factor release on radiation resistance. Oncol Rep 2007; 18: 1597-601.
29. Gorski DH, Beckett MA, Jaskowiak NT, et al. Blockage of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res 1999; 59: 3374-8.
30. Ushio-Fukai M, Alexander RW. Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase. Mol Cell Biochem 2004; 264: 85-97.
31. Ushio-Fukai M, Nakamura Y. Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett 2008; 266: 37-52.
32. Simon HU, Haj-Yehia A, Levi-Schaffer F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 2000; 5: 415-8.
33. Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology 2000; 7: 153-63.
34. Davis W Jr, Ronai Z, Tew KD. Cellular thiols and reactive oxygen species in drug-induced apoptosis. J Pharmacol Exp Ther 2001; 296: 1-6.
35. Clément MV, Stamenkovic I. Superoxide anion is a natural inhibitor of FAS-mediated cell death. EMBO J 1996; 15: 216-25.
36. Lin KI, Pasinelli P, Brown RH, Hardwick JM, Ratan RR. Decreased intracellular superoxide levels activate Sindbis virus-induced apoptosis. J Biol Chem 1999; 274: 13650-5.
37. Brar SS, Corbin Z, Kennedy TP, et al. NOX5 NAD(P)H oxidase regulates growth and apoptosis in DU 145 prostate cancer cells. Am J Physiol 2003; 285: C353-69.
38. Green DR. Death and NF-kappaB in T cell activation: life at the edge. Mol Cell 2003; 11: 551-2.
39. Garrido C, Gurbuxani S, Ravagnan L, Kroemer G. Heat shock proteins: endogenous modulators of apoptotic cell death. Biochem Biophys Res Commun 2001; 286: 433-42.
40. Gupta A, Bhatt ML, Misra MK. Assessment of free radical-mediated damage in head and neck squamous cell carcinoma patients and after treatment with radiotherapy. Indian J Biochem Biophys 2010; 47: 96-9.
41. Inci F, Korkut N, Inci E, et al. Laryngeal cancer: in relation to oxidative stress. Tohoku J Exp Med 2003; 200: 17-23.
42. Pervaiz S, Clement MV. Tumor intracellular redox status and drug resistance - serendipity or a causal relationship? Curr Pharm Des 2004; 10: 1969-77.
43. Bionda C, Hadchity E, Alphonse G, et al. Radioresistance of human carcinoma cells is correlated to a defect in raft membrane clustering. Free Radic Biol Med 2007; 43: 681-94.
44. Martin KR, Barrett JC. Reactive oxygen species as double-edged swords in cellular processes: low-dose cell signaling versus high-dose toxicity. Hum Exp Toxicol 2002; 21: 71-5.
45. Son Y, Cheong YK, Kim NH, Chung HT, Kang DG, Pae HO. Mitogen-activated protein kinases and reactive oxygen species: How can ROS activate MAPK pathways? J Signal Transduct 2011; 792639.
46. Liu SL, Lin X, Shi DY, Cheng J, Wu CQ, Zhang YD. Reactive oxygen species stimulated human hepatoma cell proliferation via cross talk between PI3-K/PKB and JNK signaling pathways. Arch Biochem Biophys 2002; 406: 173-82.
47. Wang XT, McCullough KD, Wang XJ, Carpenter G, Holbrook NJ. Oxidative stress-induced phospholipase C-gamma 1 activation enhances cell survival. J Biol Chem 2001; 276: 28364-71.
48. Zou Y, Komuro I, Yamazaki T, et al. Protein kinase C, but not tyrosine kinases or Ras, plays a critical role in angiotensin II-induced activation of Raf-1 kinase and extracellular signal-regulated protein kinases in cardiac myocytes. J Biol Chem 1996; 271: 33592-7.