Catalase protects tumor cells from apoptosis induction by intercellular ROS signaling

Anticancer Research

Volumn 29, Issue 11, 2009, Pages 4541-4557

  Bechtel, Wibke ^a,b   Bauer, Georg ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

HOCl signaling pathway; Hydrogen peroxide; Hydroxyl radical; Hypochlorous acid

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; HYDROXYL RADICAL; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIOCHEMICAL COMPOSITION; CELL DESTRUCTION; CELL MEMBRANE; CELL PROTECTION; CELL TRANSFORMATION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SYNTHESIS; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; TUMOR CELL;

ANIMALS; APOPTOSIS; CATALASE; CELL COMMUNICATION; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; COCULTURE TECHNIQUES; HUMANS; HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; MICE; NEOPLASMS; RATS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 75149195862     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. Weinberg RA: Oncogenes, Anti-oncogenes and the molecular basis of multistep carcinogenesis. Cancer Res 49: 3713-3721, 1989.
2. Hanahan D and Weinberg RA: The hallmarks of cancer. Cell 100: 57-70, 2000.
3. Vogelstein B and Kinzler KW: Cancer genes and the pathways they control. Nature Medicine 10: 789-799, 2004.
4. Temin HM: Control by factors in serum of multiplication of uninfected and cells infected and converted by avian sarcoma viruses. In: Growth Regulatory Substances for Animal Cells in Culture. Vol. 7. Defendi V and Stoker M (eds.). Philadelphia, The Wistar Symposium Monograph, Wistar Institute Press, pp. 103-116, 1967.
5. Sporn MB and Todaro GJ: Autocrine secretion and malignant transformation. New Engl J Med 303: 878-880, 1980.
6. Heldin CH and Westermark B: Growth factors as transforming proteins. Eur J Biochem 184: 487-496, 1989.
7. Stoker MGP, Shearer M and O'Neill C: Growth inhibition of polyoma-transformed cells by contact with static normal fibroblasts. J Cell Sci 1: 297-310, 1966.
8. Delinassios JG: Fibroblasts against cancer cells in vitro. Anticancer Res 7: 1005-1010, 1987.
9. Trosko JE, Chang CC, Madhukar BV and Klaunig JE: Chemical, oncogene and growth factor inhibition of gap junctional intercellular communication: an integrative hypothesis of carcinogenesis. Pathobiology 58: 265-278, 1990.
10. Barcellos-Hoff MH: It takes a tissue to make a tumor. Epigenetics, cancer and microenvironment. J Mammary Gland Biol Neoplasia 6: 213-221, 2001.
11. Deichman G, Matveeva VA, Kashkina LM, Dyakova NA, Uvarova EN, Nikiforov MA and Gudkov AV: Cell transforming genes and tumor progression: in vivo unified secondary phenotypic cell changes. Int J Cancer 75: 277-283, 1998.
12. Deichman G: Natural selection and early changes of phenotype of tumor cells in vivo: Acquisition of new defense mechanisms. Biochem (Mosc) 65: 78-94, 2000.
13. Deichman G: Early phenotypic changes of in vitro transformed cells during in vivo progression: possible role of the host innate immunity. Sem Cancer Biol 12: 317-326, 2002.
14. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW and Giaccia AJ: Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91, 1996.
15. Kinzler KW and Vogelstein B: Life (and death) in a malignant tumour. Nature 379: 19-20, 1996.
16. Bauer G: Resistance to TGF-β-induced elimination of transformed cells is required during tumor progression. Int J Oncol 6: 1227-1229, 1995.
17. Bauer G: Elimination of transformed cells by normal cells: a novel concept for the control of carcinogenesis. Histol Histopathol 11: 237-255, 1996.
18. Bauer G; Reactive oxygen and nitrogen species: efficient, selective and interactive signals during intercellular induction of apoptosis. Anticancer Res 20: 4115-4140, 2000.
19. Bauer G: Signaling and proapoptotic functions of transformed cell-derived reactive oxygen species. Prostagl Leukotri Essent Fatty Acid 66: 41-56, 2002.
20. Bauer G: Low dose radiation and intercellular induction of apoptosis: potential implications for the control of oncogenesis. Int J Radiation Biol 83: 887-902, 2007.
21. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T and Goldschmidt-Clermont PJ: Mitogenic signalling by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652, 1997.
22. Irani K and Goldschmidt-Clermont PJ: Ras, superoxide and signal transduction. Biochem Pharmacol 55: 1339-1346, 1998.
23. Suh Y-A, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK and Lambeth JD: Cell transformation by the superoxide-generating oxidase Mox1. Nature 401: 79-82, 1999.
24. Yang JQ, Li S, Domann FE, Buettner G and Oberley LW : Superoxide generation in v-Ha-ras-transduced human keratinocyte HaCaT cells. Mol. Carcinogenesis 26: 180-188, 1999.
25. Herdener M, Heigold S, Saran M and Bauer G: Target cell-derived superoxide anions cause efficiency and selectivity of intercellular induction of apoptosis. Free Radical Biol Med 29: 1260-1271, 2000.
26. Schwieger A, Bauer L, Hanusch J, Sers C, Schäfer R and Bauer G: Ras oncogene expression determines sensitivity for intercellular induction of apoptosis. Carcinogenesis 22: 1385-1392, 2001.
27. Heigold S, Sers C, Bechtel W, Ivanovas B, Schäfer R and Bauer G: Nitric oxide mediates apoptosis induction selectively in transformed fibroblasts compared to nontransformed fibroblasts. Carcinogenesis 23: 929-941, 2002.
28. Mitsushita J, Lambeth JD and Kamata T: The superoxide-generating oxidase Nox1 is functionally required for Ras oncogenic transformation. Cancer Res 64: 3580-3585, 2004.
29. Cheng G, Diebold BA, Hughes Y and Lambeth JD: Nox1-dependent reactive oxygen generation is regulated by Rac1. J Biol Chem 281: 17718-17726, 2006.
30. Arnold RS, Shi J, Murad E, Whalen AM, Sun CQ, Palavarapu R, Parthasarathy S, Petros JA and Lambeth JD: Hydrogen peroxide mediates the cell growth and transformation caused by the mitogenic oxidase Nox1. Proc Natl Acad Sci USA 98: 5550-5555, 2001.
31. Shinohara M, Shang W-H, Kubodera M, Hanada S, Mitsushita J, Kato M, Miyazaki H, Suminoto H and Kamata T: Nox1 redox signaling mediates oncogenic Ras-induced disruption of stress fibers and focal adhesions by down-regulating Rho. J Biol Chem 282: 17640-17648, 2007.
32. Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, Cohen C, Moses M, Kilroy S, Arnold RS and Lambeth JD: Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Acad Natl Acad Sci USA 99: 715-720, 2002.
33. Tominaga K, Kawahara T, Sano t, Toida K, Kuwano Y, Sasaki H and Kawai T: Evidence for cancer-associated expression of NADPH oxidase 1 (Nox1)-base oxidase system in the human stomach. Free Radical Biol Med 43: 1627-1638, 2007.
34. Laurent E, McCoy JW, Maccina RA, Liu W, Cheng GJ, Robine S, Papkoff J and Lambeth JD: Nox1 is overexpressed in human colon cancers and correlates with activating mutations in K-Ras. Int J Cancer 123: 100-107, 2008.
35. Jürgensmeier J, Schmitt CP, Viesel E, Höfler P and Bauer G: TGF-β-treated normal fibroblasts eliminate transformed fibroblasts by induction of apoptosis. Cancer Res 54: 393-398, 1994.
36. Steinebach C and Bauer G: An alternative signalling pathway based on nitryl chloride during intercellular induction of apoptosis. In vitro and applied molecular toxicology 14: 107-120, 2001.
37. Schimmel M and Bauer G: Proapoptotic and redox state-related signalling of reactive oxygen species generated by transformed fibroblasts. Oncogene 21: 5886-5896, 2002.
38. Engelmann I, Dormann S, Saran M and Bauer G: Transformed target cell-derived superoxide anions drive apoptosis induction by myeloperoxidase. Redox Report 5: 207-214, 2000.
39. Ivanovas B and Bauer G: Selective and nonselective apoptosis induction in transformed and nontransformed fibroblasts by exogenous reactive oxygen and nitrogen species. Anticancer Res 22: 841-856, 2002.
40. Long CA and Bielski BH: Rate of reaction of superoxide radical with chloride-containing species. J Phys Chem 84: 555-557, 1980.
41. Candeias LP, Patel KB, Stratford MRL and Wardmann P: Free hydroxyl radicals are formed on reaction between the neutrophil-derived species superoxide anion and hypochlorous acid. FEBS 333: 151-153, 1993.
42. Folkes LK, Candeias LP and Wardman P: Kinetics and mechanisms of hypochlorous acid reactions. Arch Biochem Biophys 323: 120-126, 1995.
43. - and NO: how far can either radical, or any specific reaction product, transmit a message under in vivo conditions? Che Biol Inter 90: 35-45, 1994.
44. Saran M, Michel C and Bors W: Radical functions in vivo: a critical review of current concepts and hypotheses. Zeitschrift für Naturforschung 53 c: 210-227, 1998.
45. Engelmann I and Bauer G: How can tumor cells escape intercellular induction of apoptosis? Anticancer Res 20: 2297-2306, 2000.
46. Engelmann I, Eichholtz-Wirth H and Bauer G: Ex vivo tumor cell lines are resistant to intercellular induction of apoptosis and independent of exogenous survival factors. Anticancer Res 20: 2361-2370, 2000.
47. Diatchuk V, Lotan O, Koshkin V, Wikstroem P and Pick E: Inhibition of NADPH oxidase activation by 4-(2-aminoethyl-) benzenesulfonyl fluoride and related compounds. J Biol Chem 272: 13292-13301, 1997.
48. Kettle AJ, Gedye CA, Hampton MB and Winterbourn CC: Inhibition of myeloperoxidase by benzoic acid hydrazides. Biochem J 308: 559-563, 1995.
49. Kettle AJ, Gedye CA and Winterbourn CC: Mechanisms of inactivation of myeloperoxidase by 4-aminobenzoic acid hydrazide. Biochem J 321: 503-508, 1997.
50. Putnam CD, Arvai AS and Bourne Y: Active and inhibited human catalase structures: Ligand and NADPH binding and catalytic mechanism. J Mol Biol 296: 295-309, 2000.
51. Goldstein S and Czapski G: Mannitol as an OH. scavenger in aqueous solutions and in biological systems. Int J Rad Biol 46: 725-729, 1984.
52. Aruoma OI, Halliwell B, Hoey BM and Butler J: The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem J 256: 251-256, 1988.
53. Klebanoff SJ: Myeloperoxidase: friend and foe. J Leucocyte Biol 77: 1-28, 2005.
54. Konorev EA, Kennedy MC and Kalyanaraman B: Cell-permeable superoxide dismutase and glutathione peroxidase mimetics afford superior protection against doxorubicin-induced cardiotoxicity: The role of reactive oxygen and nitrogen intermediates. Arch Biochem Biophys 368: 421-428, 1999.
55. Estevez AG, Sampson JB, Zhuang YX, Spear N, Richardson GJ, Crow JP, Tarpey MM, Barbeito L and Beckman JS: Liposome-delivered superoxide dismutase prevents nitric oxide-dependent motor neuron death induced by trophic factor withdrawal. Free Radical Biol Med 28: 437-446, 2000.
56. Bauer G, Höfler P and Simon M: Epstein-Barr virus induction by a serum factor II. Purification of a highmolecular weight protein that is responsible for induction. J Biol Chem 257: 11405-11410, 1982.
57. Beck E, Schäfer R and Bauer G: Sensitivity of transformed fibroblasts for intercellular induction of apoptosis is determined by their transformed phenotype. Exp Cell Res 234: 47-56, 1997.
58. Gorcyca W, Gong J and Darzynkiewicz Z: Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res 53: 1945-1951, 1993.
59. Kroemer G, Zamzami N and Susin SA: Mitochondrial control of apoptosis. Immunol Today 18: 44-51, 1997.
60. Sandstrom PA and Buttke TM: Autocrine production of extracellular catalase prevents apoptosis of the human CEM T-cell line in serum-free medium. Proc Natl Acad Sci USA 90: 4708-4712, 1993.
61. Tome ME, Baker AF, Powis G, Payne CM and Briehl MM: Catalase- overexpressing thymocytes are resistant to glucocorticoid-induced apoptosis and exhibit increased net tumor growth. Cancer Res 61: 2766-2773, 2001.
62. Moran EC, Kamiguti AS, Cawley JC and Pettitt AR: Cytoprotective antioxidant activity of serum albumin and autocrine catalase in chronic lymphatic leukaemia. Br J Haematol 116: 316-328, 2002.
63. 2-halide system: cytotoxic effect on mammalian tumor cells. Blood 45: 161-170, 1975.
64. Clark RA and Klebanoff SJ: Neutrophil-mediated tumor cell cytotxicity - role of peroxidase system. J Exp Med 141: 1442-1447, 1975.
65. 2-halide system in concanavalin A-induced tumor cell killing by human neutrophils. J Immunol 122: 2605-2610, 1979.
66. Clark RA and Szot S: The myeloperoxidase-hydrogen peroxide-halide system as effector of neutrophil-mediated tumor-cell cytotxicity. J Immunol 126: 1295-1301, 1981.
67. Okajima T, Onishi M, Hayama E, Motoji N and Momose Y: Cytolysis of B-16 melanoma tumor cells mediated by the myeloperoxidase and lactoperoxidase systems. Biol Chem 377: 689-693, 1996.
68. Weiss SJ and Slivka A: Monocyte and granulocyte-mediated tumor cell destruction. A role for the hydrogen peroxidase-myeloperoxidase-chloride system. J Clin Invest 69: 255-262, 1982.
69. Wagner BA, Britigan BE, ReszkaKJ, McCormick ML and Burns CP: Hydrogen peroxide-induced apoptosis of HL-60 human leukemia cells is mediated by the oxidants hypochlorous acid and chloramines. Arch Biochem Biophys 401: 223-234, 2002.
70. Ottaviano FG, Handy DE and Loscalzo J: Redox regulation in the extracellular environment. Cir J 72: 1-16, 2008.
71. Jang JH and Hanah S: Profiling of the cell surface proteome. Proteomics 3: 1947-1954, 2003.
72. Gupta A, Butts B, Kwei KA, Dvorakova K, Stratton SP, Briehl MM and Bowden GT: Attenuation of catalase activity in the malignant phenotype plays a functional role in an in vitro model for tumor progression. Cancer Lett 173: 115-125, 2001.
73. Finch JS, Tome ME, Kwei KA and Bowden GT: Catalase reverses tumorigenicity in a malignant cell line by an epidermal growth factor receptor pathway. Free Radical Biol Med 40: 863-875, 2006.
74. Ho JCM, Zheng S, Comhair SAA, Farver C and Erzurum SC: Differential expression of manganese superoxide dismutase and catalase in lung cancer. Cancer Res 61: 8578-8585, 2001.