Interferon-gamma induced cell death: Regulation and contributions of nitric oxide, cJun N-terminal kinase, reactive oxygen species and peroxynitrite

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 11, 2014, Pages 2645-2661

  Rakshit, Srabanti ^a   Chandrasekar, Bhagawat S ^a   Saha, Banishree ^a   Victor, Emmanuel S ^a   Majumdar, Shamik ^a   Nandi, Dipankar ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

Cell death; Free radical; Interferon gamma; Mitogen activated protein kinase; Nitrosative stress; Oxidative stress

Indexed keywords

3 NITROTYROSINE; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NITRIC OXIDE; PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CARCINOMA CELL LINE; CONTROLLED STUDY; ENZYME ACTIVATION; FIBROSARCOMA CELL LINE; HEPATOMA CELL; IMMUNOREGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TUMOR CELL LINE; UPREGULATION;

EID: 84905668374     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.06.014     Document Type: Article

References (50)

1. Boehm U., Klamp T., Groot M., Howard J.C. Cellular responses to interferon-γ. Annu. Rev. Immunol. 1997, 15:749-795.
2. Schroder K., Hertzog P.J., Ravasi T., Hume D.A. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004, 75:163-189.
3. Miller C.H., Maher S.G., Young H.A. Clinical use of interferon-gamma. Ann. N. Y. Acad. Sci. 2009, 1182:69-79.
4. Saha B., Prasanna S.J., Chandrasekar B., Nandi D. Gene modulation and immunoregulatory roles of interferon gamma. Cytokine 2010, 50:1-14.
5. Taniguchi K., Petersson M., Höglund P., Kiessling R., Klein G., Kärre K. Interferon gamma induces lung colonization by intravenously inoculated B16 melanoma cells in parallel with enhanced expression of class I major histocompatibility complex antigens. Proc. Natl. Acad. Sci. U. S. A. 1987, 84:3405-3409.
6. Zaidi M.R., Merlino G. The two faces of interferon-γ in cancer. Clin. Cancer Res. 2011, 17:6118-6124.
7. + T cell population in Interferon γ-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J. Exp. Med. 2000, 192:123-128.
8. Sun R., Gao B. Negative regulation of liver regeneration by innate immunity (natural killer cells/interferon-gamma). Gastroenterology 2004, 127:1525-1539.
9. Kaplan D.H., Shankaran V., Dighe A.S., Stockert E., Aguet M., Old L.J., Schreiber R.D. Demonstration of an interferon γ-dependent tumor surveillance system in immunocompetent mice. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:7556-7561.
10. Chawla-Sarkar M., Lindner D.J., Liu Y.F., Williams B.R., Sen G.C., Silverman R.H., Borden E.C. Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 2003, 8:237-249.
11. Zhou Y., Weyman C.M., Liu H., Almasan A., Zhou A. IFN-gamma induces apoptosis in HL-60 cells through decreased Bcl-2 and increased Bak expression. J. Interferon Cytokine Res. 2008, 28:65-72.
12. Bernabei P., Coccia E.M., Rigamonti L., Bosticardo M., Forni G., Pestka S., Krause C.D., Battistini A., Novelli F. Interferon-gamma receptor 2 expression as the deciding factor in human T, B, and myeloid cell proliferation or death. J. Leukoc. Biol. 2001, 70:950-960.
13. Dighe A.S., Richards E., Old L.J., Schreiber R.D. Enhanced in vivo growth and resistance to rejection of tumor cells expressing dominant negative IFN gamma receptors. Immunity 1994, 1:447-456.
14. Vadrot N., Legrand A., Nello E., Bringuier A.F., Guillot R., Feldmann G. Inducible nitric oxide synthase (iNOS) activity could be responsible for resistance or sensitivity to IFN-gamma-induced apoptosis in several human hepatoma cell lines. J. Interferon Cytokine Res. 2006, 26:901-913.
15. Prasanna S.J., Saha B., Nandi D. Involvement of oxidative and nitrosative stress in modulation of gene expression and functional responses by IFNgamma. Int. Immunol. 2007, 19:867-879.
16. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39:44-84.
17. Blaise G.A., Gauvin D., Gangal M., Authier S. Nitric oxide, cell signaling and cell death. Toxicology 2005, 208:177-192.
18. Circu M.L., Aw T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48:749-762.
19. MacMicking J., Xie Q.W., Nathan C. Nitric oxide and macrophage function. Annu. Rev. Immunol. 1997, 15:323-350.
20. Gross T.J., Kremens K., Powers L.S., Brink B., Knutson T., Domann F.E., Philibert R.A., Milhem M.M., Monick M.M. Epigenetic silencing of the human NOS2 gene: rethinking the role of nitric oxide in human macrophage inflammatory responses. J. Immunol. 2014, 192:2326-2338.
21. Watanabe Y., Suzuki O., Haruyama T., Akaike T. Interferon-gamma induces reactive oxygen species and endoplasmic reticulum stress at the hepatic apoptosis. J. Cell. Biochem. 2003, 89:244-253.
22. Kanki K., Kawamura T., Watanabe Y. Control of ER stress by a chemical chaperone counteracts apoptotic signals in IFN-gamma-treated murine hepatocytes. Apoptosis 2009, 14:309-319.
23. Prasanna S.J., Nandi D. The MHC-encoded class I molecule, H-2Kk, demonstrates distinct requirements of assembly factors for cell surface expression: roles of TAP, Tapasin and beta2-microglobulin. Mol. Immunol. 2004, 41:1029-1045.
24. Malu S., Srinivasan S., Kumar Maiti P., Rajagopal D., John B., Nandi D. IFN-gamma bioassay: development of a sensitive method by measuring nitric oxide production by peritoneal exudate cells from C57BL/6 mice. J. Immunol. Methods 2003, 272:55-65.
25. Chandrasekar B., Deobagkar-Lele M., Victor E.S., Nandi D. Regulation of chemokines, CCL3 and CCL4, by interferon γ and nitric oxide synthase 2 in mouse macrophages and during Salmonella enterica serovar typhimurium infection. J. Infect. Dis. 2013, 207:1556-1568.
26. Zhou F. Molecular mechanisms of IFN-gamma to upregulate MHC class I antigen processing and presentation. Int. Rev. Immunol. 2009, 28:239-260.
27. Curtin J.F., Donovan M., Cotter T.G. Regulation and measurement of oxidative stress in apoptosis. J. Immunol. Methods 2002, 265:49-72.
28. Valledor A.F., Sánchez-Tilló E., Arpa L., Park J.M., Caelles C., Lloberas J., Celada A. Selective roles of MAPKs during the macrophage response to IFN-gamma. J. Immunol. 2008, 180:4523-4529.
29. Seminara A.R., Ruvolo P.P., Murad F. LPS/IFNgamma-induced RAW 264.7 apoptosis is regulated by both nitric oxide-dependent and -independent pathways involving JNK and the Bcl-2 family. Cell Cycle 2007, 6:1772-1778.
30. Street S.E., Trapani J.A., MacGregor D., Smyth M.J. Suppression of lymphoma and epithelial malignancies effected by interferonγ. J. Exp. Med. 2002, 196:129-134.
31. Young H.A., Bream J.H. IFN-γ: recent advances in understanding regulation of expression, biological functions, and clinical applications. Curr. Top. Microbiol. Immunol. 2007, 316:97-117.
32. Shankaran V., Ikeda H., Bruce A.T., White J.M., Swanson P.E., Old L.J., Schreiber R.D. IFN-γ and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 2001, 410:1107-1111.
33. Dunn G.P., Koebel C.M., Schreiber R.D. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 2006, 6:836-848.
34. Chae H.J., Ha K.C., Kim D.S., Cheung G.S., Kwak Y.G., Kim H.M., Kim Y.M., Pae H.O., Chung H.T., Chae S.W., Kim H.R. Catalase protects cardiomyocytes via its inhibition of nitric oxide synthesis. Nitric Oxide 2006, 14:189-199.
35. Rauen U., Li T., Ioannidis I., de Groot H. Nitric oxide increases toxicity of hydrogen peroxide against rat liver endothelial cells and hepatocytes by inhibition of hydrogen peroxide degradation. Am. J. Physiol. Cell Physiol. 2007, 292:C1440-C1449.
36. Burke A.J., Sullivan F.J., Giles F.J., Glynn S.A. The yin and yang of nitric oxide in cancer progression. Carcinogenesis 2013, 34:503-512.
37. Horras C.J., Lamb C.L., Mitchell K.A. Regulation of hepatocyte fate by interferon-γ. Cytokine Growth Factor Rev. 2011, 22:35-43.
38. Heigold S., Sers C., Bechtel W., Ivanovas B., Schäfer R., Bauer G. Nitric oxide mediates apoptosis induction selectively in transformed fibroblasts compared to nontransformed fibroblasts. Carcinogenesis 2002, 23:929-941.
39. Packer M.A., Murphy M.P. Peroxynitrite formed by simultaneous nitric oxide and superoxide generation causes cyclosporin-A-sensitive mitochondrial calcium efflux and depolarisation. Eur. J. Biochem. 1995, 234:231-239.
40. Genius J., Fandrey J. Nitric oxide affects the production of reactive oxygen species in hepatoma cells: implications for the process of oxygen sensing. Free Radic. Biol. Med. 2000, 29:515-521.
41. Wu F., Tyml K., Wilson J.X. iNOS expression requires NADPH oxidase-dependent redox signaling in microvascular endothelial cells. J. Cell. Physiol. 2008, 217:207-214.
42. Sestili P., Clementi E., Guidarelli A., Sciorati C., Cantoni O. Endogenous and exogenous nitric oxide enhance the DNA strand scission induced by tert-butylhydroperoxide in PC12 cells via peroxynitrite-dependent and independent mechanisms, respectively. Eur. J. Neurosci. 2000, 12:145-154.
43. Palomba L., Sestili P., Cantoni O. tert-Butylhydroperoxide induces peroxynitrite-dependent mitochondrial permeability transition leading PC12 cells to necrosis. J. Neurosci. Res. 2001, 65:387-395.
44. Szabó C., Ischiropoulos H., Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 2007, 6:662-680.
45. Calcerrada P., Peluffo G., Radi R. Nitric oxide-derived oxidants with a focus on peroxynitrite: molecular targets, cellular responses and therapeutic implications. Curr. Pharm. Des. 2011, 17:3905-3932.
46. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87:315-424.
47. Forstermann U., Munzel T. Endothelial NO synthase in vascular disease: from marvel to menace. Circulation 2006, 113:1708-1714.
48. Kim W.H., Lee J.W., Gao B., Jung M.H. Synergistic activation of JNK/SAPK induced by TNF-alpha and IFN-gamma: apoptosis of pancreatic beta-cells via the p53 and ROS pathway. Cell. Signal. 2005, 17:1516-1532.
49. + thymocytes during Salmonella enterica serovar Typhimurium infection. Eur. J. Immunol. 2014, 44:137-149.
50. González R., Ferrín G., Aguilar-Melero P., Ranchal I., Linares C.I., Bello R.I., De la Mata M., Gogvadze V., Bárcena J.A., Alamo J.M., Orrenius S., Padillo F.J., Zhivotovsky B., Muntané J. Targeting hepatoma using nitric oxide donor strategies. Antioxid. Redox Signal. 2013, 18:491-506.