Synergistic activity of interleukin-17 and tumor necrosis factor-α enhances oxidative stress-mediated oligodendrocyte apoptosis

Journal of Neurochemistry

Volumn 116, Issue 4, 2011, Pages 508-521

  Paintlia, Manjeet K ^a   Paintlia, Ajaib S ^a   Singh, Avtar K ^b   Singh, Inderjit ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

apoptosis and multiple sclerosis; interleukin 17; oligodendrocyte; tumor necrosis factor

Indexed keywords

4 [4 [3 (4 ACETYL 3 HYDROXY 2 PROPYLPHENOXY)PROPOXY]PHENOXY]ACETIC ACID; ACETYLCYSTEINE; CASPASE 8; DELTA15 PROSTAGLANDIN J2; INTERLEUKIN 17; INTERLEUKIN 17 RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PROTEIN BAX; PROTEIN BID; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTOXICITY; MITOCHONDRIAL MEMBRANE POTENTIAL; NERVE CELL DIFFERENTIATION; NONHUMAN; OLIGODENDROGLIA; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CELL SURVIVAL; CELLS, CULTURED; DRUG SYNERGISM; GROWTH INHIBITORS; INTERLEUKIN-17; MEMBRANE POTENTIAL, MITOCHONDRIAL; OLIGODENDROGLIA; OXIDATIVE STRESS; RATS; REACTIVE OXYGEN SPECIES; STEM CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79551645701     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07136.x     Document Type: Article

References (66)

1. Afif H., Benderdour M., Mfuna-Endam L., Martel-Pelletier J., Pelletier J. P., Duval N., and, Fahmi H., (2007) Peroxisome proliferator-activated receptor gamma1 expression is diminished in human osteoarthritic cartilage and is downregulated by interleukin-1beta in articular chondrocytes. Arthritis Res. Ther. 9, R31.
2. Akassoglou K., Bauer J., Kassiotis G., Pasparakis M., Lassmann H., Kollias G., and, Probert L., (1998) Oligodendrocyte apoptosis and primary demyelination induced by local TNF/p55TNF receptor signaling in the central nervous system of transgenic mice: models for multiple sclerosis with primary oligodendrogliopathy. Am. J. Pathol. 153, 801-813.
3. Amadi-Obi A., Yu C. R., Liu X., Mahdi R. M., Clarke G. L., Nussenblatt R. B., Gery I., Lee Y. S., and, Egwuagu C. E., (2007) TH17 cells contribute to uveitis and scleritis and are expanded by IL-2 and inhibited by IL-27/STAT1. Nat. Med. 13, 711-718.
4. Bernardo A., Bianchi D., Magnaghi V., and, Minghetti L., (2009) Peroxisome proliferator-activated receptor-gamma agonists promote differentiation and antioxidant defenses of oligodendrocyte progenitor cells. J. Neuropathol. Exp. Neurol. 68, 797-808.
5. Bettelli E., Oukka M., and, Kuchroo V. K., (2007) T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8, 345-350.
6. Boldin M. P., Goncharov T. M., Goltsev Y. V., and, Wallach D., (1996) Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 85, 803-815.
7. Bonetti B., and, Raine C. S., (1997) Multiple sclerosis: oligodendrocytes display cell death-related molecules in situ but do not undergo apoptosis. Ann. Neurol. 42, 74-84.
8. Brown K. D., Claudio E., and, Siebenlist U., (2008) The roles of the classical and alternative nuclear factor-kappaB pathways: potential implications for autoimmunity and rheumatoid arthritis. Arthritis Res. Ther. 10, 212.
9. Calderon F. H., von Bernhardi R., De Ferrari G., Luza S., Aldunate R., and, Inestrosa N. C., (1998) Toxic effects of acetylcholinesterase on neuronal and glial-like cells in vitro. Mol. Psychiatry 3, 247-255.
10. Casaccia-Bonnefil P., (2000) Cell death in the oligodendrocyte lineage: a molecular perspective of life/death decisions in development and disease. Glia 29, 124-135.
11. Chabaud M., Garnero P., Dayer J. M., Guerne P. A., Fossiez F., and, Miossec P., (2000) Contribution of interleukin 17 to synovium matrix destruction in rheumatoid arthritis. Cytokine 12, 1092-1099.
12. Chang S. H., and, Dong C., (2009) IL-17F: regulation, signaling and function in inflammation. Cytokine 46, 7-11.
13. Cimini A., Bernardo A., Cifone M. G., Di Marzio L., and, Di Loreto S., (2003) TNFalpha downregulates PPARdelta expression in oligodendrocyte progenitor cells: implications for demyelinating diseases. Glia 41, 3-14.
14. De Smaele E., Zazzeroni F., Papa S., Nguyen D. U., Jin R., Jones J., Cong R., and, Franzoso G., (2001) Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 414, 308-313.
15. Diab A., Deng C., Smith J. D., Hussain R. Z., Phanavanh B., Lovett-Racke A. E., Drew P. D., and, Racke M. K., (2002) Peroxisome proliferator-activated receptor-gamma agonist 15-deoxy-Delta(12, 14)-prostaglandin J(2) ameliorates experimental autoimmune encephalomyelitis. J. Immunol. 168, 2508-2515.
16. D'Souza S., Alinauskas K., McCrea E., Goodyer C., and, Antel J. P., (1995) Differential susceptibility of human CNS-derived cell populations to TNF-dependent and independent immune-mediated injury. J. Neurosci. 15, 7293-7300.
17. Gilgun-Sherki Y., Melamed E., and, Offen D., (2004) The role of oxidative stress in the pathogenesis of multiple sclerosis: the need for effective antioxidant therapy. J. Neurol. 251, 261-268.
18. Giri S., Nath N., Smith B., Viollet B., Singh A. K., and, Singh I., (2004) 5-Aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside inhibits proinflammatory response in glial cells: a possible role of AMP-activated protein kinase. J. Neurosci. 24, 479-487.
19. Haq E., Giri S., Singh I., and, Singh A. K., (2003) Molecular mechanism of psychosine-induced cell death in human oligodendrocyte cell line. J. Neurochem. 86, 1428-1440.
20. Hisahara S., Shoji S., Okano H., and, Miura M., (1997) ICE/CED-3 family executes oligodendrocyte apoptosis by tumor necrosis factor. J. Neurochem. 69, 10-20.
21. Hofman F. M., Hinton D. R., Johnson K., and, Merrill J. E., (1989) Tumor necrosis factor identified in multiple sclerosis brain. J. Exp. Med. 170, 607-612.
22. Hsu H., Xiong J., and, Goeddel D. V., (1995) The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81, 495-504.
23. Hsu H., Shu H. B., Pan M. G., and, Goeddel D. V., (1996) TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 84, 299-308.
24. Hue S., Ahern P., Buonocore S., Kullberg M. C., Cua D. J., McKenzie B. S., Powrie F., and, Maloy K. J., (2006) Interleukin-23 drives innate and T cell-mediated intestinal inflammation. J. Exp. Med. 203, 2473-2483.
25. Huppert J., Closhen D., Croxford A., et al. (2010) Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J., 24, 1023-1034.
26. Iyoda M., Shibata T., Kawaguchi M., Hizawa N., Yamaoka T., Kokubu F., and, Akizawa T., (2010) IL-17A and IL-17F stimulate chemokines via MAPK pathways (ERK1/2 and p38 but not JNK) in mouse cultured mesangial cells: synergy with TNF-alpha and IL-1beta. Am. J. Physiol. Renal. Physiol. 298, F779-F787.
27. Jackson-Bernitsas D. G., Ichikawa H., Takada Y., Myers J. N., Lin X. L., Darnay B. G., Chaturvedi M. M., and, Aggarwal B. B., (2007) Evidence that TNF-TNFR1-TRADD-TRAF2-RIP-TAK1-IKK pathway mediates constitutive NF-kappaB activation and proliferation in human head and neck squamous cell carcinoma. Oncogene 26, 1385-1397.
28. Jana M., and, Pahan K., (2005) Redox regulation of cytokine-mediated inhibition of myelin gene expression in human primary oligodendrocytes. Free Radic. Biol. Med. 39, 823-831.
29. Jeffery N. D., and, Blakemore W. F., (1997) Locomotor deficits induced by experimental spinal cord demyelination are abolished by spontaneous remyelination. Brain 120 (Pt 1), 27-37.
30. Jovanovic D. V., Di Battista J. A., Martel-Pelletier J., Jolicoeur F. C., He Y., Zhang M., Mineau F., and, Pelletier J. P., (1998) IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J. Immunol. 160, 3513-3521.
31. Jurewicz A., Matysiak M., Tybor K., and, Selmaj K., (2003) TNF-induced death of adult human oligodendrocytes is mediated by c-jun NH2-terminal kinase-3. Brain 126, 1358-1370.
32. Kebir H., Kreymborg K., and, Ifergan I., et al. (2007) Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 13, 1173-1175.
33. Koch M., Ramsaransing G. S., Arutjunyan A. V., Stepanov M., Teelken A., Heersema D. J., and, De Keyser J., (2006) Oxidative stress in serum and peripheral blood leukocytes in patients with different disease courses of multiple sclerosis. J. Neurol. 253, 483-487.
34. Kopnin P. B., Kravchenko I. V., Furalyov V. A., Pylev L. N., and, Kopnin B. P., (2004) Cell type-specific effects of asbestos on intracellular ROS levels, DNA oxidation and G1 cell cycle checkpoint. Oncogene 23, 8834-8840.
35. McCarthy K. D., and, de Vellis J., (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
36. McKenzie B. S., Kastelein R. A., and, Cua D. J., (2006) Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27, 17-23.
37. Nakae S., Nambu A., Sudo K., and, Iwakura Y., (2003) Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171, 6173-6177.
38. Nath N., Giri S., Prasad R., Singh A. K., and, Singh I., (2004) Potential targets of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitor for multiple sclerosis therapy. J. Immunol. 172, 1273-1286.
39. Ozawa K., Suchanek G., Breitschopf H., Bruck W., Budka H., Jellinger K., and, Lassmann H., (1994) Patterns of oligodendroglia pathology in multiple sclerosis. Brain 117 (Pt 6), 1311-1322.
40. Paintlia M. K., Paintlia A. S., Barbosa E., Singh I., and, Singh A. K., (2004) N-acetylcysteine prevents endotoxin-induced degeneration of oligodendrocyte progenitors and hypomyelination in developing rat brain. J. Neurosci. Res. 78, 347-361.
41. Paintlia A. S., Paintlia M. K., Khan M., Vollmer T., Singh A. K., and, Singh I., (2005) HMG-CoA reductase inhibitor augments survival and differentiation of oligodendrocyte progenitors in animal model of multiple sclerosis. FASEB J. 19, 1407-1421.
42. Paintlia A. S., Paintlia M. K., Singh I., and, Singh A. K., (2006) IL-4-induced peroxisome proliferator-activated receptor gamma activation inhibits NF-kappaB trans activation in central nervous system (CNS) glial cells and protects oligodendrocyte progenitors under neuroinflammatory disease conditions: implication for CNS-demyelinating diseases. J. Immunol., 176, 4385-4398.
43. Paintlia A. S., Paintlia M. K., Singh A. K., and, Singh I., (2008a) Inhibition of rho family functions by lovastatin promotes myelin repair in ameliorating experimental autoimmune encephalomyelitis. Mol. Pharmacol. 73, 1381-1393.
44. Paintlia M. K., Paintlia A. S., Khan M., Singh I., and, Singh A. K., (2008b) Modulation of peroxisome proliferator-activated receptor-alpha activity by N-acetyl cysteine attenuates inhibition of oligodendrocyte development in lipopolysaccharide stimulated mixed glial cultures. J. Neurochem. 105, 956-970.
45. Paintlia A. S., Paintlia M. K., Singh A. K., Orak J. K., and, Singh I., (2010) Activation of PPAR-gamma and PTEN cascade participates in lovastatin-mediated accelerated differentiation of oligodendrocyte progenitor cells. Glia 58, 1669-1685.
46. Park H., Li Z., and, Yang X. O., et al. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141.
47. Polak P. E., Kalinin S., and, Dello Russo C., et al. (2005) Protective effects of a peroxisome proliferator-activated receptor-beta/delta agonist in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 168, 65-75.
48. Prasad R., Giri S., Nath N., Singh I., and, Singh A. K., (2006) 5-Aminoimidazole-4-carboxamide-1-beta-4-ribofuranoside attenuates experimental autoimmune encephalomyelitis via modulation of endothelial-monocyte interaction. J. Neurosci. Res. 84, 614-625.
49. Prineas J. W., Barnard R. O., Kwon E. E., Sharer L. R., and, Cho E. S., (1993) Multiple sclerosis: remyelination of nascent lesions. Ann. Neurol. 33, 137-151.
50. Qanungo S., Das M., Haldar S., and, Basu A., (2005) Epigallocatechin-3- gallate induces mitochondrial membrane depolarization and caspase-dependent apoptosis in pancreatic cancer cells. Carcinogenesis 26, 958-967.
51. Rattan R., Giri S., Singh A. K., and, Singh I., (2005) 5-Aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside inhibits cancer cell proliferation in vitro and in vivo via AMP-activated protein kinase. J. Biol. Chem. 280, 39582-39593.
52. Roth A. D., Leisewitz A. V., Jung J. E., Cassina P., Barbeito L., Inestrosa N. C., and, Bronfman M., (2003) PPAR gamma activators induce growth arrest and process extension in B12 oligodendrocyte-like cells and terminal differentiation of cultured oligodendrocytes. J. Neurosci. Res. 72, 425-435.
53. Saluja I., Granneman J. G., and, Skoff R. P., (2001) PPAR delta agonists stimulate oligodendrocyte differentiation in tissue culture. Glia 33, 191-204.
54. Selmaj K. W., and, Raine C. S., (1988) Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol. 23, 339-346.
55. Selmaj K., Raine C. S., Cannella B., and, Brosnan C. F., (1991a) Identification of lymphotoxin and tumor necrosis factor in multiple sclerosis lesions. J. Clin. Invest. 87, 949-954.
56. Selmaj K., Raine C. S., Farooq M., Norton W. T., and, Brosnan C. F., (1991b) Cytokine cytotoxicity against oligodendrocytes. Apoptosis induced by lymphotoxin. J. Immunol. 147, 1522-1529.
57. Sharief M. K., and, Hentges R., (1991) Association between tumor necrosis factor-alpha and disease progression in patients with multiple sclerosis. N. Engl. J. Med. 325, 467-472.
58. Smith K. J., Kapoor R., and, Felts P. A., (1999) Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol. 9, 69-92.
59. Sospedra M., and, Martin R., (2005) Immunology of multiple sclerosis. Annu. Rev. Immunol. 23, 683-747.
60. Stanislaus R., Gilg A. G., Singh A. K., and, Singh I., (2005) N-acetyl-L-cysteine ameliorates the inflammatory disease process in experimental autoimmune encephalomyelitis in Lewis rats. J. Autoimmune Dis. 2, 4.
61. Stromnes I. M., Cerretti L. M., Liggitt D., Harris R. A., and, Goverman J. M., (2008) Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 14, 337-342.
62. Takada Y., Fang X., Jamaluddin M. S., Boyd D. D., and, Aggarwal B. B., (2004) Genetic deletion of glycogen synthase kinase-3beta abrogates activation of IkappaBalpha kinase, JNK, Akt, and p44/p42 MAPK but potentiates apoptosis induced by tumor necrosis factor. J. Biol. Chem. 279, 39541-39554.
63. Tang G., Minemoto Y., Dibling B., Purcell N. H., Li Z., Karin M., and, Lin A., (2001) Inhibition of JNK activation through NF-kappaB target genes. Nature 414, 313-317.
64. Weaver C. T., Hatton R. D., Mangan P. R., and, Harrington L. E., (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25, 821-852.
65. Zamvil S. S., and, Steinman L., (1990) The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 8, 579-621.
66. Zheng Y., Danilenko D. M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., and, Ouyang W., (2007) Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445, 648-651.