CNS-Targeted Production of IL-17A Induces Glial Activation, Microvascular Pathology and Enhances the Neuroinflammatory Response to Systemic Endotoxemia

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Zimmermann, Julian ^a   Krauthausen, Marius ^a   Hofer, Markus J ^b   Heneka, Michael T ^a,c   Campbell, Iain L ^d   Müller, Marcus ^a,d  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY HOSPITAL MARBURG   (Germany)

^c UNIVERSITY OF BONN   (Germany)

^d UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 17; LIPOPOLYSACCHARIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN DAMAGE; BRAIN TISSUE; CELL ACTIVATION; CELL EXPANSION; CELL INFILTRATION; CELL POPULATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DEMYELINATION; ENDOTOXEMIA; GLIA CELL; HISTOLOGY; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; MICROANGIOPATHY; MICROGLIA; MOUSE; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARENCHYMA; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; SYMPTOMATOLOGY; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE; VASCULAR DISEASE;

ANIMALS; BLOOD-BRAIN BARRIER; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; ENDOTOXEMIA; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; INFLAMMATION; INTERLEUKIN-17; MICE; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROVESSELS; NEUROGLIA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84874549416     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057307     Document Type: Article

References (98)

1. Zepp J, Wu L, Li X, (2011) IL-17 receptor signaling and T helper 17-mediated autoimmune demyelinating disease. Trends Immunol 32: 232-239.
2. Rouvier E, Luciani M, Mattei M, Denizot F, Golstein P, (1993) CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a Herpesvirus saimiri gene. J Immunol150: 5445-5456.
3. Weaver CT, Hatton RD, Mangan PR, Harrington LE, (2007) IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25: 821-852.
4. Cua DJ, Tato CM, (2010) Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 10: 479-489.
5. Puel A, Cypowyj S, Bustamante J, Wright JF, Liu L, et al. (2011) Chronic Mucocutaneous Candidiasis in Humans with Inborn Errors of Interleukin-17 Immunity. Science 332:65 -68.
6. Kolls JK, McCray PB, Chan YR, (2008) Cytokine-mediated regulation of antimicrobial proteins. Nat Rev Immunol 8: 829-835.
7. Curtis MM, Way SS, (2009) Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126: 177-185.
8. Peck A, Mellins ED 2010) Precarious balance: Th17 cells in host defense. Infect Immun 78: 32-38.
9. Bettelli E, Korn T, Oukka M, Kuchroo VK, (2008) Induction and effector functions of T(H)17 cells. Nature 453: 1051-1057.
10. Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201: 233-240.
11. Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, et al. (2003) Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52: 65-70.
12. Lock C, Hermans G, Pedotti R, Brendolan A, Schadt E, et al. (2002) Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat Med 8: 500-508.
13. Teunissen MB, Koomen CW, de Waal Malefyt R, Wierenga EA, Bos JD, (1998) Interleukin-17 and interferon-gamma synergize in the enhancement of proinflammatory cytokine production by human keratinocytes. J Invest Dermatol 111: 645-649.
14. Ziolkowska M, Koc A, Luszczykiewicz G, Ksiezopolska-Pietrzak K, Klimczak E, et al. (2000) High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J Immunol164: 2832-2838.
15. Tzartos JS, Friese MA, Craner MJ, Palace J, Newcombe J, et al. (2008) Interleukin-17 Production in Central Nervous System-Infiltrating T Cells and Glial Cells Is Associated with Active Disease in Multiple Sclerosis. Am J Pathol 172: 146-155.
16. Guiton R, Vasseur V, Charron S, Arias MT, Van Langendonck N, et al. (2010) Interleukin 17 Receptor Signaling Is Deleterious during Toxoplasma gondii Infection in Susceptible BL6 Mice. J Infect Dis 202: 427-435.
17. Li G-Z, Zhong D, Yang L-M, Sun B, Zhong Z-H, et al. (2005) Expression of Interleukin-17 in Ischemic Brain Tissue. Scand J Immunol62: 481-486.
18. Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, et al. (2009) Pivotal role of cerebral interleukin-17-producing [gamma][delta]T cells in the delayed phase of ischemic brain injury. Nat Med 15: 946-950.
19. Smith E, Prasad K-MR, Butcher M, Dobrian A, Kolls JK, et al. (2010) Blockade of Interleukin-17A Results in Reduced Atherosclerosis in Apolipoprotein E-Deficient Mice. Circulation121: 1746-1755.
20. von Vietinghoff S, Ley K, (2010) Interleukin 17 in vascular inflammation. Cytokine & Growth Factor Rev 21: 463-469.
21. Brucklacher-Waldert V, Stuerner K, Kolster M, Wolthausen J, Tolosa E, (2009) Phenotypical and functional characterization of T helper 17 cells in multiple sclerosis. Brain 132: 3329.
22. Hofstetter H, Gold R, Hartung H-P, (2009) Th17 Cells in MS and Experimental Autoimmune Encephalomyelitis. Int MS J 16: 12-18.
23. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, et al. (2009) Interleukin-1 and IL-23 Induce Innate IL-17 Production from gammadelta T Cells, Amplifying Th17 Responses and Autoimmunity. Immunity 31: 331-341.
24. Rachitskaya AV, Hansen AM, Horai R, Li Z, Villasmil R, et al. (2008) Cutting Edge: NKT Cells Constitutively Express IL-23 Receptor and RORγt and Rapidly Produce IL-17 upon Receptor Ligation in an IL-6-Independent Fashion. J Immunol180: 5167-5171.
25. Li L, Huang L, Vergis AL, Ye H, Bajwa A, et al. (2010) IL-17 produced by neutrophils regulates IFN-γ-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J Clin Invest 120: 331-342.
26. Hoshino A, Nagao T, Nagi-Miura N, Ohno N, Yasuhara M, et al. (2008) MPO-ANCA induces IL-17 production by activated neutrophils in vitro via its Fc region- and complement-dependent manner. J Autoimmun 31: 79-89.
27. Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, et al. (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
28. Korn T, Bettelli E, Oukka M, Kuchroo VK, (2009) IL-17 and Th17 Cells. Annu Rev Immunol 27: 485-517.
29. Tran EH, Prince EN, Owens T, (2000) IFN-γ Shapes Immune Invasion of the Central Nervous System Via Regulation of Chemokines. J Immunol164: 2759-2768.
30. Zhang G-X, Gran B, Yu S, Li J, Siglienti I, et al. (2003) Induction of Experimental Autoimmune Encephalomyelitis in IL-12 Receptor-β2-Deficient Mice: IL-12 Responsiveness Is Not Required in the Pathogenesis of Inflammatory Demyelination in the Central Nervous System. J Immunol170: 2153-2160.
31. Park H, Li Z, Yang XO, Chang SH, Nurieva R, et al. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6: 1133-1141.
32. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, et al. (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6: 1123-1132.
33. Veldhoen M, Hocking RJ, Flavell RA, Stockinger B, (2006) Signals mediated by transforming growth factor-[beta] initiate autoimmune encephalomyelitis, but chronic inflammation is needed to sustain disease. Nat Immunol 7: 1151-1156.
34. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
35. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, et al. (2006) Transforming growth factor-[beta] induces development of the TH17 lineage. Nature 441: 231-234.
36. Korn T, Bettelli E, Gao W, Awasthi A, Jager A, et al. (2007) IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 448: 484-487.
37. Sarma JD, Ciric B, Marek R, Sadhukhan S, Caruso ML, et al. (2009) Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. J Neuroinflammation 6: 14.
38. Kebir H, Kreymborg K, Ifergan I, Dodelet-Devillers A, Cayrol R, et al. (2007) Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat Med 13: 1173-1175.
39. Chang SH, Park H, Dong C, (2006) Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J Biol Chem281: 35603-35607.
40. Qian Y, Liu C, Hartupee J, Altuntas CZ, Gulen MF, et al. (2007) The adaptor Act1 is required for interleukin 17-dependent signaling associated with autoimmune and inflammatory disease. Nat Immunol 8: 247-256.
41. Ouyang W, Kolls JK, Zheng Y, (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
42. Carlson T, Kroenke M, Rao P, Lane TE, Segal B, (2008) The Th17-ELR+ CXC chemokine pathway is essential for the development of central nervous system autoimmune disease. J Exp Med 205: 811-823.
43. Fossiez F, Djossou O, Chomarat P, Flores-Romo L, Ait-Yahia S, et al. (1996) T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 183: 2593-2603.
44. Kawanokuchi J, Shimizu K, Nitta A, Yamada K, Mizuno T, et al. (2008) Production and functions of IL-17 in microglia. J Neuroimmunol 194: 54-61.
45. Ma X, Reynolds SL, Baker BJ, Li X, Benveniste EN, et al. (2010) IL-17 enhancement of the IL-6 signaling cascade in astrocytes. J Immunol184: 4898.
46. Huppert J, Closhen D, Croxford A, White R, Kulig P, et al. (2010) Cellular Mechanisms of IL-17-Induced Blood-Brain Barrier Disruption. FASEB J 24: 1023-1034.
47. Hofstetter HH, Ibrahim SM, Koczan D, Kruse N, Weishaupt A, et al. (2005) Therapeutic efficacy of IL-17 neutralization in murine experimental autoimmune encephalomyelitis. Cell Immunol 237: 123-130.
48. Komiyama Y, Nakae S, Matsuki T, Nambu A, Ishigame H, et al. (2006) IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J Immunol177: 566-573.
49. Uyttenhove C, Sommereyns C, Théate I, Michiels T, Van Snick J, (2007) Anti-IL-17A Autovaccination Prevents Clinical and Histological Manifestations of Experimental Autoimmune Encephalomyelitis. Ann N Y Acad Sci 1110: 330-336.
50. Kap YS, Jagessar SA, Driel N, Blezer E, Bauer J, et al. (2010) Effects of Early IL-17A Neutralization on Disease Induction in a Primate Model of Experimental Autoimmune Encephalomyelitis. J Neuroimmune Pharmacol 6: 341-353.
51. Haak S, Croxford AL, Kreymborg K, Heppner FL, Pouly S, et al. (2009) IL-17A and IL-17F do not contribute vitally to autoimmune neuro-inflammation in mice. J Clin Invest 119: 61-69.
52. Hu Y, Ota N, Peng I, Refino CJ, Danilenko DM, et al. (2010) IL-17RC Is Required for IL-17A- and IL-17F-Dependent Signaling and the Pathogenesis of Experimental Autoimmune Encephalomyelitis. J Immunol184: 4307-4316.
53. Kang Z, Altuntas CZ, Gulen MF, Liu C, Giltiay N, et al. (2010) Astrocyte-Restricted Ablation of Interleukin-17-Induced Act1-Mediated Signaling Ameliorates Autoimmune Encephalomyelitis. Immunity 32: 414-425.
54. Hou W, Kang HS, Kim BS, (2009) Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J Exp Med 206: 313-328.
55. Kelly MN, Kolls JK, Happel K, Schwartzman JD, Schwarzenberger P, et al. (2005) Interleukin-17/Interleukin-17 Receptor-Mediated Signaling Is Important for Generation of an Optimal Polymorphonuclear Response against Toxoplasma gondii Infection. Infect Immun 73: 617-621.
56. Mucke L, Oldstone MB, Morris JC, Nerenberg MI, (1991) Rapid activation of astrocyte-specific expression of GFAP-lacZ transgene by focal injury. New Biol 3: 465-474.
57. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, et al. (1993) Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. PNAS 90: 10061.
58. Pagenstecher A, Lassmann S, Carson MJ, Kincaid CL, Stalder AK, et al. (2000) Astrocyte-targeted expression of IL-12 induces active cellular immune responses in the central nervous system and modulates experimental allergic encephalomyelitis. J Immunol164: 4481.
59. Boztug K, Carson MJ, Pham-Mitchell N, Asensio VC, DeMartino J, et al. (2002) Leukocyte infiltration, but not neurodegeneration, in the CNS of transgenic mice with astrocyte production of the CXC chemokine ligand 10. J Immunol2002 169: 1505.
60. Giulian D, Baker T, (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci6: 2163-2178.
61. Bancroft JD, Gamble M (2008) Theory and practice of histological techniques. Amsterdam, Elsevier Health Sciences.
62. Tamboli IY, Barth E, Christian L, Siepmann M, Kumar S, et al. (2010) Statins Promote the Degradation of Extracellular Amyloid β-Peptide by Microglia via Stimulation of Exosome-associated Insulin-degrading Enzyme (IDE) Secretion. J Biol Chem285: 37405-37414.
63. Getts DR, Terry RL, Getts MT, Müller M, Rana S, et al. (2008) Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med. 205: 2319-2337.
64. de Haas AH, Boddeke HWGM, Biber K, (2008) Region-specific expression of immunoregulatory proteins on microglia in the healthy CNS. Glia 56: 888-894.
65. Krauthausen M, Ellis SL, Zimmermann J, Sarris M, Wakefield D, et al. (2011) Opposing roles for CXCR3 signaling in central nervous system versus ocular inflammation mediated by the astrocyte-targeted production of IL-12. Am J Pathol 179: 2346-2359.
66. Saria A, Lundberg JM, (1983) Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues. J NeurosciMethods 8: 41-49.
67. Ay I, Francis JW, Brown RH Jr, (2008) VEGF increases blood-brain barrier permeability to Evans blue dye and tetanus toxin fragment C but not adeno-associated virus in ALS mice. Brain Research 1234: 198-205.
68. Campbell IL, Hofer MJ, Pagenstecher A, (2010) Transgenic models for cytokine-induced neurological disease. Biochimi Biophys Acta (BBA)- Molecular Basis of Disease 1802: 903-917.
69. Stalder AK, Pagenstecher A, Yu NC, Kincaid C, Chiang CS, et al. (1997) Lipopolysaccharide-induced IL-12 expression in the central nervous system and cultured astrocytes and microglia. J Immunol159: 1344-1351.
70. Bohatschek M, Werner A, Raivich G, (2001) Systemic LPS Injection Leads to Granulocyte Influx into Normal and Injured Brain: Effects of ICAM-1 Deficiency. Exp Neurol 172: 137-152.
71. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, et al. (2006) Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9: 917-924.
72. Chiang CS, Powell HC, Gold LH, Samimi A, Campbell IL, (1996) Macrophage/microglial-mediated primary demyelination and motor disease induced by the central nervous system production of interleukin-3 in transgenic mice. J Clin Invest 97: 1512-1524.
73. Akwa Y, Hassett DE, Eloranta M-L, Sandberg K, Masliah E, et al. (1998) Transgenic Expression of IFN-α in the Central Nervous System of Mice Protects Against Lethal Neurotropic Viral Infection but Induces Inflammation and Neurodegeneration. J Immunol161:5016 -5026.
74. Reiman R, Torres AC, Martin BK, Ting JP, Campbell IL, et al. (2005) Expression of C5a in the brain does not exacerbate experimental autoimmune encephalomyelitis. Neurosci Lett 390: 134-138.
75. Yao Z, Fanslow WC, Seldin MF, Rousseau A-M, Painter SL, et al. (1995) Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3: 811-821.
76. Ge D, You Z, (2008) Expression of interleukin-17RC protein in normal human tissues. Int Arch Med 1: 19.
77. Martin AP, Coronel EC, Sano G-I, Chen S-C, Vassileva G, et al. (2004) A Novel Model for Lymphocytic Infiltration of the Thyroid Gland Generated by Transgenic Expression of the CC Chemokine CCL21. J Immunol173: 4791-4798.
78. Ploix CC, Noor S, Crane J, Masek K, Carter W, et al. (2011) CNS-derived CCL21 is both sufficient to drive homeostatic CD4+ T cell proliferation and necessary for efficient CD4+ T cell migration into the CNS parenchyma following Toxoplasma gondii infection. Brain Behav Immun 25: 883-896.
79. Trajkovic V, Stosic-Grujicic S, Samardzic T, Markovic M, Miljkovic D, et al. (2001) Interleukin-17 stimulates inducible nitric oxide synthase activation in rodent astrocytes. J Neuroimmunol 119: 183-191.
80. Joutel A, Monet-Leprêtre M, Gosele C, Baron-Menguy C, Hammes A, et al. (2010) Cerebrovascular dysfunction and microcirculation rarefaction precede white matter lesions in a mouse genetic model of cerebral ischemic small vessel disease. J Clin Invest 120: 433-445.
81. Suzuki K, Masawa N, Sakata N, Takatama M, (2003) Pathologic evidence of microvascular rarefaction in the brain of renal hypertensive rats. J Stroke Cerebrovasc Dis 12: 8-16.
82. Jiang N, Li X, Qi T, Guo S, Liang F, et al. (2011) Susceptible gene single nucleotide polymorphism and hemorrhage risk in patients with brain arteriovenous malformation. J Clin Neurosci 18: 1279-1281.
83. Erbel C, Dengler TJ, Wangler S, Lasitschka F, Bea F, et al. (2010) Expression of IL-17A in human atherosclerotic lesions is associated with increased inflammation and plaque vulnerability. Basic Res Cardiol 106: 125-134.
84. Erbel C, Chen L, Bea F, Wangler S, Celik S, et al. (2009) Inhibition of IL-17A Attenuates Atherosclerotic Lesion Development in ApoE-Deficient Mice. J Immunol183:8167 -8175.
85. Smith E, Prasad KMR, Butcher M, Dobrian A, Kolls JK, et al. (2010) Blockade of Interleukin-17A Results in Reduced Atherosclerosis in Apolipoprotein E-Deficient Mice. Circulation121: 1746-1755.
86. Madhur MS, Funt SA, Li L, Vinh A, Chen W, et al. (2011) Role of Interleukin 17 in Inflammation, Atherosclerosis, and Vascular Function in Apolipoprotein E-Deficient Mice. Arterioscler Thromb Vasc Biol 31:1565 -1572.
87. Kalueff A, Loseva E, Haapasalo H, Rantala I, Keranen J, et al. (2006) Thalamic calcification in vitamin D receptor knockout mice. Neuroreport 17: 717-721.
88. Bruce D, Yu S, Ooi JH, Cantorna MT, (2011) Converging pathways lead to overproduction of IL-17 in the absence of vitamin D signaling. Int Immunol 23: 519-528.
89. Joshi S, Pantalena L-C, Liu XK, Gaffen SL, Liu H, et al. (2011) 1,25-Dihydroxyvitamin D3 Ameliorates Th17 Autoimmunity via Transcriptional Modulation of Interleukin-17A. Mol Cell Biol 31: 3653-3669.
90. Wyss-Coray T, Feng L, Masliah E, Ruppe MD, Lee HS, et al. (1995) Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol 147: 53-67.
91. Wyss-Coray T, Lin C, Von Euw D, Masliah E, Mucke L, et al. (2000) Alzheimer's Disease-like Cerebrovascular Pathology in Transforming Growth Factor-β1 Transgenic Mice and Functional Metabolic Correlates. Ann N Y Acad Sci 903: 317-323.
92. Wyss-Coray T, Lin C, Sanan DA, Mucke L, Masliah E, (2000) Chronic Overproduction of Transforming Growth Factor-β1 by Astrocytes Promotes Alzheimer's Disease-Like Microvascular Degeneration in Transgenic Mice. Am J Pathol 156: 139-150.
93. Audoy-Rémus J, Richard J-F, Soulet D, Zhou H, Kubes P, et al. (2008) Rod-Shaped Monocytes Patrol the Brain Vasculature and Give Rise to Perivascular Macrophages under the Influence of Proinflammatory Cytokines and Angiopoietin-2. J Neurosci28: 10187-10199.
94. Zhou H, Lapointe BM, Clark SR, Zbytnuik L, Kubes P, (2006) A Requirement for Microglial TLR4 in Leukocyte Recruitment into Brain in Response to Lipopolysaccharide. J Immunol177: 8103-8110.
95. Paintlia MK, Paintlia AS, Singh AK, Singh I, (2011) Synergistic activity of interleukin-17 and tumor necrosis factor-α enhances oxidative stress-mediated oligodendrocyte apoptosis. J Neurochem 116: 508-521.
96. Chiricozzi A, Guttman-Yassky E, Suarez-Farinas M, Nograles KE, Tian S, et al. (2011) Integrative Responses to IL-17 and TNF-[alpha] in Human Keratinocytes Account for Key Inflammatory Pathogenic Circuits in Psoriasis. J Invest Dermatol 131: 677-687.
97. Liu Y, Mei J, Gonzales L, Yang G, Dai N, et al. (2011) IL-17A and TNF-α Exert Synergistic Effects on Expression of CXCL5 by Alveolar Type II Cells In Vivo and In Vitro. JImmunol186: 3197-3205.
98. Hartupee J, Liu C, Novotny M, Li X, Hamilton T, (2007) IL-17 Enhances Chemokine Gene Expression through mRNA Stabilization. J Immunol179: v-4141.