γδ T cells provide the early source of IFN-γ to aggravate lesions in spinal cord injury

Journal of Experimental Medicine

Volumn 215, Issue 2, 2018, Pages 521-535

  Sun, Guodong ^a   Yang, Shuxian ^a   Cao, Guangchao ^a   Wang, Qianghua ^a   Hao, Jianlei ^a   Wen, Qiong ^a   Li, Zhizhong ^a   So, Kwok Fai ^a   Liu, Zonghua ^a,c   Zhou, Sufang ^d   Zhao, Yongxiang ^d   Yang, Hengwen ^a,c   Zhou, Libing ^a,b,e   Yin, Zhinan ^a,c  

^a JINAN UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c SICHUAN UNIVERSITY   (China)

^d GUANGXI MEDICAL UNIVERSITY   (China)

^e GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR; IFNG PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL FUNCTION; CELL INFILTRATION; CELL LOSS; CEREBROSPINAL FLUID; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CONVALESCENCE; CYTOKINE PRODUCTION; DISEASE EXACERBATION; FEMALE; FUNCTIONAL DISEASE; GAMMA DELTA T LYMPHOCYTE; GENE KNOCKOUT; HUMAN; HUMAN CELL; LYMPHOCYTE FUNCTION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; T CELL DEPLETION; ADULT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE DEPLETION; MALE; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; T LYMPHOCYTE RECEPTOR GENE; T LYMPHOCYTE SUBPOPULATION; YOUNG ADULT;

ADULT; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; GENES, T-CELL RECEPTOR DELTA; HUMANS; INTERFERON-GAMMA; LYMPHOCYTE DEPLETION; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES; T-LYMPHOCYTE SUBSETS; YOUNG ADULT;

EID: 85041376228     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20170686     Document Type: Article

References (76)

1. Ankeny, D.P., and P.G. Popovich. 2009. Mechanisms and implications of adaptive immune responses after traumatic spinal cord injury. Neuroscience. 158:1112-1121. https ://doi. org /10. 1016 /j. neuroscience. 2008. 07. 001
2. Anwar, M.A., T.S. Al Shehabi, and A.H. Eid. 2016. Inflammogenesis of Secondary Spinal Cord Injury. Front. Cell. Neurosci. 10:98. https ://doi. org /10. 3389 /fncel. 2016. 00098
3. Baskin, D.S., and R.K. Simpson Jr. 1987. Corticomotor and somatosensory evoked potential evaluation of acute spinal cord injury in the rat. Neurosurgery. 20:871-877. https ://doi. org /10. 1227 /00006123-198706000-00009
4. Bayrakli, F., H. Balaban, U. Ozum, C. Duger, S. Topaktas, and H.Z. Kars. 2012. Etanercept treatment enhances clinical and neuroelectrophysiological recovery in partial spinal cord injury. Eur. Spine J. 21:2588-2593. https :// doi. org /10. 1007 /s00586-012-2319-7
5. Becher, B., S. Spath, and J. Goverman. 2017. Cytokine networks in neuroinflammation. Nat. Rev. Immunol. 17:49-59. https ://doi. org /10. 1038 /nri. 2016. 123
6. Beg, A.A., and D. Baltimore. 1996. An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science. 274:782-784. https ://doi. org /10. 1126 /science. 274. 5288. 782
7. Beg, A.A., T.S. Finco, P.V. Nantermet, and A.S. Baldwin Jr. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of I kappa B alpha: a mechanism for NF-kappa B activation. Mol. Cell. Biol. 13:3301-3310. https ://doi. org /10. 1128 /MCB. 13. 6. 3301
8. Benakis, C., D. Brea, S. Caballero, G. Faraco, J. Moore, M. Murphy, G. Sita, G. Racchumi, L. Ling, E.G. Pamer, et al. 2016. Commensal microbiota affects ischemic stroke outcome by regulating intestinal γδ T cells. Nat. Med. 22:516-523. https ://doi. org /10. 1038 /nm. 4068
9. Bonneville, M., R.L. O'Brien, and W.K. Born. 2010. Gammadelta T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10:467-478. https ://doi. org /10. 1038 /nri2781
10. Ceccarelli, F., U. Massafra, C. Perricone, L. Idolazzi, R. Giacomelli, R. Tirri, R. Russo, G. Pistone, P. Ruscitti, S. Parisi, et al. 2017. Anti-TNF treatment response in rheumatoid arthritis patients with moderate disease activity: a prospective observational multicentre study (MOD ERA TE). Clin. Exp. Rheumatol. 35:24-32
11. Chen, L., W. He, S.T. Kim, J. Tao, Y. Gao, H. Chi, A.M. Intlekofer, B. Harvey, S.L. Reiner, Z. Yin, et al. 2007. Epigenetic and transcriptional programs lead to default IFN-gamma production by gammadelta T cells. J. Immunol. 178:2730-2736. https ://doi. org /10. 4049 /jimmunol. 178. 5. 2730
12. Cusimano, M., D. Biziato, E. Brambilla, M. Donegà, C. Alfaro-Cervello, S. Snider, G. Salani, F. Pucci, G. Comi, J.M. Garcia-Verdugo, et al. 2012. Transplanted neural stem/precursor cells instruct phagocytes and reduce secondary tissue damage in the injured spinal cord. Brain. 135:447-460. https ://doi. org /10. 1093 /brain /awr339
13. Daley, D., C.P. Zambirinis, L. Seifert, N. Akkad, N. Mohan, G. Werba, R. Barilla, A. Torres-Hernandez, M. Hundeyin, V.R.K. Mani, et al. 2016. γδ T Cells Support Pancreatic Oncogenesis by Restraining αβ T Cell Activation. Cell. 166:1485-1499.e15. https ://doi. org /10. 1016 /j. cell. 2016. 07. 046
14. David, S., and A. Kroner. 2011. Repertoire of microglial and macrophage responses after spinal cord injury. Nat. Rev. Neurosci. 12:388-399. https ://doi. org /10. 1038 /nrn3053
15. Ding, Y., Y. Qu, J. Feng, M. Wang, Q. Han, K.F. So, W. Wu, and L. Zhou. 2014. Functional motor recovery from motoneuron axotomy is compromised in mice with defective corticospinal projections. PLoS One. 9:e101918. https ://doi. org /10. 1371 /journal. pone. 0101918
16. Fu, Q., M.M. Zou, J.W. Zhu, Y. Zhang, W.J. Chen, M. Cheng, C.F. Liu, Q.H. Ma, and R.X. Xu. 2017. TRIM32 affects the recovery of motor function following spinal cord injury through regulating proliferation of glia. Oncotarget. 8:45380-45390. https ://doi. org /10. 18632 /oncotarget. 17492
17. Fujiyoshi, T., T. Kubo, C.C. Chan, M. Koda, A. Okawa, K. Takahashi, and M. Yamazaki. 2010. Interferon-γ decreases chondroitin sulfate proteoglycan expression and enhances hindlimb function after spinal cord injury in mice. J. Neurotrauma. 27:2283-2294. https ://doi. org /10. 1089 /neu. 2009. 1144
18. Gao, Y., W. Yang, M. Pan, E. Scully, M. Girardi, L.H. Augenlicht, J. Craft, and Z. Yin. 2003. γδ T cells provide an early source of interferon gamma in tumor immunity. J. Exp. Med. 198:433-442. https ://doi. org /10. 1084 / jem. 20030584
19. Genovese, T., E. Mazzon, C. Crisafulli, R. Di Paola, C. Muià, P. Bramanti, and S. Cuzzocrea. 2006. Immunomodulatory effects of etanercept in an experimental model of spinal cord injury. J. Pharmacol. Exp. Ther. 316:1006-1016. https ://doi. org /10. 1124 /jpet. 105. 097188
20. Genovese, T., E. Mazzon, C. Crisafulli, E. Esposito, R. Di Paola, C. Muià, P. Di Bella, R. Meli, P. Bramanti, and S. Cuzzocrea. 2007. Combination of dexamethasone and etanercept reduces secondary damage in experimental spinal cord trauma. Neuroscience. 150:168-181. https ://doi. org /10. 1016 /j. neuroscience. 2007. 06. 059
21. Gordon, S., and P.R. Taylor. 2005. Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5:953-964. https ://doi. org /10. 1038 /nri1733
22. Gu, W., F. Zhang, Q. Xue, Z. Ma, P. Lu, and B. Yu. 2010. Transplantation of bone marrow mesenchymal stem cells reduces lesion volume and induces axonal regrowth of injured spinal cord. Neuropathology. 30:205-217. https ://doi. org /10. 1111 /j. 1440-1789. 2009. 01063. x
23. Hahn, Y.-S., C. Taube, N. Jin, L. Sharp, J.M. Wands, M.K. Aydintug, M. Lahn, S.A. Huber, R.L. O'Brien, E.W. Gelfand, and W.K. Born. 2004. Different potentials of gamma delta T cell subsets in regulating airway responsiveness: V gamma 1+ cells, but not V gamma 4+ cells, promote airway hyperreactivity, Th2 cytokines, and airway inflammation. J. Immunol. 172:2894-2902. https ://doi. org /10. 4049 /jimmunol. 172. 5. 2894
24. Hao, J., S. Dong, S. Xia, W. He, H. Jia, S. Zhang, J. Wei, R.L. O'Brien, W.K. Born, Z. Wu, et al. 2011. Regulatory role of Vγ1 γδ T cells in tumor immunity through IL-4 production. J. Immunol. 187:4979-4986. https ://doi. org /10. 4049 /jimmunol. 1101389
25. He, W., J. Hao, S. Dong, Y. Gao, J. Tao, H. Chi, R. Flavell, R.L. O'Brien, W.K. Born, J. Craft, et al. 2010. Naturally activated V γ 4 γδ T cells play a protective role in tumor immunity through expression of eomesodermin. J. Immunol. 185:126-133. https ://doi. org /10. 4049 /jimmunol. 0903767
26. Heilig, J.S., and S. Tonegawa. 1986. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature. 322:836-840. https ://doi. org /10. 1038 /322836a0
27. Holderness, J., J.F. Hedges, A. Ramstead, and M.A. Jutila. 2013. Comparative biology of γδ T cell function in humans, mice, and domestic animals. Annu. Rev. Anim. Biosci. 1:99-124. https ://doi. org /10. 1146 /annurev-animal-031412-103639
28. Huang, Y., N. Jin, C.L. Roark, M.K. Aydintug, J.M. Wands, H. Huang, R.L. O'Brien, and W.K. Born. 2009. The influence of IgE-enhancing and IgE-suppressive gammadelta T cells changes with exposure to inhaled ovalbumin. J. Immunol. 183:849-855. https ://doi. org /10. 4049 /jimmunol. 0804104
29. Huber, S.A., D. Graveline, M.K. Newell, W.K. Born, and R.L. O'Brien. 2000. V γ 1+ T cells suppress and V γ 4+ T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice. J. Immunol. 165:4174-4181. https ://doi. org /10. 4049 /jimmunol. 165. 8. 4174
30. Ishii, H., S. Tanabe, M. Ueno, T. Kubo, H. Kayama, S. Serada, M. Fujimoto, K. Takeda, T. Naka, and T. Yamashita. 2013. ifn-γ-dependent secretion of IL-10 from Th1 cells and microglia/macrophages contributes to functional recovery after spinal cord injury. Cell Death Dis. 4:e710. https ://doi. org /10. 1038 /cddis. 2013. 234
31. Ito, K., M. Bonneville, Y. Takagaki, N. Nakanishi, O. Kanagawa, E.G. Krecko, and S. Tonegawa. 1989. Different gamma delta T-cell receptors are expressed on thymocytes at different stages of development. Proc. Natl. Acad. Sci. USA. 86:631-635. https ://doi. org /10. 1073 /pnas. 86. 2. 631
32. Itohara, S., P. Mombaerts, J. Lafaille, J. Iacomini, A. Nelson, A.R. Clarke, M.L. Hooper, A. Farr, and S. Tonegawa. 1993. T cell receptor delta gene mutant mice: independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell. 72:337-348. https :// doi. org /10. 1016 /0092-8674(93)90112-4
33. Jensen, K.D., X. Su, S. Shin, L. Li, S. Youssef, S. Yamasaki, L. Steinman, T. Saito, R.M. Locksley, M.M. Davis, et al. 2008. Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity. 29:90-100. https ://doi. org /10. 1016 /j. immuni. 2008. 04. 022
34. Kemény-Beke, A., Z. Szekanecz, S. Szántó, N. Bodnár, L. Módis Jr., R. Gesztelyi, J. Zsuga, P. Szodoray, and A. Berta. 2010. Safety and efficacy of etanercept therapy in ankylosing spondylitis patients undergoing phacoemulsification surgery. Rheumatology (Oxford). 49:2220-2221. https ://doi. org /10. 1093 /rheumatology /keq288
35. Kigerl, K.A., J.C. Gensel, D.P. Ankeny, J.K. Alexander, D.J. Donnelly, and P.G. Popovich. 2009. Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J. Neurosci. 29:13435-13444. https ://doi. org /10. 1523 /JNE URO SCI. 3257-09. 2009
36. Kleine, T.O., P. Zwerenz, P. Zöfel, and K. Shiratori. 2003. New and old diagnostic markers of meningitis in cerebrospinal fluid (CSF). Brain Res. Bull. 61:287-297. https ://doi. org /10. 1016 /S0361-9230(03)00092-3
37. Koenecke, C., V. Chennupati, S. Schmitz, B. Malissen, R. Förster, and I. Prinz. 2009. In vivo application of mAb directed against the gammadelta TCR does not deplete but generates "invisible" gammadelta T cells. Eur. J. Immunol. 39:372-379. https ://doi. org /10. 1002 /eji. 200838741
38. Koopmans, G.C., R. Deumens, W.M. Honig, F.P. Hamers, H.W. Steinbusch, and E.A. Joosten. 2005. The assessment of locomotor function in spinal cord injured rats: the importance of objective analysis of coordination. J. Neurotrauma. 22:214-225. https ://doi. org /10. 1089 /neu. 2005. 22. 214
39. Kwon, B.K., A.M. Stammers, L.M. Belanger, A. Bernardo, D. Chan, C.M. Bishop, G.P. Slobogean, H. Zhang, H. Umedaly, M. Giffin, et al. 2010. Cerebrospinal fluid inflammatory cytokines and biomarkers of injury severity in acute human spinal cord injury. J. Neurotrauma. 27:669-682. https ://doi. org /10. 1089 /neu. 2009. 1080
40. Lech, M., and H.J. Anders. 2013. Macrophages and fibrosis: How resident and infiltrating mononuclear phagocytes orchestrate all phases of tissue injury and repair. Biochim. Biophys. Acta. 1832:989-997. https ://doi. org /10. 1016 /j. bbadis. 2012. 12. 001
41. Libermann, T.A., and D. Baltimore. 1990. Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol. Cell. Biol. 10:2327-2334. https ://doi. org /10. 1128 /MCB. 10. 5. 2327
42. Luan, H., Q. Zhang, L. Wang, C. Wang, M. Zhang, X. Xu, H. Zhou, X. Li, Q. Xu, F. He, et al. 2014. OM85-BV induced the productions of IL-1β, IL-6, and TNF-α via TLR4-and TLR2-mediated ERK1/2/NF-κB pathway in RAW264.7 cells. J. Interferon Cytokine Res. 34:526-536. https ://doi. org /10. 1089 /jir. 2013. 0077
43. Ma, S.F., Y.J. Chen, J.X. Zhang, L. Shen, R. Wang, J.S. Zhou, J.G. Hu, and H.Z. Lü. 2015. Adoptive transfer of M2 macrophages promotes locomotor recovery in adult rats after spinal cord injury. Brain Behav. Immun. 45:157-170. https ://doi. org /10. 1016 /j. bbi. 2014. 11. 007
44. Malik, S., M.Y. Want, and A. Awasthi. 2016. The Emerging Roles of Gamma-Delta T Cells in Tissue Inflammation in Experimental Autoimmune Encephalomyelitis. Front. Immunol. 7:14. https ://doi. org /10. 3389 / fimmu. 2016. 00014
45. Marchand, F., C. Tsantoulas, D. Singh, J. Grist, A.K. Clark, E.J. Bradbury, and S.B. McMahon. 2009. Effects of Etanercept and Minocycline in a rat model of spinal cord injury. Eur. J. Pain. 13:673-681. https ://doi. org /10. 1016 /j. ejpain. 2008. 08. 001
46. Mattson, M.P., and S. Camandola. 2001. NF-kappaB in neuronal plasticity and neurodegenerative disorders. J. Clin. Invest. 107:247-254. https :// doi. org /10. 1172 /JCI11916
47. Mozaffari, S., S. Nikfar, A.H. Abdolghaffari, and M. Abdollahi. 2014. New biologic therapeutics for ulcerative colitis and Crohn's disease. Expert Opin. Biol. Ther. 14:583-600. https ://doi. org /10. 1517 /14712598. 2014. 885945
48. Murray, P.J., J.E. Allen, S.K. Biswas, E.A. Fisher, D.W. Gilroy, S. Goerdt, S. Gordon, J.A. Hamilton, L.B. Ivashkiv, T. Lawrence, et al. 2014. Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity. 41:14-20. https ://doi. org /10. 1016 /j. immuni. 2014. 06. 008
49. Olmos, G., and J. Lladó. 2014. Tumor necrosis factor alpha: a link between neuroinflammation and excitotoxicity. Mediators Inflamm. 2014:861231. https ://doi. org /10. 1155 /2014 /861231
50. Ottum, P.A., G. Arellano, L.I. Reyes, M. Iruretagoyena, and R. Naves. 2015. Opposing Roles of Interferon-Gamma on Cells of the Central Nervous System in Autoimmune Neuroinflammation. Front. Immunol. 6:539. https ://doi. org /10. 3389 /fimmu. 2015. 00539
51. Papoutsaki, M., and A. Costanzo. 2013. Treatment of psoriasis and psoriatic arthritis. BioDrugs. 27(S1, Suppl 1):3-12. https ://doi. org /10. 1007 / BF03325637
52. Pereira, P., D. Gerber, S.Y. Huang, and S. Tonegawa. 1995. Ontogenic development and tissue distribution of V gamma 1-expressing gamma/ delta T lymphocytes in normal mice. J. Exp. Med. 182:1921-1930. https ://doi. org /10. 1084 /jem. 182. 6. 1921
53. Pitt, D., P. Werner, and C.S. Raine. 2000. Glutamate excitotoxicity in a model of multiple sclerosis. Nat. Med. 6:67-70. https ://doi. org /10. 1038 /71555
54. Prescott, K., M. Costner, S. Cohen, and S. Kazi. 2007. Tumor necrosis factoralpha inhibitor associated ulcerative colitis. Am. J. Med. Sci. 333:137-139. https ://doi. org /10. 1097 /MAJ. 0b013e3180312362
55. Prieur, X., C.Y. Mok, V.R. Velagapudi, V. Núñez, L. Fuentes, D. Montaner, K. Ishikawa, A. Camacho, N. Barbarroja, S. O'Rahilly, et al. 2011. Differential lipid partitioning between adipocytes and tissue macrophages modulates macrophage lipotoxicity and M2/M1 polarization in obese mice. Diabetes. 60:797-809. https ://doi. org /10. 2337 /db10-0705
56. Prinz, I., A. Sansoni, A. Kissenpfennig, L. Ardouin, M. Malissen, and B. Malissen. 2006. Visualization of the earliest steps of gammadelta T cell development in the adult thymus. Nat. Immunol. 7:995-1003. https :// doi. org /10. 1038 /ni1371
57. Prinz, I., B. Silva-Santos, and D.J. Pennington. 2013. Functional development of γδ T cells. Eur. J. Immunol. 43:1988-1994. https ://doi. org /10. 1002 / eji. 201343759
58. Ramer, L.M., M.S. Ramer, and E.J. Bradbury. 2014. Restoring function after spinal cord injury: towards clinical translation of experimental strategies. Lancet Neurol. 13:1241-1256. https ://doi. org /10. 1016 /S1474-4422(14)70144-9
59. Rayen, J., T. Currie, R.B. Gearry, F. Frizelle, and T. Eglinton. 2017. The longterm outcome of anti-TNF alpha therapy in perianal Crohn's disease. Tech. Coloproctol. 21:119-124. https ://doi. org /10. 1007 /s10151-016-1578-4
60. Rubiano, A.M., N. Carney, R. Chesnut, and J.C. Puyana. 2015. Global neurotrauma research challenges and opportunities. Nature. 527:S193-S197. https ://doi. org /10. 1038 /nature16035
61. Schmolka, N., M. Wencker, A.C. Hayday, and B. Silva-Santos. 2015. Epigenetic and transcriptional regulation of γδ T cell differentiation: Programming cells for responses in time and space. Semin. Immunol. 27:19-25. https :// doi. org /10. 1016 /j. smim. 2015. 01. 001
62. Schnell, L., S. Fearn, H. Klassen, M.E. Schwab, and V.H. Perry. 1999. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 11:3648-3658. https :// doi. org /10. 1046 /j. 1460-9568. 1999. 00792. x
63. Shichita, T., Y. Sugiyama, H. Ooboshi, H. Sugimori, R. Nakagawa, I. Takada, T. Iwaki, Y. Okada, M. Iida, D.J. Cua, et al. 2009. Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat. Med. 15:946-950. https ://doi. org /10. 1038 /nm. 1999
64. Silver, J., M.E. Schwab, and P.G. Popovich. 2015. Central nervous system regenerative failure: role of oligodendrocytes, astrocytes, and microglia. Cold Spring Harb. Perspect. Biol. 7:a020602. https ://doi. org /10. 1101 / cshperspect. a020602
65. Skeen, M.J., E.P. Rix, M.M. Freeman, and H.K. Ziegler. 2001. Exaggerated proinflammatory and Th1 responses in the absence of gamma/delta T cells after infection with Listeria monocytogenes. Infect. Immun. 69:7213-7223. https ://doi. org /10. 1128 /IAI. 69. 12. 7213-7223. 2001
66. Smith, J.A., R. Zhang, A.K. Varma, A. Das, S.K. Ray, and N.L. Banik. 2009. Estrogen partially down-regulates PTEN to prevent apoptosis in VSC4.1 motoneurons following exposure to IFN-gamma. Brain Res. 1301:163-170. https ://doi. org /10. 1016 /j. brainres. 2009. 09. 016
67. Sumitomo, M., M. Tachibana, J. Nakashima, M. Murai, A. Miyajima, F. Kimura, M. Hayakawa, and H. Nakamura. 1999. An essential role for nuclear factor kappa B in preventing TNF-alpha-induced cell death in prostate cancer cells. J. Urol. 161:674-679. https ://doi. org /10. 1016 / S0022-5347(01)61993-1
68. Ung, R.V., N.P. Lapointe, C. Tremblay, A. Larouche, and P.A. Guertin. 2007. Spontaneous recovery of hindlimb movement in completely spinal cord transected mice: a comparison of assessment methods and conditions. Spinal Cord. 45:367-379. https ://doi. org /10. 1038 /sj. sc. 3101970
69. Victório, S.C., L.P. Cartarozzi, R.C. Hell, and A.L. Oliveira. 2012. Decreased MHC I expression in IFN γ mutant mice alters synaptic elimination in the spinal cord after peripheral injury. J. Neuroinflammation. 9:88. https :// doi. org /10. 1186 /1742-2094-9-88
70. Wang, X., K. Cao, X. Sun, Y. Chen, Z. Duan, L. Sun, L. Guo, P. Bai, D. Sun, J. Fan, et al. 2015. Macrophages in spinal cord injury: phenotypic and functional change from exposure to myelin debris. Glia. 63:635-651. https ://doi. org /10. 1002 /glia. 22774
71. Wu, D., P. Wu, F. Qiu, Q. Wei, and J. Huang. 2017. Human γδT-cell subsets and their involvement in tumor immunity. Cell. Mol. Immunol. 14:245-253. https ://doi. org /10. 1038 /cmi. 2016. 55
72. Yu, X.-J., D.-M. Zhang, L.-L. Jia, J. Qi, X.-A. Song, H. Tan, W. Cui, W. Chen, G.-Q. Zhu, D.-N. Qin, and Y.M. Kang. 2015. Inhibition of NF-κB activity in the hypothalamic paraventricular nucleus attenuates hypertension and cardiac hypertrophy by modulating cytokines and attenuating oxidative stress. Toxicol. Appl. Pharmacol. 284:315-322. https ://doi. org /10. 1016 /j. taap. 2015. 02. 023
73. Zhang, X., R. Goncalves, and D.M. Mosser. 2008. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. https :// doi. org /10. 1002 /0471142735. im1401s83
74. Zhao, N., J. Hao, Y. Ni, W. Luo, R. Liang, G. Cao, Y. Zhao, P. Wang, L. Zhao, Z. Tian, et al. 2011. Vγ4 γδ T cell-derived IL-17A negatively regulates NKT cell function in Con A-induced fulminant hepatitis. J. Immunol. 187:5007-5014. https ://doi. org /10. 4049 /jimmunol. 1101315
75. Zhao, R., Y. Liu, H. Wang, J. Yang, W. Niu, S. Fan, W. Xiong, J. Ma, X. Li, J.B. Phillips, et al. 2017. BRD7 plays an anti-inflammatory role during early acute inflammation by inhibiting activation of the NF-κB signaling pathway. Cell. Mol. Immunol. 14:830-841. https ://doi. org /10. 1038 /cmi. 2016. 31
76. Zhu, E., X. Wang, B. Zheng, Q. Wang, J. Hao, S. Chen, Q. Zhao, L. Zhao, Z. Wu, and Z. Yin. 2014. miR-20b suppresses Th17 differentiation and the pathogenesis of experimental autoimmune encephalomyelitis by targeting RORγt and STAT3. J. Immunol. 192:5599-5609. https ://doi. org /10. 4049 /jimmunol. 1303488