Non-MHC gene regulation of nerve root injury induced spinal cord inflammation and neuron death

Journal of Neuroimmunology

Volumn 101, Issue 1, 1999, Pages 87-97

  Piehl, Fredrik ^a   Lundberg, Cecilia ^a   Khademi, Mohsen ^a   Bucht, Anders ^a   Dahlman, Ingrid ^a   Lorentzen, Johnny C ^a   Olsson, Tomas ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Axotomy; Cytokine; Genetic regulation; Microglia; Nerve cell death

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; NEUROTROPHIC FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE CONTROL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR CLONING; MYELITIS; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NERVE ROOT INJURY; NONHUMAN; PRIORITY JOURNAL; RAT; T LYMPHOCYTE;

ANIMALS; CELL DEATH; CROSSES, GENETIC; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERFERON TYPE II; MAJOR HISTOCOMPATIBILITY COMPLEX; MOTOR NEURONS; MYELITIS; NEUROGLIA; RATS; RATS, INBRED ACI; SPECIES SPECIFICITY; SPINAL NERVE ROOTS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0032752118     PISSN: 01655728     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-5728(99)00136-8     Document Type: Article

References (62)

1. Baker D., Butler D., Scallon B.J., O'Neill J.K., Turk J.L., Feldmann M. Control of established experimental allergic encephalomyelitis by inhibition of tumor necrosis factor (TNF) activity within the central nervous system using monoclonal antibodies and TNF receptor-immunoglobulin fusion proteins. Eur. J. Immunol. 24:1994;2040-2048.
2. Bisby M., Chen S. Delayed wallerian degeneration in sciatic nerves of C57BL/Ola mice is associated with impaired regeneration of sensory axons. Brain Res. 530:1990;117-120.
3. Blight A.R. Effects of silica on the outcome from experimental spinal cord injury: implication of macrophages in secondary tissue damage. Neuroscience. 60:1994;263-273.
4. Chao C., Hu S., Molitor T., Shaskan E., Peterson P. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 149:1992;2736-2741.
5. Chung I.Y., Norris J.G., Benveniste E.N. Differential tumor necrosis factor alpha expression by astrocytes from experimental allergic encephalomyelitis-susceptible and -resistant rat strains. J. Exp. Med. 173:1991;801-811.
6. Dahlman I., Lorentzen J., de Graaf K., Stefferl A., Linington C., Luthman H., Olsson T. Quantitative trait loci disposing for both experimental arthritis and encephalomyelitis in the DA rat; impact on severity of myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis and antibody isotype pattern. Eur. J. Immunol. 28:1998;2188-2196.
7. David S., Bouchard C., Tsatas O., Giftochristos N. Macrophages can modify the nonpermissive nature of the adult mammalian central nervous system. Neuron. 5:1990;463-469.
8. De Simone R., Levi G., Aloisi F. Interferon gamma gene expression in rat central nervous system glial cells. Cytokine. 10:1998;418-422.
9. Encinas J., Lees M., Sobel R., Symonowicz C., Greer J., Shovlin C.L., Weiner H., Seidman C., Seidman J., Kuchroo V. Genetic analysis of susceptibility to experimental autoimmune encephalomyelitis in a cross between SJL/J. and B10.S mice. J. Immunol. 157:1996;2186-2192.
10. Fierz W., Endler B., Reske K., Wekerle H., Fontana A. Astrocytes as antigen-presenting cells: I. Induction of Ia antigen expression on astrocytes by T cells via immune interferon and its effect on antigen presentation. J. Immunol. 134:1985;3785-3793.
11. Giulian D., Corpuz M., Chapman S., Mansouri M., Robertson C. Reactive mononuclear phagocytes release neurotoxins after ischemic and traumatic injury to the central nervous system. J. Neurosci. Res. 36:1993;681-693.
12. Goldschmidt T., Holmdahl R. Therapeutic effects of monoclonal antibodies to alpha beta TCR but not to CD4 on collagen-induced arthritis in the rat. Cell Immunol. 154:1994;240-248.
13. Hedrich, H.J., 1990. List of congenic and segregating inbred strains. In: Hedrich, H.J. (Ed.), Genetic Monitoring of Inbred Strains of Rats, Gustav Fischer Verlag, Stuttgart, p. 481.
14. Hirschberg D.L., Yoles E., Belkin M., Schwartz M. Inflammation after axonal injury has conflicting consequences for recovery of function: rescue of spared axons is impaired but regeneration is supported. J. Neuroimmunol. 50:1994;9-16.
15. Horwitz M., Evans C., McGavern D., Rodriguez M., Oldstone M. Primary demyelination in transgenic mice expressing interferon-gamma. Nat. Med. 3:1997;1037-1041.
16. Issazadeh S., Lorentzen J.C., Mustafa M.I., Höjeberg B., Mussener Å., Olsson T. Cytokines in relapsing experimental autoimmune encephalomyelitis in DA rats: persistent mRNA expression of proinflammatory cytokines and absent expression of interleukin-10 and transforming growth factor-beta. J. Neuroimmunol. 69:1996;103-115.
17. Issazadeh S., Kjellén P., Olsson T., Mustafa M., Holmdahl R. Major histocompatibility complex-controlled protective influences on experimental autoimmune encephalomyelitis are peptide specific. Eur. J. Immunol. 27:1997;1584-1587.
18. Jacob H., Brown D., Bunker R., Daly M., Dzau V., Goodman A., Koike G., Kren V., Kurtz T., Lernmark A.et al. A genetic linkage map of the laboratory rat, Rattus norvegicus. Nat. Genet. 9:1995;63-69.
19. Kiefer R., Lindholm D., Kreutzberg G.W. Interleukin-6 and transforming growth factor-beta 1 mRNAs are induced in rat facial nucleus following motoneuron axotomy. Eur. J. Neurosci. 5:1993;775-781.
20. Kishino A., Ishige Y., Tatsuno T., Nakayama C., Noguchi H. BDNF prevents and reverses adult rat motor neuron degeneration and induces axonal outgrowth. Exp. Neurol. 144:1997;273-286.
21. Koliatsos V.E., Price W.L., Pardo C.A., Price D.L. Ventral root avulsion: an experimental model of death of adult motor neurons. J. Comp. Neurol. 342:1994;35-44.
22. Kreutzberg G.W., Graeber M.B., Streit W.J. Neuron-glial relationship during regeneration of motorneurons. Metab. Brain Dis. 4:1989;81-85.
23. Lee S.C., Dickson D.W., Liu W., Brosnan C.F. Induction of nitric oxide synthase activity in human astrocytes by interleukin-1 beta and interferon-gamma. J. Neuroimmunol. 46:1993;19-24.
24. Lieberman A.R. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 14:1971;49-124.
25. Lorentzen J.C., Issazadeh S., Storch M., Mustafa M.I., Lassmann H., Linington C., Klareskog L., Olsson T. Protracted, relapsing and demyelinating experimental autoimmune encephalomyelitis in DA rats immunized with syngeneic spinal cord and incomplete Freund's adjuvant. J. Neuroimmunol. 63:1995;193-205.
26. Lorentzen J.C., Andersson M., Issazadeh S., Dahlman I., Luthman H., Weissert R., Olsson T. Genetic analysis of inflammation, cytokine mRNA expression and disease course of relapsing experimental autoimmune encephalomyelitis in DA rats. J. Neuroimmunol. 80:1997;31-37.
27. Louis J.C., Magal E., Takayama S., Varon S. CNTF protection of oligodendrocytes against natural and tumor necrosis factor-induced death. Science. 259:1993;689-692.
28. Lu X., Richardson P.M. Inflammation near the nerve cell body enhances axonal regeneration. J. Neurosci. 11:1991;972-978.
29. Maehlen J., Schroder H., Klareskog L., Olsson T., Kristensson K. Axotomy induces MHC class I antigen expression on rat nerve cells. Neurosci. Lett. 92:1988;8-13.
30. Mathieson P., Gillespie K. Cloning of a partial cDNA for rat interleukin-12 (IL-12) and analysis of IL-12 expression in vivo. Scand. J. Immunol. 44:1996;11-14.
31. Mattsson L., Lorentzen J.C., Svelander L., Bucht A., Nyman U., Klareskog L., Larsson P. Immunization with alum-collagen II complex suppresses the development of collagen-induced arthritis in rats by deviating the immune response. Scand. J. Immunol. 46:1997;619-624.
32. Merrill J.E., Ignarro L.J., Sherman M.P., Melinek J., Lane T.E. Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J. Immunol. 151:1993;2132-2141.
33. Mustafa M., Vingsbo C., Olsson T., Issazadeh S., Ljungdahl Å., Holmdahl R. Protective influences on experimental autoimmune encephalomyelitis by MHC class I and class II alleles. J. Immunol. 153:1994;3337-3344.
34. Neumann H., Schmidt H., Cavalie A., Jenne D., Wekerle H. Major histocompatibility complex (MHC) class I gene expression in single neurons of the central nervous system: differential regulation by interferon (IFN)-gamma and tumor necrosis factor (TNF)-alpha. J. Exp. Med. 185:1997;305-316.
35. Neumann H., Schmidt H., Wilharm E., Behrens L., Wekerle H. Interferon gamma gene expression in sensory neurons: evidence for autocrine gene regulation. J. Exp. Med. 186:1997;2023-2031.
36. Novikov L., Novikova L., Kellerth J.O. Brain-derived neurotrophic factor promotes axonal regeneration and long-term survival of adult rat spinal motoneurons in vivo. Neuroscience. 79:1997;765-774.
37. Olsson T. Critical influences of the cytokine orchestration on the outcome of myelin antigen-specific T-cell autoimmunity in experimental autoimmune encephalomyelitis and multiple sclerosis. Immunol. Rev. 144:1995;245-268.
38. Olsson T., Kristensson K., Ljungdahl Å., Maehlen J., Holmdahl R., Klareskog L. Gamma-interferon-like immunoreactivity in axotomized rat motor neurons. J. Neurosci. 9:1989;3870-3875.
39. Perry V., Brown M., Gordon S. The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration. J. Exp. Med. 165:1987;1218-1223.
40. Piani D., Spranger M., Frei K., Schaffner A., Fontana A. Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur. J. Immunol. 22:1992;2429-2436.
41. Piehl F., Tabar G., Cullheim S. Expression of NMDA receptor mRNAs in rat motoneurons is down-regulated after axotomy. Eur. J. Neurosci. 7:1995;2101-2110.
42. Popovich P.G., Wei P., Stokes B.T. Cellular inflammatory response after spinal cord injury in Sprague-Dawley and Lewis rats. J. Comp. Neurol. 377:1996;443-464.
43. Probert L., Akassoglou K., Pasparakis M., Kontogeorgos G., Kollias G. Spontaneous inflammatory demyelinating disease in transgenic mice showing central nervous system-specific expression of tumor necrosis factor alpha. Proc. Natl. Acad. Sci. U.S.A. 92:1995;11294-11298.
44. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite-induced membrane lipid peroxidation: the cytotoxic potential of superoxide and nitric oxide. Arch. Biochem. Biophys. 288:1991;481-487.
45. Raivich G., Jones L.J., Kloss C.U.A., Werner A., Neumann H., Kreutzberg G.W. Immune surveillance in the injured nervous system: T-lymphocytes invade the axotomized mouse facial motor nucleus and aggregate around sites of neuronal degeneration. J. Neurosci. 18:1998;5804-5816.
46. Remmers E., Du Y., Zha H., Goldmuntz E., Wilder R. Ten polymorphic DNA loci, including five in the rat MHC (RT1) region, form a single linkage group on rat chromosome 20. Immunogenetics. 41:1995;316-319.
47. Renno T., Krakowski M., Piccirillo C., Lin J.Y., Owens T. TNF-alpha expression by resident microglia and infiltrating leukocytes in the central nervous system of mice with experimental allergic encephalomyelitis. Regulation by Th1 cytokines. J. Immunol. 154:1995;944-953.
48. Siegling A., Lehmann M., Platzer C., Emmrich F., Volk H. A novel multispecific competitor fragment for quantitative PCR analysis of cytokine gene expression in rats. J. Immunol. Methods. 177:1994;23-28.
49. Steiniger B., van der Meide P. Rat ependyma and microglia cells express class II MHC antigens after intravenous infusion of recombinant gamma interferon. J. Neuroimmunol. 19:1988;111-118.
50. Streit W.J., Graeber M.B., Kreutzberg G.W. Expression of Ia antigen on perivascular and microglial cells after sublethal and lethal motor neuron injury. Exp. Neurol. 105:1989;115-126.
51. Streit W., Semple-Rowland S.L., Hurley S.D., Miller R.C., Popovich P.G., Stokes B.T. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 152:1998;74-87.
52. Sundvall M., Jirholt J., Yang H., Jansson L., Engström A., Pettersson U., Holmdahl R. Identification of murine loci associated with susceptibility to chronic experimental autoimmune encephalomyelitis. Nat. Genet. 10:1995;313-317.
53. Suzumura A., Mezitis S.G., Gonatas N.K., Silberberg D.H. MHC antigen expression on bulk isolated macrophage-microglia from newborn mouse brain: induction of Ia antigen expression by gamma-interferon. J. Neuroimmunol. 15:1987;263-278.
54. Talley A.K., Dewhurst S., Perry S.W., Dollard S.C., Gummuluru S., Fine S.M., New D., Epstein L.G., Gendelman H.E., Gelbard H.A. Tumor necrosis factor alpha-induced apoptosis in human neuronal cells: protection by the antioxidant N-acetylcysteine and the genes bcl-2 and crmA. Mol. Cell. Biol. 15:1995;2359-2366.
55. Trapp B., Peterson J., Ransohoff R., Rudick R., Mørk S., Bø L. Axonal transection in the lesions of multiple sclerosis. N. Engl. J. Med. 338:1998;278-285.
56. van der Veen R.C., Hinton D.R., Incardonna F., Hofman F.M. Extensive peroxynitrite activity during progressive stages of central nervous system inflammation. J. Neuroimmunol. 77:1997;1-7.
57. Vartanian T., Li Y., Zhao M., Stefansson K. Interferon-gamma-induced oligodendrocyte cell death: implications for the pathogenesis of multiple sclerosis. Mol. Med. 1:1995;732-743.
58. Vidovic M., Sparacio S., Elovitz M., Benveniste E. Induction and regulation of class II major histocompatibility complex mRNA expression in astrocytes by interferon-gamma and tumor necrosis factor-alpha. J. Neuroimmunol. 30:1990;189-200.
59. Weissert R., Wallström E., Storch M., Stefferl A., Lorentzen J., Lassmann H., Linington C., Olsson T. MHC haplotype-dependent regulation of MOG-induced EAE in rats. J. Clin. Invest. 102:1998;1265-1273.
60. Williams R., Moore M. Linkage of susceptibility to experimental allergic encephalomyelitis to the major histocompatibility locus in the rat. J. Exp. Med. 138:1973;775-783.
61. Wu W. Potential roles of gene expression change in adult rat spinal motoneurons following axonal injury: a comparison among c-jun, off-affinity nerve growth factor receptor (LNGFR), and nitric oxide synthase (NOS). Exp. Neurol. 141:1996;190-200.
62. Yoshino S., Kinne R., Hünig T., Emmrich F. The suppressive effect of an antibody to the alpha beta cell receptor in rat adjuvant arthritis: studies on optimal treatment protocols. Autoimmunity. 7:1990;255-266.