Axotomy-induced target disconnection promotes an additional death mechanism involved in motoneuron degeneration in amyotrophic lateral sclerosis transgenic mice

Journal of Comparative Neurology

Volumn 522, Issue 10, 2014, Pages 2349-2376

  Haulcomb, Melissa M ^a,b   Mesnard, Nichole A ^a,b   Batka, Richard J ^c,d   Alexander, Thomas D ^b   Sanders, Virginia M ^e   Jones, Kathryn J ^c,d  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b HINES VA HOSPITAL   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d RICHARD L ROUDEBUSH VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

ALS; Facial nerve axotomy; Gene expression; MN; Motoneuron; SOD1

Indexed keywords

DEATH RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR 1; COPPER ZINC SUPEROXIDE DISMUTASE; FAS ANTIGEN; FAS PROTEIN, MOUSE; MESSENGER RNA; SUPEROXIDE DISMUTASE; TNFRSF1A PROTEIN, MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FACIAL NERVE NUCLEUS; FEMALE; GENE EXPRESSION; GLIA CELL; MOUSE; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE FIBER TRANSECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL DEATH; FACIAL NERVE; GENETICS; GLIA; METABOLISM; MOTONEURON; MOTOR ACTIVITY; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIGENS, CD95; AXOTOMY; CELL DEATH; DISEASE PROGRESSION; FACIAL NERVE; FACIAL NUCLEUS; FEMALE; GENE EXPRESSION; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MOTOR NEURONS; NERVE DEGENERATION; NEUROGLIA; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUPEROXIDE DISMUTASE;

EID: 84898687719     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23538     Document Type: Article

References (103)

1. Andersen PM. 2006. Amyotrophic lateral sclerosis associated with mutations in the CuZn superoxide dismutase gene. Curr Neurol Neurosci Rep 6:37-46.
2. Aronica E, Catania MV, Geurts J, Yankaya B, Troost D. 2001. Immunohistochemical localization of group I and II metabotropic glutamate receptors in control and amyotrophic lateral sclerosis human spinal cord: upregulation in reactive astrocytes. Neuroscience 105:509-520.
3. Banati RB, Graeber MB. 1994. Surveillance, intervention and cytotoxicity: is there a protective role of microglia? Dev Neurosci 16:114-127.
4. Beahrs T, Tanzer L, Sanders VM, Jones KJ. 2010. Functional recovery and facial motoneuron survival are influenced by immunodeficiency in crush-axotomized mice. Exp Neurol 221:225-230.
5. Bilsland LG, Sahai E, Kelly G, Golding M, Greensmith L, Schiavo G. 2010. Deficits in axonal transport precede ALS symptoms in vivo. Proc Natl Acad Sci U S A 107:20523-20528.
6. Blinzinger K, Kreutzberg G. 1968. Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z Zellforsch Mikrosk Anat 85:145-157.
7. Brooks BR, Miller RG, Swash M, Munsat TL. 2000. El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis Other Motor Neuron Disord 1:293-299.
8. Brown GC, Bal-Price A. 2003. Inflammatory neurodegeneration mediated by nitric oxide, glutamate, and mitochondria. Mol Neurobiol 27:325-355.
9. Cabal-Hierro L, Lazo PS. 2012. Signal transduction by tumor necrosis factor receptors. Cell Signal 24:1297-1305.
10. Canh MY, Serpe CJ, Sanders V, Jones KJ. 2006. CD4+ T cell-mediated facial motoneuron survival after injury: distribution pattern of cell death and rescue throughout the extent of the facial motor nucleus. J Neuroimmunol 181:93-99.
11. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, Huang D, Kidd G, Dombrowski S, Dutta R, Lee JC, Cook DN, Jung S, Lira SA, Littman DR, Ransohoff RM. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9:917-924.
12. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ. 2000. Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci 20:RC87.
13. Chaudhry V, Clawson LL. 1997. Entrapment of motor nerves in motor neuron disease: does double crush occur? J Neurol Neurosurg Psychiatry 62:71-76.
14. Chen G, Goeddel DV. 2002. TNF-R1 signaling: a beautiful pathway. Science 296:1634-1635.
15. Chen LC, Smith A, Ben Y, Zukic B, Ignacio S, Moore D, Lee N. 2004. Temporal gene expression patterns in G93A/SOD1 mouse. Amyotrophic Lateral Sclerosis Other Motor Neuron Disord 5:164-171.
16. Chiu AY, Zhai P, Dal Canto MC, Peters TM, Kwon YW, Prattis SM, Gurney ME. 1995. Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Mol Cell Neurosci 6:349-362.
17. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, McMahon AP, Doucette W, Siwek D, Ferrante RJ, Brown RH Jr, Julien JP, Goldstein LS, Cleveland DW. 2003. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 302:113-117.
18. Coggeshall RE. 1992. A consideration of neural counting methods. Trends Neurosci 15:9-13.
19. Dadon-Nachum M, Melamed E, Offen D. 2011. The "dying-back" phenomenon of motor neurons in ALS. J Mol Neurosci 43:470-477.
20. Dissing-Olesen L, Ladeby R, Nielsen HH, Toft-Hansen H, Dalmau I, Finsen B. 2007. Axonal lesion-induced microglial proliferation and microglial cluster formation in the mouse. Neuroscience 149:112-122.
21. Facchinetti F, Sasaki M, Cutting FB, Zhai P, MacDonald JE, Reif D, Beal MF, Huang PL, Dawson TM, Gurney ME, Dawson VL. 1999. Lack of involvement of neuronal nitric oxide synthase in the pathogenesis of a transgenic mouse model of familial amyotrophic lateral sclerosis. Neuroscience 90:1483-1492.
22. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. 2004. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci 24:2143-2155.
23. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD. 2004. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185:232-240.
24. Fu SY, Gordon T. 1997. The cellular and molecular basis of peripheral nerve regeneration. Mol Neurobiol 14:67-116.
25. Graeber MB, Tetzlaff W, Streit WJ, Kreutzberg GW. 1988. Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy. Neurosci Lett 85:317-321.
26. Graeber MB, Streit WJ, Kiefer R, Schoen SW, Kreutzberg GW. 1990. New expression of myelomonocytic antigens by microglia and perivascular cells following lethal motor neuron injury. J Neuroimmunol 27:121-132.
27. Grivennikov SI, Kuprash DV, Liu ZG, Nedospasov SA. 2006. Intracellular signals and events activated by cytokines of the tumor necrosis factor superfamily: from simple paradigms to complex mechanisms. Int Rev Cytol 252:129-161.
28. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, et al. 1994. Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science 264:1772-1775.
29. Haenggeli C, Kato AC. 2002. Differential vulnerability of cranial motoneurons in mouse models with motor neuron degeneration. Neurosci Lett 335:39-43.
30. Hailer NP, Grampp A, Nitsch R. 1999. Proliferation of microglia and astrocytes in the dentate gyrus following entorhinal cortex lesion: a quantitative bromodeoxyuridine-labelling study. Eur J Neurosci 11:3359-3364.
31. Harrington JR. 2000. SODD-silencer of death domains. Stem Cells 18:388-389.
32. Hensley K, Floyd RA, Gordon B, Mou S, Pye QN, Stewart C, West M, Williamson K. 2002. Temporal patterns of cytokine and apoptosis-related gene expression in spinal cords of the G93A-SOD1 mouse model of amyotrophic lateral sclerosis. J Neurochem 82:365-374.
33. Hoffman PN, Cleveland DW. 1988. Neurofilament and tubulin expression recapitulates the developmental program during axonal regeneration: induction of a specific beta-tubulin isotype. Proc Natl Acad Sci U S A 85:4530-4533.
34. Holness CL, Simmons DL. 1993. Molecular cloning of CD68, a human macrophage marker related to lysosomal glycoproteins. Blood 81:1607-1613.
35. Hu JH, Chernoff K, Pelech S, Krieger C. 2003. Protein kinase and protein phosphatase expression in the central nervous system of G93A mSOD over-expressing mice. J Neurochem 85:422-431.
36. Ikeda K, Aoki M, Kawazoe Y, Sakamoto T, Hayashi Y, Ishigaki A, Nagai M, Kamii R, Kato S, Itoyama Y, Watabe K. 2005. Motoneuron degeneration after facial nerve avulsion is exacerbated in presymptomatic transgenic rats expressing human mutant Cu/Zn superoxide dismutase. J Neurosci Res 82:63-70.
37. Ilieva H, Polymenidou M, Cleveland DW. 2009. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J Cell Biol 187:761-772.
38. Irwin S. 1968. Comprehensive observational assessment: Ia. A systematic, quantitative procedure for assessing the behavioral and physiologic state of the mouse. Psychopharmacologia 13:222-257.
39. Jones KJ, Oblinger MM. 1994. Androgenic regulation of tubulin gene expression in axotomized hamster facial motoneurons. J Neurosci 14:3620-3627.
40. Jones KJ, Kinderman NB, Oblinger MM. 1997. Alterations in glial fibrillary acidic protein (GFAP) mRNA levels in the hamster facial motor nucleus: effects of axotomy and testosterone. Neurochem Res 22:1359-1366.
41. Jones KJ, Storer PD, Drengler SM, Oblinger MM. 1999. Differential regulation of cytoskeletal gene expression in hamster facial motoneurons: effects of axotomy and testosterone treatment. J Neurosci Res 57:817-823.
42. Kage M, Ikemoto A, Akiguchi I, Kimura J, Matsumoto S, Kimura H, Tooyama I. 1998. Primary structure of GAP-43 mRNA expressed in the spinal cord of ALS patients. Neuroreport 9:1403-1406.
43. Knippenberg S, Thau N, Dengler R, Petri S. 2010. Significance of behavioural tests in a transgenic mouse model of amyotrophic lateral sclerosis (ALS). Behav Brain Res 213:82-87.
44. Kraemer M, Buerger M, Berlit P. 2010. Diagnostic problems and delay of diagnosis in amyotrophic lateral sclerosis. Clin Neurol Neurosurg 112:103-105.
45. Lemstra AW, Groen in't Woud JC, Hoozemans JJ, van Haastert ES, Rozemuller AJ, Eikelenboom P, van Gool WA. 2007. Microglia activation in sepsis: a case-control study. J Neuroinflamm 4:4.
46. Li M, Ona VO, Guegan C, Chen M, Jackson-Lewis V, Andrews LJ, Olszewski AJ, Stieg PE, Lee JP, Przedborski S, Friedlander RM. 2000. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 288:335-339.
47. Lieberman AR. 1971. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int Rev Neurobiol 14:49-124.
48. Liscic RM, Breljak D. 2011. Molecular basis of amyotrophic lateral sclerosis. Prog Neuropsychopharmacol Biol Psychiatry 35:370-372.
49. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-delta delta C(T) method. Methods 25:402-408.
50. Lobsiger CS, Boillee S, Cleveland DW. 2007. Toxicity from different SOD1 mutants dysregulates the complement system and the neuronal regenerative response in ALS motor neurons. Proc Natl Acad Sci U S A 104:7319-7326.
51. Locatelli F, Corti S, Papadimitriou D, Fortunato F, Del Bo R, Donadoni C, Nizzardo M, Nardini M, Salani S, Ghezzi S, Strazzer S, Bresolin N, Comi GP. 2007. Fas small interfering RNA reduces motoneuron death in amyotrophic lateral sclerosis mice. Ann Neurol 62:81-92.
52. Malaspina A, de Belleroche J. 2004. Spinal cord molecular profiling provides a better understanding of amyotrophic lateral sclerosis pathogenesis. Brain Res Brain Res Rev 45:213-229.
53. Marchetti L, Klein M, Schlett K, Pfizenmaier K, Eisel UL. 2004. Tumor necrosis factor (TNF)-mediated neuroprotection against glutamate-induced excitotoxicity is enhanced by N-methyl-D-aspartate receptor activation. Essential role of a TNF receptor 2-mediated phosphatidylinositol 3-kinase-dependent NF-kappa B pathway. J Biol Chem 279:32869-32881.
54. Marcuzzo S, Zucca I, Mastropietro A, de Rosbo NK, Cavalcante P, Tartari S, Bonanno S, Preite L, Mantegazza R, Bernasconi P. 2011. Hind limb muscle atrophy precedes cerebral neuronal degeneration in G93A-SOD1 mouse model of amyotrophic lateral sclerosis: a longitudinal MRI study. Exp Neurol 231:30-37.
55. Mariotti R, Cristino L, Bressan C, Boscolo S, Bentivoglio M. 2002. Altered reaction of facial motoneurons to axonal damage in the presymptomatic phase of a murine model of familial amyotrophic lateral sclerosis. Neuroscience 115:331-335.
56. Martin LJ, Chen K, Liu Z. 2005. Adult motor neuron apoptosis is mediated by nitric oxide and Fas death receptor linked by DNA damage and p53 activation. J Neurosci 25:6449-6459.
57. Mesnard NA, Alexander TD, Sanders VM, Jones KJ. 2010. Use of laser microdissection in the investigation of facial motoneuron and neuropil molecular phenotypes after peripheral axotomy. Exp Neurol 225:94-103.
58. Mesnard NA, Sanders VM, Jones KJ. 2011. Differential gene expression in the axotomized facial motor nucleus of pre-symptomatic SOD1 mice. J Comp Neurol 519:3499-3506.
59. Moran LB, Graeber MB. 2004. The facial nerve axotomy model. Brain Res Brain Res Rev 44:154-178.
60. Moskowitz PF, Oblinger MM. 1995. Transcriptional and posttranscriptional mechanisms regulating neurofilament and tubulin gene expression during normal development of the rat brain. Brain Res Mol Brain Res 30:211-222.
61. Mulder DW, Kurland LT, Offord KP, Beard CM. 1986. Familial adult motor neuron disease: amyotrophic lateral sclerosis. Neurology 36:511-517.
62. Naganska E, Matyja E. 2011. Amyotrophic lateral sclerosis-looking for pathogenesis and effective therapy. Fol Neuropathol 49:1-13.
63. Niessen HG, Angenstein F, Sander K, Kunz WS, Teuchert M, Ludolph AC, Heinze HJ, Scheich H, Vielhaber S. 2006. In vivo quantification of spinal and bulbar motor neuron degeneration in the G93A-SOD1 transgenic mouse model of ALS by T2 relaxation time and apparent diffusion coefficient. Exp Neurol 201:293-300.
64. Nimchinsky EA, Young WG, Yeung G, Shah RA, Gordon JW, Bloom FE, Morrison JH, Hof PR. 2000. Differential vulnerability of oculomotor, facial, and hypoglossal nuclei in G86R superoxide dismutase transgenic mice. J Comp Neurol 416:112-125.
65. Parhad IM, Oishi R, Clark AW. 1992. GAP-43 gene expression is increased in anterior horn cells of amyotrophic lateral sclerosis. Ann Neurol 31:593-597.
66. Perrin FE, Boisset G, Docquier M, Schaad O, Descombes P, Kato AC. 2005. No widespread induction of cell death genes occurs in pure motoneurons in an amyotrophic lateral sclerosis mouse model. Hum Mol Genet 14:3309-3320.
67. Philips T, Robberecht W. 2011. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol 10:253-263.
68. Pramatarova A, Laganiere J, Roussel J, Brisebois K, Rouleau GA. 2001. Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment. J Neurosci 21:3369-3374.
69. Raivich G, Jones LL, Kloss CU, Werner A, Neumann H, Kreutzberg GW. 1998. 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 18:5804-5816.
70. Raivich G, Liu ZQ, Kloss CU, Labow M, Bluethmann H, Bohatschek M. 2002. Cytotoxic potential of proinflammatory cytokines: combined deletion of TNF receptors TNFR1 and TNFR2 prevents motoneuron cell death after facial axotomy in adult mouse. Exp Neurol 178:186-193.
71. Raoul C, Estevez AG, Nishimune H, Cleveland DW, deLapeyriere O, Henderson CE, Haase G, Pettmann B. 2002. Motoneuron death triggered by a specific pathway downstream of Fas. Potentiation by ALS-linked SOD1 mutations. Neuron 35:1067-1083.
72. Raoul C, Buhler E, Sadeghi C, Jacquier A, Aebischer P, Pettmann B, Henderson CE, Haase G. 2006. Chronic activation in presymptomatic amyotrophic lateral sclerosis (ALS) mice of a feedback loop involving Fas, Daxx, and FasL. Proc Natl Acad Sci U S A 103:6007-6012.
73. Reglodi D, Kiss P, Lubics A, Tamas A. 2011. Review on the protective effects of PACAP in models of neurodegenerative diseases in vitro and in vivo. Curr Pharm Des 17:962-972.
74. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, et al. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362:59-62.
75. Rowland LP, Shneider NA. 2001. Amyotrophic lateral sclerosis. N Engl J Med 344:1688-1700.
76. Saeed M, Yang Y, Deng HX, Hung WY, Siddique N, Dellefave L, Gellera C, Andersen PM, Siddique T. 2009. Age and founder effect of SOD1 A4V mutation causing ALS. Neurology 72:1634-1639.
77. Sargsyan SA, Monk PN, Shaw PJ. 2005. Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis. Glia 51:241-253.
78. Satoh J, Nakanishi M, Koike F, Miyake S, Yamamoto T, Kawai M, Kikuchi S, Nomura K, Yokoyama K, Ota K, Kanda T, Fukazawa T, Yamamura T. 2005. Microarray analysis identifies an aberrant expression of apoptosis and DNA damage-regulatory genes in multiple sclerosis. Neurobiol Dis 18:537-550.
79. Schaefer AM, Sanes JR, Lichtman JW. 2005. A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J Comp Neurol 490:209-219.
80. Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108.
81. Serpe CJ, Kohm AP, Huppenbauer CB, Sanders VM, Jones KJ. 1999. Exacerbation of facial motoneuron loss after facial nerve transection in severe combined immunodeficient (scid) mice. J Neurosci 19:RC7.
82. Sharma N, Marzo SJ, Jones KJ, Foecking EM. 2010. Electrical stimulation and testosterone differentially enhance expression of regeneration-associated genes. Exp Neurol 223:183-191.
83. Shibata N. 2001. Transgenic mouse model for familial amyotrophic lateral sclerosis with superoxide dismutase-1 mutation. Neuropathology 21:82-92.
84. Somogyvari-Vigh A, Reglodi D. 2004. Pituitary adenylate cyclase activating polypeptide: a potential neuroprotective peptide. Curr Pharm Des 10:2861-2889.
85. Streit WJ, Kreutzberg GW. 1988. Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248-263.
86. Streit WJ, Graeber MB, Kreutzberg GW. 1988. Functional plasticity of microglia: a review. Glia 1:301-307.
87. Tada S, Okuno T, Yasui T, Nakatsuji Y, Sugimoto T, Kikutani H, Sakoda S. 2011. Deleterious effects of lymphocytes at the early stage of neurodegeneration in an animal model of amyotrophic lateral sclerosis. J Neuroinflam 8:19.
88. Takada H, Chen NJ, Mirtsos C, Suzuki S, Suzuki N, Wakeham A, Mak TW, Yeh WC. 2003. Role of SODD in regulation of tumor necrosis factor responses. Mol Cell Biol 23:4026-4033.
89. Tetzlaff W, Graeber MB, Bisby MA, Kreutzberg GW. 1988. Increased glial fibrillary acidic protein synthesis in astrocytes during retrograde reaction of the rat facial nucleus. Glia 1:90-95.
90. Tetzlaff W, Alexander SW, Miller FD, Bisby MA. 1991. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J Neurosci 11:2528-2544.
91. Turner MR, Cagnin A, Turkheimer FE, Miller CC, Shaw CE, Brooks DJ, Leigh PN, Banati RB. 2004. Evidence of widespread cerebral microglial activation in amyotrophic lateral sclerosis: an [11C](R)-PK11195 positron emission tomography study. Neurobiol Dis 15:601-609.
92. Tweedie D, Sambamurti K, Greig NH. 2007. TNF-alpha inhibition as a treatment strategy for neurodegenerative disorders: new drug candidates and targets. Curr Alzheimers Res 4:378-385.
93. Ueki A, Namba Y, Otsuka M, Okuno M, Nishimura M, Oda M, Ikeda K. 1993. GAP-43 immunoreactivity is detected in the nerve terminals of patients with amyotrophic lateral sclerosis. Ann Neurol 33:226-227.
94. Vanderluit JL, McPhail LT, Fernandes KJ, McBride CB, Huguenot C, Roy S, Robertson GS, Nicholson DW, Tetzlaff W. 2000. Caspase-3 is activated following axotomy of neonatal facial motoneurons and caspase-3 gene deletion delays axotomy-induced cell death in rodents. Eur J Neurosci 12:3469-3480.
95. Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H. 2000. Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 52:269-324.
96. Veroni C, Gabriele L, Canini I, Castiello L, Coccia E, Remoli ME, Columba-Cabezas S, Arico E, Aloisi F, Agresti C. 2010. Activation of TNF receptor 2 in microglia promotes induction of anti-inflammatory pathways. Mol Cell Neurosci 45:234-244.
97. Wainwright DA, Mesnard NA, Xin J, Sanders VM, Jones KJ. 2009. Effects of facial nerve axotomy on Th2-associated and Th1-associated chemokine mRNA expression in the facial motor nucleus of wild-type and presymptomatic SOD1 mice. J Neurodegen Regen 2:39-44.
98. Wijesekera LC, Leigh PN. 2009. Amyotrophic lateral sclerosis. Orphanet J Rare Dis 4:3.
99. Xin J, Wainwright DA, Mesnard NA, Serpe CJ, Sanders VM, Jones KJ. 2011. IL-10 within the CNS is necessary for CD4+ T cells to mediate neuroprotection. Brain Behav Immun 25:820-829.
100. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleveland DW. 2008. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 11:251-253.
101. Yi FH, Lautrette C, Vermot-Desroches C, Bordessoule D, Couratier P, Wijdenes J, Preud'homme JL, Jauberteau MO. 2000. In vitro induction of neuronal apoptosis by anti-Fas antibody-containing sera from amyotrophic lateral sclerosis patients. J Neuroimmunol 109:211-220.
102. Yoshihara T, Ishigaki S, Yamamoto M, Liang Y, Niwa J, Takeuchi H, Doyu M, Sobue G. 2002. Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J Neurochem 80:158-167.
103. Zhou X, Rodriguez WI, Casillas RA, Ma V, Tam J, Hu Z, Lelievre V, Chao A, Waschek JA. 1999. Axotomy-induced changes in pituitary adenylate cyclase activating polypeptide (PACAP) and PACAP receptor gene expression in the adult rat facial motor nucleus. J Neurosci Res 57:953-961.