Use of laser microdissection in the investigation of facial motoneuron and neuropil molecular phenotypes after peripheral axotomy

Experimental Neurology

Volumn 225, Issue 1, 2010, Pages 94-103

  Mesnard, Nichole A ^a,b   Alexander, Thomas D ^b   Sanders, Virginia M ^c   Jones, Kathryn J ^a,b  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b HINES VA HOSPITAL   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Facial motor nucleus; Facial nerve axotomy; Motoneuron; Neuropil; Subnuclei

Indexed keywords

CYTOKINE; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL SURVIVAL; CONTROLLED STUDY; FACIAL NERVE NUCLEUS; FEMALE; GEL ELECTROPHORESIS; GLIA; HYPOTHALAMUS VENTROMEDIAL NUCLEUS; LASER MICRODISSECTION; MOTONEURON; MOUSE; NERVE FIBER TRANSECTION; NEUROPIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; C57BL MOUSE; COMPARATIVE STUDY; DEVICES; DISEASE MODEL; FACIAL NERVE; LOW LEVEL LASER THERAPY; METABOLISM; MICRODISSECTION; PATHOLOGY; PATHOPHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; RETROGRADE DEGENERATION; THALAMUS VENTRAL NUCLEUS;

ANIMALS; AXOTOMY; DISEASE MODELS, ANIMAL; FACIAL NERVE; FEMALE; LASER THERAPY; MICE; MICE, INBRED C57BL; MICRODISSECTION; MOTOR NEURONS; NEUROPIL; PHENOTYPE; PREFRONTAL CORTEX; RETROGRADE DEGENERATION; VENTRAL THALAMIC NUCLEI;

EID: 77955659638     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2010.05.019     Document Type: Article

References (127)

1. Aigner L., Arber S., et al. Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 1995, 83(2):269-278.
2. Akazawa C., Tsuzuki H., et al. The upregulated expression of sonic hedgehog in motor neurons after rat facial nerve axotomy. J. Neurosci. 2004, 24(36):7923-7930.
3. Aldskogius H., Kozlova E.N. Central neuron-glial and glial-glial interactions following axon injury. Prog. Neurobiol. 1998, 55(1):1-26.
4. Ando Y., Liang Y., et al. Caspase-1 and -3 mRNAs are differentially upregulated in motor neurons and glial cells in mutant SOD1 transgenic mouse spinal cord: a study using laser microdissection and real-time RT-PCR. Neurochem. Res. 2003, 28(6):839-846.
5. Armstrong B.D., Hu Z., et al. Lymphocyte regulation of neuropeptide gene expression after neuronal injury. J. Neurosci. Res. 2003, 74(2):240-247.
6. Armstrong B.D., Abad C., et al. Restoration of axotomy-induced PACAP gene induction in SCID mice with CD4+ T-lymphocytes. NeuroReport 2004, 15(17):2647-2650.
7. Armstrong B.D., Hu Z., et al. Induction of neuropeptide gene expression and blockade of retrograde transport in facial motor neurons following local peripheral nerve inflammation in severe combined immunodeficiency and BALB/C mice. Neuroscience 2004, 129(1):93-99.
8. Armstrong B.D., Abad C., et al. Impairment of axotomy-induced pituitary adenylyl cyclase-activating peptide gene expression in T helper 2 lymphocyte-deficient mice. NeuroReport 2006, 17(3):309-312.
9. Armstrong B.D., Abad C., et al. Impaired nerve regeneration and enhanced neuroinflammatory response in mice lacking pituitary adenylyl cyclase activating peptide. Neuroscience 2008, 151(1):63-73.
10. Ashwell K.W. The adult mouse facial nerve nucleus: morphology and musculotopic organization. J. Anat. 1982, 135(Pt 3):531-538.
11. Azoulay D., Urshansky N., et al. Low and dysregulated BDNF secretion from immune cells of MS patients is related to reduced neuroprotection. J. Neuroimmunol. 2008, 195(1-2):186-193.
12. Baker S.J., Reddy E.P. Modulation of life and death by the TNF receptor superfamily. Oncogene 1998, 17(25):3261-3270.
13. Besser M., Wank R. Cutting edge: clonally restricted production of the neurotrophins brain-derived neurotrophic factor and neurotrophin-3 mRNA by human immune cells and Th1/Th2-polarized expression of their receptors. J. Immunol. 1999, 162(11):6303-6306.
14. Bigini P., Mennini T. Immunohistochemical localization of TNFalpha and its receptors in the rodent central nervous system. Meth. Mol. Med. 2004, 98:73-80.
15. Bignami A., Eng L.F., et al. Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res. 1972, 43(2):429-435.
16. Blinzinger K., Kreutzberg G. Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z. Zellforsch. Mikrosk. Anat. 1968, 85(2):145-157.
17. Bruce-Keller A.J. Microglial-neuronal interactions in synaptic damage and recovery. J. Neurosci. Res. 1999, 58(1):191-201.
18. Byram S.C., Serpe C.J., et al. Natural killer cells do not mediate facial motoneuron survival after facial nerve transection. Brain Behav. Immun. 2003, 17(6):417-425.
19. Byram S.C., Carson M.J., et al. CD4-positive T cell-mediated neuroprotection requires dual compartment antigen presentation. J. Neurosci. 2004, 24(18):4333-4339.
20. Canh M.Y., Serpe C.J., et al. 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. 2006, 181(1-2):93-99.
21. Chen K., Huang J., et al. CD40/CD40L dyad in the inflammatory and immune responses in the central nervous system. Cell. Mol. Immunol. 2006, 3(3):163-169.
22. Davalos D., Grutzendler J., et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat. Neurosci. 2005, 8(6):752-758.
23. de Haas A.H., van Weering H.R., et al. Neuronal chemokines: versatile messengers in central nervous system cell interaction. Mol. Neurobiol. 2007, 36(2):137-151.
24. DeBoy C.A., Byram S.C., et al. CD4+CD25+ regulatory T cells and CD1-restricted NKT cells do not mediate facial motoneuron survival after axotomy. J. Neuroimmunol. 2006, 176(1-2):34-38.
25. Delgado M., Munoz-Elias E.J., et al. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide enhance IL-10 production by murine macrophages: in vitro and in vivo studies. J. Immunol. 1999, 162(3):1707-1716.
26. Delgado M., Pozo D., et al. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit endotoxin-induced TNF-alpha production by macrophages: in vitro and in vivo studies. J. Immunol. 1999, 162(4):2358-2367.
27. Delgado M., Jonakait G.M., et al. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit chemokine production in activated microglia. Glia 2002, 39(2):148-161.
28. Delgado M., Leceta J., et al. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide promote in vivo generation of memory Th2 cells. FASEB J. 2002, 16(13):1844-1846.
29. Delgado M., Leceta J., et al. Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit the production of inflammatory mediators by activated microglia. J. Leukoc. Biol. 2003, 73(1):155-164.
30. Engh C.A., Schofield B.H. A review of the central response to peripheral nerve injury and its significance in nerve regeneration. J. Neurosurg. 1972, 37(2):195-203.
31. Fargo K.N., Alexander T.D., et al. Androgen regulates neuritin mRNA levels in an in vivo model of steroid-enhanced peripheral nerve regeneration. J. Neurotrauma 2008, 25(5):561-566.
32. Fawcett J.W., Keynes R.J. Peripheral nerve regeneration. Annu. Rev. Neurosci. 1990, 13:43-60.
33. Friedlander R.M. Apoptosis and caspases in neurodegenerative diseases. N. Engl. J. Med. 2003, 348(14):1365-1375.
34. Fu S.Y., Gordon T. The cellular and molecular basis of peripheral nerve regeneration. Mol. Neurobiol. 1997, 14(1-2):67-116.
35. Galiano M., Liu Z.Q., et al. Interleukin-6 (IL6) and cellular response to facial nerve injury: effects on lymphocyte recruitment, early microglial activation and axonal outgrowth in IL6-deficient mice. Eur. J. Neurosci. 2001, 14(2):327-341.
36. Gehrmann J., Mies G., et al. Microglial reaction in the rat cerebral cortex induced by cortical spreading depression. Brain Pathol. 1993, 3(1):11-17.
37. Gomariz R.P., Juarranz Y., et al. VIP-PACAP system in immunity: new insights for multitarget therapy. Ann. N. Y. Acad. Sci. 2006, 1070:51-74.
38. Gordon T. The role of neurotrophic factors in nerve regeneration. Neurosurg. Focus 2009, 26(2):E3.
39. Goto T., Hisatomi O., et al. Induced expression of hematopoietic- and neurologic-expressed sequence 1 in retinal pigment epithelial cells during newt retina regeneration. Exp. Eye Res. 2006, 83(4):972-980.
40. Graeber M.B., Kreutzberg G.W. Delayed astrocyte reaction following facial nerve axotomy. J. Neurocytol. 1988, 17(2):209-220.
41. Graeber M.B., Tetzlaff W., et al. Microglial cells but not astrocytes undergo mitosis following rat facial nerve axotomy. Neurosci. Lett. 1988, 85(3):317-321.
42. Guirland C., Buck K.B., et al. Direct cAMP signaling through G-protein-coupled receptors mediates growth cone attraction induced by pituitary adenylate cyclase-activating polypeptide. J. Neurosci. 2003, 23(6):2274-2283.
43. Guntinas-Lichius O., Neiss W.F., et al. Quantitative image analysis of the chromatolysis in rat facial and hypoglossal motoneurons following axotomy with and without reinnervation. Cell Tissue Res. 1996, 286(3):537-541.
44. Ha G.K., Huang Z., et al. Endogenous T lymphocytes and microglial reactivity in the axotomized facial motor nucleus of mice: effect of genetic background and the RAG2 gene. J. Neuroimmunol. 2006, 172(1-2):1-8.
45. Hall S.M. Regeneration in the peripheral nervous system. Neuropathol. Appl. Neurobiol. 1989, 15(6):513-529.
46. Hanisch U.K. Microglia as a source and target of cytokines. Glia 2002, 40(2):140-155.
47. Harrison J.K., Jiang Y., et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(18):10896-10901.
48. Hickey W.F., Hsu B.L., et al. T-lymphocyte entry into the central nervous system. J. Neurosci. Res. 1991, 28(2):254-260.
49. Hoffman P.N., Cleveland D.W. 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. 1988, 85(12):4530-4533.
50. Huang Z., Ha G.K., et al. IL-15 and IL-15R alpha gene deletion: effects on T lymphocyte trafficking and the microglial and neuronal responses to facial nerve axotomy. Neurosci. Lett. 2007, 417(2):160-164.
51. Hurley S.D., Coleman P.D. Facial nerve axotomy in aged and young adult rats: analysis of the glial response. Neurobiol. Aging 2003, 24(3):511-518.
52. Jones K.J., LaVelle A. Changes in nuclear envelope invaginations in axotomized immature and mature hamster facial motoneurons. Brain Res. 1985, 353(2):241-249.
53. Jones K.J., Lavelle A. Differential effects of axotomy on immature and mature hamster facial neurons: a time course study of initial nucleolar and nuclear changes. J. Neurocytol. 1986, 15(2):197-206.
54. Jones K.J., Oblinger M.M. Androgenic regulation of tubulin gene expression in axotomized hamster facial motoneurons. J. Neurosci. 1994, 14(6):3620-3627.
55. Jones K.J., Drengler S.M., et al. Gonadal steroid regulation of growth-associated protein GAP-43 mRNA expression in axotomized hamster facial motor neurons. Neurochem. Res. 1997, 22(11):1367-1374.
56. Jones K.J., Kinderman N.B., et al. Alterations in glial fibrillary acidic protein (GFAP) mRNA levels in the hamster facial motor nucleus: effects of axotomy and testosterone. Neurochem. Res. 1997, 22(11):1359-1366.
57. Jones K.J., Coers S., et al. Androgenic regulation of the central glia response following nerve damage. J. Neurobiol. 1999, 40(4):560-573.
58. Jones K.J., Storer P.D., et al. Differential regulation of cytoskeletal gene expression in hamster facial motoneurons: effects of axotomy and testosterone treatment. J. Neurosci. Res. 1999, 57(6):817-823.
59. Jones K.J., Alexander T.D., et al. Gonadal steroid enhancement of facial nerve regeneration: role of heat shock protein 70. J. Neurocytol. 2000, 29(5-6):341-349.
60. Jones K.J., Serpe C.J., et al. Role of the immune system in the maintenance of mouse facial motoneuron viability after nerve injury. Brain Behav. Immun. 2005, 19(1):12-19.
61. Kalla R., Liu Z., et al. Microglia and the early phase of immune surveillance in the axotomized facial motor nucleus: impaired microglial activation and lymphocyte recruitment but no effect on neuronal survival or axonal regeneration in macrophage-colony stimulating factor-deficient mice. J. Comp. Neurol. 2001, 436(2):182-201.
62. Kiefer R., Gold R., et al. Transforming growth factor beta expression in reactive spinal cord microglia and meningeal inflammatory cells during experimental allergic neuritis. J. Neurosci. Res. 1993, 36(4):391-398.
63. Kim W.K., Kan Y., et al. Vasoactive intestinal peptide and pituitary adenylyl cyclase-activating polypeptide inhibit tumor necrosis factor-alpha production in injured spinal cord and in activated microglia via a cAMP-dependent pathway. J. Neurosci. 2000, 20(10):3622-3630.
64. Kobayashi N.R., Bedard A.M., et al. Increased expression of BDNF and trkB mRNA in rat facial motoneurons after axotomy. Eur. J. Neurosci. 1996, 8(5):1018-1029.
65. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19(8):312-318.
66. Kreutzberg G.W. Principles of neuronal regeneration. Acta Neurochir. Suppl. 1996, 66:103-106.
67. Kreutzberg G.W., Graeber M.B., et al. Neuron-glial relationship during regeneration of motorneurons. Metab. Brain Dis. 1989, 4(1):81-85.
68. Laskawi R., Wolff J.R. Changes in glial fibrillary acidic protein immunoreactivity in the rat facial nucleus following various types of nerve lesions. Eur. Arch. Otorhinolaryngol. 1996, 253(8):475-480.
69. Lieberman A.R. The axon reaction: a review of the principal features of perikaryal responses to axon injury. Int. Rev. Neurobiol. 1971, 14:49-124.
70. Liuzzi F.J., Tedeschi B. Peripheral nerve regeneration. Neurosurg. Clin. N. Am. 1991, 2(1):31-42.
71. Mader K., Andermahr J., et al. Dual mode of signalling of the axotomy reaction: retrograde electric stimulation or block of retrograde transport differently mimic the reaction of motoneurons to nerve transection in the rat brainstem. J. Neurotrauma 2004, 21(7):956-968.
72. Martin L.J., Chen K., et al. Adult motor neuron apoptosis is mediated by nitric oxide and Fas death receptor linked by DNA damage and p53 activation. J. Neurosci. 2005, 25(27):6449-6459.
73. Meyer M., Matsuoka I., et al. Enhanced synthesis of brain-derived neurotrophic factor in the lesioned peripheral nerve: different mechanisms are responsible for the regulation of BDNF and NGF mRNA. J. Cell Biol. 1992, 119(1):45-54.
74. Mojsilovic-Petrovic J., Jeong G.B., et al. Protecting motor neurons from toxic insult by antagonism of adenosine A2a and Trk receptors. J. Neurosci. 2006, 26(36):9250-9263.
75. Moran L.B., Graeber M.B. The facial nerve axotomy model. Brain Res. Brain Res. Rev. 2004, 44(2-3):154-178.
76. Moskowitz P.F., Oblinger M.M. Transcriptional and post-transcriptional mechanisms regulating neurofilament and tubulin gene expression during normal development of the rat brain. Brain Res. Mol. Brain Res. 1995, 30(2):211-222.
77. Namgung U., Routtenberg A. Transcriptional and post-transcriptional regulation of a brain growth protein: regional differentiation and regeneration induction of GAP-43. Eur. J. Neurosci. 2000, 12(9):3124-3136.
78. Nimmerjahn A., Kirchhoff F., et al. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308(5726):1314-1318.
79. Oliveira A.L., Thams S., et al. A role for MHC class I molecules in synaptic plasticity and regeneration of neurons after axotomy. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(51):17843-17848.
80. Olsson T., Kristensson K., et al. Gamma-interferon-like immunoreactivity in axotomized rat motor neurons. J. Neurosci. 1989, 9(11):3870-3875.
81. Paden C.M., Zhou X., et al. Distribution of growth-associated class I alpha-tubulin and class II beta-tubulin mRNAs in adult rat brain. J. Comp. Neurol. 1995, 362(3):368-384.
82. Palacios G., Mengod G., et al. De novo synthesis of GAP-43: in situ hybridization histochemistry and light and electron microscopy immunocytochemical studies in regenerating motor neurons of cranial nerve nuclei in the rat brain. Brain Res. Mol. Brain Res. 1994, 24(1-4):107-117.
83. Raff M.C., Whitmore A.V., et al. Axonal self-destruction and neurodegeneration. Science 2002, 296(5569):868-871.
84. Raivich G. Like cops on the beat: the active role of resting microglia. Trends Neurosci. 2005, 28(11):571-573.
85. Raivich G., Jones L.L., et al. 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. 1998, 18(15):5804-5816.
86. Raivich G., Liu Z.Q., et al. 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. 2002, 178(2):186-193.
87. Raivich G., Bohatschek M., et al. Lymphocyte infiltration in the injured brain: role of proinflammatory cytokines. J. Neurosci. Res. 2003, 72(6):726-733.
88. Saika T., Kiyama H., et al. GAP-43 mRNA expression in facial motoneurons during regeneration: in situ hybridization histochemistry study using an alkaline phosphatase-labelled probe. Acta Otolaryngol. Suppl. 1993, 501:80-84.
89. Sanders V.M., Jones K.J. Role of immunity in recovery from a peripheral nerve injury. J. Neuroimmune Pharmacol. 2006, 1(1):11-19.
90. Schiefer J., Kampe K., et al. Microglial motility in the rat facial nucleus following peripheral axotomy. J. Neurocytol. 1999, 28(6):439-453.
91. Schoen S.W., Graeber M.B., et al. 5'-Nucleotidase immunoreactivity of perineuronal microglia responding to rat facial nerve axotomy. Glia 1992, 6(4):314-317.
92. Schoenborn J.R., Wilson C.B. Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 2007, 96:41-101.
93. Schwaiger F.W., Hager G., et al. Cellular activation in neuroregeneration. Prog. Brain Res. 1998, 117:197-210.
94. Sendtner M., Kreutzberg G.W., et al. Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 1990, 345(6274):440-441.
95. Sendtner M., Holtmann B., et al. Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 1992, 360(6406):757-759.
96. Serpe C.J., Kohm A.P., et al. Exacerbation of facial motoneuron loss after facial nerve transection in severe combined immunodeficient (scid) mice. J. Neurosci. 1999, 19(11):RC7.
97. Serpe C.J., Sanders V.M., et al. Kinetics of facial motoneuron loss following facial nerve transection in severe combined immunodeficient mice. J. Neurosci. Res. 2000, 62(2):273-278.
98. Serpe C.J., Coers S., et al. CD4+ T, but not CD8+ or B, lymphocytes mediate facial motoneuron survival after facial nerve transection. Brain Behav. Immun. 2003, 17(5):393-402.
99. Serpe C.J., Byram S.C., et al. Brain-derived neurotrophic factor supports facial motoneuron survival after facial nerve transection in immunodeficient mice. Brain Behav. Immun. 2005, 19(2):173-180.
100. Sharma N., Marzo S.J., et al. Electrical stimulation and testosterone differentially enhance expression of regeneration-associated genes. Exp. Neurol. 2009.
101. Shioda S., Ohtaki H., et al. Pleiotropic functions of PACAP in the CNS: neuroprotection and neurodevelopment. Ann. N. Y. Acad. Sci. 2006, 1070:550-560.
102. Skene J.H. Axonal growth-associated proteins. Annu. Rev. Neurosci. 1989, 12:127-156.
103. Skene J.H., Willard M. Axonally transported proteins associated with axon growth in rabbit central and peripheral nervous systems. J. Cell Biol. 1981, 89(1):96-103.
104. Stoll G., Muller H.W. Nerve injury, axonal degeneration and neural regeneration: basic insights. Brain Pathol. 1999, 9(2):313-325.
105. Storer P.D., Jones K.J. Glial fibrillary acidic protein expression in the hamster red nucleus: effects of axotomy and testosterone treatment. Exp. Neurol. 2003, 184(2):939-946.
106. Streit W.J. Microglial-neuronal interactions. J. Chem. Neuroanat. 1993, 6(4):261-266.
107. Streit W.J. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 2002, 40(2):133-139.
108. Streit W.J., Semple-Rowland S.L., et al. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp. Neurol. 1998, 152(1):74-87.
109. Strittmatter S.M., Valenzuela D., et al. Growth cone transduction: Go and GAP-43. J. Cell Sci. Suppl. 1991, 15:27-33.
110. Suarez V., Guntinas-Lichius O., et al. The axotomy-induced neuropeptides galanin and pituitary adenylate cyclase-activating peptide promote axonal sprouting of primary afferent and cranial motor neurones. Eur. J. Neurosci. 2006, 24(6):1555-1564.
111. Tang W., Lai Y.H., et al. Murine Hn1 on chromosome 11 is expressed in hemopoietic and brain tissues. Mamm. Genome 1997, 8(9):695-696.
112. Tetzlaff W., Bisby M.A., et al. Changes in cytoskeletal proteins in the rat facial nucleus following axotomy. J. Neurosci. 1988, 8(9):3181-3189.
113. Tetzlaff W., Graeber M.B., et al. Increased glial fibrillary acidic protein synthesis in astrocytes during retrograde reaction of the rat facial nucleus. Glia 1988, 1(1):90-95.
114. Tetzlaff W., Alexander S.W., et al. Response of facial and rubrospinal neurons to axotomy: changes in mRNA expression for cytoskeletal proteins and GAP-43. J. Neurosci. 1991, 11(8):2528-2544.
115. Thorburn A. Death receptor-induced cell killing. Cell. Signal. 2004, 16(2):139-144.
116. Veglianese P., Lo Coco D., et al. Activation of the p38MAPK cascade is associated with upregulation of TNF alpha receptors in the spinal motor neurons of mouse models of familial ALS. Mol. Cell. Neurosci. 2006, 31(2):218-231.
117. Verge G.M., Milligan E.D., et al. Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur. J. Neurosci. 2004, 20(5):1150-1160.
118. Wainwright D.A., Xin J., et al. Effects of facial nerve axotomy on Th2- and Th1-associated chemokine expression in the facial motor nucleus of wild-type and presymptomatic mSOD1 mice. J. Neuroimmunol. 2009, 216(1-2):66-75.
119. Wainwright D.A., Xin J., et al. Exacerbation of facial motoneuron loss after facial nerve axotomy in CCR3-deficient mice. ASN Neuro 2009.
120. Widenfalk J., Lundstromer K., et al. Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J. Neurosci. 2001, 21(10):3457-3475.
121. Xin J., Wainwright D.A., et al. Phenotype of CD4+ T cell subsets that develop following mouse facial nerve axotomy. Brain Behav. Immun. 2008, 22(4):528-537.
122. Yan Q., Matheson C., et al. The biological responses of axotomized adult motoneurons to brain-derived neurotrophic factor. J. Neurosci. 1994, 14(9):5281-5291.
123. Zhang Y.Z., Hannibal J., et al. Pituitary adenylate cyclase activating peptide expression in the rat dorsal root ganglia: up-regulation after peripheral nerve injury. Neuroscience 1996, 74(4):1099-1110.
124. Zhao Z., Alam S., et al. Overexpression of glial cell line-derived neurotrophic factor in the CNS rescues motoneurons from programmed cell death and promotes their long-term survival following axotomy. Exp. Neurol. 2004, 190(2):356-372.
125. Zhou X., Rodriguez W.I., et al. 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. 1999, 57(6):953-961.
126. Zhuang Z.Y., Kawasaki Y., et al. Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injury-induced cleavage of fractalkine. Brain Behav. Immun. 2007, 21(5):642-651.
127. Zujovic V., Luo D., et al. The facial motor nucleus transcriptional program in response to peripheral nerve injury identifies Hn1 as a regeneration-associated gene. J. Neurosci. Res. 2005, 82(5):581-591.