L1 cell adhesion molecule is essential for the maintenance of hyperalgesia after spinal cord injury

Experimental Neurology

Volumn 216, Issue 1, 2009, Pages 22-34

  Hoschouer, Emily L ^a,b,c   Yin, Feng Qin ^a,c   Jakeman, Lyn B ^a,b,c  

^a Department of Physiology and Cell Biology ^*  (United States)

^b Neurbio Anat Div Neurosci O   (United States)

^c THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Allodynia; Calcitonin gene related peptide; Neuropathic pain; Plasticity; Primary afferent; Protein kinase C; Sensory; Sprouting

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NERVE CELL ADHESION MOLECULE L1; PROTEIN KINASE C GAMMA;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HOT PLATE TEST; HYPERALGESIA; IMMUNOCYTOCHEMISTRY; KNOCKOUT MOUSE; LATENT PERIOD; MALE; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NERVE CELL PLASTICITY; NERVE SPROUTING; NEUROPATHIC PAIN; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; SENSORY NERVE; SPINAL CORD INJURY;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CELL ADHESION; GROWTH CONES; HYPERALGESIA; INTERNEURONS; MALE; MICE; MICE, KNOCKOUT; NEURAL CELL ADHESION MOLECULE L1; NEURONAL PLASTICITY; POSTERIOR HORN CELLS; PROTEIN KINASE C; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; SPINAL NERVE ROOTS; UP-REGULATION;

EID: 59749093986     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2008.10.025     Document Type: Article

References (88)

1. Akopians A., Runyan S.A., and Phelps P.E. Expression of L1 decreases during postnatal development of rat spinal cord. J. Comp. Neurol. 467 (2003) 375-388
2. Anderson K.D. Targeting recovery: priorities of the spinal cord-injured population. J. Neurotrauma 21 (2004) 1371-1383
3. Arami S., Jucker M., Schachner M., and Welzl H. The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav. Brain Res. 81 (1996) 81-87
4. Basso D.M., Fisher L.C., Anderson A.J., Jakeman L.B., McTigue D.M., and Popovich P.G. Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J. Neurotrauma 23 (2006) 635-659
5. Becker C.G., Lieberoth B.C., Morellini F., Feldner J., Becker T., and Schachner M. L1.1 is involved in spinal cord regeneration in adult zebrafish. J. Neurosci. 24 (2004) 7837-7842
6. Becker T., Lieberoth B.C., Becker C.G., and Schachner M. Differences in the regenerative response of neuronal cell populations and indications for plasticity in intraspinal neurons after spinal cord transection in adult zebrafish. Mol. Cell. Neurosci. 30 (2005) 265-278
7. Beggs S., and Salter M.W. Stereological and somatotopic analysis of the spinal microglial response to peripheral nerve injury. Brain Behav. Immun. 21 (2007) 624-633
8. Bennett A.D., Everhart A.W., and Hulsebosch C.E. Intrathecal administration of an NMDA or a non-NMDA receptor antagonist reduces mechanical but not thermal allodynia in a rodent model of chronic central pain after spinal cord injury. Brain Res. 859 (2000) 72-82
9. Bradbury E.J., Khemani S., King V.R., Priestley J.V., and McMahon S.B. NT-3 promotes growth of lesioned adult rat sensory axons ascending in the dorsal columns of the spinal cord. Eur. J. Neurosci. 11 (1999) 3873-3883
10. Bradbury E.J., and McMahon S.B. Spinal cord repair strategies: why do they work?. Nat. Rev. Neurosci. 7 (2006) 644-653
11. Brenner G.J., Ji R.R., Shaffer S., and Woolf C.J. Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. Eur. J. Neurosci. 20 2 (2004) 375-384
12. Burden-Gulley S.M., Pendergast M., and Lemmon V. The role of cell adhesion molecule L1 in axonal extension, growth cone motility, and signal transduction. Cell Tiss. Res. 290 (1997) 415-422
13. Cameron A.A., Smith G.M., Randall D.C., Brown D.R., and Rabchevsky A.G. Genetic manipulation of intraspinal plasticity after spinal cord injury alters the severity of autonomic dysreflexia. J. Neurosci. 26 (2006) 2923-2932
14. Castellani V., Chedotal A., Schachner M., Faivre-Sarrailh C., and Rougon G. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron. 27 (2000) 237-249
15. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., and Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53 (1994) 55-63
16. Chaudhry N., de S.U., and Smith G.M. Cell adhesion molecule L1 modulates nerve-growth-factor-induced CGRP-IR fiber sprouting. Exp. Neurol. 202 (2006) 238-249
17. Chen J., Wu J., Apostolova I., Skup M., Irintchev A., Kugler S., and Schachner M. Adeno-associated virus-mediated L1 expression promotes functional recovery after spinal cord injury. Brain 130 (2007) 954-969
18. Christensen M.D., and Hulsebosch C.E. Spinal cord injury and anti-NGF treatment results in changes in CGRP density and distribution in the dorsal horn in the rat. Exp. Neurol. 147 (1997) 463-475
19. Cohen N.R., Taylor J.S., Scott L.B., Guillery R.W., Soriano P., and Furley A.J. Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Current biology : CB 8 (1998) 26-33
20. Dahme M., Bartsch U., Martini R., Anliker B., Schachner M., and Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nature Genetics 17 (1997) 346-349
21. Demyanenko G.P., Tsai A.Y., and Maness P.F. Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knockout mice. J. Neurosci. 19 (1999) 4907-4920
22. Detloff M.R., Fisher L.C., McGaughy V., Longbrake E.E., Popovich P.G., and Basso D.M. Remote activation of microglia and pro-inflammatory cytokines predict the onset and severity of below-level neuropathic pain after spinal cord injury in rats. Exp. Neurol. 212 (2008) 337-347
23. Deumens R., Joosten E.A., Waxman S.G., and Hains B.C. Locomotor dysfunction and pain: the scylla and charybdis of fiber sprouting after spinal cord injury. Mol. Neurobiol. 37 (2008) 52-63
24. Deumens R., Lubbers M., Jaken R.J., Meijs M.F., Thurlings R.M., Honig W.M., Schachner M., Brook G.A., and Joosten E.A. Mice lacking L1 have reduced CGRP fibre in-growth into spinal transection lesions. Neurosci. Lett. 420 (2007) 277-281
25. Dixon W.J. Efficient analysis of experimental observations. Annu. Rev. Pharmacol. Toxicol. 20 (1980) 441-462
26. Dobkin B.H., and Havton L.A. Basic advances and new avenues in therapy of spinal cord injury. Annu. Rev. Med. 55 (2004) 255-282
27. Engesser-Cesar C., Anderson A.J., Basso D.M., Edgerton V.R., and Cotman C.W. Voluntary wheel running improves recovery from a moderate spinal cord injury. J. Neurotrauma 22 (2005) 157-171
28. Feeney D.M., Gonzalez A., and Law W.A. Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science 217 (1982) 855-857
29. Finnerup N.B., Johannesen I.L., Bach F.W., and Jensen T.S. Sensory function above lesion level in spinal cord injury patients with and without pain. Somatosens. Mot. Res. 20 (2003) 71-76
30. Fransen E., D'Hooge R., Van Camp G., Verhoye M., Sijbers J., Reyniers E., Soriano P., Kamiguchi H., Willemsen R., Koekkoek S.K., De Zeeuw C.I., De Deyn P.P., Van der Linden A., Lemmon V., Kooy R.F., and Willems P.J. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Human Mol. Genet. 7 (1998) 999-1009
31. Godenschwege T.A., Kristiansen L.V., Uthaman S.B., Hortsch M., and Murphey R.K. A conserved role for Drosophila Neuroglian and human L1-CAM in central-synapse formation. Curr. Biol. 16 (2006) 12-23
32. Hains B.C., and Waxman S.G. Activated microglia contribute to the maintenance of chronic pain after spinal cord injury. J. Neurosci. 26 (2006) 4308-4317
33. Hald A., Nedergaard S., Hansen R.R., Ding M., and Heegaard A.M. Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain. Eur. J. Pain (2008)
34. Haney C.A., Sahenk Z., Li C., Lemmon V.P., Roder J., and Trapp B.D. Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival. J. Cell Biol. 146 (1999) 1173-1184
35. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
36. Hofstetter C.P., Holmstrom N.A., Lilja J.A., Schweinhardt P., Hao J., Spenger C., Wiesenfeld-Hallin Z., Kurpad S.N., Frisen J., and Olson L. Allodynia limits the usefulness of intraspinal neural stem cell grafts; directed differentiation improves outcome. Nat. Neurosci. 8 (2005) 346-353
37. Jakeman L.B., Chen Y., Lucin K.M., and McTigue D.M. Mice lacking L1 cell adhesion molecule have deficits in locomotion and exhibit enhanced corticospinal tract sprouting following mild contusion injury to the spinal cord. Eur. J. Neurosci. 23 (2006) 1997-2011
38. Jakeman L.B., Guan Z., Wei P., Ponnappan R., Dzwonczyk R., Popovich P.G., and Stokes B.T. Traumatic spinal cord injury produced by controlled contusion in mouse. J. Neurotrauma 17 (2000) 299-319
39. Kamiguchi H. The mechanism of axon growth: what we have learned from the cell adhesion molecule L1. Mol. Neurobiol. 28 (2003) 219-228
40. Karl T., Pabst R., and von H.S. Behavioral phenotyping of mice in pharmacological and toxicological research. Exp. Toxicol. Pathol. 55 (2003) 69-83
41. Kerr B.J., and David S. Pain behaviors after spinal cord contusion injury in two commonly used mouse strains. Exp. Neurol. 206 (2007) 240-247
42. Kloos A.D., Fisher L.C., Detloff M.R., Hassenzahl D.L., and Basso D.M. Stepwise motor and all-or-none sensory recovery is associated with nonlinear sparing after incremental spinal cord injury in rats. Exp. Neurol. 191 (2005) 251-265
43. Krenz N.R., and Weaver L.C. Sprouting of primary afferent fibers after spinal cord transection in the rat. Neuroscience 85 (1998) 443-458
44. Law J.W.S., Lee A.Y.W., Sun M., Nikonenko A.G., Chung S.K., Dityatev A., Schachner M., and Morellini F. Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J. Neurosci. 23 (2003) 10419-10432
45. Leo S., Straetemans R., D'Hooge R., and Meert T. Differences in nociceptive behavioral performance between C57BL/6J, 129S6/SvEv, B6 129 F1 and NMRI mice. Behav. Brain Res. 190 2 (2008) 233-242
46. Lu P., Jones L.L., Snyder E.Y., and Tuszynski M.H. Neural stem cells constitutively secrete neurotrophic factors and promote extensive host axonal growth after spinal cord injury. Exp. Neurol. 181 (2003) 115-129
47. Luthi A., Mohajeri H., Schachner M., and Laurent J.P. Reduction of hippocampal long-term potentiation in transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. J. Neurosci. Res. 46 (1996) 1-6
48. Luthi A., Laurent J.P., Figurov A., Muller D., and Schachner M. Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372 (1994) 777-779
49. Ma M., Basso D.M., Walters P., Stokes B.T., and Jakeman L.B. Behavioral and histological outcome following graded contusion injury in C57Bl/6 mice. Exp. Neurol. 169 (2001) 239-254
50. Ma M., Wei P., Wei T., Ransohoff R.M., and Jakeman L.B. Enhanced axonal growth into a spinal cord contusion injury site in a strain of mouse (129X1/SvJ) with a diminished inflammatory response. J. Comp. Neurol. 474 (2004) 469-486
51. Malmberg A.B., Chen C., Tonegawa S., and Basbaum A.I. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 278 (1997) 279-283
52. Maness P.F., and Schachner M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat. Neurosci. 10 (2007) 19-26
53. Mao J., Price D.D., Phillips L.L., Lu J., and Mayer D.J. Increases in protein kinase C gamma immunoreactivity in the spinal cord dorsal horn of rats with painful mononeuropathy. Neurosci. Lett. 198 (1995) 75-78
54. Martin W.J., Liu H., Wang H., Malmberg A.B., and Basbaum A.I. Inflammation-induced up-regulation of protein kinase Cgamma immunoreactivity in rat spinal cord correlates with enhanced nociceptive processing. Neuroscience 88 (1999) 1267-1274
55. Metz G.A., Merkler D., Dietz V., Schwab M.E., and Fouad K. Efficient testing of motor function in spinal cord injured rats. Brain Res. 883 (2000) 165-177
56. Miletic V., Bowen K.K., and Miletic G. Loose ligation of the rat sciatic nerve is accompanied by changes in the subcellular content of protein kinase C beta II and gamma in the spinal dorsal horn. Neurosci. Lett. 288 (2000) 199-202
57. Mire E., Thomasset N., Jakeman L.B., and Rougon G. Modulating Sema3A signal with a L1 mimetic peptide is not sufficient to promote motor recovery and axon regeneration after spinal cord injury. Mol. Cell. Neurosci. 37 (2008) 222-235
58. Mogil J.S., Wilson S.G., Bon K., Lee S.E., Chung K., Raber P., Pieper J.O., Hain H.S., Belknap J.K., Hubert L., Elmer G.I., Chung J.M., and Devor M. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 80 (1999) 67-82
59. Narita M., Yoshida T., Nakajima M., Narita M., Miyatake M., Takagi T., Yajima Y., and Suzuki T. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J. Neurochem. 97 (2006) 1337-1348
60. Nesic O., Lee J., Johnson K.M., Ye Z., Xu G.Y., Unabia G.C., Wood T.G., McAdoo D.J., Westlund K.N., Hulsebosch C.E., and Regino Perez-Polo J. Transcriptional profiling of spinal cord injury-induced central neuropathic pain. J. Neurochem. 95 (2005) 998-1014
61. Neumann S., Braz J.M., Skinner K., Llewellyn-Smith I.J., and Basbaum A.I. Innocuous, not noxious, input activates PKCgamma interneurons of the spinal dorsal horn via myelinated afferent fibers. J. Neurosci. 28 (2008) 7936-7944
62. Obata K., Katsura H., Miyoshi K., Kondo T., Yamanaka H., Kobayashi K., Dai Y., Fukuoka T., Akira S., and Noguchi K. Toll-like receptor 3 contributes to spinal glial activation and tactile allodynia after nerve injury. J. Neurochem. (2008)
63. Ondarza A.B., Ye Z., and Hulsebosch C.E. Direct evidence of primary afferent sprouting in distant segments following spinal cord injury in the rat: colocalization of GAP-43 and CGRP. Exp. Neurol. 184 (2003) 373-380
64. Panicker A.K., Buhusi M., Thelen K., and Maness P.F. Cellular signalling mechanisms of neural cell adhesion molecules. Front Biosci. 8 (2003) 900-911
65. Polgar E., Fowler J.H., McGill M.M., and Todd A.J. The types of neuron which contain protein kinase C gamma in rat spinal cord. Brain Res. 833 (1999) 71-80
66. Romero M.I., Rangappa N., Li L., Lightfoot E., Garry M.G., and Smith G.M. Extensive sprouting of sensory afferents and hyperalgesia induced by conditional expression of nerve growth factor in the adult spinal cord. J. Neurosci. 20 (2000) 4435-4445
67. Rosenzweig E.S., and McDonald J.W. Rodent models for treatment of spinal cord injury: research trends and progress toward useful repair. Curr. Opin. Neurol. 17 (2004) 121-131
68. Runyan S.A., Roy R., Zhong H., and Phelps P.E. L1 CAM expression in the superficial dorsal horn is derived from the dorsal root ganglion. J. Comp. Neurol. 485 (2005) 267-279
69. Runyan S.A., Roy R.R., Zhong H., and Phelps P.E. L1 cell adhesion molecule is not required for small-diameter primary afferent sprouting after deafferentation. Neuroscience 150 (2007) 959-969
70. Sawatzky B., Bishop C.M., and Miller W.C. Classification and measurement of pain in the spinal cord-injured population. Spinal Cord. 46 (2008) 2-10
71. Siddall P.J., McClelland J.M., Rutkowski S.B., and Cousins M.J. A longitudinal study of the prevalence and characteristics of pain in the first 5 years following spinal cord injury. Pain 103 (2003) 249-257
72. Sluka K.A., and Audette K.M. Activation of protein kinase C in the spinal cord produces mechanical hyperalgesia by activating glutamate receptors, but does not mediate chronic muscle-induced hyperalgesia. Mol. Pain 2 (2006) 13
73. Stormer S., Gerner H.J., Gruninger W., Metzmacher K., Follinger S., Wienke C., Aldinger W., Walker N., Zimmermann M., and Paeslack V. Chronic pain/dysaesthesiae in spinal cord injury patients: results of a multicentre study. Spinal Cord. 35 (1997) 446-455
74. Tate D.G., and Forchheimer M. Quality of life, life satisfaction, and spirituality: comparing outcomes between rehabilitation and cancer patients. Am. J. Phys. Med. Rehabil. 81 (2002) 400-410
75. Terayama R., Omura S., Fujisawa N., Yamaai T., Ichikawa H., and Sugimoto T. Activation of microglia and p38 mitogen-activated protein kinase in the dorsal column nucleus contributes to tactile allodynia following peripheral nerve injury. Neuroscience 153 (2008) 1245-1255
76. Thelin J., Waldenstrom A., Bartsch U., Schachner M., and Schouenborg J. Heat nociception is severely reduced in a mutant mouse deficient for the L1 adhesion molecule. Brain Res. 965 (2003) 75-82
77. Thuret S., Moon L.D., and Gage F.H. Therapeutic interventions after spinal cord injury. Nat. Rev. Neurosci. 7 (2006) 628-643
78. Triana-Baltzer G.B., Liu Z., Gounko N.V., and Berg D.K. Multiple cell adhesion molecules shaping a complex nicotinic synapse on neurons. Mol. Cell Neurosci. (2008)
79. Tsuda M., Shigemoto-Mogami Y., Koizumi S., Mizokoshi A., Kohsaka S., Salter M.W., and Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424 (2003) 778-783
80. Vega-Avelaira D., Moss A., and Fitzgerald M. Age-related changes in the spinal cord microglial and astrocytic response profile to nerve injury. Brain Behav. Immun. 21 5 (2007) 617-623
81. Venero C., Tilling T., Hermans-Borgmeyer I., Herrero A.I., Schachner M., and Sandi C. Water maze learning and forebrain mRNA expression of the neural cell adhesion molecule L1. J. Neurosci. Res. 75 (2004) 172-181
82. Whittard J.D., Sakurai T., Cassella M.R., Gazdoiu M., and Felsenfeld D.P. MAP kinase pathway-dependent phosphorylation of the L1-CAM ankyrin binding site regulates neuronal growth. Mol. Biol. Cell 17 (2006) 2696-2706
83. Widerstrom-Noga E.G., Cruz-Almeida Y., Martinez-Arizala A., and Turk D.C. Internal consistency, stability, and validity of the spinal cord injury version of the multidimensional pain inventory. Arch. Phys. Med. Rehabil. 87 (2006) 516-523
84. Widerstrom-Noga E.G., Felix E.R., Cruz-Almeida Y., and Turk D.C. Psychosocial subgroups in persons with spinal cord injuries and chronic pain. Arch. Phys. Med. Rehabil. 88 (2007) 1628-1635
85. Wolfer D.P., Mohajeri H.M., Lipp H.P., and Schachner M. Increased flexibility and selectivity in spatial learning of transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. The European journal of neuroscience 10 (1998) 708-717
86. Wong E.V., Kenwrick S., Willems P., and Lemmon V. Mutations in the cell adhesion molecule L1 cause mental retardation. Trends in Neurosciences 18 (1995) 168-172
87. Wong S.T., Atkinson B.A., and Weaver L.C. Confocal microscopic analysis reveals sprouting of primary afferent fibres in rat dorsal horn after spinal cord injury. Neurosci. Lett. 296 (2000) 65-68
88. Yamanaka H., Obata K., Kobayashi K., Dai Y., Fukuoka T., and Noguchi K. Alteration of the cell adhesion molecule L1 expression in a specific subset of primary afferent neurons contributes to neuropathic pain. Eur. J. Neurosci. 25 (2007) 1097-1111