p53 regulates the neuronal intrinsic and extrinsic responses affecting the recovery of motor function following spinal cord injury

Journal of Neuroscience

Volumn 32, Issue 40, 2012, Pages 13956-13970

  Floriddia, Elisa M ^a,b   Rathore, Khizr I ^a   Tedeschi, Andrea ^a,c   Quadrato, Giorgia ^a   Wuttke, Anja ^a   Lueckmann, Jan Matthis ^a   Kigerl, Kristina A ^d   Popovich, Phillip G ^d   Di Giovanni, Simone ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CD11B ANTIGEN; CD16 ANTIGEN; CD32 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; KI 67 ANTIGEN; PROTEIN P53;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; HISTOLOGY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MACROPHAGE; MALE; MICROGLIA; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NERVE REGENERATION; NERVE SPROUTING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL TRACT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORIMOTOR CORTEX; SEROTONINERGIC NERVE; SPINAL CORD INJURY; TRAINING; WESTERN BLOTTING;

ANIMALS; CELLS, CULTURED; CICATRIX; CORDOTOMY; EXPLORATORY BEHAVIOR; GENES, P53; HOT TEMPERATURE; LAMENESS, ANIMAL; LOCOMOTION; MACROPHAGE ACTIVATION; MALE; MICE; MICE, KNOCKOUT; MICROGLIA; NEURONAL PLASTICITY; NEURONS; PYRAMIDAL TRACTS; RECOVERY OF FUNCTION; RETROGRADE DEGENERATION; SENSORY THRESHOLDS; SEROTONERGIC NEURONS; SPINAL CORD INJURIES; SPINAL CORD REGENERATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84867027499     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1925-12.2012     Document Type: Article

References (85)

1. Abbas T, Dutta A (2009) p21 in cancer: intricate networks and multiple activities. Nat Rev Cancer 9:400-414.
2. Alexander JK, Popovich PG (2009) Neuroinflammation in spinal cord injury: therapeutic targets for neuroprotection and regeneration. Prog Brain Res 175:125-137.
3. Aloyz RS, Bamji SX, Pozniak CD, Toma JG, Atwal J, Kaplan DR, Miller FD (1998) p53 is essential for developmental neuron death as regulated by the TrkA and p75 neurotrophin receptors. J Cell Biol 143:1691-1703.
4. Bareyre FM, Schwab ME (2003) Inflammation, degeneration and regeneration in the injured spinal cord: insights from DNA microarrays. Trends Neurosci 26:555-563.
5. Bareyre FM, Kerschensteiner M, Raineteau O, Mettenleiter TC, Weinmann O, Schwab ME (2004) The injured spinal cord spontaneously forms a new intraspinal circuit in adult rats. Nat Neurosci 7:269-277.
6. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG (2006) Basso Mouse Scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23:635-659.
7. Behrmann DL, Bresnahan JC, Beattie MS, Shah BR (1992) Spinal cord injury produced by consistent mechanical displacement of the cord in rats: behavioral and histologic analysis. J Neurotrauma 9:197-217.
8. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB (2002) Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature 416:636-640.
9. Bregman BS, Kunkel-Bagden E, Schnell L, Dai HN, Gao D, Schwab ME (1995) Recovery from spinal cord injury mediated by antibodies to neurite growth inhibitors. Nature 378:498-501.
10. Byrnes KR, Garay J, Di Giovanni S, De Biase A, Knoblach SM, Hoffman EP, Movsesyan V, Faden AI (2006) Expression of two temporally distinct microglia-related gene clusters after spinal cord injury. Glia 53:420-433.
11. Byrnes KR, Stoica BA, Fricke S, Di Giovanni S, Faden AI (2007) Cell cycle activation contributes to post-mitotic cell death and secondary damage after spinal cord injury. Brain 130:2977-2992.
12. Cafferty WB, McGee AW, Strittmatter SM (2008) Axonal growth therapeutics: regeneration or sprouting or plasticity? Trends Neurosci 31:215-220.
13. Camand E, Morel MP, Faissner A, Sotelo C, Dusart I (2004) Long-term changes in the molecular composition of the glial scar and progressive increase of serotoninergic fibre sprouting after hemisection of the mouse spinal cord. Eur J Neurosci 20:1161-1176.
14. Carmel JB, Galante A, Soteropoulos P, Tolias P, Recce M, Young W, Hart RP (2001) Gene expression profiling of acute spinal cord injury reveals spreading inflammatory signals and neuron loss. Physiol Genomics 7:201-213.
15. Chen MS, Huber AB, van der Haar ME, Frank M, Schnell L, Spillmann AA, Christ F, Schwab ME (2000) Nogo-A is a myelin-associated neurite outgrowth inhibitor and an antigen for monoclonal antibody IN-1. Nature 403:434-439.
16. Culmsee C, Mattson MP (2005) p53 in neuronal apoptosis. Biochem Biophys Res Commun 331:761-777.
17. David S, Kroner A (2011) Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci 12:388-399.
18. Davies SJ, Goucher DR, Doller C, Silver J (1999) Robust regeneration of adult sensory axons in degenerating white matter of the adult rat spinal cord. J Neurosci 19:5810-5822.
19. Di Giovanni S (2009) Molecular targets for axon regeneration: focus on the intrinsic pathways. Expert Opin Ther Targets 13:1387-1398.
20. Di Giovanni S, Knoblach SM, Brandoli C, Aden SA, Hoffman EP, Faden AI (2003) Gene profiling in spinal cord injury shows role of cell cycle in neuronal death. Ann Neurol 53:454-468.
21. Di Giovanni S, Faden AI, Yakovlev A, Duke-Cohan JS, Finn T, Thouin M, Knoblach S, De Biase A, Bregman BS, Hoffman EP (2005a) Neuronal plasticity after spinal cord injury: identification of a gene cluster driving neurite outgrowth. FASEB J 19:153-154.
22. Di Giovanni S, De Biase A, Yakovlev A, Finn T, Beers J, Hoffman EP, Faden AI (2005b) In vivo and in vitro characterization of novel neuronal plasticity factors identified following spinal cord injury. J Biol Chem 280:2084-2091.
23. Di Giovanni S, Movsesyan V, Ahmed F, Cernak I, Schinelli S, Stoica B, Faden AI (2005c) Cell cycle inhibition provides neuroprotection and reduces glial proliferation and scar formation after traumatic brain injury. Proc Natl Acad Sci U S A 102:8333-8338.
24. Di Giovanni S, Knights CD, Rao M, Yakovlev A, Beers J, Catania J, Avantaggiati ML, Faden AI (2006) The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J 25:4084-4096.
25. el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
26. Faden AI, Gannon A, Basbaum AI (1988) Use of serotonin immunocytochemistry as a marker of injury severity after experimental spinal trauma in rats. Brain Res 450:94-100.
27. Floriddia E, Nguyen T, Di Giovanni S (2011) Chromatin immunoprecipitation from dorsal root ganglia tissue following axonal injury. J Vis Exp pii:2803.
28. Giger RJ, Venkatesh K, Chivatakarn O, Raiker SJ, Robak L, Hofer T, Lee H, Rader C (2008) Mechanisms of CNS myelin inhibition: evidence for distinct and neuronal cell type specific receptor systems. Restor Neurol Neurosci 26:97-115.
29. GrandPré T, Li S, Strittmatter SM (2002) Nogo-66 receptor antagonist peptide promotes axonal regeneration. Nature 417:547-551.
30. Hamers FP, Lankhorst AJ, van Laar TJ, Veldhuis WB, Gispen WH (2001) Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J Neurotrauma 18:187-201.
31. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88.
32. Hellal F, Hurtado A, Ruschel J, Flynn KC, Laskowski CJ, Umlauf M, Kapitein LC, Strikis D, Lemmon V, Bixby J, Hoogenraad CC, Bradke F (2011) Microtubule stabilization reduces scarring and causes axon regeneration after spinal cord injury. Science 331:928-931.
33. Hill RL, Zhang YP, Burke DA, Devries WH, Zhang Y, Magnuson DS, Whittemore SR, Shields CB (2009) Anatomical and functional outcomes following a precise, graded, dorsal laceration spinal cord injury in C57BL/6 mice. J Neurotrauma 26:1-15.
34. Horn KP, Busch SA, Hawthorne AL, van Rooijen N, Silver J (2008) Another barrier to regeneration in the CNS: activated macrophages induce extensive retraction of dystrophic axons through direct physical interactions. J Neurosci 28:9330-9341.
35. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA (1994) Tumor spectrum analysis in p53-mutant mice. Curr Biol 4:1-7.
36. Johnson DG, Walker CL (1999) Cyclins and cell cycle checkpoints. Annu Rev Pharmacol Toxicol 39:295-312.
37. Jones LL, Tuszynski MH (2002) Spinal cord injury elicits expression of keratan sulfate proteoglycans by macrophages, reactive microglia, and oligodendrocyte progenitors. J Neurosci 22:4611-4624.
38. Jones TB, McDaniel EE, Popovich PG (2005) Inflammatory-mediated injury and repair in the traumatically injured spinal cord. Curr Pharm Des 11:1223-1236.
39. Kigerl KA, Gensel JC, Ankeny DP, Alexander JK, Donnelly DJ, Popovich PG (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.
40. Klapka N, Hermanns S, Straten G, Masanneck C, Duis S, Hamers FP, Muller D, Zuschratter W, Muller HW (2005) Suppression of fibrous scarring in spinal cord injury of rat promotes long-distance regeneration of corticospinal tract axons, rescue of primary motoneurons in somatosensory cortex and significant functional recovery. Eur J Neurosci 22:3047-3058.
41. Knoblach SM, Huang X, VanGelderen J, Calva-Cerqueira D, Faden AI (2005) Selective caspase activation may contribute to neurological dysfunction after experimental spinal cord trauma. J Neurosci Res 80:369-380.
42. Komarova EA, Krivokrysenko V, Wang K, Neznanov N, Chernov MV, Komarov PG, Brennan ML, Golovkina TV, Rokhlin OW, Kuprash DV, Nedospasov SA, Hazen SL, Feinstein E, Gudkov AV (2005) p53 is a suppressor of inflammatory response in mice. FASEB J 19:1030-1032.
43. Kottis V, Thibault P, Mikol D, Xiao ZC, Zhang R, Dergham P, Braun PE (2002) Oligodendrocyte-myelin glycoprotein (OMgp) is an inhibitor of neurite outgrowth. J Neurochem 82:1566-1569.
44. Liebermann DA, Hoffman B, Vesely D (2007) p53 induced growth arrest versus apoptosis and its modulation by survival cytokines. Cell Cycle 6:166-170.
45. Liu K, Tedeschi A, Park KK, He Z (2011) Neuronal intrinsic mechanisms of axon regeneration. Annu Rev Neurosci 34:131-152.
46. Loane DJ, Byrnes KR (2010) Role of microglia in neurotrauma. Neurotherapeutics 7:366-377.
47. Ma M, Basso DM, Walters P, Stokes BT, Jakeman LB (2001) Behavioral and histological outcomes following graded spinal cord contusion injury in the C57BL/6 mouse. Exp Neurol 169:239-254.
48. Maier IC, Ichiyama RM, Courtine G, Schnell L, Lavrov I, Edgerton VR, Schwab ME (2009) Differential effects of anti-Nogo-A antibody treatment and treadmill training in rats with incomplete spinal cord injury. Brain 132:1426-1440.
49. McKerracher L, David S, Jackson DL, Kottis V, Dunn RJ, Braun PE (1994) Identification of myelin-associated glycoprotein as a major myelinderived inhibitor of neurite growth. Neuron 13:805-811.
50. Missero C, Di Cunto F, Kiyokawa H, Koff A, Dotto GP (1996) The absence of p21Cip1/WAF1 alters keratinocyte growth and differentiation and promotes ras-tumor progression. Genes Dev 10:3065-3075.
51. Mogil JS, Wilson SG, Bon K, Lee SE, Chung K, Raber P, Pieper JO, Hain HS, Belknap JK, Hubert L, Elmer GI, Chung JM, Devor M (1999) Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain 80:67-82.
52. Moore DL, Goldberg JL (2011) Multiple transcription factor families regulate axon growth and regeneration. Dev Neurobiol 71:1186-1211.
53. Mullner A, Gonzenbach RR, Weinmann O, Schnell L, Liebscher T, Schwab ME (2008) Lamina-specific restoration of serotonergic projections after Nogo-A antibody treatment of spinal cord injury in rats. Eur J Neurosci 27:326-333.
54. Oatway MA, Chen Y, Bruce JC, Dekaban GA, Weaver LC (2005) Anti-CD11d integrin antibody treatment restores normal serotonergic projections to the dorsal, intermediate, and ventral horns of the injured spinal cord. J Neurosci 25:637-647.
55. Oren M (2003) Decision making by p53: life, death and cancer. Cell Death Differ 10:431-442.
56. Park JB, Yiu G, Kaneko S, Wang J, Chang J, He XL, Garcia KC, He Z (2005) A TNF receptor family member, TROY, is a coreceptor with Nogo receptor in mediating the inhibitory activity of myelin inhibitors. Neuron 45: 345-351.
57. Pietenpol JA, Stewart ZA (2002) Cell cycle checkpoint signaling: cell cycle arrest versus apoptosis. Toxicology 181-182:475-481.
58. Popovich PG, Guan Z, Wei P, Huitinga I, van Rooijen N, Stokes BT (1999) Depletion of hematogenous macrophages promotes partial hindlimb recovery and neuroanatomical repair after experimental spinal cord injury. Exp Neurol 158:351-365.
59. Qin Q, Baudry M, Liao G, Noniyev A, Galeano J, Bi X (2009) A novel function for p53: regulation of growth cone motility through interaction with Rho kinase. J Neurosci 29:5183-5192.
60. Qin Q, Liao G, Baudry M, Bi X (2010) Role of calpain-mediated p53 truncation in semaphorin 3A-induced axonal growth regulation. Proc Natl Acad Sci U S A 107:13883-13887.
61. Raineteau O, Schwab ME (2001) Plasticity of motor systems after incomplete spinal cord injury. Nat Rev Neurosci 2:263-273.
62. Raineteau O, Fouad K, Bareyre FM, Schwab ME (2002) Reorganization of descending motor tracts in the rat spinal cord. Eur J Neurosci 16:1761-1771.
63. Rhodes KE, Moon LD, Fawcett JW (2003) Inhibiting cell proliferation during formation of the glial scar: effects on axon regeneration in the CNS. Neuroscience 120:41-56.
64. Saito N, Yamamoto T, Watanabe T, Abe Y, Kumagai T (2000) Implications of p53 protein expression in experimental spinal cord injury. J Neurotrauma 17:173-182.
65. Sakaguchi K, Herrera JE, Saito S, Miki T, Bustin M, Vassilev A, Anderson CW, Appella E (1998) DNA damage activates p53 through a phosphorylationacetylation cascade. Genes Dev 12:2831-2841.
66. Saruhashi Y, Young W, Perkins R (1996) The recovery of 5-HT immunoreactivity in lumbosacral spinal cord and locomotor function after thoracic hemisection. Exp Neurol 139:203-213.
67. Saura J, Tusell JM, Serratosa J (2003) High-yield isolation of murine microglia by mild trypsinization. Glia 44:183-189.
68. Savio T, Schwab ME (1990) Lesioned corticospinal tract axons regenerate in myelin-free rat spinal cord. Proc Natl Acad Sci U S A 87:4130-4133.
69. Schnell L, Schwab ME (1990) Axonal regeneration in the rat spinal cord produced by an antibody against myelin-associated neurite growth inhibitors. Nature 343:269-272.
70. Schnell L, Schwab ME (1993) Sprouting and regeneration of lesioned corticospinal tract fibres in the adult rat spinal cord. Eur J Neurosci 5:1156-1171.
71. Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596.
72. Silver J, Miller JH (2004) Regeneration beyond the glial scar. Nat Rev Neurosci 5:146-156.
73. Simonen M, Pedersen V, Weinmann O, Schnell L, Buss A, Ledermann B, Christ F, Sansig G, van der Putten H, Schwab ME (2003) Systemic deletion of the myelin-associated outgrowth inhibitor Nogo-A improves regenerative and plastic responses after spinal cord injury. Neuron 38:201-211.
74. Sroga JM, Jones TB, Kigerl KA, McGaughy VM, Popovich PG (2003) Rats and mice exhibit distinct inflammatory reactions after spinal cord injury. J Comp Neurol 462:223-240.
75. Steward O, Zheng B, Tessier-Lavigne M (2003) False resurrections: distinguishing regenerated from spared axons in the injured central nervous system. J Comp Neurol 459:1-8.
76. Steward O, Zheng B, Tessier-Lavigne M, Hofstadter M, Sharp K, Yee KM (2008) Regenerative growth of corticospinal tract axons via the ventral column after spinal cord injury in mice. J Neurosci 28:6836-6847.
77. Stichel CC, Hermanns S, Luhmann HJ, Lausberg F, Niermann H, D'Urso D, Servos G, Hartwig HG, Muller HW (1999) Inhibition of collagen IV deposition promotes regeneration of injured CNS axons. Eur J Neurosci 11:632-646.
78. Tedeschi A, Nguyen T, Puttagunta R, Gaub P, Di Giovanni S (2009a) A p53-CBP/p300 transcription module is required for GAP-43 expression, axon outgrowth, and regeneration. Cell Death Differ 16:543-554.
79. Tedeschi A, Nguyen T, Steele SU, Feil S, Naumann U, Feil R, Di Giovanni S (2009b) The tumor suppressor p53 transcriptionally regulates cGKI expression during neuronal maturation and is required for cGMP-dependent growth cone collapse. J Neurosci 29:15155-15160.
80. Tian DS, Yu ZY, Xie MJ, Bu BT, Witte OW, Wang W (2006) Suppression of astroglial scar formation and enhanced axonal regeneration associated with functional recovery in a spinal cord injury rat model by the cell cycle inhibitor olomoucine. J Neurosci Res 84:1053-1063.
81. Tian DS, Xie MJ, Yu ZY, Zhang Q, Wang YH, Chen B, Chen C, Wang W (2007) Cell cycle inhibition attenuates microglia induced inflammatory response and alleviates neuronal cell death after spinal cord injury in rats. Brain Res 1135:177-185.
82. Wang D, Ichiyama RM, Zhao R, Andrews MR, Fawcett JW (2011) Chondroitinase combined with rehabilitation promotes recovery of forelimb function in rats with chronic spinal cord injury. J Neurosci 31:9332-9344.
83. Wu J, Stoica BA, Faden AI (2011) Cell cycle activation and spinal cord injury. Neurotherapeutics 8:221-228.
84. Wynn TA, Barron L (2010) Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 30:245-257.
85. Yiu G, He Z (2006) Glial inhibition of CNS axon regeneration. Nat Rev Neurosci 7:617-627.