Sciatic nerve injury induces apoptosis of dorsal root ganglion satellite glial cells and selectively modifies neurosteroidogenesis in sensory neurons

GLIA

Volumn 58, Issue 2, 2010, Pages 169-180

  Schaeffer, Véronique ^a   Meyer, Laurence ^a   Patte Mensah, Christine ^a   Eckert, Anne ^b   Mensah Nyagan, Ayikoe G ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Cell death; Nerve cell viability; Neuropathy; Neuroprotection; Neurosteroid; Pain

Indexed keywords

AROMATASE; ESTRADIOL; GLUTAMATE AMMONIA LIGASE; NEUROSTEROID; PREGNENOLONE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INTERACTION; CELL VIABILITY; CONTROLLED STUDY; GLIA CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; NERVE INJURY; NEUROPATHIC PAIN; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RAT; SATELLITE CELL; SCIATIC NERVE; SENSORY NERVE; SPINAL CORD; SPINAL GANGLION;

EID: 73149094723     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20910     Document Type: Article

References (73)

1. Azcoitia I, Sierra A, Veiga S, Honda S, Harada N, Garcia-Segura LM. 2001. Brain aromatase is neuroprotective. J Neurobiol 47:318-329.
2. Azkue JJ, Zimmermann M, Hsieh TF, Herdegen T. 1998. Peripheral nerve insult induces NMDA receptor-mediated, delayed degeneration in spinal neurons. Eur J Neurosci 10:2204-2206.
3. Basbaum AI, Gautron M, Jazat F, Mayes M, Guilbaud G. 1991. The spectrum of fiber loss in a model of neuropathic pain in the rat: An electron microscopic study. Pain 47:359-367.
4. Baulieu EE, Robel P, Schumacher M. 1999. Contemporary Endocrinology, Totowa, NJ.
5. Bennett GJ. 1998. Neuropathic pain: New insights, new interventions. Hosp Pract (Minneap) 33:95-98, 101-104, 107-110 passim.
6. Bennett GJ, Xie YK. 1988. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33:87-107.
7. Brinkhus HB, Zimmermann M. 1983. Characteristics of spinal dorsal horn neurons after partial chronic deafferentation by dorsal root transection. Pain 15:221-236.
8. Brinton RD, Wang JM. 2006a. Preclinical analyses of the therapeutic potential of allopregnanolone to promote neurogenesis in vitro and in vivo in transgenic mouse model of Alzheimer's disease. Curr Alzheimer Res 3:11-17.
9. Brinton RD, Wang JM. 2006b. Therapeutic potential of neurogenesis for prevention and recovery from Alzheimer's disease: Allopregnanolone as a proof of concept neurogenic agent. Curr Alzheimer Res 3:185-190.
10. Buzdar AU. 2001. A summary of second-line randomized studies of aromatase inhibitors. J Steroid Biochem Mol Biol 79:109-114.
11. Campana WM, Myers RR. 2003. Exogenous erythropoietin protects against dorsal root ganglion apoptosis and pain following peripheral nerve injury. Eur J Neurosci 18:1497-1506.
12. Campbell JN, Meyer RA. 2006. Mechanisms of neuropathic pain. Neuron 52:77-92.
13. de Novellis V, Siniscalco D, Galderisi U, Fuccio C, Nolano M, Santoro L, Cascino A, Roth KA, Rossi F, Maione S. 2004. Blockade of glutamate mGlu5 receptors in a rat model of neuropathic pain prevents early over-expression of pro-apoptotic genes and morphological changes in dorsal horn lamina II. Neuropharmacology 46:468-479.
14. Fester L, Ribeiro-Gouveia V, Prange-Kiel J, von Schassen C, Böttner M, Jarry H, Rune GM. 2006. Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J Neurochem 97:1136-1144.
15. Garcia-Segura LM, Azcoitia I, DonCarlos LL. 2001. Neuroprotection by estradiol. Prog Neurobiol 63:29-60.
16. Garcia-Segura LM, Naftolin F, Hutchison JB, Azcoitia I, Chowen JA. 1999a. Role of astroglia in estrogen regulation of synaptic plasticity and brain repair. J Neurobiol 40:574-584.
17. Garcia-Segura LM, Veiga S, Sierra A, Melcangi RC, Azcoitia I. 2003. Aromatase: A neuroprotective enzyme. Prog Neurobiol 71:31-41.
18. Garcia-Segura LM, Wozniak A, Azcoitia I, Rodriguez JR, Hutchison RE, Hutchison JB. 1999b. Aromatase expression by astrocytes after brain injury: Implications for local estrogen formation in brain repair. Neuroscience 89:567-578.
19. Ghoumari AM, Dusart I, El-Etr M, Tronche F, Sotelo C, Schumacher M, Baulieu EE. 2003. Mifepristone (RU486) protects Purkinje cells from cell death in organotypic slice cultures of postnatal rat and mouse cerebellum. Proc Natl Acad Sci USA 100:7953-7958.
20. Griffin LD, Gong W, Verot L, Mellon SH. 2004. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat Med 10:704-711.
21. Hanani M. 2005. Satellite glial cells in sensory ganglia: From form to function. Brain Res Brain Res Rev 48:457-476.
22. 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.
23. Kawakami M, Weinstein JN, Chatani K, Spratt KF, Meller ST, Gebhart GF. 1994. Experimental lumbar radiculopathy. Behavioral and histologic changes in a model of radicular pain after spinal nerve root irritation with chromic gut ligatures in the rat. Spine 19:1795-1802.
24. Kibaly C, Meyer L, Patte-Mensah C, Mensah-Nyagan AG. 2008. Biochemical and functional evidence for the control of pain mechanisms by dehydroepiandrosterone endogenously synthesized in the spinal cord. FASEB J 22:93-104.
25. Kibaly C, Patte-Mensah C, Mensah-Nyagan AG. 2005. Molecular and neurochemical evidence for the biosynthesis of dehydroepiandrosterone in the adult rat spinal cord. J Neurochem 93:1220-1230.
26. Koenig HL, Schumacher M, Ferzaz B, Thi AN, Ressouches A, Guennoun R, Jung-Testas I, Robel P, Akwa Y, Baulieu EE. 1995. Progesterone synthesis and myelin formation by Schwann cells. Science 268:1500-1503.
27. Lamb HM, Adkins JC. 1998. Letrozole. A review of its use in postmenopausal women with advanced breast cancer. Drugs 56:1125-1140.
28. Lee BH, Won R, Baik EJ, Lee SH, Moon CH. 2000. An animal model of neuropathic pain employing injury to the sciatic nerve branches. Neuroreport 11:657-661.
29. Leonelli E, Bianchi R, Cavaletti G, Caruso D, Crippa D, Garcia-Segura LM, Lauria G, Magnaghi V, Roglio I, Melcangi RC. 2007. Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: A multimodal analysis. Neuroscience 144:1293-1304.
30. Lind D, Franken S, Kappler J, Jankowski J, Schilling K. 2005. Characterization of the neuronal marker NeuN as a multiply phosphorylated antigen with discrete subcellular localization. J Neurosci Res 79:295-302.
31. Lombard MC, Nashold BS, Jr., Albe-Fessard D, Salman N, Sakr C. 1979. Deafferentation hypersensitivity in the rat after dorsal rhizotomy: A possible animal model of chronic pain. Pain 6:163-174.
32. Maione S, Siniscalco D, Galderisi U, de Novellis V, Uliano R, Di Bernardo G, Berrino L, Cascino A, Rossi F. 2002. Apoptotic genes expression in the lumbar dorsal horn in a model neuropathic pain in rat. Neuroreport 13:101-106.
33. McCullough LD, Blizzard K, Simpson ER, Oz OK, Hurn PD. 2003. Aromatase cytochrome P450 and extragonadal estrogen play a role in ischemic neuroprotection. J Neurosci 23:8701-8705.
34. Mensah-Nyagan AG, Do-Rego JL, Beaujean D, Luu-The V, Pelletier G, Vaudry H. 1999. Neurosteroids: Expression of steroidogenic enzymes and regulation of steroid biosynthesis in the central nervous system. Pharmacol Rev 51:63-81.
35. Mensah-Nyagan AG, Do-Rego JL, Feuilloley M, Marcual A, Lange C, Pelletier G, Vaudry H. 1996a. In vivo and in vitro evidence for the biosynthesis of testosterone in the telencephalon of the female frog. J Neurochem 67:413-422.
36. Mensah-Nyagan AG, Feuilloley M, Do-Rego JL, Marcual A, Lange C, Tonon MC, Pelletier G, Vaudry H. 1996b. Localization of 17betahydroxysteroid dehydrogenase and characterization of testosterone in the brain of the male frog. Proc Natl Acad Sci USA 93:1423-1428.
37. Mensah-Nyagan AG, Feuilloley M, Dupont E, Do-Rego JL, Leboulenger F, Pelletier G, Vaudry H. 1994. Immunocytochemical localization and biological activity of 3 beta-hydroxysteroid dehydrogenase in the central nervous system of the frog. J Neurosci 14:7306-7318.
38. Mestre C, Pelissier T, Fialip J, Wilcox G, Eschalier A. 1994. A method to perform direct transcutaneous intrathecal injection in rats. J Pharmacol Toxicol Methods 32:197-200.
39. Meyer L, Venard C, Schaeffer V, Patte-Mensah C, Mensah-Nyagan AG. 2008. The biological activity of 3alpha-hydroxysteroid oxido-reductase in the spinal cord regulates thermal and mechanical pain thresholds after sciatic nerve injury. Neurobiol Dis 30:30-41.
40. Mills CD, Grady JJ, Hulsebosch CE. 2001. Changes in exploratory behavior as a measure of chronic central pain following spinal cord injury. J Neurotrauma 18:1091-1105.
41. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
42. Munger BL, Bennett GJ, Kajander KC. 1992. An experimental painful peripheral neuropathy due to nerve constriction. I. Axonal pathology in the sciatic nerve. Exp Neurol 118:204-214.
43. Muñoz-Fernández MA, Fresno M. 1998. The role of tumour necrosis factor, interleukin 6, interferon-gamma and inducible nitric oxide synthase in the development and pathology of the nervous system. Prog Neurobiol 56:307-340.
44. Myers RR, Wagner R, Sorkin LS. 1999. Hyperalgesic actions of cytokines on peripheral nerves. In: Watkins LR, Maier SR, editors. Cytokines and pain. Basel, Switzerland: Birkhauser Verlag. pp 133-157.
45. Nuytten D, Kupers R, Lammens M, Dom R, Van Hees J, Gybels J. 1992. Further evidence for myelinated as well as unmyelinated fibre damage in a rat model of neuropathic pain. Exp Brain Res 91:73-78.
46. Ohtori S, Takahashi K, Moriya H, Myers RR. 2004. TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: Studies in murine DRG, spinal cord. Spine 29:1082-1088.
47. Patte-Mensah C, Kappes V, Freund-Mercier MJ, Tsutsui K, Mensah-Nyagan AG. 2003. Cellular distribution and bioactivity of the key steroidogenic enzyme, cytochrome P450side chain cleavage, in sensory neural pathways. J Neurochem 86:1233-1246.
48. Patte-Mensah C, Kibaly C, Boudard D, Schaeffer V, Béglé A, Saredi S, Meyer L, Mensah-Nyagan AG. 2006. Neurogenic Pain and Steroid Synthesis in the Spinal Cord. J Mol Neurosci 28:17-32.
49. Patte-Mensah C, Kibaly C, Mensah-Nyagan AG. 2005. Substance P inhibits progesterone conversion to neuroactive metabolites in spinal sensory circuit: A potential component of nociception. Proc Natl Acad Sci USA 102:9044-9049.
50. Patte-Mensah C, Li S, Mensah-Nyagan AG. 2004. Impact of neuropathic pain on the gene expression and activity of cytochrome P450side-chain-cleavage in sensory neural networks. Cell Mol Life Sci 61:2274-2284.
51. Patte-Mensah C, Mensah-Nyagan AG. 2008. Peripheral neuropathy and neurosteroid formation in the central nervous system. Brain Res Rev 57:454-459.
52. Polgár E, Gray S, Riddell JS, Todd AJ. 2004. Lack of evidence for significant neuronal loss in laminae I-III of the spinal dorsal horn of the rat in the chronic constriction injury model. Pain 111:144-150.
53. Polgár E, Hughes DI, Arham AZ, Todd AJ. 2005. Loss of neurons from laminas I-III of the spinal dorsal horn is not required for development of tactile allodynia in the spared nerve injury model of neuropathic pain. J Neurosci 25:6658-6666.
54. Polgár E, Hughes DI, Riddell JS, Maxwell DJ, Puskár Z, Todd AJ. 2003. Selective loss of spinal GABAergic or glycinergic neurons is not necessary for development of thermal hyperalgesia in the chronic constriction injury model of neuropathic pain. Pain 104:229-239.
55. Sasano H, Anderson TJ, Silverberg SG, Santen RJ, Conway M, Edwards DP, Krause A, Bhatnagar AS, Evans DB, Miller WR. 2005. Validation of new aromatase monoclonal antibodies for immunohistochemistry - A correlation with biochemical activities in 46 cases of breast cancer. J Steroid Biochem Mol Biol 95:35-39.
56. Sasano H, Edwards DP, Anderson TJ, Silverberg SG, Evans DB, Santen RJ, Ramage P, Simpson ER, Bhatnagar AS, Miller WR. 2003. Validation of new aromatase monoclonal antibodies for immunohistochemistry: Progress report. J Steroid Biochem Mol Biol 86:239-244.
57. Schaeffer V, Meyer L, Patte-Mensah C, Eckert A, Mensah-Nyagan AG. 2008a. Dose-dependent and sequence-sensitive effects of amyloid-beta peptide on neurosteroidogenesis in human neuroblastoma cells. Neurochem Int 52:948-955.
58. Schaeffer V, Patte-Mensah C, Eckert A, Mensah-Nyagan AG. 2006. Modulation of neurosteroid production in human neuroblastoma cells by Alzheimer's disease key proteins. J Neurobiol 66:868-881.
59. Schaeffer V, Patte-Mensah C, Eckert A, Mensah-Nyagan AG. 2008b. Selective regulation of neurosteroid biosynthesis in human neuroblas-toma cells under hydrogen peroxide-induced oxidative stress condition. Neuroscience 151:758-770.
60. Scholz J, Woolf CJ. 2007. The neuropathic pain triad: Neurons, immune cells and glia. Nat Neurosci 10:1361-1368.
61. Schumacher M, Guennoun R, Ghoumari A, Massaad C, Robert F, El-Etr M, Akwa Y, Rajkowski K, Baulieu EE. 2007. Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocr Rev 28:387-439.
62. Schumacher M, Guennoun R, Robert F, Carelli C, Gago N, Ghoumari A, Gonzalez Deniselle MC, Gonzalez SL, Ibanez C, Labombarda F, Coirini H, Baulieu EE, De Nicola AF. 2004. Local synthesis and dual actions of progesterone in the nervous system: Neuroprotection and myelination. Growth Horm IGF Res 14(Suppl A):S18-S33.
63. Thomas AJ, Nockels RP, Pan HQ, Shaffrey CI, Chopp M. 1999. Progesterone is neuroprotective after acute experimental spinal cord trauma in rats. Spine 24:2134-2138.
64. Veiga S, Azcoitia I, Garcia-Segura LM. 2005. Extragonadal synthesis of estradiol is protective against kainic acid excitotoxic damage to the hippocampus. Neuroreport 16:1599-1603.
65. Venard C, Boujedaini N, Belon P, Mensah-Nyagan AG, Patte-Mensah C. 2008. Regulation of neurosteroid allopregnanolone biosynthesis in the rat spinal cord by glycine and the alkaloidal analogs strychnine and gelsemine. Neuroscience 153:154-161.
66. Wang JM, Johnston PB, Ball BG, Brinton RD. 2005. The neurosteroid allopregnanolone promotes proliferation of rodent and human neural progenitor cells and regulates cell-cycle gene and protein expression. J Neurosci 25:4706-4718.
67. Watkins LR, Maier SR. 2002. Beyond neurons: Evidence that immune and glial cells contribute to pathological pain states. Physiol Rev 82:981-1011.
68. Whiteside G, Doyle CA, Hunt SP, Munglani R. 1998. Differential time course of neuronal and glial apoptosis in neonatal rat dorsal root ganglia after sciatic nerve axotomy. Eur J Neurosci 10:3400-3408.
69. Whiteside GT, Munglani R. 2001. Cell death in the superficial dorsal horn in a model of neuropathic pain. J Neurosci Res 64:168-173.
70. Wolf HK, Buslei R, Schmidt-Kastner R, Pietsch T, Wiestler OD, Blümcke I. 1996. NeuN: A useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44:1167-1171.
71. Woolf CJ, Mannion RJ. 1999. Neuropathic pain: Aetiology, symptoms, mechanisms, and management. Lancet 353:1959-1964.
72. Zimmermann M. 1983. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16:109-110.
73. Zimmermann M. 2001. Pathobiology of neuropathic pain. Eur J Pharmacol 429:23-37.