Prostaglandin E2 contributes to the synthesis of brain-derived neurotrophic factor in primary sensory neuron in ganglion explant cultures and in a neuropathic pain model

Experimental Neurology

Volumn 234, Issue 2, 2012, Pages 466-481

  Cruz Duarte, Pedro ^a   St Jacques, Bruno ^a   Ma, Weiya ^a,b  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Brain derived neurotrophic factor; Dorsal root ganglion; Explant culture; Inflammatory mediator; Nerve injury; Neuropathic pain; Neurotrophin; Prostaglandin E2; Sciatic nerve; Tract tracing

Indexed keywords

16,16 DIMETHYLPROSTAGLANDIN E2; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; PROSTAGLANDIN E RECEPTOR 1; PROSTAGLANDIN E RECEPTOR 1 ANTAGONIST; PROSTAGLANDIN E RECEPTOR 2; PROSTAGLANDIN E RECEPTOR 3; PROSTAGLANDIN E RECEPTOR 4; PROSTAGLANDIN E RECEPTOR 4 ANTAGONIST; PROSTAGLANDIN E2; PROSTAGLANDIN E2 DERIVATIVE; PROSTAGLANDIN RECEPTOR BLOCKING AGENT; PROSTAGLANDIN SYNTHASE INHIBITOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DOSE RESPONSE; EXPLANT; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL CULTURE; NERVE INJURY; NEUROPATHIC PAIN; NEUROPATHOLOGY; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RAT; SCIATIC NERVE; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SPINAL GANGLION; UPREGULATION;

ANIMALS; BIPHENYL COMPOUNDS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELLS, CULTURED; CYCLOOXYGENASE INHIBITORS; DINOPROSTONE; GANGLIA, SPINAL; HYPERALGESIA; MALE; NEURALGIA; NITROBENZENES; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PROSTAGLANDIN E, EP1 SUBTYPE; RECEPTORS, PROSTAGLANDIN E, EP4 SUBTYPE; SCIATIC NERVE; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SULFONAMIDES; UP-REGULATION;

EID: 84858150429     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.01.021     Document Type: Article

References (64)

1. Apfel S.C., Wright D.E., Wiideman A.M., Dormia C., Snider W.D., Kessler J.A. Nerve growth factor regulates the expression of brain-derived neurotrophic factor mRNA in the peripheral nervous system. Mol. Cell. Neurosci. 1996, 7:134-142.
2. Balkowiec-Iskra E., Vermehren-Schmaedick A., Balkowiec A. Tumor necrosis factor-alpha increases brain-derived neurotrophic factor expression in trigeminal ganglion neurons in an activity-dependent manner. Neuroscience 2011, 180:322-333.
3. Cho H.J., Kim J.K., Zhou X.F., Rush R.A. Increased brain-derived neurotrophic factor immunoreactivity in rat dorsal root ganglia and spinal cord following peripheral inflammation. Brain Res. 1997, 764:269-272.
4. Cruz Duarte P., St-Jacques B., Ma W. Contribution of injured nerve-derived COX2/PGE2 to the up-regulation of brain derived neurotrophic factor in dorsal root ganglion neurons of neuropathic rats. Soc. Neurosci. 2010, Abstr. 175.12.
5. Deng Y.S., Zhong J.H., Zhou X.F. BDNF is involved in sympathetic sprouting in the dorsal root ganglia following peripheral nerve injury in rats. Neurotox. Res. 2000, 1:311-322.
6. Durrenberger P.F., Facer P., Casula M.A., Yiangou Y., Gray R.A., Chessell I.P., Day N.C., Collins S.D., Bingham S., Wilson A.W., Elliot D., Birch R., Anand P. Prostanoid receptor EP1 and Cox-2 in injured human nerves and a rat model of nerve injury: a time-course study. BMC Neurol. 2006, 6:1-11.
7. Fukuoka T., Kondo E., Dai Y., Hashimoto N., Noguchi K. Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J. Neurosci. 2001, 21:4891-4900.
8. Groth R., Aanonsen L. Spinal brain-derived neurotrophic factor (BDNF) produces hyperalgesia in normal mice while antisense directed against either BDNF or trkB, prevent inflammation-induced hyperalgesia. Pain 2002, 100:171-181.
9. Ha S.O., Kim J.K., Hong H.S., Kim D.S., Cho H.J. Expression of brain-derived neurotrophic factor in rat dorsal root ganglia, spinal cord and gracile nuclei in experimental models of neuropathic pain. Neuroscience 2001, 107:301-309.
10. Lin C.R., Amaya F., Barrett L., WANG H., Takada J., Samad T.A., Woolf C.J. Prostaglandin E2 receptor EP4 contributes to inflammatory pain hypersensitivity. J. Pharmacol. Exp. Ther. 2006, 319:1096-1103.
11. Ma W. Chronic prostaglandin E2 treatment induces the synthesis of the pain-related peptide substance P and calcitonin gene-related peptide in cultured sensory ganglion explants. J. Neurochem. 2010, 115:363-372.
12. Ma W., Bisby M.A. Increase of calcitonin gene-related peptide immunoreactivity in the axonal fibers of the gracile nuclei of adult and aged rats after complete and partial sciatic nerve injuries. Exp. Neurol. 1998, 152:137-149.
13. Ma W., Bisby M.A. Increase of preprotachykinin mRNA and substance P immunoreactivity in spared primary sensory neurons following partial sciatic nerve injuries. Eur. J. Neurosci. 1998, 10:2388-2399.
14. Ma W., Eisenach J.C. Morphological and pharmacological evidence for the role of peripheral prostaglandins in the pathogenesis of neuropathic pain. Eur. J. Neurosci. 2002, 15:1037-1047.
15. Ma W., Eisenach J.C. Cyclooxygenase 2 in infiltrating inflammatory cells in injured nerve is universally up-regulated following various types of nerve injury. Neuroscience 2003, 121:691-704.
16. Ma W., Eisenach J.C. Four EP receptors are up-regulated in injured nerve following partial sciatic nerve ligation. Exp. Neurol. 2003, 183:581-592.
17. Ma W., Quirion R. Up-regulation of interleukin 6 induced by prostaglandin E2 from invading macrophages following nerve injury: an in vivo and in vitro study. J. Neurochem. 2005, 93:664-673.
18. Ma W., Quirion R. Increased calcitonin gene-related peptide in neuroma and invading macrophages is involved in the up-regulation of interleukin-6 and nerve injury associated thermal hyperalgesia in a rat model of mononeuropathy. J. Neurochem. 2006, 98:180-192.
19. Ma W., Quirion R. Does COX2-dependent PGE2 play a role in neuropathic pain?. Neurosci. Lett. 2008, 437:165-169.
20. Ma W., Ramer M.S., Bisby M.A. Increased calcitonin gene related peptide immunoreactivity in gracile nucleus after partial sciatic nerve injury: age-dependent and originating from spared sensory neurons. Exp. Neurol. 1999, 159:459-473.
21. Ma W., Zhang Y., Bantel C., Eisenach J.C. Medium and large injured dorsal root ganglion cells increase TRPV-1, accompanied by increased alpha2C-adrenoceptor co-expression and functional inhibition by clonidine. Pain 2005, 113:386-394.
22. Ma W., Chabot J.G., Vercauteren F., Quirion R. Injured nerve-derived COX2/PGE2 contributes to the maintenance of neuropathic pain in aged rats. Neurobiol. Aging 2010, 31:1227-1237.
23. Ma W., Dumont Y., Vercauteren F., Quirion R. Lipopolysaccharide induces calcitonin gene-related peptide in the RAW264.7 macrophage cell line. Immunology 2010, 130:399-409.
24. Mannion R.J., Costigan M., Decosterd I., Amaya F., Ma Q.P., Holstege J.C., Ji R.R., Acheson A., Lindsay R.M., Wilkinson G.A., Woolf C.J. Neurotrophins: peripherally and centrally acting modulators of tactile stimulus-induced inflammatory pain hypersensitivity. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9385-9390.
25. Mattson M.P. Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann. N. Y. Acad. Sci. 2008, 1144:97-112.
26. Mcmahon S.B. NGF as a mediator of inflammatory pain. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1996, 351:431-440.
27. Merighi A., Carmignoto G., Gobbo S., Lossi L., Salio C., Vergnano A.M., Zonta M. Neurotrophins in spinal cord nociceptive pathways. Prog. Brain Res. 2004, 146:291-321.
28. Merighi A., Salio C., Ghirri A., Lossi L., Ferrini F., Betelli C., Bardoni R. BDNF as a pain modulator. Prog. Neurobiol. 2008, 85:297-317.
29. Michael G.J., Averill S., Nitkunan A., Rattray M., Bennett D.L., Yan Q., Priestley J.V. Nerve growth factor treatment increases brain-derived neurotrophic factor selectively in TrkA-expressing dorsal root ganglion cells and in their central terminations within the spinal cord. J. Neurosci. 1997, 17:8476-8490.
30. Michael G.J., Averill S., Shortland P.J., Yan Q., Priestley J.V. Axotomy results in major changes in BDNF expression by dorsal root ganglion cells: BDNF expression in large trkB and trkC cells, in pericellular baskets, and in projections to deep dorsal horn and dorsal column nuclei. Eur. J. Neurosci. 1999, 11:3539-3551.
31. Miki K., Fukuoka T., Tokunaga A., Noguchi K. Calcitonin gene-related peptide increase in the rat spinal dorsal horn and dorsal column nucleus following peirpheral nerve injury: up-regulation in a subpopulation of primary afferent sensory neurons. Neuroscience 1997, 82:1243-1252.
32. Muja N., Devries G.H. Prostaglandin E(2) and 6-keto-prostaglandin F(1alpha) production is elevated following traumatic injury to sciatic nerve. GLIA 2004, 46:116-129.
33. Nestler E.J., Greengard P. Serine and threonine phosphorylation. Basic Neurochemistry Molecular 1999, 471-495. Cellular and Medical Aspects Lippincott-Raven Publishers, Philadelphia. G.J. Siegel, B.W. Agranoff, R.W. Albers, S.K. Fisher, M.D. Uhler (Eds.).
34. Noguchi K., Kawai Y., Fukuoka T., Senba E., Miki K. Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J. Neurosci. 1995, 15:7633-7643.
35. Obata K., Noguchi K. BDNF in sensory neurons and chronic pain. Neurosci. Res. 2006, 55:1-10.
36. Obata K., Yamanaka H., Dai Y., Tachibana T., Fukuoka T., Tokunaga A., Yoshikawa H., Noguchi K. Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J. Neurosci. 2003, 23:4117-4126.
37. Ossipov M.H., Zhang E.T., Carvajal C., Gardell L., Quirion R., Dumont Y., Lai J., Porreca F. Selective mediation of nerve injury-induced tactile hypersensitivity by neuropeptide Y. J. Neurosci. 2002, 22:9858-9867.
38. Pezet S., Mcmahon S.B. Neurotrophins: mediators and modulators of pain. Annu. Rev. Neurosci. 2006, 29:507-538.
39. Pezet S., MALCANGIO M., Mcmahon S.B. BDNF: a neuromodulator in nociceptive pathways?. Brain Res. Rev. 2002, 40:240-249.
40. Quintao N.L., Santos A.R., Campos M.M., CALIXTO J.B. The role of neurotrophic factors in genesis and maintenance of mechanical hypernociception after brachial plexus avulsion in mice. Pain 2008, 136:125-133.
41. Rage F., Silhol M., Tapia-Arancibia L. IL-1beta regulation of BDNF expression in rat cultured hypothalamic neurons depends on the presence of glial cells. Neurochem. Int. 2006, 49:433-441.
42. Salio C., Lossi L., Ferrini F., Merighi A. Ultrastructural evidence for a pre- and postsynaptic localization of full-length trkB receptors in substantia gelatinosa (lamina II) of rat and mouse spinal cord. Eur. J. Neurosci. 2005, 22:1951-1966.
43. Schafers M., Geis C., Brors D., Yaksh T.L., Sommer C. Anterograde transport of tumor necrosis factor-alpha in the intact and injured rat sciatic nerve. J. Neurosci. 2002, 22:536-545.
44. Schafers M., Marziniak M., Sorkin L.S., Yaksh T.L., Sommer C. Cyclooxygenase inhibition in nerve-injury- and TNF-induced hyperalgesia in the rat. Exp. Neurol. 2004, 185:160-168.
45. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 2007, 10:1361-1368.
46. Seltzer Z., Dubner R., Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990, 43:205-218.
47. Shu X.Q., Mendell L.M. Neurotrophins and hyperalgesia. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7693-7696.
48. Smith J.A., Davis C.L., Burgess G.M. Prostaglandin E2-induced sensitization of bradykinin-evoked responses in rat dorsal root ganglion neurons is mediated by cAMP-dependent protein kinase A. Eur. J. Neurosci. 2000, 12:3250-3258.
49. St-Jacques B., Ma W. Role of prostaglandin E2 in the synthesis of the pro-inflammatory cytokine interleukin-6 in primary sensory neurons: an in vivo and in vitro study. J. Neurochem. 2011, 118(5):841-854.
50. Sun H., Ren K., Zhong C.M., Ossipov M.H., Malan T.P., Lai J., Porreca F. Nerve injury-induced tactile allodynia is mediated via ascending spinal dorsal column projections. Pain 2001, 90:105-111.
51. Syriatowicz J.P., Hu D., Walker J.S., Tracey D.J. Hyperalgesia due to nerve injury: role of prostaglandins. Neuroscience 1999, 94:587-594.
52. Takahashi M., Kawaguchi M., Shimada K., Konishi N., Furuya H., Nakashima T. Cyclooxygenase-2 expression in Schwann cells and macrophages in the sciatic nerve after single spinal nerve injury in rats. Neurosci. Lett. 2004, 363:203-206.
53. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 1998, 20:709-726.
54. Thompson S.W., Bennett D.L., Kerr B.J., Bradbury E.J., Mcmahon S.B. Brain-derived neurotrophic factor is an endogenous modulator of nociceptive responses in the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7714-7718.
55. Toyomoto M., Ohta M., Okumura K., Yano H., Matsumoto K., Inoue S., Hayashi K., Ikeda K. Prostaglandins are powerful inducers of NGF and BDNF production in mouse astrocyte cultures. FEBS Lett. 2004, 562:211-215.
56. Vanegas H., Schaible H.G. Prostaglandins and cycloxygenases in the spinal cord. Prog. Neurobiol. 2001, 64:327-363.
57. Wang X., Ratnam J., Zou B., England P.M., Basbaum A.I. TrkB signaling is required for both the induction and maintenance of tissue and nerve injury-induced persistent pain. J. Neurosci. 2009, 29:5508-5515.
58. Yajima Y., NARITA M., NARITA M., Matsumoto N., Suzuki T. Involvement of a spinal brain-derived neurotrophic factor/full-length TrkB pathway in the development of nerve injury-induced thermal hyperalgesia in mice. Brain Res. 2002, 958:338-346.
59. Yajima Y., NARITA M., Usui A., Kaneko C., Miyatake M., NARITA M., Yamaguchi T., Tamaki H., Wachi H., Seyama Y., Suzuki T. Direct evidence for the involvement of brain-derived neurotrophic factor in the development of a neuropathic pain-like state in mice. J. Neurochem. 2005, 93:584-594.
60. Zhang H., Torregrossa M.M., Jutkiewicz E.M., Shi Y.G., Rice K.C., Woods J.H., Watson S.J., Ko M.C. Endogenous opioids upregulate brain-derived neurotrophic factor mRNA through delta- and micro-opioid receptors independent of antidepressant-like effects. Eur. J. Neurosci. 2006, 23:984-994.
61. Zhao J., Seereeram A., Nassar M.A., Levato A., Pezet S., Hathaway G., Morenilla-Palao C., Stirling C., Fitzgerald M., Mcmahon S.B., Rios M., Wood J.N. Nociceptor-derived brain-derived neurotrophic factor regulates acute and inflammatory but not neuropathic pain. Mol. Cell. Neurosci. 2006, 31:539-548.
62. Zhou X.F., Chie E.T., Deng Y.S., Zhong J.H., Xue Q., Rush R.A., Xian C.J. Injured primary sensory neurons switch phenotype for brain-derived neurotrophic factor in the rat. Neuroscience 1999, 92:841-853.
63. Zhou X.F., Deng Y.S., Xian C.J., Zhong J.H. Neurotrophins from dorsal root ganglia trigger allodynia after spinal nerve injury in rats. Eur. J. Neurosci. 2000, 12:100-105.
64. Zhou L.J., Ren W.J., Zhong Y., Yang T., Wei X.H., Xin W.J., Liu C.C., Zhou L.H., Li Y.Y., Liu X.G. Limited BDNF contributes to the failure of injury to skin afferents to produce a neuropathic pain condition. Pain 2010, 148:148-157.