Brain-derived neurotrophic factor, acting at the spinal cord level, participates in bladder hyperactivity and referred pain during chronic bladder inflammation

Neuroscience

Volumn 234, Issue , 2013, Pages 88-102

  Frias, B ^a,b   Allen, S ^c   Dawbarn, D ^c   Charrua, A ^a,b   Cruz, F ^b,d   Cruz, C D ^a,b  

^a University of Porto   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

^d HOSPITAL DE SÃO JOÃO   (Portugal)

Author keywords

BDNF; Bladder; Bladder hyperactivity; Cystitis; Inflammation; Visceral pain

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; TYROSINE KINASE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER CONTRACTION; BLADDER DISEASE; BLADDER HYPERACTIVITY; CHRONIC DISEASE; CONTROLLED STUDY; CYSTITIS; ENZYME PHOSPHORYLATION; FEMALE; GRAY MATTER; MICTURITION REFLEX; NONHUMAN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REFERRED PAIN; SKIN SENSITIVITY; SPINAL CORD;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CARBAZOLES; CYCLOPHOSPHAMIDE; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; INDOLE ALKALOIDS; INJECTIONS, SPINAL; PAIN, REFERRED; PROTEIN KINASE INHIBITORS; RATS; RECEPTOR, TRKB; SPINAL CORD; URINARY BLADDER; UVEITIS, INTERMEDIATE;

EID: 84873488462     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.12.044     Document Type: Article

References (52)

1. Ahmed S., Reynolds B.A., Weiss S. BDNF enhances the differentiation but not the survival of CNS stem cell-derived neuronal precursors. J Neurosci 1995, 15:5765-5778.
2. Banfield M.J., Naylor R.L., Robertson A.G., Allen S.J., Dawbarn D., Brady R.L. Specificity in Trk receptor:neurotrophin interactions: the crystal structure of TrkB-d5 in complex with neurotrophin-4/5. Structure 2001, 9:1191-1199.
3. Bardoni R., Ghirri A., Salio C., Prandini M., Merighi A. BDNF-mediated modulation of GABA and glycine release in dorsal horn lamina II from postnatal rats. Dev Neurobiol 2007, 67:960-975.
4. Blok B.F., de Weerd H., Holstege G. The pontine micturition center projects to sacral cord GABA immunoreactive neurons in the cat. Neurosci Lett 1997, 233:109-112.
5. Coggeshall R.E. Fos, nociception and the dorsal horn. Prog Neurobiol 2005, 77:299-352.
6. Costigan M., Woolf C.J. Pain: molecular mechanisms. J Pain 2000, 1:35-44.
7. Cruz C.D., Avelino A., McMahon S.B., Cruz F. Increased spinal cord phosphorylation of extracellular signal-regulated kinases mediates micturition overactivity in rats with chronic bladder inflammation. Eur J Neurosci 2005, 21:773-781.
8. Cruz C.D., Cruz F. The ERK 1 and 2 pathway in the nervous system: from basic aspects to possible clinical applications in pain and visceral dysfunction. Curr Neuropharmacol 2007, 5:244-252.
9. Delafoy L., Gelot A., Ardid D., Eschalier A., Bertrand C., Doherty A.M., Diop L. Interactive involvement of brain derived neurotrophic factor, nerve growth factor, and calcitonin gene related peptide in colonic hypersensitivity in the rat. Gut 2006, 55:940-945.
10. Dinis P., Charrua A., Avelino A., Yaqoob M., Bevan S., Nagy I., Cruz F. Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J Neurosci 2004, 24:11253-11263.
11. Fumagalli F., Racagni G., Riva M.A. Shedding light into the role of BDNF in the pharmacotherapy of Parkinson's disease. Pharmacogenomics J 2006, 6:95-104.
12. 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.
13. Haddad J.J. N-methyl-D-aspartate (NMDA) and the regulation of mitogen-activated protein kinase (MAPK) signaling pathways: a revolving neurochemical axis for therapeutic intervention?. Prog Neurobiol 2005, 77:252-282.
14. Hashimoto K. Brain-derived neurotrophic factor as a biomarker for mood disorders: an historical overview and future directions. Psychiatry Clin Neurosci 2010, 64:341-357.
15. Hashimoto K., Koizumi H., Nakazato M., Shimizu E., Iyo M. Role of brain-derived neurotrophic factor in eating disorders: recent findings and its pathophysiological implications. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:499-504.
16. Hughes M.S., Shenoy M., Liu L., Colak T., Mehta K., Pasricha P.J. Brain-derived neurotrophic factor is upregulated in rats with chronic pancreatitis and mediates pain behavior. Pancreas 2011, 40:551-556.
17. Jarrell, J. 2009. Demonstration of cutaneous allodynia in association with chronic pelvic pain. J Vis Exp. (28). Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2796663/.
18. Ji R.R., Baba H., Brenner G.J., Woolf C.J. Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 1999, 2:1114-1119.
19. Ji R.R., Gereau R.W.t., Malcangio M., Strichartz G.R. MAP kinase and pain. Brain Res Rev 2009, 60:135-148.
20. Jungbluth S., Koentges G., Lumsden A. Coordination of early neural tube development by BDNF/trkB. Development 1997, 124:1877-1885.
21. Kernie S.G., Liebl D.J., Parada L.F. BDNF regulates eating behavior and locomotor activity in mice. EMBO J 2000, 19:1290-1300.
22. Kerr B.J., Bradbury E.J., Bennett D.L., Trivedi P.M., Dassan P., French J., Shelton D.B., McMahon S.B., Thompson S.W. Brain-derived neurotrophic factor modulates nociceptive sensory inputs and NMDA-evoked responses in the rat spinal cord. J Neurosci 1999, 19:5138-5148.
23. Kim J.C., Kim D.B., Seo S.I., Park Y.H., Hwang T.K. Nerve growth factor and vanilloid receptor expression, and detrusor instability, after relieving bladder outlet obstruction in rats. BJU Int 2004, 94:915-918.
24. Latremoliere A., Woolf C.J. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain 2009, 10:895-926.
25. Lever I., Cunningham J., Grist J., Yip P.K., Malcangio M. Release of BDNF and GABA in the dorsal horn of neuropathic rats. Eur J Neurosci 2003, 18:1169-1174.
26. Lever I.J., Bradbury E.J., Cunningham J.R., Adelson D.W., Jones M.G., McMahon S.B., Marvizon J.C., Malcangio M. Brain-derived neurotrophic factor is released in the dorsal horn by distinctive patterns of afferent fiber stimulation. J Neurosci 2001, 21:4469-4477.
27. Lever I.J., Pezet S., McMahon S.B., Malcangio M. The signaling components of sensory fiber transmission involved in the activation of ERK MAP kinase in the mouse dorsal horn. Mol Cell Neurosci 2003, 24:259-270.
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. Miyazato M., Sasatomi K., Hiragata S., Sugaya K., Chancellor M.B., de Groat W.C., Yoshimura N. Suppression of detrusor-sphincter dysynergia by GABA-receptor activation in the lumbosacral spinal cord in spinal cord-injured rats. Am J Physiol Regul Integr Comp Physiol 2008, 295:R336-R342.
30. Miyazato M., Yoshimura N., Nishijima S., Sugaya K. Roles of glycinergic and gamma-aminobutyric-ergic mechanisms in the micturition reflex in rats. Low Urin Tract Symptom 2009, 1:S70-S73.
31. Muda M., Boschert U., Dickinson R., Martinou J.C., Martinou I., Camps M., Schlegel W., Arkinstall S. MKP-3, a novel cytosolic protein-tyrosine phosphatase that exemplifies a new class of mitogen-activated protein kinase phosphatase. J Biol Chem 1996, 271:4319-4326.
32. Naylor R.L., Robertson A.G., Allen S.J., Sessions R.B., Clarke A.R., Mason G.G., Burston J.J., Tyler S.J., Wilcock G.K., Dawbarn D. A discrete domain of the human TrkB receptor defines the binding sites for BDNF and NT-4. Biochem Biophys Res Commun 2002, 291:501-507.
33. Pezet S., Cunningham J., Patel J., Grist J., Gavazzi I., Lever I.J., Malcangio M. BDNF modulates sensory neuron synaptic activity by a facilitation of GABA transmission in the dorsal horn. Mol Cell Neurosci 2002, 21:51-62.
34. Pezet S., Malcangio M., Lever I.J., Perkinton M.S., Thompson S.W., Williams R.J., McMahon S.B. Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn. Mol Cell Neurosci 2002, 21:684-695.
35. Pezet S., Malcangio M., McMahon S.B. BDNF: a neuromodulator in nociceptive pathways?. Brain Res Brain Res Rev 2002, 40:240-249.
36. Pezet S., McMahon S.B. Neurotrophins: mediators and modulators of pain. Annu Rev Neurosci 2006, 29:507-538.
37. Pinto R., Frias B., Allen S., Dawbarn D., McMahon S.B., Cruz F., Cruz C.D. Sequestration of brain derived nerve factor by intravenous delivery of TrkB-Ig2 reduces bladder overactivity and noxious input in animals with chronic cystitis. Neuroscience 2010, 166:907-916.
38. Ren K., Dubner R. Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-TrkB signaling and NMDA receptors. Mol Neurobiol 2007, 35:224-235.
39. Salio C., Averill S., Priestley J.V., Merighi A. Costorage of BDNF and neuropeptides within individual dense-core vesicles in central and peripheral neurons. Dev Neurobiol 2007, 67:326-338.
40. 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.
41. Shu X.Q., Llinas A., Mendell L.M. Effects of trkB and trkC neurotrophin receptor agonists on thermal nociception: a behavioral and electrophysiological study. Pain 1999, 80:463-470.
42. Shu X.Q., Mendell L.M. Neurotrophins and hyperalgesia. Proc Natl Acad Sci U S A 1999, 96:7693-7696.
43. Slack S.E., Grist J., Mac Q., McMahon S.B., Pezet S. TrkB expression and phospho-ERK activation by brain-derived neurotrophic factor in rat spinothalamic tract neurons. J Comp Neurol 2005, 489:59-68.
44. Slack S.E., Pezet S., McMahon S.B., Thompson S.W., Malcangio M. Brain-derived neurotrophic factor induces NMDA receptor subunit one phosphorylation via ERK and PKC in the rat spinal cord. Eur J Neurosci 2004, 20:1769-1778.
45. Slack S.E., Thompson S.W. Brain-derived neurotrophic factor induces NMDA receptor 1 phosphorylation in rat spinal cord. Neuroreport 2002, 13:1967-1970.
46. 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.
47. Tian S.L., Wang X.Y., Ding G.H. Repeated electro-acupuncture attenuates chronic visceral hypersensitivity and spinal cord NMDA receptor phosphorylation in a rat irritable bowel syndrome model. Life Sci 2008, 83:356-363.
48. Vizzard M.A. Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 2000, 161:273-284.
49. Woolf C.J. Central sensitization: implications for the diagnosis and treatment of pain. Pain 2011, 152:S2-S15.
50. 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.
51. Zhu Z.W., Friess H., Wang L., Zimmermann A., Buchler M.W. Brain-derived neurotrophic factor (BDNF) is upregulated and associated with pain in chronic pancreatitis. Dig Dis Sci 2001, 46:1633-1639.
52. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.