Visceral hyperalgesia induced by neonatal maternal separation is associated with nerve growth factor-mediated central neuronal plasticity in rat spinal cord

Neuroscience

Volumn 149, Issue 3, 2007, Pages 685-695

  Chung, E K Y ^a   Zhang, X J ^a   Xu, H X ^b   Sung, J J Y ^c   Bian, Z X ^a  

^a HONG KONG BAPTIST UNIVERSITY   (Hong Kong)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

colorectal distention; irritable bowel syndrome; neonatal maternal separation; nerve growth factor; tyrosine kinase receptor A; visceral hyperalgesia

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NERVE GROWTH FACTOR; PROTEIN TYROSINE KINASE A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM; CHRONIC PAIN; COLON DILATATION; CONTROLLED STUDY; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IRRITABLE COLON; LUMBAR SPINAL CORD; LUMBOSACRAL SPINE; NERVE CELL PLASTICITY; NEUROENDOCRINE SYSTEM; NEWBORN; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SACRAL SPINAL CORD; VISCERAL PAIN; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ANXIETY, SEPARATION; BLOTTING, WESTERN; CALCITONIN GENE-RELATED PEPTIDE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MATERNAL DEPRIVATION; NERVE GROWTH FACTOR; NEURONAL PLASTICITY; PREGNANCY; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; RECEPTOR, TRKA; SPINAL CORD;

EID: 35448947305     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2007.07.055     Document Type: Article

References (52)

1. Al-Chaer E.D., Kawasaki M., and Pasricha P.J. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 119 (2000) 1276-1285
2. Al-Chaer E.D., and Traub R.J. Biological basis of visceral pain: recent developments. Pain 96 (2002) 221-225
3. Anand P., Aziz Q., Willert R., and van Oudenhove L. Peripheral and central mechanisms of visceral sensitization in man. Neurogastroenterol Motil 19 (2007) 29-46
4. Barreau F., Cartier C., Ferrier L., Fioramonti J., and Bueno L. Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology 127 (2004) 524-534
5. Barreau F., Cartier C., Leveque M., Ferrier L., Moriez R., Laroute V., Rosztoczy A., Fioramonti J., and Bueno L. Pathways involved in gut mucosal barrier dysfunction induced in adult rats by maternal deprivation: CRF and NGF interplay. J Physiol 580 (2007) 347-356
6. Barreau F., Ferrier L., Fioramonti J., and Bueno L. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 53 (2004) 501-506
7. Benarroch E.E. Pain-autonomic interactions: a selective review. Clin Auton Res 11 (2001) 343-349
8. Bielefeldt K., Lamb K., and Gebhart G.F. Convergence of sensory pathways in the development of somatic and visceral hypersensitivity. Am J Physiol Gastrointest Liver Physiol 291 (2006) G658-G665
9. Brown A., Ricci M.J., and Weaver L.C. NGF message and protein distribution in the injured rat spinal cord. Exp Neurol 188 (2004) 115-127
10. Caldji C., Diorio J., and Meaney M.J. Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48 (2000) 1164-1174
11. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., and Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 95 (1998) 5335-5340
12. 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
13. Chung E.K.Y., Zhang X., Li Z., Zhang H., Xu H., and Bian Z. Neonatal maternal separation enhances central sensitivity to noxious colorectal distention in rat. Brain Res 1153 (2007) 68-77
14. Cirulli F., Alleva E., Antonelli A., and Aloe L. NGF expression in the developing rat brain: effects of maternal separation. Brain Res Dev Brain Res 123 (2000) 129-134
15. Coutinho S.V., Plotsky P.M., Sablad M., Miller J.C., Zhou H., Bayati A.I., McRoberts J.A., and Mayer E.A. Neonatal maternal separation alters stress-induced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 282 (2002) G307-G316
16. Davis B.M., Albers K.M., Seroogy K.B., and Katz D.M. Overexpression of nerve growth factor in transgenic mice induces novel sympathetic projections to primary sensory neurons. J Comp Neurol 349 (1994) 464-474
17. Delafoy L., Gelot A., Ardid D., Eschalier A., Bertrand C., Doherty A.M., and Diop L. Interactive involvement of brain derived neurotrophic factor, nerve growth factor, and calcitonin gene related peptide in colonic hypersensitivity in the rat. Gut 55 (2006) 940-945
18. Fitzgerald M. The development of nociceptive circuits. Nat Rev Neurosci 6 (2005) 507-520
19. Fjell J., Cummins T.R., Fried K., Black J.A., and Waxman S.G. In vivo NGF deprivation reduces SNS expression and TTX-R sodium currents in IB4-negative DRG neurons. J Neurophysiol 81 (1999) 803-810
20. Gareau M.G., Jury J., Yang P.C., MacQueen G., and Perdue M.H. Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr Res 59 (2006) 83-88
21. Genest S.E., Gulemetova R., Laforest S., Drolet G., and Kinkead R. Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J Physiol 554 (2004) 543-557
22. Giovengo S.L., Russell I.J., and Larson A.A. Increased concentrations of nerve growth factor in cerebrospinal fluid of patients with fibromyalgia. J Rheumatol 26 (1999) 1564-1569
23. Gould III H.J., Gould T.N., England J.D., Paul D., Liu Z.P., and Levinson S.R. A possible role for nerve growth factor in the augmentation of sodium channels in models of chronic pain. Brain Res 854 (2000) 19-29
24. Gue M., Del Rio-Lacheze C., Eutamene H., Theodorou V., Fioramonti J., and Bueno L. Stress-induced visceral hypersensitivity to rectal distension in rats: role of CRF and mast cells. Neurogastroenterol Motil 9 (1997) 271-279
25. Ji R.R., Samad T.A., Jin S.X., Schmoll R., and Woolf C.J. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Neuron 36 (2002) 57-68
26. Kerr B.J., Souslova V., McMahon S.B., and Wood J.N. A role for the TTX-resistant sodium channel Nav 1.8 in NGF-induced hyperalgesia, but not neuropathic pain. Neuroreport 12 (2001) 3077-3080
27. Krenz N.R., Meakin S.O., Krassioukov A.V., and Weaver L.C. Neutralizing intraspinal nerve growth factor blocks autonomic dysreflexia caused by spinal cord injury. J Neurosci 19 (1999) 7405-7414
28. Lessmann V., Gottmann K., and Malcangio M. Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69 (2003) 341-374
29. Lewin G.R., Rueff A., and Mendell L.M. Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur J Neurosci 6 (1994) 1903-1912
30. Lindholm D., Castren E., Berzaghi M., Blochl A., and Thoenen H. Activity-dependent and hormonal regulation of neurotrophin mRNA levels in the brain-implications for neuronal plasticity. J Neurobiol 25 (1994) 1362-1372
31. Liu D., Caldji C., Sharma S., Plotsky P.M., and Meaney M.J. Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinephrine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12 (2000) 5-12
32. Malcangio M., Bowery N.G., Flower R.J., and Perretti M. Effect of interleukin-1 beta on the release of substance P from rat isolated spinal cord. Eur J Pharmacol 299 (1996) 113-118
33. Malcangio M., Garrett N.E., Cruwys S., and Tomlinson D.R. Nerve growth factor- and neurotrophin-3-induced changes in nociceptive threshold and the release of substance P from the rat isolated spinal cord. J Neurosci 17 (1997) 8459-8467
34. Mayer E.A. Spinal and supraspinal modulation of visceral sensation. Gut 47 Suppl 4 (2000) iv69-iv72
35. Mayer E.A., Naliboff B.D., and Craig A.D. Neuroimaging of the brain-gut axis: from basic understanding to treatment of functional GI disorders. Gastroenterology 131 (2006) 1925-1942
36. Mendell L.M. Neurotrophin action on sensory neurons in adults: an extension of the neurotrophic hypothesis. Pain Suppl 6 (1999) S127-S132
37. Michael G.J., Averill S., Nitkunan A., Rattray M., Bennett D.L., Yan Q., and 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 17 (1997) 8476-8490
38. Michael G.J., Kaya E., Averill S., Rattray M., Clary D.O., and Priestley J.V. TrkA immunoreactive neurones in the rat spinal cord. J Comp Neurol 385 (1997) 441-455
39. Millan M.J. The induction of pain: an integrative review. Prog Neurobiol 57 (1999) 1-164
40. Molliver D.C., Wright D.E., Leitner M.L., Parsadanian A.S., Doster K., Wen D., Yan Q., and Snider W.D. IB4-binding DRG neurons switch from NGF to GDNF dependence in early postnatal life. Neuron 19 (1997) 849-861
41. Petruska J.C., and Mendell L.M. The many functions of nerve growth factor: multiple actions on nociceptors. Neurosci Lett 361 (2004) 168-171
42. Pezet S., Onteniente B., Grannec G., and Calvino B. Chronic pain is associated with increased TrkA immunoreactivity in spinoreticular neurons. J Neurosci 19 (1999) 5482-5492
43. Pezet S., Onteniente B., Jullien J., Junier M.P., Grannec G., Rudkin B.B., and Calvino B. Differential regulation of NGF receptors in primary sensory neurons by adjuvant-induced arthritis in the rat. Pain 90 (2001) 113-125
44. Pihoker C., Owens M.J., Kuhn C.M., Schanberg S.M., and Nemeroff C.B. Maternal separation in neonatal rats elicits activation of the hypothalamic-pituitary-adrenocortical axis: a putative role for corticotropin-releasing factor. Psychoneuroendocrinology 18 (1993) 485-493
45. Ramer M.S., Bradbury E.J., and McMahon S.B. Nerve growth factor induces P2X(3) expression in sensory neurons. J Neurochem 77 (2001) 864-875
46. 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
47. Sarchielli P., Alberti A., Floridi A., and Gallai V. Levels of nerve growth factor in cerebrospinal fluid of chronic daily headache patients. Neurology 57 (2001) 132-134
48. Spillantini M.G., Aloe L., Alleva E., De Simone R., Goedert M., and Levi-Montalcini R. Nerve growth factor mRNA and protein increase in hypothalamus in a mouse model of aggression. Proc Natl Acad Sci U S A 86 (1989) 8555-8559
49. Stam R., Ekkelenkamp K., Frankhuijzen A.C., Bruijnzeel A.W., Akkermans L.M., and Wiegant V.M. Long-lasting changes in central nervous system responsivity to colonic distention after stress in rats. Gastroenterology 123 (2002) 1216-1225
50. Welting O., Van Den Wijngaard R.M., De Jonge W.J., Holman R., and Boeckxstaens G.E. Assessment of visceral sensitivity using radio telemetry in a rat model of maternal separation. Neurogastroenterol Motil 17 (2005) 838-845
51. Woolf C.J. Phenotypic modification of primary sensory neurons: the role of nerve growth factor in the production of persistent pain. Philos Trans R Soc Lond B Biol Sci 351 (1996) 441-448
52. Zafra F., Hengerer B., Leibrock J., Thoenen H., and Lindholm D. Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J 9 (1990) 3545-3550