Interactive Involvement of Brain Derived Neurotrophic Factor, Nerve Growth Factor, and Calcitonin Gene Related Peptide in Colonic Hypersensitivity in the Rat

Overview

Journal Gut

Specialty Gastroenterology

Date 2006 Jan 13

PMID 16401692

Citations 58

Authors

L Delafoy

A Gelot

D Ardid

A Eschalier

C Bertrand

A M Doherty

L Diop

Affiliations

Soon will be listed here.

Abstract

Background And Aims: Neutrophins are involved in somatic and visceral hypersensitivity. The action of nerve growth factor (NGF) on sensory neurones contributes to the development of referred colonic hypersensitivity induced by trinitrobenzene sulfonic acid (TNBS). Based on data on brain derived neurotrophic factor (BDNF) and calcitonin gene related peptide (CGRP) in pain, the aims of the present study were: (1) to investigate the involvement of BDNF and CGRP in this model of referred colonic hypersensitivity, (2) to test the effect of exogenous BDNF and CGRP on the colonic pain threshold, and (3) to investigate the relationship between BDNF, NGF, and CGRP by testing antineurotrophin antibodies or h-CGRP 8-37 (a CGRP antagonist) on bowel hypersensitivity induced by these peptides.

Methods: Colonic sensitivity was assessed using a colonic distension procedure.

Results: Anti-BDNF antibody and h-CGRP 8-37 reversed the induced decrease in colonic threshold (33.4 (2.1) and 40.3 (4.1) mm Hg, respectively, compared with a vehicle score of approximately 18 mm Hg; p<0.001). BDNF (1-100 ng/rat intraperitoneally) induced a significant dose dependent decrease in colonic reaction threshold in healthy rats. This effect was reversed by an anti-BDNF antibody and an anti-NGF antibody (33.4 (0.6) v 18.7 (0.7) mm Hg (p<0.001), anti-NGF v vehicle). NGF induced colonic hypersensitivity was reversed by h-CGRP 8-37 but not by the anti-BDNF antibody. Finally, antineurotrophin antibody could not reverse CGRP induced colonic hypersensitivity (at a dose of 1 microg/kg intraperitoneally).

Conclusion: Systemic BDNF, NGF, and CGRP can induce visceral hypersensitivity alone and interactively. This cascade might be involved in TNBS induced referred colonic hypersensitivity in which each of these peptides is involved.

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References

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(13):4891-900. PMC: 6762362. View

Donnerer J, Amann R, Schuligoi R, Skofitsch G . Complete recovery by nerve growth factor of neuropeptide content and function in capsaicin-impaired sensory neurons. Brain Res. 1996; 741(1-2):103-8. DOI: 10.1016/s0006-8993(96)00905-5. View

Zhu Z, Friess H, Wang L, Zimmermann A, Buchler M . Brain-derived neurotrophic factor (BDNF) is upregulated and associated with pain in chronic pancreatitis. Dig Dis Sci. 2001; 46(8):1633-9. DOI: 10.1023/a:1010684916863. View

Skaper S, Pollock M, Facci L . Mast cells differentially express and release active high molecular weight neurotrophins. Brain Res Mol Brain Res. 2001; 97(2):177-85. DOI: 10.1016/s0169-328x(01)00314-x. View

Miletic G, Miletic V . Increases in the concentration of brain derived neurotrophic factor in the lumbar spinal dorsal horn are associated with pain behavior following chronic constriction injury in rats. Neurosci Lett. 2002; 319(3):137-40. DOI: 10.1016/s0304-3940(01)02576-9. View

Herbert M, Holzer P . [Neurogenic inflammation. I. Basic mechanisms, physiology and pharmacology]. Anasthesiol Intensivmed Notfallmed Schmerzther. 2002; 37(6):314-25. DOI: 10.1055/s-2002-32233. View

Herbert M, Holzer P . [Neurogenic inflammation. II. pathophysiology and clinical implications]. Anasthesiol Intensivmed Notfallmed Schmerzther. 2002; 37(7):386-94. DOI: 10.1055/s-2002-32701. View

Torrents D, Torres R, De Mora F, Vergara P . Antinerve growth factor treatment prevents intestinal dysmotility in Trichinella spiralis-infected rats. J Pharmacol Exp Ther. 2002; 302(2):659-65. DOI: 10.1124/jpet.102.035287. View

Diop L, Raymond F, Fargeau H, Petoux F, Chovet M, Doherty A . Pregabalin (CI-1008) inhibits the trinitrobenzene sulfonic acid-induced chronic colonic allodynia in the rat. J Pharmacol Exp Ther. 2002; 302(3):1013-22. DOI: 10.1124/jpet.302.3.1013. View

10.

Tarrerias A, Millecamps M, Alloui A, Beaughard C, Kemeny J, Bourdu S . Short-chain fatty acid enemas fail to decrease colonic hypersensitivity and inflammation in TNBS-induced colonic inflammation in rats. Pain. 2002; 100(1-2):91-7. DOI: 10.1016/s0304-3959(02)00234-8. View

11.

Pezet S, Malcangio M, Lever I, Perkinton M, Thompson S, Williams R . Noxious stimulation induces Trk receptor and downstream ERK phosphorylation in spinal dorsal horn. Mol Cell Neurosci. 2002; 21(4):684-95. DOI: 10.1006/mcne.2002.1205. View

12.

Pardridge W . Neurotrophins, neuroprotection and the blood-brain barrier. Curr Opin Investig Drugs. 2003; 3(12):1753-7. View

13.

Pezet S, Malcangio M, McMahon S . BDNF: a neuromodulator in nociceptive pathways?. Brain Res Brain Res Rev. 2003; 40(1-3):240-9. DOI: 10.1016/s0165-0173(02)00206-0. View

14.

Chao M . Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat Rev Neurosci. 2003; 4(4):299-309. DOI: 10.1038/nrn1078. View

15.

Delafoy L, Raymond F, Doherty A, Eschalier A, Diop L . Role of nerve growth factor in the trinitrobenzene sulfonic acid-induced colonic hypersensitivity. Pain. 2003; 105(3):489-497. DOI: 10.1016/S0304-3959(03)00266-5. View

16.

Lu B . Acute and long-term synaptic modulation by neurotrophins. Prog Brain Res. 2004; 146:137-50. DOI: 10.1016/s0079-6123(03)46010-x. View

17.

Barreau F, Cartier C, Ferrier L, Fioramonti J, Bueno L . Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology. 2004; 127(2):524-34. DOI: 10.1053/j.gastro.2004.05.019. View

18.

Ritchie J . Pain from distension of the pelvic colon by inflating a balloon in the irritable colon syndrome. Gut. 1973; 14(2):125-32. PMC: 1412559. DOI: 10.1136/gut.14.2.125. View

19.

Zimmermann M . Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983; 16(2):109-110. DOI: 10.1016/0304-3959(83)90201-4. View

20.

Clague J, Sternini C, Brecha N . Localization of calcitonin gene-related peptide-like immunoreactivity in neurons of the rat gastrointestinal tract. Neurosci Lett. 1985; 56(1):63-8. DOI: 10.1016/0304-3940(85)90441-0. View