Neonatal maternal deprivation sensitizes voltage-gated sodium channel currents in colon-specific dorsal root ganglion neurons in rats

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 4, 2013, Pages

  Hu, Shufen ^a   Xiao, Ying ^a   Zhu, Liyan ^a   Li, Lin ^a   Hu, Chuang Ying ^a   Jiang, Xinghong ^a   Xu, Guang Yin ^a  

^a SOOCHOW UNIVERSITY   (China)

Author keywords

Dorsal root ganglion; Irritable bowel syndrome; Neonatal maternal deprivation; Visceral pain; Voltage gated sodium channel

Indexed keywords

VOLTAGE GATED SODIUM CHANNEL;

ABDOMINAL REFLEX; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; IRRITABLE COLON; MALE; MATERNAL DEPRIVATION; NERVE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; SENSITIZATION; SPINAL GANGLION; VISCERAL PAIN; WESTERN BLOTTING; WITHDRAWAL REFLEX;

ANIMALS; COLON; GANGLIA, SPINAL; HYPERALGESIA; IRRITABLE BOWEL SYNDROME; MALE; MATERNAL DEPRIVATION; NAV1.8 VOLTAGE-GATED SODIUM CHANNEL; NEURONS; RATS; REFLEX, ABDOMINAL; TETRODOTOXIN;

EID: 84874032095     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00338.2012     Document Type: Article

References (46)

1. Al-Chaer ED, Kawasaki M, Pasricha PJ. A new model of chronic visceral hypersensitivity in adult rats induced by colon irritation during postnatal development. Gastroenterology 119: 1276-1285, 2000.
2. Arisawa T, Tahara T, Shiroeda H, Minato T, Matsue Y, Saito T, Fukuyama T, Otsuka T, Fukumura A, Nakamura M, Shibata T. Genetic polymorphisms of SCN10A are associated with functional dyspepsia in Japanese subjects. J Gastroenterol 2012 May 23. [Epub ahead of print].
3. Barreau F, Ferrier L, Fioramonti J, Bueno L. Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut 53: 501-506, 2004.
4. Bennett EJ, Tennant CC, Piesse C, Badcock CA, Kellow JE. Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 43: 256-261, 1998.
5. Bercik P, Wang L, Verdu EF, Mao YK, Blennerhassett P, Khan WI, Kean I, Tougas G, Collins SM. Visceral hyperalgesia and intestinal dysmotility in a mouse model of postinfective gut dysfunction. Gastroenterology 127: 179-187, 2004.
6. + currents in mouse colonic dorsal root ganglia neurons and their role in colitis-induced hyperexcitability. Am J Physiol Gastrointest Liver Physiol 287: G845-G855, 2004.
7. Beyak MJ, Vanner S. Inflammation-induced hyperexcitability of nociceptive gastrointestinal DRG neurones: the role of voltage-gated ion channels. Neurogastroenterol Motil 17: 175-186, 2005.
8. Blackshaw LA, Gebhart GF. The pharmacology of gastrointestinal nociceptive pathways. Curr Opin Pharmacol 2: 642-649, 2002.
9. Catterall WA, Perez-Reyes E, Snutch TP, Striessnig J. International Union of Pharmacology. XLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels. Pharmacol Rev 57: 411-425, 2005.
10. Chahine M, Chatelier A, Babich O, Krupp JJ. Voltage-gated sodium channels in neurological disorders. CNS Neurol Disord Drug Targets 7: 144-158, 2008.
11. Chung EK, Zhang X, Li Z, Zhang H, Xu H, Bian Z. Neonatal maternal separation enhances central sensitivity to noxious colorectal distention in rat. Brain Res 1153: 68-77, 2007.
12. Coutinho SV, Plotsky PM, Sablad M, Miller JC, Zhou H, Bayati AI, McRoberts JA, Mayer EA. Neonatal maternal separation alters stressinduced responses to viscerosomatic nociceptive stimuli in rat. Am J Physiol Gastrointest Liver Physiol 282: G307-G316, 2002.
13. Cregg R, Momin A, Rugiero F, Wood JN, Zhao J. Pain channelopathies. J Physiol 588: 1897-1904, 2010.
14. Cummins NW, Deziel PJ, Abraham RS, Razonable RR. Deficiency of cytomegalovirus (CMV)-specific CD8+ T cells in patients presenting with late-onset CMV disease several years after transplantation. Transpl Infect Dis 11: 20-27, 2009.
15. Dib-Hajj SD, Binshtok AM, Cummins TR, Jarvis MF, Samad T, Zimmermann K. Voltage-gated sodium channels in pain states: role in pathophysiology and targets for treatment. Brain Res Rev 60: 65-83, 2009.
16. Dib-Hajj SD, Cummins TR, Black JA, Waxman SG. Sodium channels in normal and pathological pain. Annu Rev Neurosci 33: 325-347, 2010.
17. + channel alpha subunit protein. J Physiol 546: 565-576, 2003.
18. Drossman DA, Camilleri M, Mayer EA, Whitehead WE. AGA technical review on irritable bowel syndrome. Gastroenterology 123: 2108-2131, 2002.
19. Frieboes LR, Palispis WA, Gupta R. Nerve compression activates selective nociceptive pathways and upregulates peripheral sodium channel expression in Schwann cells. J Orthop Res 28: 753-761, 2010.
20. Gareau MG, Jury J, Yang PC, MacQueen G, Perdue MH. Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr Res 59: 83-88, 2006.
21. + currents and inflammatory hyperalgesia. Proc Natl Acad Sci USA 96: 7645-7649, 1999.
22. Gold MS, Zhang L, Wrigley DL, Traub RJ. Prostaglandin E2 modulates TTX-RINa in rat colonic sensory neurons. J Neurophysiol 88: 1512-1522, 2002.
23. Goldin AL. Resurgence of sodium channel research. Annu Rev Physiol 63: 871-894, 2001.
24. Harty TP, Dib-Hajj SD, Tyrrell L, Blackman R, Hisama FM, Rose JB, Waxman SG. NaV1.7 mutant A863P in erythromelalgia: effects of altered activation and steady-state inactivation on excitability of nociceptive dorsal root ganglion neurons. J Neurosci 26: 12566-12575, 2006.
25. + current affects resting potential and response to depolarization in simulated spinal sensory neurons. J Neurophysiol 86: 1351-1364, 2001.
26. Hill OW, Price JS. Childhood bereavement and adult depression. Br J Psychiatry 113: 743-751, 1967.
27. Hodgdon KE, Hingtgen CM, Nicol GD. Dorsal root ganglia isolated from Nf1+/-mice exhibit increased levels of mRNA expression of voltage-dependent sodium channels. Neuroscience 206: 237-244, 2012.
28. Hogan QH. Role of decreased sensory neuron membrane calcium currents in the genesis of neuropathic pain. Croat Med J 48: 9-21, 2007.
29. Hu S, Yang J, Li L, Zhu L, Zhou Y, Xiao Y, Xu GY. Upregulation of endogenous cystathionine--synthase contributes to visceral hypersensitivity in adult rats following neonatal maternal deprivation (Abstract). Gastroenterology 142, Suppl 1: S-702, 2012.
30. Liu XM, Tao M, Han XD, Fan Q, Lin JR. Gating kinetics of potassium channel and effects of nerve growth factors in PC12 cells analyzed with fractal model. Acta Pharmacol Sin 22: 103-110, 2001.
31. Luo JL, Qin HY, Wong CK, Tsang SY, Huang Y, Bian ZX. Enhanced excitability and down-regulated voltage-gated potassium channels in colonic DRG neurons from neonatal maternal separation rats. J Pain 12: 600-609, 2011.
32. Rosztoczy A, Fioramonti J, Jarmay K, Barreau F, Wittmann T, Bueno L. Influence of sex and experimental protocol on the effect of maternal deprivation on rectal sensitivity to distension in the adult rat. Neurogastroenterol Motil 15: 679-686, 2003.
33. Sandler RS, Drossman DA, Nathan HP, McKee DC. Symptom complaints and health care seeking behavior in subjects with bowel dysfunction. Gastroenterology 87: 314-318, 1984.
34. Schwartz ES, Christianson JA, Chen X, La JH, Davis BM, Albers KM, Gebhart GF. Synergistic role of TRPV1 and TRPA1 in pancreatic pain and inflammation. Gastroenterology 140: 1283-1291. e1-2, 2011.
35. Shimazu K, Takeda K, Yu ZX, Jiang H, Liu XW, Nelson PG, Guroff G. Multiple acute effects on the membrane potential of PC12 cells produced by nerve growth factor (NGF). J Cell Physiol 203: 501-509, 2005.
36. Stewart T, Beyak MJ, Vanner S. Ileitis modulates potassium and sodium currents in guinea pig dorsal root ganglia sensory neurons. J Physiol 552: 797-807, 2003.
37. Toma H, Winston J, Micci MA, Shenoy M, Pasricha PJ. Nerve growth factor expression is up-regulated in the rat model of L-arginine-induced acute pancreatitis. Gastroenterology 119: 1373-1381, 2000.
38. Wada A. Roles of voltage-dependent sodium channels in neuronal development, pain, and neurodegeneration. J Pharm Sci 102: 253-268, 2006.
39. Whitehead WE, Crowell MD, Robinson JC, Heller BR, Schuster MM. Effects of stressful life events on bowel symptoms: subjects with irritable bowel syndrome compared with subjects without bowel dysfunction. Gut 33: 825-830, 1992.
40. Winston J, Shenoy M, Medley D, Naniwadekar A, Pasricha PJ. The vanilloid receptor initiates and maintains colonic hypersensitivity induced by neonatal colon irritation in rats. Gastroenterology 132: 615-627, 2007.
41. Winston JH, He ZJ, Shenoy M, Xiao SY, Pasricha PJ. Molecular and behavioral changes in nociception in a novel rat model of chronic pancreatitis for the study of pain. Pain 117: 214-222, 2005.
42. Woolf CJ, Safieh-Garabedian B, Ma QP, Crilly P, Winter J. Nerve growth factor contributes to the generation of inflammatory sensory hypersensitivity. Neuroscience 62: 327-331, 1994.
43. Xu GY, Huang LY. Peripheral inflammation sensitizes P2X receptormediated responses in rat dorsal root ganglion neurons. J Neurosci 22: 93-102, 2002.
44. Xu GY, Shenoy M, Winston JH, Mittal S, Pasricha PJ. P2X receptormediated visceral hyperalgesia in a rat model of chronic visceral hypersensitivity. Gut 57: 1230-1237, 2008.
45. + current of pancreas-specific afferent neurons in a rat model of chronic pancreatitis. Am J Physiol Gastrointest Liver Physiol 291: G424-G431, 2006.
46. Yoshimura N, de Groat WC. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 19: 4644-4653, 1999.