TRPV1 mediates the uterine capsaicin-induced NMDA NR2B-dependent cross-organ reflex sensitization in anesthetized rats

American Journal of Physiology - Renal Physiology

Volumn 295, Issue 5, 2008, Pages

  Peng, Hsien Yu ^a,b   Chang, Hung Ming ^a   Lee, Shin Da ^c   Huang, Pei Chen ^d   Chen, Gin Den ^e   Lai, Cheng Hung ^b   Lai, Cheng Yuan ^a,b   Chiu, Chun Hsien ^a,b   Tung, Kwong Chung ^b   Lin, Tzer Bin ^a,f,g  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^e CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^f SAINT PAUL S HOSPITAL   (Taiwan)

^g NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

C fiber; Desensitization; Pain; Spinal cord

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 HYDROXY 1 [2 (4 HYDROXYPHENOXY)ETHYL] 4 (4 METHYLBENZYL)PIPERIDINE; CAPSAICIN; CAPSAZEPINE; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; AMINO ACID RECEPTOR BLOCKING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; DRUG DERIVATIVE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR2B NMDA RECEPTOR; PD 174494; PIPERIDINE DERIVATIVE; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; FEMALE; NERVE FIBER; NONHUMAN; PELVIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REFLEX; SENSITIZATION; SENSORY NERVE; SENSORY NERVE CONDUCTION; STIMULATION; URETHRA; URETHRA PRESSURE; UTERUS; UTERUS HORN; ACTION POTENTIAL; ANESTHESIA; ANIMAL; DOSE RESPONSE; DRUG ANTAGONISM; DRUG EFFECT; ELECTROSTIMULATION; INNERVATION; METABOLISM; PATHOPHYSIOLOGY; PELVIS PAIN SYNDROME; PHOSPHORYLATION; PHYSIOLOGY; SENSORY NERVE CELL; SMOOTH MUSCLE; SPINAL CORD; SPRAGUE DAWLEY RAT;

2-AMINO-5-PHOSPHONOVALERATE; ACTION POTENTIALS; ANESTHESIA; ANIMALS; CAPSAICIN; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; MUSCLE, SMOOTH; NEURONS, AFFERENT; PELVIC PAIN; PHOSPHORYLATION; PIPERIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; REFLEX; SPINAL CORD; TRPV CATION CHANNELS; UTERUS;

EID: 57349181516     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00126.2008     Document Type: Article

References (86)

1. Alagiri M, Chottiner S, Ratner V, Slade D, Hanno PM. Interstitial cystitis: unexplained associations with other chronic disease and pain syndromes. Urology 49: 52-57, 1997.
2. Avelino A, Cruz F. TRPV1 (vanilloid receptor) in the urinary tract: expression, function and clinical applications. Naunyn Schmiedebergs Arch Pharmacol 373: 287-299, 2006.
3. Berkley KJ. A life of pelvic pain. Physiol Behav 86: 272-280, 2005.
4. Berkley KJ, Dmitrieva N, Curtis KS, Papka RE. Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci USA 101: 11094-11098, 2004.
5. Berkley KJ, Hubscher CH. Are there separate central nervous system pathways for touch and pain? Nat Med 1: 766-773, 1995.
6. Birder LA, Kanaj AJ, De Groat WC, Kiss S, Nealen ML, Wang E, Burke NE, Dineley KE, Watkins S, Caterina MJ. Vanilloid receptor expression suggests a sensory role for urinary bladder epithelial cells. Proc Natl Acad Sci USA 98: 13396-13401, 2001.
7. Birder LA, Kullmann FA, Lee H, Barrick S, de Groat WC, Kanai A, Caterina M. Activation of urothelial transient receptor potential vanilloid 4 by 4alpha-phorbol 12,13-didecanoate contributes to altered bladder reflexes in the rat. J Pharmacol Exp Ther 323: 227-235, 2007.
8. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanaj AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid recerptor TRPV1. Nat Neurosci 5: 856-860, 2002.
9. Bley KR. Recent developments in transient receptor potential vanilloid receptor1 agonist-based therapies. Expert Opin Investig Drugs 13: 1445-1456, 2004.
10. Boyce S, Wyatt A, Webb JK, O'Donnell R, Mason G, Rigby M, Sirinathsinghji D, Hill RG, Rupniak NM. Selective NMDA NR2B antagonists induce antinociception without motor dysfunction: correlation with restricted localisation of NR2B subunit in dorsal horn. Neuropharmacology 38: 611-623, 1999.
11. Cason AM, Samuelsen CL, Berkley KJ. Estrous changes in vaginal nociception in a rat model of endometriosis. Horm Behav 44: 123-131, 2003.
12. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D. Impaired nocieption and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313, 2000.
13. Chandler MJ, Qin C, Zang J, Foreman RD. Differential effects of urinary bladder distension on high cervical projection neurons in primates. Brain Res 949: 97-104, 2002.
14. Chen GD, Peng HY, Tung KC, Cheng CL, Chen YJ, Liao JM, Ho YC, Pan SF, Chen MJ, Lin TB. Descending facilitation of spinal NMDA-dependent reflex potentiation from pontine tegmentum in rats. Am J Physiol Renal Physiol 293: F1115-F1122, 2007.
15. Chen GD, Peng ML, Wang PY, Lee SD, Chang HM, Pan SF, Chen MJ, Tung KC, Lai CY, Lin TB. Calcium/calmodulin-dependent kinase II mediates NO-elicited PKG activation to participate in spinal reflex potentiation in anesthetized rats. Am J Physiol Regul Integr Comp Physiol 294: R487-R493, 2008.
16. Chen KJ, Chen LW, Liao JM, Chen CH, Ho YC, Cheng CL, Lin JJ, Huang PC, Lin TB. Effects of a calcineurin inhibitor, tacrolimus (FK-506), on glutamate dependent potentiation in pelvic-urethral reflex in anesthetized rats. Neuroscience 138: 69-76, 2006.
17. Chen KJ, Peng HY, Cheng CL, Chen CH, Liao JM, Ho YC, Liou JD, Tung KC, Hsu TH, Lin TB. Acute unilateral ureter distension inhibits glutamate-dependent spinal pelvic-urethra reflex potentiation via GABAergic neurotransmission in anesthetized rats. Am J Physiol Renal Physiol 292: F1007-F1015, 2007.
18. Chuang YC, Chancellor MB, Seki S, Yoshimura N, Tyagi P, Huang L, Lavelle JP, De Groat WC, Fraser MO. Intravesical potamine sulfate and potassium chloride as a model for bladder hyperactivity. Urology 61: 664-670, 2003.
19. Cruz F, Dinis P. Resinferatoxin and botulinum toxin type A for treatment of lower urinary tract syndrome. Neurourol Urodyn 26: 920-927, 2007.
20. Cull-Candy S, Brickley S, Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11: 327-335, 2001.
21. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA. Vanilloid receptor-1 is essential for inflammatory thermal hypergesia. Nature 405: 183-187, 2000.
22. De Groat WC, Yoshimura N. Pharmacology of the lower urinary tract. Annu Rev Pharmacol Toxicol 41: 691-721, 2001.
23. Dmitrieva N, Berkley KJ. Contrasting effects of WIN 55212-2 on motility of the rat bladder and uterus. J Neurosci 22: 7147-7153, 2002.
24. Dmitrieva N, Johnson OL, Berkley KJ. Bladder inflammation and hypogastric neurectomy influence uterine motility in the rat. Neurosci Lett 313: 49-52, 2001.
25. Doyle MW, Bailey TW, Jin YH, Andresen MC. Vanilloid receptors presynaptically modulate cranial visceral afferent synaptic transmission in nucleus tractus solitarius. J Neurosci 22: 8222-8229, 2002.
26. Fagerlin J, Fraser MO, de Groat WC, Chancellor MB, Flood HD, Smith D, Jordan ML. Intravesical capsaicin for the treatment of interstitial cystitis: a pilot study. Can J Urol 6: 737-744, 1999.
27. Gilron I, Coderre TJ. Emerging drugs in neuropathic pain. Expert Opin Emerg Drugs 12: 113-126, 2007.
28. Hamlin GP, Williams MJ, Nimmo AJ, Crane LH. Hormonal variation of rat uterine contractile responsiveness to selective neurokinin receptor agonists. Biol Reprod 62: 1661-1666, 2000.
29. Hwang SJ, Burette A, Rustioni A, Valtschanoff JG. Vanilloid receptor VR1-positive primary afferents are glutamatergic and contact spinal neurons that co-express neurokinin receptor NK1 and glutamate receptors. J Neurocytol 33: 321-329, 2004.
30. Immke DC, Gavva NR. The TRPV1 receptor and nociception. Semin Cell Dev Biol 17: 582-591, 2006.
31. Jancso G, Kiraly W, Jancso-Gabor A. Pharmacologically induced selective degeneration of chemosensitive primary sensory neurons. Nature 270: 741-743, 1977.
32. Jennings EA, Vaughan CW, Roberts LA, Christie MJ. The actions of anandamide on rat superficial medullary dorsal horn neurons in vitro. J Physiol 548: 121-129, 2003.
33. Jones III RCW, Xu L, Gebhart GF. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediaters require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J Neurosci 25: 10981-10989, 2005.
34. Kiraly E, Jancso G, Hajos M. Possible morphological correlates of capsaicin desensitization. Brain Res 540: 279-282, 1991.
35. Klukovits A, Gaspar R, Santha P, Jancso G, Falkay G. Role of capsaicin-sensitive nerve fibers in uterine contractility in the rat. Biol Reprod 70: 184-190, 2004.
36. Levine JD, Alessandri-Haber N. TRP channels: targets for the relief of pain. Biochim Biophys Acta 1772: 989-1003, 2007.
37. Liao JM, Huang PC, Pan SF, Chen MJ, Tung KC, Peng HY, Shih CC, Liou YM, Chen GD, Lin TB. Spinal glutamatergic NMDA-dependent pelvic nerve-to-external urethra sphincter reflex potentiation caused by a mechanical stimulation in anesthetized rats. Am J Physiol Renal Physiol 292: F1791-F1801, 2007.
38. Liao JM, Yang CH, Cheng CL, Pan SF, Chen MJ, Huang PC, Chen GD, Tung KC, Peng HY, Lin TB. Spinal glutamatergic NMDA-dependent cyclic pelvic nerve-to-external urethra sphincter reflex potentiation in anesthetized rats. Am J Physiol Renal Physiol 293: F790-F800, 2007.
39. Lin SY, Chen GD, Liao JM, Pan SF, Chen MJ, Chen CJ, Peng HY, Ho YC, Huang PC, Lin JJ, Lin TB. Estrogen modulates the spinal NMDA-mediated pelvic nerve-to-urethra reflex plasticity in rats. Endocrinology 147: 2956-2963, 2006.
40. Lin TB. Dynamic pelvic-pudendal reflex plasticity mediated by glutamate in anesthetized rats. Neuropharmacology 44: 163-170, 2003.
41. Lin TB. Tetanization-induced pelvic to pudendal reflex plasticity in anesthetized rat. Am J Physiol Renal Physiol 287: F245-F251, 2004.
42. Liu B, Eisenach JC, Tong C. Chronic estrogen sensitizes a subset of mechanosensitive afferents innervating the utrine cervix. J Neurophysiol 93: 2167-2173, 2005.
43. Luque I, Flores E, Herrero A. Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 5794, 1994.
44. Ma W, Quirion R. Inflammatory mediators modulating the transient receptor potential vanilloid 1 receptor: therapeutic targets to treat inflammation and neuropathic pain. Expert Opin Ther Targets 11: 307-320, 2007.
45. Malykhina AP, Qin C, Greenwood-Van Meerveld B, Foreman RD, Lupu F, Akbarali HI. Hyperexcitability of convergent colon and dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol Motil 18: 936-948, 2006.
46. Marinelli S, Vaughan CW, Christie MJ, Connor M. Capsaicin activation of glutamatergic synaptic transmission in the rat locus coeruleus in vitro. J Physiol 543: 531-540, 2002.
47. McMahon SB, Morrison JFB. Two groups of spinal interneurones that respond to stimulation of the abdominal viscera of the cat. J Physiol 322: 21-34, 1982.
48. Minowa S, Ishihar S, Tsuchiya S, Horie S, Murayama T. Capsaicin-and anandamid-induced gastric acid secretion via vanilloid receptor type 1 (TRPV1) in rat brain. Brain Res 1039: 75-83, 2005.
49. Morikawa K, Kakiuchi M, Fukuoka M, Kato H, Ito Y, Gomi Y. Effects of various drugs on bladder function in conscious restrained-denervated rats placed in a rstraining cage and produced by transection of the hypogastric nerve. Jpn J Pharmacol 52: 405-411, 1990.
50. Morikawa K, Fukuoka M, Kakiuchi M, Kato H, Ito Y, Gomi Y. Detrusor hyperreflexia induced by intravesical instillation of xylene in conscious rats. Jpn J Pharmacol 52: 587-595, 1990.
51. Palazzo E, de Novellis V, Marabese I, Cuomo D, Rossi F, Berrino L, Maione S. Interaction between vanilloid and glutamate receptors in the central modulation of nociception. Eur J Pharmacol 439: 69-75, 2002.
52. Pan SF, Peng HY, Chen CC, Chen MJ, Lee SD, Cheng CL, Shyu JC, Liao JM, Chen GD, Lin TB. Nicotine-activated descending facilitation on spinal NMDA-dependent reflex potentiation from pontine tegmentum in rats. Am J Physiol Renal Physiol 294: F1195-F1204, 2008.
53. Payne CK, Mosbaugh PG, Forrest JB, Evans RJ, Whitmore KF, Antoci JP, Perez-Marrero R, Jacoby K, Diokno AC, O'Reilly KJ, Griebling TL, Vasavada SP, Yu AS, Frumkin LR. Intravesical resiniferatoxin for the treatment of interstitial cystitis: a randomized, doubleb-lind, placebo controlled trial. J Urol 173: 1590-1594, 2005.
54. Peng HY, Chang HM, Sarah Chang Y, Tung KC, Lee SD, Chou D, Lai CY, Chiu CH, Chen GD, Lin TB. Orexin-A modulates glutamatergic NMDA-dependent spinal reflex potentiation via inhibition of NR2B subunit. Am J Physiol Endocrinol Metab 295: E117-E129, 2008.
55. Peng HY, Chien YW, Lee SD, Ho YC, Chou D, Chen GD, Cheng CL, Hsu TH, Tung KC, Lin TB. Glutamate-mediated spinal reflex potentiation involves ERK 1/2 phosphorylation in anesthetized rats. Neuropharmacology 54: 686-698, 2008.
56. Peng HY, Huang PC, Liao JM, Tung KC, Lee SD, Cheng CL, Shyu JC, Lai CY, Chen GD, Lin TB. Estrous cycle variation of TRPV1-mediated cross-organ sensitization between uterus and NMDA-dependent pelvic-urethra reflex activity. Am J Physiol Endocrinol Metab In press.
57. Petralia RS, Wang YX, Wenthold RJ. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14: 6102-6120, 1994.
58. Pezzone MA, Liang R, Fraser MO. A model of neural cross-talk and irritation in the pelvis: implications for the overlap of chronic pelvic pain disorders. Gastroenterology 128: 1953-1964, 2005.
59. Pogatzki-Zahn EM, Shimizu I, Caterina M, Raja SN. Heat hyperalgesia after incision requires TRPV1 and is distinct from pure inflammatory pain. Pain 115: 296-307, 2005.
60. Prior A, Wilson K, Whorwell PJ, Faragher EB. Irritable bowel syndrome in the gynecological clinic. Survey of 798 new referrals. Dig Dis Sci 34: 1820-1824, 1989.
61. Prybylowski K, Wenthold RJ. N-methyl-D-aspartate receptors: subunit assembly and trafficking to the synapse. J Biol Chem 279: 9673-9676, 2004.
62. Qin C, Foreman RD. Viscerovisceral convergency of urinary and colorectal inputs to lumbosacral spinal neurons in the rats. Neuroreport 15: 467-471, 2004.
63. Rong W, Hillsley K, Davis JB, Hicks G, Winchester WJ, Grundy D. Jejunal afferent nerve sensitivity in wild-type and TRPV1 knockout mice. J Physiol 560: 867-881, 2004.
64. Sandner-Kiesling A, Eisenach JC. Estrogen reduces efficacy of mu- but not Kappa-opioid agonist inhibition in response to uterine cervical distension. Anesthesiology 96: 375-379, 2002.
65. Shrew RL, Papka RE, Mcneill DL. Substance P and calcitonin gene-related peptide immunoreactivity in nerves of the rat uterus: localization, colocalization and effects on uterine contractility. Peptides 12: 593-600, 1991.
66. Soliman AC, Yu JS, Coderre TJ. mGlu and NMDA receptor contributions to capsaicin-induced thermal and mechanical hypersensitivity. Neuropharmacology 48: 325-332, 2005.
67. Tohda C, Sasaki M, Konemura T, Sasamura T, Itoh M, Kuraishi Y. Axonal transport of VR1 capsaicin receptor mRNA in primary afferents and its participation in inflammation-induced increase in capsaicin sensitivity. J Neurochem 76: 1628-1635, 2001.
68. Tong C, Conklin D, Clyne BB, Stanislaus JK, Eisenach JC. Uterine cervical afferents in thoracolumbar dorsal root ganglia express transient receptor potential vanilloid type 1 channel and calcitonin gene-related peptide, but not P2X3 receptor and somatostatin. Anesthesiology 104: 651-657, 2006.
69. Torebjork HE, LaMotte RH, Robinson CJ. Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia simultaneous recordings in hymans of sensory judgments of pain and evoked responses in nociceptors with C-fibers. J Neurophysiol 51: 325-339, 1984.
70. Torebjork HE, Lundberg LE, LaMotte RH. Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 448: 765-780, 1992.
71. 71a. Traurig HH, Papka RE, Rush ME. Effects of capsaicin on reproductive function in the female rat: role of peptide-containing primary afferent nerve in innervating the uterine cervix in the neuroendocrine copulatory response. Cell Tissue Res 253: 573-581, 1988.
72. Treede RD, Meyer RA, Raja SN, Campbell JN. Peripheral and central mechanisms of cutaneous hyperalgesia. Prog Neurobiol 38: 397-421, 1992.
73. Ustinova EE, Gutkin DW, Pezzone MA. Sensitization of pelvic nerve afferents and mast cell infiltration in the urinary bladder following chronic colonic irritation is medidated by neuropeptide. Am J Physiol Renal Physiol 292: F123-F130, 2007.
74. Ustinova EE, Fraser MO, Pezzone MA. Colonic irritation in the rat sensitizes urinary bladder afferents to mechanical and chemical stimuli: an afferent origin of pelvic organ sensitization. Am J Physiol Renal Physiol 290: F478-F487, 2006.
75. Whorwell PJ, McCallum M, Creed FH, Roberts CT. Noncolonic features of irritable bowel syndrome. Gut 27: 37-40, 1986.
76. Willis WD. Role of neurotransmitters in sensitization of pain responses. Ann NY Acad Sci 933: 142-156, 2001.
77. Winnard KP, Dmitrieva N, Berkley KJ. Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve. Am J Physiol Regul Integr Comp Physiol 291: R1592-R1601, 2006.
78. Woolf CJ. Evidence for a central component of postinjury pain hypersensitivity. Nature 306: 686-688, 1983.
79. Woolf CJ. Generation of acute pain: central mechanisms. Br Med Bull 47: 523-533, 1991.
80. Woolf CJ, Thompson SW. The induction and maintainance of central sensitization is dependent on N-methyl-D-aspartatic acid receptor activation: implications for the treatment of postinjury pain hypersensitivity states. Pain 44: 293-299, 1991.
81. Woolf CJ. Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 106: 864-867, 2007.
82. Xing J, Li J. TRPV1 receptor mediates glutamatergic synaptic input to dorsolateral periaqueductal gray (dl-PAG) neurons. J Neurophysiol 97: 503-511, 2007.
83. Yan T, Liu B, Du D, Eisenach JC, Tong C. Estrogen amplifies pain response to uterine cervical distension in rats by altering transient receptor potential-1 function. Anesth Analg 104: 1246-1250, 2007.
84. Yung KK. Localization of glutamate receptors in dorsal horn of rat spinal cord. Neuroreport 9: 1639-1644, 1998.
85. Zhang X, Wu J, Lei Y, Fang L, Willis WD. Protein phosphatase modulates the phosphorylation of spinal cord NMDA receptors in rats following intradermal injection of capsaicin. Brain Res Mol Brain Res 138: 264-272, 2005.
86. Zou X, Lin Q, Willis WD. Role of protein kinase A in phosphorylation of NMDA receptor 1 subunits in dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats. Neuroscience 115: 775-786, 2002.