Cystitis increases colorectal afferent sensitivity in the mouse

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 297, Issue 6, 2009, Pages

  Brumovsky, Pablo Rodolfo ^a   Feng, Bin ^a   Xu, Linjing ^b   McCarthy, Carly Jane ^a   Gebhart, G F ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

Bladder; Colon; Inflammatory soup; Pelvic nerve; Sensitization

Indexed keywords

CYCLOPHOSPHAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; COLON; CONTROLLED STUDY; CYSTITIS; HISTOLOGY; INFLAMMATION; MALE; MOUSE; MUSCLE SPINDLE AFFERENT NERVE; NONHUMAN; PELVIS; PRIORITY JOURNAL; RECTUM; SENSITIZATION; SENSORY NERVE; SENSORY NERVE CONDUCTION;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; COLON; CYCLOPHOSPHAMIDE; CYSTITIS; DISEASE MODELS, ANIMAL; EDEMA; HYDROGEN-ION CONCENTRATION; HYPERSENSITIVITY; INFLAMMATION MEDIATORS; MALE; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, INBRED C57BL; RECTUM; TIME FACTORS; URINARY BLADDER;

EID: 72749111394     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00329.2009     Document Type: Article

References (66)

1. Ahluwalia A, Maggi CA, Santicioli P, Lecci A, Giuliani S. Characterization of the capsaicin-sensitive component of cyclophosphamide- induced inflammation in the rat urinary bladder. Br J Pharmacol 111: 1017-1022, 1994. (Pubitemid 24148764)
2. 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. (Pubitemid 27193952)
3. Anton E. Delayed toxicity of cyclophosphamide on the bladder of DBA/2 and C57BL/6 female mouse. Int J Exp Pathol 83: 47-53, 2002. (Pubitemid 34638946)
4. Applebaum AE, Vance WH, Coggeshall RE. Segmental localization of sensory cells that innervate the bladder. J Comp Neurol 192: 203-209, 1980.
5. Arendt-Nielsen L, Schipper KP, Dimcevski G, Sumikura H, Krarup AL, Giamberardino MA, Drewes AM. Viscero-somatic reflexes in referred pain areas evoked by capsaicin stimulation of the human gut. Eur J Pain 12: 544-551, 2008. (Pubitemid 351626941)
6. Batista CK, Brito GA, Souza ML, Leitao BT, Cunha FQ, Ribeiro RA. A model of hemorrhagic cystitis induced with acrolein in mice. Braz J Med Biol Res 39: 1475-1481, 2006.
7. Berkley KJ. A life of pelvic pain. Physiol Behav 86: 272-280, 2005.
8. Bielefeldt K, Lamb K, Gebhart GF. Convergence of sensory pathways in the development of somatic and visceral hypersensitivity. Am J Physiol Gastrointest Liver Physiol 291: G658-G665, 2006. (Pubitemid 44511682)
9. Bjorling DE, Elkahwaji JE, Bushman W, Janda LM, Boldon K, Hopkins WJ, Wang ZY. Acute acrolein-induced cystitis in mice. BJU Int 99: 1523-1529, 2007.
10. Bon K, Lichtensteiger CA, Wilson SG, Mogil JS. Characterization of cyclophosphamide cystitis, a model of visceral and referred pain, in the mouse: species and strain differences. J Urol 170: 1008-1012, 2003. (Pubitemid 36999622)
11. Boucher M, Meen M, Codron JP, Coudore F, Kemeny JL, Eschalier A. Cyclophosphamide-induced cystitis in freely-moving conscious rats: behavioral approach to a new model of visceral pain. J Urol 164: 203-208, 2000. (Pubitemid 30434301)
12. Brierley SM, Jones RC III, Gebhart GF, Blackshaw LA. Splanchnic and pelvic mechanosensory afferents signal different qualities of colonic stimuli in mice. Gastroenterology 127: 166-178, 2004.
13. Brumovsky P, Gebhart GF. Visceral organ cross-sensitization - an integrated perspective. Auton Neurosci (August 11, 2009). doi:10.1016/j.autneu. 2009.07.006.
14. Brumovsky P, Shi TS, Landry M, Villar MJ, Hokfelt T. Neuropeptide tyrosine and pain. Trends Pharmacol Sci 28: 93-102, 2007.
15. Cervero F. Neurophysiology of gastrointestinal pain. Baillieres Clin Gastroenterol 2: 183-199, 1988.
16. Christianson JA, Liang R, Ustinova EE, Davis BM, Fraser MO, Pezzone MA. Convergence of bladder and colon sensory innervation occurs at the primary afferent level. Pain 128: 235-243, 2007. (Pubitemid 46367418)
17. Cox PJ. Cyclophosphamide cystitis - identification of acrolein as the causative agent. Biochem Pharmacol 28: 2045-2049, 1979.
18. Dechant KL, Brogden RN, Pilkington T, Faulds D. Ifosfamide/mesna. A review of its antineoplastic activity, pharmacokinetic properties and therapeutic efficacy in cancer. Drugs 42: 428-467, 1991. (Pubitemid 21920771)
19. Foreman RD. Neurological mechanisms of chest pain and cardiac disease. Cleve Clin J Med 74, Suppl 1: S30-S33, 2007.
20. Fraiser L, Kehrer JP. Murine strain differences in metabolism and bladder toxicity of cyclophosphamide. Toxicology 75: 257-272, 1992.
21. Fraiser LH, Kanekal S, Kehrer JP. Cyclophosphamide toxicity. Characterising and avoiding the problem. Drugs 42: 781-795, 1991. (Pubitemid 21920784)
22. Francis CY, Duffy JN, Whorwell PJ, Morris J. High prevalence of irritable bowel syndrome in patients attending urological outpatient departments. Dig Dis Sci 42: 404-407, 1997. (Pubitemid 27112990)
23. Francis CY, Whorwell PJ. The irritable bowel syndrome. Postgrad Med J 73: 1-7, 1997.
24. Gebhart GF, Ness TJ. Central mechanisms of visceral pain. Can J Physiol Pharmacol 69: 627-634, 1991.
25. Giamberardino MA, Affaitati G, Costantini R. Chapter 24. Referred pain from internal organs. Handb Clin Neurol 81: 343-361, 2006.
26. Holzer P. Taste Receptors in the Gastrointestinal Tract. V. Acid sensing in the gastrointestinal tract. Am J Physiol Gastrointest Liver Physiol 292: G699-G705, 2007. (Pubitemid 46440373)
27. Hubscher CH, Kaddumi EG, Johnson RD. Brain stem convergence of pelvic viscerosomatic inputs via spinal and vagal afferents. Neuroreport 15: 1299-1302, 2004.
28. Jeong MS, Kang JH. Acrolein, the toxic endogenous aldehyde, induces neurofilament-L aggregation. BMB Rep 41: 635-639, 2008.
29. Jones RC III, Xu L, Gebhart GF. The mechanosensitivity of mouse colon afferent fibers and their sensitization by inflammatory mediators require transient receptor potential vanilloid 1 and acid-sensing ion channel 3. J Neurosci 25: 10981-10989, 2005. (Pubitemid 41692628)
30. Kanekal S, Fraiser L, Kehrer JP. Pharmacokinetics, metabolic activation, and lung toxicity of cyclophosphamide in C57/B16 and ICR mice. Toxicol Appl Pharmacol 114: 1-8, 1992.
31. Keast JR, de Groat WC. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J Comp Neurol 319: 615-623, 1992.
32. Korkmaz A, Topal T, Oter S. Pathophysiological aspects of cyclophosphamide and ifosfamide induced hemorrhagic cystitis; implication of reactive oxygen and nitrogen species as well as PARP activation. Cell Biol Toxicol 23: 303-312, 2007. (Pubitemid 46919119)
33. Krawisz JE, Sharon P, Stenson WF. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology 87: 1344-1350, 1984. (Pubitemid 15201434)
34. Kress M, Waldmann R. Acid sensing ionic channels. Curr Top Membranes 57: 241-276, 2006.
35. Lamb K, Zhong F, Gebhart GF, Bielefeldt K. Experimental colitis in mice and sensitization of converging visceral and somatic afferent pathways. Am J Physiol Gastrointest Liver Physiol 290: G451-G457, 2006.
36. Lanteri-Minet M, Bon K, de PJ, Michiels JF, Menetrey D. Cyclophosphamide cystitis as a model of visceral pain in rats: model elaboration and spinal structures involved as revealed by the expression of c-Fos and Krox-24 proteins. Exp Brain Res 105: 220-232, 1995.
37. Maggi CA, Lecci A, Santicioli P, Del BE, Giuliani S. Cyclophosphamide cystitis in rats: involvement of capsaicin-sensitive primary afferents. J Auton Nerv Syst 38: 201-208, 1992.
38. Malykhina AP. Neural mechanisms of pelvic organ cross-sensitization. Neuroscience 149: 660-672, 2007.
39. + currents in bladder sensory neurons. Neuroreport 15: 2601-2605, 2004.
40. Malykhina AP, Qin C, Greenwood-Van MB, Foreman RD, Lupu F, Akbarali HI. Hyperexcitability of convergent colon and bladder dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol Motil 18: 936-948, 2006. (Pubitemid 44358864)
41. Matheis A, Martens U, Kruse J, Enck P. Irritable bowel syndrome and chronic pelvic pain: a singular or two different clinical syndrome? World J Gastroenterol 13: 3446-3455, 2007. (Pubitemid 47162018)
42. Meyer RA, Ringkamp M. A role for uninjured afferents in neuropathic pain. Sheng Li Xue Bao 60: 605-609, 2008.
43. Morrison TC, Dmitrieva N, Winnard KP, Berkley KJ. Opposing viscerovisceral effects of surgically induced endometriosis and a control abdominal surgery on the rat bladder. Fertil Steril 86: 1067-1073, 2006. (Pubitemid 44427813)
44. Ness TJ, Gebhart GF. Characterization of neurons responsive to noxious colorectal distension in the T13-L2 spinal cord of the rat. J Neurophysiol 60: 1419-1438, 1988.
45. Ness TJ, Gebhart GF. Visceral pain: a review of experimental studies. Pain 41: 167-234, 1990.
46. Neuhuber WL, Appelt M, Polak JM, Baier-Kustermann W, Abelli L, Ferri GL. Rectospinal neurons: cell bodies, pathways, immunocytochemistry and ultrastructure. Neuroscience 56: 367-378, 1993. (Pubitemid 23274756)
47. Noronha R, Akbarali H, Malykhina A, Foreman RD, Greenwood-Van MB. Changes in urinary bladder smooth muscle function in response to colonic inflammation. Am J Physiol Renal Physiol 293: F1461-F1467, 2007. (Pubitemid 350085981)
48. Peng HY, Chen GD, Tung KC, Lai CY, Hsien MC, Chiu CH, Lu HT, Liao JM, Lee SD, Lin TB. Colon mustard oil instillation induced cross-organ reflex sensitization on the pelvic-urethra reflex activity in rats. Pain 142: 75-88, 2009.
49. 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.
50. Qiao LY, Grider JR. Up-regulation of calcitonin gene-related peptide and receptor tyrosine kinase TrkB in rat bladder afferent neurons following TNBS colitis. Exp Neurol 204: 667-679, 2007.
51. Qin C, Foreman RD. Viscerovisceral convergence of urinary bladder and colorectal inputs to lumbosacral spinal neurons in rats. Neuroreport 15: 467-471, 2004. (Pubitemid 38328142)
52. Qin C, Malykhina AP, Akbarali HI, Foreman RD. Cross-organ sensitization of lumbosacral spinal neurons receiving urinary bladder input in rats with inflamed colon. Gastroenterology 129: 1967-1978, 2005.
53. Rouzade-Dominguez ML, Miselis R, Valentino RJ. Central representation of bladder and colon revealed by dual transsynaptic tracing in the rat: substrates for pelvic visceral coordination. Eur J Neurosci 18: 3311-3324, 2003. (Pubitemid 38031056)
54. Rouzade-Dominguez ML, Pernar L, Beck S, Valentino RJ. Convergent responses of Barrington's nucleus neurons to pelvic visceral stimuli in the rat: a juxtacellular labelling study. Eur J Neurosci 18: 3325-3334, 2003. (Pubitemid 38031057)
55. Rudick CN, Chen MC, Mongiu AK, Klumpp DJ. Organ cross talk modulates pelvic pain. Am J Physiol Regul Integr Comp Physiol 293: R1191-R1198, 2007.
56. Suckow SK, Caudle RM. Identification and immunohistochemical characterization of colospinal afferent neurons in the rat. Neuroscience 153: 803-813, 2008.
57. 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 cross-sensitization. Am J Physiol Renal Physiol 290: F1478-F1487, 2006.
58. Ustinova EE, Gutkin DW, Pezzone MA. Sensitization of pelvic nerve afferents and mast cell infiltration in the urinary bladder following chronic colonic irritation is mediated by neuropeptides. Am J Physiol Renal Physiol 292: F123-F130, 2007.
59. Vilensky JA, Bell DR, Gilman S. "On the physiology of micturition" by Denny-Brown and Robertson: a classic paper revisited. Urology 64: 182-186, 2004. (Pubitemid 38887610)
60. Wang ZY, Wang P, Merriam FV, Bjorling DE. Lack of TRPV1 inhibits cystitis-induced increased mechanical sensitivity in mice. Pain 139: 158-167, 2008.
61. Wemmie JA, Price MP, Welsh MJ. Acid-sensing ion channels: advances, questions and therapeutic opportunities. Trends Neurosci 29: 578-586, 2006.
62. Whorwell PJ, McCallum M, Creed FH, Roberts CT. Non-colonic features of irritable bowel syndrome. Gut 27: 37-40, 1986. (Pubitemid 16134473)
63. Willis WD Jr. Dorsal root potentials and dorsal root reflexes: a doubleedged sword. Exp Brain Res 124: 395-421, 1999.
64. 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. (Pubitemid 44904124)
65. Woolf CJ. Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology 106: 864-867, 2007.
66. Xu L, Gebhart GF. Characterization of mouse lumbar splanchnic and pelvic nerve urinary bladder mechanosensory afferents. J Neurophysiol 99: 244-253, 2008.