Expression and function of CXCL12/CXCR4 in rat urinary bladder with cyclophosphamide-induced cystitis

American Journal of Physiology - Renal Physiology

Volumn 298, Issue 3, 2010, Pages

  Arms, Lauren ^a   Girard, Beatrice M ^a   Vizzard, Margaret A ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

AMD 3100; Bladder hyperreflexia; Chemokines; Cystometry; Urothelium

Indexed keywords

CHEMOKINE RECEPTOR CCR4; CYCLOPHOSPHAMIDE; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER CAPACITY; CONTROLLED STUDY; CYSTOMETRY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; FEMALE; IMMUNOPATHOGENESIS; INTERSTITIAL CYSTITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 77649177189     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00628.2009     Document Type: Article

References (83)

1. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci USA 100: 7947-7952, 2003.
2. Apodaca G, Balestreire E, Birder LA. The uroepithelial-associated sensory web. Kidney Int 72: 1057-1064, 2007.
3. Arms L, Vizzard MA. Distribution and function of chemokine/receptor systems in cyclophosphamide (CYP)-induced cystitis in rats (Abstract). Program No. 372.19. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009. Online.
4. Azab AK, Runnels JM, Pitsillides C, Moreau AS, Azab F, Leleu X, Jia X, Wright R, Ospina B, Carlson AL, Alt C, Burwick N, Roccaro AM, Ngo HT, Farag M, Melhem MR, Sacco A, Munshi NC, Hideshima T, Rollins BJ, Anderson KC, Kung AL, Lin CP, Ghobrial IM. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 113: 4341-4351, 2009.
5. Balabanian K, Lagane B, Infantino S, Chow KY, Harriague J, Moepps B, Arenzana-Seisdedos F, Thelen M, Bachelerie F. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem 280: 35760-35766, 2005.
6. Bhangoo S, Ren D, Miller RJ, Henry KJ, Lineswala J, Hamdouchi C, Li B, Monahan PE, Chan DM, Ripsch MS, White FA. Delayed functional expression of neuronal chemokine receptors following focal nerve demyelination in the rat: a mechanism for the development of chronic sensitization of peripheral nociceptors (Abstract). Mol Pain 3: 38, 2007.
7. Bhangoo SK, Ren D, Miller RJ, Chan DM, Ripsch MS, Weiss C, McGinnis C, White FA. CXCR4 chemokine receptor signaling mediates pain hypersensitivity in association with antiretroviral toxic neuropathy. Brain Behav Immun 21: 581-591, 2007.
8. Birder LA. Urinary bladder urothelium: molecular sensors of chemical/ thermal/mechanical stimuli. Vascul Pharmacol 45: 221-226, 2006.
9. Birder LA, de Groat WC. Mechanisms of disease: involvement of the urothelium in bladder dysfunction. Nat Clin Pract Urol 4: 46-54, 2007.
10. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5: 856-860, 2002.
11. Birder LA, Wolf-Johnston A, Buffington CA, Roppolo JR, de Groat WC, Kanai AJ. Altered inducible nitric oxide synthase expression and nitric oxide production in the bladder of cats with feline interstitial cystitis. J Urol 173: 625-629, 2005.
12. Braas KM, May V, Zvara P, Nausch B, Kliment J, Dunleavy JD, Nelson MT, Vizzard MA. Role for pituitary adenylate cyclase activating polypeptide in cystitis-induced plasticity of micturition reflexes. Am J Physiol Regul Integr Comp Physiol 290: R951-R962, 2006.
13. Cheppudira BP, Girard BM, Malley SE, Dattilio A, Schutz KC, May V, Vizzard MA. Involvement of JAK-STAT signaling/function after cyclophosphamide-induced bladder inflammation in female rats. Am J Physiol Renal Physiol 297: F1038-F1044, 2009.
14. Cheppudira BP, Girard BM, Malley SE, Schutz KC, May V, Vizzard MA. Upregulation of vascular endothelial growth factor isoform VEGF-164 and receptors (VEGFR-2, Npn-1, and Npn-2) in rats with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 295: F826-F836, 2008.
15. Chuang YC, Chancellor MB, Seki S, Yoshimura N, Tyagi P, Huang L, Lavelle JP, De Groat WC, Fraser MO. Intravesical protamine sulfate and potassium chloride as a model for bladder hyperactivity. Urology 61: 664-670, 2003.
16. Corrow KA, Vizzard MA. Phosphorylation of extracellular signal-regulated kinases in urinary bladder in rats with cyclophosphamide- induced cystitis. Am J Physiol Regul Integr Comp Physiol 293: R125-R134, 2007.
17. Dorr W. Cystometry in mice-influence of bladder filling rate and circadian variations in bladder compliance. J Urol 148: 183-187, 1992.
18. Driscoll A, Teichman JM. How do patients with interstitial cystitis present? J Urol 166: 2118-2120, 2001.
19. Erickson DR, Xie SX, Bhavanandan VP, Wheeler MA, Hurst RE, Demers LM, Kushner L, Keay SK. A comparison of multiple urine markers for interstitial cystitis. J Urol 167: 2461-2469, 2002.
20. Fitzgerald MP, Koch D, Senka J. Visceral and cutaneous sensory testing in patients with painful bladder syndrome. Neurourol Urodyn 24: 627-632, 2005.
21. Foster R, McClung C, Feldman P, Matthew R, Fitzgerald MP, White FA. Pelvic floor muscle injury-induced tactile hypernoniceptive behavior is reversed by the administration of CXCR4 antagonist, AMD3100 (Abstract). Program No. 655.6. 2009 Neuroscience Meeting Planner. Chicago, IL: Society for Neuroscience, 2009. Online.
22. Girard BM, May V, Bora SH, Fina F, Braas KM. Regulation of neurotrophic peptide expression in sympathetic neurons: quantitative analysis using radioimmunoassay and real-time quantitative polymerase chain reaction. Regul Pept 109: 89-101, 2002.
23. Gosselin RD, Dansereau MA, Pohl M, Kitabgi P, Beaudet N, Sarret P, Melik Parsadaniantz S. Chemokine network in the nervous system: a new target for pain relief. Curr Med Chem 15: 2866-2875, 2008.
24. Guerios SD, Wang ZY, Boldon K, Bushman W, Bjorling DE. Blockade of NGF and trk receptors inhibits increased peripheral mechanical sensitivity accompanying cystitis in rats. Am J Physiol Regul Integr Comp Physiol 295: R111-R122, 2008.
25. Hartmann TN, Grabovsky V, Pasvolsky R, Shulman Z, Buss EC, Spiegel A, Nagler A, Lapidot T, Thelen M, Alon R. A crosstalk between intracellular CXCR7 and CXCR4 involved in rapid CXCL12-triggered integrin activation but not in chemokine-triggered motility of human T lymphocytes and CD34+ cells. J Leukoc Biol 84: 1130-1140, 2008.
26. Hatse S, Princen K, Bridger G, De Clercq E, Schols D. Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett 527: 255-262, 2002.
27. Herrera GM, Pozo MJ, Zvara P, Petkov GV, Bond CT, Adelman JP, Nelson MT. Urinary bladder instability induced by selective suppression of the murine small conductance calcium-activated potassium (SK3) channel. J Physiol 551: 893-903, 2003.
28. Hu VY, Malley S, Dattilio A, Folsom JB, Zvara P, Vizzard MA. COX-2 and prostanoid expression in micturition pathways after cyclophosphamide- induced cystitis in the rat. Am J Physiol Regul Integr Comp Physiol 284: R574-R585, 2003.
29. Hu VY, Zvara P, Dattilio A, Redman TL, Allen SJ, Dawbarn D, Stroemer RP, Vizzard MA. Decrease in bladder overactivity with REN1820 in rats with cyclophosphamide induced cystitis. J Urol 173: 1016-1021, 2005.
30. Hurst RE, Moldwin RM, Mulholland SG. Bladder defense molecules, urothelial differentiation, urinary biomarkers, and interstitial cystitis. Urology 69: 17-23, 2007.
31. Jennings L, Vizzard MA. Cyclophosphamide-induced inflammation of the urinary bladder alters electrical properties of small diameter afferent neurons from dorsal root ganglia (Abstracat). FASEB J 13: A57, 1999.
32. Johansson S, Ogawa K, Fall M. Interstitial cystitis. In: The Pathology of Interstitial Cystitis, edited by Sant GR. Philadelphia, PA: Lippincott-Raven, 1997, p. 143-152.
33. Jung H, Bhangoo S, Banisadr G, Freitag C, Ren D, White FA, Miller RJ. Visualization of chemokine receptor activation in transgenic mice reveals peripheral activation of CCR2 receptors in states of neuropathic pain. J Neurosci 29: 8051-8062, 2009.
34. Jung H, Toth PT, White FA, Miller RJ. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurochem 104: 254-263, 2008.
35. Kajiyama H, Shibata K, Terauchi M, Ino K, Nawa A, Kikkawa F. Involvement of SDF-1alpha/CXCR4 axis in the enhanced peritoneal metastasis of epithelial ovarian carcinoma. Int J Cancer 122: 91-99, 2008.
36. Kalatskaya I, Berchiche YA, Gravel S, Limberg BJ, Rosenbaum JS, Heveker N. AMD3100 is a CXCR7 ligand with allosteric agonist properties. Mol Pharmacol 75: 1240-1247, 2009.
37. Klinger MB, Dattilio A, Vizzard MA. Expression of cyclooxygenase-2 in urinary bladder in rats with cyclophosphamide-induced cystitis. Am J Physiol Regul Integr Comp Physiol 293: R677-R685, 2007.
38. Klinger MB, Girard B, Vizzard MA. p75NTR expression in rat urinary bladder sensory neurons and spinal cord with cyclophosphamide-induced cystitis. J Comp Neurol 507: 1379-1392, 2008.
39. Klinger MB, Vizzard MA. Role of p75NTR in female rat urinary bladder with cyclophosphamide-induced cystitis. Am J Physiol Renal Physiol 295: F1778-F1789, 2008.
40. Lamale LM, Lutgendorf SK, Zimmerman MB, Kreder KJ. Interleukin-6, histamine, and methylhistamine as diagnostic markers for interstitial cystitis. Urology 68: 702-706, 2006.
41. Lindia JA, McGowan E, Jochnowitz N, Abbadie C. Induction of CX3CL1 expression in astrocytes and CX3CR1 in microglia in the spinal cord of a rat model of neuropathic pain. J Pain 6: 434-438, 2005.
42. Luker K, Gupta M, Luker G. Bioluminescent CXCL12 fusion protein for cellular studies of CXCR4 and CXCR7. Biotechniques 47: 625-632, 2009.
43. Malley SE, Vizzard MA. Changes in urinary bladder cytokine mRNA and protein after cyclophosphamide-induced cystitis. Physiol Genomics 9: 5-13, 2002.
44. Matthys P, Hatse S, Vermeire K, Wuyts A, Bridger G, Henson GW, De Clercq E, Billiau A, Schols D. AMD3100, a potent and specific antagonist of the stromal cell-derived factor-1 chemokine receptor CXCR4, inhibits autoimmune joint inflammation in IFN-gamma receptordeficient mice. J Immunol 167: 4686-4692, 2001.
45. Mikami S, Nakase H, Yamamoto S, Takeda Y, Yoshino T, Kasahara K, Ueno S, Uza N, Oishi S, Fuji N, Nagasawa T, Chiba T. Blockade of CXCL12/CXCR4 axis ameliorates murine experimental colitis. J Pharmacol Exp Ther 327: 383-392, 2008.
46. Milligan ED, Zapata V, Chacur M, Schoeniger D, Biedenkapp J, O'Connor KA, Verge GM, Chapman G, Green P, Foster AC, Naeve GS, Maier SF, Watkins LR. Evidence that exogenous and endogenous fractalkine can induce spinal nociceptive facilitation in rats. Eur J Neurosci 20: 2294-2302, 2004.
47. Nazif O, Teichman JM, Gebhart GF. Neural upregulation in interstitial cystitis. Urology 69: 24-33, 2007.
48. Oh SB, Endoh T, Simen AA, Ren D, Miller RJ. Regulation of calcium currents by chemokines and their receptors. J Neuroimmunol 123: 66-75, 2002.
49. Oh SB, Tran PB, Gillard SE, Hurley RW, Hammond DL, Miller RJ. Chemokines and glycoprotein120 produce pain hypersensitivity by directly exciting primary nociceptive neurons. J Neurosci 21: 5027-5035, 2001.
50. Parsons CL. The role of the urinary epithelium in the pathogenesis of interstitial cystitis/prostatitis/urethritis. Urology 69: 9-16, 2007.
51. Petrone R, Agha A, Roy J, Hurst R. Urodynamic findings in patients with interstitial cystitis (Abstract). J Urol 153: 290A, 1995.
52. Qin X, Wan Y, Wang X. CCL2 and CXCL1 trigger calcitonin generelated peptide release by exciting primary nociceptive neurons. J Neurosci Res 82: 51-62, 2005.
53. Rutkowski MD, DeLeo JA. The Role of Cytokines in the Initiation and Maintenance of Chronic Pain. Drug News Perspect 15: 626-632, 2002.
54. Sakthivel SK, Singh UP, Singh S, Taub DD, Novakovic KR, Lillard JW Jr. CXCL10 blockade protects mice from cyclophosphamide-induced cystitis (Abstract). J Immune Based Ther Vaccines 6: 6, 2008.
55. Sant GR, Hanno PM. Interstitial cystitis: current issues and controversies in diagnosis. Urology 57: 82-88, 2001.
56. Sant GR, Kempuraj D, Marchand JE, Theoharides TC. The mast cell in interstitial cystitis: role in pathophysiology and pathogenesis. Urology 69: 34-40, 2007.
57. Savarin-Vuaillat C, Ransohoff RM. Chemokines and chemokine receptors in neurological disease: raise, retain, or reduce? Neurotherapeutics 4: 590-601, 2007.
58. Sengupta S, Schiff R, Katzenellenbogen BS. Post-transcriptional regulation of chemokine receptor CXCR4 by estrogen in HER2 overexpressing, estrogen receptor-positive breast cancer cells. Breast Cancer Res Treat 117: 243-251, 2009.
59. Studeny S, Cheppudira BP, Meyers S, Balestreire EM, Apodaca G, Birder LA, Braas KM, Waschek JA, May V, Vizzard MA. Urinary Bladder Function and Somatic Sensitivity in Vasoactive Intestinal Polypeptide (VIP)(-/-) Mice. J Mol Neurosci 36: 175-187, 2008.
60. Sun JH, Yang B, Donnelly DF, Ma C, LaMotte RH. MCP-1 enhances excitability of nociceptive neurons in chronically compressed dorsal root ganglia. J Neurophysiol 96: 2189-2199, 2006.
61. Sun Y, Chai TC. Augmented extracellular ATP signaling in bladder urothelial cells from patients with interstitial cystitis. Am J Physiol Cell Physiol 290: C27-C34, 2006.
62. Sun Y, Chai TC. Up-regulation of P2X3 receptor during stretch of bladder urothelial cells from patients with interstitial cystitis. J Urol 171: 448-452, 2004.
63. Sun Y, Keay S, De Deyne PG, Chai TC. Augmented stretch activated adenosine triphosphate release from bladder uroepithelial cells in patients with interstitial cystitis. J Urol 166: 1951-1956, 2001.
64. Sun Y, Keay S, Lehrfeld TJ, Chai TC. Changes in adenosine triphosphate-stimulated ATP release suggest association between cytokine and purinergic signaling in bladder urothelial cells. Urology 74: 1163-1168, 2009.
65. Tanaka T, Minami M, Nakagawa T, Satoh M. Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: possible involvement in the development of neuropathic pain. Neurosci Res 48: 463-469, 2004.
66. Vera PL, Iczkowski KA, Wang X, Meyer-Siegler KL. Cyclophosphamide-induced cystitis increases bladder CXCR4 expression and CXCR4-macrophage migration inhibitory factor association. PLoS ONE 3: e3898, 2008.
67. Verge GM, Milligan ED, Maier SF, Watkins LR, Naeve GS, Foster AC. Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur J Neurosci 20: 1150-1160, 2004.
68. Vizzard MA. Alterations in neuropeptide expression in lumbosacral bladder pathways following chronic cystitis. J Chem Neuroanat 21: 125-138, 2001.
69. Vizzard MA. Alterations in spinal cord Fos protein expression induced by bladder stimulation following cystitis. Am J Physiol Regul Integr Comp Physiol 278: R1027-R1039, 2000.
70. Vizzard MA. Changes in urinary bladder neurotrophic factor mRNA and NGF protein following urinary bladder dysfunction. Exp Neurol 161: 273-284, 2000.
71. Vizzard MA. Up-regulation of pituitary adenylate cyclase-activating polypeptide in urinary bladder pathways after chronic cystitis. J Comp Neurol 420: 335-348, 2000.
72. Vizzard MA, Boyle MM. Increased expression of growth-associated protein (GAP-43) in lower urinary tract pathways following cyclophosphamide (CYP)-induced cystitis. Brain Res 844: 174-187, 1999.
73. White FA, Jung H, Miller RJ. Chemokines and the pathophysiology of neuropathic pain. Proc Natl Acad Sci USA 104: 20151-20158, 2007.
74. White FA, Sun J, Waters SM, Ma C, Ren D, Ripsch M, Steflik J, Cortright DN, Lamotte RH, Miller RJ. Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci USA 102: 14092-14097, 2005.
75. Wu XR, Kong XP, Pellicer A, Kreibich G, Sun TT. Uroplakins in urothelial biology, function, and disease. Kidney Int 75: 1153-1165, 2009.
76. Yoshimura N, Bennett NE, Hayashi Y, Ogawa T, Nishizawa O, Chancellor MB, de Groat WC, Seki S. Bladder overactivity and hyperexcitability of bladder afferent neurons after intrathecal delivery of nerve growth factor in rats. J Neurosci 26: 10847-10855, 2006.
77. Yoshimura N, de Groat WC. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 19: 4644-4653, 1999.
78. Yuridullah R, Corrow KA, Malley SE, Vizzard MA. Expression of fractalkine and fractalkine receptor in urinary bladder after cyclophosphamide (CYP)-induced cystitis. Auton Neurosci 126-127: 380-389, 2006.
79. Zabel BA, Wang Y, Lewen S, Berahovich RD, Penfold ME, Zhang P, Powers J, Summers BC, Miao Z, Zhao B, Jalili A, Janowska-Wieczorek A, Jaen JC, Schall TJ. Elucidation of CXCR7-mediated signaling events and inhibition of CXCR4-mediated tumor cell transendothelial migration by CXCR7 ligands. J Immunol 183: 3204-3211, 2009.
80. Zhang N, Inan S, Cowan A, Sun R, Wang JM, Rogers TJ, Caterina M, Oppenheim JJ. A proinflammatory chemokine, CCL3, sensitizes the heat- and capsaicin-gated ion channel TRPV1. Proc Natl Acad Sci USA 102: 4536-4541, 2005.
81. Zhang Z, Zhong W, Hall MJ, Kurre P, Spencer D, Skinner A, O'Neill S, Xia Z, Rosenbaum JT. CXCR4 but not CXCR7 is mainly implicated in ocular leukocyte trafficking during ovalbumin-induced acute uveitis. Exp Eye Res 89: 522-531, 2009.
82. Zvara P, Vizzard MA. Exogenous overexpression of nerve growth factor in the urinary bladder produces bladder overactivity and altered micturition circuitry in the lumbosacral spinal cord (Abstract). BMC Physiol 7: 9, 2007.
83. Zvarova K, Vizzard MA. Changes in galanin immunoreactivity in rat micturition reflex pathways after cyclophosphamide-induced cystitis. Cell Tissue Res 324: 213-224, 2006.