Clcn5 knockout mice exhibit novel immunomodulatory effects and are more susceptible to dextran sulfate sodium-induced colitis

Journal of Immunology

Volumn 184, Issue 7, 2010, Pages 3988-3996

  Alex, Philip ^a,b   Ye, Mei ^a,c   Zachos, Nicholas C ^a   Sipes, Jennifer ^a   Nguyen, Thuan ^b   Suhodrev, Maxim ^a   Gonzales, Liberty ^b   Arora, Zubin ^a   Zhang, Ting ^a   Centola, Michael ^b   Guggino, Sandra E ^a   Li, Xuhang ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^c WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE CHANNEL; DEXTRAN SULFATE; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 6; MYELOPEROXIDASE; TUMOR NECROSIS FACTOR ALPHA; VITAMIN D; CLC 5 CHLORIDE CHANNEL; CLC-5 CHLORIDE CHANNEL; CYTOKINE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON MUCOSA; CONTROLLED STUDY; DIET; DISEASE ACTIVITY; DISEASE EXACERBATION; ENZYME ACTIVITY; HISTOPATHOLOGY; IMMUNOFLUORESCENCE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; ULCERATIVE COLITIS; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; COLITIS; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; MALE; METABOLISM; MOUSE MUTANT;

ANIMALS; BLOTTING, WESTERN; CHLORIDE CHANNELS; COLITIS; CYTOKINES; DEXTRAN SULFATE; FLUORESCENT ANTIBODY TECHNIQUE; INTERLEUKIN-17; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; TH1 CELLS; VITAMIN D;

EID: 77951635681     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901657     Document Type: Article

References (76)

1. Podolsky, D. K. 2002. Inflammatory bowel disease. N. Engl. J. Med. 347: 417-429.
2. Xavier, R. J., and D. K. Podolsky. 2007. Unravelling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434. (Pubitemid 47123518)
3. O'Shea, J. J., and P. J. Murray. 2008. Cytokine signaling modules in inflammatory responses. Immunity 28: 477-487.
4. Pizarro, T. T., and F. Cominelli. 2007. Cytokine therapy for Crohn's disease: advances in translational research. Annu. Rev. Med. 58: 433-444.
5. Elson, C. O., Y. Cong, R. Lorenz, and C. T. Weaver. 2004. New developments in experimental models of inflammatory bowel disease. Curr. Opin. Gastroenterol. 20: 360-367.
6. Alex, P., N. C. Zachos, T. Nguyen, L. Gonzales, T. E. Chen, L. S. Conklin, M. Centola, and X. Li. 2009. Distinct cytokine patterns identified from multiplex profiles of murine DSS and TNBS-induced colitis. Inflamm. Bowel Dis. 15: 341-352.
7. + lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J. Immunol. 157: 1261-1270.
8. Russell, R. K., E. R. Nimmo, and J. Satsangi. 2004. Molecular genetics of Crohn's disease. Curr. Opin. Genet. Dev. 14: 264-270.
9. Schreiber, S., P. Rosenstiel, M. Albrecht, J. Hampe, and M. Krawczak. 2005. Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat. Rev. Genet. 6: 376-388.
10. Shah, S. B., and S. B. Hanauer. 2007. Treatment of diarrhea in patients with inflammatory bowel disease: concepts and cautions. Rev. Gastroenterol. Disord. 7(Suppl 3): S3-S10.
11. Binder, H. J., G. I. Sandle, and V. M. Rajendran. 1991. Colonic fluid and electrolyte transport in health and disease. In The Large Intestine: Physiology, Pathophysiology, and Disease. S. F. Philips, J. H. Pemberton, and R. D. Shorter, eds. Raven Press, New York, p. 141-168.
12. Sandle, G. I. 1998. Salt and water absorption in the human colon: a modern appraisal. Gut 43: 294-299.
13. +-ATPase expression in human intestinal xenografts in vivo. Am. J. Physiol. Gastrointest. Liver Physiol. 286: G157-G165.
14. +-ATPase. J. Clin. Invest. 110: 1739-1747.
15. +-ATPase by interferon gamma down-regulates intestinal epithelial transport and barrier function. Gastroenterology 120: 1393-1403.
16. Amasheh, S., C. Barmeyer, C. S. Koch, S. Tavalali, J. Mankertz, H. J. Epple, M. M. Gehring, P. Florian, A. J. Kroesen, M. Zeitz, et al. 2004. Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis. Gastroenterology 126: 1711-1720. (Pubitemid 38736336)
17. Amin, M. R., J. Malakooti, R. Sandoval, P. K. Dudeja, and K. Ramaswamy. 2006. IFN-gamma and TNF-alpha regulate human NHE3 gene expression by modulating the Sp family transcription factors in human intestinal epithelial cell line C2BBe1. Am. J. Physiol. Cell Physiol. 291: C887-C896.
18. Clayburgh, D. R., M. W. Musch, M. Leitges, Y. X. Fu, and J. R. Turner. 2006. Coordinated epithelial NHE3 inhibition and barrier dysfunction are required for TNF-mediated diarrhea in vivo. J. Clin. Invest. 116: 2682-2694.
19. Sullivan, S., P. Alex, T. Dassopoulos, N. C. Zachos, C. Iacobuzio-Donahue, M. Donowitz, S. R. Brant, C. Cuffari, M. L. Harris, L. W. Datta, et al. 2009. Downregulation of sodium transporters and NHERF proteins in IBD patients and mouse colitis models: potential contributors to IBD-associated diarrhea. Inflamm. Bowel Dis. 15: 261-274.
20. Devuyst, O., and W. B. Guggino. 2002. Chloride channels in the kidney: lessons learned from knockout animals. Am. J. Physiol. Renal Physiol. 283: F1176-F1191.
21. Jentsch, T. J. 1996. Chloride channels: a molecular perspective. Curr. Opin. Neurobiol. 6: 303-310.
22. Kornak, U., D. Kasper, M. R. Bösl, E. Kaiser, M. Schweizer, A. Schulz, W. Friedrich, G. Delling, and T. J. Jentsch. 2001. Loss of the ClC-7 chloride channel leads to osteopetrosis in mice and man. Cell 104: 205-215. (Pubitemid 32174837)
23. Simon, D. B., R. S. Bindra, T. A. Mansfield, C. Nelson-Williams, E. Mendonca, R. Stone, S. Schurman, A. Nayir, H. Alpay, A. Bakkaloglu, et al. 1997. Mutations in the chloride channel gene, CLCNKB, cause Bartter's syndrome type III. Nat. Genet. 17: 171-178.
24. Steinmeyer, K., R. Klocke, C. Ortland, M. Gronemeier, H. Jockusch, S. Gründer, and T. J. Jentsch. 1991. Inactivation of muscle chloride channel by transposon insertion in myotonic mice. Nature 354: 304-308. (Pubitemid 21896882)
25. Stobrawa, S. M., T. Breiderhoff, S. Takamori, D. Engel, M. Schweizer, A. A. Zdebik, M. R. Bösl, K. Ruether, H. Jahn, A. Draguhn, et al. 2001. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of the hippocampus. Neuron 29: 185-196.
26. Scheel, O., A. A. Zdebik, S. Lourdel, and T. J. Jentsch. 2005. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436: 424-427. (Pubitemid 41059055)
27. Dent, C. E., and M. Friedman. 1964. Hypercalcuric rickets associated with renal tubular damage. Arch. Dis. Child. 39: 240-249.
28. Souza-Menezes, J., M. M. Morales, D. N. Tukaye, S. E. Guggino, and W. B. Guggino. 2007. Absence of ClC5 in knockout mice leads to glycosuria, impaired renal glucose handling and low proximal tubule GLUT2 protein expression. Cell. Physiol. Biochem. 20: 455-464.
29. Guggino, S. E. 2007. Mechanisms of disease: what can mouse models tell us about the molecular processes underlying Dent disease? Nat. Clin. Pract. Nephrol. 3: 449-455.
30. Wang, Y., H. Cai, L. Cebotaru, D. H. Hryciw, E. J. Weinman, M. Donowitz, S. E. Guggino, and W. B. Guggino. 2005. ClC-5: role in endocytosis in the proximal tubule. Am. J. Physiol. Renal Physiol. 289: F850-F862.
31. Wrong, O. M., A. G. Norden, and T. G. Feest. 1994. Dent's disease; a familial proximal renal tubular syndrome with low-molecular-weight proteinuria, hypercalciuria, nephrocalcinosis, metabolic bone disease, progressive renal failure and a marked male predominance. QJM 87: 473-493.
32. Fisher, S. E., G. C. Black, S. E. Lloyd, E. Hatchwell, O. Wrong, R. V. Thakker, and I. W. Craig. 1994. Isolation and partial characterization of a chloride channel gene which is expressed in kidney and is a candidate for Dent's disease (an X-linked hereditary nephrolithiasis). Hum. Mol. Genet. 3: 2053-2059.
33. Lloyd, S. E., S. H. Pearce, S. E. Fisher, K. Steinmeyer, B. Schwappach, S. J. Scheinman, B. Harding, A. Bolino, M. Devoto, P. Goodyer, et al. 1996. A common molecular basis for three inherited kidney stone diseases. Nature 379: 445-449. (Pubitemid 26039523)
34. Lloyd, S. E., S. H. Pearce, W. Günther, H. Kawaguchi, T. Igarashi, T. J. Jentsch, and R. V. Thakker. 1997. Idiopathic low molecular weight proteinuria associated with hypercalciuric nephrocalcinosis in Japanese children is due to mutations of the renal chloride channel (CLCN5). J. Clin. Invest. 99: 967-974.
35. Wang, S. S., O. Devuyst, P. J. Courtoy, X. T. Wang, H. Wang, Y. Wang, R. V. Thakker, S. Guggino, and W. B. Guggino. 2000. Mice lacking renal chloride channel, CLC-5, are a model for Dent's disease, a nephrolithiasis disorder associated with defective receptor-mediated endocytosis. Hum. Mol. Genet. 9: 2937-2945.
36. Cheng, G., A. Ramanathan, Z. Shao, and D. K. Agrawal. 2008. Chloride channel expression and functional diversity in the immune cells of allergic diseases. Curr. Mol. Med. 8: 401-407.
37. Cheng, G., Z. Shao, B. Chaudhari, and D. K. Agrawal. 2007. Involvement of chloride channels in TGF-beta1-induced apoptosis of human bronchial epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 293: L1339-L1347.
38. Obermeier, F., G. Kojouharoff, W. Hans, J. Schölmerich, V. Gross, and W. Falk. 1999. Interferon-gamma (IFN-gamma)- and tumour necrosis factor (TNF)-induced nitric oxide as toxic effector molecule in chronic dextran sulphate sodium (DSS)-induced colitis in mice. Clin. Exp. Immunol. 116: 238-245.
39. Chin, K. W., and K. E. Barrett. 1994. Mast cells are not essential to inflammation in murine model of colitis. Dig. Dis. Sci. 39: 513-525.
40. Li, X., T. Galli, S. Leu, J. B. Wade, E. J. Weinman, G. Leung, A. Cheong, D. Louvard, and M. Donowitz. 2001. Na+-H+ exchanger 3 (NHE3) is present in lipid rafts in the rabbit ileal brush border: a role for rafts in trafficking and rapid stimulation of NHE3. J. Physiol. 537: 537-552. (Pubitemid 33130508)
41. Alex, P., P. Szodoray, E. Arthur, L. Willis, R. Hynd, D. Flinn, and M. Centola. 2007. Influence of intraarticular corticosteroid administration on serum cytokines in rheumatoid arthritis. Clin. Rheumatol. 26: 845-848.
42. Davies, J. Q., and S. Gordon. 2005. Isolation and culture of murine macrophages. Methods Mol. Biol. 290: 91-103.
43. Borg, I., and P. J. F. Groenen. 2005. Modern Multidimensional Scaling: Theory and Applications (Springer Series in Statistics), 2nd Ed. Springer, New York.
44. Ihaka, R., and R. Gentleman. 1996. R: a language for data analysis and graphics. J. Comput. Graph. Statist. 5: 299-314.
45. Szodoray, P., P. Alex, C. M. Chappell-Woodward, T. M. Madland, N. Knowlton, I. Dozmorov, M. Zeher, J. N. Jarvis, B. Nakken, J. G. Brun, and M. Centola. 2007. Circulating cytokines in Norwegian patients with psoriatic arthritis determined by a multiplex cytokine array system. Rheumatology (Oxford) 46: 417-425. (Pubitemid 46344652)
46. Szodoray, P., P. Alex, M. V. Jonsson, N. Knowlton, I. Dozmorov, B. Nakken, N. Delaleu, R. Jonsson, and M. Centola. 2005. Distinct profiles of Sjögren's syndrome patients with ectopic salivary gland germinal centers revealed by serum cytokines and BAFF. Clin. Immunol. 117: 168-176.
47. Wright, H., P. Alex, T. Nguyen, T. Bader, A. Gurakar, A. Sebastian, L. Gonzales, G. Wallis, M. Naylor, I. Dozmorov, et al. 2005. Multiplex cytokine profiling of initial therapeutic response in patients with chronic hepatitis C virus infection. Dig. Dis. Sci. 50: 1793-1803.
48. Cebotaru, V., S. Kaul, O. Devuyst, H. Cai, L. Racusen, W. B. Guggino, and S. E. Guggino. 2005. High citrate diet delays progression of renal insufficiency in the ClC-5 knockout mouse model of Dent's disease. Kidney Int. 68: 642-652. (Pubitemid 43323119)
49. Guggino, S. E. 2009. Can we generate new hypotheses about Dent's disease from gene analysis of a mouse model? Exp. Physiol. 94: 191-196.
50. Silva, I. V., V. Cebotaru, H. Wang, X. T. Wang, S. S. Wang, G. Guo, O. Devuyst, R. V. Thakker, W. B. Guggino, and S. E. Guggino. 2003. The ClC-5 knockout mouse model of Dent's disease has renal hypercalciuria and increased bone turnover. J. Bone Miner. Res. 18: 615-623.
51. Fonseca, J. E., M. J. Santos, H. Canhão, and E. Choy. 2009. Interleukin-6 as a key player in systemic inflammation and joint destruction. Autoimmun. Rev. 8: 538-542.
52. Cantorna, M. T., C. Munsick, C. Bemiss, and B. D. Mahon. 2000. 1,25-Dihydroxycholecalciferol prevents and ameliorates symptoms of experimental murine inflammatory bowel disease. J. Nutr. 130: 2648-2652.
53. Barrett, K. E., and K. Dharmsathaphorn. 1988. Pharmacological aspects of therapy in inflammatory bowel diseases: antidiarrheal agents. J. Clin. Gastroenterol. 10: 57-63.
54. Beeken, W. L. 1975. Remediable defects in Crohn disease: a prospective study of 63 patients. Arch. Intern. Med. 135: 686-690.
55. Piwon, N., W. Günther, M. Schwake, M. R. Bösl, and T. J. Jentsch. 2000. ClC-5 Cl2-channel disruption impairs endocytosis in a mouse model for Dent's disease. Nature 408: 369-373.
56. Hara-Chikuma, M., Y. Wang, S. E. Guggino, W. B. Guggino, and A. S. Verkman. 2005. Impaired acidification in early endosomes of ClC-5 deficient proximal tubule. Biochem. Biophys. Res. Commun. 329: 941-946.
57. Christensen, E. I., O. Devuyst, G. Dom, R. Nielsen, P. Van der Smissen, P. Verroust, M. Leruth, W. B. Guggino, and P. J. Courtoy. 2003. Loss of chloride channel ClC-5 impairs endocytosis by defective trafficking of megalin and cubilin in kidney proximal tubules. Proc. Natl. Acad. Sci. USA 100: 8472-8477.
58. Donowitz, M., and X. Li. 2007. Regulatory binding partners and complexes of NHE3. Physiol. Rev. 87: 825-872.
59. Laubitz, D., C. B. Larmonier, A. Bai, M. T. Midura-Kiela, M. A. Lipko, R. D. Thurston, P. R. Kiela, and F. K. Ghishan. 2008. Colonic gene expression profile in NHE3-deficient mice: evidence for spontaneous distal colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G63-G77.
60. Zimmerman, N. P., R. A. Vongsa, M. K. Wendt, and M. B. Dwinell. 2008. Chemokines and chemokine receptors in mucosal homeostasis at the intestinal epithelial barrier in inflammatory bowel disease. Inflamm. Bowel Dis. 14: 1000-1011.
61. Keates, S., A. C. Keates, E. Mizoguchi, A. Bhan, and C. P. Kelly. 1997. Enterocytes are the primary source of the chemokine ENA-78 in normal colon and ulcerative colitis. Am. J. Physiol. 273: G75-G82.
62. Blumberg, R., and M. F. Neurath, ed. 2006. Immune Mechanisms in Inflammatory Bowel Disease (Advances in Experimental Medicine and Biology). Vol. 579. Springer, New York.
63. Schreiber, S., S. Nikolaus, and J. Hampe. 1998. Activation of nuclear factor kappa B inflammatory bowel disease. Gut 42: 477-484. (Pubitemid 28186562)
64. Mudter, J., and M. F. Neurath. 2007. Il-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm. Bowel Dis. 13: 1016-1023.
65. Neurath, M. F., S. Finotto, I. Fuss, M. Boirivant, P. R. Galle, and W. Strober. 2001. Regulation of T-cell apoptosis in inflammatory bowel disease: to die or not to die, that is the mucosal question. Trends Immunol. 22: 21-26.
66. Moschen, A. R., A. Kaser, B. Enrich, O. Ludwiczek, M. Gabriel, P. Obrist, A. M. Wolf, and H. Tilg. 2005. The RANKL/OPG system is activated in inflammatory bowel disease and relates to the state of bone loss. Gut 54: 479-487.
67. Boonla, C., C. Hunapathed, S. Bovornpadungkitti, K. Poonpirome, K. Tungsanga, P. Sampatanukul, and P. Tosukhowong. 2008. Messenger RNA expression of monocyte chemoattractant protein-1 and interleukin-6 in stone-containing kidneys. BJU Int. 101: 1170-1177. (Pubitemid 351502659)
68. Ghazali, A., V. Fuentès, C. Desaint, P. Bataille, A. Westeel, M. Brazier, L. Prin, and A. Fournier. 1997. Low bone mineral density and peripheral blood monocyte activation profile in calcium stone formers with idiopathic hypercalciuria. J. Clin. Endocrinol. Metab. 82: 32-38.
69. Dent, C. E. 1971. Rickets and osteomalacia of various origins. Birth Defects Orig. Artic. Ser. 7: 79-85.
70. Scheinman, S. J. 1998. X-linked hypercalciuric nephrolithiasis: clinical syndromes and chloride channel mutations. Kidney Int. 53: 3-17.
71. Sylvester, F. A., N. Wyzga, J. S. Hyams, and G. A. Gronowicz. 2002. Effect of Crohn's disease on bone metabolism in vitro: a role for interleukin-6. J. Bone Miner. Res. 17: 695-702.
72. Teahon, K., I. Bjarnason, M. Pearson, and A. J. Levi. 1990. Ten years' experience with an elemental diet in the management of Crohn's disease. Gut 31: 1133-1137. (Pubitemid 20343054)
73. Winitz, M., R. F. Adams, D. A. Seedman, P. N. Davis, L. G. Jayko, and J. A. Hamilton. 1970. Studies in metabolic nutrition employing chemically defined diets. II. Effects on gut microflora populations. Am. J. Clin. Nutr. 23: 546-559.
74. Moro, J. R., M. Iwata, and U. H. von Andrian. 2008. Vitamin effects on the immune system: vitamins A and D take centre stage. Nat. Rev. Immunol. 8: 685-698.
75. Froicu, M., and M. T. Cantorna. 2007. Vitamin D and the vitamin D receptor are critical for control of the innate immune response to colonic injury. BMC Immunol. 8: 5.
76. Kong, J., Z. Zhang, M. W. Musch, G. Ning, J. Sun, J. Hart, M. Bissonnette, and Y. C. Li. 2008. Novel role of the vitamin D receptor in maintaining the integrity of the intestinal mucosal barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 294: G208-G216.