Mycophenolic acid mediated disruption of the intestinal epithelial tight junctions

Experimental Cell Research

Volumn 322, Issue 2, 2014, Pages 277-289

  Qasim, Muhammad ^a,b   Rahman, Hazir ^a,b   Ahmed, Raees ^c   Oellerich, Michael ^a   Asif, Abdul R ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b KOHAT UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Pakistan)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Mycophenolic acid; Myosin light chain 2; Permeability; Tight junctions

Indexed keywords

1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; DEXTRAN; F ACTIN; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; MYCOPHENOLIC ACID; MYOSIN LIGHT CHAIN; MYOSIN LIGHT CHAIN KINASE; OCCLUDIN;

APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL STRAIN CACO 2; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GASTROINTESTINAL TOXICITY; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM; MEMBRANE RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TIGHT JUNCTION;

MYCOPHENOLIC ACID; MYOSIN LIGHT CHAIN 2; PERMEABILITY; TIGHT JUNCTIONS;

ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; BLOTTING, WESTERN; CACO-2 CELLS; CARDIAC MYOSINS; CASPASE 3; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; DEXTRANS; EPITHELIAL CELLS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INTESTINES; MICROSCOPY, FLUORESCENCE; MYCOPHENOLIC ACID; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN KINASE; OCCLUDIN; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TIGHT JUNCTIONS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84896055316     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.01.021     Document Type: Article

References (68)

1. Alvarez-Hernandez X., Nichols G.M., Glass J. Caco-2 cell line: a system for studying intestinal iron transport across epithelial cell monolayers. Biochim. Biophys. Acta (BBA) - Biomembr. 1991, 1070:205-208.
2. Anderson J.M., Van Itallie C.M. Tight junctions and the molecular basis for regulation of paracellular permeability. Am. J. Physiol. 1995, 269:G467-G475.
3. Arslan H., Inci E.K., Azap O.K., Karakayali H., Torgay A., Haberal M. Etiologic agents of diarrhea in solid organ recipients. Transpl. Infect. Dis. 2007, 9:270-275.
4. Bullingham N.A.K.B., Clinical R.E. Pharmacokinetics of mycophenolate mofetil. Clin. Pharmacokinet. 1998, 34:425-455.
5. Catalioto R.M., Maggi C.A., Giuliani S. Intestinal epithelial barrier dysfunction in disease and possible therapeutical interventions. Curr. Med. Chem. 2011, 18:398-426.
6. Clayburgh D.R., Barrett T.A., Tang Y., Meddings J.B., Van Eldik L.J., Watterson D.M., Clarke L.L., Mrsny R.J., Turner J.R. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J. Clin. Invest. 2005, 115:2702-2715.
7. Clayburgh D.R., Barrett T.A., Tang Y., Meddings J.B., Van Eldik L.J., Watterson D.M., Clarke L.L., Mrsny R.J., Turner J.R. Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo. J. Clin. Invest. 2005, 115:2702-2715.
8. Clayburgh D.R., Shen L., Turner J.R. A porous defense: the leaky epithelial barrier in intestinal disease. Lab. Invest. 2004, 84:282-291.
9. Dalle I.J., Maes B.D., Geboes K.P., Lemahieu W., Geboes K. Crohn's-like changes in the colon due to mycophenolate?. Colorectal Dis. 2005, 7:27-34.
10. Davies N.M., Grinyo J., Heading R., Maes B., Meier-Kriesche H.U., Oellerich M. Gastrointestinal side effects of mycophenolic acid in renal transplant patients: a reappraisal. Nephrol. Dial. Transpl. 2007, 22:2440-2448.
11. Dodane V., Amin K.M., Merwin J.R. Effect of chitosan on epithelial permeability and structure. Int. J. Pharm. 1999, 182:21-32.
12. Duggan C., Gannon J., Walker W.A. Protective nutrients and functional foods for the gastrointestinal tract. Am. J. Clin. Nutr. 2002, 75:789-808.
13. Dunlop S.P., Hebden J., Campbell E., Naesdal J., Olbe L., Perkins A.C., Spiller R.C. Abnormal intestinal permeability in subgroups of diarrhea-predominant irritable bowel syndromes. Am. J. Gastroenterol. 2006, 101:1288-1294.
14. Farquhar M.G., Palade G.E. Junctional complexes in various epithelila. J. Cell Biol. 1963, 17:375-412.
15. Feighery L.M., Cochrane S.W., Quinn T., Baird A.W., O'Toole D., Owens S.E., O'Donoghue D., Mrsny R.J., Brayden D.J. Myosin light chain kinase inhibition: correction of increased intestinal epithelial permeability in vitro. Pharm. Res. 2008, 25:1377-1386.
16. Furuse M., Itoh M., Hirase T., Nagafuchi A., Yonemura S., Tsukita S., Tsukita S. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J. Cell Biol. 1994, 127:1617-1626.
17. Gonzalez-Mariscal L., Tapia R., Chamorro D. Crosstalk of tight junction components with signaling pathways. Biochim. Biophys. Acta 2008, 1778:729-756.
18. Guntaka S.R., Samak G., Seth A., Larusso N.F., Rao R. Epidermal growth factor protects the apical junctional complexes from hydrogen peroxide in bile duct epithelium. Lab. Invest. 2011, 91:1396-1409.
19. Helderman J.H., Goral S. Gastrointestinal complications of transplant immunosuppression. J. Am. Soc. Nephrol. 2002, 13:277-287.
20. Jain S., Suzuki T., Seth A., Samak G., Rao R. Protein kinase C ⊗ phosphorylates occludin and promotes assembly of epithelial tight junctions. Biochem. J. 2011, 437:289-299.
21. Kim H.C., Park S.B. Mycophenolate mofetil-induced ischemic colitis. Transpl. Proc. 2000, 32:1896-1897.
22. Koeneman B.A., Zhang Y., Westerhoff P., Chen Y., Crittenden J.C., Capco D.G. Toxicity and cellular responses of intestinal cells exposed to titanium dioxide. Cell Biol. Toxicol. 2010, 26:225-238.
23. Levy P., Robin H., Bertrand F., Kornprobst M., Capeau J. Butyrate-treated colonic Caco-2 cells exhibit defective integrin-mediated signaling together with increased apoptosis and differentiation. J. Cell. Physiol. 2003, 197:336-347.
24. Ma T.Y., Hoa N.T., Tran D.D., Bui V., Pedram A., Mills S., Merryfield M. Cytochalasin B modulation of Caco-2 tight junction barrier: role of myosin light chain kinase. Am. J. Physiol. Gastrointest. Liver Physiol. 2000, 279:G875-G885.
25. Ma T.Y., Nguyen D., Bui V., Nguyen H., Hoa N. Ethanol modulation of intestinal epithelial tight junction barrier. Am. J. Physiol. 1999, 276:G965-G974.
26. Madara J.L., Pappenheimer J.R. Structural basis for physiological regulation of paracellular pathways in intestinal epithelia. J. Membr. Biol. 1987, 100:149-164.
27. Maes B.D., Dalle I., Geboes K., Oellerich M., Armstrong V.W., Evenepoel P., Geypens B., Kuypers D., Shipkova M., Geboes K., Vanrenterghem Y.F. Erosive enterocolitis in mycophenolate mofetil-treated renal-transplant recipients with persistent afebrile diarrhea. Transplantation 2003, 75:665-672.
28. Malinowski M., Martus P., Lock J.F., Neuhaus P., Stockmann M. Systemic influence of immunosuppressive drugs on small and large bowel transport and barrier function. Transpl. Int. 2011, 24:184-193.
29. Marchiando A.M., Graham W.V., Turner J.R. Epithelial barriers in homeostasis and disease. Annu. Rev. Pathol. 2010, 5:119-144.
30. Matter K., Balda M.S. Signalling to and from tight junctions. Nat. Rev. Mol. Cell Biol. 2003, 4:225-236.
31. Newbold N., Riley B., Hardiner K. A review of enteric-coated mycophenolate sodium for renal transplant immunosuppression. Clin. Med.: Ther. 2009, 1:927-933.
32. Nguyen T., Park J.Y., Scudiere J.R., Montgomery E. Mycophenolic acid (cellcept and myofortic) induced injury of the upper GI tract. Am. J. Surg. Pathol. 2009, 33:1355-1363.
33. Nusrat A., Giry M., Turner J.R., Colgan S.P., Parkos C.A., Carnes D., Lemichez E., Boquet P., Madara J.L. Rho protein regulates tight junctions and perijunctional actin organization in polarized epithelia. Proc. Natl. Acad. Sci. 1995, 92:10629-10633.
34. Papadimitriou J.C., Cangro C.B., Lustberg A., Khaled A., Nogueira J., Wiland A., Ramos E., Klassen D.K., Drachenberg C.B. Histologic features of mycophenolate mofetil-related colitis: a graft-versus-host disease-like pattern. Int. J. Surg. Pathol. 2003, 11:295-302.
35. Parfitt J.R., Jayakumar S., Driman D.K. Mycophenolate mofetil-related gastrointestinal mucosal injury: variable injury patterns, including graft-versus-host disease-like changes. Am. J. Surg. Pathol. 2008, 32:1367-1372.
36. Peterson M.D., Mooseker M.S. Characterization of the enterocyte-like brush border cytoskeleton of the C2BBe clones of the human intestinal cell line, Caco-2. J. Cell Sci. 1992, 102:581-600.
37. Phatak U.P., Seo-Mayer P., Jain D., Selbst M., Husain S., Pashankar D.S. Mycophenolate mofetil-induced colitis in children. J. Clin. Gastroenterol. 2009, 43:967-969.
38. Ponticelli C., Passerini P. Gastrointestinal complications in renal transplant recipients. Transpl. Int. 2005, 18:643-650.
39. Qasim M., Rahman H., Oellerich M., Asif A. Differential proteome analysis of human embryonic kidney cell line (HEK-293) following mycophenolic acid treatment. Proteome Sci. 2011, 9:57.
40. Ranaldi G., Marigliano I., Vespignani I., Perozzi G., Sambuy Y. The effect of chitosan and other polycations on tight junction permeability in the human intestinal Caco-2 cell line(1). J. Nutr. Biochem. 2002, 13:157-167.
41. Rozen S.H., Primer3 S. on the WWW for general users and for biologist programmers. Methods Mol. Bio. 2000, 132:365-386.
42. Saitoh M., Ishikawa T., Matsushima S., Naka M., Hidaka H. Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J. Biol. Chem. 1987, 262:7796-7801.
43. Salim S.Y., Soderholm J.D. Importance of disrupted intestinal barrier in inflammatory bowel diseases. Inflamm. Bowel Dis. 2011, 17:362-381.
44. Sambuy Y., De Angelis I., Ranaldi G., Scarino M.L., Stammati A., Zucco F. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol.Toxicol. 2005, 21:1-26.
45. Sawada N., Murata M., Kikuchi K., Osanai M., Tobioka H., Kojima T., Chiba H. Tight junctions and human diseases. Med. Electron Microsc. 2003, 36:147-156.
46. Schlegel N., Burger S., Golenhofen N., Walter U., Drenckhahn D., Waschke J. The role of VASP in regulation of cAMP- and Rac 1-mediated endothelial barrier stabilization. Am. J. Physiol.: Cell Physiol. 2008, 294:C178-C188.
47. Schlegel N., Meir M., Spindler V., Germer C.T., Waschke J. Differential role of Rho GTPases in intestinal epithelial barrier regulation in vitro. J. Cell. Physiol. 2011, 226:1196-1203.
48. Schliwa M. Action of cytochalasin D on cytoskeletal networks. J. Cell Biol. 1982, 92:79-91.
49. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
50. Schneeberger E.E., Lynch R.D. The tight junction: a multifunctional complex. Am. J. Physiol.: Cell Physiol. 2004, 286:C1213-C1228.
51. Scott K.G., Meddings J.B., Kirk D.R., Lees-Miller S.P., Buret A.G. Intestinal infection with Giardia spp. reduces epithelial barrier function in a myosin light chain kinase-dependent fashion. Gastroenterology 2002, 123:1179-1190.
52. Shen L., Black E.D., Witkowski E.D., Lencer W.I., Guerriero V., Schneeberger E.E., Turner J.R. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J. Cell Sci. 2006, 119:2095-2106.
53. Shimizu M. Interaction between food substances and the intestinal epithelium. Biosci. Biotechnol. Biochem. 2010, 74:232-241.
54. Shin K., Fogg V.C., Margolis B. Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 2006, 22:207-235.
55. Shipkova M., Armstrong V.W., Oellerich M., Wieland E. Acyl glucuronide drug metabolites: toxicological and analytical implications. Ther. Drug Monit. 2003, 25:1-16.
56. Shipkova M., Armstrong V.W., Oellerich M., Wieland E. Mycophenolate mofetil in organ transplantation: focus on metabolism, safety and tolerability. Expert Opin. Drug Metab. Toxicol. 2005, 1:505-526.
57. Stassen P.M., Kallenberg C.G., Stegeman C.A. Use of mycophenolic acid in non-transplant renal diseases. Nephrol. Dial. Transpl. 2007, 22:1013-1019.
58. Steed E., Balda M.S., Matter K. Dynamics and functions of tight junctions. Trends Cell Biol. 2010, 20:142-149.
59. Stevenson B.R., Begg D.A. Concentration-dependent effects of cytochalasin D on tight junctions and actin filaments in MDCK epithelial cells. J. Cell Sci. 1994, 107:367-375.
60. Subramanian V.S., Marchant J.S., Ye D., Ma T.Y., Said H.M. Tight junction targeting and intracellular trafficking of occludin in polarized epithelial cells. Am. J. Physiol.: Cell Physiol. 2007, 293:C1717-C1726.
61. Terry S., Nie M., Matter K., Balda M.S. Rho signaling and tight junction functions. Physiology 2010, 25:16-26.
62. Turner J.R., Rill B.K., Carlson S.L., Carnes D., Kerner R., Mrsny R.J., Madara J.L. Physiological regulation of epithelial tight junctions is associated with myosin light-chain phosphorylation. Am. J. Physiol. 1997, 273:C1378-C1385.
63. + exchanger NHE3. Am. J. Physiol.: Cell Physiol. 2000, 279:C1918-C1924.
64. van Breemen R.B., Li Y. Caco-2 cell permeability assays to measure drug absorption. Expert Opin. Drug Metab. Toxicol. 2005, 1:175-185.
65. von Bonsdorff C.H., Fuller S.D., Simons K. Apical and basolateral endocytosis in Madin-Darby canine kidney (MDCK) cells grown on nitrocellulose filters. EMBO J. 1985, 4:2781-2792.
66. Wang F., Graham W.V., Wang Y., Witkowski E.D., Schwarz B.T., Turner J.R. Interferon-gamma and tumor necrosis factor-alpha synergize to induce intestinal epithelial barrier dysfunction by up-regulating myosin light chain kinase expression. Am. J. Pathol. 2005, 166:409-419.
67. Xu L.f., Xu C., Mao Z.Q., Teng X., Ma L., Sun M. Disruption of the F-actin cytoskeleton and monolayer barrier integrity induced by PAF and the protective effect of ITF on intestinal epithelium. Arch. Pharm. Res. 2011, 34:245-251.
68. Yu D., Marchiando A.M., Weber C.R., Raleigh D.R., Wang Y., Shen L., Turner J.R. MLCK-dependent exchange and actin binding region-dependent anchoring of ZO-1 regulate tight junction barrier function. Proc. Natl. Acad. Sci. USA 2010, 107:8237-8241.