Myofibroblast keratinocyte growth factor reduces tight junctional integrity and increases claudin-2 levels in polarized Caco-2 cells

Growth Factors

Volumn 30, Issue 5, 2012, Pages 320-332

  Kim, Tae Il ^a   Poulin, Emily J ^b   Blask, Elliot ^a   Bukhalid, Raghida ^c   Whitehead, Robert H ^a   Franklin, Jeffrey L ^b   Coffey, Robert J ^a,b,c,d,e  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MERRIMACK PHARMACEUTICALS   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

Amphiregulin; Claudin 2; Keratinocyte growth factor; Pericryptal myofibroblasts; Tight junction

Indexed keywords

AMPHIREGULIN; CLAUDIN 2; EPIDERMAL GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR;

ARTICLE; CELL CULTURE; CELL STRAIN CACO 2; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENTERITIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MYOFIBROBLAST; PARACRINE SIGNALING; PRIORITY JOURNAL; RECEPTOR UPREGULATION; TIGHT JUNCTION;

CACO-2 CELLS; CELL COMMUNICATION; CELL LINE, TUMOR; CELL MEMBRANE PERMEABILITY; CELL PROLIFERATION; CLAUDIN-2; CULTURE MEDIA, CONDITIONED; ELECTRIC IMPEDANCE; FIBROBLAST GROWTH FACTOR 7; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTESTINAL MUCOSA; LIGANDS; MYOFIBROBLASTS; RECEPTOR, EPIDERMAL GROWTH FACTOR; TIGHT JUNCTIONS;

EID: 84867093123     PISSN: 08977194     EISSN: 10292292     Source Type: Journal    
DOI: 10.3109/08977194.2012.717076     Document Type: Article

References (77)

1. Amasheh S, Meiri N, Gitter AH, Schoneberg T, Mankertz J, Schulzke JD, Fromm M. 2002. Claudin-2 expression inducescation-selective channels in tight junctions of epithelial cells. J Cell Sci 115:4969-4976.
2. Amasheh M, Fromm A, Krug SM, Amasheh S, Andres S, Zeitz M, Fromm M, Schulzke JD. 2010. TNFa-induced and berberineantagonizedtight junction barrier impairment via tyrosinekinase, Akt and NFkB signaling. J Cell Sci 123:4145-4155.
3. Anderson JM. 2001. Molecular structure of tight junctions and theirrole in epithelial transport. News Physiol Sci 16:126-130.
4. Angelow S, Ahlstrom R, Yu AS. 2008. Biology of claudins. Am JPhysiol Renal Physiol 295:F867-F876.
5. Bajaj-Elliott M, Breese E, Poulsom R, Fairclough PD, MacDonald TT. 1997. Keratinocyte growth factor in inflammatorybowel disease. Increased mRNA transcripts in ulcerativecolitis compared with Crohn's disease in biopsies and isolatedmucosal myofibroblasts. Am J Pathol 151:1469-1476.
6. Bajaj-Elliott M, Pender SL, Poulsom R, Macdonald TT. 1998a. Upregulation of keratinocyte growth factor during T-cellimmunity in the gut mucosa. Ann NY Acad Sci 859:184-187.
7. Bajaj-Elliott M, Poulsom R, Pender SL, Wathen NC, MacDonald TT. 1998b. Interactions between stromalcell-derived keratinocyte growth factor and epithelial transforminggrowth factor in immune-mediated crypt cell hyperplasia. J Clin Invest 102:1473-1480.
8. Balda MS, Matter K. 2009. Tight junctions and the regulation ofgene expression. Biochim Biophys Acta 1788:761-767.
9. Bhowmick NA, Neilson EG, Moses HL. 2004. Stromal fibroblastsin cancer initiation and progression. Nature 432:332-337.
10. Boismenu R, Havran WL. 1994. Modulation of epithelial cellgrowth by intraepithelial gamma delta T cells. Science 266:1253-1255.
11. Brauchle M, Angermeyer K, Hubner G, Werner S. 1994. Largeinduction of keratinocyte growth factor expression by serumgrowth factors and pro-inflammatory cytokines in culturedfibroblasts. Oncogene 9:3199-3204.
12. Brauchle M, Madlener M, Wagner AD, Angermeyer K, Lauer U, Hofschneider PH, Gregor M, Werner S. 1996. Keratinocytegrowth factor is highly overexpressed in inflammatory boweldisease. Am J Pathol 149:521-529.
13. Buchert M, Papin M, Bonnans C, Darido C, Raye WS, Garambois V, Pelegrin A, Bourgaux JF, Pannequin J, Joubert D, Hollande F. 2010. Symplekin promotes tumorigenicityby up-regulating claudin-2 expression. Proc Natl Acad SciUSA 107:2628-2633.
14. Bü cker R, SchumannM, Amasheh S, Schulzke J-D. 2010. Claudinsin intestinal function and disease. Current Topics in Membranes65:195-227.
15. Chantret I, Barbat A, Dussaulx E, Brattain MG, Zweibaum A. 1988. Epithelial polarity, villin expression, and enterocyticdifferentiation of cultured human colon carcinoma cells: a surveyof twenty cell lines. Cancer Res 48:1936-1942.
16. Chedid M, Rubin JS, Csaky KG, Aaronson SA. 1994. Regulation ofkeratinocyte growth factor gene expression by interleukin 1. J Biol Chem 269:10753-10757.
17. Chen Y, Chou K, Fuchs E, Havran WL, Boismenu R. 2002. Protection of the intestinal mucosa by intraepithelial gammadelta T cells. Proc Natl Acad Sci USA 99:14338-14343.
18. Chiba H, Osanai M, Murata M, Kojima T, Sawada N. 2008. Transmembrane proteins of tight junctions. Biochim BiophysActa 1778:588-600.
19. Colegio OR, Van Itallie C, Rahner C, Anderson JM. 2003. Claudinextracellular domains determine paracellular charge selectivityand resistance but not tight junction fibril architecture. Am JPhysiol Cell Physiol 284:C1346-C1354.
20. Cutler NS, Graves-Deal R, LaFleur BJ, Gao Z, Boman BM, Whitehead RH, Terry E, Morrow JD, Coffey RJ. 2003. Stromalproduction of prostacyclin confers an antiapoptotic effect tocolonic epithelial cells. Cancer Res 63:1748-1751.
21. Damstrup L, Kuwada SK, Dempsey PJ, Brown CL, Hawkey CJ, Poulsen HS, Wiley HS, Coffey RJ, Jr. 1999. Amphiregulin actsas an autocrine growth factor in two human polarizing coloncancer lines that exhibit domain selective EGF receptormitogenesis. Br J Cancer 80:1012-1019.
22. Denker BM, Nigam SK. 1998. Molecular structure and assembly ofthe tight junction. Am J Physiol 274:F1-F9.
23. Dhawan P, Ahmad R, Chaturvedi R, Smith JJ, Midha R, Mittal MK, Krishnan M, Chen X, Eschrich S, Yeatman TJ, Harris RC, Washington MK, Wilson KT, Beauchamp RD, Singh AB. 2011. Claudin-2 expression increases tumorigenicity of colon cancercells: Role of epidermal growth factor receptor activation. Oncogene 30:3234-3247.
24. Dlugosz AA, Cheng C, Denning MF, Dempsey PJ, Coffey RJ, Jr, Yuspa SH. 1994. Keratinocyte growth factor receptor ligandsinduce transforming growth factor alpha expression and activatethe epidermal growth factor receptor signaling pathway incultured epidermal keratinocytes. Cell Growth Differ 5:1283-1292.
25. Egger B, Procaccino F, Sarosi I, Tolmos J, Buchler MW, Eysselein VE. 1999. Keratinocyte growth factor amelioratesdextran sodium sulfate colitis in mice. Dig Dis Sci 44:836-844.
26. Enck AH, Berger UV, Yu AS. 2001. Claudin-2 is selectivelyexpressed in proximal nephron in mouse kidney. Am J PhysiolRenal Physiol 281:F966-F974.
27. Escaffit F, Boudreau F, Beaulieu JF. 2005. Differential expression ofclaudin-2 along the human intestine: Implication of GATA-4 inthe maintenance of claudin-2 in differentiating cells. J CellPhysiol 203:15-26.
28. Farrell CL, Bready JV, Rex KL, Chen JN, DiPalma CR, WhitcombKL, Yin S, Hill DC, Wiemann B, Starnes CO, Havill AM, Lu ZN, Aukerman SL, Pierce GF, Thomason A, Potten CS, Ulich TR, Lacey DL. 1998. Keratinocyte growth factor protectsmice from chemotherapy and radiation-induced gastrointestinalinjury and mortality. Cancer Res 58:933-939.
29. Finch PW, Cheng AL. 1999. Analysis of the cellular basis ofkeratinocyte growth factor overexpression in inflammatorybowel disease. Gut 45:848-855.
30. Finch PW, Rubin JS. 2004. Keratinocyte growth factor/fibroblastgrowth factor 7, a homeostatic factor with therapeutic potentialfor epithelial protection and repair. Adv Cancer Res 91:69-136.
31. Finch PW, Rubin JS, Miki T, Ron D, Aaronson SA. 1989. HumanKGF is FGF-related with properties of a paracrine effector ofepithelial cell growth. Science 245:752-755.
32. Finch PW, Cunha GR, Rubin JS, Wong J, Ron D. 1995. Pattern ofkeratinocyte growth factor and keratinocyte growth factorreceptor expression during mouse fetal development suggests arole in mediating morphogenetic mesenchymal- epithelial interactions. Dev Dyn 203:223-240.
33. Finch PW, Pricolo V, Wu A, Finkelstein SD. 1996. Increasedexpression of keratinocyte growth factor messenger RNAassociated with inflammatory bowel disease. Gastroenterology110:441-451.
34. Furuse M, Sasaki H, Tsukita S. 1999. Manner of interaction ofheterogeneous claudin species within and between tight junctionstrands. J Cell Biol 147:891-903.
35. Furuse M, Furuse K, Sasaki H, Tsukita S. 2001. Conversion ofzonulae occludentes from tight to leaky strand type byintroducing claudin-2 into Madin-Darby canine kidney I cells. J Cell Biol 153:263-272.
36. Gonzalez-Mariscal L, Tapia R, Chamorro D. 2008. Crosstalk oftight junction components with signaling pathways. BiochimBiophys Acta 1778:729-756.
37. Heller F, Florian P, Bojarski C, Richter J, Christ M, Hillenbrand B, Mankertz J, Gitter AH, Burgel N, Fromm M, Zeitz M, Fuss I, Strober W, Schulzke JD. 2005. Interleukin-13 is the key effectorTh2 cytokine in ulcerative colitis that affects epithelial tightjunctions, apoptosis, and cell restitution. Gastroenterology 129:550-564.
38. Housley RM, Morris CF, Boyle W, Ring B, Biltz R, Tarpley JE, Aukerman SL, Devine PL, Whitehead RH, Pierce F. 1994. Keratinocyte growth factor induces proliferation of hepatocytesand epithelial cells throughout the rat gastrointestinal tract. JClin Invest 94:1764-1777.
39. Kinugasa T, Sakaguchi T, Gu X, Reinecker HC. 2000. Claudinsregulate the intestinal barrier in response to immune mediators. Gastroenterology 118:1001-1011.
40. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S. 2002. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13:875-886.
41. Krause G, Winkler L, Mueller SL, Haseloff RF, Piontek J, Blasig IE. 2008. Structure and function of claudins. Biochim Biophys Acta1778:631-645.
42. MacDonald TT, Monteleone G, Pender SL. 2000. Recentdevelopments in the immunology of inflammatory bowel disease. Scand J Immunol 51:2-9.
43. Mankertz J, Amasheh M, Krug SM, Fromm A, Amasheh S, Hillenbrand B, Tavalali S, Fromm M, Schulzke JD. 2009. TNFalpha up-regulates claudin-2 expression in epithelialHT-29/B6 cells via phosphatidylinositol-3-kinase signaling. Cell Tissue Res 336:67-77.
44. Merchant NB, Rogers CM, Trivedi B, Morrow J, Coffey RJ. 2005. Ligand-dependent activation of the epidermal growth factorreceptor by secondary bile acids in polarizing colon cancer cells. Surgery 138:415-421.
45. Merchant NB, Voskresensky I, Rogers CM, Lafleur B, Dempsey PJ, Graves-Deal R, Revetta F, Foutch AC, Rothenberg ML, Washington MK, Coffey RJ. 2008. TACE/ADAM-17: acomponent of the epidermal growth factor receptor axis and apromising therapeutic target in colorectal cancer. Clin CancerRes 14:1182-1191.
46. Miki T, Bottaro DP, Fleming TP, Smith CL, Burgess WH, Chan AM, Aaronson SA. 1992. Determination of ligandbindingspecificity by alternative splicing: Two distinct growthfactor receptors encoded by a single gene. Proc Natl Acad SciUSA 89:246-250.
47. Mineta K, Yamamoto Y, Yamazaki Y, Tanaka H, Tada Y, Saito K, Tamura A, Igarashi M, Endo T, Takeuchi K, Tsukita S. 2011. Predicted expansion of the claudin multigene family. FEBS Lett585:606-612.
48. Piepkorn M, Underwood RA, Henneman C, Smith LT. 1995. Expression of amphiregulin is regulated in cultured humankeratinocytes and in developing fetal skin. J Invest Dermatol 105:802-809.
49. Piontek J, Winkler L, Wolburg H, Muller SL, Zuleger N, Piehl C, Wiesner B, Krause G, Blasig IE. 2008. Formation of tightjunction: Determinants of homophilic interaction betweenclassic claudins. FASEB J 22:146-158.
50. Potten CS, O'Shea JA, Farrell CL, Rex K, Booth C. 2001. Theeffects of repeated doses of keratinocyte growth factor on cellproliferation in the cellular hierarchy of the crypts of the murinesmall intestine. Cell Growth Differ 12:265-275.
51. Powell DW. 1981. Barrier function of epithelia. Am J Physiol 241:G275-G288.
52. Powell DW. 2000. Myofibroblasts: Paracrine cells importantin health and disease. Trans Am Clin Climatol Assoc111(271-292):271-293.
53. PowellDW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB. 1999a. Myofibroblasts. I. Paracrine cells important in health anddisease. Am J Physiol 277:C1-C9.
54. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, WestAB. 1999b. Myofibroblasts. II. Intestinal subepithelial myofi-broblasts. Am J Physiol 277:C183-C201.
55. Powell DW, Adegboyega PA, Di Mari JF, Mifflin RC. 2005. Epithelial cells and their neighbors I. Role of intestinalmyofibroblasts in development, repair, and cancer. Am J PhysiolGastrointest Liver Physiol 289:G2-G7.
56. Prasad S, Mingrino R, Kaukinen K, Hayes KL, Powell RM, MacDonald TT, Collins JE. 2005. Inflammatory processes havedifferential effects on claudins 2, 3 and 4 in colonic epithelialcells. Lab Invest 85:1139-1162.
57. Rosenthal R, Milatz S, Krug SM, Oelrich B, Schulzke JD, Amasheh S, Gunzel D, Fromm M. 2010. Claudin-2, acomponent of the tight junction, forms a paracellular waterchannel. J Cell Sci 123:1913-1921.
58. Rubin JS, Osada H, Finch PW, Taylor WG, Rudikoff S, Aaronson SA. 1989. Purification and characterization of anewly identified growth factor specific for epithelial cells. ProcNatl Acad Sci USA 86:802-806.
59. Sambuy Y, De Angelis I, Ranaldi G, Scarino ML, Stammati A, Zucco F. 2005. The Caco-2 cell line as a model of the intestinalbarrier: Influence of cell and culture-related factors on Caco-2cell functional characteristics. Cell Biol Toxicol 21:1-26.
60. Schneeberger EE, Lynch RD. 2004. The tight junction: amultifunctional complex. Am J Physiol Cell Physiol 286:C1213-C1228.
61. Schulzke JD, Ploeger S, Amasheh M, Fromm A, Zeissig S, Troeger H, Richter J, Bojarski C, Schumann M, Fromm M. 2009. Epithelial tight junctions in intestinal inflammation. AnnNY Acad Sci 1165:294-300.
62. Shao J, Sheng GG, Mifflin RC, PowellDW, Sheng H. 2006. Roles ofmyofibroblasts in prostaglandin E2-stimulated intestinal epithelialproliferation and angiogenesis. Cancer Res 66:846-855.
63. Suzuki T, Yoshinaga N, Tanabe S. 2011. Interleukin-6 (IL-6)regulates claudin-2 expression and tight junction permeability inintestinal epithelium. J Biol Chem 286:31263-31271.
64. Takehara M, Nishimura T, Mima S, Hoshino T, Mizushima T. 2009. Effect of claudin expression on paracellular permeability, migration and invasion of colonic cancer cells. Biol Pharm Bull32:825-831.
65. Thorne BA, Plowman GD. 1994. The heparin-binding domain ofamphiregulin necessitates the precursor pro-region for growthfactor secretion. Mol Cell Biol 14:1635-1646.
66. Valentich JD, Popov V, Saada JI, Powell DW. 1997. Phenotypiccharacterization of an intestinal subepithelial myofibroblast cellline. Am J Physiol 272:C1513-C1524.
67. Van Itallie CM, Anderson JM. 2004a. The molecular physiology oftight junction pores. Physiology (Bethesda) 19:331-338.
68. Van Itallie CM, Anderson JM. 2004b. The role of claudins indetermining paracellular charge selectivity. Proc Am Thorac Soc1:38-41.
69. Van Itallie CM, Fanning AS, Anderson JM. 2003. Reversal ofcharge selectivity in cation or anion-selective epithelial lines byexpression of different claudins. Am J Physiol Renal Physiol 285:F1078-F1084.
70. Van Itallie CM, Mitic LL, Anderson JM. 2011. Claudin-2 formshomodimers and is a component of a high molecular weightprotein complex. J Biol Chem 286:3442-3450.
71. Visco V, Bava FA, d'Alessandro F, Cavallini M, Ziparo V, Torrisi MR. 2009. Human colon fibroblasts induce differentiationand proliferation of intestinal epithelial cells through thedirect paracrine action of keratinocyte growth factor. J CellPhysiol 220:204-213.
72. Weber CR, Nalle SC, Tretiakova M, Rubin DT, Turner Jr. 2008. Claudin-1 and claudin-2 expression is elevated in inflammatorybowel disease and may contribute to early neoplastic transformation. Lab Invest 88:1110-1120.
73. Wisner DM, Harris LR, III, Green CL, Poritz LS. 2008. Opposingregulation of the tight junction protein claudin-2 by interferongammaand interleukin-4. J Surg Res 144:1-7.
74. Yang H, Antony PA, Wildhaber BE, Teitelbaum DH. 2004. Intestinal intraepithelial lymphocyte gamma delta-T cell-derivedkeratinocyte growth factor modulates epithelial growth in themouse. J Immunol 172:4151-4158.
75. Zeeh JM, Procaccino F, Hoffmann P, Aukerman SL, McRoberts JA, Soltani S, Pierce GF, Lakshmanan J, Lacey D, Eysselein VE. 1996. Keratinocyte growth factor ameliorates mucosal injury inan experimental model of colitis in rats. Gastroenterology 110:1077-1083.
76. Zeissig S, Burgel N, Gunzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD. 2007. Changes in expression and distribution ofclaudin 2, 5 and 8 lead to discontinuous tight junctions andbarrier dysfunction in active Crohn's disease. Gut 56:61-72.
77. Zigrino P, Loffek S, Mauch C. 2005. Tumor-stroma interactions:Their role in the control of tumor cell invasion. Biochimie 87: 321-328.