The tight junction protein claudin-3 shows conserved expression in the nephric duct and ureteric bud and promotes tubulogenesis in vitro

American Journal of Physiology - Renal Physiology

Volumn 301, Issue 5, 2011, Pages

  Haddad, Nicholas ^a   El Andalousi, Jasmine ^a   Khairallah, Halim ^a   Yu, Melissa ^a   Ryan, Aimee K ^a   Gupta, Indra R ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Claudins; mIMCD 3 cells; Tight junction; Tubule

Indexed keywords

CLAUDIN 3; COLLAGEN TYPE 1; ENHANCED GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTEIN ZO1;

ANIMAL CELL; ARTICLE; CELL EXPANSION; CELL MEMBRANE; CELL PROLIFERATION; CELL SHAPE; CONTROLLED STUDY; EPITHELIUM CELL; GENITAL SYSTEM; IMMUNOASSAY; IN SITU HYBRIDIZATION; IN VITRO STUDY; KIDNEY DEVELOPMENT; KIDNEY FUNCTION; MOUSE; MUELLERIAN DUCT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; STABLE TRANSFECTION; TIGHT JUNCTION; TRANSMISSION ELECTRON MICROSCOPY; TUBULOGENESIS; URETER BUD;

EID: 80055089226     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00497.2010     Document Type: Article

References (60)

1. Abuazza G, Becker A, Williams SS, Chakravarty S, Truong HT, Lin F, Baum M. Claudins 6, 9, and 13 are developmentally expressed renal tight junction proteins. Am J Physiol Renal Physiol 291: F1132-F1141, 2006.
2. Agarwal R, D'Souza T, Morin PJ. Claudin-3 and claudin-4 expression in ovarian epithelial cells enhances invasion and is associated with increased matrix metalloproteinase-2 activity. Cancer Res 65: 7378-7385, 2005.
3. Alie TM, Vrljicak PJ, Myburgh DB, Gupta IR. Microinjection and electroporation of embryonic kidney explants: an improved method. Kidney Int 72: 121-125, 2007.
4. Angelow S, Ahlstrom R, Yu AS. Biology of claudins. Am J Physiol Renal Physiol 295: F867-F876, 2008.
5. Baker PC, Schroeder TE. Cytoplasmic filaments and morphogenetic movement in the amphibian neural tube. Dev Biol 15: 432-450, 1967.
6. Barasch J, Yang J, Qiao J, Tempst P, Erdjument-Bromage H, Leung W, Oliver JA. Tissue inhibitor of metalloproteinase-2 stimulates mesenchymal growth and regulates epithelial branching during morphogenesis of the rat metanephros. J Clin Invest 103: 1299-1307, 1999.
7. Blanchard AA, Watson PH, Shiu RP, Leygue E, Nistor A, Wong P, Myal Y. Differential expression of claudin 1, 3, and 4 during normal mammary gland development in the mouse. DNA Cell Biol 25: 79-86, 2006.
8. Bouchard M. Transcriptional control of kidney development. Differentiation 72: 295-306, 2004.
9. Brizuela BJ, Wessely O, De Robertis EM. Overexpression of the Xenopus tight-junction protein claudin causes randomization of the leftright body axis. Dev Biol 230: 217-229, 2001.
10. Cebrian C, Borodo K, Charles N, Herzlinger DA. Morphometric index of the developing murine kidney. Dev Dyn 231: 601-608, 2004.
11. Chiba H, Osanai M, Murata M, Kojima T, Sawada N. Transmembrane proteins of tight junctions. Biochim Biophys Acta 1778: 588-600, 2008.
12. Costantini F. Renal branching morphogenesis: concepts, questions, and recent advances. Differentiation 74: 402-421, 2006.
13. D'Souza T, Agarwal R, Morin PJ. Phosphorylation of claudin-3 at threonine 192 by cAMP-dependent protein kinase regulates tight junction barrier function in ovarian cancer cells. J Biol Chem 280: 26233-26240, 2005.
14. Dressler GR. Advances in early kidney specification, development and patterning. Development 136: 3863-3874, 2009.
15. Dressler GR. The cellular basis of kidney development. Annu Rev Cell Dev Biol 22: 509-529, 2006.
16. Durbec P, Marcos-Gutierrez CV, Kilkenny C, Grigoriou M, Wartiowaara K, Suvanto P, Smith D, Ponder B, Costantini F, Saarma M, Sariola H, Pachnis V. GDNF signalling through the Ret receptor tyrosine kinase. Nature 381: 789-93, 1996.
17. Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM Jr, Milbrandt J. GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21: 317-324, 1998.
18. Furuse M, Hata M, Furuse K, Yoshida Y, Haratake A, Sugitani Y, Noda T, Kubo A, Tsukita S. Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. J Cell Biol 156: 1099-1111, 2002.
19. Furuse M, Sasaki H, Fujimoto K, Tsukita S. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143: 391-401, 1998.
20. Gupta IR, Macias-Silva M, Kim S, Zhou X, Piscione TD, Whiteside C, Wrana JL, Rosenblum ND. BMP-2/ALK3 and HGF signal in parallel to regulate renal collecting duct morphogenesis. J Cell Sci 113: 269-278, 2000.
21. Gupta IR, Piscione TD, Grisaru S, Phan T, Macias-Silva M, Zhou X, Whiteside C, Wrana JL, Rosenblum ND. Protein kinase A is a negative regulator of renal branching morphogenesis and modulates inhibitory and stimulatory bone morphogenetic proteins. J Biol Chem 274: 26305-26314, 1999.
22. Gupta IR, Ryan AK. Claudins: unlocking the code to tight junction function during embryogenesis and in disease. Clin Genet 77: 314-325, 2010.
23. Haworth KE, El-Hanfy A, Prayag S, Healy C, Dietrich S, Sharpe P. Expression of claudin-3 during chick development. Gene Expr Patterns: 40-44, 2005.
24. Heinzelmann-Schwarz VA, Gardiner-Garden M, Henshall SM, Scurry J, Scolyer RA, Davies MJ, Heinzelmann M, Kalish LH, Bali A, Kench JG, Edwards LS, Vanden Bergh PM, Hacker NF, Sutherland RL, O'Brien PM. Overexpression of the cell adhesion molecules DDR1, claudin 3, and Ep-CAM in metaplastic ovarian epithelium and ovarian cancer. Clin Cancer Res 10: 4427-4436, 2004.
25. Hough CD, Sherman-Baust CA, Pizer ES, Montz FJ, Im DD, Rosenshein NB, Cho KR, Riggins GJ, Morin PJ. Large-scale serial analysis of gene expression reveals genes differentially expressed in ovarian cancer. Cancer Res 60: 6281-6287, 2000.
26. Huang YH, Bao Y, Peng W, Goldberg M, Love K, Bumcrot DA, Cole G, Langer R, Anderson DG, Sawicki JA. Claudin-3 gene silencing with siRNA suppresses ovarian tumor growth and metastasis. Proc Natl Acad Sci USA 106: 3426-3430, 2009.
27. James RG, Kamei CN, Wang Q, Jiang R, Schultheiss TM. Oddskipped related 1 is required for development of the metanephric kidney and regulates formation and differentiation of kidney precursor cells. Development 133: 2995-3004, 2006.
28. Kaarteenaho R, Merikallio H, Lehtonen S, Harju T, Soini Y. Divergent expression of claudin -1, -3, -4, -5 and -7 in developing human lung. Respir Res 11: 59, 2010.
29. Kim D, Dressler GR. PTEN modulates GDNF/RET mediated chemotaxis and branching morphogenesis in the developing kidney. Dev Biol 307: 290-299, 2007.
30. Kiuchi-Saishin Y, Gotoh S, Furuse M, Takasuga A, Tano Y, Tsukita S. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments. J Am Soc Nephrol 13: 875-886, 2002.
31. Kollmar R, Nakamura SK, Kappler JA, Hudspeth AJ. Expression and phylogeny of claudins in vertebrate primordia. Proc Natl Acad Sci USA 98: 10196-10201, 2001.
32. Krause G, Winkler L, Mueller SL, Haseloff RF, Piontek J, Blasig IE. Structure and function of claudins. Biochim Biophys Acta 1778: 631-645, 2008.
33. 2+-independent cell-adhesion activity of claudins, a family of integral membrane proteins localized at tight junctions. Curr Biol 9: 1035-1038, 1999.
34. Lopardo T, Lo Iacono N, Marinari B, Giustizieri ML, Cyr DG, Merlo G, Crosti F, Costanzo A, Guerrini L. Claudin-1 is a p63 target gene with a crucial role in epithelial development. PLoS One 3: e2715, 2008.
35. Lourenco SV, Coutinho-Camillo CM, Buim ME, Uyekita SH, Soares FA. Human salivary gland branching morphogenesis: morphological localization of claudins and its parallel relation with developmental stages revealed by expression of cytoskeleton and secretion markers. Histochem Cell Biol 128: 361-369, 2007.
36. Meyer TN, Schwesinger C, Bush KT, Stuart RO, Rose DW, Shah MM, Vaughn DA, Steer DL, Nigam SK. Spatiotemporal regulation of morphogenetic molecules during in vitro branching of the isolated ureteric bud: toward a model of branching through budding in the developing kidney. Dev Biol 275: 44-67, 2004.
37. Milatz S, Krug SM, Rosenthal R, Gunzel D, Muller D, Schulzke JD, Amasheh S, Fromm M. Claudin-3 acts as a sealing component of the tight junction for ions of either charge and uncharged solutes. Biochim Biophys Acta 1798: 2048-2057, 2010.
38. Miyamori H, Takino T, Kobayashi Y, Tokai H, Itoh Y, Seiki M, Sato H. Claudin promotes activation of pro-matrix metalloproteinase-2 mediated by membrane-type matrix metalloproteinases. J Biol Chem 276: 28204-28211, 2001.
39. Moriwaki K, Tsukita S, Furuse M. Tight junctions containing claudin 4 and 6 are essential for blastocyst formation in preimplantation mouse embryos. Dev Biol 312: 509-522, 2007.
40. Nieto MA, Patel K, Wilkinson DG. In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51: 219-235, 1996.
41. Nigam SK, Shah MM. How does the ureteric bud branch? J Am Soc Nephrol 20: 1465-1469, 2009.
42. Obara-Ishihara T, Kuhlman J, Niswander L, Herzlinger D. The surface ectoderm is essential for nephric duct formation in intermediate mesoderm. Development 126: 1103-1108, 1999.
43. Ohta H, Adachi H, Inaba M. Developmental changes in the expression of tight junction protein claudins in murine metanephroi and embryonic kidneys. J Vet Med Sci 68: 149-155, 2006.
44. Piscione TD, Yager TD, Gupta IR, Grinfeld B, Pei Y, Attisano L, Wrana JL, Rosenblum ND. BMP-2 and OP-1 exert direct and opposite effects on renal branching morphogenesis. Am J Physiol Renal Physiol 273: F961-F975, 1997.
45. Pohl M, Sakurai H, Bush KT, Nigam SK. Matrix metalloproteinases and their inhibitors regulate in vitro ureteric bud branching morphogenesis. Am J Physiol Renal Physiol 279: F891-F900, 2000.
46. Poole TJ, Steinberg MS. Amphibian pronephric duct morphogenesis: segregation, cell rearrangement and directed migration of the Ambystoma duct rudiment. J Embryol Exp Morphol 63: 1-16, 1981.
47. Rangel LB, Agarwal R, D'Souza T, Pizer ES, Alo PL, Lancaster WD, Gregoire L, Schwartz DR, Cho KR, Morin PJ. Tight junction proteins claudin-3 and claudin-4 are frequently overexpressed in ovarian cancer but not in ovarian cystadenomas. Clin Cancer Res 9: 2567-2575, 2003.
48. Rangel LB, Sherman-Baust CA, Wernyj RP, Schwartz DR, Cho KR, Morin PJ. Characterization of novel human ovarian cancer-specific transcripts (HOSTs) identified by serial analysis of gene expression. Oncogene 22: 7225-7232, 2003.
49. Rauchman MI, Nigam SK, Delpire E, Gullans SR. An osmotically tolerant inner medullary collecting duct cell line from an SV40 transgenic mouse. Am J Physiol Renal Fluid Electrolyte Physiol 265: F416-F424, 1993.
50. Schmidt-Ott KM, Yang J, Chen X, Wang H, Paragas N, Mori K, Li JY, Lu B, Costantini F, Schiffer M, Bottinger E, Barasch J. Novel regulators of kidney development from the tips of the ureteric bud. J Am Soc Nephrol 16: 1993-2002, 2005.
51. Schuchardt A, D'Agati V, Pachnis V, Costantini F. Renal agenesis and hypodysplasia in ret-k-mutant mice result from defects in ureteric bud development. Development 122: 1919-1929, 1996.
52. Schwab K, Patterson LT, Aronow BJ, Luckas R, Liang HC, Potter SS. A catalogue of gene expression in the developing kidney. Kidney Int 64: 1588-1604, 2003.
53. Simard A, Di Pietro E, Ryan AK. Gene expression pattern of Claudin-1 during chick embryogenesis. Gene Expr Patterns 5: 553-560, 2005.
54. Stuart RO, Bush KT, Nigam SK. Changes in gene expression patterns in the ureteric bud and metanephric mesenchyme in models of kidney development. Kidney Int 64: 1997-2008, 2003.
55. Tsukita S, Furuse M. The structure and function of claudins, cell adhesion molecules at tight junctions. Ann NY Acad Sci 915: 129-135, 2000.
56. Tsukita S, Yamazaki Y, Katsuno T, Tamura A. Tight junction-based epithelial microenvironment and cell proliferation. Oncogene 27: 6930-6938, 2008.
57. Turksen K, Troy TC. Barriers built on claudins. J Cell Sci 117: 2435-2447, 2004.
58. Turksen K, Troy TC. Permeability barrier dysfunction in transgenic mice overexpressing claudin 6. Development 129: 1775-1784, 2002.
59. Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol 68: 403-429, 2006.
60. Yamauchi K, Rai T, Kobayashi K, Sohara E, Suzuki T, Itoh T, Suda S, Hayama A, Sasaki S, Uchida S. Disease-causing mutant WNK4 increases paracellular chloride permeability and phosphorylates claudins. Proc Natl Acad Sci USA 101: 4690-4694, 2004.