CFTR interacts with ZO-1 to regulate tight junction assembly and epithelial differentiation through the ZONAB pathway

Journal of Cell Science

Volumn 127, Issue 20, 2014, Pages 4396-4408

  Ruan, Ye Chun ^a,b   Wang, Yan ^b   da Silva, Nicolas ^a   Kim, Bongki ^a   Diao, Rui Ying ^b   Hill, Eric ^a   Brown, Dennis ^a   Chan, Hsiao Chang ^b   Breton, Sylvie ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

Author keywords

CFTR; Embryonic development; Epithelial remodeling; Male fertility; Morphogenesis; Proliferation; ZO 1; ZONAB

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; LEUPEPTIN; PROTEIN ZO1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZONAB TRANSCRIPTION FACTOR; CFTR PROTEIN, HUMAN; CSDA PROTEIN, MOUSE; CYCLIN D1; DNA BINDING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, MOUSE; PROTEIN BINDING; TJP1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYSTIC FIBROSIS; EMBRYO; EMBRYONIC STRUCTURES; EPIDIDYMIS; EPITHELIUM CELL; FEMALE; IMMUNOFLUORESCENCE; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TIGHT JUNCTION; TRACHEA; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; METABOLISM; ORGANOGENESIS; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

MUS; WOLFFIA;

ANIMALS; CELL DIFFERENTIATION; CELL NUCLEUS; CELLS, CULTURED; CYCLIN D1; CYSTIC FIBROSIS; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; DNA-BINDING PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORGANOGENESIS; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; TRANSCRIPTION FACTORS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84918582197     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.148098     Document Type: Article

References (68)

1. Anguiano, A., Oates, R. D., Amos, J. A., Dean, M., Gerrard, B., Stewart, C., Maher, T. A., White, M. B. and Milunsky, A. (1992). Congenital bilateral absence of the vas deferens. A primarily genital form of cystic fibrosis. JAMA 267, 1794-1797.
2. Araki, Y., Suzuki, K., Matusik, R. J., Obinata, M. and Orgebin-Crist, M. C. (2002). Immortalized epididymal cell lines from transgenic mice overexpressing temperature-sensitive simian virus 40 large T-antigen gene. J. Androl. 23, 854-869.
3. Balda, M. S. and Matter, K. (2000). The tight junction protein ZO-1 and an interacting transcription factor regulate ErbB-2 expression. EMBO J. 19, 2024-2033.
4. Balda, M. S. and Matter, K. (2009). Tight junctions and the regulation of gene expression. Biochim. Biophys. Acta 1788, 761-767.
5. Berdiev, B. K., Qadri, Y. J. and Benos, D. J. (2009). Assessment of the CFTR and ENaC association. Mol. Biosyst. 5, 123-127.
6. Blau, H., Freud, E., Mussaffi, H., Werner, M., Konen, O. and Rathaus, V. (2002). Urogenital abnormalities in male children with cystic fibrosis. Arch. Dis. Child. 87, 135-138.
7. Bomberger, J. M., Guggino, W. B. and Stanton, B. A. (2011). Methods to monitor cell surface expression and endocytic trafficking of CFTR in polarized epithelial cells. Methods Mol. Biol. 741, 271-283.
8. Brown, D., Smith, P. J. and Breton, S. (1997). Role of V-ATPase-rich cells in acidification of the male reproductive tract. J. Exp. Biol. 200, 257-262.
9. Castellani, S., Guerra, L., Favia, M., Di Gioia, S., Casavola, V. and Conese, M. (2012). NHERF1 and CFTR restore tight junction organisation and function in cystic fibrosis airway epithelial cells: role of ezrin and the RhoA/ROCK pathway. Lab. Invest. 92, 1527-1540.
10. Chan, H. C., Ruan, Y. C., He, Q., Chen, M. H., Chen, H., Xu, W. M., Chen, W. Y., Xie, C., Zhang, X. H. and Zhou, Z. (2009). The cystic fibrosis transmembrane conductance regulator in reproductive health and disease. J. Physiol. 587, 2187-2195.
11. Chen, H., Guo, J. H., Lu, Y. C., Ding, G. L., Yu, M. K., Tsang, L. L., Fok, K. L., Liu, X. M., Zhang, X. H., Chung, Y. W. et al. (2012a). Impaired CFTR-dependent amplification of FSH-stimulated estrogen production in cystic fibrosis and PCOS. J. Clin. Endocrinol. Metab. 97, 923-932.
12. Chen, H., Ruan, Y. C., Xu, W. M., Chen, J. and Chan, H. C. (2012b). Regulation of male fertility by CFTR and implications in male infertility. Hum. Reprod. Update 18, 703-713.
13. Cornwall, G. A. (2009). New insights into epididymal biology and function. Hum. Reprod. Update 15, 213-227.
14. Cuppens, H. and Cassiman, J. J. (2004). CFTR mutations and polymorphisms in male infertility. Int. J. Androl. 27, 251-256.
15. Fanning, A. S., Ma, T. Y. and Anderson, J. M. (2002). Isolation and functional characterization of the actin binding region in the tight junction protein ZO-1. FASEB J. 16, 1835-1837.
16. Gaillard, D., Ruocco, S., Lallemand, A., Dalemans, W., Hinnrasky, J. and Puchelle, E. (1994). Immunohistochemical localization of cystic fibrosis transmembrane conductance regulator in human fetal airway and digestive mucosa. Pediatr. Res. 36, 137-143.
17. Gaillard, D. A., Carré-Pigeon, F. and Lallemand, A. (1997). Normal vas deferens in fetuses with cystic fibrosis. J. Urol. 158, 1549-1552.
18. Galietta, L. J. (2013). Managing the underlying cause of cystic fibrosis: a future role for potentiators and correctors. Paediatr. Drugs 15, 393-402.
19. Gallagher, A. M. and Gottlieb, R. A. (2001). Proliferation, not apoptosis, alters epithelial cell migration in small intestine of CFTR null mice. Am. J. Physiol. 281, G681-G687.
20. Guggino, W. B. and Stanton, B. A. (2006). New insights into cystic fibrosis: molecular switches that regulate CFTR. Nat. Rev. Mol. Cell Biol. 7, 426-436.
21. Hajj, R., Lesimple, P., Nawrocki-Raby, B., Birembaut, P., Puchelle, E. and Coraux, C. (2007). Human airway surface epithelial regeneration is delayed and abnormal in cystic fibrosis. J. Pathol. 211, 340-350.
22. Hihnala, S., Kujala, M., Toppari, J., Kere, J., Holmberg, C. and Höglund, P. (2006). Expression of SLC26A3, CFTR and NHE3 in the human male reproductive tract: role in male subfertility caused by congenital chloride diarrhoea. Mol. Hum. Reprod. 12, 107-111.
23. Hollande, E., Fanjul, M., Chemin-Thomas, C., Devaux, C., Demolombe, S., Van Rietschoten, J., Guy-Crotte, O. and Figarella, C. (1998). Targeting of CFTR protein is linked to the polarization of human pancreatic duct cells in culture. Eur. J. Cell Biol. 76, 220-227.
24. Joseph, A., Yao, H. and Hinton, B. T. (2009). Development and morphogenesis of the Wolffian/epididymal duct, more twists and turns. Dev. Biol. 325, 6-14.
25. Katsuno, T., Umeda, K., Matsui, T., Hata, M., Tamura, A., Itoh, M., Takeuchi, K., Fujimori, T., Nabeshima, Y., Noda, T. et al. (2008). Deficiency of zonula occludens-1 causes embryonic lethal phenotype associated with defected yolk sac angiogenesis and apoptosis of embryonic cells. Mol. Biol. Cell 19, 2465-2475.
26. Krapf, D., Ruan, Y. C., Wertheimer, E. V., Battistone, M. A., Pawlak, J. B., Sanjay, A., Pilder, S. H., Cuasnicu, P., Breton, S. and Visconti, P. E. (2012). cSrc is necessary for epididymal development and is incorporated into sperm during epididymal transit. Dev. Biol. 369, 43-53.
27. LeSimple, P., Liao, J., Robert, R., Gruenert, D. C. and Hanrahan, J. W. (2010). Cystic fibrosis transmembrane conductance regulator trafficking modulates the barrier function of airway epithelial cell monolayers. J. Physiol. 588, 1195-1209.
28. Li, X., Comellas, A. P., Karp, P. H., Ernst, S. E., Moninger, T. O., Gansemer, N. D., Taft, P. J., Pezzulo, A. A., Rector, M. V., Rossen, N. et al. (2012). CFTR is required for maximal transepithelial liquid transport in pig alveolar epithelia. Am. J. Physiol. 303, L152-L160.
29. Lima, W. R., Parreira, K. S., Devuyst, O., Caplanusi, A., N'kuli, F., Marien, B., Van Der Smissen, P., Alves, P. M., Verroust, P., Christensen, E. I. et al. (2010). ZONAB promotes proliferation and represses differentiation of proximal tubule epithelial cells. J. Am. Soc. Nephrol. 21, 478-488.
30. Lu, Y. C., Chen, H., Fok, K. L., Tsang, L. L., Yu, M. K., Zhang, X. H., Chen, J., Jiang, X., Chung, Y. W., Ma, A. C. et al. (2012). CFTR mediates bicarbonatedependent activation of miR-125b in preimplantation embryo development. Cell Res. 22, 1453-1466.
31. Ma, T., Thiagarajah, J. R., Yang, H., Sonawane, N. D., Folli, C., Galietta, L. J. and Verkman, A. S. (2002). Thiazolidinone CFTR inhibitor identified by highthroughput screening blocks cholera toxin-induced intestinal fluid secretion. J. Clin. Invest. 110, 1651-1658.
32. Marcorelles, P., Gillet, D., Friocourt, G., Ledé, F., Samaison, L., Huguen, G. and Ferec, C. (2012). Cystic fibrosis transmembrane conductance regulator protein expression in the male excretory duct system during development. Hum. Pathol. 43, 390-397.
33. Martinez-Palomo, A., Meza, I., Beaty, G. and Cereijido, M. (1980). Experimental modulation of occluding junctions in a cultured transporting epithelium. J. Cell Biol. 87, 736-745.
34. Meyerholz, D. K., Stoltz, D. A., Namati, E., Ramachandran, S., Pezzulo, A. A., Smith, A. R., Rector, M. V., Suter, M. J., Kao, S., McLennan, G. et al. (2010). Loss of cystic fibrosis transmembrane conductance regulator function produces abnormalities in tracheal development in neonatal pigs and young children. Am. J. Respir. Crit. Care Med. 182, 1251-1261.
35. Nilsson, H. E., Dragomir, A., Lazorova, L., Johannesson, M. and Roomans, G. M. (2010). CFTR and tight junctions in cultured bronchial epithelial cells. Exp. Mol. Pathol. 88, 118-127.
36. O'Neal, W. K., Hasty, P., McCray, P. B., Jr, Casey, B., Rivera-Pérez, J., Welsh, M. J., Beaudet, A. L. and Bradley, A. (1993). A severe phenotype in mice with a duplication of exon 3 in the cystic fibrosis locus. Hum. Mol. Genet. 2, 1561-1569.
37. O'Sullivan, B. P. and Freedman, S. D. (2009). Cystic fibrosis. Lancet 373, 1891-1904.
38. Oates, R. D. and Amos, J. A. (1994). The genetic basis of congenital bilateral absence of the vas deferens and cystic fibrosis. J. Androl. 15, 1-8.
39. Oppenheimer, E. H. and Esterly, J. R. (1969). Observations on cystic fibrosis of the pancreas. V. Developmental changes in the male genital system. J. Pediatr. 75, 806-811.
40. Ostedgaard, L. S., Randak, C., Rokhlina, T., Karp, P., Vermeer, D., Ashbourne Excoffon, K. J. and Welsh, M. J. (2003). Effects of C-terminal deletions on cystic fibrosis transmembrane conductance regulator function in cystic fibrosis airway epithelia. Proc. Natl. Acad. Sci. USA 100, 1937-1942.
41. Pastor-Soler, N., Bagnis, C., Sabolic, I., Tyszkowski, R., McKee, M., Van Hoek, A., Breton, S. and Brown, D. (2001). Aquaporin 9 expression along the male reproductive tract. Biol. Reprod. 65, 384-393.
42. Pastor-Soler, N., Isnard-Bagnis, C., Herak-Kramberger, C., Sabolic, I., Van Hoek, A., Brown, D. and Breton, S. (2002). Expression of aquaporin 9 in the adult rat epididymal epithelium is modulated by androgens. Biol. Reprod. 66, 1716-1722.
43. Pastor-Soler, N. M., Fisher, J. S., Sharpe, R., Hill, E., Van Hoek, A., Brown, D. and Breton, S. (2010). Aquaporin 9 expression in the developing rat epididymis is modulated by steroid hormones. Reproduction 139, 613-621.
44. Patrizio, P. and Zielenski, J. (1996). Congenital absence of the vas deferens: a mild form of cystic fibrosis. Mol. Med. Today 2, 24-31.
45. Pezzulo, A. A., Tang, X. X., Hoegger, M. J., Alaiwa, M. H., Ramachandran, S., Moninger, T. O., Karp, P. H., Wohlford-Lenane, C. L., Haagsman, H. P. et al. (2012). Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487, 109-113.
46. Pietrement, C., Sun-Wada, G. H., Silva, N. D., McKee, M., Marshansky, V., Brown, D., Futai, M. and Breton, S. (2006). Distinct expression patterns of different subunit isoforms of the V-ATPase in the rat epididymis. Biol. Reprod. 74, 185-194.
47. Pietrement, C., Da Silva, N., Silberstein, C., James, M., Marsolais, M., Van Hoek, A., Brown, D., Pastor-Soler, N., Ameen, N., Laprade, R. et al. (2008). Role of NHERF1, cystic fibrosis transmembrane conductance regulator, and cAMP in the regulation of aquaporin 9. J. Biol. Chem. 283, 2986-2996.
48. Quinton, P. M. (1999). Physiological basis of cystic fibrosis: a historical perspective. Physiol. Rev. 79 Suppl., S3-S22.
49. Ramsey, B. W., Banks-Schlegel, S., Accurso, F. J., Boucher, R. C., Cutting, G. R., Engelhardt, J. F., Guggino, W. B., Karp, C. L., Knowles, M. R., Kolls, J. K. et al. (2012). Future directions in early cystic fibrosis lung disease research: an NHLBI workshop report. Am. J. Respir. Crit. Care Med. 185, 887-892.
50. Reynaert, I., Van Der Schueren, B., Degeest, G., Manin, M., Cuppens, H., Scholte, B. and Cassiman, J. J. (2000). Morphological changes in the vas deferens and expression of the cystic fibrosis transmembrane conductance regulator (CFTR) in control, deltaF508 and knock-out CFTR mice during postnatal life. Mol. Reprod. Dev. 55, 125-135.
51. Robaire, B., Hinton, B. T. and Orgebin-Crist, M. C. (2006). The epididymis. In Physiology of Reproduction (ed. J. D. Neill), pp. 1071-1148. New York, NY: Elsevier.
52. Rowe, S. M. and Verkman, A. S. (2013). Cystic fibrosis transmembrane regulator correctors and potentiators. Cold Spring Harb. Perspect Med. 3, a009761.
53. Rowe, S. M., Miller, S. and Sorscher, E. J. (2005). Cystic fibrosis. N. Engl. J. Med. 352, 1992-2001.
54. Ruan, Y. C., Shum, W. W., Belleannée, C., Da Silva, N. and Breton, S. (2012). ATP secretion in the male reproductive tract: essential role of CFTR. J. Physiol. 590, 4209-4222.
55. Ruz, R., Andonian, S. and Hermo, L. (2004). Immunolocalization and regulation of cystic fibrosis transmembrane conductance regulator in the adult rat epididymis. J. Androl. 25, 265-273.
56. Schulz, S., Jakubiczka, S., Kropf, S., Nickel, I., Muschke, P. and Kleinstein, J. (2006). Increased frequency of cystic fibrosis transmembrane conductance regulator gene mutations in infertile males. Fertil. Steril. 85, 135-138.
57. Shum, W. W., Ruan, Y. C., Da Silva, N. and Breton, S. (2011). Establishment of cell-cell cross talk in the epididymis: control of luminal acidification. J. Androl. 32, 576-586.
58. Snouwaert, J. N., Brigman, K. K., Latour, A. M., Malouf, N. N., Boucher, R. C., Smithies, O. and Koller, B. H. (1992). An animal model for cystic fibrosis made by gene targeting. Science 257, 1083-1088.
59. Sourisseau, T., Georgiadis, A., Tsapara, A., Ali, R. R., Pestell, R., Matter, K. and Balda, M. S. (2006). Regulation of PCNA and cyclin D1 expression and epithelial morphogenesis by the ZO-1-regulated transcription factor ZONAB/DbpA. Mol. Cell. Biol. 26, 2387-2398.
60. Tizzano, E. F., Chitayat, D. and Buchwald, M. (1993). Cell-specific localization of CFTR mRNA shows developmentally regulated expression in human fetal tissues. Hum. Mol. Genet. 2, 219-224.
61. van der Ven, K., Messer, L., van der Ven, H., Jeyendran, R. S. and Ober, C. (1996). Cystic fibrosis mutation screening in healthy men with reduced sperm quality. Hum. Reprod. 11, 513-517.
62. Weiser, N., Molenda, N., Urbanova, K., Bähler, M., Pieper, U., Oberleithner, H. and Schillers, H. (2011). Paracellular permeability of bronchial epithelium is controlled by CFTR. Cell. Physiol. Biochem. 28, 289-296.
63. Wilke, M., Buijs-Offerman, R. M., Aarbiou, J., Colledge, W. H., Sheppard, D. N., Touqui, L., Bot, A., Jorna, H., de Jonge, H. R. and Scholte, B. J. (2011). Mouse models of cystic fibrosis: phenotypic analysis and research applications. J. Cyst. Fibros. 10 Suppl. 2, S152-S171.
64. Xu, W. M., Shi, Q. X., Chen, W. Y., Zhou, C. X., Ni, Y., Rowlands, D. K., Yi Liu, G., Zhu, H., Ma, Z. G., Wang, X. F. et al. (2007). Cystic fibrosis transmembrane conductance regulator is vital to sperm fertilizing capacity and male fertility. Proc. Natl. Acad. Sci. USA 104, 9816-9821.
65. Yoo, D., Flagg, T. P., Olsen, O., Raghuram, V., Foskett, J. K. and Welling, P. A. (2004). Assembly and trafficking of a multiprotein ROMK (Kir 1.1) channel complex by PDZ interactions. J. Biol. Chem. 279, 6863-6873.
66. Yu, J., Chen, Z., Ni, Y. and Li, Z. (2012). CFTR mutations in men with congenital bilateral absence of the vas deferens (CBAVD): a systemic review and metaanalysis. Hum. Reprod. 27, 25-35.
67. Zeiher, B. G., Eichwald, E., Zabner, J., Smith, J. J., Puga, A. P., McCray, P. B., Jr, Capecchi, M. R., Welsh, M. J. and Thomas, K. R. (1995). A mouse model for the delta F508 allele of cystic fibrosis. J. Clin. Invest. 96, 2051-2064.
68. Zhou, Z., Wang, X., Li, M., Sohma, Y., Zou, X. and Hwang, T. C. (2005). High affinity ATP/ADP analogues as new tools for studying CFTR gating. J. Physiol. 569, 447-457.