ZO-2, a tight junction scaffold protein involved in the regulation of cell proliferation and apoptosis

Annals of the New York Academy of Sciences

Volumn 1257, Issue 1, 2012, Pages 133-141

  Gonzalez Mariscal, Lorenza ^a   Bautista, Pablo ^a   Lechuga, Susana ^a   Quiros, Miguel ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Apoptosis; Cell proliferation; Scaffold; Tight junctions; ZO 2

Indexed keywords

MESSENGER RNA; PROTEIN ZO2; WNT PROTEIN;

ACTIN FILAMENT; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CHEMICAL STRUCTURE; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HEARING IMPAIRMENT; HUMAN; MUTATION; NEOPLASM; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

EID: 84861976724     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06537.x     Document Type: Article

References (67)

1. Gumbiner, B., T. Lowenkopf & D. Apatira. 1991. Identification of a 160-kDa polypeptide that binds to the tight junction protein ZO-1. Proc. Natl. Acad. Sci. USA 88: 3460-3464.
2. Traweger, A., R. Fuchs, I.A. Krizbai, et al. 2003. The tight junction protein ZO-2 localizes to the nucleus and interacts with the heterogeneous nuclear ribonucleoprotein scaffold attachment factor-B. J. Biol. Chem. 278: 2692-2700.
3. Itoh, M., M. Furuse, K. Morita, et al. 1999. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J. Cell Biol. 147: 1351-1363.
4. Nayler, O., W. Stratling, J.P. Bourquin, et al. 1998. SAF-B protein couples transcription and pre-mRNA splicing to SAR/MAR elements. Nucleic Acids Res. 26: 3542-3549.
5. Glaunsinger, B.A., R.S. Weiss, S.S. Lee & R. Javier. 2001. Link of the unique oncogenic properties of adenovirus type 9 E4-ORF1 to a select interaction with the candidate tumor suppressor protein ZO-2. EMBO J. 20: 5578-5586.
6. Remue, E., K. Meerschaert, T. Oka, et al. 2010. TAZ interacts with zonula occludens-1 and -2 proteins in a PDZ-1 dependent manner. FEBS Lett. 584: 4175-4180.
7. Oka, T., E. Remue, K. Meerschaert, et al. 2010. Functional complexes between YAP2 and ZO-2 are PDZ domain-dependent, and regulate YAP2 nuclear localization and signalling. Biochem. J. 432: 461-472.
8. Itoh, M., K. Morita & S. Tsukita. 1999. Characterization of ZO-2 as a MAGUK family member associated with tight as well as adherens junctions with a binding affinity to occludin and alpha catenin. J. Biol. Chem. 274: 5981-5986.
9. Utepbergenov, D.I., A.S. Fanning & J.M. Anderson. 2006. Dimerization of the scaffolding protein ZO-1 through the second PDZ domain. J. Biol. Chem. 281: 24671-24677.
10. Chen, H., S. Tong, X. Li, et al. 2009. Structure of the second PDZ domain from human zonula occludens 2. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 65: 327-330.
11. Wu, J., Y. Yang, J. Zhang, et al. 2007. Domain-swapped dimerization of the second PDZ domain of ZO2 may provide a structural basis for the polymerization of claudins. J. Biol. Chem. 282: 35988-35999.
12. Singh, D., J.L. Solan, S.M. Taffet, et al. 2005. Connexin 43 interacts with zona occludens-1 and -2 proteins in a cell cycle stage-specific manner. J. Biol. Chem. 280: 30416-30421.
13. Meerschaert, K., M.P. Tun, E. Remue, et al. 2009. The PDZ2 domain of zonula occludens-1 and -2 is a phosphoinositide-binding domain. Cell Mol. Life Sci. 66: 3951-3966.
14. Ebnet, K., C.U. Schulz, M.K. Meyer Zu Brickwedde, et al. 2000. Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J. Biol. Chem. 275: 27979-27988.
15. Itoh, M., H. Sasaki, M. Furuse, et al. 2001. Junctional adhesion molecule (JAM) binds to PAR-3: a possible mechanism for the recruitment of PAR-3 to tight junctions. J. Cell Biol. 154: 491-497.
16. Lechuga, S., L. Alarcon, J. Solano, et al. 2010. Identification of ZASP, a novel protein associated to Zona occludens-2. Exp. Cell Res. 316: 3124-3139.
17. Tkachuk, N., S. Tkachuk, M. Patecki, et al. 2011. The tight junction protein ZO-2 and Janus kinase 1 mediate intercellular communications in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 410: 531-536.
18. Kausalya, P.J., D.C. Phua & W. Hunziker. 2004. Association of ARVCF with zonula occludens (ZO)-1 and ZO-2: binding to PDZ-domain proteins and cell-cell adhesion regulate plasma membrane and nuclear localization of ARVCF. Mol. Biol. Cell 15: 5503-5515.
19. Lye, M.F., A.S. Fanning, Y. Su, et al. 2010. Insights into regulated ligand-binding sites from the structure of ZO-1 Src homology 3-guanylate kinase module. J. Biol. Chem. 285: 13907-13917.
20. Wittchen, E.S., J. Haskins & B.R. Stevenson. 1999. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J. Biol. Chem. 274: 35179-35185.
21. Muller, S.L., M. Portwich, A. Schmidt, et al. 2005. The tight junction protein occludin and the adherens junction protein alpha-catenin share a common interaction mechanism with ZO-1. J. Biol. Chem. 280: 3747-3756.
22. Schmidt, A., D.I. Utepbergenov, S.L. Mueller, et al. 2004. Occludin binds to the SH3-hinge-GuK unit of zonula occludens protein 1: potential mechanism of tight junction regulation. Cell Mol. Life Sci. 61: 1354-1365.
23. Mattagajasingh, S.N., S.C. Huang, J.S. Hartenstein & E.J. Benz, Jr. 2000. Characterization of the interaction between protein 4.1R and ZO-2. A possible link between the tight junction and the actin cytoskeleton. J. Biol. Chem. 275: 30573-30585.
24. Lallena, M.J. & I. Correas. 1997. Transcription-dependent redistribution of nuclear protein 4.1 to SC35-enriched nuclear domains. J. Cell Sci. 110(Pt 2): 239-247.
25. Betanzos, A., M. Huerta, E. Lopez-Bayghen, et al. 2004. The tight junction protein ZO-2 associates with Jun, Fos, and C/EBP transcription factors in epithelial cells. Exp. Cell Res. 292: 51-66.
26. Metais, J.Y., C. Navarro, M.J. Santoni, et al. 2005. hScrib interacts with ZO-2 at the cell-cell junctions of epithelial cells. FEBS Lett. 579: 3725-3730.
27. Cordenonsi, M., F. D'Atri, E. Hammar, et al. 1999. Cingulin contains globular and coiled-coil domains and interacts with ZO-1, ZO-2, ZO-3, and myosin. J. Cell Biol. 147: 1569-1582.
28. Yamazaki, Y., K. Umeda, M. Wada, et al. 2008. ZO-1- and ZO-2-dependent integration of myosin-2 to epithelial zonula adherens. Mol. Biol. Cell 19: 3801-3811.
29. Avila-Flores, A., E. Rendon-Huerta, J. Moreno, et al. 2001. Tight-junction protein zonula occludens 2 is a target of phosphorylation by protein kinase C. Biochem. J. 360: 295-304.
30. Saito, K., K. Enya, C. Oneyama, et al. 2008. Proteomic identification of ZO-1/2 as a novel scaffold for Src/Csk regulatory circuit. Biochem. Biophys. Res. Commun. 366: 969-975.
31. Jaramillo, B.E., A. Ponce, J. Moreno, et al. 2004. Characterization of the tight junction protein ZO-2 localized at the nucleus of epithelial cells. Exp. Cell Res. 297: 247-258.
32. Huerta, M., R. Munoz, R. Tapia, et al. 2007. Cyclin D1 is transcriptionally down-regulated by ZO-2 via an E box and the transcription factor c-Myc. Mol. Biol. Cell 18: 4826-4836.
33. Huang, H.Y., R. Li, Q. Sun, et al. 2002. [LIM protein KyoT2 interacts with human tight junction protein ZO-2-i3]. Yi. Chuan Xue. Bao. 29: 953-958.
34. Gottardi, C.J., M. Arpin, A.S. Fanning & D. Louvard. 1996. The junction-associated protein, zonula occludens-1, localizes to the nucleus before the maturation and during the remodeling of cell-cell contacts. Proc. Natl. Acad. Sci. USA 93: 10779-10784.
35. Islas, S., J. Vega, L. Ponce & L. Gonzalez-Mariscal. 2002. Nuclear localization of the tight junction protein ZO-2 in epithelial cells. Exp. Cell Res. 274: 138-148.
36. Tapia, R., M. Huerta, S. Islas, et al. 2009. Zona occludens-2 inhibits cyclin D1 expression and cell proliferation and exhibits changes in localization along the cell cycle. Mol. Biol. Cell 20: 1102-1117.
37. Lopez-Bayghen, E., B. Jaramillo, M. Huerta, et al. 2006. TJ proteins that make round trips to the nucleus. In Tight Junctions. L. Gonzalez-Mariscal, Ed.: 76-100. Springer Science and Landes Bioscience. New York and Georgetown.
38. Gonzalez-Mariscal, L., A. Ponce, L. Alarcon & B.E. Jaramillo. 2006. The tight junction protein ZO-2 has several functional nuclear export signals. Exp. Cell Res. 312: 3323-3335.
39. Chamorro, D., L. Alarcon, A. Ponce, et al. 2009. Phosphorylation of zona occludens-2 by protein kinase C epsilon regulates its nuclear exportation. Mol. Biol. Cell 20: 4120-4129.
40. Oka, T., A.P. Schmitt & M. Sudol. 2012. Opposing roles of angiomotin-like-1 and zona occludens-2 on pro-apoptotic function of YAP. Oncogene 31: 128-134.
41. Wang, H., L. Luan, T. Ding, et al. 2011. Dynamics of zonula occludens-2 expression during pre-implantation embryonic development in the hamster. Theriogenology 76: 678-686.
42. Sheth, B., R.L. Nowak, R. Anderson, et al. 2008. Tight junction protein ZO-2 expression and relative function of ZO-1 and ZO-2 during mouse blastocyst formation. Exp. Cell Res. 314: 3356-3368.
43. Adams, L.D., J.M. Lemire & S.M. Schwartz. 1999. A systematic analysis of 40 random genes in cultured vascular smooth muscle subtypes reveals a heterogeneity of gene expression and identifies the tight junction gene zonula occludens 2 as a marker of epithelioid "pup" smooth muscle cells and a participant in carotid neointimal formation. Arterioscler. Thromb. Vasc. Biol. 19: 2600-2608.
44. Kusch, A., S. Tkachuk, N. Tkachuk, et al. 2009. The tight junction protein ZO-2 mediates proliferation of vascular smooth muscle cells via regulation of Stat1. Cardiovasc. Res. 83: 115-122.
45. Adachi, M., A. Inoko, M. Hata, et al. 2006. Normal establishment of epithelial tight junctions in mice and cultured cells lacking expression of ZO-3, a tight-junction MAGUK protein. Mol. Cell Biol. 26: 9003-9015.
46. Umeda, K., J. Ikenouchi, S. Katahira-Tayama, et al. 2006. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight junction strand formation. Cell 126: 741-754.
47. Hernandez, S., M.B. Chavez & L. Gonzalez-Mariscal. 2007. ZO-2 silencing in epithelial cells perturbs the gate and fence function of tight junctions and leads to an atypical monolayer architecture. Exp. Cell Res. 313: 1533-1547.
48. Van Itallie, C.M., A.S. Fanning, A. Bridges & J.M. Anderson. 2009. ZO-1 stabilizes the tight junction solute barrier through coupling to the perijunctional cytoskeleton. Mol. Biol. Cell 20: 3930-3940.
49. Xu, J., P.J. Kausalya, D.C. Phua, et al. 2008. Early embryonic lethality of mice lacking ZO-2, but Not ZO-3, reveals critical and non-redundant roles for individual zonula occludens proteins in mammalian development. Mol. Cell Biol. 28: 1669-1678.
50. Xu, J., F. Anuar, S.M. Ali, et al. 2009. Zona occludens-2 is critical for blood-testis barrier integrity and male fertility. Mol. Biol. Cell 20: 4268-4277.
51. Kiener, T.K., I. Sleptsova-Friedrich & W. Hunziker. 2007. Identification, tissue distribution, and developmental expression of tjp1/zo-1, tjp2/zo-2 and tjp3/zo-3 in the zebrafish, Danio rerio. Gene Expr. Patterns. 7: 767-776.
52. Jho, E.H., T. Zhang, C. Domon, et al. 2002. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell Biol. 22: 1172-1183.
53. Traweger, A., C. Lehner, A. Farkas, et al. 2008. Nuclear Zonula occludens-2 alters gene expression and junctional stability in epithelial and endothelial cells. Differentiation 76: 99-106.
54. Bauer, H., J. Zweimueller-Mayer, P. Steinbacher, et al. 2010. The dual role of zonula occludens (ZO) proteins. J. Biomed. Biotechnol. 2010: 402593.
55. Osborne, S.L., C.L. Thomas, S. Gschmeissner & G. Schiavo. 2001. Nuclear PtdIns(4, 5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J. Cell Sci. 114: 2501-2511.
56. Carlton, V.E., B. Z. Harris, E.G. Puffenberger, et al. 2003. Complex inheritance of familial hypercholanemia with associated mutations in TJP2 and BAAT. Nat. Genet. 34: 91-96.
57. Walsh, T., S.B. Pierce, D.R. Lenz, et al. 2010. Genomic duplication and overexpression of TJP2/ZO-2 leads to altered expression of apoptosis genes in progressive non-syndromic hearing loss DFNA51. Am. J. Hum. Genet. 87: 101-109.
58. Op de Beeck, K., J. Schacht & G. Van Camp. 2011. Apoptosis in acquired and genetic hearing impairment: the programmed death of the hair cell. Hearing Res. 281: 18-27.
59. Willott, E., M.S. Balda, A.S. Fanning, et al. 1993. The tight junction protein ZO-1 is homologous to the Drosophila discs-large tumor suppressor protein of septate junctions. Proc. Natl. Acad. Sci. USA 90: 7834-7838.
60. Latorre, I.J., M.H. Roh, K.K. Frese, et al. 2005. Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell Sci. 118: 4283-4293.
61. Paschoud, S., M. Bongiovanni, J.C. Pache & S. Citi. 2007. Claudin-1 and claudin-5 expression patterns differentiate lung squamous cell carcinomas from adenocarcinomas. Mod. Pathol. 20: 947-954.
62. Martin, T.A., G. Watkins, R.E. Mansel & W.G. Jiang. 2004. Loss of tight junction plaque molecules in breast cancer tissues is associated with a poor prognosis in patients with breast cancer. Eur. J. Cancer 40: 2717-2725.
63. Fink, C., R. Weigel, T. Hembes, et al. 2006. Altered expression of ZO-1 and ZO-2 in Sertoli cells and loss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 8: 1019-1027.
64. Chlenski, A., K.V. Ketels, M.S. Tsao, et al. 1999. Tight junction protein ZO-2 is differentially expressed in normal pancreatic ducts compared to human pancreatic adenocarcinoma. Int. J. Cancer 82: 137-144.
65. Chlenski, A., K.V. Ketels, J.L. Engeriser, et al. 1999. zo-2 gene alternative promoters in normal and neoplastic human pancreatic duct cells. Int. J. Cancer 83: 349-358.
66. Wang, Y., Q. Yu, A.H. Cho, et al. 2005. Survey of differentially methylated promoters in prostate cancer cell lines. Neoplasia 7: 748-760.
67. Chlenski, A., K.V. Ketels, G.I. Korovaitseva, et al. 2000. Organization and expression of the human zo-2 gene (tjp-2) in normal and neoplastic tissues. Biochim. Biophys. Acta 1493: 319-324.