Hippo pathway elements Co-localize with Occludin: A possible sensor system in pancreatic epithelial cells

Tissue Barriers

Volumn 3, Issue 3, 2015, Pages 1-14

  Cravo, Ana Santos ^a   Carter, Edward ^a   Erkan, Mert ^b   Harvey, Emma ^a   Furutani Seiki, Makoto ^a   Mrsny, Randall ^a  

^a University of Bath   (United Kingdom)

^b KOÇ UNIVERSITY   (Turkey)

Author keywords

dobutamine; occludin; pancreatic cancer cells; tight junctions; YAP

Indexed keywords

DOBUTAMINE; OCCLUDIN; PROTEIN KINASE; PROTEIN KINASE C ZETA; PROTEIN KINASE HIPPO; TRANSCRIPTION FACTOR YAP1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELL MEMBRANE PERMEABILITY; CELL POLARITY; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRIC RESISTANCE; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NONHUMAN; PANCREAS CELL; PROTEIN ANALYSIS; TIGHT JUNCTION; WNT SIGNALING PATHWAY;

EID: 84981240003     PISSN: 21688362     EISSN: 21688370     Source Type: Journal    
DOI: 10.1080/21688370.2015.1037948     Document Type: Article

References (58)

1. M.Aragona, T.Panciera, A.Manfrin S.Giulitti, F.Michielin, N.Elvassore, S.Dupont, S.Piccolo. A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 2013; 154:1047-59; PMID:23954413; http://dx.doi.org/10.1016/j.cell.2013.07.042
2. M.S.Balda, J.A.Whitney, C.Flores, S.Gonzalez, M.Cereijido, K.Matter. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol 1996; 134:1031-49; PMID:8769425; http://dx.doi.org/10.1083/jcb.134.4.1031
3. Y.Bao, Y.Hata, M.Ikeda, K.Withanage. Mammalian Hippo pathway: from development to cancer and beyond. J Biochem 2011; 149:361-79; PMID:21324984; http://dx.doi.org/10.1093/jb/mvr021
4. M.Bruewer, A.Luegering, T.Kucharzik, C.A.Parkos, J.L.Madara, A.M.Hopkins, A.Nusrat. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol 2003; 171:6164-72; PMID:14634132; http://dx.doi.org/10.4049/jimmunol.171.11.6164
5. M.Bruewer, S.Samarin, A.Nusrat. Inflammatory bowel disease and the apical junctional complex. Ann N Y Acad Sci 2006; 1072:242-52; PMID:17057204; http://dx.doi.org/10.1196/annals.1326.017
6. S.W.Chan, C.J.Lim, Y.F.Chong, A.V.Pobbati, C.Huang, W.Hong. Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J Biol Chem 2011; 286:7018-26; PMID:21224387; http://dx.doi.org/10.1074/jbc.C110.212621
7. L.M.Chen, P.G.Loh, H.W.Song. Structural and functional insights into the TEAD-YAP complex in the Hippo signaling pathway. Protein Cell 2010; 1:1073-83; PMID:21213102; http://dx.doi.org/10.1007/s13238-010-0138-3
8. X.Chen, S.T.Cheung, S.So, S.T.Fan, C.Barry, J.Higgins, K.M.Lai, J.Ji, S.Dudoit, I.O.Ng, et al. Gene expression patterns in human liver cancers. Mol Biol Cell 2002a; 13:1929-39; PMID:12058060; http://dx.doi.org/10.1091/mbc.02-02-0023.
9. Y.H.Chen, Q.Lu. Association of nonreceptor tyrosine kinase c-yes with tight junction protein occludin by coimmunoprecipitation assay. Methods Mol Biol 2003; 218:127-32; PMID:12616717
10. Y.H.Chen, Q.Lu, D.A.Goodenough, B.Jeansonne. Nonreceptor tyrosine kinase c-Yes interacts with occludin during tight junction formation in canine kidney epithelial cells. Mol Biol Cell 2002b; 13:1227-37; PMID:11950934; http://dx.doi.org/10.1091/mbc.01-08-0423
11. J.Cording, J.Berg, N.Kading, C.Bellmann, C.Tscheik, J.K.Westphal, S.Milatz, D.Gunzel, H.Wolburg, J.Piontek, et al. In tight junctions, claudins regulate the interactions between occludin, tricellulin and marvelD3, which, inversely, modulate claudin oligomerization. J Cell Sci 2013; 126:554-64; PMID:23203797; http://dx.doi.org/10.1242/jcs.114306
12. V.Dodane, B.Kachar. Identification of isoforms of G proteins and PKC that colocalize with tight junctions. J Membrane Biol 1996; 149:199-209; PMID:8801352; http://dx.doi.org/10.1007/s002329900020
13. M.J.Dorfel, O.Huber. Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. J Biomed Biotechnol 2012; 2012:807356; PMID:22315516; http://dx.doi.org/10.1155/2012/807356
14. K.L.Edelblum, J.R.Turner. The tight junction in inflammatory disease: communication breakdown. Curr Opin Pharmacol 2009; 9:715-20; PMID:19632896; http://dx.doi.org/10.1016/j.coph.2009.06.022
15. S.Etienne-Manneville, A.Hall. Rho GTPases in cell biology. Nature 2002; 420:629-35; PMID:12478284; http://dx.doi.org/10.1038/nature01148
16. A.E.Farkas, C.T.Capaldo, A.Nusrat. Regulation of epithelial proliferation by tight junction proteins. Ann N Y Acad Sci 2012; 1258:115-24; PMID:22731724; http://dx.doi.org/10.1111/j.1749-6632.2012.06556.x
17. M.Furuse. Knockout animals and natural mutations as experimental and diagnostic tool for studying tight junction functions in vivo. Biochim Biophys Acta 2009; 1788:813-9; PMID:18706387; http://dx.doi.org/10.1016/j.bbamem.2008.07.017
18. M.Furuse. Molecular basis of the core structure of tight junctions. Cold Spring Harb Perspect Biol 2010; 2:a002907; PMID:20182608; http://dx.doi.org/10.1101/cshperspect.a002907
19. M.Furuse, T.Hirase, M.Itoh, A.Nagafuchi, S.Yonemura, S.Tsukita, S.Tsukita. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 1993; 123:1777-88; PMID:8276896; http://dx.doi.org/10.1083/jcb.123.6.1777
20. B.M.Gumbiner, N.G.Kim. The Hippo-YAP signaling pathway and contact inhibition of growth. J Cell Sci 2014; 127:709-17; PMID:24532814; http://dx.doi.org/10.1242/jcs.140103
21. K.F.Harvey, X.Zhang, D.M.Thomas. The Hippo pathway and human cancer. Nat Rev Cancer 2013; 13:246-57; PMID:23467301; http://dx.doi.org/10.1038/nrc3458
22. J.Ikenouchi, M.Furuse, K.Furuse, H.Sasaki, S.Tsukita, S.Tsukita. Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J Cell Biol 2005; 171:939-45; PMID:16365161; http://dx.doi.org/10.1083/jcb.200510043
23. J.Ikenouchi, H.Sasaki, S.Tsukita, M.Furuse, S.Tsukita. Loss of occludin affects tricellular localization of tricellulin. Mol Biol Cell 2008; 19:4687-93; PMID:18768749; http://dx.doi.org/10.1091/mbc.E08-05-0530
24. T.Ishizaki, M.Uehata, I.Tamechika, J.Keel, K.Nonomura, M.Maekawa, S.Narumiya. Pharmacological properties of Y-27632, a specific inhibitor of rho-associated kinases. Mol Pharmacol 2000; 57:976-83; PMID:10779382
25. R.Johnson, G.Halder. The two faces of Hippo: targeting the Hippo pathway for regenerative medicine and cancer treatment. Nat Rev Drug Discov 2014; 13:63-79; PMID:24336504; http://dx.doi.org/10.1038/nrd4161
26. Y.W.Kim, H.F.Kern, T.D.Mullins, M.J.Koriwchak, R.S.Metzgar. Characterization of clones of a human pancreatic adenocarcinoma cell-line representing different stages of differentiation. Pancreas 1989; 4:353-62; PMID:2734279; http://dx.doi.org/10.1097/00006676-198906000-00013
27. T.Kojima, A.Takasawa, D.Kyuno, T.Ito, H.Yamaguchi, K.Hirata, M.Tsujiwaki, M.Murata, S.Tanaka, N.Sawada. Downregulation of tight junction-associated MARVEL protein marvelD3 during epithelial-mesenchymal transition in human pancreatic cancer cells. Exp Cell Re 2011; 317:2288-98; PMID:21763689; http://dx.doi.org/10.1016/j.yexcr.2011.06.020
28. T.Kubo, Y.Kuroda, A.Kokubu, F.Hosoda, Y.Arai, N.Hiraoka, S.Hirohashi, T.Shibata. Resequencing analysis of the human tyrosine kinase gene family in pancreatic cancer. Pancreas 2009; 38:e200-06; PMID:19893451; http://dx.doi.org/10.1097/MPA.0b013e3181b8feb0
29. S.Lim, J.W.Choi, H.S.Kim, Y.H.Kim, K.Yea, K.Heo, J.H.Kim, S.H.Kim, M.Song, J.I.Kim, et al. A myristoylated pseudosubstrate peptide of PKC-zeta induces degranulation in HMC-1 cells independently of PKC-zeta activity. Life Sci 2008; 82:733-40; PMID:18289606; http://dx.doi.org/10.1016/j.lfs.2008.01.005
30. C.Mariano, H.Sasaki, D.Brites, M.A.Brito. A look at tricellulin and its role in tight junction formation and maintenance (vol 90, pg 787. 2011). Eur J Cell Biol 2011; 90:1061-1061; PMID:21868126; http://dx.doi.org/10.1016/j.ejcb.2011.09.001
31. T.A.Martin, R.E.Mansel, W.G.Jiang. Loss of occludin leads to the progression of human breast cancer. Int J Mol Med 2010; 26:723-34; PMID:20878095; http://dx.doi.org/10.3892/ijmm_00000519
32. K.Matter, M.S.Balda. Signalling to and from tight junctions. Nat Rev Mol Cell Bio 2003; 4:225-36; PMID:12612641; http://dx.doi.org/10.1038/nrm1055
33. B.D.Matthews, D.R.Overby, R.Mannix, D.E.Ingber. Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J Cell Sci 2006; 119:508-18; PMID:16443749; http://dx.doi.org/10.1242/jcs.02760
34. A.Nusrat, J.A.Chen, C.S.Foley, T.W.Liang, J.Tom, M.Cromwell, C.Quan, R.J.Mrsny. The coiled-coil domain of occludin can act to organize structural and functional elements of the epithelial tight junction. J Biol Chem 2000; 275:29816-22; PMID:10887180; http://dx.doi.org/10.1074/jbc.M002450200
35. M.Osanai, M.Murata, N.Nishikiori, H.Chiba, T.Kojima, N.Sawada. Epigenetic silencing of occludin promotes tumorigenic and metastatic properties of cancer cells via modulations of unique sets of apoptosis-associated genes. Cancer Res 2006; 66:9125-33; PMID:16982755; http://dx.doi.org/10.1158/0008-5472.CAN-06-1864
36. D.Pan. The hippo signaling pathway in development and cancer. Dev Cell 2010; 19:491-505; PMID:20951342; http://dx.doi.org/10.1016/j.devcel.2010.09.011
37. C.L.C.Poon, J.I.Lin, X.M.Zhang, K.F.Harvey. The sterile 20-like kinase Tao-1 controls tissue growth by regulating the Salvador-Warts-Hippo pathway. Dev Cell 2011; 21:896-906; PMID:22075148; http://dx.doi.org/10.1016/j.devcel.2011.09.012
38. D.R.Raleigh, D.M.Boe, D.Yu, C.R.Weber, A.M.Marchiando, E.M.Bradford, Y.M.Wang, L.C.Wu, E.E.Schneeberger, L.Shen, et al. Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. J Cell Biol 2011; 193:565-82; PMID:21536752; http://dx.doi.org/10.1083/jcb.201010065
39. M.Saitou, M.Furuse, H.Sasaki, J.D.Schulzke, M.Fromm, H.Takano, T.Noda, S.Tsukita. Complex phenotype of mice lacking occludin, a component of tight junction strands. Mol Biol Cell 2000; 11:4131-42; PMID:11102513; http://dx.doi.org/10.1091/mbc.11.12.4131
40. N.Sawada. Tight junction-related human diseases. Pathol Int 2013 63:1-12; PMID:23356220; http://dx.doi.org/10.1111/pin.12021
41. K.Schlegelmilch, M.Mohseni, O.Kirak, J.Pruszak, J.R.Rodriguez, D.Zhou, B.T.Kreger, V.Vasioukhin, J.Avruch, T.R.Brummelkamp, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011; 144:782-95; PMID:21376238; http://dx.doi.org/10.1016/j.cell.2011.02.031
42. D.Shao, P.Zhai, D.P.Del Re, S.Sciarretta, N.Yabuta, H.Nojima, D.S.Lim, D.Pan, J.Sadoshima. A functional interaction between Hippo-YAP signalling and FoxO1 mediates the oxidative stress response. Nat Commun 2014; 5:3315; PMID:24525530
43. L.Shen, C.R.Weber, D.R.Raleigh, D.Yu, J.R.Tumer. Tight, junction pore and leak pathways: a dynamic duo. Annu Rev Physiol 2011; 73:283-309; PMID:20936941; http://dx.doi.org/10.1146/annurev-physiol-012110-142150
44. S.R.Shi, B.Chaiwun, L.Young, R.J.Cote, C.R.Taylor. Antigen retrieval technique utilizing citrate buffer or urea solution for immunohistochemical demonstration of androgen receptor in formalin-fixed paraffin sections. J Histochem Cytochem 1993; 41:1599-604; PMID:7691930; http://dx.doi.org/10.1177/41.11.7691930
45. D.Spadaro, R.Tapia, P.Pulimeno, S.Citi. The control of gene expression and cell proliferation by the epithelial apical junctional complex. Essays Biochem 2012; 53:83-93; PMID:22928510; http://dx.doi.org/10.1042/bse0530083
46. R.O.Stuart, S.K.Nigam. Regulated assembly of tight junctions by Protein-Kinase-C. Proc Natl Acad Sci U S A 1995; 92:6072-6; PMID:7597083; http://dx.doi.org/10.1073/pnas.92.13.6072
47. M.Sudol. Yes-associated protein (YAP65) is a proline-rich phosphoprotein that binds to the SH3 domain of the Yes proto-oncogene product. Oncogene 1994; 9:2145-52; PMID:8035999
48. A.Suzuki, T.Yamanaka, T.Hirose, N.Manabe, K.Mizuno, M.Shimizu, K.Akimoto, Y.Izumi, T.Ohnishi, S.Ohno. Atypical protein kinase C is involved in the evolutionarily conserved PAR protein complex and plays a critical role in establishing epithelia-specific junctional structures. J Cell Biol 2001; 152:1183-96; PMID:11257119; http://dx.doi.org/10.1083/jcb.152.6.1183
49. M.H.Tan, T.M.Chu. Characterization of the tumorigenic and metastatic properties of a human pancreatic tumor cell line (AsPc1) implanted orthotopically into nude mice. Tumour Biol 1985; 6:89-98; PMID:4023565
50. H.Tobioka, H.Isomura, Y.Kokai, Y.Tokunaga, J.Yamaguchi, N.Sawada. Occludin expression decreases with the progression of human endometrial carcinoma. Hum Pathol 2004a; 35:159-164; PMID:14991532; http://dx.doi.org/10.1016/j.humpath.2003.09.013
51. H.Tobioka, Y.Tokunaga, H.Isomura, Y.Kokai, J.Yamaguchi, N.Sawada. Expression of occludin, a tight-junction-associated protein, in human lung carcinomas. Virchows Arch 2004b; 445:472-6; PMID:15232740; http://dx.doi.org/10.1007/s00428-004-1054-9
52. A.Vassilev, K.J.Kaneko, H.Shu, Y.Zhao, M.L.DePamphilis. TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev 2001; 15:1229-41; PMID:11358867; http://dx.doi.org/10.1101/gad.888601
53. N.C.Veitch. Horseradish peroxidase: a modern view of a classic enzyme. Phytochemistry 2004; 65:249-59; PMID:14751298; http://dx.doi.org/10.1016/j.phytochem.2003.10.022
54. A.S.Yu, K.M.McCarthy, S.A.Francis, J.M.McCormack, J.Lai, R.A.Rogers, R.D.Lynch, E.E.Schneeberger. Knockdown of occludin expression leads to diverse phenotypic alterations in epithelial cells. Am J Physiol Cell Physiol 2005; 288:C1231-41; PMID:15689410; http://dx.doi.org/10.1152/ajpcell.00581.2004
55. F.X.Yu, K.L.Guan. The Hippo pathway: regulators and regulations. Gene Dev 2013; 27:355-71; PMID:23431053; http://dx.doi.org/10.1101/gad.210773.112
56. X.D.Tan,, Y.Tamori,, H.Egami,, S.Ishikawa,, T.Kurizaki,, E.Takai,, M.Hirota,, and M.Ogawa, (2004). Analysis of invasion-metastasis mechanism in pancreatic cancer: Involvement of tight junction transmembrane protein occludin and MEK/ERK signal transduction pathway in cancer cell dissociation. Oncol Rep 11, 993–998.
57. B.Cerruti,, A.Puliafito,, A.M.Shewan,, W.Yu,, A.N.Combes,, M.H.Little,, F.Chianale,, L.Primo,, G.Serini,, K.E.Mostov,, (2013). Polarity, cell division, and out-of-equilibrium dynamics control the growth of epithelial structures. The Journal of Cell Biology 203, 359–372.
58. M.Erkan,, J.Kleeff,, I.Esposito,, T.Giese,, K.Ketterer,, M.W.Buchler,, N.A.Giese,, and H.Friess, (2005). Loss of BNIP3 expression is a late event in pancreatic cancer contributing to chemoresistance and worsened prognosis. Oncogene 24, 4421–4432.