Role of Dlg5/lp-dlg, a membrane-associated guanylate kinase family protein, in epithelial-mesenchymal transition in LLc-PK1 renal epithelial cells

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Sezaki, Takuhito ^a   Inada, Kohki ^a   Sogabe, Takayuki ^a   Kakuda, Kumiyo ^a   Tomiyama, Lucia ^a   Matsuno, Yohsuke ^a   Ichikawa, Takafumi ^a   Matsuo, Michinori ^a   Ueda, Kazumitsu ^a,b   Kioka, Noriyuki ^a  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; DISCS LARGE HOMOLOG 5 PROTEIN; FIBRONECTIN; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; ACTIN; CADHERIN; GUANYLATE KINASE; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; ENZYME ACTIVATION; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM CELL; GENE SILENCING; KIDNEY EPITHELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SWINE; ANIMAL; CELL STRAIN; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; RNA INTERFERENCE;

ACTINS; ANIMALS; CADHERINS; EPITHELIAL-MESENCHYMAL TRANSITION; FIBRONECTINS; GUANYLATE KINASE; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LLC-PK1 CELLS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA INTERFERENCE; RNA, SMALL INTERFERING; SWINE; TRANSFORMING GROWTH FACTOR BETA;

EID: 84859992632     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035519     Document Type: Article

References (54)

1. Reichert M, Muller T, Hunziker W, (2000) The PDZ domains of zonula occludens-1 induce an epithelial to mesenchymal transition of Madin-Darby canine kidney I cells. Evidence for a role of beta-catenin/Tcf/Lef signaling. J Biol Chem 275: 9492-9500.
2. Ryeom SW, Paul D, Goodenough DA, (2000) Truncation mutants of the tight junction protein ZO-1 disrupt corneal epithelial cell morphology. Mol Biol Cell 11: 1687-1696.
3. Nakamura H, Sudo T, Tsuiki H, Miyake H, Morisaki T, et al. (1998) Identification of a novel human homolog of the Drosophila dlg, P-dlg, specifically expressed in the gland tissues and interacting with p55. FEBS Lett 433: 63-67.
4. Friedrichs F, Henckaerts L, Vermeire S, Kucharzik T, Seehafer T, et al. (2008) The Crohn's disease susceptibility gene DLG5 as a member of the CARD interaction network. J Mol Med 86: 423-432.
5. Stoll M, Corneliussen B, Costello CM, Waetzig GH, Mellgard B, et al. (2004) Genetic variation in DLG5 is associated with inflammatory bowel disease. Nat Genet 36: 476-480.
6. Cullen G, O'Toole A, Keegan D, Sheahan K, Hyland JM, et al. (2007) Long-term clinical results of ileocecal resection for Crohn's disease. Inflamm Bowel Dis 13: 1369-1373.
7. Van Limbergen J, Wilson DC, Satsangi J, (2009) The genetics of Crohn's disease. Annual review of genomics and human genetics 10: 89-116.
8. Biank V, Friedrichs F, Babusukumar U, Wang T, Stoll M, et al. (2007) DLG5 R30Q variant is a female-specific protective factor in pediatric onset Crohn's disease. Am J Gastroenterol 102: 391-398.
9. Browning BL, Annese V, Barclay ML, Bingham SA, Brand S, et al. (2008) Gender-stratified analysis of DLG5 R30Q in 4707 patients with Crohn disease and 4973 controls from 12 Caucasian cohorts. J Med Genet 45: 36-42.
10. Lin Z, Poritz L, Franke A, Li TY, Ruether A, et al. (2009) Genetic association of DLG5 R30Q with familial and sporadic inflammatory bowel disease in men. Disease markers 27: 193-201.
11. Wakabayashi M, Ito T, Mitsushima M, Aizawa S, Ueda K, et al. (2003) Interaction of lp-dlg/KIAA0583, a membrane-associated guanylate kinase family protein, with vinexin and beta-catenin at sites of cell-cell contact. J Biol Chem 278: 21709-21714.
12. Kioka N, Ueda K, Amachi T, (2002) Vinexin, CAP/ponsin, ArgBP2: a Novel Adaptor Protein Family Regulating Cytoskeletal Organization and Signal Transduction. Cell Struct Funct 27: 1-7.
13. Nechiporuk T, Fernandez TE, Vasioukhin V, (2007) Failure of epithelial tube maintenance causes hydrocephalus and renal cysts in Dlg5-/- mice. Dev Cell 13: 338-350.
14. Chang Y, Klezovitch O, Walikonis RS, Vasioukhin V, Loturco JJ, (2010) Discs large 5 is required for polarization of citron kinase in mitotic neural precursors. Cell Cycle 9: 1990-1997.
15. Lee JM, Dedhar S, Kalluri R, Thompson EW, (2006) The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J Cell Biol 172: 973-981.
16. Thiery JP, Sleeman JP, (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142.
17. Kalluri R, Weinberg RA, (2009) The basics of epithelial-mesenchymal transition. J Clin Invest 119: 1420-1428.
18. Zeisberg M, Neilson EG, (2009) Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 119: 1429-1437.
19. Thiery JP, (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
20. Liu Y, (2004) Epithelial to mesenchymal transition in renal fibrogenesis: pathologic significance, molecular mechanism, and therapeutic intervention. J Am Soc Nephrol 15: 1-12.
21. Kalluri R, Neilson EG, (2003) Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784.
22. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA, (2009) Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119: 1438-1449.
23. Kioka N, Sakata S, Kawauchi T, Amachi T, Akiyama SK, et al. (1999) Vinexin: a novel vinculin-binding protein with multiple SH3 domains enhances actin cytoskeletal organization. J Cell Biol 144: 59-69.
24. Wang H, Ikeda S, Kanno S, Guang LM, Ohnishi M, et al. (2001) Activation of c-Jun amino-terminal kinase is required for retinoic acid-induced neural differentiation of P19 embryonal carcinoma cells. FEBS letters 503: 91-96.
25. Ura S, Masuyama N, Graves JD, Gotoh Y, (2001) MST1-JNK promotes apoptosis via caspase-dependent and independent pathways. Genes to cells: devoted to molecular & cellular mechanisms 6: 519-530.
26. Yamashita H, Ueda K, Kioka N, (2011) WAVE2 forms a complex with PKA and is involved in PKA enhancement of membrane protrusions. The Journal of biological chemistry 286: 3907-3914.
27. Umemoto T, Inomoto T, Ueda K, Hamaguchi M, Kioka N, (2009) v-Src-mediated Transformation Suppresses the Expression of Focal Adhesion Protein Vinexin. Cancer Lett 279: 22-29.
28. Mitsushima M, Ueda K, Kioka N, (2006) Vinexin beta regulates the phosphorylation of epidermal growth factor receptor on the cell surface. Genes Cells 11: 971-982.
29. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, et al. (2003) Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 284: F911-924.
30. Chen CL, Chou KJ, Lee PT, Chen YS, Chang TY, et al. (2010) Erythropoietin suppresses epithelial to mesenchymal transition and intercepts Smad signal transduction through a MEK-dependent mechanism in pig kidney (LLC-PK1) cell lines. Exp Cell Res 316: 1109-1118.
31. Heldin CH, Landstrom M, Moustakas A, (2009) Mechanism of TGF-beta signaling to growth arrest, apoptosis, and epithelial-mesenchymal transition. Curr Opin Cell Biol 21: 166-176.
32. Derynck R, Zhang YE, (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584.
33. Wrana JL, Attisano L, Wieser R, Ventura F, Massague J, (1994) Mechanism of activation of the TGF-beta receptor. Nature 370: 341-347.
34. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, et al. (1997) The MAD-related protein Smad7 associates with the TGFbeta receptor and functions as an antagonist of TGFbeta signaling. Cell 89: 1165-1173.
35. Kavsak P, Rasmussen RK, Causing CG, Bonni S, Zhu H, et al. (2000) Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF beta receptor for degradation. Mol Cell 6: 1365-1375.
36. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, et al. (1997) Identification of Smad7, a TGFbeta-inducible antagonist of TGF-beta signalling. Nature 389: 631-635.
37. Torok HP, Glas J, Endres I, Tonenchi L, Teshome MY, et al. (2009) Epistasis between Toll-like receptor-9 polymorphisms and variants in NOD2 and IL23R modulates susceptibility to Crohn's disease. Am J Gastroenterol 104: 1723-1733.
38. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, et al. (2002) Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350.
39. Smolen GA, Zhang J, Zubrowski MJ, Edelman EJ, Luo B, et al. (2010) A genome-wide RNAi screen identifies multiple RSK-dependent regulators of cell migration. Genes & development 24: 2654-2665.
40. Nakamura T, Furukawa Y, Nakagawa H, Tsunoda T, Ohigashi H, et al. (2004) Genome-wide cDNA microarray analysis of gene expression profiles in pancreatic cancers using populations of tumor cells and normal ductal epithelial cells selected for purity by laser microdissection. Oncogene 23: 2385-2400.
41. Taniuchi K, Nakagawa H, Nakamura T, Eguchi H, Ohigashi H, et al. (2005) Down-regulation of RAB6KIFL/KIF20A, a kinesin involved with membrane trafficking of discs large homologue 5, can attenuate growth of pancreatic cancer cell. Cancer Res 65: 105-112.
42. Boirivant M, Pallone F, Di Giacinto C, Fina D, Monteleone I, et al. (2006) Inhibition of Smad7 with a specific antisense oligonucleotide facilitates TGF-beta1-mediated suppression of colitis. Gastroenterology 131: 1786-1798.
43. Monteleone G, Kumberova A, Croft NM, McKenzie C, Steer HW, et al. (2001) Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. J Clin Invest 108: 601-609.
44. Neurath MF, Fuss I, Kelsall BL, Presky DH, Waegell W, et al. (1996) Experimental granulomatous colitis in mice is abrogated by induction of TGF-beta-mediated oral tolerance. J Exp Med 183: 2605-2616.
45. Powrie F, Carlino J, Leach MW, Mauze S, Coffman RL, (1996) A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J Exp Med 183: 2669-2674.
46. Mu Y, Gudey SK, Landstrom M, (2011) Non-Smad signaling pathways. Cell and tissue research.
47. Pallet N, Thervet E, Anglicheau D, (2012) c-Jun-N-Terminal Kinase Signaling Is Involved in Cyclosporine-Induced Epithelial Phenotypic Changes. Journal of transplantation 2012: 348604.
48. Medici D, Potenta S, Kalluri R, (2011) Transforming growth factor-beta2 promotes Snail-mediated endothelial-mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling. The Biochemical journal 437: 515-520.
49. Lv ZM, Wang Q, Wan Q, Lin JG, Hu MS, et al. (2011) The role of the p38 MAPK signaling pathway in high glucose-induced epithelial-mesenchymal transition of cultured human renal tubular epithelial cells. PloS one 6: e22806.
50. Li Y, Liu Y, Xu Y, Voorhees JJ, Fisher GJ, (2010) UV irradiation induces Snail expression by AP-1 dependent mechanism in human skin keratinocytes. Journal of dermatological science 60: 105-113.
51. Mu Y, Sundar R, Thakur N, Ekman M, Gudey SK, et al. (2011) TRAF6 ubiquitinates TGFbeta type I receptor to promote its cleavage and nuclear translocation in cancer. Nature communications 2: 330.
52. Sorrentino A, Thakur N, Grimsby S, Marcusson A, von Bulow V, et al. (2008) The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat Cell Biol 10: 1199-1207.
53. Yamashita M, Fatyol K, Jin C, Wang X, Liu Z, et al. (2008) TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta. Mol Cell 31: 918-924.
54. Zuo W, Chen YG, (2009) Specific activation of mitogen-activated protein kinase by transforming growth factor-beta receptors in lipid rafts is required for epithelial cell plasticity. Mol Biol Cell 20: 1020-1029.