Delineation of the key aspects in the regulation of epithelial monolayer formation

Molecular and Cellular Biology

Volumn 33, Issue 13, 2013, Pages 2535-2550

  Aschauer, Lydia ^a   Gruber, Leonhard N ^a   Pfaller, Walter ^a   Limonciel, Alice ^a   Athersuch, Toby J ^b   Cavill, Rachel ^b   Khan, Abdulhameed ^c   Gstraunthaler, Gerhard ^a   Grillari, Johannes ^c,e   Grillari, Regina ^c,e   Hewitt, Philip ^d   Leonard, Martin O ^f   Wilmes, Anja ^a   Jennings, Paul ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF AGRICULTURAL SCIENCES   (Austria)

^d Merck Serono GmbH   (Germany)

^e Evercyte GmbH   (Australia)

^f UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MYC PROTEIN; PROTEIN P53; TRANSCRIPTION FACTOR FKHR; UVOMORULIN;

AEROBIC METABOLISM; ARTICLE; BIOGENESIS; CELL ADHESION; CELL CYCLE PHASE; CELL JUNCTION; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; ENERGY METABOLISM; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FUNCTIONAL ASSESSMENT; GENE EXPRESSION; GENETIC ASSOCIATION; HOMEOSTASIS; HUMAN; HUMAN CELL; KIDNEY EPITHELIUM; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE FUNCTION; METABOLOMICS; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MONOLAYER CULTURE; PRIORITY JOURNAL; TIGHT JUNCTION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

EID: 84880682418     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01435-12     Document Type: Article

References (76)

1. Jennings P, Koppelstaetter C, Lechner J, Pfaller W. 2008. Renal culture models: contribution to the understanding of nephrotoxic mechanisms, p. 223-250. In Broe ME, Porter GA (ed), Clinical nephrotoxins: renal injury from drugs and chemicals, 3rd ed. Springer, New York, NY.
2. Muto S, Hata M, Taniguchi J, Tsuruoka S, Moriwaki K, Saitou M, Furuse K, Sasaki H, Fujimura A, Imai M, Kusano E, Tsukita S, Furuse M. 2010. Claudin-2-deficient mice are defective in the leaky and cation-selective paracellular permeability properties of renal proximal tubules. Proc. Natl. Acad. Sci. U. S. A. 107:8011-8016.
3. Gstraunthaler G, Pfaller W, Kotanko P. 1985. Interrelation between oxygen consumption and Na-K-ATPase activity in rat renal proximal tubule suspension. Ren. Physiol. 8:38-44.
4. Pfaller W, Gstraunthaler G. 1998. Nephrotoxicity testing in vitro-what we know and what we need to know. Environ. Health Perspect 106(Suppl.2):559-569.
5. Jennings P. 2009. Epithelial cell cultures as tools to study human disease and the adverse effects of pharmaceuticals and chemicals. Habilitation thesis. Medizinische Universität Innsbruck, Innsbruck, Austria.
6. Wilmes A, Crean D, Aydin S, Pfaller W, Jennings P, Leonard MO. 2011. Identification and dissection of the Nrf2 mediated oxidative stress pathway in human renal proximal tubule toxicity. Toxicol. In Vitro 25:613-622.
7. Lima WR, Parreira KS, Devuyst O, Caplanusi A, N'Kuli F, Marien B, Van Der Smissen P, Alves PM, Verroust P, Christensen EI, Terzi F, Matter K, Balda MS, Pierreux CE, Courtoy PJ. 2010. ZONAB promotes proliferation and represses differentiation of proximal tubule epithelial cells. J. Am. Soc. Nephrol. 21:478-488.
8. Moncada S, Higgs EA, Colombo SL. 2012. Fulfilling the metabolic requirements for cell proliferation. Biochem. J. 446:1-7.
9. Ullrich SJ, Anderson CW, Mercer WE, Appella E. 1992. The p53 tumor suppressor protein, a modulator of cell proliferation. J. Biol. Chem. 267: 15259-15262.
10. Syed V, Mak P, Du C, Balaji KC. 2008. Beta-catenin mediates alteration in cell proliferation, motility and invasion of prostate cancer cells by differential expression of E-cadherin and protein kinase D1. J. Cell. Biochem. 104:82-95.
11. Miyoshi J, Takai Y. 2005. Molecular perspective on tight-junction assembly and epithelial polarity. Adv. Drug Deliv. Rev. 57:815-855.
12. Balda MS, Garrett MD, Matter K. 2003. The ZO-1-associated Y-box factor ZONAB regulates epithelial cell proliferation and cell density. J. Cell Biol. 160:423-432.
13. Jennings P, Koppelstaetter C, Aydin S, Abberger T, Wolf AM, Mayer G, Pfaller W. 2007. Cyclosporine A induces senescence in renal tubular epithelial cells. Am. J. Physiol. Renal Physiol. 293:F831-F838.
14. Wieser M, Stadler G, Jennings P, Streubel B, Pfaller W, Ambros P, Riedl C, Katinger H, Grillari J, Grillari-Voglauer R. 2008. hTERT alone immortalizes epithelial cells of renal proximal tubules without changing their functional characteristics. Am. J. Physiol. Renal Physiol. 295:F1365-1375.
15. Zidek N, Hellmann J, Kramer PJ, Hewitt PG. 2007. Acute hepatotoxicity: a predictive model based on focused Illumina microarrays. Toxicol. Sci. 99:289-302.
16. Bolstad BM, Irizarry RA, Astrand M, Speed TP. 2003. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185-193.
17. Simon R, Lam A, Li MC, Ngan M, Menenzes S, Zhao Y. 2007. Analysis of gene expression data using BRB-ArrayTools. Cancer Inform. 3:11-17.
18. Limonciel A, Aschauer L, Wilmes A, Prajczer S, Leonard MO, Pfaller W, Jennings P. 2011. Lactate is an ideal non-invasive marker for evaluating temporal alterations in cell stress and toxicity in repeat dose testing regimes. Toxicol. In Vitro 25:1855-1862.
19. Jennings P, Aydin S, Bennett J, McBride R, Weiland C, Tuite N, Gruber LN, Perco P, Gaora PO, Ellinger-Ziegelbauer H, Ahr HJ, Kooten CV, Daha MR, Prieto P, Ryan MP, Pfaller W, McMorrow T. 2009. Inter-laboratory comparison of human renal proximal tubule (HK-2) transcriptome alterations due to cyclosporine A exposure and medium exhaustion. Toxicol. In Vitro 23:486-499.
20. Ellis JK, Athersuch TJ, Cavill R, Radford R, Slattery C, Jennings P, McMorrow T, Ryan MP, Ebbels TM, Keun HC. 2011. Metabolic response to low-level toxicant exposure in a novel renal tubule epithelial cell system. Mol. Biosyst. 7:247-257.
21. Pfaller W, Gstraunthaler G, Loidl P. 1990. Morphology of the differentiation and maturation of LLC-PK1 epithelia. J. Cell. Physiol. 142:247-254.
22. Weibel ER. 1979. Morphometry of the human lung: the state of the art after two decades. Bull. Eur. Physiopathol. Respir. 15:999-1013.
23. Giepmans BN, van Ijzendoorn SC. 2009. Epithelial cell-cell junctions and plasma membrane domains. Biochim. Biophys. Acta 1788:820-831.
24. Balda MS, Matter K. 2009. Tight junctions and the regulation of gene expression. Biochim. Biophys. Acta 1788:761-767.
25. Terada H. 1990. Uncouplers of oxidative phosphorylation. Environ. Health Perspect. 87:213-218.
26. Ino Y, Gotoh M, Sakamoto M, Tsukagoshi K, Hirohashi S. 2002. Dysadherin, a cancer-associated cell membrane glycoprotein, down-regulates E-cadherin and promotes metastasis. Proc. Natl. Acad. Sci. U. S. A. 99:365-370.
27. Lee TH, Streb JW, Georger MA, Miano JM. 2006. Tissue expression of the novel serine carboxypeptidase Scpep1. J. Histochem. Cytochem. 54: 701-711.
28. Baum B, Georgiou M. 2011. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J. Cell Biol. 192:907-917.
29. Yonemura S. 2011. Cadherin-actin interactions at adherens junctions. Curr. Opin. Cell Biol. 23:515-522.
30. Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G, Brasch J, Wu Y, Vendome J, Felsovalyi K, Hampton CM, Troyanovsky RB, Ben-Shaul A, Frank J, Troyanovsky SM, Shapiro L, Honig B. 2011. The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19:244-256.
31. Johnson E, Theisen CS, Johnson KR, Wheelock MJ. 2004. R-cadherin influences cell motility via Rho family GTPases. J. Biol. Chem. 279:31041-31049.
32. Thomson RB, Igarashi P, Biemesderfer D, Kim R, Abu-Alfa A, So-leimani M, Aronson PS. 1995. Isolation and cDNA cloning of Kspcadherin, a novel kidney-specific member of the cadherin multigene family. J. Biol. Chem. 270:17594-17601.
33. Mullin JM, Fluk L, Tchao R. 1985. Mitosis in domes of renal epithelial (LLC-PK[1]) cell cultures. Mol. Physiol. 8:317-328.
34. Li J, Ananthapanyasut W, Yu AS. 2011. Claudins in renal physiology and disease. Pediatr. Nephrol. 26:2133-2142.
35. Kirk A, Campbell S, Bass P, Mason J, Collins J. 2010. Differential expression of claudin tight junction proteins in the human cortical nephron. Nephrol. Dial. Transplant. 25:2107-2119.
36. Furuse M, Furuse K, Sasaki H, Tsukita S. 2001. Conversion of zonulae occludentes from tight to leaky strand type by introducing claudin-2 into Madin-Darby canine kidney I cells. J. Cell Biol. 153:263-272.
37. Rosenthal R, Milatz S, Krug SM, Oelrich B, Schulzke JD, Amasheh S, Gunzel D, Fromm M. 2010. Claudin-2, a component of the tight junction, forms a paracellular water channel. J. Cell Sci. 123:1913-1921.
38. Van Itallie CM, Rogan S, Yu A, Vidal LS, Holmes J, Anderson JM. 2006. Two splice variants of claudin-10 in the kidney create paracellular pores with different ion selectivities. Am. J. Physiol. Renal Physiol. 291:F1288-F1299.
39. Limonciel A, Wilmes A, Aschauer L, Radford R, Bloch KM, McMorrow T, Pfaller W, van Delft JH, Slattery C, Ryan MP, Lock EA, Jennings P. 2012. Oxidative stress induced by potassium bromate exposure results in altered tight junction protein expression in renal proximal tubule cells. Arch. Toxicol. 86:1741-1751.
40. Jennings P, Limonciel A, Felice L, Leonard MO. 2012. An overview of transcriptional regulation in response to toxicological insult. Arch. Toxi-col. 87:49-72.
41. Capaldo CT, Koch S, Kwon M, Laur O, Parkos CA, Nusrat A. 2011. Tight function zonula occludens-3 regulates cyclin D1-dependent cell proliferation. Mol. Biol. Cell 22:1677-1685.
42. Sourisseau T, Georgiadis A, Tsapara A, Ali RR, Pestell R, Matter K, Balda MS. 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.
43. Traweger A, Lehner C, Farkas A, Krizbai IA, Tempfer H, Klement E, Guenther B, Bauer HC, Bauer H. 2008. Nuclear Zonula occludens-2 alters gene expression and junctional stability in epithelial and endothelial cells. Differentiation 76:99-106.
44. Bauer H, Zweimueller-Mayer J, Steinbacher P, Lametschwandtner A, Bauer HC. 2010. The dual role of zonula occludens (ZO) proteins. J. Biomed. Biotechnol. 2010:402593. doi:10.1155/2010/402593.
45. Mulukutla BC, Khan S, Lange A, Hu WS. 2010. Glucose metabolism in mammalian cell culture: new insights for tweaking vintage pathways. Trends Biotechnol. 28:476-484.
46. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP. 2000. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106:847-856.
47. Burgess SC, Leone TC, Wende AR, Croce MA, Chen Z, Sherry AD, Malloy CR, Finck BN. 2006. Diminished hepatic gluconeogenesis via defects in tricarboxylic acid cycle flux in peroxisome proliferator-activated receptor gamma coactivator-1alpha (PGC-1alpha)-deficient mice. J. Biol. Chem. 281:19000-19008.
48. Vega RB, Huss JM, Kelly DP. 2000. The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol. 20:1868-1876.
49. Sugden MC, Holness MJ. 2003. Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am. J. Physiol. Endocrinol. Metab. 284:E855-862.
50. +-ATPase. J. Biol. Chem. 269: 19659-19662.
51. Geering K. 2008. Functional roles of Na, K-ATPase subunits. Curr. Opin. Nephrol. Hypertens. 17:526-532.
52. +-ATPase gamma-subunit. Biochim. Biophys. Acta 1350:133-135.
53. Therien AG, Goldshleger R, Karlish SJ, Blostein R. 1997. Tissue-specific distribution and modulatory role of the gamma subunit of the Na, K-ATPase. J. Biol. Chem. 272:32628-32634.
54. Yoder BK. 2007. Role of primary cilia in the pathogenesis of polycystic kidney disease. J. Am. Soc. Nephrol. 18:1381-1388.
55. Forsythe E, Beales PL. 2013. Bardet-Biedl syndrome. Eur. J. Hum. Genet. 21:8-13.
56. Radford R, Slattery C, Jennings P, Blaque O, Pfaller W, Gmuender H, Van Delft J, Ryan MP, McMorrow T. 2012. Carcinogens induce loss of the primary cilium in human renal proximal tubular epithelial cells independently of effects on the cell cycle. Am. J. Physiol. Renal Physiol. 302: F905-F916.
57. Puzio-Kuter AM. 2011. The role of p53 in metabolic regulation. Genes Cancer 2:385-391.
58. Wang PY, Zhuang J, Hwang PM. 2012. p53: exercise capacity and metabolism. Curr. Opin. Oncol. 24:76-82.
59. Russo AA, Tong L, Lee JO, Jeffrey PD, Pavletich NP. 1998. Structural basis for inhibition of the cyclin-dependent kinase Cdk6 by the tumour suppressor p16INK4a. Nature 395:237-243.
60. Shapiro GI, Edwards CD, Rollins BJ. 2000. The physiology of p16(INK4A)-mediated G1 proliferative arrest. Cell Biochem. Biophys. 33: 189-197.
61. Chellappan SP, Hiebert S, Mudryj M, Horowitz JM, Nevins JR. 1991. The E2F transcription factor is a cellular target for the RB protein. Cell 65:1053-1061.
62. Lees JA, Saito M, Vidal M, Valentine M, Look T, Harlow E, Dyson N, Helin K. 1993. The retinoblastoma protein binds to a family of E2F transcription factors. Mol. Cell. Biol. 13:7813-7825.
63. DeGregori J, Johnson DG. 2006. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr. Mol. Med. 6:739-748.
64. Lu J, Li XP, Dong Q, Kung HF, He ML. 2010. TBX2 and TBX3: the special value for anticancer drug targets. Biochim. Biophys. Acta 1806: 268-274.
65. Kim JW, Gao P, Liu YC, Semenza GL, Dang CV. 2007. Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol. Cell. Biol. 27:7381-7393.
66. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. 2006. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3:177-185.
67. Wierstra I, Alves J. 2007. FOXM1, a typical proliferation-associated transcription factor. Biol. Chem. 388:1257-1274.
68. van der Vos KE, Coffer PJ. 2011. The extending network of FOXO transcriptional target genes. Antioxid. Redox Signal. 14:579-592.
69. Guo S, Rena G, Cichy S, He X, Cohen P, Unterman T. 1999. Phosphor-ylation of serine 256 by protein kinase B disrupts transactivation by FKHR and mediates effects of insulin on insulin-like growth factor-binding protein-1 promoter activity through a conserved insulin response sequence. J. Biol. Chem. 274:17184-17192.
70. Hall RK, Yamasaki T, Kucera T, Waltner-Law M, O'Brien R, Granner DK. 2000. Regulation of phosphoenolpyruvate carboxykinase and insulin-like growth factor-binding protein-1 gene expression by insulin. The role of winged helix/forkhead proteins. J. Biol. Chem. 275:30169-30175.
71. Medema RH, Kops GJ, Bos JL, Burgering BM. 2000. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404:782-787.
72. Takano M, Lu Z, Goto T, Fusi L, Higham J, Francis J, Withey A, Hardt J, Cloke B, Stavropoulou AV, Ishihara O, Lam EW, Unterman TG, Brosens JJ, Kim JJ. 2007. Transcriptional cross talk between the forkhead transcription factor forkhead box O1A and the progesterone receptor coordinates cell cycle regulation and differentiation in human endometrial stromal cells. Mol. Endocrinol. 21:2334-2349.
73. Daitoku H, Yamagata K, Matsuzaki H, Hatta M, Fukamizu A. 2003. Regulation of PGC-1 promoter activity by protein kinase B and the fork-head transcription factor FKHR. Diabetes 52:642-649.
74. Nowak K, Killmer K, Gessner C, Lutz W. 2007. E2F-1 regulates expression of FOXO1 and FOXO3a. Biochim. Biophys. Acta 1769:244-252.
75. Calnan DR, Brunet A. 2008. The FoxO code. Oncogene 27:2276-2288.
76. Zhang W, Patil S, Chauhan B, Guo S, Powell DR, Le J, Klotsas A, Matika R, Xiao X, Franks R, Heidenreich KA, Sajan MP, Farese RV, Stolz DB, Tso P, Koo SH, Montminy M, Unterman TG. 2006. FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression. J. Biol. Chem. 281:10105-10117.