TRAF4 Is a Novel Phosphoinositide-Binding Protein Modulating Tight Junctions and Favoring Cell Migration

PLoS Biology

Volumn 11, Issue 12, 2013, Pages

  Rousseau, Adrien ^a,b,c,d   McEwen, Alastair G ^a,b,c,d   Poussin Courmontagne, Pierre ^a,b,c,d   Rognan, Didier ^d,e   Nominé, Yves ^d,f   Rio, Marie Christine ^a,b,c,d   Tomasetto, Catherine ^a,b,c,d   Alpy, Fabien ^a,b,c,d  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e Faculté de Pharmacie   (France)

^f Institut de Recherche de l'Ecole de Biotechnologie de Strasbourg   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITIDE; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 4;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER GROWTH; CELL MEMBRANE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; GENE OVEREXPRESSION; MOLECULAR MODEL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; REGULATORY MECHANISM; STRUCTURE ACTIVITY RELATION; TIGHT JUNCTION;

ANIMALS; CELL MEMBRANE; CELL MOVEMENT; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; PHOSPHATIDYLINOSITOLS; RECOMBINANT PROTEINS; TIGHT JUNCTIONS; TNF RECEPTOR-ASSOCIATED FACTOR 4;

EID: 84892702772     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001726     Document Type: Article

References (102)

1. Régnier CH, Tomasetto C, Moog-Lutz C, Chenard MP, Wendling C, et al. (1995) Presence of a new conserved domain in CART1, a novel member of the tumor necrosis factor receptor-associated protein family, which is expressed in breast carcinoma. J Biol Chem 270: 25715-25721.
2. Tomasetto C, Régnier C, Moog-Lutz C, Mattei MG, Chenard MP, et al. (1995) Identification of four novel human genes amplified and overexpressed in breast carcinoma and localized to the q11-q21.3 region of chromosome 17. Genomics 28: 367-376 doi:10.1006/geno.1995.1163.
3. Camilleri-Broët S, Cremer I, Marmey B, Comperat E, Viguié F, et al. (2007) TRAF4 overexpression is a common characteristic of human carcinomas. Oncogene 26: 142-147 doi:10.1038/sj.onc.1209762.
4. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, et al. (2004) Large-scale meta-analysis of cancer microarray data identifies common transcriptional profiles of neoplastic transformation and progression. Proc Natl Acad Sci USA 101: 9309-9314 doi:10.1073/pnas.0401994101.
5. Bradley JR, Pober JS, (2001) Tumor necrosis factor receptor-associated factors (TRAFs). Oncogene 20: 6482-6491 doi:10.1038/sj.onc.1204788.
6. Zotti T, Vito P, Stilo R, (2012) The seventh ring: exploring TRAF7 functions. J Cell Physiol 227: 1280-1284 doi:10.1002/jcp.24011.
7. Kedinger V, Rio M-C, (2007) TRAF4, the unique family member. Adv Exp Med Biol 597: 60-71 doi:_10.1007/978-0-387-70630-6_5.
8. Zapata JM, Martínez-García V, Lefebvre S, (2007) Phylogeny of the TRAF/MATH domain. Adv Exp Med Biol 597: 1-24 doi:_10.1007/978-0-387-70630-6_1.
9. Preiss A, Johannes B, Nagel AC, Maier D, Peters N, et al. (2001) Dynamic expression of Drosophila TRAF1 during embryogenesis and larval development. Mechanisms of Development 100: 109-113 doi:10.1016/S0925-4773(00)00506-2.
10. Grech A, Quinn R, Srinivasan D, Badoux X, Brink R, (2000) Complete structural characterisation of the mammalian and Drosophila TRAF genes: implications for TRAF evolution and the role of RING finger splice variants. Mol Immunol 37: 721-734.
11. Cha G-H, Cho KS, Lee JH, Kim M, Kim E, et al. (2003) Discrete functions of TRAF1 and TRAF2 in Drosophila melanogaster mediated by c-Jun N-terminal kinase and NF-kappaB-dependent signaling pathways. Mol Cell Biol 23: 7982-7991.
12. Mathew SJ, Rembold M, Leptin M, (2011) Role for Traf4 in polarizing adherens junctions as a prerequisite for efficient cell shape changes. Mol Cell Biol 31: 4978-4993 doi:10.1128/MCB.05542-11.
13. Régnier CH, Masson R, Kedinger V, Textoris J, Stoll I, et al. (2002) Impaired neural tube closure, axial skeleton malformations, and tracheal ring disruption in TRAF4-deficient mice. Proc Natl Acad Sci USA 99: 5585-5590 doi:10.1073/pnas.052124799.
14. Shiels H, Li X, Schumacker PT, Maltepe E, Padrid PA, et al. (2000) TRAF4 deficiency leads to tracheal malformation with resulting alterations in air flow to the lungs. Am J Pathol 157: 679-688 doi:10.1016/S0002-9440(10)64578-6.
15. Blaise S, Kneib M, Rousseau A, Gambino F, Chenard M-P, et al. (2012) In vivo evidence that TRAF4 is required for central nervous system myelin homeostasis. PLoS One 7: e30917 doi:10.1371/journal.pone.0030917.
16. Glauner H, Siegmund D, Motejadded H, Scheurich P, Henkler F, et al. (2002) Intracellular localization and transcriptional regulation of tumor necrosis factor (TNF) receptor-associated factor 4 (TRAF4). Eur J Biochem 269: 4819-4829.
17. Kedinger V, Alpy F, Baguet A, Polette M, Stoll I, et al. (2008) Tumor necrosis factor receptor-associated factor 4 is a dynamic tight junction-related shuttle protein involved in epithelium homeostasis. PLoS One 3: e3518 doi:10.1371/journal.pone.0003518.
18. Krajewska M, Krajewski S, Zapata JM, Van Arsdale T, Gascoyne RD, et al. (1998) TRAF-4 expression in epithelial progenitor cells. Analysis in normal adult, fetal, and tumor tissues. Am J Pathol 152: 1549-1561.
19. Kédinger V, Alpy F, Baguet A, Polette M, Stoll I, et al. (2008) Tumor necrosis factor receptor-associated factor 4 is a dynamic tight junction-related shuttle protein involved in epithelium homeostasis. PLoS One 3: e3518 doi:10.1371/journal.pone.0003518.
20. Yi P, Xia W, Wu R-C, Lonard DM, Hung M-C, et al. (2013) SRC-3 coactivator regulates cell resistance to cytotoxic stress via TRAF4-mediated p53 destabilization. Genes Dev 27: 274-287 doi:10.1101/gad.203760.112.
21. Wang H, Cai Y, Chia W, Yang X, (2006) Drosophila homologs of mammalian TNF/TNFR-related molecules regulate segregation of Miranda/Prospero in neuroblasts. EMBO J 25: 5783-5793 doi:10.1038/sj.emboj.7601461.
22. Li J-M, Fan LM, Christie MR, Shah AM, (2005) Acute tumor necrosis factor alpha signaling via NADPH oxidase in microvascular endothelial cells: role of p47phox phosphorylation and binding to TRAF4. Mol Cell Biol 25: 2320-2330 doi:10.1128/MCB.25.6.2320-2330.2005.
23. Wu RF, Xu YC, Ma Z, Nwariaku FE, Sarosi GA Jr, et al. (2005) Subcellular targeting of oxidants during endothelial cell migration. J Cell Biol 171: 893-904 doi:10.1083/jcb.200507004.
24. Rousseau A, Rio M-C, Alpy F, (2011) TRAF4, at the crossroad between morphogenesis and cancer. Cancers 3: 2734-2749 doi:10.3390/cancers3022734.
25. Kalkan T, Iwasaki Y, Park CY, Thomsen GH, (2009) Tumor necrosis factor-receptor-associated factor-4 is a positive regulator of transforming growth factor-β signaling that affects neural crest formation. Mol Biol Cell 20: 3436-3450 doi:10.1091/mbc.E08-03-0325.
26. Masson R, Régnier CH, Chenard MP, Wendling C, Mattei MG, et al. (1998) Tumor necrosis factor receptor associated factor 4 (TRAF4) expression pattern during mouse development. Mech Dev 71: 187-191.
27. Barcellos-Hoff MH, Aggeler J, Ram TG, Bissell MJ, (1989) Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105: 223-235.
28. Bazzoun D, Lelièvre S, Talhouk R, (2013) Polarity proteins as regulators of cell junction complexes: Implications for breast cancer. Pharmacology & Therapeutics Available http://www.sciencedirect.com/science/article/pii/S0163725813000454. Accessed April 9, 2013.
29. Debnath J, Mills KR, Collins NL, Reginato MJ, Muthuswamy SK, et al. (2002) The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111: 29-40.
30. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, et al. (1990) Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Res 50: 6075-6086.
31. Brown KA, Aakre ME, Gorska AE, Price JO, Eltom SE, et al. (2004) Induction by transforming growth factor-β1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Res 6: 1-17 doi:10.1186/bcr778.
32. Brysse A, Mestdagt M, Polette M, Luczka E, Hunziker W, et al. (2012) Regulation of CXCL8/IL-8 expression by zonula occludens-1 in human breast cancer cells. Mol Cancer Res 10: 121-132 doi:10.1158/1541-7786.MCR-11-0180.
33. Ivanov AI, Hunt D, Utech M, Nusrat A, Parkos CA, (2005) Differential roles for actin polymerization and a myosin II motor in assembly of the epithelial apical junctional complex. Mol Biol Cell 16: 2636-2650 doi:10.1091/mbc.E05-01-0043.
34. Van Deurs B, Zou ZZ, Briand P, Balslev Y, Petersen OW, (1987) Epithelial membrane polarity: a stable, differentiated feature of an established human breast carcinoma cell line MCF-7. J Histochem Cytochem 35: 461-469.
35. Meerschaert K, Tun MP, Remue E, Ganck AD, Boucherie C, et al. (2009) The PDZ2 domain of zonula occludens-1 and-2 is a phosphoinositide binding domain. Cell Mol Life Sci 66: 3951-3966 doi:10.1007/s00018-009-0156-6.
36. Wu H, Feng W, Chen J, Chan L-N, Huang S, et al. (2007) PDZ domains of Par-3 as potential phosphoinositide signaling integrators. Mol Cell 28: 886-898 doi:10.1016/j.molcel.2007.10.028.
37. Dowler S, (2002) Protein lipid overlay assay. Science's STKE 2002: 6pl-6 doi:10.1126/stke.2002.129.pl6.
38. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, et al. (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229 doi:10.1006/meth.2001.1183.
39. Potier N, Rogniaux H, Chevreux G, Van Dorsselaer A (2005) Ligand-metal ion binding to proteins: investigation by ESI mass spectrometry. In: A. L Burlingame, editor. Methods in enzymology. Academic Press, Vol. Volume 402. pp. 361-389. Available http://www.sciencedirect.com/science/article/pii/S0076687905020112. Accessed March 4, 2013.
40. Park YC, Burkitt V, Villa AR, Tong L, Wu H, (1999) Structural basis for self-association and receptor recognition of human TRAF2. Nature 398: 533-538 doi:10.1038/19110.
41. Zheng C, Kabaleeswaran V, Wang Y, Cheng G, Wu H, (2010) Crystal structures of the TRAF2: cIAP2 and the TRAF1: TRAF2: cIAP2 complexes: affinity, specificity, and regulation. Mol Cell 38: 101-113 doi:10.1016/j.molcel.2010.03.009.
42. Bigay J, Casella J-F, Drin G, Mesmin B, Antonny B, (2005) ArfGAP1 responds to membrane curvature through the folding of a lipid packing sensor motif. The EMBO J 24: 2244-2253 doi:10.1038/sj.emboj.7600714.
43. Manneville J-B, Leduc C, Sorre B, Drin G, (2012) Studying in vitro membrane curvature recognition by proteins and its role in vesicular trafficking. Methods Cell Biol 108: 47-71 doi:10.1016/B978-0-12-386487-1.00003-1.
44. Ye H, Wu H, (2000) Thermodynamic characterization of the interaction between TRAF2 and tumor necrosis factor receptor peptides by isothermal titration calorimetry. PNAS 97: 8961-8966 doi:10.1073/pnas.160241997.
45. Yan J, Wen W, Xu W, Long J-F, Adams ME, et al. (2005) Structure of the split PH domain and distinct lipid-binding properties of the PH-PDZ supramodule of alpha-syntrophin. EMBO J 24: 3985-3995 doi:10.1038/sj.emboj.7600858.
46. Yu JW, Mendrola JM, Audhya A, Singh S, Keleti D, et al. (2004) Genome-wide analysis of membrane targeting by S. cerevisiae pleckstrin homology domains. Molecular Cell 13: 677-688 doi:10.1016/S1097-2765(04)00083-8.
47. Zhang P, Reichardt A, Liang H, Aliyari R, Cheng D, et al. (2012) Single amino acid substitutions confer the antiviral activity of the TRAF3 adaptor protein onto TRAF5. Sci Signal 5: ra81 doi:10.1126/scisignal.2003152.
48. Wu H (2004) Assembly of post-receptor signaling complexes for the tumor necrosis factor receptor superfamily. In: K. Christopher Garcia, editor. Advances in protein chemistry. Academic Press, Vol. Volume 68. pp. 225-279. Available http://www.sciencedirect.com/science/article/pii/S0065323304680077. Accessed March 28, 2013.
49. Shewan A, Eastburn DJ, Mostov K, (2011) Phosphoinositides in cell architecture. Cold Spring Harb Perspect Biol 3: a004796 doi:10.1101/cshperspect.a004796.
50. Rosenhouse-Dantsker A, Logothetis DE, (2007) Molecular characteristics of phosphoinositide binding. Pflugers Arch- Eur J Physiol 455: 45-53 doi:10.1007/s00424-007-0291-6.
51. Elavazhagan M, Lakshminarayanan R, Zhou L, Ting LW, Tong L, et al. (2012) Expression, purification and characterization of fourth FAS1 domain of TGFβIp-associated corneal dystrophic mutants. Protein Expression and Purification 84: 108-115 doi:10.1016/j.pep.2012.04.018.
52. Jones G, Willett P, Glen RC, Leach AR, Taylor R, (1997) Development and validation of a genetic algorithm for flexible docking. J Mol Biol 267: 727-748 doi:10.1006/jmbi.1996.0897.
53. Di Paolo G, De Camilli P, (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443: 651-657 doi:10.1038/nature05185.
54. Balla T, Varnai P, (2009) Visualisation of cellular phosphoinositide pools with GFP-fused protein-domains. Curr Protoc Cell Biol CHAPTER Unit-24.4. doi:10.1002/0471143030.cb2404s42.
55. Várnai P, Balla T, (2006) Live cell imaging of phosphoinositide dynamics with fluorescent protein domains. Biochimica et Biophysica Acta (BBA)- Molecular and Cell Biology of Lipids 1761: 957-967 doi:10.1016/j.bbalip.2006.03.019.
56. Gassama-Diagne A, Yu W, ter Beest M, Martin-Belmonte F, Kierbel A, et al. (2006) Phosphatidylinositol-3,4,5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat Cell Biol 8: 963-970 doi:10.1038/ncb1461.
57. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U, et al. (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128: 383-397 doi:10.1016/j.cell.2006.11.051.
58. Lee E, Marcucci M, Daniell L, Pypaert M, Weisz OA, et al. (2002) Amphiphysin 2 (Bin1) and T-tubule biogenesis in muscle. Science 297: 1193-1196 doi:10.1126/science.1071362.
59. Garcia P, Gupta R, Shah S, Morris AJ, Rudge SA, et al. (1995) The pleckstrin homology domain of phospholipase C-delta 1 binds with high affinity to phosphatidylinositol 4,5-bisphosphate in bilayer membranes. Biochemistry 34: 16228-16234.
60. Huo L, Wen W, Wang R, Kam C, Xia J, et al. (2011) Cdc42-dependent formation of the ZO-1/MRCKβ complex at the leading edge controls cell migration. EMBO J 30: 665-678 doi:10.1038/emboj.2010.353.
61. Tanos B, Rodriguez-Boulan E, (2008) The epithelial polarity program: machineries involved and their hijacking by cancer. Oncogene 27: 6939-6957 doi:10.1038/onc.2008.345.
62. Gassama-Diagne A, Payrastre B, (2009) Phosphoinositide signaling pathways: promising role as builders of epithelial cell polarity. Int Rev Cell Mol Biol 273: 313-343 doi:10.1016/S1937-6448(08)01808-X.
63. Kutateladze TG, (2010) Translation of the phosphoinositide code by PI effectors. Nat Chem Biol 6: 507-513 doi:10.1038/nchembio.390.
64. Chockalingam PS, Gee SH, Jarrett HW, (1999) Pleckstrin homology domain 1 of mouse alpha 1-syntrophin binds phosphatidylinositol 4,5-bisphosphate. Biochemistry 38: 5596-5602 doi:+10.1021/bi982564+.
65. Ni C-Z, Welsh K, Leo E, Chiou C, Wu H, et al. (2000) Molecular basis for CD40 signaling mediated by TRAF3. PNAS 97: 10395-10399 doi:10.1073/pnas.97.19.10395.
66. Ye H, Arron JR, Lamothe B, Cirilli M, Kobayashi T, et al. (2002) Distinct molecular mechanism for initiating TRAF6 signalling. Nature 418: 443-447 doi:10.1038/nature00888.
67. Wang Y, Zhang P, Liu Y, Cheng G, (2010) TRAF-mediated regulation of immune and inflammatory responses. Sci China Life Sci 53: 159-168 doi:10.1007/s11427-010-0050-3.
68. Kuriyan J, Cowburn D, (1997) Modular peptide recognition domains in eukaryotic signaling. Annual Review of Biophysics and Biomolecular Structure 26: 259-288 doi:10.1146/annurev.biophys.26.1.259.
69. Eom DS, Amarnath S, Agarwala S, (2013) Apicobasal polarity and neural tube closure. Dev Growth Differ 55: 164-172 doi:10.1111/dgd.12030.
70. Kalkan T, Iwasaki Y, Park CY, Thomsen GH, (2009) Tumor necrosis factor-receptor-associated factor-4 is a positive regulator of transforming growth factor-beta signaling that affects neural crest formation. Mol Biol Cell 20: 3436-3450 doi:10.1091/mbc.E08-03-0325.
71. Lander R, Nasr T, Ochoa SD, Nordin K, Prasad MS, et al. (2013) Interactions between Twist and other core epithelial-mesenchymal transition factors are controlled by GSK3-mediated phosphorylation. Nat Commun 4: 1542 doi:10.1038/ncomms2543.
72. Le Bras GF, Taubenslag KJ, Andl CD, (2012) The regulation of cell-cell adhesion during epithelial-mesenchymal transition, motility and tumor progression. Cell Adh Migr 6: 365-373 doi:10.4161/cam.21326.
73. Bièche I, Tomasetto C, Régnier CH, Moog-Lutz C, Rio MC, et al. (1996) Two distinct amplified regions at 17q11-q21 involved in human primary breast cancer. Cancer Res 56: 3886-3890.
74. Zhang L, Zhou F, García de Vinuesa A, de Kruijf EM, Mesker WE, et al. (2013) TRAF4 promotes TGF-β receptor signaling and drives breast cancer metastasis. Mol Cell doi:10.1016/j.molcel.2013.07.014.
75. Wang X, Jin C, Tang Y, Tang L-Y, Zhang YE, (2013) Ubiquitination of tumor necrosis factor receptor-associated factor 4 (TRAF4) by Smad ubiquitination regulatory factor 1 (Smurf1) regulates motility of breast epithelial and cancer cells. J Biol Chem 288: 21784-21792 doi:10.1074/jbc.M113.472704.
76. Degot S, Hir HL, Alpy F, Kedinger V, Stoll I, et al. (2004) Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J Biol Chem 279: 33702-33715 doi:10.1074/jbc.M402754200.
77. Kédinger V, Alpy F, Baguet A, Polette M, Stoll I, et al. (2008) Tumor necrosis factor receptor-associated factor 4 is a dynamic tight junction-related shuttle protein involved in epithelium homeostasis. PLoS One 3: e3518 doi:10.1371/journal.pone.0003518.
78. Tramier M, Zahid M, Mevel JC, Masse MJ, Coppey-Moisan M, (2006) Sensitivity of CFP/YFP and GFP/mCherry pairs to donor photobleaching on FRET determination by fluorescence lifetime imaging microscopy in living cells. Microsc Res Tech 69: 933-939.
79. Moffat J, Grueneberg DA, Yang X, Kim SY, Kloepfer AM, et al. (2006) A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124: 1283-1298 doi:10.1016/j.cell.2006.01.040.
80. Alpy F, Stoeckel ME, Dierich A, Escola JM, Wendling C, et al. (2001) The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J Biol Chem 276: 4261-4269 doi:10.1074/jbc.M006279200.
81. Dowler S, Kular G, Alessi DR, (2002) Protein Lipid Overlay Assay. Sci STKE 2002: pl6 doi:10.1126/stke.2002.129.pl6.
82. Whitmore L, Woollett B, Miles AJ, Klose DP, Janes RW, et al. (2011) PCDDB: the Protein Circular Dichroism Data Bank, a repository for circular dichroism spectral and metadata. Nucleic Acids Res 39: D480-D486 doi:10.1093/nar/gkq1026.
83. Kabsch W, (2010) XDS. Acta Crystallogr D Biol Crystallogr 66: 125-132 doi:10.1107/S0907444909047337.
84. Evans P, (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82 doi:10.1107/S0907444905036693.
85. Evans PR, (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr D Biol Crystallogr 67: 282-292 doi:10.1107/S090744491003982X.
86. The CCP4 suite: programs for protein crystallography (1994) Acta Crystallogr D Biol Crystallog 50: 760-763 doi:10.1107/S0907444994003112.
87. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674 doi:10.1107/S0021889807021206.
88. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221 doi:10.1107/S0907444909052925.
89. Stein N, (2008) CHAINSAW: a program for mutating pdb files used as templates in molecular replacement. Journal of Applied Crystallography 41: 641-643 doi:10.1107/S0021889808006985.
90. Matthews BW, (1968) Solvent content of protein crystals. J Mol Biol 33: 491-497 doi:10.1016/0022-2836(68)90205-2.
91. Emsley P, Lohkamp B, Scott WG, Cowtan K, (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501 doi:10.1107/S0907444910007493.
92. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM, et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21 doi:10.1107/S0907444909042073.
93. Laskowski RA, MacArthur MW, Moss DS, Thornton JM, (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystal 26: 283-291 doi:10.1107/S0021889892009944.
94. Delano W (2002) The PyMOL molecular graphics system. San Carlos, CA: Delano Scientific. Available: http://www.pymol.org/.
95. Sadowski J, Gasteiger J, Klebe G, (1994) Comparison of automatic three-dimensional model builders using 639 X-ray structures. J Chem Inf Comput Sci 34: 1000-1008 doi:10.1021/ci00020a039.
96. FILTER (n.d.). Santa Fe: OpenEye Scientific Software. Available http://www.eyesopen.com/filter.
97. SYBYL-X (n.d.). 1699 South Hanley Rd., St. Louis, Missouri, 63144, USA: Tripos International.
98. GOLD (n.d.). Cambridge CB2 1EZ, United Kingdom: Cambridge Cristallographic Data Centre.
99. Wang J, Wang W, Kollman PA, Case DA, (2006) Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 25: 247-260 doi:10.1016/j.jmgm.2005.12.005.
100. Case DA, Cheatham TE 3rd, Darden T, Gohlke H, Luo R, et al. (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688 doi:10.1002/jcc.20290.
101. Gao L, Joberty G, Macara IG, (2002) Assembly of epithelial tight junctions is negatively regulated by Par6. Curr Biol 12: 221-225 doi:10.1016/S0960-9822(01)00663-7.
102. Gumbiner B, Simons K, (1986) A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J Cell Biol 102: 457-468 doi:10.1083/jcb.102.2.457.