p120catenin alteration in cancer and its role in tumour invasion

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1629, 2013, Pages

  Peglion, Florent ^a   Etienne Manneville, Sandrine ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Adherens junctions; Cadherin; Catenin; Invasion; Migration; Rho GTPases

Indexed keywords

ADHESION; CANCER; ENZYME; ENZYME ACTIVITY; IMMUNITY; MEMBRANE; MIGRATION; MORPHOGENESIS; PLASMA; TUMOR;

CADHERIN; CATENIN; DELTA CATENIN;

CELL JUNCTION; CELL MOTION; CYTOSKELETON; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR INVASION; TUMOR MICROENVIRONMENT; INVASION; MIGRATION; REVIEW; RHO-GTPASES;

ADHERENS JUNCTIONS; CADHERINS; CATENINS; CELL MOVEMENT; CYTOSKELETON; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; TUMOR MICROENVIRONMENT;

ADHERENS JUNCTIONS; CADHERIN; CATENIN; INVASION; MIGRATION; RHO-GTPASES;

EID: 84884495955     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0015     Document Type: Review

References (161)

1. Reynolds AB, Roesel DJ, Kanner SB, Parsons JT. 1989 Transformation-specific tyrosine phosphorylation of a novel cellular protein in chicken cells expressing oncogenic variants of the avian cellular src gene. Mol. Cell Biol. 9, 629-698.
2. Reynolds AB, Daniel J, McCrea PD, Wheelock MJ, Wu J, Zhang Z. 1994 Identification of a new catenin: the tyrosine kinase substrate p120cas associates with E-cadherin complexes. Mol. Cell Biol. 14, 8333-8342.
3. Kourtidis A, Ngok SP, Anastasiadis PZ. 2013 p120 catenin: an essential regulator of cadherin stability, adhesion-induced signaling, and cancer progression. Prog. Mol. Biol. Transl. Sci. 116, 409-432. (doi:10. 1016/B978-0-12-394311-8.00018-2)
4. Menke A, Giehl K. 2012 Regulation of adherens junctions by Rho GTPases and p120-catenin. Arch. Biochem. Biophys. 524, 48-55. (doi:10.1016/j.abb. 2012.04.019)
5. Pieters T, van Roy F, van Hengel J. 2012 Functions of p120ctn isoforms in cell-cell adhesion and intracellular signaling. Front. Biosci. 17, 1669-1694. (doi:10.2741/4012)
6. Anastasiadis PZ, Reynolds AB. 2000 The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 113, 1319-1334.
7. Reynolds AB, Roczniak-Ferguson A. 2004 Emerging roles for p120-catenin in cell adhesion and cancer. Oncogene 23, 7947-7956. (doi:10.1038/sj.onc. 1208161)
8. Israely I, Costa RM, Xie CW, Silva AJ, Kosik KS, Liu X. 2004 Deletion of the neuron-specific protein deltacatenin leads to severe cognitive and synaptic dysfunction. Curr. Biol. 14, 1657-1663. (doi:10. 1016/j.cub.2004.08.065)
9. Pieters T, van Hengel J, van Roy F. 2012 Functions of p120ctn in development and disease. Front. Biosci. 17, 760-783. (doi:10. 2741/3956)
10. Marciano DK et al. 2011 p120 catenin is required for normal renal tubulogenesis and glomerulogenesis. Development 138, 2099-2109. (doi:10.1242/dev. 056564)
11. Stairs DB et al. 2011 Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene. Cancer Cell 19, 470-483. (doi:10.1016/j.ccr.2011.02.007)
12. McCrea PD, Park JI. 2007 Developmental functions of the P120-catenin sub-family. Biochim. Biophys. Acta 1773, 17-33. (doi:10.1016/j.bbamcr. 2006.06.009)
13. Davis MA, Reynolds AB. 2006 Blocked acinar development, E-cadherin reduction, and intraepithelial neoplasia upon ablation of p120-catenin in the mouse salivary gland. Dev. Cell 10, 21-31. (doi:10.1016/j.devcel.2005.12.004)
14. Perez-Moreno M, Davis MA, Wong E, Pasolli HA, Reynolds AB, Fuchs E. 2006 p120-catenin mediates inflammatory responses in the skin. Cell 124, 631-644. (doi:10.1016/j.cell.2005.11.043)
15. Perez-Moreno M, Song W, Pasolli HA, Williams SE, Fuchs E. 2008 Loss of p120 catenin and links to mitotic alterations, inflammation, and skin cancer. Proc. Natl Acad. Sci. USA 105, 15 399-15 404. (doi:10.1073/pnas.0807301105)
16. van Hengel J, van Roy F. 2007 Diverse functions of p120ctn in tumors. Biochim. Biophys. Acta 1773, 78-88. (doi:10.1016/j.bbamcr.2006.08.033)
17. Thoreson MA, Reynolds AB. 2002 Altered expression of the catenin p120 in human cancer: implications for tumor progression. Differentiation 70, 583-589. (doi:10.1046/j.1432-0436.2002.700911.x)
18. Ishizaki Y, Omori Y, Momiyama M, Nishikawa Y, Tokairin T, Manabe M, Enomoto K. 2004 Reduced expression and aberrant localization of p120catenin in human squamous cell carcinoma of the skin. J. Dermatol. Sci. 34, 99-108. (doi:10.1016/j. jdermsci.2003.12.001)
19. Nakopoulou L, Zervas A, Gakiopoulou-Givalou H, Constantinides C, Doumanis G, Davaris P, Dimopoulos C. 2000 Prognostic value of E-cadherin, beta-catenin, p120ctn in patients with transitional cell bladder cancer. Anticancer Res. 20, 4571-4578.
20. Shimazui T, Schalken JA, Giroldi LA, Jansen CF, Akaza H, Koiso K, Debruyne FM, Bringuier PP. 1996 Prognostic value of cadherin-associated molecules (alpha-, beta-, and gamma-catenins and p120cas) in bladder tumors. Cancer Res. 56, 4154-4158.
21. Syrigos KN, Karayiannakis A, Syrigou EI, Harrington K, Pignatelli M. 1998 Abnormal expression of p120 correlates with poor survival in patients with bladder cancer. Eur. J. Cancer 34, 2037-2040. (doi:10.1016/S0959-8049(98)00279-2)
22. Gimelbrant AA, Ensminger AW, Qi P, Zucker J, Chess A. 2005 Monoallelic expression and asynchronous replication of p120 catenin in mouse and human cells. J. Biol. Chem. 280, 1354-1359. (doi:10.1074/ jbc.M411283200)
23. Ireton RC et al. 2002 A novel role for p120 catenin in E-cadherin function. J. Cell Biol. 159, 465-476. (doi:10.1083/jcb.200205115)
24. Wood LD et al. 2007 The genomic landscapes of human breast and colorectal cancers. Science 318, 1108-1113. (doi:10.1126/science.1145720)
25. Mortazavi F, An J, Dubinett S, Rettig M. 2010 p120-catenin is transcriptionally downregulated by FOXC2 in non-small cell lung cancer cells. Mol. Cancer Res. 8, 762-774. (doi:10.1158/1541-7786. MCR-10-0004)
26. Hamada S et al. 2013 miR-197 induces epithelialmesenchymal transition in pancreatic cancer cells by targeting p120 catenin. J. Cell Physiol. 228, 1255-1263. (doi:10.1002/jcp.24280)
27. 2+ channel to maintain endothelial integrity. Proc. Natl Acad. Sci. USA 107, 19 308-19 313. (doi:10.1073/pnas.1008544107)
28. Ohno H, Uemura K, Shintani-Ishida K, Nakamura M, Inomata M, Yoshida K. 2007 Ischemia promotes calpain-mediated degradation of p120-catenin in SH-SY5Y cells. Biochem. Biophys. Res. Commun. 353, 547-552. (doi:10.1016/j.bbrc.2006.12.061)
29. Wang Y, Minshall RD, Schwartz DE, Hu G. 2011 Cyclic stretch induces alveolar epithelial barrier dysfunction via calpain-mediated degradation of p120-catenin. Am. J. Physiol. Lung Cell Mol. Physiol. 301, L197-L206. (doi:10.1152/ajplung. 00048.2011)
30. Xia X, Mariner DJ, Reynolds AB. 2003 Adhesionassociated and PKC-modulated changes in serine/ threonine phosphorylation of p120-catenin. Biochemistry 42, 9195-9204. (doi:10.1021/ bi034597h)
31. Smalley-Freed WG, Efimov A, Short SP, Jia P, Zhao Z, Washington MK, Robine S, Coffey RJ, Reynolds AB. 2011 Adenoma formation following limited ablation of p120-catenin in the mouse intestine. PLoS ONE 6, e19880. (doi:10.1371/journal. pone.0019880)
32. Sarrio D, Perez-Mies B, Hardisson D, Moreno-Bueno G, Suarez A, Cano A, Martin-Perez J, Gamallo C, Palacios J. 2004 Cytoplasmic localization of p120ctn and E-cadherin loss characterize lobular breast carcinoma from preinvasive to metastatic lesions. Oncogene 23, 3272-3283. (doi:10.1038/sj.onc. 1207439)
33. Shibata T, Kokubu A, Sekine S, Kanai Y, Hirohashi S. 2004 Cytoplasmic p120ctn regulates the invasive phenotypes of E-cadherin-deficient breast cancer. Am. J. Pathol. 164, 2269-2278. (doi:10.1016/ S0002-9440(10)63783-2)
34. Debald M, Kaiser C, Abramian A, Schildhaus HU, Locher P, Wolfgarten M, Kuhn W, Braun M. 2013 Evaluation of E-cadherin, Ki-67 and lymphatic vessel invasion in abdominal metastases of human breast cancer. Anticancer Res. 33, 1971-1975.
35. Ionescu Popescu C et al. 2013 E-cadherin expression in molecular types of breast carcinoma. Rom. J. Morphol. Embryol. 54, 267-273.
36. Chu K, Boley KM, Moraes R, Barsky SH, Robertson FM. 2013 The paradox of E-cadherin, role in response to hypoxia in the tumor microenvironment and regulation of energy metabolism. Oncotarget 4, 446-462.
37. Silvera D, Arju R, Darvishian F, Levine PH, Zolfaghari L, Goldberg J, Hochman T, Formenti SC, Schneider RJ. 2009 Essential role for eIF4GI overexpression in the pathogenesis of inflammatory breast cancer. Nat. Cell Biol. 11, 903-908. (doi:10.1038/ncb1900)
38. Coman DR. 1944 Decreased mutual adhesiveness, a property of cells from squamous cell carcinomas. Cancer Res. 4, 625-629.
39. Birchmeier W, Behrens J. 1994 Cadherin expression in carcinomas, role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta 1198, 11-26.
40. Vasioukhin V. 2012 Adherens junctions and cancer. Subcell Biochem. 60, 379-414. (doi:10.1007/978-94-007-4186-7_16)
41. Perl AK, Wilgenbus P, Dahl U, Semb H, Christofori G. 1998 A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 392, 190-193. (doi:10.1038/32433)
42. Vleminckx K, Vakaet Jr L, Mareel M, Fiers W, van Roy F. 1991 Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66, 107-119. (doi:10. 1016/0092-8674(91)90143-M)
43. Derksen PW et al. 2006 Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10, 437-449. (doi:10.1016/j.ccr.2006.09.013)
44. Camand E, Peglion F, Osmani N, Sanson M, Etienne-Manneville S. 2012 N-cadherin expression level modulates integrin-mediated polarity and strongly impacts on the speed and directionality of glial cell migration. J. Cell Sci. 125, 844-857. (doi:10.1242/ jcs.087668)
45. Etienne-Manneville S. 2012 Adherens junctions during cell migration. Subcell Biochem. 60, 225-249. (doi:10.1007/978-94-007-4186-7_10)
46. Peglion F, Etienne-Manneville S. 2012 N-cadherin expression level as a critical indicator of invasion in non-epithelial tumors. Cell Adhes. Migr. 6, 327-332. (doi:10.4161/cam.20855)
47. Kowalczyk AP, Nanes BA. 2012 Adherens junction turnover: regulating adhesion through cadherin endocytosis, degradation, and recycling. Subcell Biochem. 60, 197-222. (doi:10.1007/978-94-007-4186-7_9)
48. Thoreson MA, Anastasiadis PZ, Daniel JM, Ireton RC, Wheelock MJ, Johnson KR, Hummingbird DK, Reynolds AB. 2000 Selective uncoupling of p120(ctn) from E-cadherin disrupts strong adhesion. J. Cell Biol. 148, 189-202. (doi:10.1083/jcb. 148.1.189)
49. Davis MA, Ireton RC, Reynolds AB. 2003 A core function for p120-catenin in cadherin turnover. J. Cell Biol. 163, 525-34. (doi:10.1083/jcb. 200307111)
50. Miyashita Y, Ozawa M. 2007 Increased internalization of p120-uncoupled E-cadherin and a requirement for a dileucine motif in the cytoplasmic domain for endocytosis of the protein. J. Biol. Chem. 282, 11 540-11 548. (doi:10.1074/jbc. M608351200)
51. Xiao K, Garner J, Buckley KM, Vincent PA, Chiasson CM, Dejana E, Faundez V, Kowalczyk AP. 2005 p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin. Mol. Biol. Cell 16, 5141-5151. (doi:10. 1091/mbc.E05-05-0440)
52. Chiasson CM, Wittich KB, Vincent PA, Faundez V, Kowalczyk AP. 2009 p120-catenin inhibits VEcadherin internalization through a Rho-independent mechanism. Mol. Biol. Cell 20, 1970-1980. (doi:10. 1091/mbc.E08-07-0735)
53. Ishiyama N, Lee SH, Liu S, Li GY, Smith MJ, Reichardt LF, Ikura M. 2010 Dynamic and static interactions between p120 catenin and E-cadherin regulate the stability of cell-cell adhesion. Cell 141, 117-128. (doi:10.1016/j.cell.2010.01.017)
54. Nanes BA, Chiasson-MacKenzie C, Lowery AM, Ishiyama N, Faundez V, Ikura M, Vincent PA, Kowalczyk AP. 2012 p120-catenin binding masks an endocytic signal conserved in classical cadherins. J. Cell Biol. 199, 365-380. (doi:10.1083/jcb. 201205029)
55. Kelly BT, McCoy AJ, Spate K, Miller SE, Evans PR, Honing S, Owen DJ. 2008 A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456, 976-979. (doi:10.1038/ nature07422)
56. Fujita Y, Krause G, Scheffner M, Zechner D, Leddy HE, Behrens J, Sommer T, Birchmeier W. 2002 Hakai, a c-Cbl-like protein, ubiquitinates and induces endocytosis of the E-cadherin complex. Nat. Cell Biol. 4, 222-231. (doi:10.1038/ncb758)
57. Dupin I, Camand E, Etienne-Manneville S. 2009 Classical cadherins control nucleus and centrosome position and cell polarity. J. Cell Biol. 185, 779-786. (doi:10.1083/jcb.200812034)
58. Elia LP, Yamamoto M, Zang K, Reichardt LF. 2006 p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51, 43-56. (doi:10.1016/j. neuron.2006.05.018)
59. Wildenberg GA, Dohn MR, Carnahan RH, Davis MA, Lobdell NA, Settleman J, Reynolds AB. 2006 p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027-1039. (doi:10.1016/j.cell. 2006.09.046)
60. Smith AL, Dohn MR, Brown MV, Reynolds AB. 2011 Association of Rho-associated protein kinase 1 with E-cadherin complexes is mediated by p120-catenin. Mol. Biol. Cell 23, 99-110. (doi:10.1091/mbc.E11-06-0497)
61. Hirano M, Hashimoto S, Yonemura S, Sabe H, Aizawa S. 2008 EPB41L5 functions to posttranscriptionally regulate cadherin and integrin during epithelial-mesenchymal transition. J. Cell Biol. 182, 1217-1230. (doi:10.1083/jcb.200712086)
62. Wang T, Pei X, Zhan J, Hu J, Yu Y, Zhang H. 2012 FERM-containing protein FRMD5 is a p120-catenin interacting protein that regulates tumor progression. FEBS Lett. 586, 3044-3050. (doi:10.1016/j.febslet. 2012.07.019)
63. Hernandez MV, Wehrendt DP, Arregui CO. 2010 The protein tyrosine phosphatase PTP1B is required for efficient delivery of N-cadherin to the cell surface. Mol. Biol. Cell 21, 1387-1397. (doi:10.1091/mbc. E09-10-0880)
64. Yanagisawa M, Kaverina IN, Wang A, Fujita Y, Reynolds AB, Anastasiadis PZ. 2004 A novel interaction between kinesin and p120 modulates p120 localization and function. J. Biol. Chem. 279, 9512-9521. (doi:10.1074/jbc. M310895200)
65. Chen X, Kojima S, Borisy GG, Green KJ. 2003 p120 catenin associates with kinesin and facilitates the transport of cadherin-catenin complexes to intercellular junctions. J. Cell Biol. 163, 547-557. (doi:10.1083/jcb.200305137)
66. Miranda KC, Joseph SR, Yap AS, Teasdale RD, Stow JL. 2003 Contextual binding of p120ctn to E-cadherin at the basolateral plasma membrane in polarized epithelia. J. Biol. Chem. 278, 43 480-43 488. (doi:10.1074/jbc.M305525200)
67. Meng W, Mushika Y, Ichii T, Takeichi M. 2008 Anchorage of microtubule minus ends to adherens junctions regulates epithelial cell-cell contacts. Cell 135, 948-959. (doi:10.1016/j.cell.2008.09.040)
68. Kumper S, Ridley AJ. 2010 p120ctn and P-cadherin but not E-cadherin regulate cell motility and invasion of DU145 prostate cancer cells. PLoS ONE 5, e11801. (doi:10.1371/journal.pone.0011801)
69. Liu Y et al. 2009 Ablation of p120-catenin enhances invasion and metastasis of human lung cancer cells. Cancer Sci. 100, 441-448. (doi:10.1111/j.1349-7006.2008.01067.x)
70. Gold JS, Reynolds AB, Rimm DL. 1998 Loss of p120ctn in human colorectal cancer predicts metastasis and poor survival. Cancer Lett. 132, 193-201. (doi:10.1016/S0304-3835(98)00190-6)
71. Talvinen K, Tuikkala J, Nykanen M, Nieminen A, Anttinen J, Nevalainen OS, Hurme S, Kuopio T, Krongvist P. 2010 Altered expression of p120catenin predicts poor outcome in invasive breast cancer. J. Cancer Res. Clin. Oncol. 136, 1377-1387. (doi:10. 1007/s00432-010-0789-8)
72. Macpherson IR, Hooper S, Serrels A, McGarry L, Ozanne BW, Harrington K, Frame MC, Sahai E, Brunton VG. 2007 p120-catenin is required for the collective invasion of squamous cell carcinoma cells via a phosphorylation-independent mechanism. Oncogene 26, 5214-5228. (doi:10.1038/sj.onc. 1210334)
73. Yanagisawa M, Anastasiadis PZ. 2006 p120 catenin is essential for mesenchymal cadherin-mediated regulation of cell motility and invasiveness. J. Cell Biol. 174, 1087-1096. (doi:10.1083/jcb.200605022)
74. Friedl P, Locker J, Sahai E, Segall JE. 2012 Classifying collective cancer cell invasion. Nat. Cell Biol. 14, 777-783. (doi:10.1038/ncb2548)
75. Johnson E, Seachrist DD, DeLeon-Rodriguez CM, Lozada KL, Miedler J, Abdul-Karim FW, Keri RA. 2010 HER2/ErbB2-induced breast cancer cell migration and invasion require p120 catenin activation of Rac1 and Cdc42. J. Biol. Chem. 285, 29 491-29 501. (doi:10.1074/jbc.M110.136770)
76. Hazan RB, Qiao R, Keren R, Badano I, Suyama K. 2004 Cadherin switch in tumor progression. Ann. NY Acad. Sci. 1014, 155-163. (doi:10.1196/annals. 1294.016)
77. Christofori G. 2006 New signals from the invasive front. Nature 441, 444-450. (doi:10.1038/ nature04872)
78. Taniuchi K, Nakagawa H, Hosokawa M, Nakamura T, Eguchi H, Ohigashi H, Ishikawa O, Katagiri T, Nakamura Y. 2005 Overexpressed P-cadherin/CDH3 promotes motility of pancreatic cancer cells by interacting with p120ctn and activating rho-family GTPases. Cancer Res. 65, 3092-3099.
79. Grosheva I, Shtutman M, Elbaum M, Bershadsky AD. 2001 p120 catenin affects cell motility via modulation of activity of Rho-family GTPases: a link between cell-cell contact formation and regulation of cell locomotion. J. Cell Sci. 114, 695-707.
80. Bellovin DI, Bates RC, Muzikansky A, Rimm DL, Mercurio AM. 2005 Altered localization of p120 catenin during epithelial to mesenchymal transition of colon carcinoma is prognostic for aggressive disease. Cancer Res. 65, 10 938-10945. (doi:10. 1158/0008-5472.CAN-05-1947)
81. Anastasiadis PZ, Reynolds AB. 2001 Regulation of Rho GTPases by p120-catenin. Curr. Opin. Cell Biol. 13, 604-610. (doi:10.1016/S0955-0674(00) 00258-1)
82. Kinch MS, Clark GJ, Der CJ, Burridge K. 1995 Tyrosine phosphorylation regulates the adhesions of ras-transformed breast epithelia. J. Cell Biol. 130, 461-471. (doi:10.1083/jcb.130.2.461)
83. Ozawa M, Ohkubo T. 2001 Tyrosine phosphorylation of p120(ctn) in v-Src transfected L cells depends on its association with E-cadherin and reduces adhesion activity. J. Cell Sci. 114, 503-512.
84. Ma LW, Zhou ZT, He QB, Jiang WW. 2012 Phosphorylated p120-catenin expression has predictive value for oral cancer progression. J. Clin. Pathol. 65, 315-319. (doi:10.1136/jclinpath-2011-200516)
85. Huveldt D, Lewis-Tuffin LJ, Carlson BL, Schroeder MA, Rodriguez F, Giannini C, Galanis E, Sarkaria JN, Anastasiadis PZ. 2013 Targeting Src family kinases inhibits bevacizumab-induced glioma cell invasion. PLoS ONE 8, e56505. (doi:10.1371/journal.pone. 0056505)
86. Mariner DJ, Anastasiadis P, Keilhack H, Bohmer FD, Wang J, Reynolds AB. 2001 Identification of Src phosphorylation sites in the catenin p120ctn. J. Biol. Chem. 276, 28 006-28 013. (doi:10.1074/jbc. M102443200)
87. Piedra J, Miravet S, Castano J, Palmer HG, Heisterkamp N, Garcia de Herreros A, Dunach M. 2003 p120 Catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and beta-catenin-alpha-catenin interaction. Mol. Cell Biol. 23, 2287-2297. (doi:10. 1128/MCB.23.7.2287-2297.2003)
88. Keilhack H, Hellman U, van Hengel J, van Roy F, Godovac-Zimmermann J, Bohmer FD. 2000 The protein-tyrosine phosphatase SHP-1 binds to and dephosphorylates p120 catenin. J. Biol. Chem. 275, 26 376-26 384. (doi:10.1074/jbc.M001315200)
89. Zondag GC, Reynolds AB, Moolenaar WH. 2000 Receptor protein-tyrosine phosphatase RPTPmu binds to and dephosphorylates the catenin p120(ctn). J. Biol. Chem. 275, 11 264-11 269. (doi:10.1074/jbc.275.15.11264)
90. Alema S, Salvatore AM. 2007 p120 catenin and phosphorylation: mechanisms and traits of an unresolved issue. Biochim. Biophys. Acta 1773, 47-58. (doi:10.1016/j.bbamcr.2006.06.001)
91. Keirsebilck A, Bonne S, Staes K, van Hengel J, Nollet F, Reynolds A, van Roy F. 1998 Molecular cloning of the human p120ctn catenin gene (CTNND1): expression of multiple alternatively spliced isoforms. Genomics 50, 129-146. (doi:10.1006/geno. 1998.5325)
92. Mo YY, Reynolds AB. 1996 Identification of murine p120 isoforms and heterogeneous expression of p120cas isoforms in human tumor cell lines. Cancer Res. 56, 2633-2640.
93. Aho S, Levansuo L, Montonen O, Kari C, Rodeck U, Uitto J. 2002 Specific sequences in p120ctn determine subcellular distribution of its multiple isoforms involved in cellular adhesion of normal and malignant epithelial cells. J. Cell Sci. 115, 1391-1402.
94. Montonen O, Aho M, Uitto J, Aho S. 2001 Tissue distribution and cell type-specific expression of p120ctn isoforms. J. Histochem. Cytochem. 49, 1487-1496. (doi:10.1177/ 002215540104901202)
95. Eger A, Stockinger A, Schaffhauser B, Beug H, Foisner R. 2000 Epithelial mesenchymal transition by c-Fos estrogen receptor activation involves nuclear translocation of beta-catenin and upregulation of beta-catenin/lymphoid enhancer binding factor-1 transcriptional activity. J. Cell Biol. 148, 173-188. (doi:10.1083/jcb.148.1.173)
96. Husmark J, Heldin NE, Nilsson M. 1999 N-cadherinmediated adhesion and aberrant catenin expression in anaplastic thyroid-carcinoma cell lines. Int. J. Cancer 83, 692-699. (doi:10.1002/ (SICI)1097-0215(19991126)83:5<692::AIDIJC21>3.0. CO;2-1)
97. Tran NL, Nagle RB, Cress AE, Heimark RL. 1999 Ncadherin expression in human prostate carcinoma cell lines. An epithelial-mesenchymal transformation mediating adhesion with stromal cells. Am. J. Pathol. 155, 787-798. (doi:10.1016/ S0002-9440(10)65177-2)
98. Seidel B, Braeg S, Adler G, Wedlich D, Menke A. 2004 E-and N-cadherin differ with respect to their associated p120ctn isoforms and their ability to suppress invasive growth in pancreatic cancer cells. Oncogene 23, 5532-5542. (doi:10.1038/sj.onc. 1207718)
99. Miao Y, Liu N, Zhang Y, Liu Y, Yu JH, Dai SD, Xu HT, Wang EH. 2010 p120ctn isoform 1 expression significantly correlates with abnormal expression of E-cadherin and poor survival of lung cancer patients. Med. Oncol. 27, 880-886. (doi:10.1007/ s12032-009-9300-2)
100. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. 2009 ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol. Cell 33, 591-601. (doi:10.1016/j.molcel. 2009.01.025)
101. Ohkubo T, Ozawa M. 2004 The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J. Cell Sci. 117, 1675-1685. (doi:10.1242/jcs.01004)
102. Etienne-Manneville S, Hall A. 2002 Rho GTPases in cell biology. Nature 420, 629-635. (doi:10.1038/ nature01148)
103. Raftopoulou M, Hall A. 2004 Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32. (doi:10.1016/j.ydbio.2003.06.003)
104. Anastasiadis PZ, Moon SY, Thoreson MA, Mariner DJ, Crawford HC, Zheng Y, Reynolds AB. 2000 Inhibition of RhoA by p120 catenin. Nat. Cell Biol. 2, 637-644. (doi:10.1038/35023588)
105. Noren NK, Liu BP, Burridge K, Kreft B. 2000 p120 catenin regulates the actin cytoskeleton via Rho family GTPases. J. Cell Biol. 150, 567-580. (doi:10. 1083/jcb.150.3.567)
106. Cozzolino M, Stagni V, Spinardi L, Campioni N, Fiorentini C, Salvati E, Alema S, Salvatore AM. 2003 p120 catenin is required for growth factordependent cell motility and scattering in epithelial cells. Mol. Biol. Cell 14, 1964-1977. (doi:10.1091/ mbc.E02-08-0469)
107. Castano J, Solanas G, Casagolda D, Raurell I, Villagrasa P, Bustelo XR, Herreros AG, Dunach M. 2007 Specific phosphorylation of p120-catenin regulatory domain differently modulates its binding to RhoA. Mol. Cell Biol. 27, 1745-1757. (doi:10. 1128/MCB.01974-06)
108. Yanagisawa M, Huveldt D, Kreinest P, Lohse CM, Cheville JC, Parker AS, Copland JA, Anastasiadis PZ. 2008 A p120 catenin isoform switch affects Rho activity, induces tumor cell invasion, and predicts metastatic disease. J. Biol. Chem. 283, 18 344-18 354. (doi:10.1074/jbc.M801192200)
109. Zebda N, Tian Y, Tian X, Gawlak G, Higginbotham K, Reynolds AB, Birukova AA, Birukov KG. 2013 Interaction of p190RhoGAP with C-terminal domain of p120-catenin modulates endothelial cytoskeleton and permeability. J. Biol. Chem. 288, 18 290-18 299. (doi:10.1074/jbc.M112.432757)
110. Schackmann RC et al. 2011 Cytosolic p120-catenin regulates growth of metastatic lobular carcinoma through Rock1-mediated anoikis resistance. J. Clin. Invest. 121, 3176-3188. (doi:10.1172/JCI41695)
111. Dohn MR, Brown MV, Reynolds AB. 2009 An essential role for p120-catenin in Src-and Rac1-mediated anchorage-independent cell growth. J. Cell Biol. 184, 437-450. (doi:10.1083/jcb. 200807096)
112. Simpson CD, Anyiwe K, Schimmer AD. 2008 Anoikis resistance and tumor metastasis. Cancer Lett. 272, 177-185. (doi:10.1016/j.canlet.2008.05.029)
113. Cheung LW, Leung PC, Wong AS. 2010 Cadherin switching and activation of p120 catenin signaling are mediators of gonadotropin-releasing hormone to promote tumor cell migration and invasion in ovarian cancer. Oncogene 29, 2427-2440. (doi:10. 1038/onc.2009.523)
114. Soto E, Yanagisawa M, Marlow LA, Copland JA, Perez EA, Anastasiadis PZ. 2008 p120 catenin induces opposing effects on tumor cell growth depending on E-cadherin expression. J. Cell Biol. 183, 737-749. (doi:10.1083/jcb.200805113)
115. Valls G et al. 2012 Upon Wnt stimulation, Rac1 activation requires Rac1 and Vav2 binding to p120-catenin. J. Cell Sci. 125, 5288-5301. (doi:10.1242/ jcs.101030)
116. Rajput C et al. 2013 Neural Wiskott-Aldrich syndrome protein (N-WASP)-mediated p120-catenin interaction with Arp2-Actin complex stabilizes endothelial adherens junctions. J. Biol. Chem. 288, 4241-4250. (doi:10.1074/jbc.M112.440396)
117. Boguslavsky S, Grosheva I, Landau E, Shtutman M, Cohen M, Arnold K, Feinstein E, Geiger B, Bershadsky A. 2007 p120 catenin regulates lamellipodial dynamics and cell adhesion in cooperation with cortactin. Proc. Natl Acad. Sci. USA 104, 10 882-10 887. (doi:10.1073/pnas. 0702731104)
118. Ichii T, Takeichi M. 2007 p120-catenin regulates microtubule dynamics and cell migration in a cadherin-independent manner. Genes Cells 12, 827-839. (doi:10.1111/j.1365-2443.2007.01095.x)
119. Roczniak-Ferguson A, Reynolds AB. 2003 Regulation of p120-catenin nucleocytoplasmic shuttling activity. J. Cell Sci. 116, 4201-4212. (doi:10.1242/ jcs.00724)
120. Franz CM, Ridley AJ. 2004 p120 catenin associates with microtubules, inverse relationship between microtubule binding and Rho GTPase regulation. J. Biol. Chem. 279, 6588-6594. (doi:10.1074/jbc. M312812200)
121. Cook TA, Nagasaki T, Gundersen GG. 1998 Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J. Cell Biol. 141, 175-185. (doi:10.1083/jcb.141.1.175)
122. Palazzo AF, Cook TA, Alberts AS, Gundersen GG. 2001 mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell Biol. 3, 723-729. (doi:10.1038/35087035)
123. Falconer MM, Vielkind U, Brown DL. 1989 Establishment of a stable, acetylated microtubule bundle during neuronal commitment. Cell Motil. Cytoskeleton 12, 169-180. (doi:10.1002/cm. 970120306)
124. Mayerle J, Friess H, Buchler MW, Schnekenburger J, Weiss FU, Zimmer KP, Domschke W, Lerch MM. 2003 Up-regulation, nuclear import, and tumor growth stimulation of the adhesion protein p120 in pancreatic cancer. Gastroenterology 124, 949-960. (doi:10.1053/gast.2003.50142)
125. Kelly KF, Spring CM, Otchere AA, Daniel JM. 2004 NLS-dependent nuclear localization of p120ctn is necessary to relieve Kaiso-mediated transcriptional repression. J. Cell Sci. 117, 2675-2686. (doi:10. 1242/jcs.01101)
126. Chausovsky A, Bershadsky AD, Borisy GG. 2000 Cadherin-mediated regulation of microtubule dynamics. Nat. Cell Biol. 2, 797-804. (doi:10.1038/ 35041037)
127. Giannakakou P, Nakano M, Nicolaou KC, O'Brate A, Yu J, Blagosklonny MV, Greber UF, Fojo T. 2000 Enhanced microtubule-dependent trafficking and p53 nuclear accumulation by suppression of microtubule dynamics. Proc. Natl Acad. Sci. USA 99, 10 855-10 860. (doi:10.1073/pnas.132275599)
128. Dong C, Li Z, Alvarez Jr R, Feng XH, Goldschmidt-Clermont PJ. 2002 Microtubule binding to Smads may regulate TGF beta activity. Mol. Cell 5, 27-34. (doi:10.1016/S1097-2765(00)80400-1)
129. Li Y, Kufe D. 2001 The human DF3/MUC1 carcinoma-associated antigen signals nuclear localization of the catenin p120(ctn). Biochem. Biophys. Res. Commun. 281, 440-443. (doi:10. 1006/bbrc.2001.4383)
130. Wen Y, Caffrey TC, Wheelock MJ, Johnson KR, Hollingsworth MA. 2003 Nuclear association of the cytoplasmic tail of MUC1 and beta-catenin. J. Biol. Chem. 278, 38 029-38 039. (doi:10.1074/jbc. M304333200)
131. Wesseling J, van der Valk SW, Hilkens J. 1996 A mechanism for inhibition of E-cadherin-mediated cell-cell adhesion by the membrane-associated mucin episialin/MUC1. Mol. Biol. Cell 7, 565-577.
132. Willert K, Jones KA. 2006 Wnt signaling: is the party in the nucleus? Genes Dev. 20, 1394-1404. (doi:10.1101/gad.1424006)
133. Daniel JM, Reynolds AB. 1999 The catenin p120(ctn) interacts with Kaiso, a novel BTB/POZ domain zinc finger transcription factor. Mol. Cell Biol. 19, 3614-3623.
134. Prokhortchouk A, Hendrich B, Jorgensen H, Ruzov A, Wilm M, Georgiev G, Bird A, Prokhortchouk E. 2001 The p120 catenin partner Kaiso is a DNA methylation-dependent transcriptional repressor. Genes Dev. 15, 1613-1618. (doi:10.1101/ gad.198501)
135. Daniel JM, Spring CM, Crawford HC, Reynolds AB, Baig A. 2002 The p120(ctn)-binding partner Kaiso is a bi-modal DNA-binding protein that recognizes both a sequence-specific consensus and methylated CpG dinucleotides. Nucleic Acids Res. 30, 2911-2919. (doi:10.1093/nar/gkf398)
136. Yoon HG, Chan DW, Reynolds AB, Qin J, Wong J. 2003 N-CoR mediates DNA methylation-dependent repression through a methyl CpG binding protein Kaiso. Mol. Cell 12, 723-734. (doi:10.1016/j.molcel. 2003.08.008)
137. Jones J et al. 2012 Nuclear Kaiso indicates aggressive prostate cancers and promotes migration and invasiveness of prostate cancer cells. Am. J. Pathol. 181, 1836-1846. (doi:10.1016/j.ajpath. 2012.08.008)
138. Yildirim E, Kirby JE, Brown DE, Mercier FE, Sadreyev RI, Scadden DT, Lee JT. 2013 Xist RNA is a potent suppressor of hematologic cancer in mice. Cell 152, 727-742. (doi:10.1016/j.cell.2013.01.034)
139. Murphree AL, Benedict WF. 1984 Retinoblastoma: clues to human oncogenesis. Science 223, 1028-1033. (doi:10.1126/science.6320372)
140. Caldas C et al. 1994 Frequent somatic mutations and homozygous deletions of the p16 (MTS1) gene in pancreatic adenocarcinoma. Nat. Genet. 8, 27-32. (doi:10.1038/ng0994-27)
141. Kim SW, Park JI, Spring CM, Sater AK, Ji H, Otchere AA, Daniel JM, McCrea PD. 2004 Non-canonical Wnt signals are modulated by the Kaiso transcriptional repressor and p120-catenin. Nat. Cell Biol. 6, 1212-1220. (doi:10.1038/ncb1191)
142. Park JI, Ji H, Jun S, Gu D, Hikasa H, Li L, Sokol SY, McCrea PD. 2006 Frodo links Dishevelled to the p120-catenin/Kaiso pathway: distinct catenin subfamilies promote Wnt signals. Dev. Cell 11, 683-695. (doi:10.1016/j.devcel.2006.09.022)
143. Anastas JN, Moon RT. 2013 WNT signalling pathways as therapeutic targets in cancer. Nat. Rev. Cancer 13, 11-26. (doi:10.1038/nrc3419)
144. DiMeo TA, Anderson K, Phadke P, Fan C, Perou CM, Naber S, Kuperwasser C. 2009 A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. Cancer Res. 69, 5364-5373. (doi:10.1158/0008-5472)
145. Spring CM, Kelly KF, O'Kelly I, Graham M, Crawford HC, Daniel JM. 2005 The catenin p120ctn inhibits Kaiso-mediated transcriptional repression of the beta-catenin/TCF target gene matrilysin. Exp. Cell Res. 305, 253-265. (doi:10.1016/j.yexcr.2005. 01.007)
146. Casagolda D et al. 2010 A p120-catenin-CK1epsilon complex regulates Wnt signaling. J. Cell Sci. 123, 2621-2631. (doi:10.1242/jcs.067512)
147. Del Valle-Perez B, Casagolda D, Lugilde E, Valls G, Codina M, Dave N, Herreros AG, Dunach M. 2011 Wnt controls the transcriptional activity of Kaiso through CK1epsilon-dependent phosphorylation of p120-catenin. J. Cell Sci. 124, 2298-2309. (doi:10. 1242/jcs.082693)
148. Dvorak HF. 1986 Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N. Engl. J. Med. 315, 1650-1659. (doi:10.1056/NEJM198612253152606)
149. Coussens LM, Werb Z. 2002 Inflammation and cancer. Nature 420, 860-867. (doi:10.1038/ nature01322)
150. Maeda H, Akaike T. 1998 Nitric oxide and oxygen radicals in infection, inflammation, and cancer. Biochemistry (Mosc.) 63, 854-865.
151. Meira LB et al. 2008 DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice. J. Clin. Invest. 118, 2516-2525. (doi:10.1172/JCI35073)
152. Radisky DC et al. 2005 Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123-127. (doi:10.1038/ nature03688)
153. Williams IR, Parkos CA. 2007 Colonic neutrophils in inflammatory bowel disease: double-edged swords of the innate immune system with protective and destructive capacity. Gastroenterology 133, 2049-2052. (doi:10.1053/j.gastro.2007.10.031)
154. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, Sahai E. 2007 Fibroblastled collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9, 1392-1400. (doi:10.1038/ncb1658)
155. Bhowmick NA, Neilson EG, Moses HL. 2004 Stromal fibroblasts in cancer initiation and progression. Nature 432, 332-337. (doi:10.1038/nature03096)
156. De Wever O, Nguyen QD, Van Hoorde L, Bracke M, Bruyneel E, Gespach C, Mareel M. 2009 Tenascin-C and SF/HGF produced by myofibroblasts in vitro provide convergent pro-invasive signals to human colon cancer cells through RhoA and Rac. FASEB J. 18, 1016-1018.
157. + T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 16, 91-102. (doi:10. 1016/j.ccr.2009.06.018)
158. Ferrara N. 2010 Role of myeloid cells in vascular endothelial growth factor-independent tumor angiogenesis. Curr. Opin. Hematol. 17, 219-224.
159. Gabrilovich DI, Nagaraj S. 2009 Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9, 162-174. (doi:10. 1038/nri2506)
160. Ostrand-Rosenberg S, Sinha P. 2009 Myeloid-derived suppressor cells: linking inflammation and cancer. J. Immunol. 182, 4499-4506. (doi:10.4049/ jimmunol.0802740)
161. Smalley-Freed WG et al. 2010 p120-catenin is essential for maintenance of barrier function and intestinal homeostasis in mice. J. Clin. Invest. 120, 1824-1835. (doi:10.1172/JCI41414)