Should I stay or should I go? Shedding of RPTPs in cancer cells switches signals from stabilizing cell-cell adhesion to driving cell migration

Cell Adhesion and Migration

Volumn 5, Issue 4, 2011, Pages

  Phillips Mason, Polly J ^a   Craig, Sonya E L ^a   Brady Kalnay, Susann M ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cadherins; Catenins; Cell adhesion; IQGAP1 protein; Phospholipase C gamma; Protein kinase C; Receptor protein tyrosine kinase; Receptor like protein tyrosine phosphatase; Regulated intramembrane proteolysis; Signal transduction

Indexed keywords

CADHERIN; CELL ADHESION MOLECULE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE; RECEPTOR PROTEIN TYROSINE PHOSPHATASE; UNCLASSIFIED DRUG; BETA CATENIN; CTNNB1 PROTEIN, HUMAN; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; TYROSINE;

CANCER CELL; CANCER INVASION; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELLULAR DISTRIBUTION; EXTRACELLULAR MATRIX; HUMAN; METASTASIS; NOTE; PHENOTYPE; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; ACTIN FILAMENT; ARTICLE; CELL MEMBRANE; CELL MOTION; CHEMISTRY; ENZYME ACTIVATION; METABOLISM; NEOPLASM; PATHOLOGY; PHOSPHORYLATION;

ACTIN CYTOSKELETON; BETA CATENIN; CELL ADHESION; CELL ADHESION MOLECULES; CELL MEMBRANE; CELL MOVEMENT; CELL-MATRIX JUNCTIONS; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES; SIGNAL TRANSDUCTION; TYROSINE;

EID: 85046979797     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: 10.4161/cam.5.4.16970     Document Type: Note

References (69)

1. Teodorczyk M, Martin-Villalba A. Sensing invasion: cell surface receptors driving spreading of glioblastoma. J Cell Physiol 2010; 222:1-10.
2. Ullrich A, Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell 1990; 61:203-212
3. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010; 141:1117-1134
4. Tonks NK. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 2006; 7:833-846 (Pubitemid 44627477)
5. Soulsby M, Bennett AM. Physiological signaling specificity by protein tyrosine phosphatases. Physiology (Bethesda) 2009; 24:281-289
6. Blume-Jensen P, Hunter T. Oncogenic kinase signalling. Nature 2001; 411:355-365 (Pubitemid 32467045)
7. Julien SG, Dube N, Hardy S, Tremblay ML. Inside the human cancer tyrosine phosphatome. Nat Rev Cancer 2011; 11:35-49.
8. Östman A, Hellberg C, Böhmer FD. Protein-tyrosine phosphatases and cancer. Nat Rev Cancer 2006; 6:307-320
9. Tiscornia MM, Riera MA, Lorenzati MA, Zapata PD. Phosphotyrosine phosphatases in cancer diagnostic and treatment. Recent Pat DNA Gene Seq 4:46-51.
10. McArdle L, Rafferty MM, Satyamoorthy K, Maelandsmo GM, Dervan PA, Herlyn M, et al. Microarray analysis of phosphatase gene expression in human melanoma. Br J Dermatol 2005; 152:925-930 (Pubitemid 40704932)
11. Francavilla C, Maddaluno L, Cavallaro U. The functional role of cell adhesion molecules in tumor angiogenesis. Semin Cancer Biol 2009; 19:298-309.
12. Parsons JT, Horwitz AR, Schwartz MA. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 2010; 11:633-643
13. Lilien J, Balsamo J. The regulation of cadherinmediated adhesion by tyrosine phosphorylation/ dephosphorylation of beta-catenin. Curr Opin Cell Biol 2005; 17:459-465 (Pubitemid 41267159)
14. Craig SE, Brady-Kalnay SM. Tumor-derived extracellular fragments of receptor protein tyrosine phosphatases (RPTPs) as cancer molecular diagnostic tools. Anticancer Agents Med Chem 2011; 11:133-140
15. Craig SE, Brady-Kalnay SM. Cancer cells cut homophilic cell adhesion molecules and run. Cancer Res 2011; 71:303-309
16. McCusker CD, Alfandari D. Life after proteolysis: Exploring the signaling capabilities of classical cadherin cleavage fragments. Commun Integr Biol 2009; 2:155-157
17. Fortini ME. Gamma-secretase-mediated proteolysis in cell-surface-receptor signalling. Nat Rev Mol Cell Biol 2002; 3:673-684
18. Brady-Kalnay SM, Tonks NK. Protein tyrosine phosphatases as adhesion receptors. Curr Opin Cell Biol 1995; 7:650-657
19. Beltran PJ, Bixby JL. Receptor protein tyrosine phosphatases as mediators of cellular adhesion. Front Biosci 2003; 8:87-99.
20. Burridge K, Sastry SK, Sallee JL. Regulation of cell adhesion by protein-tyrosine phosphatases. I. Cell-matrix adhesion. J Biol Chem 2006; 281:15593-15596 (Pubitemid 43848444)
21. Sallee JL, Wittchen ES, Burridge K. Regulation of cell adhesion by protein-tyrosine phosphatases: II. Cell-cell adhesion. J Biol Chem 2006; 281:16189-16192
22. Ruhe JE, Streit S, Hart S, Ullrich A. EGFR signaling leads to downregulation of PTP-LAR via TACE-mediated proteolytic processing. Cell Signal 2006; 18:1515-1527 (Pubitemid 43832087)
23. Edwards DR, Handsley MM, Pennington CJ. The ADAM metalloproteinases. Mol Aspects Med 2008; 29:258-289
24. Anders L, Mertins P, Lammich S, Murgia M, Hartmann D, Saftig P, et al. Furin-, ADAM 10- and gamma-Secretase-Mediated cleavage of a receptor tyrosine phosphatase and regulation of beta-catenin's transcriptional activity. Mol Cell Biol 2006; 26:3917-3934 (Pubitemid 43726407)
25. Gil-Henn H, Volohonsky G, Elson A. Regulation of protein-tyrosine phosphatases alpha and epsilon by calpain-mediated proteolytic cleavage. J Biol Chem 2001; 276:31772-31779
26. Kulas DT, Goldstein BJ, Mooney RA. The transmembrane protein-tyrosine phosphatase LAR modulates signaling by multiple receptor tyrosine kinases. J Biol Chem 1996; 271:748-754 (Pubitemid 26034923)
27. Uetani N, Bertozzi K, Chagnon MJ, Hendriks W, Tremblay ML, Bouchard M. Maturation of ureterbladder connection in mice is controlled by LAR family receptor protein tyrosine phosphatases. J Clin Invest 2009; 119:924-935
28. Suárez Pestana E, Tenev T, Gross S, Stoyanov B, Ogata M, Böhmer FD. The transmembrane protein tyrosine phosphatase RPTPsigma modulates signaling of the epidermal growth factor receptor in A431 cells. Oncogene 1999; 18:4069-4079
29. Xu Y, Tan LJ, Grachtchouk V, Voorhees JJ, Fisher GJ. Receptor-type protein-tyrosine phosphatase-kappa regulates epidermal growth factor receptor function. J Biol Chem 2005; 280:42694-42700 (Pubitemid 43049228)
30. Perez-Pinera P, Zhang W, Chang Y, Vega JA, Deuel TF. Anaplastic lymphoma kinase is activated through the pleiotrophin/receptor protein-tyrosine phosphatase beta/zeta signaling pathway: an alternative mechanism of receptor tyrosine kinase activation. J Biol Chem 2007; 282:28683-28690 (Pubitemid 47606064)
31. Phillips-Mason PJ, Gates TJ, Major DL, Sacks DB, Brady-Kalnay SM. The receptor protein-tyrosine phosphatase PTPμ interacts with IQGAP1. J Biol Chem 2006; 281:4903-4910 (Pubitemid 43847752)
32. Phillips-Mason PJ, Kaur H, Burden-Gulley SM, Craig SE, Brady-Kalnay SM. Identification of phospholipase Cgamma1 as a protein tyrosine phosphatase mu substrate that regulates cell migration. J Cell Biochem 2011; 112:39-48.
33. Bunney TD, Katan M. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat Rev Cancer 2010; 10:342-352
34. Wells A, Grandis JR. Phospholipase C-gamma1 in tumor progression. Clin Exp Metastasis 2003; 20:285-290
35. Piccolo E, Innominato PF, Mariggio MA, Maffucci T, Iacobelli S, Falasca M. The mechanism involved in the regulation of phospholipase Cgamma1 activity in cell migration. Oncogene 2002; 21:6520-6529 (Pubitemid 35155456)
36. Poulin B, Sekiya F, Rhee SG. Intramolecular interaction between phosphorylated tyrosine-783 and the C-terminal Src homology 2 domain activates phospholipase C-gamma1. Proc Natl Acad Sci USA 2005; 102:4276-4281 (Pubitemid 40397102)
37. Schiller MR. Coupling receptor tyrosine kinases to Rho GTPases-GEFs what's the link. Cell Signal 2006; 18:1834-1843 (Pubitemid 44485993)
38. Mackay DJ, Hall A. Rho GTPases. J Biol Chem 1998; 273:20685-20688 (Pubitemid 28385341)
39. Bos JL, Rehmann H, Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007; 129:865-877 (Pubitemid 46802708)
40. Li S, Wang Q, Wang Y, Chen X, Wang Z. PLCgamma1 and Rac1 coregulate EGF-induced cytoskeleton remodeling and cell migration. Mol Endocrinol 2009; 23:901-913
41. Jones NP, Katan M. Role of phospholipase Cgamma1 in cell spreading requires association with a beta-Pix/ GIT1-containing complex, leading to activation of Cdc42 and Rac1. Mol Cell Biol 2007; 27:5790-5805 (Pubitemid 47257834)
42. Brady-Kalnay SM, Flint AJ, Tonks NK. Homophilic binding of PTP mu, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J Cell Biol 1993; 122:961-72.
43. Gebbink MF, Zondag GC, Wubbolts RW, Beijersbergen RL, van Etten I, Moolenaar WH. Cellcell adhesion mediated by a receptor-like protein tyrosine phosphatase. J Biol Chem 1993; 268:16101-16104
44. Hellberg CB, Burden-Gulley SM, Pietz GE, Brady- Kalnay SM. Expression of the receptor proteintyrosine phosphatase, PTPmu, restores E-cadherindependent adhesion in human prostate carcinoma cells. J Biol Chem 2002; 277:11165-11173 (Pubitemid 34952878)
45. Burgoyne AM, Palomo JM, Phillips-Mason PJ, Burden-Gulley SM, Major DL, Zaremba A, et al. PTPmu suppresses glioma cell migration and dispersal. Neuro Oncol 2009; 11:767-778
46. Burgoyne AM, Phillips-Mason PJ, Burden-Gulley SM, Robinson S, Sloan AE, Miller RH, et al. Proteolytic cleavage of protein tyrosine phosphatase mu regulates glioblastoma cell migration. Cancer Res 2009; 69:6960-6968
47. Larsson C. Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal 2006; 18:276-284 (Pubitemid 41661343)
48. McCahill A, Warwicker J, Bolger GB, Houslay MD, Yarwood SJ. The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol Pharmacol 2002; 62:1261-1273 (Pubitemid 35403822)
49. Mourton T, Hellberg CB, Burden-Gulley SM, Hinman J, Rhee A, Brady-Kalnay SM. The PTPmu protein-tyrosine phosphatase binds and recruits the scaffolding protein RACK1 to cell-cell contacts. J Biol Chem 2001; 276:14896-14901
50. Ensslen-Craig SE, Brady-Kalnay SM. Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev Biol 2004; 275:12-22. (Pubitemid 39298172)
51. Pariser H, Herradon G, Ezquerra L, Perez-Pinera P, Deuel TF. Pleiotrophin regulates serine phosphorylation and the cellular distribution of beta-adducin through activation of protein kinase C. Proc Natl Acad Sci USA 2005; 102:12407-12412 (Pubitemid 41266372)
52. Shima T, Okumura N, Takao T, Satomi Y, Yagi T, Okada M, et al. Interaction of the SH2 domain of Fyn with a cytoskeletal protein, beta-adducin. J Biol Chem 2001; 276:42233-42240
53. Pariser H, Perez-Pinera P, Ezquerra L, Herradon G, Deuel TF. Pleiotrophin stimulates tyrosine phosphorylation of beta-adducin through inactivation of the transmembrane receptor protein tyrosine phosphatase beta/zeta. Biochem Biophys Res Commun 2005; 335:232-239 (Pubitemid 41350785)
54. Wang B, Kishihara K, Zhang D, Sakamoto T, Nomoto K. Transcriptional regulation of a receptor protein tyrosine phosphatase gene hPTP-J by PKCmediated signaling pathways in Jurkat and Molt-4 T lymphoma cells. Biochim Biophys Acta 1999; 1450:331-340 (Pubitemid 29295483)
55. Tracy S, van der Geer P, Hunter T. The receptor-like protein-tyrosine phosphatase, RPTPalpha, is phosphorylated by protein kinase C on two serines close to the inner face of the plasma membrane. J Biol Chem 1995; 270:10587-10594
56. Hartsock A, Nelson WJ. Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 2008; 1778:660-9.
57. Muller T, Choidas A, Reichmann E, Ullrich A. Phosphorylation and free pool of beta-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration. J Biol Chem 1999; 274:10173-10183
58. Yan HX, He YQ, Dong H, Zhang P, Zeng JZ, Cao HF, et al. Physical and functional interaction between receptor-like protein tyrosine phosphatase PCP-2 and beta-catenin. Biochemistry 2002; 41:15854-15860 (Pubitemid 36062491)
59. Meng K, Rodriguez-Pena A, Dimitrov T, Chen W, Yamin M, Noda M, et al. Pleiotrophin signals increased tyrosine phosphorylation of beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc Natl Acad Sci USA 2000; 97:2603-2608 (Pubitemid 30159217)
60. Perez-Pinera P, Alcantara S, Dimitrov T, Vega JA, Deuel TF. Pleiotrophin disrupts calcium-dependent homophilic cell-cell adhesion and initiates an epithelial- mesenchymal transition. Proc Natl Acad Sci USA 2006; 103:17795-17800 (Pubitemid 44852239)
61. Kim YS, Kang HY, Kim JY, Oh S, Kim CH, Ryu CJ, et al. Identification of target proteins of N-acetylglucosaminyl transferase V in human colon cancer and implications of protein tyrosine phosphatase kappa in enhanced cancer cell migration. Proteomics 2006; 6:1187-1191
62. Reiss K, Maretzky T, Ludwig A, Tousseyn T, de Strooper B, Hartmann D, et al. ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J 2005; 24:742-752 (Pubitemid 40396104)
63. Brown MD, Sacks DB. IQGAP1 in cellular signaling: bridging the GAP. Trends Cell Biol 2006; 16:242-249 (Pubitemid 43744436)
64. Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K. IQGAP1: a key regulator of adhesion and migration. J Cell Sci 2005; 118:2085-2092 (Pubitemid 40872832)
65. Alema S, Salvatore AM. p120 catenin and phosphorylation: Mechanisms and traits of an unresolved issue. Biochim Biophys Acta 2007; 1773:47-58.
66. Ferber EC, Kajita M, Wadlow A, Tobiansky L, Niessen C, Ariga H, et al. A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. J Biol Chem 2008; 283:12691-12700
67. Anastasiadis PZ. p120-ctn: A nexus for contextual signaling via Rho GTPases. Biochim Biophys Acta 2007; 1773:34-46.
68. Dohn MR, Brown MV, Reynolds AB. An essential role for p120-catenin in Src- and Rac1-mediated anchorage-independent cell growth. J Cell Biol 2009; 184:437-450
69. Wang C, Yang Y, Yang Z, Liu M, Li Z, Sun L, et al. EGF-mediated migration signaling activated by N-acetylglucosaminyltransferase-V via receptor protein tyrosine phosphatase kappa. Arch Biochem Biophys 2009; 486:64-72.