Identification of phospholipase C gamma1 as a protein tyrosine phosphatase mu substrate that regulates cell migration

Journal of Cellular Biochemistry

Volumn 112, Issue 1, 2011, Pages 39-48

  Phillips Mason, Polly J ^a   Kaur, Harpreet ^a   Burden Gulley, Susan M ^a   Craig, Sonya E L ^a   Brady Kalnay, Susann M ^a  

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

Author keywords

Cell migration; Glioblastoma; Phospholipase C; Protein kinase C ; RACK1; Receptor protein tyrosine phosphatase; Tyrosine phosphorylation

Indexed keywords

PHOSPHODIESTERASE INHIBITOR; PHOSPHOLIPASE C GAMMA1; PROTEIN KINASE C DELTA; PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE MU; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ARTICLE; BRAIN SLICE; CANCER INVASION; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME SUBSTRATE; GLIOMA CELL; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; REGULATORY MECHANISM;

BRAIN NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; GLIOMA; HUMANS; PHOSPHOLIPASE C GAMMA; PHOSPHORYLATION; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 2; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 78651326871     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22710     Document Type: Article

References (51)

1. Blanchetot C, Chagnon M, Dube N, Halle M, Tremblay ML. 2005. Substratetrapping techniques in the identification of cellular PTP targets. Methods 35:44-53.
2. Brady-Kalnay SM, Tonks NK. 1994. Identification of the homophilic binding site of the receptor protein tyrosine phosphatase PTP mu. J Biol Chem 269:28472-28477.
3. Brady-Kalnay SM, Flint AJ, Tonks NK. 1993. Homophilic binding of PTP mu, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J Cell Biol 122:961-972.
4. Bruce JN, Parsa A. 1999. Inhibition of phospholipase C gamma 1 activation blocks glioma cell motility and invasion of fetal rat brain aggregates. Neurosurgery 44:577.
5. Burden-Gulley SM, Brady-Kalnay SM. 1999. PTPmu regulates N-cadherindependent neurite outgrowth. J Cell Biol 144:1323-1336.
6. Burden-Gulley SM, Gates TJ, Burgoyne AM, Cutter JL, Lodowski D, Robinson S, Sloan AE, Miller RH, Basilion JP, Brady-Kalnay SM. 2010. A novel molecular diagnostic of Glioblastomas: Detection of an extracellular fragment of PTPmu. Neoplasia 4:305-316.
7. Burgoyne AM, Palomo JM, Phillips-Mason PJ, Burden-Gulley SM, Major DL, Zaremba A, Robinson S, Sloan AE, Vogelbaum MA, Miller RH, Brady-Kalnay SM. 2009a. PTPmu suppresses glioma cell migration and dispersal. Neuro Oncol 11:767-778.
8. Burgoyne AM, Phillips-Mason PJ, Burden-Gulley SM, Robinson S, Sloan AE, Miller RH, Brady-Kalnay SM. 2009b. Proteolytic cleavage of protein tyrosine phosphatase mu regulates glioblastoma cell migration. Cancer Res 69:6960-6968.
9. Choi JH, Ryu SH, Suh PG. 2007. On/off-regulation of phospholipase C-gamma 1-mediated signal transduction. Adv Enzyme Regul 47:104-116.
10. Disatnik MH, Hernandez-Sotomayor SM, Jones G, Carpenter G, Mochly- Rosen D. 1994. Phospholipase C-gamma 1 binding to intracellular receptors for activated protein kinase C. Proc Natl Acad Sci USA 91:559-563.
11. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. 1998. A third-generation lentivirus vector with a conditional packaging system. J Virol 72:8463-8471.
12. Ensslen SE, Brady-Kalnay SM. 2004. PTPmu signaling via PKCdelta is instructive for retinal ganglion cell guidance. Mol Cell Neurosci 25:558-571.
13. Ensslen-Craig SE, Brady-Kalnay SM. 2005. PTP mu expression and catalytic activity are required for PTP mu-mediated neurite outgrowth and repulsion. Mol Cell Neurosci 28:177-188.
14. Flint AJ, Tiganis T, Barford D, Tonks NK. 1997. Development of "substratetrapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci USA 94:1680-1685.
15. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA, Cavenee WK. 2007. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev 21:2683-2710.
16. Gebbink MF, Verheijen MH, Zondag GC, van Etten I, Moolenaar WH. 1993. Purification and characterization of the cytoplasmic domain of human receptor-like protein tyrosine phosphatase RPTP mu. Biochemistry 32: 13516-13522.
17. Gogolla N, Galimberti I, DePaola V, Caroni P. 2006. Preparation of organotypic hippocampal slice cultures for long-term live imaging. Nat Protoc 1:1165-1171.
18. Hellberg CB, Burden-Gulley SM, Pietz GE, Brady-Kalnay SM. 2002. Expression of the receptor protein-tyrosine phosphatase, PTPmu, restores E-cadherin-dependent adhesion in human prostate carcinoma cells. J Biol Chem 277:11165-11173.
19. Jacobsen CT, Miller RH. 2003. Control of astrocyte migration in the developing cerebral cortex. Dev Neurosci 25:207-216.
20. Jones NP, Katan M. 2007. Role of phospholipase C gamma1 in cell spreading requires association with a beta-Pix/GIT1-containing complex, leading to activation of Cdc42 and Rac1. Mol Cell Biol 27:5790-5805.
21. Kanu OO, Hughes B, Di C, LinN, Fu J, Bigner DD, Yan H, Adamson C. 2009. Glioblastoma multiforme oncogenomics and signaling pathways. Clin Med Oncol 3:39-52.
22. Kassis J, Moellinger J, Lo H, Greenberg NM, Kim HG, Wells A. 1999. A role for phospholipase C-gamma-mediated signaling in tumor cell invasion. Clin Cancer Res 5:2251-2260.
23. Li S, Wang Q, Wang Y, Chen X, Wang Z. 2009. PLC-gamma1 and Rac1 coregulate EGF-induced cytoskeleton remodeling and cell migration. Mol Endocrinol 23:901-913.
24. McCahill A, Warwicker J, Bolger GB, Houslay MD, Yarwood SJ. 2002. The RACK1 scaffold protein: A dynamic cog in cell response mechanisms. Mol Pharmacol 62:1261-1273.
25. Mouneimne G, Soon L, DesMarais V, Sidani M, Song X, Yip SC, Ghosh M, Eddy R, Backer JM, Condeelis J. 2004. Phospholipase C and cofilin are required for carcinoma cell directionality in response to EGF stimulation. J Cell Biol 166:697-708.
26. Mourton T, Hellberg CB, Burden-Gulley SM, Hinman J, Rhee A, Brady- Kalnay SM. 2001. The PTPmu protein-tyrosine phosphatase binds and recruits the scaffolding protein RACK1 to cell-cell contacts. J Biol Chem 276:14896-14901.
27. Nakada M, Nakada S, Demuth T, Tran NL, Hoelzinger DB, Berens ME. 2007. Molecular targets of glioma invasion. Cell Mol Life Sci 64:458-478.
28. Oblander SA, Brady-Kalnay SM. 2010. Distinct PTPmu-associated signaling molecules differentially regulate neurite outgrowth on E-, N-, and R-cadherin. Mol Cell Neurosci 44:78-93.
29. Oblander SA, Ensslen-Craig SE, Longo FM, Brady-Kalnay SM. 2007. E-cadherin promotes retinal ganglion cell neurite outgrowth in a protein tyrosine phosphatase-mu-dependent manner. Mol Cell Neurosci 34:481-492.
30. Ostman A, Hellberg C, Bohmer FD. 2006. Protein-tyrosine phosphatases and cancer. Nat Rev Cancer 6:307-320.
31. Peak JC, Jones NP, Hobbs S, Katan M, Eccles SA. 2008. Phospholipase C gamma 1 regulates the Rap GEF1-Rap1 signalling axis in the control of human prostate carcinoma cell adhesion. Oncogene 27:2823-2832.
32. Phillips-Mason PJ, Gates TJ, Major DL, Sacks DB, Brady-Kalnay SM. 2006. The receptor protein-tyrosine phosphatase PTPm interacts with IQGAP1. J Biol Chem 281:4903-4910.
33. Phillips-Mason PJ, Mourton T, Major DL, Brady-Kalnay SM. 2008. BCCIP associates with the receptor protein tyrosine phosphatase PTPmu. J Cell Biochem 105:1059-1072.
34. Piccolo E, Innominato PF, Mariggio MA, Maffucci T, Iacobelli S, Falasca M. 2002. The mechanism involved in the regulation of phospholipase C gamma1 activity in cell migration. Oncogene 21:6520-6529.
35. Poulin B, Sekiya F, Rhee SG. 2005. Intramolecular interaction between phosphorylated tyrosine-783 and the C-terminal Src homology 2 domain activates phospholipase C-gamma1. Proc Natl Acad Sci USA 102:4276-4281.
36. Rao JS. 2003. Molecular mechanisms of glioma invasiveness: The role of proteases. Nat Rev Cancer 3:489-501.
37. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. 2003. Cell migration: Integrating signals from front to back. Science 302:1704-1709.
38. Rosdahl JA, Mourton TL, Brady-Kalnay SM. 2002. Protein kinase C delta (PKCdelta) is required for protein tyrosine phosphatase mu (PTPmu)-dependent neurite outgrowth. Mol Cell Neurosci 19:292-306.
39. Sala G, Dituri F, Raimondi C, Previdi S, Maffucci T, Mazzoletti M, Rossi C, Iezzi M, Lattanzio R, Piantelli M, Iacobelli S, Broggini M, Falasca M. 2008. Phospholipase C gamma1 is required for metastasis development and progression. Cancer Res 68:10187-10196.
40. Schlessinger J. 2000. Cell signaling by receptor tyrosine kinases. Cell 103: 211-225.
41. Sekiya F, Poulin B, Kim YJ, Rhee SG. 2004. Mechanism of tyrosine phosphorylation and activation of phospholipase C-gamma 1. Tyrosine 783 phosphorylation is not sufficient for lipase activation. J Biol Chem 279: 32181-32190.
42. Serrano CJ, Graham L, DeBell K, Rawat R, Veri MC, Bonvini E, Rellahan BL, Reischl IG. 2005. A new tyrosine phosphorylation site in PLC gamma 1: The role of tyrosine 775 in immune receptor signaling. J Immunol 174:6233-6237.
43. Teodorczyk M, Martin-Villalba A. 2010. Sensing invasion: Cell surface receptors driving spreading of glioblastoma. J Cell Physiol 222:1-10.
44. Thomas SM, Coppelli FM, Wells A, Gooding WE, Song J, Kassis J, Drenning SD, Grandis JR. 2003. Epidermal growth factor receptor-stimulated activation of phospholipase C gamma-1 promotes invasion of head and neck squamous cell carcinoma. Cancer Res 63:5629-5635.
45. Tiganis T, Bennett AM. 2007. Protein tyrosine phosphatase function: The substrate perspective. Biochem J 402:1-15.
46. Turner T, Epps-Fung MV, Kassis J, Wells A. 1997. Molecular inhibition of phospholipase c gamma signaling abrogates DU-145 prostate tumor cell invasion. Clin Cancer Res 3:2275-2282.
47. Ullrich A, Schlessinger J. 1990. Signal transduction by receptors with tyrosine kinase activity. Cell 61:203-212.
48. Wells A, Grandis JR. 2003. Phospholipase C-gamma1 in tumor progression. Clin Exp Metastasis 20:285-290.
49. Yamaguchi H, Condeelis J. 2007. Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 1773:642-652.
50. Yu H, Fukami K, Itoh T, Takenawa T. 1998. Phosphorylation of phospholipase C gamma1 on tyrosine residue 783 by platelet-derived growth factor regulates reorganization of the cytoskeleton. Exp Cell Res 243:113-122.
51. Zondag GC, Reynolds AB, Moolenaar WH. 2000. Receptor protein-tyrosine phosphatase RPTPmu binds to and dephosphorylates the catenin p120(ctn). J Biol Chem 275:11264-11269.