PTPμ suppresses glioma cell migration and dispersal

Neuro-Oncology

Volumn 11, Issue 6, 2009, Pages 767-778

  Burgoyne, Adam M ^a   Palomo, Juan M ^b   Phillips Mason, Polly J ^a   Burden Gulley, Susan M ^a   Major, Denice L ^a   Zaremba, Anita ^a   Robinson, Shenandoah ^a   Sloan, Andrew E ^a   Vogelbaum, Michael A ^b   Miller, Robert H ^a   Brady Kalnay, Susann M ^a  

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

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Cell migration; Dispersal; Glioblastoma; Protein tyrosine phosphatase; PTP

Indexed keywords

PROTEIN TYROSINE PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE MU; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; MESSENGER RNA; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTOMA; CANCER GRADING; CELL ADHESION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; EX VIVO STUDY; GLIOBLASTOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; BRAIN TUMOR; CELL CYCLE; CELL MOTION; CELL PROLIFERATION; DRUG SCREENING; FEMALE; GENETICS; GLIOMA; IMMUNOBLOTTING; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; WOUND HEALING;

ANIMALS; BRAIN NEOPLASMS; CELL ADHESION; CELL CYCLE; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; GLIOMA; HUMANS; IMMUNOBLOTTING; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; WOUND HEALING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 70449650636     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1215/15228517-2009-019     Document Type: Article

References (49)

1. Louis DN. Molecular pathology of malignant gliomas. Annu Rev Pathol. 2006;1:97-117.
2. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, eds. World Health Organization Classification of Tumours of the Nervous System. Lyon, France: International Agency for Research on Cancer; 2007.
3. Collins VP. Brain tumours: classification and genes. J Neurol Neurosurg Psychiatry. 2004;75(suppl 2):ii2-11.
4. Furnari FB, Fenton T, Bachoo RM, et al. Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 2007;21:2683-2710.
5. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;359:492-507.
6. Ricci PE, Dungan DH. Imaging of low- and intermediate-grade gliomas. Semin Radiat Oncol. 2001;11:103-112.
7. Giese A, Bjerkvig R, Berens ME, Westphal M. Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol. 2003;21:1624-1636.
8. Demuth T, Berens ME. Molecular mechanisms of glioma cell migration and invasion. J Neurooncol. 2004;70:217-228.
9. Libermann TA, Razon N, Bartal AD, Yarden Y, Schlessinger J, Soreq H. Expression of epidermal growth factor receptors in human brain tumors. Cancer Res. 1984;44:753-760.
10. Wong AJ, Ruppert JM, Bigner SH, et al. Structural alterations of the epidermal growth factor receptor gene in human gliomas. Proc Natl Acad Sci U S A. 1992;89:2965-2969.
11. Tonks NK. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol. 2006;7:833-846.
12. Ensslen-Craig SE, Brady-Kalnay SM. Receptor protein tyrosine phosphatases regulate neural development and axon guidance. Dev Biol. 2004;275:12-22.
13. Brady-Kalnay SM, Flint AJ, Tonks NK. Homophilic binding of PTPm, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J Cell Biol. 1993;122:961-972.
14. Gebbink MFBG, Zondag GCM, Wubbolts RW, Beijersbergen RL, van Etten I, Moolenaar WH. Cell-cell adhesion mediated by a receptor-like protein tyrosine phosphatase. J Biol Chem. 1993;268:16101-16104.
15. Sap J, Jiang YP, Friedlander D, Grumet M, Schlessinger J. Receptor tyrosine phosphatase R-PTP-κ mediates homophilic binding. Mol Cell Biol. 1994;14:1-9.
16. Yu J, Becka S, Zhang P, Zhang X, Brady-Kalnay SM, Wang Z. Tumorderived extracellular mutations of PTPRT/PTPρ are defective in cell adhesion. Mol Cancer Res. 2008;6:1106-1113.
17. Cheng J, Wu K, Armanini M, O'Rourke N, Dowbenko D, Lasky LA. A novel protein-tyrosine phosphatase related to the homotypically adhering κ and μ receptors. J Biol Chem. 1997;272:7264-7277.
18. Brady-Kalnay SM. Protein tyrosine phosphatases. In: Beckerle M, ed. Cell Adhesion: Frontiers in Molecular Biology. Vol. 39. Oxford: Oxford University Press; 2001:217-258.
19. Takai Y, Miyoshi J, Ikeda W, Ogita H. Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat Rev Mol Cell Biol. 2008;9:603-615.
20. Jacobsen CT, Miller RH. Control of astrocyte migration in the developing cerebral cortex. Dev Neurosci. 2003;25:207-216.
21. Brady-Kalnay SM, Tonks NK. Purification and characterization of the human protein tyrosine phosphatase, PTP mu, from a baculovirus expression system. Mol Cell Biochem. 1993;127-128:131-141.
22. Rasband WS, ImageJ. Bethesda, MD: U.S. National Institutes of Health; 1997-2008. Accessed 18 April 2008.
23. Dull T, Zufferey R, Kelly M, et al. A third-generation lentivirus vector with a conditional packaging system. J Virol. 1998;72:8463-8471.
24. Desire L, Bourdin J, Loiseau N, et al. RAC1 inhibition targets amyloid precursor protein processing by gamma-secretase and decreases Abeta production in vitro and in vivo. J Biol Chem. 2005;280:37516-37525.
25. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci U S A. 2004;101:7618-7623.
26. Schimenti KJ, Jacobberger JW. Fixation of mammalian cells for flow cytometric evaluation of DNA content and nuclear immunofluorescence. Cytometry. 1992;13:48-59.
27. Gogolla N, Galimberti I, DePaola V, Caroni P. Preparation of organotypic hippocampal slice cultures for long-term live imaging. Nat Protoc. 2006;1:1165-1171.
28. Yoshida D, Watanabe K, Noha M, Takahashi H, Teramoto A, Sugisaki Y. Anti-invasive effect of an anti-matrix metalloproteinase agent in a murine brain slice model using the serial monitoring of green fluorescent protein-labeled glioma cells. Neurosurgery. 2003;52:187-196.
29. Nakatsuji Y, Miller RH. Density dependent modulation of cell cycle protein expression in astrocytes. J Neurosci Res. 2001;66:487-496.
30. Brady-Kalnay SM, Tonks NK. Identification of the homophilic binding site of the receptor protein tyrosine phosphatase PTPm. J Biol Chem. 1994;269:28472-28477.
31. Gebbink MFBG, Zondag GCM, Koningstein GM, Feiken E, Wubbolts RW, Moolenaar WH. Cell surface expression of receptor protein tyrosine phosphatase RPTPm is regulated by cell-cell contact. J Cell Biol. 1995;131:251-260.
32. Jarzynka MJ, Hu B, Hui KM, et al. ELMO1 and Dock180, a bipartite Rac1 guanine nucleotide exchange factor, promote human glioma cell invasion. Cancer Res. 2007;67:7203-7211.
33. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992;70:401-410.
34. Ulbricht U, Eckerich C, Fillbrandt R, Westphal M, Lamszus K. RNA interference targeting protein tyrosine phosphatase ζ/receptor-type protein tyrosine phosphatase β suppresses glioblastoma growth in vitro and in vivo. J Neurochem. 2006;98:1497-1506.
35. Muller S, Lamszus K, Nikolich K, Westphal M. Receptor protein tyrosine phosphatase ζ as a therapeutic target for glioblastoma therapy. Expert Opin Ther Targets. 2004;8:211-220.
36. Wu M, Gan K, Huang C, et al. LRRC4 controls in vitro invasion of glioblastoma cells through inhibiting RPTP-zeta expression. J Neurooncol. 2006;80:133-142.
37. Mourton T, Hellberg CB, Burden-Gulley SM, Hinman J, Rhee A, Brady-Kalnay SM. The PTPm protein-tyrosine phosphatase binds and recruits the scaffolding protein RACK1 to cell-cell contacts. J Biol Chem. 2001;276:14896-14901.
38. Rosdahl JA, Mourton TL, Brady-Kalnay SM. Protein kinase C δ (PKCδ) is required for protein tyrosine phosphatase μ (PTPμ)-dependent neurite outgrowth. Mol Cell Neurosci. 2002;19:292-306.
39. Ensslen SE, Brady-Kalnay SM. PTPm signaling via PKCμ is instructive for retinal ganglion cell guidance. Mol Cell Neurosci. 2004;25:558-571.
40. Mandil R, Ashkenazi E, Blass M, et al. Protein kinase Ca and protein kinase Cδ play opposite roles in the proliferation and apoptosis of glioma cells. Cancer Res. 2001;61:4612-4619.
41. Renault-Mihara F, Beuvon F, Iturrioz X, et al. Phosphoprotein enriched in astrocytes-15 kDa expression inhibits astrocyte migration by a protein kinase Cδ-dependent mechanism. Mol Biol Cell. 2006;17:5141-5152.
42. Oblander SA, Ensslen-Craig SE, Longo FM, Brady-Kalnay SM. E-cadherin promotes retinal ganglion cell neurite outgrowth in a protein tyrosine phosphatase-mu-dependent manner. Mol Cell Neurosci. 2007;34:481-492.
43. Burden-Gulley SM, Brady-Kalnay SM. PTPm regulates N-cadherindependent neurite outgrowth. J Cell Biol. 1999;144:1323-1336. 44. Brady-Kalnay SM, Mourton T, Nixon JP, et al. Dynamic interaction of PTPmu with multiple cadherins in vivo. J Cell Biol. 1998;141:287-296.
44. Phillips-Mason PJ, Gates TJ, Major DL, Sacks DB, Brady-Kalnay SM. The receptor protein-tyrosine phosphatase PTPm interacts with IQGAP1. J Biol Chem. 2006;281:4903-4910.
45. Aznar S, Fernandez-Valeron P, Espina C, Lacal JC. Rho GTPases: potential candidates for anticancer therapy. Cancer Lett. 2004;206:181-191.
46. Ridley AJ. Rho proteins and cancer. Breast Cancer Res Treat. 2004; 84:13-19.
47. Raftopoulou M, Hall A. Cell migration: rho GTPases lead the way. Dev Biol. 2004;265:23-32.
48. Rosdahl JA, Ensslen SE, Niedenthal JA, Brady-Kalnay SM. PTPmdependent growth cone rearrangement is regulated by Cdc42. J Neurobiol. 2003;56:199-208.
49. Major DL, Brady-Kalnay SM. Rho GTPases regulate PTPm-mediated nasal neurite outgrowth and temporal repulsion of retinal ganglion cell neurons. Mol Cell Neurosci. 2007;34:453-467.