A specific isoform of glial cell line-derived neurotrophic factor family receptor alpha 1 regulates RhoA expression and glioma cell migration

Journal of Neurochemistry

Volumn 115, Issue 3, 2010, Pages 759-770

  Wan, Guoqiang ^a,b   Too, Heng Phon ^a,b  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

C6 glioma; Cell migration; GDNF; GFR 1; RhoA; Spliced isoform

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR FAMILY RECEPTOR ALPHA 1A; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR FAMILY RECEPTOR ALPHA 1B; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR; GUANOSINE TRIPHOSPHATASE; NERVE CELL ADHESION MOLECULE; PROTEIN RET; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA SMALL GUANOSINE TRIPHOSPHATASE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER INHIBITION; CANCER INVASION; CELL ELONGATION; CELL MIGRATION; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE SILENCING; GLIOBLASTOMA; GLIOMA CELL; IN VITRO STUDY; MIGRATION INHIBITION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELL DIVISION; CELL MOVEMENT; FLUORESCENT ANTIBODY TECHNIQUE; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR RECEPTORS; GLIOMA; ISOMERISM; MICROSCOPY, CONFOCAL; NEOPLASM INVASIVENESS; NEURAL CELL ADHESION MOLECULES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 78651277157     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06975.x     Document Type: Article

References (51)

1. Airaksinen M. S. and Saarma M. (2002) The GDNF family: Signalling, biological functions and therapeutic value. Nat. Rev. Neurosci. 3, 383-394.
2. Auer R. N., Del Maestro R. F. and Anderson R. (1981) A simple and reproducible experimental in vivo glioma model. Can. J. Neurol. Sci. 8, 325-331.
3. Barth R. F. (1998) Rat brain tumor models in experimental neurooncology: The 9L, C6, T9, F98, RG2 (D74), RT-2 and CNS-1 gliomas. J. Neurooncol. 36, 91-102.
4. Benda P., Lightbody J., Sato G., Levine L. and Sweet W. (1968) Differentiated rat glial cell strain in tissue culture. Science 161, 370-371.
5. Boran M. S. and Garcia A. (2007) The cyclic GMP-protein kinase G pathway regulates cytoskeleton dynamics and motility in astrocytes. J. Neurochem. 102, 216-230.
6. Brozzi F., Arcuri C., Giambanco I. and Donato R. (2009) S100B protein regulates astrocyte shape and migration via interaction with src kinase: Implications for astrocyte development, activation, and tumor growth. J. Biol. Chem. 284, 8797-8811.
7. Cao L., Su Z., Zhou Q. et al. (2006) Glial cell line-derived neurotrophic factor promotes olfactory ensheathing cells migration. Glia 54, 536-544.
8. Couldwell W. T., Yong V. W., Dore-Duffy P., Freedman M. S. and Antel J. P. (1992) Production of soluble autocrine inhibitory factors by human glioma cell lines. J. Neurol. Sci. 110, 178-185.
9. DeAngelis L. M. (2001) Brain tumors. N. Engl. J. Med. 344, 114-123.
10. Demuth T. and Berens M. E. (2004) Molecular mechanisms of glioma cell migration and invasion. J. Neurooncol. 70, 217-228.
11. Dey B. K., Wong Y. W. and Too H. P. (1998) Cloning of a novel murine isoform of the glial cell line-derived neurotrophic factor receptor. Neuroreport 9, 37-42.
12. El-Obeid A., Bongcam-Rudloff E., Sorby M., Ostman A., Nister M. and Westermark B. (1997) Cell scattering and migration induced by autocrine transforming growth factor alpha in human glioma cells in vitro. Cancer Res. 57, 5598-5604.
13. Giese A. and Westphal M. (1996) Glioma invasion in the central nervous system. Neurosurgery 39, 235-250.
14. Grobben B., De Deyn P. P. and Slegers H. (2002) Rat C6 glioma as experimental model system for the study of glioblastoma growth and invasion. Cell Tissue Res. 310, 257-270.
15. Guo X. J., Fantini J., Roubin R., Marvaldi J. and Rougon G. (1990) Evaluation of the effect of suramin on neural cell growth and N-CAM expression. Cancer Res. 50, 5164-5170.
16. Ho S. N., Hunt H. D., Horton R. M., Pullen J. K. and Pease L. R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
17. Hoelzinger D. B., Demuth T. and Berens M. E. (2007) Autocrine factors that sustain glioma invasion and paracrine biology in the brain microenvironment. J. Natl Cancer Inst. 99, 1583-1593.
18. Iwanicki M. P., Vomastek T., Tilghman R. W., Martin K. H., Banerjee J., Wedegaertner P. B. and Parsons J. T. (2008) FAK, PDZRhoGEF and ROCKII cooperate to regulate adhesion movement and trailing-edge retraction in fibroblasts. J. Cell Sci. 121, 895-905.
19. Iwase T., Jung C. G., Bae H., Zhang M. and Soliven B. (2005) Glial cell line-derived neurotrophic factor-induced signaling in Schwann cells. J. Neurochem. 94, 1488-1499.
20. Koochekpour S., Jeffers M., Rulong S., Taylor G., Klineberg E., Hudson E. A., Resau J. H. and Vande Woude G. F. (1997) Met and hepatocyte growth factor/scatter factor expression in human gliomas. Cancer Res. 57, 5391-5398.
21. Lange K., Kammerer M., Saupe F., Hegi M. E., Grotegut S., Fluri E. and Orend G. (2008) Combined lysophosphatidic acid/plateletderived growth factor signaling triggers glioma cell migration in a tenascin-C microenvironment. Cancer Res. 68, 6942-6952.
22. Lin L. F., Doherty D. H., Lile J. D., Bektesh S. and Collins F. (1993) GDNF: A glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260, 1130-1132.
23. Lu C. and Shervington A. (2008) Chemoresistance in gliomas. Mol. Cell. Biochem. 312, 71-80.
24. Lu D. Y., Leung Y. M., Cheung C. W., Chen Y. R. and Wong K. L. (2010) Glial cell line-derived neurotrophic factor induces cell migration and matrix metalloproteinase-13 expression in glioma cells. Biochem. Pharmacol. 80, 1201-1209.
25. Mohseni M. and Chishti A. H. (2008) The headpiece domain of dematin regulates cell shape, motility, and wound healing by modulating RhoA activation. Mol. Cell. Biol. 28, 4712-4718.
26. Nakada M., Nakada S., Demuth T., Tran N. L., Hoelzinger D. B. and Berens M. E. (2007) Molecular targets of glioma invasion. Cell. Mol. Life Sci. 64, 458-478.
27. Natarajan M., Stewart J. E., Golemis E. A., Pugacheva E. N., Alexandropoulos K., Cox B. D., Wang W., Grammer J. R. and Gladson C. L. (2006) HEF1 is a necessary and specific downstream effector of FAK that promotes the migration of glioblastoma cells. Oncogene 25, 1721-1732.
28. Ng W. H., Wan G. Q., Peng Z. N. and Too H. P. (2009) Glial cell-line derived neurotrophic factor (GDNF) family of ligands confer chemoresistance in a ligand-specific fashion in malignant gliomas. J. Clin. Neurosci. 16, 427-436.
29. Oh-hashi K., Ito M., Tanaka T., Hirata Y. and Kiuchi K. (2009) Biosynthesis, processing, and secretion of glial cell line-derived neurotrophic factor in astroglial cells. Mol. Cell. Biochem. 323, 1-7.
30. Okada Y., Takeyama H., Sato M., Morikawa M., Sobue K., Asai K., Tada T., Kato T. and Manabe T. (1999) Experimental implication of celiac ganglionotropic invasion of pancreatic-cancer cells bearing c-ret proto-oncogene with reference to glial-cell-line-derived neurotrophic factor (GDNF). Int. J. Cancer 81, 67-73.
31. Paratcha G., Ledda F. and Ibanez C. F. (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113, 867-879.
32. Paratcha G., Ibanez C. F. and Ledda F. (2006) GDNF is a chemoattractant factor for neuronal precursor cells in the rostral migratory stream. Mol. Cell. Neurosci. 31, 505-514.
33. Ramnarain D. B., Park S., Lee D. Y. et al. (2006) Differential gene expression analysis reveals generation of an autocrine loop by a mutant epidermal growth factor receptor in glioma cells. Cancer Res. 66, 867-874.
34. Ridley A. J., Schwartz M. A., Burridge K., Firtel R. A., Ginsberg M. H., Borisy G., Parsons J. T. and Horwitz A. R. (2003) Cell migration: Integrating signals from front to back. Science 302, 1704-1709.
35. Sariola H. and Saarma M. (2003) Novel functions and signalling pathways for GDNF. J. Cell Sci. 116, 3855-3862.
36. Shefelbine S. E., Khorana S., Schultz P. N. et al. (1998) Mutational analysis of the GDNF/RET-GDNFR alpha signaling complex in a kindred with vesicoureteral reflux. Hum. Genet. 102, 474-478.
37. Shimizu A., Mammoto A., Italiano J. E., Jr, Pravda E., Dudley A. C., Ingber D. E. and Klagsbrun M. (2008) ABL2/ARG tyrosine kinase mediates SEMA3F-induced RhoA inactivation and cytoskeleton collapse in human glioma cells. J. Biol. Chem. 283, 27230-27238.
38. Sibenaller Z. A., Etame A. B., Ali M. M., Barua M., Braun T. A., Casavant T. L. and Ryken T. C. (2005) Genetic characterization of commonly used glioma cell lines in the rat animal model system. Neurosurg. Focus 19, E1.
39. Song H. and Moon A. (2006) Glial cell-derived neurotrophic factor (GDNF) promotes low-grade Hs683 glioma cell migration through JNK, ERK-1/2 and p38 MAPK signaling pathways. Neurosci. Res. 56, 29-38.
40. Su C. M., Lu D. Y., Hsu C. J. et al. (2009) Glial cell-derived neurotrophic factor increases migration of human chondrosarcoma cells via ERK and NF-kappaB pathways. J. Cell. Physiol. 220, 499-507.
41. Too H. P. (2003) Real time PCR quantification of GFRalpha-2 alternatively spliced isoforms in murine brain and peripheral tissues. Brain Res. Mol. Brain Res. 114, 146-153.
42. Veit C., Genze F., Menke A., Hoeffert S., Gress T. M., Gierschik P. and Giehl K. (2004) Activation of phosphatidylinositol 3-kinase and extracellular signal-regulated kinase is required for glial cell linederived neurotrophic factor-induced migration and invasion of pancreatic carcinoma cells. Cancer Res. 64, 5291-5300.
43. Wen P. Y. and Kesari S. (2008) Malignant gliomas in adults. N. Engl. J. Med. 359, 492-507.
44. Wiesenhofer B., Stockhammer G., Kostron H., Maier H., Hinterhuber H. and Humpel C. (2000) Glial cell line-derived neurotrophic factor (GDNF) and its receptor (GFR-alpha 1) are strongly expressed in human gliomas. Acta Neuropathol. 99, 131-137.
45. Yamana N., Arakawa Y., Nishino T. et al. (2006) The Rho-mDia1 pathway regulates cell polarity and focal adhesion turnover in migrating cells through mobilizing Apc and c-Src. Mol. Cell. Biol. 26, 6844-6858.
46. Yamazaki D., Kurisu S. and Takenawa T. (2005) Regulation of cancer cell motility through actin reorganization. Cancer Sci. 96, 379-386.
47. Yan B., Chour H. H., Peh B. K., Lim C. and Salto-Tellez M. (2006) RhoA protein expression correlates positively with degree of malignancy in astrocytomas. Neurosci. Lett. 407, 124-126.
48. Yoong L. F., Peng Z. N., Wan G. and Too H. P. (2005) Tissue expression of alternatively spliced GFRalpha1, NCAM and RET isoforms and the distinct functional consequence of ligandinduced activation of GFRalpha1 isoforms. Brain Res. Mol. Brain Res. 139, 1-12.
49. Yoong L. F., Wan G. and Too H. P. (2009) GDNF-induced cell signaling and neurite outgrowths are differentially mediated by GFRalpha1 isoforms. Mol. Cell. Neurosci. 41, 464-473.
50. You L., Ebner S. and Kruse F. E. (2001) Glial cell-derived neurotrophic factor (GDNF)-induced migration and signal transduction in corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 42, 2496-2504.
51. Zhang X., Li X., Wu J. W., Gao D. K., Liang J. W. and Liu X. Z. (2002) Experiment and observation on invasion of brain glioma in vivo. J. Clin. Neurosci. 9, 668-671.