Microglia activate migration of glioma cells through a Pyk2 intracellular pathway

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Rolón Reyes, Kimberleve ^a   Kucheryavykh, Yuriy V ^a   Cubano, Luis A ^a   Inyushin, Mikhail ^a   Skatchkov, Serguei N ^a   Eaton, Misty J ^a   Harrison, Jeffrey K ^b   Kucheryavykh, Lilia Y ^a  

^a Universidad Central del Caribe School of Medicine   (Puerto Rico)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; EPIDERMAL GROWTH FACTOR RECEPTOR; FOCAL ADHESION KINASE 2; GLYCOSYLPHOSPHATIDYLINOSITOL DIACYLGLYCEROL LYASE; PHOSPHOLIPASE A2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL MIGRATION; CENTRIFUGATION; CONTROLLED STUDY; DEGRADATION; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; GLIOMA; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MICROGLIA; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RAT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR ABLATION; TUMOR MICROENVIRONMENT; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN TUMOR; C57BL MOUSE; CELL MOTION; GENE SILENCING; GENETICS; MALE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; TUMOR CELL LINE; TUMOR INVASION; UPREGULATION;

RODENTIA;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; FOCAL ADHESION KINASE 2; GENE KNOCKDOWN TECHNIQUES; GLIOMA; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; NEOPLASM INVASIVENESS; RATS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; UP-REGULATION;

EID: 84939175656     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131059     Document Type: Article

References (58)

1. Laws ER Jr, Goldberg WJ, Bernsteins JJ. Migration of human malignant astrocytoma cells in the mammalian brain: Scherer revisited. Int J Dev Neurosci. 1993;11:691-7. PMID: 8116480
2. Hingtgen S, Figueiredo JL, Farrar C, Duebgen M, Martinez-Quintanilla J, Bhere D, et al. Real-time multimodality imaging of glioblastoma tumor resection and recurrence. J Neurooncol. 2013;111:153-61. doi: 10.1007/s11060-012-1008-z PMID: 23242736
3. Gilbert MR. Recurrent glioblastoma: afresh look at current therapies and emerging novel approaches. Semin Oncol. 2011;38: Suppl 4:S21-33. doi: 10.1053/j.seminoncol.2011.09.008 PMID: 22078645
4. Platten M, Kretz A, Naumann U, Aulwurm S, Egashira K, Isenmann S, et al. Monocyte chemoattractant protein-1 increases microglial infiltration and aggressiveness of gliomas. Ann Neurol. 2003;54:388-92. PMID: 12953273
5. Graeber MB, Scheithauer BW, Kreutzberg GW. Microglia in brain tumors. Glia. 2002;40:252-9. PMID: 12379912
6. Strik HM, Stoll M, Meyermann R. Immune cell infiltration of intrinsic and metastatic intracranial tumours. Anticancer Res. 2004;24:37-42. PMID: 15015573
7. Markovic DS, Glass R, Synowitz M, Rooijen NV, Kettenmann H. Microglia stimulate the invasiveness of glioma cells by increasing the activity of matalloprotease-2. J Neuropathol. Exp. Neurol. 2005;64:754-762. PMID: 16141784
8. Markovic DS, Vinnakota K, Chirasani S, Synowitz M, Raguet H, Stock K, et al. Gliomas induce and exploit microglial MT1-MMPexpression for tumor expansion. Proc. Natl. Acad. Sci. 2009;106:12530-12535. doi: 10.1073/pnas.0804273106 PMID: 19617536
9. Zhai H, Heppner FL, Tsirka SE. Microglia/Macrophages Promote Glioma Progression. Glia. 2011;59:472-485. doi: 10.1002/glia.21117 PMID: 21264953
10. Denny WA. Prodrugs for Gene-Directed Enzyme-Prodrug Therapy (Suicide Gene Therapy). J Biomed Biotechnol. 2003;2003:48-70 PMID: 12686722
11. Jiang YX, Lu Y, Liu TJ, Yang J, Chen Y, Fang YW. Using HSV-TK/GCV suicide gene therapy to inhibit lens epithelial cell proliferation for treatment of posterior capsular opacification. Mol Vis. 2011;17:291-9. PMID: 21283526
12. Jacobs VL, Liu Y, De Leo JA. Propentofylline targets TROY, a novel microglial signaling pathway. PLoSOne. 2012;7:e37955. doi: 10.1371/journal.pone.0037955 PMID: 22649568
13. Roggendorf W, Strupp S, Paulus W. Distribution and characterization of microglia/macrophages in human brain tumours. Acta Neuropathol. 1996;92:288-293. PMID: 8870831
14. Badie B, Schartner J. Role of microglia in glioma biology. Microsc. Res. Tech. 2001;54:106-113. PMID: 11455617
15. Hussain SF, Yang D, Suki D, Aldape K, Grimm E, Heimberger AB. The role of human glioma-infiltrating microglia/macrophages in mediating antitumor immune responses. Neuro. Oncol. 2006;8:261-279. PMID: 16775224
16. Sliwa M, Markovic D, Gabrusiewicz K, Synowitz M, Glass R, Zawadzka M, et al. The invasion promoting effect of microglia on glioblastoma cells is inhibited by cyclosporin A. Brain. 2007;130:476-489. PMID: 17107968
17. Bettinger I, Thanos S, Paulus W. Microglia promote glioma migration. Acta Neuropathol. 2002;103:351-355. PMID: 11904754
18. Li W, Graeber MB. The molecular profile of microglia under the influence of glioma. Neuro Oncol. 2012;14:958-78. doi: 10.1093/neuonc/nos116 PMID: 22573310
19. Eaton MJ, Skatchkov SN, Brune A. SURI and Kir6.1 subunits of K (ATP)-channels are co-localized in retinal glial (Müller) cells. Neuroreport. 2002;13:57-60. PMID: 11924895
20. Watters JJ., Schartner JM, Badie B. Microglia function in braintumors. J. Neurosci. Res. 2005;81:447-455. PMID: 15959903
21. Dunty JM, Schaller MD. The N termini of focal adhesion kinase family members regulate substrate phosphorylation, localization, and cell morphology. J Biol Chem. 2002;277:45644-54. PMID: 12223467
22. Riggs D, Yang Z, Kloss J. The Pyk2 FERM regulates Pyk2 complex formation and phosphorylation. Cell Signal. 2011;23:288-96. doi: 10.1016/j.cellsig.2010.09.015 PMID: 20849950
23. Loftus JC, Yang Z, Tran NL, Kloss J, Viso C, Berens ME, et al. The Pyk2 FERM domain as a target to inhibit glioma migration. Mol Cancer Ther. 2009;8:1505-14. doi: 10.1158/1535-7163. MCT-08-1055 PMID: 19509258
24. Paulino VM, Yang Z, Kloss J, Ennis MJ, Armstrong BA, Loftus JC, et al. TROY (TNFRSF19) is overexpressed in advanced glial tumors and promotes glioblastoma cell invasion via Pyk2-Rac1 signaling. Mol Cancer Res. 2010;8:1558-67. doi: 10.1158/1541-7786. MCR-10-0334 PMID: 20881009
25. Lipinski CA, Tran NL, Menashi E, Rohl C, Kloss J, Bay RC, et al. The tyrosine kinase pyk2 promotes migration and invasion of glioma cells. Neoplasia. 2005;7:435-45. PMID: 15967096
26. Gutenberg A, Brck W, Buchfelder M. Expression of tyrosine kinases FAK and Pyk2 in 331 human astrocytomas. Acta Neuropathol. 2004;108:224-30. PMID: 15221336
27. Lipinski CA, Tran NL, Viso C, Kloss J, Yang Z, Berens ME, et al. Extended survival of Pyk2 or FAK deficient orthotopic glioma xenografts. J Neurooncol. 2008;90:181-9. doi: 10.1007/s 11060-008-9656-8 PMID: 18648907
28. Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, Dosik H, et al. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst. 1973;51:1417-23. PMID: 4357758
29. Fogh J, Fogh JM, Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J. Natl. Cancer Inst. 1977;59:221-226. PMID: 327080
30. Gershwin ME, Ikeda RM, Kawakami TG, Owens RB. Immunobiology of heterotransplanted human tumors in nude mice. J. Natl. Cancer Inst. 1977;58:1455-1463. PMID: 857033
31. Janabi N, Peudenier S, Heron B, Ng KH, Tardieu M. Establishment of human microglial cell lines after transfection of primary cultures of embryonic microglial cells with the SV40 large T antigen. Neurosci Lett. 1995;195:105-108. PMID: 7478261
32. Streit WJ and Kreutzberg GW. Lectin binding by resting and reactive microglia. J Neurocytol. 1987;16:249-60. PMID: 3625239
33. Baugher PJ, Krishnamoorthy L, Price JE, Dharmawardhane SF. Rac1 and Rac3 isoform activation is involved in the invasive and metastatic phonotype of human breast cancer cells. Breast Cancer Res. 2005;7:R965-R974. PMID: 16280046
34. Liu C, Luo D, Streit WJ, Harrison JK. CX3CL1 and CX3CR1 in the GL261 murine model of glioma: CX3CR1 deficiency does not impact tumor growth or infiltration of microglia and lymphocytes. J Neuroimmunol. 2008;198:98-105. doi: 10.1016/j.jneuroim.2008.04.016 PMID: 18508133
35. Kucheryavykh LY, Kucheryavykh YV, Rolón-Reyes K, Skatchkov SN, Eaton MJ, Cubano LA, et al. Visualization of implanted GL261 glioma cells in living mouse brain slices using fluorescent 4-(4-(dimethylamino)-styryl)-N-methylpyridinium iodide (ASP+). Biotechniques, 2012;0:1-4. doi: 10.2144/000113926 PMID: 22946677
36. Heppner FL, Greter M, Marino D, Falsig J, Raivich G, Hövelmeyer N, et al. Experimental autoimmune encephalomyelitis repressed by microglial paralysis. Nat Med. 2005;11:146-52. PMID: 15665833
37. Roberts WG, Ung E, Whalen P, Cooper B, Hulford C, Autry C, et al. Antitumor activity and pharmacology of a selective focal adhesion kinase inhibitor, PF-562, 271. Cancer Res. 2008;68:1935-44. doi: 10.1158/0008-5472. CAN-07-5155 PMID: 18339875
38. Kucheryavykh YV, Kucheryavykh LY, Nichols CG, Maldonado HM, Baksi K, Reichenbach A, et al. Downregulation of Kir4.1 Inward Rectifying Potassium Channel Subunit Expression by RNAi Impairs Potassium Transfer and Glutamate Uptake by Cultured Cortical Astrocytes. Glia, 2007;55:274-281. PMID: 17091490
39. Tian D, Litvak V, Lev S. Cerebral ischemia and seizures induce tyrosine phosphorylation of PYK2 in neurons and microglial cells. J Neurosci. 2002;20:6478-87.
40. Combs CK, Johnson DE, Cannady SB, Lehman TM, Landreth GE. Identification of microglial signal transduction pathways mediating a neurotoxic response to amyloidogenic fragments of beta-amyloid and prion proteins. J Neurosci. 1999;19:928-39. PMID: 9920656
41. Rolls A, Avidan H, Cahalon L, Schori H, Bakalash S, Litvak V, et al. A disaccharide derived from chondroitin sulphate proteoglycan promotes central nervous system repair in rats and mice. Eur J Neurosci. 2004;20:1973-83. PMID: 15450076
42. Graeber MB, Streit WJ. Microglia: biology and pathology. Acta Neuropathol. 2010;119:89-105. doi: 0.1007/s00401-009-0622-0 PMID: 20012873
43. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat Neurosci. 2007;10:1387-94. PMID: 17965659
44. Gabrusiewicz K, Ellert-Miklaszewska A, Lipko M, Sielska M, Frankowska M, Kaminska B. Characteristics of the alternative phenotype of microglia/macrophages and its modulation in experimental gliomas. PLoS One. 2011;6:e23902. doi: 10.1371/journal.pone.0023902 PMID: 21901144
45. Rao JS. Molecular mechanisms of glioma invasiveness: the role of proteases. Nat. Rev. Cancer. 2003;3:489-501. PMID: 12835669
46. Platten M, Wick W, Weller M. Malignant glioma biology: role forTGF-beta in growth, motility, angiogenesis, and immune escape. Microsc Res Tech. 2001;52:401-10. PMID: 11170299
47. Arnold T, Betsholtz C. The importance of microglia in the development of the vasculature in the central nervous system. Vasc Cell. 2013;5:4. doi: 10.1186/2045-824X-5-4 PMID: 23422217
48. Charles NA, Holland EC, Gilbertson R, Glass R, Kettenmann H. (2011) The brain tumor microenvironment. Glia. 2011;59:1169-1180. doi: 10.1002/glia.21136 PMID: 21446047
49. Sloane BF, Rozhin J, Robinson D, Honn KV. Role for cathepsin B and cystatins in tumor growth and progression. Biol. Chem. HoppeSeyler. 1990;371: Suppl, 193-198. PMID: 2400581
50. Rempel SA, Rosenblum ML, Mikkelsen T, Yan PS, Ellis KD, Golembieski WA, et al. Cathepsin B expression and localization in glioma progression and invasion. Cancer Res. 1994;54:6027-6031. PMID: 7954439
51. Mai J, Sameni M, Mikkelsen T, Sloane BF. Degradation of extracellular matrix protein tenascin-C by cathepsin B: an interaction involved in the progression of gliomas. Biol. Chem. 2002;383:1407-1413. PMID: 12437133
52. Flannery T, Gibson D, Mirakhur M, McQuaid S, Greenan C, Trimble A, et al. The Clinical Significance of Cathepsin S Expression in Human Astrocytomas. Am. J. Path. 2003;163:175-182. PMID: 12819022
53. Thota B, Arimappamagan A, Kandavel T, Shastry AH, Pandey P, Chandramouli BA, et al. STAT-1 expression is regulated by IGFBP-3in malignant glioma cells and is a strong predictor of poor survival in patients with glioblastoma. J Neurosurg. 2014;121:374-83. doi: 10.3171/2014.4. JNS131198 PMID: 24878287
54. Fan YC, Zhu YS, Mei PJ, Sun SG, Zhang H, Chen HF, et al. Cullin1 regulates proliferation, migration and invasion of glioma cells. Med Oncol. 2014;31:227. doi: 10.1007/s12032-014-0227-x PMID: 25201578
55. Zhang X, Ding Z, Mo J, Sang B, Shi Q, Hu J, et al. GOLPH3 promotes glioblastoma cell migration and invasion via the mTOR-YB1 pathway in vitro. Mol. Carcinog. 2014 Aug. 23. doi: 10.1002/mc.22197
56. La Porta C. AQP1 is not only a water channel: It contributes to cell migration through Lin7/beta-catenin. Cell Adh Migr. 2010 Apr-Jun; 4(2):204-6. PMID: 20168076
57. Yang M, Li Y, Chilukuri K, Brady OA, Boulos MI, Kappes JC, et al. L1 stimulation of human glioma cell motility correlates with FAK activation. J Neurooncol. 2011;105:27-44. doi: 10.1007/s11060-011-0557-x PMID: 21373966
58. Lindemann C, Hackmann O, Delic S, Schmidt N, Reifenberger G, Riemenschneider MJ. SOCS3 promoter methylation is mutually exclusive to EGFR amplification in gliomas and promotes glioma cell invasion through STAT3and FAK activation. Acta Neuropathol. 2011;122:241-51. doi: 10.1007/s00401-011-0832-0 PMID: 21590492