Opposing signaling of ROCK1 and ROCK2 determines the switching of substrate specificity and the mode of migration of glioblastoma cells

Molecular Neurobiology

Volumn 49, Issue 2, 2014, Pages 900-915

  Mertsch, Sonja ^a   Thanos, Solon ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Cell lines; Cell signaling; Glioblastoma multiforme; Migration; Stripe assay

Indexed keywords

REGULATOR PROTEIN; RHO KINASE; RHO KINASE 1; RHO KINASE 2; UNCLASSIFIED DRUG; ROCK1 PROTEIN, HUMAN; ROCK2 PROTEIN, HUMAN;

ANTIDROMIC STIMULATION; ARTICLE; CELL ASSAY; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SPECIFICITY; GLIOBLASTOMA; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; NERVE CELL STIMULATION; REGULATORY MECHANISM; TUMOR CELL LINE; TUMOR INVASION; BIOSYNTHESIS; BRAIN TUMOR; CELL MOTION; GENE SILENCING; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; GENE KNOCKDOWN TECHNIQUES; GLIOBLASTOMA; HUMANS; RHO-ASSOCIATED KINASES; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 84896544493     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8568-6     Document Type: Article

References (49)

1. Louis DN et al (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathologica 114:97-109. doi: 10.1007/s00401-007-0243-4 (Pubitemid 47103521)
2. Giese A (2003) Glioma invasion - pattern of dissemination by mechanisms of invasion and surgical intervention, pattern of gene expression and its regulatory control by tumor suppressor p53 and protooncogene ETS-1. Acta Neurochirurgica Suppl 88:153-162
3. Guillamo JS et al (2001) Migration pathways of human glioblastoma cells xenografted into the immunosuppressed rat brain. J Neuro-Oncol 52:205-215 (Pubitemid 33638519)
4. Oellers P et al (2009) A coculture assay to visualize and monitor interactions between migrating glioma cells and nerve fibers. Nature Protocols 4:923-927. doi:10.1038/nprot.2009.62
5. Pilkington GJ (1994) Tumour cell migration in the central nervous system. Brain Pathol 4:157-166
6. Scherer HJ (1940) A critical review: the pathology of cerebral gliomas. J Neurol Psychiatr 3:147-177
7. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Ann Rev Cell Dev Biol 21:247-269. doi:10.1146/annurev.cellbio.21.020604.150721 (Pubitemid 41740635)
8. Ridley AJ (2004) Rho proteins and cancer. Breast Cancer Res Treat 84:13-19. doi:10.1023/B:BREA.0000018423.47497.c6
9. Sahai E, Marshall CJ (2002) ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat Cell Biol 4:408-415. doi:10.1038/ncb796 (Pubitemid 34746158)
10. Amano M, Fukata Y, Kaibuchi K (2000) Regulation and functions of Rho-associated kinase. Exp Cell Res 261:44-51. doi:10.1006/excr.2000.5046
11. Amano M, Fukata Y, Shimokawa H, Kaibuchi K (2000) Purification and in vitro activity of Rho-associated kinase. Methods Enzymol 325:149-155
12. Riento K, Ridley AJ (2003) ROCKs: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4:446-456. doi:10.1038/nrm1128 (Pubitemid 36648590)
13. Muller JM et al (2002) The transcriptional coactivator FHL2 transmits Rho signals from the cell membrane into the nucleus. EMBO J 21:736-748 (Pubitemid 34174054)
14. Su LF, Knoblauch R, Garabedian MJ (2001) Rho GTPases as modulators of the estrogen receptor transcriptional response. J Biol Chem 276:3231-3237. doi:10.1074/jbc.M005547200
15. Yamazaki D, Kurisu S, Takenawa T (2009) Involvement of Rac and Rho signaling in cancer cell motility in 3D substrates. Oncogene 28: 1570-1583. doi:10.1038/onc.2009.2
16. Oellers P, Schroer U, Senner V, Paulus W, Thanos S (2009) ROCKs are expressed in brain tumors and are required for glioma-cell migration on myelinated axons. Glia 57:499-509. doi:10.1002/glia.20777
17. Mertsch S, Oellers P, Wendling M, Stracke W, Thanos S (2013) Dissecting the inter-substrate navigation of migrating glioblastoma cells with the stripe assay reveals a causative role of ROCK. Mol Neurobiol 48:169-179. doi:10.1007/s12035-013-8429-3
18. Mertsch S, Schurgers LJ, Weber K, Paulus W, Senner V (2009) Matrix gla protein (MGP): an overexpressed and migration-promoting mesenchymal component in glioblastoma. BMC cancer 9:302. doi:10.1186/1471-2407-9-302
19. Bigner DD et al (1981) Heterogeneity of genotypic and phenotypic characteristics of fifteen permanent cell lines derived from human gliomas. J Neuropathol Exp Neurol 40:201-229 (Pubitemid 12168784)
20. Bilzer T et al (1991) Morphological, immunocytochemical and growth characteristics of three human glioblastomas established in vitro. Virchows Archiv A, Pathol Anat Histopathol 418:281-293
21. Knoll B, Weinl C, Nordheim A, Bonhoeffer F (2007) Stripe assay to examine axonal guidance and cell migration. Nature Protocols 2: 1216-1224. doi:10.1038/nprot.2007.157 (Pubitemid 46901301)
22. Croft DR, Olson MF (2006) The Rho GTPase effector ROCK regulates cyclin A, cyclin D1, and p27Kip1 levels by distinct mechanisms. Mol Cell Biol 26:4612-4627. doi:10.1128/MCB.02061-05 (Pubitemid 43877579)
23. Chen J, Guerriero E, Lathrop K, SundarRaj N (2008) Rho/ROCK signaling in regulation of corneal epithelial cell cycle progression. Investig Ophthalmol Vis Sci 49:175-183. doi:10.1167/iovs.07-0488
24. Iwamoto H, Nakamuta M, Tada S, Sugimoto R, Enjoji M, Nawata H (2000) A p160ROCK-specific inhibitor, Y-27632, attenuates rat hepatic stellate cell growth. J Hepatol 32:762-770 (Pubitemid 30262736)
25. Shtutman M et al (1999) The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 96:5522-5527 (Pubitemid 29234650)
26. Tetsu O, McCormick F (1999) Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422-426. doi:10.1038/18884 (Pubitemid 29180374)
27. Boku S, Nakagawa S, Toda H, Kato A, Takamura N, Omiya Y, Inoue T, Koyama T (2013) ROCK2 regulates bFGF-induced proliferation of SH-SY5Y cells through GSK-3beta and beta-catenin pathway. Brain Research 1492:7-17
28. Deng L, Li G, Li R, Liu Q, He Q, Zhang J (2010) Rho-kinase inhibitor, fasudil, suppresses glioblastoma cell line progression in vitro and in vivo. Cancer Biol Ther 9:875-884
29. Nakabayashi H, Shimizu K (2011) HA1077, a Rho kinase inhibitor, suppresses glioma-induced angiogenesis by targeting the Rho-ROCK and the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase (MEK/ERK) signal pathways. Cancer Sci 102:393-399. doi:10.1111/j.1349-7006.2010. 01794.x
30. Vielmetter J, Stolze B, Bonhoeffer F, Stuermer CA (1990) In vitro assay to test differential substrate affinities of growing axons and migratory cells. Exp Brain Res Experimentelle Hirnforschung Exp Cerebrale 81:283-287 (Pubitemid 20216603)
31. Walter J, Kern-Veits B, Huf J, Stolze B, Bonhoeffer F (1987) Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development 101:685-696 (Pubitemid 18044539)
32. Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol: off J Am Soc Clin Oncol 21:1624-1636. doi:10.1200/JCO.2003.05.063 (Pubitemid 46594118)
33. Maidment SL (1997) The cytoskeleton and brain tumour cell migration. Anticancer Res 17:4145-4149
34. Raftopoulou M, Hall A (2004) Cell migration: Rho GTPases lead the way. Dev Biol 265:23-32 (Pubitemid 38018819)
35. Nobes CD, Hall A (1999) Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol 144:1235-1244 (Pubitemid 29157301)
36. Eden S, Rohatgi R, Podtelejnikov AV, Mann M, Kirschner MW (2002) Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790-793. doi:10.1038/nature00859
37. Rohatgi R et al (1999) The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97:221-231
38. Mori K et al (2009) Rho-kinase contributes to sustained RhoA activation through phosphorylation of p190A RhoGAP. J Biol Chem 284:5067-5076. doi:10.1074/jbc.M806853200
39. Maekawa M et al (1999) Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285:895-898 (Pubitemid 29381991)
40. Arber S et al (1998) Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393:805-809. doi:10.1038/31729 (Pubitemid 28299494)
41. Sanders LC, Matsumura F, Bokoch GM, de Lanerolle P (1999) Inhibition of myosin light chain kinase by p21-activated kinase. Science 283:2083-2085
42. Hotchin NA, Hall A (1995) The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J Cell Biol 131:1857-1865 (Pubitemid 26007981)
43. Settleman J, Narasimhan V, Foster LC, Weinberg RA (1992) Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from ras to the nucleus. Cell 69:539-549
44. Kolanus W, Seed B (1997) Integrins and inside-out signal transduction: converging signals from PKC and PIP3. Curr Opin Cell Biol 9:725-731 (Pubitemid 27424930)
45. Schwartz MA, Schaller MD, Ginsberg MH (1995) Integrins: emerging paradigms of signal transduction. Ann Rev Cell Dev Biol 11:549-599. doi:10.1146/annurev.cb.11.110195.003001 (Pubitemid 26019614)
46. Shimizu Y, Mobley JL, Finkelstein LD, Chan AS (1995) A role for phosphatidylinositol 3-kinase in the regulation of beta 1 integrin activity by the CD2 antigen. J Cell Biol 131:1867-1880 (Pubitemid 26007982)
47. Lingor P et al (2008) ROCK inhibition and CNTF interact on intrinsic signalling pathways and differentially regulate survival and regeneration in retinal ganglion cells. Brain: J Neurol 131:250-263. doi:10.1093/brain/awm284
48. Ming XF et al (2002) Rho GTPase/Rho kinase negatively regulates endothelial nitric oxide synthase phosphorylation through the inhibition of protein kinase B/Akt in human endothelial cells. Mol Cell Biol 22:8467-8477
49. Wolfrum S et al (2004) Inhibition of Rho-kinase leads to rapid activation of phosphatidylinositol 3-kinase/protein kinase Akt and cardiovascular protection. Arterioscler Thromb Vasc Biol 24:1842-1847. doi:10.1161/01.ATV. 0000142813.33538.82 (Pubitemid 39350301)