Silencing GFAP isoforms in astrocytoma cells disturbs laminin-dependent motility and cell adhesion

FASEB Journal

Volumn 28, Issue 7, 2014, Pages 2942-2954

  Moeton, Martina ^a   Kanski, Regina ^a   Stassen, Oscar M J A ^a   Sluijs, Jacqueline A ^a,b   Geerts, Dirk ^c   Van Tijn, Paula ^a,d   Wiche, Gerhard ^e   Van Strien, Miriam E ^a   Hol, Elly M ^a,b,f  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d HUBRECHT INSTITUTE   (Netherlands)

^e UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Cytoskeleton; Extracellular matrix; Glia; Glioma; Intermediate filaments

Indexed keywords

GFAP ALPHA; GLIAL FIBRILLARY ACIDIC PROTEIN; INTEGRIN; ISOPROTEIN; LAMININ; LENTIVIRUS VECTOR; PLECTIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOMA CELL; ASTROCYTOMA CELL LINE; CELL ADHESION; CELL CYCLE PROGRESSION; CELL MOTILITY; CELL PROLIFERATION; CELL SPREADING; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EXTRACELLULAR MATRIX; FLOW CYTOMETRY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LENTIVIRINAE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE;

CYTOSKELETON; EXTRACELLULAR MATRIX; GLIA; GLIOMA; INTERMEDIATE FILAMENTS;

ASTROCYTES; ASTROCYTOMA; BRAIN; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DOWN-REGULATION; EXTRACELLULAR MATRIX; GLIAL FIBRILLARY ACIDIC PROTEIN; HEK293 CELLS; HUMANS; INTEGRINS; LAMININ; PROTEIN ISOFORMS;

EID: 84903737788     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-245837     Document Type: Article

References (55)

1. Middeldorp, J., Boer, K., Sluijs, J. A., De Filippis, L., Encha-Razavi, F., Vescovi, A. L., Swaab, D. F., Aronica, E., and Hol, E. M. (2010) GFAPdelta in radial glia and subventricular zone progenitors in the developing human cortex. Development 137, 313-321
2. Roelofs, R. F., Fischer, D. F., Houtman, S. H., Sluijs, J. A., Van, H. W., Van Leeuwen, F. W., and Hol, E. M. (2005) Adult human subventricular, subgranular, and subpial zones contain astro-cytes with a specialized intermediate filament cytoskeleton. Glia 52, 289-300 (Pubitemid 43076221)
3. Sanai, N., Tramontin, A. D., Quinones-Hinojosa, A., Barbaro, N. M., Gupta, N., Kunwar, S., Lawton, M. T., McDermott, M. W., Parsa, A. T., Manuel-García Verdugo, J., Berger, M. S., and Alvarez-Buylla, A. (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427, 740-744 (Pubitemid 38294593)
4. Sofroniew, M. V., and Vinters, H. V. (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35
5. Chung, B.-M., Rotty, J. D., and Coulombe, P. A. (2013) Networking galore: intermediate filaments and cell migration. Curr. Opin. Cell Biol. 25, 600-612
6. Ho, C.-L., and Liem, R. K. H. (1996) Intermediate filaments in the nervous system: implications in cancer. Cancer Metastasis Rev. 15, 483-497 (Pubitemid 27067167)
7. Deck, J. H. N., Eng, L. F., Bigbee, J., and Woodcock, S. M. (1978) The role of glial fibrillary acidic protein in the diagnosis of central nervous system tumors. Acta Neuropathol. (Berl.) 42, 183-190 (Pubitemid 9019233)
8. Louis, D. N., Ohgaki, H., Wiestler, O. D., Cavenee, W. K., Burger, P. C., Jouvet, A., Scheithauer, B. W., and Kleihues, P. (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. (Berl.) 114, 97-109 (Pubitemid 47103521)
9. Rousseau, A., Nutt, C. L., Betensky, R. A., Iafrate, A. J., Han, M., Ligon, K. L., Rowitch, D. H., and Louis, D. N. (2006) Expression of oligodendroglial and astrocytic lineage markers in diffuse gliomas: use of YKL-40, ApoE, ASCL1, and NKX2-2. J. Neuro-pathol. 65, 1149-1156 (Pubitemid 44888831)
10. Rutka, J. T., Murakami, M., Dirks, P. B., Hubbard, S. L., Becker, L. E., Fukuyama, K., Jung, S., Tsugu, A., and Matsuzawa, K. (1997) Role of glial filaments in cells and tumors of glial origin: a review. J. Neurosurg. 87, 420-430 (Pubitemid 27362576)
11. Yung W-K, Luna, M., and Borit, A. (1985) Vimentin and glial fibrillary acidic protein in human brain tumors. J. Neurooncol. 3, 35-38 (Pubitemid 15100182)
12. Rebetz, J., Tian, D., Persson, A., Widegren, B., Salford, L. G., Englund, E., Gisselsson, D., and Fan, X. (2008) Glial progenitorlike phenotype in low-grade glioma and enhanced CD133-expression and neuronal lineage differentiation potential in high-grade glioma. PLoS ONE 3, e1936
13. Skalli, O., Wilhelmsson, U., Örndahl, C., Fekete, B., Malmgren, K., Rydenhag, B., and Pekny, M. (2013) Astrocytoma grade IV (glioblastoma multiforme) displays 3 subtypes with unique expression profiles of intermediate filament proteins. Hum. Pathol. 44, 2081-2088
14. Jacque, C. M., Vinner, C., Kujas, M., Raoul, M., Racadot, J., and Baumann, N. A. (1978) Determination of glial fibrillary acidic protein (GFAP) in human brain tumors. J. Neurol. Sci. 35, 147-155 (Pubitemid 8251566)
15. Niu, C.-S. (2011) Expression of NANOG in human gliomas and its relationship with undifferentiated glioma cells. Oncol. Rep. 26, 593-601
16. Velasco, M. E., Dahl, D., Roessmann, U., and Gambetti, P. (1980) Immunohistochemical localization of glial fibrillary acidic protein in human glial neoplasms. Cancer 45, 484-494 (Pubitemid 10169294)
17. Choi, K. C., Kwak, S. E., Kim, J. E., Sheen, S. H., and Kang, T. C. (2009) Enhanced glial fibrillary acidic protein-delta expression in human astrocytic tumor. Neurosci. Lett. 463, 182-187
18. Heo, D. H., Kim, S. H., Yang, K. M., Cho, Y. J., Kim, K. N., Yoon do, H., and Kang, T. C. (2012) A histopathological diagnostic marker for human spinal astrocytoma: expression of glial fibril-lary acidic protein-delta. J. Neurooncol. 108, 45-52
19. Kamphuis, W., Middeldorp, J., Kooijman, L., Sluijs, J. A., Kooi, E., Moeton, M., Freriks, M., Mizee, M. R., and Hol, E. M. (2014) Glial fibrillary acidic protein isoform expression in plaque related astrogliosis in Alzheimer's disease. Neurobiol. Aging 35, 492-510
20. Middeldorp, J., and Hol, E. M. (2011) GFAP in health and disease. Prog. Neurobiol. 93, 421-443
21. Van den Berge, S. A., Middeldorp, J., Zhang, C. E., Curtis, M. A., Leonard, B. W., Mastroeni, D., Voorn, P., van de Berg, W. D., Huitinga, I., and Hol, E. M. (2010) Longterm quiescent cells in the aged human subventricular neurogenic system specifically express GFAP-delta. Aging Cell 9, 313-326
22. Vescovi, A. L., Galli, R., and Reynolds, B. A. (2006) Brain tumour stem cells. Nat. Rev. Cancer 6, 425-436
23. Middeldorp, J., Kamphuis, W., Sluijs, J. A., Achoui, D., Leenaars, C. H., Feenstra, M. G., van Tijn P., Fischer, D. F., Berkers, C., Ovaa, H., Quinlan, R. A., and Hol, E. M. (2009) Intermediate filament transcription in astrocytes is repressed by protea-some inhibition. FASEB J. 23, 2710-2726
24. Perng, M. D., Wen, S. F., Gibbon, T., Middeldorp, J., Sluijs, J., Hol, E. M., and Quinlan, R. A. (2008) Glial fibrillary acidic protein filaments can tolerate the incorporation of assembly-compromised GFAP-delta, but with consequences for filament organization and alphaB-crystallin association. Mol. Biol. Cell 19, 4521-4533
25. Nielsen, A. L., and Jorgensen, A. L. (2004) Self-assembly of the cytoskeletal glial fibrillary acidic protein is inhibited by an isoform-specific C terminus. J. Biol. Chem. 279, 41537-41545 (Pubitemid 39313595)
26. Lepekhin, E. A., Eliasson, C., Berthold, C. H., Berezin, V., Bock, E., and Pekny, M. (2001) Intermediate filaments regulate astro-cyte motility. J. Neurochem. 79, 617-625 (Pubitemid 33029935)
27. Rutka, J. T., and Smith, S. L. (1993) Transfection of human astrocytoma cells with glial fibrillary acidic protein complementary DNA: analysis of expression, proliferation, and tumorige-nicity. Cancer Res. 53, 3624-3631 (Pubitemid 23229647)
28. Rutka, J. T., Hubbard, S. L., Fukuyama, K., Matsuzawa, K., Dirks, P. B., and Becker, L. E. (1994) Effects of antisense glial fibrillary acidic protein complementary DNA on the growth, invasion, and adhesion of human astrocytoma cells. Cancer Res. 54, 3267-3272 (Pubitemid 24208940)
29. Weinstein, D. E., Shelanski, M. L., and Liem, R. K. (1991) Suppression by antisense mRNA demonstrates a requirement for the glial fibrillary acidic protein in the formation of stable astrocytic processes in response to neurons. J. Cell Biol. 112, 1205-1213 (Pubitemid 21909663)
30. Root, D. E., Hacohen, N., Hahn, W. C., Lander, E. S., and Sabatini, D. M. (2006) Genome-scale loss-of-function screening with a lentiviral RNAi library. Nat. Methods 3, 715-719 (Pubitemid 44275739)
31. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M., and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267 (Pubitemid 26119138)
32. Naldini, L., Blomer, U., Gage, F. H., Trono, D., and Verma, I. M. (1996) Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. U.S.A. 93, 11382-11388 (Pubitemid 26347130)
33. Ruijter, J. M., Thygesen, H. H., Schoneveld, O. J., Das, A. T., Berkhout, B., and Lamers, W. H. (2006) Factor correction as a tool to eliminate between-session variation in replicate experiments: application to molecular biology and retrovirology. Retrovirology 3, 2
34. Hol, E. M., Roelofs, R. F., Moraal, E., Sonnemans, M. A., Sluijs, J. A., Proper, E. A., de Graan, P. N., Fischer, D. F., and van Leeuwen, F. W. (2003) Neuronal expression of GFAP in patients with Alzheimer pathology and identification of novel GFAP splice forms. Mol. Psychiatry 8, 786-796 (Pubitemid 37100712)
35. Colognato, H., ffrench-Constant, C., and Feltri, M. L. (2005) Human diseases reveal novel roles for neural laminins. Trends Neurosci. 28, 480-486 (Pubitemid 41187797)
36. Franco, S. J., and Müller, U. (2011) Extracellular matrix functions during neuronal migration and lamination in the mammalian central nervous system. Dev. Neurobiol. 71, 889-900
37. Lauffenburger, D. A., and Horwitz, A. F. (1996) Cell migration: a physically integrated molecular process. Cell 84, 359-369 (Pubitemid 26058561)
38. Hynes, R. O. (2002) IntegrinsBidirectional, allosteric signaling machines. Cell 110, 673-687
39. Nishio, T., Kawaguchi, S., Yamamoto, M., Iseda, T., Kawasaki, T., and Hase, T. (2005) Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay. Neuroscience 132, 87-102 (Pubitemid 40380717)
40. Rooprai, H. K., Vanmeter, T., Panou, C., Schnüll, S., Trillo-Pazos, G., Davies, D., and Pilkington, G. J. (1999) The role of integrin receptors in aspects of glioma invasion in vitro. Int. J. Dev. Neurosci. 17, 613-623 (Pubitemid 29421847)
41. Steinböck, F.A., and Wiche, G. (1999) Plectin: a cytolinker by design. Biol. Chem. 380, 151-158 (Pubitemid 29118837)
42. Wiche, G., and Winter, L. (2011) Plectin isoforms as organizers of intermediate filament cytoarchitecture. BioArchitecture 1, 14-20
43. Kamphuis, W., Mamber, C., Moeton, M., Kooijman, L., Sluijs, J. A., Jansen, A. H., Verveer, M., de Groot, L. R., Smith, V. D., Rangarajan, S., Rodríguez, J. J., Orre, M., and Hol, E. M. (2012) GFAP isoforms in adult mouse brain with a focus on neurogenic astrocytes and reactive astrogliosis in mouse models of Alzheimer disease. PLoS One 7, e42823
44. Ogier, C., Bernard, A., Chollet, A.-M., Le Diguardher, T., Hanessian, S., Charton, G., Khrestchatisky, M., and Rivera, S. (2006) Matrix metalloproteinase-2 (MMP-2) regulates astrocyte motility in connection with the actin cytoskeleton and integrins. Glia 54, 272-284 (Pubitemid 44316232)
45. Delamarre, E., Taboubi, S., Mathieu, S., Bérenguer, C., Rigot, V., Lissitzky J.-C, Figarella-Branger, D., Ouafik, L., and Luis, J. (2009) Expression of integrin a6ß1 enhances tumorigenesis in glioma cells. Am. J. Pathol. 175, 844-855
46. Katada, K., Tomonaga, T., Satoh, M., Matsushita, K., Tonoike, Y., Kodera, Y., Hanazawa, T., Nomura, F., and Okamoto, Y (2012) Plectin promotes migration and invasion of cancer cells and is a novel prognostic marker for head and neck squamous cell carcinoma. J. Proteomics 75, 1803-1815
47. Farin, A., Suzuki, S. O., Weiker, M., Goldman, J. E., Bruce, J. N., and Canoll, P. (2006) Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 53, 799-808
48. Goldbrunner, R. H., Bernstein, J. J., and Tonn, J.-C. (1999) Cell-extracellular matrix interaction in glioma invasion. Acta Neurochir. (Wien) 141, 295-305 (Pubitemid 29137544)
49. Menet, V., Ribotta, M., Chauvet, N., Drian, M. J., Lannoy, J., Colucci-Guyon, E., and Privat, A. (2001) Inactivation of the glial fibrillary acidic protein gene, but not that of vimentin, improves neuronal survival and neurite growth by modifying adhesion molecule expression. J. Neurosci. 21, 6147-6158 (Pubitemid 32737747)
50. Toda, M., Asou, H., Miura, M., Toya, S., and Uyemura, K. (1994) GFAP transfected cells produce laminin, leading to neurite outgrowth promotion. Neuroreport 5, 1969-1972 (Pubitemid 24305434)
51. Palu, E., and Liesi, P. (2002) Differential distribution of lamin-ins in Alzheimer disease and normal human brain tissue. J. Neurosci. Res. 69, 243-256 (Pubitemid 34734155)
52. Moyano, J. V., Greciano, P. G., Buschmann, M. M., Koch, M., and Matlin, K. S. (2010) Autocrine transforming growth factor-1 activation mediated by integrin V 3 regulates transcriptional expression of laminin-332 in Madin-Darby canine kidney epithelial cells. Mol. Biol. Cell 21, 3654-3668
53. Aumailley, M., Pesch, M., Tunggal, L., Gaill, F., and Fassler, R. (2000) Altered synthesis of laminin 1 and absence of basement membrane component deposition in (beta)1 integrin-deficient embryoid bodies. J. Cell Sci. 113, 259-268 (Pubitemid 30088971)
54. Gregor, M., Osmanagic-Myers, S., Burgstaller, G., Wolfram, M., Fischer, I., Walko, G., Resch, G. P., Jörgl, A., Herrmann, H., and Wiche, G. (2014) Mechanosensing through focal adhesion-anchored intermediate filaments. FASEB J. 28, 715-729
55. Andrä, K., Kornacker, I., Jörgl, A., Zörer, M., Spazierer, D., Fuchs, P., Fischer, I., and Wiche, G. (2003) Plectin-isoform-specific rescue of hemidesmosomal defects in plectin (-/-) kera-tinocytes. J. Invest. Dermatol. 120, 189-197 (Pubitemid 36513066)