Integrins regulate centrosome integrity and astrocyte polarization following a wound

Developmental Neurobiology

Volumn 73, Issue 5, 2013, Pages 333-353

  Peng, Huashan ^a   Ong, Yen May ^a   Shah, Waris Ali ^a   Holland, Paul C ^b   Carbonetto, Salvatore ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Cell polarity; Centrosome integrity; Integrins; NMII

Indexed keywords

BETA1 INTEGRIN; BLEBBISTATIN; COMPLEMENTARY DNA; FIBRONECTIN; FOCAL ADHESION KINASE; MYOSIN IIA; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELL ADHESION; CELL MIGRATION; CELL POLARITY; CENTROSOME; CHIMERA; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EMBRYO; GENE SILENCING; MOUSE; NONHUMAN; PRIORITY JOURNAL; WOUND;

ANIMALS; ANTIGENS, CD29; ASTROCYTES; CELL ADHESION; CELL CYCLE PROTEINS; CELL POLARITY; CELLS, CULTURED; CENTROSOME; CHICK EMBRYO; DNA, COMPLEMENTARY; EXTRACELLULAR MATRIX; HETEROCYCLIC COMPOUNDS WITH 4 OR MORE RINGS; HUMANS; MICE; NONMUSCLE MYOSIN TYPE IIB; PROTEIN-TYROSINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; RETINA; RNA, SMALL INTERFERING; SUSPENSIONS; WOUND HEALING;

EID: 84876017827     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22055     Document Type: Article

References (87)

1. Andersen JS, Wilkinson CJ, Mayor T, Mortensen P, Nigg EA, Mann M. 2003.Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426:570-574.
2. Balczon R, Bao L, Zimmer WE. 1994.PCM-1, A 228-kD centrosome autoantigen with a distinct cell cycle distribution. J Cell Biol 124:783-793.
3. Basto R, Brunk K, Vinadogrova T, Peel N, Franz A, Khodjakov A, Raff JW. 2008.Centrosome amplification can initiate tumorigenesis in flies. Cell 133:1032-1042.
4. Basto R, Lau J, Vinogradova T, Gardiol A, Woods CG, Khodjakov A, Raff JW. 2006.Flies without centrioles. Cell 125:1375-1386.
5. Berrier AL, Martinez R, Bokoch GM, LaFlamme SE. 2002.The integrin β tail is required and sufficient to regulate adhesion signaling to Rac1. J Cell Sci 115:4285-4291.
6. Bettencourt-Dias M, Glover DM. 2007.Centrosome biogenesis and function: Centrosomics brings new understanding. Nat Rev Mol Cell Biol 8:451-463.
7. Bloor JW, Kiehart DP. 2001.zipper Nonmuscle myosin-II functions downstream of PS2 integrin in Drosophila myogenesis and is necessary for myofibril formation. Dev Biol 239:215-228.
8. Bodeau AL, Berrier AL, Mastrangelo AM, Martinez R, LaFlamme SE. 2001.A functional comparison of mutations in integrin β cytoplasmic domains: Effects on the regulation of tyrosine phosphorylation, cell spreading, cell attachment and β1 integrin conformation. J Cell Sci 114:2795-2807.
9. Carbonetto S, Fambrough DM. 1979.Synthesis, insertion into the plasma membrane, and turnover of α-bungarotoxin receptors in chick sympathetic neurons. J Cell Biol 81:555-569.
10. Caussinus E, Gonzalez C. 2005.Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat Genet 37:1125-1129.
11. Chodagam S, Royou A, Whitfield W, Karess R, Raff JW. 2005.The centrosomal protein CP190 regulates myosin function during early Drosophila development. Curr Biol 15:1308-1313.
12. Dammermann A, Merdes A. 2002.Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255-266.
13. de Anda FC, Meletis K, Ge X, Rei D, Tsai LH. 2010.Centrosome motility is essential for initial axon formation in the neocortex. J Neurosci 30:10391-10406.
14. de Anda FC, Pollarolo G, Da Silva JS, Camoletto PG, Feiguin F, Dotti CG. 2005.Centrosome localization determines neuronal polarity. Nature 436:704-708.
15. Devreotes PN, Fambrough DM. 1976.Turnover of acetylcholine receptors in skeletal muscle. Cold Spring Harb Symp Quant Biol 40:237-251.
16. Distel M, Hocking JC, Volkmann K, Koster RW. 2010.The centrosome neither persistently leads migration nor determines the site of axonogenesis in migrating neurons in vivo. J Cell Biol 191:875-890.
17. Doxsey S, McCollum D, Theurkauf W. 2005.Centrosomes in cellular regulation. Annu Rev Cell Dev Biol 21:411-434.
18. Duxbury MS, Ashley SW, Whang EE. 2004.Inhibition of pancreatic adenocarcinoma cellular invasiveness by blebbistatin: A novel myosin II inhibitor. Biochem Biophys Res Commun 313:992-997.
19. Ellison JA, Barone FC, Feuerstein GZ. 1999.Matrix remodeling after stroke. De novo expression of matrix proteins and integrin receptors. Ann NY Acad Sci 890:204-222.
20. Espreafico EM, Coling DE, Tsakraklides V, Krogh K, Wolenski JS, Kalinec G, Kachar B. 1998.Localization of myosin-V in the centrosome. Proc Natl Acad Sci USA 95:8636-8641.
21. Etienne-Manneville S. 2006.In vitro assay of primary astrocyte migration as a tool to study Rho GTPase function in cell polarization. Methods Enzymol 406:565-578.
22. Etienne-Manneville S. 2008.Polarity proteins in glial cell functions. Curr Opin Neurobiol 18:488-494.
23. Etienne-Manneville S, Hall A. 2001.Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489-498.
24. Fassler R, Pfaff M, Murphy J, Noegel AA, Johansson S, Timpl R, Albrecht R. 1995.Lack of β 1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J Cell Biol 128:979-988.
25. Fielding AB, Dedhar S. 2009.The mitotic functions of integrin-linked kinase. Cancer Metastasis Rev 28:99-111.
26. Fielding AB, Dobreva I, McDonald PC, Foster LJ, Dedhar S. 2008.Integrin-linked kinase localizes to the centrosome and regulates mitotic spindle organization. J Cell Biol 180:681-689.
27. Fukasawa K. 2007.Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 7:911-924.
28. Fukuda T, Sugita S, Inatome R, Yanagi S. 2010.CAMDI, a novel disrupted in schizophrenia 1 (DISC1)-binding protein, is required for radial migration. J Biol Chem 285:40554-40561.
29. Ge X, Frank CL, Calderon de Anda F, Tsai LH. 2010.Hook3 interacts with PCM1 to regulate pericentriolar material assembly and the timing of neurogenesis. Neuron 65:191-203.
30. Gee SH, Montanaro F, Lindenbaum MH, Carbonetto S. 1994.Dystroglycan-α, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77:675-686.
31. Gomes ER, Jani S, Gundersen GG. 2005.Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121:451-463.
32. Goshima G, Wollman R, Goodwin SS, Zhang N, Scholey JM, Vale RD, Stuurman N. 2007.Genes required for mitotic spindle assembly in Drosophila S2 cells. Science 316:417-421.
33. Greve JM, Gottlieb DI. 1982.Monoclonal antibodies which alter the morphology of cultured chick myogenic cells. J Cell Biochem 18:221-229.
34. Hamilton NB, Attwell D. 2010.Do astrocytes really exocytose neurotransmitters?Nat Rev Neurosci 11:227-238.
35. Heidkamp MC, Bayer AL, Kalina JA, Eble DM, Samarel AM. 2002.GFP-FRNK disrupts focal adhesions and induces anoikis in neonatal rat ventricular myocytes. Circ Res 90:1282-1289.
36. Henneberger C, Papouin T, Oliet SH, Rusakov DA. 2010.Long-term potentiation depends on release of D-serine from astrocytes. Nature 463:232-236.
37. Jakobsen L, Vanselow K, Skogs M, Toyoda Y, Lundberg E, Poser I, Falkenby LG, et al. 2011.Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods. EMBO J 30:1520-1535.
38. Kim J, Krishnaswami SR, Gleeson JG. 2008.CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum Mol Genet 17:3796-3805.
39. Kornberg LJ, Earp HS, Turner CE, Prockop C, Juliano RL. 1991.Signal transduction by integrins: Increased protein tyrosine phosphorylation caused by clustering of β 1 integrins. Proc Natl Acad Sci USA 88:8392-8396.
40. Kwon M, Godinho SA, Chandhok NS, Ganem NJ, Azioune A, Thery M, Pellman D. 2008.Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes. Genes Dev 22:2189-2203.
41. LaFlamme SE, Nieves B, Colello D, Reverte CG. 2008.Integrins as regulators of the mitotic machinery. Curr Opin Cell Biol 20:576-582.
42. LaFlamme SE, Thomas LA, Yamada SS, Yamada KM. 1994.Single subunit chimeric integrins as mimics and inhibitors of endogenous integrin functions in receptor localization, cell spreading and migration, and matrix assembly. J Cell Biol 126:1287-1298.
43. Lesage B, Gutierrez I, Marti E, Gonzalez C. 2010.Neural stem cells: The need for a proper orientation. Curr Opin Genet Dev 20:438-442.
44. Liu Z, van Grunsven LA, Van Rossen E, Schroyen B, Timmermans JP, Geerts A, Reynaert H. 2010.Blebbistatin inhibits contraction and accelerates migration in mouse hepatic stellate cells. Br J Pharmacol 159:304-315.
45. Loulier K, Lathia JD, Marthiens V, Relucio J, Mughal MR, Tang SC, Coksaygan T, et al. 2009.β1 Integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol 7:e1000176.
46. Luders J, Stearns T. 2007.Microtubule-organizing centres: A re-evaluation. Nat Rev Mol Cell Biol 8:161-167.
47. Luxton GW, Gomes ER, Folker ES, Worman HJ, Gundersen GG. 2011.TAN lines: A novel nuclear envelope structure involved in nuclear positioning. Nucleus 2:173-181.
48. Luxton GW, Gundersen GG. 2011.Orientation and function of the nuclear-centrosomal axis during cell migration. Curr Opin Cell Biol 23:579-588.
49. Martin KH, Boerner SA, Parsons JT. 2002.Regulation of focal adhesion targeting and inhibitory functions of the FAK related protein FRNK using a novel estrogen receptor "switch". Cell Motil Cytoskeleton 51:76-88.
50. Mikule K, Delaval B, Kaldis P, Jurcyzk A, Hergert P, Doxsey S. 2007.Loss of centrosome integrity induces p38-p53-p21-dependent G1-S arrest. Nat Cell Biol 9:160-170.
51. Miller T, Boettiger D. 2003.Control of intracellular signaling by modulation of fibronectin conformation at the cell-materials interface. Langmuir 19:1723-1729.
52. Minozzo FC, Rassier DE. 2010.Effects of blebbistatin and Ca2+ concentration on force produced during stretch of skeletal muscle fibers. Am J Physiol Cell Physiol 299:C1127-C1135.
53. Mori T, Buffo A, Gotz M. 2005.The novel roles of glial cells revisited: The contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol 69:67-99.
54. Muller H, Schmidt D, Steinbrink S, Mirgorodskaya E, Lehmann V, Habermann K, Dreher F, et al. 2010.Proteomic and functional analysis of the mitotic Drosophila centrosome. EMBO J 29:3344-3357.
55. Nigg EA. 2002.Centrosome aberrations: Cause or consequence of cancer progression?Nat Rev Cancer 2:815-825.
56. Park AY, Shen TL, Chien S, Guan JL. 2009.Role of focal adhesion kinase Ser-732 phosphorylation in centrosome function during mitosis. J Biol Chem 284:9418-9425.
57. Peng H, Shah W, Holland P, Carbonetto S. 2008.Integrins and dystroglycan regulate astrocyte wound healing: The integrin β1 subunit is necessary for process extension and orienting the microtubular network. Dev Neurobiol 68:559-574.
58. Petzold GC, Murthy VN. 2011.Role of astrocytes in neurovascular coupling. Neuron 71:782-797.
59. Piel M, Nordberg J, Euteneuer U, Bornens M. 2001.Centrosome-dependent exit of cytokinesis in animal cells. Science 291:1550-1553.
60. Raff JW. 2003.Cell division: Genome maintenance. Nature 423:493, 495.
61. Rebollo E, Sampaio P, Januschke J, Llamazares S, Varmark H, Gonzalez C. 2007.Functionally unequal centrosomes drive spindle orientation in asymmetrically dividing Drosophila neural stem cells. Dev Cell 12:467-474.
62. Reverte CG, Benware A, Jones CW, LaFlamme SE. 2006.Perturbing integrin function inhibits microtubule growth from centrosomes, spindle assembly, and cytokinesis. J Cell Biol 174:491-497.
63. Schenk J, Wilsch-Brauninger M, Calegari F, Huttner WB. 2009.Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc Natl Acad Sci USA 106:16487-16492.
64. Seluanov A, Vaidya A, Gorbunova V. 2010.Establishing primary adult fibroblast cultures from rodents. J Vis Exp. 44.
65. Shi Q, Boettiger D. 2003.A novel mode for integrin-mediated signaling: Tethering is required for phosphorylation of FAK Y397. Mol Biol Cell 14:4306-4315.
66. Sir JH, Barr AR, Nicholas AK, Carvalho OP, Khurshid M, Sossick A, Reichelt S, et al. 2011.A primary microcephaly protein complex forms a ring around parental centrioles. Nat Genet 43:1147-1153.
67. Slack-Davis JK, Martin KH, Tilghman RW, Iwanicki M, Ung EJ, Autry C, Luzzio MJ, et al. 2007.Cellular characterization of a novel focal adhesion kinase inhibitor. J Biol Chem 282:14845-14852.
68. Snow RL, Robson JA. 1995.Migration and differentiation of neurons in the retina and optic tectum of the chick. Exp Neurol 134:13-24.
69. Sofroniew MV. 2009.Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
70. Solecki DJ, Model L, Gaetz J, Kapoor TM, Hatten ME. 2004.Par6α signaling controls glial-guided neuronal migration. Nat Neurosci 7:1195-1203.
71. Solecki DJ, Trivedi N, Govek EE, Kerekes RA, Gleason SS, Hatten ME. 2009.Myosin II motors and F-actin dynamics drive the coordinated movement of the centrosome and soma during CNS glial-guided neuronal migration. Neuron 63:63-80.
72. Stiess M, Maghelli N, Kapitein LC, Gomis-Ruth S, Wilsch-Brauninger M, Hoogenraad CC, Tolic-Norrelykke IM, et al. 2010.Axon extension occurs independently of centrosomal microtubule nucleation. Science 327:704-707.
73. Takacs B, Billington N, Gyimesi M, Kintses B, Malnasi-Csizmadia A, Knight PJ, Kovacs M. 2010.Myosin complexed with ADP and blebbistatin reversibly adopts a conformation resembling the start point of the working stroke. Proc Natl Acad Sci USA 107:6799-6804.
74. Takada Y, Ye X, Simon S. 2007.The integrins. Genome Biol 8:215.
75. Tawil N, Wilson P, Carbonetto S. 1993.Integrins in point contacts mediate cell spreading: Factors that regulate integrin accumulation in point contacts vs. focal contacts. J Cell Biol 120:261-271.
76. Tawil NJ, Houde M, Blacher R, Esch F, Reichardt LF, Turner DC, Carbonetto S. 1990.α1 β1 Integrin heterodimer functions as a dual laminin/collagen receptor in neural cells. Biochemistry 29:6540-6544.
77. Thery M, Racine V, Pepin A, Piel M, Chen Y, Sibarita JB, Bornens M. 2005.The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7:947-953.
78. Tremblay MR, Carbonetto S. 2006.An extracellular pathway for dystroglycan function in acetylcholine receptor aggregation and laminin deposition in skeletal myotubes. J Biol Chem 281:13365-13373.
79. Turner DC, Flier LA, Carbonetto S. 1989.Identification of a cell-surface protein involved in PC12 cell-substratum adhesion and neurite outgrowth on laminin and collagen. J Neurosci 9:3287-3296.
80. Vicente-Manzanares M, Koach MA, Whitmore L, Lamers ML, Horwitz AF. 2008.Segregation and activation of myosin IIB creates a rear in migrating cells. J Cell Biol 183:543-554.
81. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. 2009.Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10:778-790.
82. Yamakita Y, Totsukawa G, Yamashiro S, Fry D, Zhang X, Hanks SK, Matsumura F. 1999.Dissociation of FAK/p130(CAS)/c-Src complex during mitosis: Role of mitosis-specific serine phosphorylation of FAK. J Cell Biol 144:315-324.
83. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT. 2007.Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518-521.
84. Yang W, Lin Q, Guan JL, Cerione RA. 1999.Activation of the Cdc42-associated tyrosine kinase-2 (ACK-2) by cell adhesion via integrin β1. J Biol Chem 274:8524-8530.
85. Yang W, Lin Q, Zhao J, Guan JL, Cerione RA. 2001.The nonreceptor tyrosine kinase ACK2, a specific target for Cdc42 and a negative regulator of cell growth and focal adhesion complexes. J Biol Chem 276:43987-43993.
86. Zhang H, Berg JS, Li Z, Wang Y, Lang P, Sousa AD, Bhaskar A, et al. 2004.Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nat Cell Biol 6:523-531.
87. Zhou H, Kramer RH. 2005.Integrin engagement differentially modulates epithelial cell motility by RhoA/ROCK and PAK1. J Biol Chem 280:10624-10635.