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Neuroscience Journal
Volume 2013, Article ID 859257, 15 pages
http://dx.doi.org/10.1155/2013/859257
Research Article

Roles of Integrins and Intracellular Molecules in the Migration and Neuritogenesis of Fetal Cortical Neurons: MEK Regulates Only the Neuritogenesis

Departments of Surgery and Physiology and Biophysics, University of Mississippi Medical Center, Room L020, Clinical Service Building, 2500 North State Street, Jackson, MS 39216, USA

Received 24 August 2012; Accepted 16 December 2012

Academic Editor: Carles Vilarino-Guell

Copyright © 2013 Ujjwal K. Rout. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. Métin, J. P. Baudoin, S. Rakić, and J. G. Parnavelas, “Cell and molecular mechanisms involved in the migration of cortical interneurons,” European The Journal of Neuroscience, vol. 23, no. 4, pp. 894–900, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. S. L. Gupton and F. B. Gertler, “Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis,” Developmental Cell, vol. 18, no. 5, pp. 725–736, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. E. S. Anton, J. A. Kreidberg, and P. Rakic, “Distinct functions of α3 and α(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex,” Neuron, vol. 22, no. 2, pp. 277–289, 1999. View at Google Scholar · View at Scopus
  4. I. D. Campbell and M. J. Humphries, “Integrin structure, activation, and interactions,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 3, pp. 1–14, 2011. View at Publisher · View at Google Scholar
  5. J. Qin, O. Vinogradova, and E. F. Plow, “Integrin bidirectional signaling: a molecular view,” PLoS Biology, vol. 2, no. 6, article e169, 2004. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Milner and I. L. Campbell, “The integrin family of cell adhesion molecules has multiple functions within the CNS,” Journal of Neuroscience Research, vol. 69, no. 3, pp. 286–291, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. M. Barczyk, S. Carracedo, and D. Gullberg, “Integrins,” Cell and Tissue Research, vol. 339, no. 1, pp. 269–280, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. L. F. Reichardt and K. J. Tomaselli, “Extracellular matrix molecules and their receptors: functions in neural development,” Annual Review of Neuroscience, vol. 14, pp. 531–570, 1991. View at Google Scholar · View at Scopus
  9. R. S. Schmid and E. S. Anton, “Role of integrins in the development of the cerebral cortex,” Cerebral Cortex, vol. 13, no. 3, pp. 219–224, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. R. S. Schmid, S. Shelton, A. Stanco, Y. Yokota, J. A. Kreidberg, and E. S. Anton, “α3β1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development,” Development, vol. 131, no. 24, pp. 6023–6031, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. E. Georges-Labouesse, M. Mark, N. Messaddeq, and A. Gansmüller, “Essential role of α6 integrins in cortical and retinal lamination,” Current Biology, vol. 8, no. 17, pp. 983–986, 1998. View at Google Scholar · View at Scopus
  12. G. Marchetti, S. Escuin, A. van der Flier, A. de Arcangelis, R. O. Hynes, and E. Georges-Labouesse, “Integrin α5β1 is necessary for regulation of radial migration of cortical neurons during mouse brain development,” European The Journal of Neuroscience, vol. 31, no. 3, pp. 399–409, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. D. S. Galileo, J. Majors, A. F. Horwitz, and J. R. Sanes, “Retrovirally introduced antisense integrin RNA inhibits neuroblast migration in vivo,” Neuron, vol. 9, no. 6, pp. 1117–1131, 1992. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Andressen, S. Adrian, R. Fässler, S. Arnhold, and K. Addicks, “The contribution of β1 integrins to neuronal migration and differentiation depends on extracellular matrix molecules,” European Journal of Cell Biology, vol. 84, no. 12, pp. 973–982, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. M. F. DeFreitas, C. K. Yoshida, W. A. Frazier, D. L. Mendrick, R. M. Kypta, and L. F. Reichardt, “Identification of integrin α3β1 as a neuronal thrombospondin receptor mediating neurite outgrowth,” Neuron, vol. 15, no. 2, pp. 333–343, 1995. View at Google Scholar · View at Scopus
  16. U. Muller, B. Bossy, K. Venstrom, and L. F. Reichardt, “Integrin α8β1 promotes attachment, cell spreading, and neurite outgrowth on fibronectin,” Molecular Biology of the Cell, vol. 6, no. 4, pp. 433–448, 1995. View at Google Scholar · View at Scopus
  17. R. Belvindrah, D. Graus-Porta, S. Goebbels, K. A. Nave, and U. Müller, “β1 integrins in radial glia but not in migrating neurons are essential for the formation of cell layers in the cerebral cortex,” The Journal of Neuroscience, vol. 27, no. 50, pp. 13854–13865, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Fassler and M. Meyer, “Consequences of lack of β1 integrin gene expression in mice,” Genes and Development, vol. 9, no. 15, pp. 1896–1908, 1995. View at Google Scholar · View at Scopus
  19. D. Graus-Porta, S. Blaess, M. Senften et al., “β1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex,” Neuron, vol. 31, no. 3, pp. 367–379, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. E. Förster, A. Tielsch, B. Saum et al., “Reelin, disabled 1, and β1 integrins are required for the formation of the radial glial scaffold in the hippocampus,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 13178–13183, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Niewmierzycka, J. Mills, R. St.-Arnaud R., S. Dedhar, and L. F. Reichardt, “Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly,” The Journal of Neuroscience, vol. 25, no. 30, pp. 7022–7031, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Belvindrah, P. Nalbant, S. Ding, C. Wu, G. M. Bokoch, and U. Müller, “Integrin-linked kinase regulates Bergmann glial differentiation during cerebellar development,” Molecular and Cellular Neuroscience, vol. 33, no. 2, pp. 109–125, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. I. Nikonenko, N. Toni, M. Moosmayer, Y. Shigeri, D. Muller, and L. S. Jones, “Integrins are involved in synaptogenesis, cell spreading, and adhesion in the postnatal brain,” Developmental Brain Research, vol. 140, no. 2, pp. 185–194, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Liesi, I. Seppala, and E. Trenkner, “Neuronal migration in cerebellar microcultures is inhibited by antibodies against a neurite outgrowth domain of laminin,” Journal of Neuroscience Research, vol. 33, no. 1, pp. 170–176, 1992. View at Google Scholar · View at Scopus
  25. B. Zassler, C. Schermer, and C. Humpel, “Protein kinase C and phosphoinositol-3-kinase mediate differentiation or proliferation of slice-derived rat microglia,” Pharmacology, vol. 67, no. 4, pp. 211–215, 2003. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Schermer and C. Humpel, “Granulocyte macrophage-colony stimulating factor activates microglia in rat cortex organotypic brain slices,” Neuroscience Letters, vol. 328, no. 2, pp. 180–184, 2002. View at Publisher · View at Google Scholar · View at Scopus
  27. E. M. Stettler and D. S. Galileo, “Radial glia produce and align the ligand fibronectin during neuronal migration in the developing chick brain,” Journal of Comparative Neurology, vol. 468, no. 3, pp. 441–451, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Liesi, D. Dahl, and A. Vaheri, “Laminin is produced by early rat astrocytes in primary culture,” Journal of Cell Biology, vol. 96, no. 3, pp. 920–924, 1983. View at Google Scholar · View at Scopus
  29. A. E. Aplin, A. Howe, S. K. Alahari, and R. L. Juliano, “Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins,” Pharmacological Reviews, vol. 50, no. 2, pp. 197–263, 1998. View at Google Scholar · View at Scopus
  30. R. L. Juliano, P. Reddig, S. Alahari, M. Edin, A. Howe, and A. Aplin, “Integrin regulation of cell signalling and motility,” Biochemical Society Transactions, vol. 32, pp. 443–446, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. B. P. Eliceiri, “Integrin and growth factor receptor crosstalk,” Circulation Research, vol. 89, no. 12, pp. 1104–1110, 2001. View at Google Scholar · View at Scopus
  32. D. A. Hsia, S. T. Lim, J. A. Bernard-Trifilo et al., “Integrin α4β1 promotes focal adhesion kinase-independent cell motility via α4 cytoplasmic domain-specific activation of c-Src,” Molecular and Cellular Biology, vol. 25, no. 21, pp. 9700–9712, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. J. E. Bleasdale, N. R. Thakur, R. S. Gremban et al., “Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils,” Journal of Pharmacology and Experimental Therapeutics, vol. 255, no. 2, pp. 756–768, 1990. View at Google Scholar · View at Scopus
  34. L. M. Gleeson, C. Chakraborty, T. Mckinnon, and P. K. Lala, “Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through α5β1 integrin via mitogen-activated protein kinase pathway,” Journal of Clinical Endocrinology and Metabolism, vol. 86, no. 6, pp. 2484–2493, 2001. View at Publisher · View at Google Scholar · View at Scopus
  35. H. T. Ma, K. Venkatachalam, H. S. Li et al., “Assessment of the role of the inositol 1,4,5-trisphosphate receptor in the activation of transient receptor potential channels and store-operated Ca2+ entry channels,” Journal of Biological Chemistry, vol. 276, no. 22, pp. 18888–18896, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. K. Hirai, H. Yoshioka, M. Kihara et al., “Inhibiting neuronal migration by blocking NMDA receptors in the embryonic rat cerebral cortex: a tissue culture study,” Developmental Brain Research, vol. 114, no. 1, pp. 63–67, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. T. Ranta-Knuuttila, T. Kiviluoto, H. Mustonen et al., “Migration of primary cultured rabbit gastric epithelial cells requires intact protein kinase C and Ca2+/calmodulin activity,” Digestive Diseases and Sciences, vol. 47, no. 5, pp. 1008–1014, 2002. View at Publisher · View at Google Scholar · View at Scopus
  38. M. Phillippe and A. Basa, “The effects of ruthenium red, an inhibitor of calcium-induced calcium release, on phasic myometrial contractions,” Biochemical and Biophysical Research Communications, vol. 221, no. 3, pp. 656–661, 1996. View at Publisher · View at Google Scholar · View at Scopus
  39. N. Maeda and M. Noda, “Involvement of receptor-like protein tyrosine phosphatase ζ/RPTPβ and its ligand pleiotrophin/heparin-binding growth-associated molecule (HB-GAM) in neuronal migration,” Journal of Cell Biology, vol. 142, no. 1, pp. 203–216, 1998. View at Publisher · View at Google Scholar · View at Scopus
  40. U. K. Rout and J. M. Dhossche, “Liquid-diet with alcohol alters maternal, fetal and placental weights and the expression of molecules involved in integrin signaling in the fetal cerebral cortex,” International Journal of Environmental Research and Public Health, vol. 7, no. 11, pp. 4023–4036, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Aarum, K. Sandberg, S. L. B. Haeberlein, and M. A. A. Persson, “Migration and differentiation of neural precursor cells can be directed by microglia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 26, pp. 15983–15988, 2003. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Segarra, L. Balenci, T. Drenth, F. Maina, and F. Lamballe, “Combined signaling through ERK, PI3K/AKT, and RAC1/p38 is required for met-triggered cortical neuron migration,” Journal of Biological Chemistry, vol. 281, no. 8, pp. 4771–4778, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. P. R. Borghesani, J. M. Peyrin, R. Klein et al., “BDNF stimulates migration of cerebellar granule cells,” Development, vol. 129, no. 6, pp. 1435–1442, 2002. View at Google Scholar · View at Scopus
  44. D. L. Mendrick and D. M. Kelly, “Temporal expression of VLA-2 and modulation of its ligand specificity by rat glomerular epithelial cells in vitro,” Laboratory Investigation, vol. 69, no. 6, pp. 690–702, 1993. View at Google Scholar · View at Scopus
  45. T. A. Ferguson and T. S. Kupper, “Antigen-independent processes in antigen-specific immunity: a role for α4 integrin,” Journal of Immunology, vol. 150, no. 4, pp. 1172–1182, 1993. View at Google Scholar · View at Scopus
  46. G. T. van Nhieu and R. R. Isberg, “The Yersinia pseudotuberculosis invasin protein and human fibronectin bind to mutually exclusive sites on the α5β1 integrin receptor,” Journal of Biological Chemistry, vol. 266, no. 36, pp. 24367–24375, 1991. View at Google Scholar · View at Scopus
  47. K. Moulder, K. Roberts, E. M. Shevach, and J. E. Coligan, “The mouse vitronectin receptor is a T cell activation antigen,” Journal of Experimental Medicine, vol. 173, no. 2, pp. 343–347, 1991. View at Google Scholar · View at Scopus
  48. M. Aumailley, R. Timpl, and A. Sonnenberg, “Antibody to integrin α6 subunit specifically inhibits cell-binding to laminin fragment 8,” Experimental Cell Research, vol. 188, no. 1, pp. 55–60, 1990. View at Publisher · View at Google Scholar · View at Scopus
  49. G. F. Burns, L. Cosgrove, and T. Triglia, “The IIb-IIIa glycoprotein complex that mediates platelet aggregation is directly implicated in leukocyte adhesion,” Cell, vol. 45, no. 2, pp. 269–280, 1986. View at Google Scholar · View at Scopus
  50. E. A. Wayner, W. G. Carter, R. S. Piotrowicz, and T. J. Kunicki, “The function of multiple extracellular matrix receptors in mediating cell adhesion to extracellular matrix: preparation of monoclonal antibodies to the fibronectin receptor that specifically inhibit cell adhesion to fibronectin and react with platelet glycoproteins Ic-IIa,” Journal of Cell Biology, vol. 107, no. 5, pp. 1881–1891, 1988. View at Google Scholar · View at Scopus
  51. U. K. Rout, “Valproate, thalidomide and ethyl alcohol alter the migration of HTR-8/SVneo cells,” Reproductive Biology and Endocrinology, vol. 4, article 44, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. N. Maitra, I. L. Flink, J. J. Bahl, and E. Morkin, “Expression of α and β integrins during terminal differentiation of cardiomyocytes,” Cardiovascular Research, vol. 47, no. 4, pp. 715–725, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. M. L. Feltri, M. Arona, S. S. Scherer, and L. Wrabetz, “Cloning and sequence of the cDNA encoding the β4 integrin subunit in rat peripheral nerve,” Gene, vol. 186, no. 2, pp. 299–304, 1997. View at Publisher · View at Google Scholar · View at Scopus
  54. M. L. Condic and P. C. Letourneau, “Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth,” Nature, vol. 389, no. 6653, pp. 852–856, 1997. View at Publisher · View at Google Scholar · View at Scopus
  55. S. P. Palecek, J. C. Loftust, M. H. Ginsberg, D. A. Lauffenburger, and A. F. Horwitz, “Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness,” Nature, vol. 385, no. 6616, pp. 537–540, 1997. View at Publisher · View at Google Scholar · View at Scopus
  56. R. P. Tucker, J. K. Brunso-Bechtold, D. A. Jenrath et al., “Cellular origins of tenascin in the developing nervous system,” Perspectives on Developmental Neurobiology, vol. 2, no. 1, pp. 89–99, 1994. View at Google Scholar · View at Scopus
  57. D. Seiffert, M. L. Iruela-Arispe, E. H. Sage, and D. J. Loskutoff, “Distribution of vitronectin mRNA during murine development,” Developmental Dynamics, vol. 203, no. 1, pp. 71–79, 1995. View at Google Scholar · View at Scopus
  58. J. H. McCarty, A. Lacy-Hulbert, A. Charest et al., “Selective ablation of αv integrins in the central nervous system leads to cerebral hemorrhage, seizures, axonal degeneration and premature death,” Development, vol. 132, no. 1, pp. 165–176, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. H. Schottelndreier, B. V. Potter, G. W. Mayr, and A. H. Guse, “Mechanisms involved in alpha6beta1-integrin-mediated Ca(2+) signalling,” Cellular Signalling, vol. 13, no. 12, pp. 895–899, 2001. View at Google Scholar
  60. K. Fukami, S. Inanobe, K. Kanemaru, and Y. Nakamura, “Phospholipase C is a key enzyme regulating intracellular calcium and modulating the phosphoinositide balance,” Progress in Lipid Research, vol. 49, no. 4, pp. 429–437, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. J. H. Choi, Y. R. Yang, S. K. Lee et al., “Phospholipase C-γ1 potentiates integrin-dependent cell spreading and migration through Pyk2/paxillin activation,” Cellular Signalling, vol. 19, no. 8, pp. 1784–1796, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Larsson, “Protein kinase C and the regulation of the actin cytoskeleton,” Cellular Signalling, vol. 18, no. 3, pp. 276–284, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Q. Zheng and M. M. Poo, “Calcium signaling in neuronal motility,” Annual Review of Cell and Developmental Biology, vol. 23, pp. 375–404, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. X. Zhang, A. Chattopadhyay, Q. S. Ji et al., “Focal adhesion kinase promotes phospholipase C-γ1 activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 16, pp. 9021–9026, 1999. View at Publisher · View at Google Scholar · View at Scopus
  65. N. P. Jones, J. Peak, S. Brader, S. A. Eccles, and M. Katan, “PLCγ1 is essential for early events in integrin signalling required for cell motility,” Journal of Cell Science, vol. 118, pp. 2695–2706, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. L. Zhou, Y. Jossin, and A. M. Goffinet, “Identification of small molecules that interfere with radial neuronal migration and early cortical plate development,” Cerebral Cortex, vol. 17, no. 1, pp. 211–220, 2007. View at Publisher · View at Google Scholar · View at Scopus
  67. C. T. Zhao, K. Li, J. T. Li et al., “PKCδ regulates cortical radial migration by stabilizing the Cdk5 activator p35,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 50, pp. 21353–21358, 2009. View at Publisher · View at Google Scholar · View at Scopus
  68. T. Ng, D. Shima, A. Squire et al., “PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic,” The EMBO Journal, vol. 18, no. 14, pp. 3909–3923, 1999. View at Publisher · View at Google Scholar · View at Scopus
  69. N. Alam, H. L. Goel, M. J. Zarif et al., “The integrin—growth factor receptor duet,” Journal of Cellular Physiology, vol. 213, no. 3, pp. 649–653, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. A. Umesh, M. A. Thompson, E. N. Chini, K. P. Yip, and J. S. K. Sham, “Integrin ligands mobilize Ca2+ from ryanodine receptor-gated stores and lysosome-related acidic organelles in pulmonary arterial smooth muscle cells,” Journal of Biological Chemistry, vol. 281, no. 45, pp. 34312–34323, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. E. T. O'Brien, E. D. Salmon, and H. P. Erickson, “How calcium causes microtubule depolymerization,” Cell Motility and the Cytoskeleton, vol. 36, no. 2, pp. 125–135, 1997. View at Google Scholar
  72. R. J. Pasterkamp, J. J. Peschon, M. K. Spriggs, and A. L. Kolodkin, “Semaphorin 7A promotes axon outgrowth through integrins and MAPKs,” Nature, vol. 424, no. 6947, pp. 398–405, 2003. View at Publisher · View at Google Scholar · View at Scopus