Age-specific function of α5β1 integrin in microglial migration during early colonization of the developing mouse cortex

GLIA

Volumn 65, Issue 7, 2017, Pages 1072-1088

  Smolders, Sophie Marie Thérèse ^a,b,c   Swinnen, Nina ^a   Kessels, Sofie ^a   Arnauts, Kaline ^a   Smolders, Silke ^a,d   Le Bras, Barbara ^b,c   Rigo, Jean Michel ^e   Legendre, Pascal ^b,c   Brône, Bert ^a  

^a BIOMED Research Institute   (Belgium)

^b and Centre National de la Recherche Scientifique Unité Mixte de Recherche 8246   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e UHasselt   (Belgium)

Author keywords

blood vessels; cell adhesion molecules; cell migration inhibition; embryo; fibronectins

Indexed keywords

ALPHAVBETA1 INTEGRIN; FIBRONECTIN; FIBRONECTIN RECEPTOR; UNCLASSIFIED DRUG; CHEMOKINE RECEPTOR CX3CR1; CX3CR1 PROTEIN, MOUSE; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; LECTIN; PHYCOERYTHRIN; VERY LATE ACTIVATION ANTIGEN 5;

ADULT; AGE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN SLICE; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EX VIVO STUDY; FEMALE; IN VITRO STUDY; MALE; MICROGLIA; MOUSE; NONHUMAN; PARENCHYMA; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN INTERACTION; TIME LAPSE IMAGING; ZEBRA FISH; AGING; ANIMAL; BLOOD VESSEL; C57BL MOUSE; CELL MOTION; CYTOLOGY; EMBRYOLOGY; EXTRACELLULAR MATRIX; GENE EXPRESSION REGULATION; GENETICS; MAMMALIAN EMBRYO; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

AGING; ANIMALS; BLOOD VESSELS; CELL MOVEMENT; CEREBRAL CORTEX; CX3C CHEMOKINE RECEPTOR 1; EMBRYO, MAMMALIAN; EXTRACELLULAR MATRIX; FIBRONECTINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; INTEGRIN ALPHA5BETA1; LECTINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROGLIA; PHYCOERYTHRIN; SIGNAL TRANSDUCTION;

EID: 85018829306     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.23145     Document Type: Article

References (78)

1. Arno, B., Grassivaro, F., Rossi, C., Bergamaschi, A., Castiglioni, V., Furlan, R., … Greter, M. (2014). Neural progenitor cells orchestrate microglia migration and positioning into the developing cortex. Nature Communications, 5, 5611.
2. Arnold, T., & Betsholtz, C. (2013). The importance of microglia in the development of the vasculature in the central nervous system. Vascular Cell, 5, 4.
3. Avila, A., Vidal, P. M., Dear, T. N., Harvey, R. J., Rigo, J. M., & Nguyen, L. (2013). Glycine receptor alpha2 subunit activation promotes cortical interneuron migration. Cellular Reports, 4, 738–750.
4. Bachman, H., Nicosia, J., Dysart, M., & Barker, T. H. (2015). Utilizing fibronectin integrin-binding specificity to control cellular responses. Advanced Wound Care (New Rochelle), 4, 501–511.
5. Barnhart, E. L., Lee, K. C., Keren, K., Mogilner, A., & Theriot, J. A. (2011). An adhesion-dependent switch between mechanisms that determine motile cell shape. PLoS Biology, 9, e1001059.
6. Belvindrah, R., Graus-Porta D., Goebbels S., Nave KA., Muller U. 2007. Beta1 integrins in radial glia but not in migrating neurons are essential for the formation of cell layers in the cerebral cortex. Journal of Neurosciences, 27:13854–13865.
7. Blandin, A. F., Noulet, F., Renner, G., Mercier, M. C., Choulier, L., Vauchelles, R., … Ronde, P. (2016). Glioma cell dispersion is driven by alpha5 integrin-mediated cell–matrix and cell–cell interactions. Cancer Letters, 376, 328–338.
8. Carbonell, W. S., Murase, S., Horwitz, A. F., & Mandell, J. W. (2005). Migration of perilesional microglia after focal brain injury and modulation by CC chemokine receptor 5: An in situ time-lapse confocal imaging study. Journal of Neurosciences, 25, 7040–7047.
9. Casano, A. M., & Peri, F. (2015). Microglia: Multitasking specialists of the brain. Developmental Cell, 32, 469–477.
10. Costa, P., Scales, T. M., Ivaska, J., & Parsons, M. (2013). Integrin-specific control of focal adhesion kinase and RhoA regulates membrane protrusion and invasion. PLoS One, 8, e74659.
11. Cukierman, E., Pankov, R., Stevens, D. R., & Yamada, K. M. (2001). Taking cell-matrix adhesions to the third dimension. Science, 294, 1708–1712.
12. Dalmau, I., Vela, J. M., Gonzalez, B., & Castellano, B. (1997). Expression of LFA-1alpha and ICAM-1 in the developing rat brain: A potential mechanism for the recruitment of microglial cell precursors. Brain Research & Developmental Brain Research, 103, 163–170.
13. De Gasperi, R., Gama Sosa, M. A., & Elder, G. A. (2012). Presenilin-1 regulates the constitutive turnover of the fibronectin matrix in endothelial cells. BMC Biochemistry, 13, 28.
14. Doyle, A. D., & Yamada, K. M. (2016). Mechanosensing via cell-matrix adhesions in 3D microenvironments. Experimental Cell Research, 343, 60–66.
15. Dudvarski Stankovic, N., Teodorczyk, M., Ploen, R., Zipp, F., & Schmidt, M. H. (2016). Microglia–blood vessel interactions: A double-edged sword in brain pathologies. Acta Neuropathology, 131, 347–363.
16. Eyo, U. B., & Dailey, M. E. (2013). Microglia: Key elements in neural development, plasticity, and pathology. Journal of Neuroimmune Pharmacology, 8, 494–509.
17. Eyo, U. B., Miner, S. A., Weiner, J. A., & Dailey, M. E. (2016). Developmental changes in microglial mobilization are independent of apoptosis in the neonatal mouse hippocampus. Brain Behaviour & Immunity, 55, 49–59.
18. Eyo, U. B., Peng, J., Swiatkowski, P., Mukherjee, A., Bispo, A., & Wu, L. J. (2014). Neuronal hyperactivity recruits microglial processes via neuronal NMDA receptors and microglial P2Y12 receptors after status epilepticus. Journal of Neurosciences, 34, 10528–10540.
19. Finlay, B. L., & Darlington, R. B. (1995). Linked regularities in the development and evolution of mammalian brains. Science, 268, 1578–1584.
20. Fraley, S. I., Feng, Y., Krishnamurthy, R., Kim, D. H., Celedon, A., Longmore, G. D., … Wirtz, D. (2010). A distinctive role for focal adhesion proteins in three-dimensional cell motility. Nature Cell Biology, 12, 598–604.
21. Frost, J. L., & Schafer, D. P. (2016). Microglia: Architects of the developing nervous system. Trends in Cell Biology, 26, 587–597.
22. Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., … Mehler, M. F. (2010). Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science, 330, 841–845.
23. Gorelik, R., & Gautreau, A. (2015). The Arp2/3 inhibitory protein arpin induces cell turning by pausing cell migration. Cytoskeleton (Hoboken), 72, 362–371.
24. Graupera, M., Guillermet-Guibert, J., Foukas, L. C., Phng, L. K., Cain, R. J., Salpekar, A., & Pearce, W. (2008). Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature, 453, 662–666.
25. Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., & Macklis, J. D. (2013). Molecular logic of neocortical projection neuron specification, development and diversity. Nature Review & Neurosciences, 14, 755–769.
26. Grinberg, Y. Y., Milton, J. G., & Kraig, R. P. (2011). Spreading depression sends microglia on Levy flights. PLoS One, 6, e19294.
27. Grossmann, R., Stence, N., Carr, J., Fuller, L., Waite, M., & Dailey, M. E. (2002). Juxtavascular microglia migrate along brain microvessels following activation during early postnatal development. Glia, 37, 229–240.
28. Hynes, R. O. (2002). Integrins: bidirectional, allosteric signaling machines. Cell, 110, 673–687.
29. Jung, S., Aliberti, J., Graemmel, P., Sunshine, M. J., Kreutzberg, G. W., Sher, A., & Littman, D. R. (2000). Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Molecular Cell Biology, 20, 4106–4114.
30. Kasahara, Y., Koyama, R., & Ikegaya, Y. (2016). Depth and time-dependent heterogeneity of microglia in mouse hippocampal slice cultures. Neurosciences Research, 111, 64–69.
31. Kierdorf, K., Erny, D., Goldmann, T., Sander, V., Schulz, C., Perdiguero, E. G., & Wieghofer, P. (2013). Microglia emerge from erythromyeloid precursors via Pu.1- and Irf8-dependent pathways. Nature & Neurosciences, 16, 273–280.
32. Kim, C., Cho, E. D., Kim, H. K., You, S., Lee, H. J., Hwang, D., & Lee, S. J. (2014). beta1-integrin-dependent migration of microglia in response to neuron-released alpha-synuclein. Experimental Molecular Medicine, 46, e91.
33. Lau, L. W., Cua, R., Keough, M. B., Haylock-Jacobs, S., & Yong, V. W. (2013). Pathophysiology of the brain extracellular matrix: A new target for remyelination. Nature Review of Neurosciences, 14, 722–729.
34. Legate, K. R., Takahashi, S., Bonakdar, N., Fabry, B., Boettiger, D., & Zent, R. (2011). Integrin adhesion and force coupling are independently regulated by localized PtdIns(4.,5)2 synthesis. EMBO Journal, 30, 4539–4553.
35. Li, C., Zhen, G., Chai, Y., Xie, L., Crane, J. L., Farber, E., … Farber, C. R. (2016). RhoA determines lineage fate of mesenchymal stem cells by modulating CTGF–VEGF complex in extracellular matrix. Nature Communications, 7, 11455.
36. Lock, J. G., Wehrle-Haller, B., & Stromblad, S. (2008). Cell–matrix adhesion complexes: Master control machinery of cell migration. Seminars in Cancer Biology, 18, 65–76.
37. Madadizadeh, F., Ezati Asar, M., & Hosseini, M. (2015). Common statistical mistakes in descriptive statistics reports of normal and non-normal variables in biomedical sciences research. Iran Journal of Public Health, 44, 1557–1558.
38. Maecker, H. T., & Trotter, J. (2006). Flow cytometry controls, instrument setup, and the determination of positivity. Cytometry A, 69, 1037–1042.
39. Marchetti, G., Escuin, S., van der Flier, A., De Arcangelis, A., Hynes, R. O., & Georges-Labouesse, E. (2010). Integrin alpha5beta1 is necessary for regulation of radial migration of cortical neurons during mouse brain development. European Journal of Neurosciences, 31, 399–409.
40. Meijering, E., Dzyubachyk, O., & Smal, I. (2012). Methods for cell and particle tracking. Methods & Enzymology, 504, 183–200.
41. Milner, R. (2009). Microglial expression of alphavbeta3 and alphavbeta5 integrins is regulated by cytokines and the extracellular matrix: Beta5 integrin null microglia show no defects in adhesion or MMP-9 expression on vitronectin. Glia, 57, 714–723.
42. Milner, R., & Campbell, I. L. (2002a). Cytokines regulate microglial adhesion to laminin and astrocyte extracellular matrix via protein kinase C-dependent activation of the alpha6beta1 integrin. Journal of Neurosciences, 22, 1562–1572.
43. Milner, R., & Campbell, I. L. (2002b). Developmental regulation of beta1 integrins during angiogenesis in the central nervous system. Molecular Cell Neurosciences, 20, 616–626.
44. Milner, R., & Campbell, I. L. (2002c). The integrin family of cell adhesion molecules has multiple functions within the CNS. Journal of Neuroscience Research, 69, 286–291.
45. Milner, R., & Campbell, I. L. (2003). The extracellular matrix and cytokines regulate microglial integrin expression and activation. Journal of Immunology, 170, 3850–3858.
46. Milner, R., Crocker, S. J., Hung, S., Wang, X., Frausto, R. F., & del Zoppo, G. J. (2007). Fibronectin- and vitronectin-induced microglial activation and matrix metalloproteinase-9 expression is mediated by integrins alpha5beta1 and alphavbeta5. Journal of Immunology, 178, 8158–8167.
47. Moroi, M., Onitsuka, I., Imaizumi, T., & Jung, S. M. (2000). Involvement of activated integrin alpha2beta1 in the firm adhesion of platelets onto a surface of immobilized collagen under flow conditions. Thrombotic & Haemostasis, 83, 769–776.
48. Nasu-Tada, K., Koizumi, S., & Inoue, K. (2005). Involvement of beta1 integrin in microglial chemotaxis and proliferation on fibronectin: Different regulations by ADP through PKA. Glia, 52, 98–107.
49. Nimmerjahn, A., Kirchhoff, F., & Helmchen, F. (2005). Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science, 308, 1314–1318.
50. Petersen, M. A., & Dailey, M. E. (2004). Diverse microglial motility behaviors during clearance of dead cells in hippocampal slices. Glia, 46, 195–206.
51. Pont-Lezica, L., Bechade, C., Belarif-Cantaut, Y., Pascual, O., & Bessis, A. (2011). Physiological roles of microglia during development. Journal of Neurochemistry, 119, 901–908.
52. Rezaie, P., Cairns, N. J., & Male, D. K. (1997). Expression of adhesion molecules on human fetal cerebral vessels: relationship to microglial colonisation during development. Brain Research & Developmental Brain Research, 104, 175–189.
53. Rigato, C., Buckinx, R., Le-Corronc, H., Rigo, J. M., & Legendre, P. (2011). Pattern of invasion of the embryonic mouse spinal cord by microglial cells at the time of the onset of functional neuronal networks. Glia, 59, 675–695.
54. Romberger, D. J. (1997). Fibronectin. International Journal of Biochemical Cell Biology, 29, 939–943.
55. Ruoslahti, E. (1996). Brain extracellular matrix. Glycobiology, 6, 489–492.
56. Sauvageot, C. M., & Stiles, C. D. (2002). Molecular mechanisms controlling cortical gliogenesis. Currents in Opinion Neurobiology, 12, 244–249.
57. Schiefer, J., Kampe, K., Dodt, H. U., Zieglgansberger, W., & Kreutzberg, G. W. (1999). Microglial motility in the rat facial nucleus following peripheral axotomy. Journal of Neurocytology, 28, 439–453.
58. Schmid, R. S., & Anton, E. S. (2003). Role of integrins in the development of the cerebral cortex. Cerebral Cortex, 13, 219–224.
59. Sheppard, A. M., Brunstrom, J. E., Thornton, T. N., Gerfen, R. W., Broekelmann, T. J., McDonald, J. A., & Pearlman, A. L. (1995). Neuronal production of fibronectin in the cerebral cortex during migration and layer formation is unique to specific cortical domains. Developmental Biology, 172, 504–518.
60. Sheppard, A. M., Hamilton, S. K., & Pearlman, A. L. (1991). Changes in the distribution of extracellular matrix components accompany early morphogenetic events of mammalian cortical development. Journal of Neurosciences, 11, 3928–3942.
61. 2+ waves transmit brain-damage signals to microglia. Developmental Cell, 22, 1138–1148.
62. Smolders, S., Smolders, S. M., Swinnen, N., Gartner, A., Rigo J. M., Legendre, P., & Brone, B. (2015). Maternal immune activation evoked by polyinosinic:polycytidylic acid does not evoke microglial cell activation in the embryo. Frontiers in Cell Neuroscience, 9, 301.
63. Stettler, E. M., & Galileo, D. S. (2004). Radial glia produce and align the ligand fibronectin during neuronal migration in the developing chick brain. Journal of Comprehensive Neurology, 468, 441–451.
64. Stewart, G. R., & Pearlman, A. L. (1987). Fibronectin-like immunoreactivity in the developing cerebral cortex. Journal of Neurosciences, 7, 3325–3333.
65. Svahn, A. J., Graeber, M. B., Ellett, F., Lieschke, G. J., Rinkwitz, S., Bennett, M. R., & Becker, T. S. (2013). Development of ramified microglia from early macrophages in the zebrafish optic tectum. Developmental Neurobiology, 73, 60–71.
66. Swinnen, N., Smolders, S., Avila, A., Notelaers, K., Paesen, R., Ameloot, M., … Brone, B. (2013). Complex invasion pattern of the cerebral cortex bymicroglial cells during development of the mouse embryo. Glia, 61, 150–163.
67. Tanzer, M. L. (2006). Current concepts of extracellular matrix. Journal of Orthopedic Sciences, 11, 326–331.
68. Toyjanova, J., Flores-Cortez, E., Reichner, J. S., & Franck, C. (2015). Matrix confinement plays a pivotal role in regulating neutrophil-generated tractions, speed, and integrin utilization. Journal of Biological Chemistry, 290, 3752–3763.
69. Ueno, M., & Yamashita, T. (2014). Bidirectional tuning of microglia in the developing brain: From neurogenesis to neural circuit formation. Currents in Opinion Neurobiology, 27, 8–15.
70. Vicente-Manzanares, M., & Horwitz, A. R. (2011). Cell migration: An overview. Methods & Molecular Biology, 769, 1–24.
71. Welser-Alves, J. V., Boroujerdi, A., Tigges, U., & Milner, R. (2011). Microglia use multiple mechanisms to mediate interactions with vitronectin: Non-essential roles for the highly-expressed alphavbeta3 and alphavbeta5 integrins. Journal of Neuroinflammation, 8, 157.
72. Yao, H., Duan, M., Yang, L., & Buch, S. (2013). Nonmuscle myosin light-chain kinase mediates microglial migration induced by HIV tat: Involvement of beta1 integrins. FASEB Journal, 27, 1532–1548.
73. Yokota, Y., Gashghaei, H. T., Han, C., Watson, H., Campbell, K. J., & Anton, E. S. (2007). Radial glial dependent and independent dynamics of interneuronal migration in the developing cerebral cortex. PLoS One, 2, e794.
74. Yoshida, N., Hishiyama, S., Yamaguchi, M., Hashiguchi, M., Miyamoto, Y., Kaminogawa, S., … Hisatsune, T. (2003). Decrease in expression of alpha 5 beta 1 integrin during neuronal differentiation of cortical progenitor cells. Experimental Cell Research, 287, 262–271.
75. Yuryev, M., Pellegrino, C., Jokinen, V., Andriichuk, L., Khirug, S., Khiroug, L., … Rivera C. (2015). In vivo calcium imaging of evoked calcium waves in the embryonic cortex. Frontiers in Cell Neuroscience, 9, 500.
76. R. P. A. Zent (Eds.) (2010), Cell–extracellular matrix interactions in cancer (p. 314). New York: Springer.
77. Zhang, F., Nance, E., Alnasser, Y., Kannan, R., & Kannan, S. (2016). Microglial migration and interactions with dendrimer nanoparticles are altered in the presence of neuroinflammation. Journal of Neuroinflammation,13, 65.
78. Zhao, H., Jiang, Y., Cao, Q., Hou, Y., & Wang. C. (2012). Role of integrin switch and transforming growth factor beta 3 in hypoxia-induced invasion inhibition of human extravillous trophoblast cells. Biology & Reproduction, 87, 47