Laminins containing the β2 and γ3 chains regulate astrocyte migration and angiogenesis in the retina

Development (Cambridge)

Volumn 140, Issue 9, 2013, Pages 2050-2061

  Gnanaguru, Gopalan ^a   Bachay, Galina ^a   Biswas, Saptarshi ^a   Pinzón Duarte, Germán ^a   Hunter, Dale D ^a   Brunken, William J ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Angiogenesis; Astrocyte; Integrins; Laminin; Mouse; Retinopathy of prematurity

Indexed keywords

BETA1 INTEGRIN; INTEGRIN; LAMININ; LAMININ BETA2; LAMININ GAMMA3; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD RETINA BARRIER; BLOOD VESSEL WALL; CELL DIFFERENTIATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; FLUORESCENCE ANGIOGRAPHY; GENE DELETION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA; RETINA BLOOD VESSEL; RETROLENTAL FIBROPLASIA;

ANIMALS; ANTIGENS, CD29; ASTROCYTES; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL MOVEMENT; CORNEAL NEOVASCULARIZATION; GENE DELETION; IMMUNOHISTOCHEMISTRY; LAMININ; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; RECEPTORS, LAMININ; RETINA;

EID: 84875999734     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.087817     Document Type: Article

References (66)

1. Abbott, N. J., Rönnbäck, L. and Hansson, E. (2006). Astrocyte-endothelial interactions at the blood-brain barrier. Nat. Rev. Neurosci. 7, 41-53.
2. Armstrong, R. C., Harvath, L. and Dubois-Dalcq, M. E. (1990). Type 1 astrocytes and oligodendrocyte-type 2 astrocyte glial progenitors migrate toward distinct molecules. J. Neurosci. Res. 27, 400-407.
3. Aumailley, M., Bruckner-Tuderman, L., Carter, W. G., Deutzmann, R., Edgar, D., Ekblom, P., Engel, J., Engvall, E., Hohenester, E., Jones, J. C. et al. (2005). A simplified laminin nomenclature. Matrix Biol. 24, 326-332.
4. Balasubramani, M., Schreiber, E. M., Candiello, J., Balasubramani, G. K., Kurtz, J. and Halfter, W. (2010). Molecular interactions in the retinal basement membrane system: a proteomic approach. Matrix Biol. 29, 471-483.
5. Bredrup, C., Matejas, V., Barrow, M., Bláhová, K., Bockenhauer, D., Fowler, D. J., Gregson, R. M., Maruniak-Chudek, I., Medeira, A., Mendonça, E. L. et al. (2008). Ophthalmological aspects of Pierson syndrome. Am. J. Ophthalmol. 146, 602-611.
6. Chen, J. and Smith, L. E. (2007). Retinopathy of prematurity. Angiogenesis 10, 133-140.
7. Choma, D. P., Milano, V., Pumiglia, K. M. and DiPersio, C. M. (2007). Integrin alpha3beta1-dependent activation of FAK/Src regulates Rac1-mediated keratinocyte polarization on laminin-5. J. Invest. Dermatol. 127, 31-40.
8. Colognato, H. and Yurchenco, P. D. (2000). Form and function: the laminin family of heterotrimers. Dev. Dyn. 218, 213-234.
9. Dénes, V., Witkovsky, P., Koch, M., Hunter, D. D., Pinzón-Duarte, G. and Brunken, W. J. (2007). Laminin deficits induce alterations in the development of dopaminergic neurons in the mouse retina. Vis. Neurosci. 24, 549-562.
10. Desban, N., Lissitzky, J. C., Rousselle, P. and Duband, J. L. (2006). alpha1beta1-integrin engagement to distinct laminin-1 domains orchestrates spreading, migration and survival of neural crest cells through independent signaling pathways. J. Cell Sci. 119, 3206-3218.
11. Dickinson, J. L., Sale, M. M., Passmore, A., FitzGerald, L. M., Wheatley, C. M., Burdon, K. P., Craig, J. E., Tengtrisorn, S., Carden, S. M., Maclean, H. et al. (2006). Mutations in the NDP gene: contribution to Norrie disease, familial exudative vitreoretinopathy and retinopathy of prematurity. Clin. Experiment. Ophthalmol. 34, 682-688.
12. Dorrell, M. I., Aguilar, E. and Friedlander, M. (2002). Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest. Ophthalmol. Vis. Sci. 43, 3500-3510.
13. Dorrell, M. I., Aguilar, E., Jacobson, R., Trauger, S. A., Friedlander, J., Siuzdak, G. and Friedlander, M. (2010). Maintaining retinal astrocytes normalizes revascularization and prevents vascular pathology associated with oxygen-induced retinopathy. Glia 58, 43-54.
14. Durbeej, M. (2010). Laminins. Cell Tissue Res. 339, 259-268.
15. Echtermeyer, F., Schöber, S., Pöschl, E., von der Mark, H. and von der Mark, K. (1996). Specific induction of cell motility on laminin by alpha 7 integrin. J. Biol. Chem. 271, 2071-2075.
16. Edwards, M. M., Mammadova-Bach, E., Alpy, F., Klein, A., Hicks, W. L., Roux, M., Simon-Assmann, P., Smith, R. S., Orend, G., Wu, J. et al. (2010). Mutations in Lama1 disrupt retinal vascular development and inner limiting membrane formation. J. Biol. Chem. 285, 7697-7711.
17. Errais, K., Ammous, I., Kamoun, R., Mili Boussen, I., Anene, R., Zhioua, R. and Meddeb Ouertani, A. (2008). [Familial exudative vitreoretinopathy associated with persistence of hyaloid artery]. J. Fr. Ophtalmol. 31, e3.
18. Estrach, S., Cailleteau, L., Franco, C. A., Gerhardt, H., Stefani, C., Lemichez, E., Gagnoux-Palacios, L., Meneguzzi, G. and Mettouchi, A. (2011). Lamininbinding integrins induce Dll4 expression and Notch signaling in endothelial cells. Circ. Res. 109, 172-182.
19. Etienne-Manneville, S. and Hall, A. (2001). Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106, 489-498.
20. Frank, D. E. and Carter, W. G. (2004). Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J. Cell Sci. 117, 1351-1363.
21. Frost, E. E., Milner, R. and Ffrench-Constant, C. (2000). Migration assays for oligodendrocyte precursor cells. Methods Mol. Biol. 139, 265-278.
22. Fruttiger, M. (2007). Development of the retinal vasculature. Angiogenesis 10, 77-88.
23. Fruttiger, M., Calver, A. R., Krüger, W. H., Mudhar, H. S., Michalovich, D., Takakura, N., Nishikawa, S. and Richardson, W. D. (1996). PDGF mediates a neuron-astrocyte interaction in the developing retina. Neuron 17, 1117-1131.
24. Fruttiger, M., Calver, A. R. and Richardson, W. D. (2000). Platelet-derived growth factor is constitutively secreted from neuronal cell bodies but not from axons. Curr. Biol. 10, 1283-1286.
25. Fujiwara, H., Gu, J. and Sekiguchi, K. (2004). Rac regulates integrin-mediated endothelial cell adhesion and migration on laminin-8. Exp. Cell Res. 292, 67-77.
26. Gardner, T. W., Lieth, E., Khin, S. A., Barber, A. J., Bonsall, D. J., Lesher, T., Rice, K. and Brennan, W. A., Jr (1997). Astrocytes increase barrier properties and ZO-1 expression in retinal vascular endothelial cells. Invest. Ophthalmol. Vis. Sci. 38, 2423-2427.
27. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177.
28. Halfter, W., Willem, M. and Mayer, U. (2005). Basement membrane-dependent survival of retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46, 1000-1009.
29. Hirrlinger, P. G., Pannicke, T., Winkler, U., Claudepierre, T., Varshney, S., Schulze, C., Reichenbach, A., Brunken, W. J. and Hirrlinger, J. (2011). Genetic deletion of laminin isoforms β2 and γ3 induces a reduction in Kir4.1 and aquaporin-4 expression and function in the retina. PLoS ONE 6, e16106.
30. Hu, H., Candiello, J., Zhang, P., Ball, S. L., Cameron, D. A. and Halfter, W. (2010). Retinal ectopias and mechanically weakened basement membrane in a mouse model of muscle-eye-brain (MEB) disease congenital muscular dystrophy. Mol. Vis. 16, 1415-1428.
31. Huttenlocher, A. (2005). Cell polarization mechanisms during directed cell migration. Nat. Cell Biol. 7, 336-337.
32. Ido, H., Ito, S., Taniguchi, Y., Hayashi, M., Sato-Nishiuchi, R., Sanzen, N., Hayashi, Y., Futaki, S. and Sekiguchi, K. (2008). Laminin isoforms containing the γ3 chain are unable to bind to integrins due to the absence of the glutamic acid residue conserved in the C-terminal regions of the γ1 and γ2 chains. J. Biol. Chem. 283, 28149-28157.
33. Kempen, J. H., O'Colmain, B. J., Leske, M. C., Haffner, S. M., Klein, R., Moss, S. E., Taylor, H. R., Hamman, R. F. and the Eye Diseases Prevalence Research Group (2004). The prevalence of diabetic retinopathy among adults in the United States. Arch. Ophthalmol. 122, 552-563.
34. Lai, C. M., Shen, W. Y., Brankov, M., Lai, Y. K., Barnett, N. L., Lee, S. Y., Yeo, I. Y., Mathur, R., Ho, J. E., Pineda, P. et al. (2005). Long-term evaluation of AAVmediated sFlt-1 gene therapy for ocular neovascularization in mice and monkeys. Mol. Ther. 12, 659-668.
35. Lee, Y., Kameya, S., Cox, G. A., Hsu, J., Hicks, W., Maddatu, T. P., Smith, R. S., Naggert, J. K., Peachey, N. S. and Nishina, P. M. (2005). Ocular abnormalities in Large(myd) and Large(vls) mice, spontaneous models for muscle, eye, and brain diseases. Mol. Cell. Neurosci. 30, 160-172.
36. Lee, H. J., Ahn, B. J., Shin, M. W., Jeong, J. W., Kim, J. H. and Kim, K. W. (2009). Ninjurin1 mediates macrophage-induced programmed cell death during early ocular development. Cell Death Differ. 16, 1395-1407.
37. Li, Y. N., Radner, S., French, M. M., Pinzón-Duarte, G., Daly, G. H., Burgeson, R. E., Koch, M. and Brunken, W. J. (2012). The γ3 chain of laminin is widely but differentially expressed in murine basement membranes: expression and functional studies. Matrix Biol. 31, 120-134.
38. Libby, R. T., Xu, Y., Selfors, L. M., Brunken, W. J. and Hunter, D. D. (1997). Identification of the cellular source of laminin β2 in the adult and developing vertebrate retina. J. Comp. Neurol. 389, 655-667.
39. Libby, R. T., Champliaud, M. F., Claudepierre, T., Xu, Y., Gibbons, E. P., Koch, M., Burgeson, R. E., Hunter, D. D. and Brunken, W. J. (2000). Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J. Neurosci. 20, 6517-6528.
40. Macdonald, P. R., Lustig, A., Steinmetz, M. O. and Kammerer, R. A. (2010). Laminin chain assembly is regulated by specific coiled-coil interactions. J. Struct. Biol. 170, 398-405.
41. Milner, R., Hung, S., Wang, X., Spatz, M. and del Zoppo, G. J. (2008). The rapid decrease in astrocyte-associated dystroglycan expression by focal cerebral ischemia is protease-dependent. J. Cereb. Blood Flow Metab. 28, 812-823.
42. Mohney, B. G., Pulido, J. S., Lindor, N. M., Hogan, M. C., Consugar, M. B., Peters, J., Pankratz, V. S., Nasr, S. H., Smith, S. J., Gloor, J. et al. (2011). A novel mutation of LAMB2 in a multigenerational mennonite family reveals a new phenotypic variant of Pierson syndrome. Ophthalmology 118, 1137-1144.
43. Nissenkorn, I., Kremer, I. and Ben-Sira, I. (1988). Association of a persistent hyaloid artery and ROP. Ophthalmology 95, 559-560.
44. Noakes, P. G., Gautam, M., Mudd, J., Sanes, J. R. and Merlie, J. P. (1995). Aberrant differentiation of neuromuscular junctions in mice lacking slaminin/ laminin beta 2. Nature 374, 258-262.
45. Outtz, H. H., Tattersall, I. W., Kofler, N. M., Steinbach, N. and Kitajewski, J. (2011). Notch1 controls macrophage recruitment and Notch signaling is activated at sites of endothelial cell anastomosis during retinal angiogenesis in mice. Blood 118, 3436-3439.
46. Peng, H., Shah, W., Holland, P. and Carbonetto, S. (2008). Integrins and dystroglycan regulate astrocyte wound healing: the integrin beta1 subunit is necessary for process extension and orienting the microtubular network. Dev. Neurobiol. 68, 559-574.
47. Pierson, M., Cordier, J., Hervouet, F. and Rauber, G. (1963). Une curieuse association malformative congenitale et familiale atteignant l'oeil et le rein. (An unusual congenital and familial congenital malformative combination involving the eye and kidney.). J. Genet. Hum. 12, 184-213.
48. Pinzón-Duarte, G., Daly, G., Li, Y. N., Koch, M. and Brunken, W. J. (2010). Defective formation of the inner limiting membrane in laminin beta2-and gamma3-null mice produces retinal dysplasia. Invest. Ophthalmol. Vis. Sci. 51, 1773-1782.
49. Provis, J. M. and Hendrickson, A. E. (2008). The foveal avascular region of developing human retina. Arch. Ophthalmol. 126, 507-511.
50. Provis, J. M., Sandercoe, T. and Hendrickson, A. E. (2000). Astrocytes and blood vessels define the foveal rim during primate retinal development. Invest. Ophthalmol. Vis. Sci. 41, 2827-2836.
51. Radner, S., Banos, C., Bachay, G., Li, Y. N., Hunter, D. D., Brunken, W. J. and Yee, K. T. (2013). β2 and γ3 laminins are critical cortical basement membrane components: Ablation of Lamb2 and Lamc3 genes disrupts cortical lamination and produces dysplasia. Dev. Neurobiol. 73, 209-229.
52. Ribatti, D. and Crivellato, E. (2012). 'Sprouting angiogenesis', a reappraisal. Dev. Biol. 372, 157-165.
53. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709.
54. Rymo, S. F., Gerhardt, H., Wolfhagen Sand, F., Lang, R., Uv, A. and Betsholtz, C. (2011). A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures. PLoS ONE 6, e15846.
55. Sapieha, P., Hamel, D., Shao, Z., Rivera, J. C., Zaniolo, K., Joyal, J. S. and Chemtob, S. (2010). Proliferative retinopathies: angiogenesis that blinds. Int. J. Biochem. Cell Biol. 42, 5-12.
56. Schnitzer, J. (1988). Astrocytes in mammalian retina. Prog. Retin. Eye Res. 7, 209-231.
57. Stone, J., Chan-Ling, T., Pe'er, J., Itin, A., Gnessin, H. and Keshet, E. (1996). Roles of vascular endothelial growth factor and astrocyte degeneration in the genesis of retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 37, 290-299.
58. Suh, H. N. and Han, H. J. (2010). Laminin regulates mouse embryonic stem cell migration: involvement of Epac1/Rap1 and Rac1/cdc42. Am. J. Physiol. Cell Physiol. 298, C1159-C1169.
59. Tagaya, M., Haring, H. P., Stuiver, I., Wagner, S., Abumiya, T., Lucero, J., Lee, P., Copeland, B. R., Seiffert, D. and del Zoppo, G. J. (2001). Rapid loss of microvascular integrin expression during focal brain ischemia reflects neuron injury. J. Cereb. Blood Flow Metab. 21, 835-846.
60. Takahashi, H., Kanesaki, H., Igarashi, T., Kameya, S., Yamaki, K., Mizota, A., Kudo, A., Miyagoe-Suzuki, Y., Takeda, S. and Takahashi, H. (2011). Reactive gliosis of astrocytes and Muller glial cells in retina of POMGnT1-deficient mice. Mol. Cell. Neurosci. 47, 119-130.
61. Uemura, A., Kusuhara, S., Wiegand, S. J., Yu, R. T. and Nishikawa, S. (2006). Tlx acts as a proangiogenic switch by regulating extracellular assembly of fibronectin matrices in retinal astrocytes. J. Clin. Invest. 116, 369-377.
62. Wagner, S., Tagaya, M., Koziol, J. A., Quaranta, V. and del Zoppo, G. J. (1997). Rapid disruption of an astrocyte interaction with the extracellular matrix mediated by integrin alpha 6 beta 4 during focal cerebral ischemia/ reperfusion. Stroke 28, 858-865.
63. Watanabe, T. and Raff, M. C. (1988). Retinal astrocytes are immigrants from the optic nerve. Nature 332, 834-837.
64. West, H., Richardson, W. D. and Fruttiger, M. (2005). Stabilization of the retinal vascular network by reciprocal feedback between blood vessels and astrocytes. Development 132, 1855-1862.
65. Wolburg, H., Neuhaus, J., Kniesel, U., Krauss, B., Schmid, E. M., Ocalan, M., Farrell, C. and Risau, W. (1994). Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J. Cell Sci. 107, 1347-1357.
66. Yurchenco, P. D. (2011). Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb. Perspect. Biol. 3, a004911.