β2 and γ3 laminins are critical cortical basement membrane components: Ablation of Lamb2 and Lamc3 genes disrupts cortical lamination and produces dysplasia

Developmental Neurobiology

Volumn 73, Issue 3, 2013, Pages 209-229

  Radner, Stephanie ^a   Banos, Charles ^a   Bachay, Galina ^b,c   Li, Yong N ^a   Hunter, Dale D ^b,c   Brunken, William J ^a,b,c   Yee, Kathleen T ^a,d  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c SUNY Downstate Medical Center   (United States)

^d UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

Author keywords

Cortical lamination; Extracellular matrix; Lissencephaly; Pial basement membrane; Radial glia

Indexed keywords

DYSTROGLYCAN; LAMININ; LAMININ BETA2; LAMININ GAMMA3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN CORTEX; CELL STRUCTURE; CELLULAR DISTRIBUTION; COBBLESTONE LISSENCEPHALY; COILED BODY; CONTROLLED STUDY; CORTICAL DYSPLASIA; DISEASE SEVERITY; GENE DISRUPTION; GENE FUSION; GLIA CELL; HOMOZYGOSITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; BASEMENT MEMBRANE; CEREBRAL CORTEX; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LAMININ; MICE; MICE, KNOCKOUT; NEUROGENESIS;

EID: 84873417754     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22057     Document Type: Article

References (56)

1. Ackroyd MR, Whitmore C, Prior S, Kaluarachchi M, Nikolic M, Mayer U, Muntoni F, et al. 2011. Fukutinrelated protein alters the deposition of laminin in the eye and brain. J Neurosci 31:12927-12935.
2. Balasubramani M, Schreiber EM, Candiello J, Balasubramani GK, Kurtz J, Halfter W. 2010. Molecular interactions in the retinal basement membrane system: A proteomic approach. Matrix Biol 29:471-483.
3. Barak T, Kwan KY, Louvi A, Demirbilek V, Saygi S, Tüysüz B, Choi M, et al. 2011. Recessive LAMC3 mutations cause malformations of the occipital cortical development. Nat Genet 43:590-594.
4. Beggs HE, Schahin-Reed D, Zang K, Goebbels S, Nave KA, Gorski J, Jones KR, et al. 2003. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40:501-514.
5. Bielle F, Griveau A, Narboux-Nême N, Vigneau S, Sigrist M, Arber S, Wassef M, et al. 2005. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8:1002-1012.
6. Blaess S, Graus-Porta D, Belvindrah R, Radakovits R, Pons S, Littlewood-Evans A, Senften M, et al. 2004. Beta1- integrins are critical for cerebellar granule cell precursor proliferation. J Neurosci 24:3402-3412.
7. Bupesh M, Legaz I, Abellán A, Median L. 2011. Multiple telencephalic and extratelencephalic embryonic domains contribute neurons to the medial extended amygdala. J Comp Neurol 519:1505-1525.
8. Costell M, Gustafsson E, Aszódi A, Mörgelin M, Bloch W, Hunziker E, Addicks K, et al. 1999. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol 147:1109-1122.
9. D'Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T. 1997. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci 17:23-31.
10. Egles C, Claudepierre T, Manglapus MK, Champliaud MF, Brunken WJ, Hunter DD. 2007. Laminins containing the beta2 chain modulate precise organization of CNS synapses. Mol Cell Neurosci 34:288-298.
11. Ervasti JM, Campbell KP. 1993. A role for the dystrophinglycoprotein complex as a transmembrane linker between laminin and actin. J Cell Biol 122:809-823.
12. Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, Wiedemann H, Mann K, et al. 1991. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10:3137-3146.
13. Georges-Labouesse E, Mark M, Messaddeq N, Gansmüller A. 1998. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr Biol 8:983-986.
14. Goulding MD, Lumsden A, Gruss P. 1993. Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 117:1001-1016.
15. García-López M, Abellan A, Legaz I, Rubenstein JLR, Puelles L, Medina L. 2008. Histogenetic compartments of the mouse centromedial and extended amygdala based on gene expression patterns during development. J Comp Neurol 506:46-74.
16. García-Moreno F, López-Mascaraque L, DeCarlos JA. 2007. Origins and migratory routes of murine cajalretzius cells. J Comp Neurol 500:419-432.
17. Graus-Porta D, Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z, Orban P, et al. 2001. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31:367-379.
18. Grimpe B, Dong S, Doller C, Temple K, Malouf AT, Silver J. 2002. The critical role of basement membrane-independent laminin gamma 1 chain during axon regeneration in the CNS. J Neurosci 22:3144-3160.
19. Halfter W, Dong S, Yip YP, Willem M, Mayer U. 2002. A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 22:6029-6040.
20. Hartfuss E, Förster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, et al. 2003. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597-4609.
21. Hatten ME. 1999. Central nervous system neuronal migration. Annu Rev Neurosci 22:511-539.
22. Hawthorne AL, Wylie CJ, Landmesser LT, Deneris ES, Silver J. 2010. Serotonergic neurons migrate radially through the neuroepithelium by dynamin-mediated somal translocation. J Neurosci 30:420-430.
23. Hirrlinger PG, Pannicke T, Winkler U, Claudepierre T, Varshney S, Schulze C, Reichenbach R, et al. 2011. Genetic deletion of laminin isoforms b2 and c3 induces a reduction in Kir4.1 and aquaporin-4 expression and function in the retina. PLoS One 6:e16106.
24. Hu H, Yang Y, Eade A, Xiong Y, Qi Y. 2007 Breaches of the pial basement membrane and disappearance of the glia limitans during development underlie the cortical lamination defect in the mouse model of muscle-eyebrain disease. J Comp Neurol 502:168-183.
25. Hunter DD, Llinas R, Ard M, Merlie JP, Sanes JR. 1992. Expression of s-laminin and laminin in the developing rat central nervous system. J Comp Neurol 323:238-251.
26. Jucker M, Bialobok P, Hagg T, Ingram DK. 1992. Laminin immunohistochemistry in brain is dependent on method of tissue fixation. Brain Res 586:166-170.
27. Kriegstein A, Alvarez-Buylla A. 2009. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149-184.
28. Labelle-Dumais C, Dilworth DJ, Harrington EP, de Leau M, Lyons D, Kabaeva Z, Manzini MC, et al. 2011. COL4A1 mutations cause ocular dysgenesis, neuronal localization defects, and myopathy in mice and Walker- Warburg syndrome in humans. PLoS Genet 7:1-14.
29. Li S, Jin Z, Koirala S, Bu L, Xu L, Hynes RO, Walsh CA, et al. 2008. GPR56 regulates pial basement membrane integrity and cortical lamination. J Neurosci 28:5817-5826.
30. Li S, Harrison D, Carbonetto S, Fassler R, Smyth N, Edgar D, Yurchenco PD. 2002. Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J Cell Biol 157:1279-1290.
31. Li YN, Radner S, French MM, Pinzón-Duarte G, Daly GH, Burgeson RE, Koch M, et al. 2012 The c3 chain of laminin is widely expressed and contributes to basement membranes in mouse: Expression and functional studies. Matrix Biol 31:120-134.
32. Libby RT, Lavallee CR, Balkema GW, Brunken WJ, Hunter DD. 1999. Disruption of laminin beta2 chain production causes alterations in morphology and function in the CNS. J Neurosci 19:9399-9411.
33. Libby RT, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, Koch M, Burgeson RE, et al. 2000. Laminin expression in adult and developing retinae: Evidence of two novel CNS laminins. J Neurosci 20:6517-6528.
34. Loulier K, Lathia JD, Marthiens V, Relucio J, Mughal MR, Tang SC, Coksaygan T, et al. 2009. b1 Integrin maintains integrity of the embryonic neocortical stem cell niche. PLoS Biol 7:e1000176.
35. Lui JH, Hansen DV, Kriegstein AR. 2011. Development and evolution of the human neocortex. Cell 146:18-36.
36. Luo R, Jeong SJ, Jin Z, Strokes N, Li S, Piao X. 2011. G-protein coupled receptor 56 and collagen III, a receptor- ligand pair, regulates cortical development and lamination. Proc Natl Acad Sci USA 108:12925-12930.
37. Marin O, Rubenstein JL. 2003. Cell migration in the forebrain. Annu Rev Neurosci 26:441-483.
38. Miosge N. 2001. The ultrastructural composition of basement membranes in vivo. Histol Histopathol 16:1239-1248.
39. Mochida GH, Walsh CA. 2004. Genetic basis of developmental malformations of the cerebral cortex. Arch Neurol 61:637-640.
40. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, et al. 2002. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418:422-425.
41. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
42. Niewmierzycka A, Mills J, St-Arnaud R, Dedhar S, Reichardt LF. 2005. Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J Neurosci 25:7022-7031.
43. Noakes PG, Gautam M, Mudd J, Sanes JR, Merlie JP. 1995. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin beta 2. Nature 374:258-262.
44. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7:136-144.
45. Olson EC, Walsh CA. 2002. Smooth, rough and upsidedown neocortical development. Curr Opin Genet Dev 3:320-327.
46. Pinto L, Götz M. 2007. Radial glial cell heterogeneity- The source of diverse progeny in the CNS. Prog Neurobiol 83:2-23.
47. Pinzón-Duarte G, Daly G, Yong Li, Hunter DD, Koch M, Brunken WJ. 2010. Genetic deletion of both b2 and c3 laminin chains produces retinal dysplasia. Invest Ophthalmol Vis Sci 51:1773-1782.
48. Pöschl E, Schlötzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U. 2004. Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131:1619-1628.
49. Postiglione MP, Jüschke C, Xie Y, Haas GA, Charalambous C, Knoblich JA. 2011. Mouse inscuteable induces apicalbasal spindle orientation to facilitate intermediate progenitor generation in the developing neocortex. Neuron 72:269-284.
50. Sanes JR, Engvall E, Butkowski R, Hunter DD. 1990. Molecular heterogeneity of basal laminae: Isoforms of laminin and collagen IV at the neuromuscular junction and elsewhere. J Cell Biol 111:1685-1699.
51. Satz JS, Ostendorf AP, Hou S, Turner A, Kusano H, Lee JC, Turk R, et al. 2010. Distinct functions of glial and neuronal dystroglycan in the developing and adult mouse brain. J Neurosci 30:14560-14572.
52. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, Paulsson M, Edgar D. 1999. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol 144:151-160.
53. Soriano E, del Río JA. 2005. The cells of Cajal-Retzius: Still a mystery one century after. Neuron 46:389-394.
54. Takiguchi-Hayashi K, Sekiguchi M, Asigaki S, Takamatsu M, Hasegawa H, Suzuki-Migishima R, Yokoyama M, et al. 2004. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J Neurosci 24:2286-2295.
55. Yurchenco PD, Amenta PS, Patton BL. 2004. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol 22:521-538.
56. Yurchenco PD, Patton BL. 2009. Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 15:1277-1294.