The extracellular matrix protein laminin α2 regulates the maturation and function of the blood–brain barrier

Journal of Neuroscience

Volumn 34, Issue 46, 2014, Pages 15260-15280

  Menezes, Michael J ^a   McClenahan, Freyja K ^a   Leiton, Cindy V ^a   Aranmolate, Azeez ^a   Shan, Xiwei ^a   Colognato, Holly ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Astrocyte; Blood brain barrier; Dystroglycan; Gliovascular; Laminin; Pericyte

Indexed keywords

ALLOGRAFT INFLAMMATORY FACTOR 1; ALPHA SMOOTH MUSCLE ACTIN; AQUAPORIN 4; BETA DYSTROGLYCAN; BETA1 INTEGRIN; CLAUDIN 5; ENDOTHELIAL PROTEIN C RECEPTOR; GLUCOSE TRANSPORTER 1; LAMININ 211; LAMININ ALPHA2; MECA 32 PROTEIN; OCCLUDIN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN ZO1; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; DYSTROGLYCAN; LAMININ; MECA-32 ANTIGEN, MOUSE; MEMBRANE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN FUNCTION; BRAIN MATURATION; BRAIN PERICYTE; BRAIN WATER; CELL DENSITY; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; GENE MUTATION; GLIOSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MICROGLIA; MOUSE; MUSCULAR DYSTROPHY; NONHUMAN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RAT; TIGHT JUNCTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; ANIMAL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; MUTATION; NERVE CELL; PATHOLOGY; PHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIGENS, SURFACE; AQUAPORIN 4; ASTROCYTES; BLOOD-BRAIN BARRIER; DYSTROGLYCANS; ENDOTHELIUM, VASCULAR; GLUCOSE TRANSPORTER TYPE 1; LAMININ; MICE; MICE, KNOCKOUT; MUTATION; NEURONS; TIGHT JUNCTIONS;

EID: 84909942455     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3678-13.2014     Document Type: Article

References (53)

1. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ (2010) Structure and function of the blood– brain barrier. Neurobiol Dis 37:13–25. CrossRef Medline
2. Abraham S, Kogata N, Fässler R, Adams RH (2008) Integrin beta1 subunit controls mural cell adhesion, spreading, and blood vessel wall stability. Circ Res 102:562–570. CrossRef Medline
3. Agrawal S, Anderson P, Durbeej M, van Rooijen N, Ivars F, Opdenakker G, Sorokin LM (2006) Dystroglycan is selectively cleaved at the parenchymal basement membrane at sites of leukocyte extravasation in experimental autoimmune encephalomyelitis. J Exp Med 203:1007–1019. CrossRef Medline
4. Allamand V, Guicheney P (2002) Merosin-deficient congenital muscular dystrophy, autosomal recessive (MDC1A, MIM#156225, Lama2gene coding for alpha2 chain of laminin). Eur JHumGenet 10:91–94. CrossRef Medline
5. Amiry-Moghaddam M, Otsuka T, Hurn PD, Traystman RJ, Haug FM, Froehner SC, Adams ME, Neely JD, Agre P, Ottersen OP, Bhardwaj A (2003a) An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci U S A 100:2106-2111. CrossRef Medline
6. Amiry-Moghaddam M, Williamson A, Palomba M, Eid T, de Lanerolle NC, Nagelhus EA, Adams ME, Froehner SC, Agre P, Ottersen OP (2003b) Delayed K_ clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci U S A 100:13615–13620. CrossRef Medline
7. Armulik A, Genove´ G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C (2010) Pericytes regulate the blood– brain barrier. Nature 468:557–561. CrossRef Medline
8. Blake DJ, Hawkes R, Benson MA, Beesley PW (1999) Different dystrophinlike complexes are expressed in neurons and glia. J Cell Biol 147:645–658. CrossRef Medline
9. Buteică E, Roşulescu E, Burada F, Stãnoiu B, Zãvãleanu M (2008) Merosindeficient congenital muscular dystrophy type 1A. Rom J Morphol Embryol 49:229-233. Medline
10. Cannella B, Cross AH, Raine CS (1991) Adhesion-related molecules in the central nervous system: upregulation correlates with inflammatory cell influx during relapsing experimental autoimmune encephalomyelitis. Lab Invest 65:23–31. Medline
11. Caro PA, Scavina M, Hoffman E, Pegoraro E, Marks HG (1999) MR imaging findings in children with merosin-deficient congenital muscular dystrophy. AJNR Am J Neuroradiol 20:324–326. Medline
12. Chen ZL, Yao Y, Norris EH, Kruyer A, Jno-Charles O, Akhmerov A, Strickland S (2013) Ablation of astrocytic laminin impairs vascular smooth muscle cell function and leads to hemorrhagic stroke. J Cell Biol 202:381–395. CrossRef Medline
13. Colognato H, Yurchenco PD (2000) Form and function: the laminin family of heterotrimers. Dev Dyn 218:213–234. CrossRef Medline
14. Daneman R, Zhou L, Agalliu D, Cahoy JD, Kaushal A, Barres BA (2010a) The mouse blood– brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells. PLoS One 5:e13741. CrossRef Medline
15. Daneman R, Zhou L, Kebede AA, Barres BA (2010b) Pericytes are required for blood– brain barrier integrity during embryogenesis. Nature 468:562–566. CrossRef Medline
16. Del Zoppo GJ, Milner R (2006) Integrin–matrix interactions in the cerebral microvasculature. Arterioscler Thromb Vasc Biol 26:1966–1975. CrossRef Medline
17. Del Zoppo GJ, Milner R, Mabuchi T, Hung S, Wang X, Koziol JA (2006) Vascular matrix adhesion and the blood– brain barrier. Biochem Soc Trans 34:1261–1266. CrossRef Medline
18. Engelhardt B, Conley FK, Butcher EC (1994) Cell adhesion molecules on vessels during inflammation in the mouse central nervous system. J Neuroimmunol 51:199–208. CrossRef Medline
19. Fujii Y, Sugiura C, Fukuda C, Maegaki Y, Ohno K (2011) Sequential neuroradiological and neurophysiological studies in a Japanese girl with merosin-deficient congenital muscular dystrophy. Brain Dev 33:140–144. CrossRef Medline
20. Girardin F (2006) Membrane transporter proteins: a challenge for CNS drug development. Dialogues Clin Neurosci 8:311–321. Medline
21. Guadagno E, Moukhles H (2004) Laminin-induced aggregation of the inwardly rectifying potassium channel, Kir4.1, and the water-permeable channel, AQP4, via a dystroglycan-containing complex in astrocytes. Glia 47:138–149. CrossRef Medline
22. Hallmann R, Mayer DN, Berg EL, Broermann R, Butcher EC (1995) Novel mouse endothelial cell surface marker is suppressed during differentiation of the blood brain barrier. Dev Dyn 202:325–332. CrossRef Medline
23. Ioannidou S, Deinhardt K, Miotla J, Bradley J, Cheung E, Samuelsson S, Ng YS, Shima DT (2006) An in vitro assay reveals a role for the diaphragm protein PV-1 in endothelial fenestra morphogenesis. Proc Natl Acad Sci U S A 103:16770–16775. CrossRef Medline
24. Jimenez-Mallebrera C, Brown SC, Sewry CA, Muntoni F (2005) Congenital muscular dystrophy: molecular and cellular aspects. Cell Mol Life Sci 62:809–823. CrossRef Medline
25. Jucker M, Tian M, Norton DD, Sherman C, Kusiak JW (1996) Laminin alpha 2 is a component of brain capillary basement membrane: reduced expression in dystrophic dy mice. Neuroscience 71:1153–1161. CrossRef Medline
26. Komarova Y, Malik AB (2010) Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 72: 463–493. CrossRef Medline
27. Lien CF, Mohanta SK, Frontczak-Baniewicz M, Swinny JD, Zablocka B, Gérecki DC (2012) Absence of glial alpha-dystrobrevin causes abnormalities of the blood– brain barrier and progressive brain edema. J Biol Chem 287:41374–41385. CrossRef Medline
28. Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, Betsholtz C (2003) Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 17:1835–1840. CrossRef Medline
29. Miner JH, Yurchenco PD (2004) Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol 20:255–284. CrossRef Medline
30. Miyagoe Y, Hanaoka K, Nonaka I, Hayasaka M, Nabeshima Y, Arahata K, Nabeshima Y,Takeda S (1997) Laminin alpha2 chain-null mutant mice by targeted disruption of the Lama2 gene: a new model of merosin (laminin 2)-deficient congenital muscular dystrophy. FEBS Lett 415:33–39. CrossRef Medline
31. Miyagoe-Suzuki Y, Nakagawa M, Takeda S (2000) Merosin and congenital muscular dystrophy. Microsc Res Tech 48:181–191. CrossRef Medline
32. Moore SA, Saito F, Chen J, Michele DE, Henry MD, Messing A, Cohn RD, Ross-Barta SE, Westra S, Williamson RA, Hoshi T, Campbell KP (2002) Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418:422–425. CrossRef Medline
33. Nico B, Paola Nicchia G, Frigeri A, Corsi P, Mangieri D, Ribatti D, Svelto M, Roncali L (2004) Altered blood– brain barrier development in dystrophic MDX mice. Neuroscience 125:921–935. CrossRef Medline
34. Noël G, Tham DK, Moukhles H (2009) Interdependence of lamininmediated clustering of lipid rafts and the dystrophin complex in astrocytes. J Biol Chem 284:19694–19704. CrossRef Medline
35. Reese TS, Karnovsky MJ (1967) Fine structural localization of a blood– brain barrier to exogenous peroxidase. J Cell Biol 34:207–217. CrossRef Medline
36. Relucio J, Menezes MJ, Miyagoe-Suzuki Y, Takeda S, Colognato H (2012) Laminin regulates postnatal oligodendrocyte production by promoting oligodendrocyte progenitor survival in the subventricular zone. Glia 60: 1451–1467. CrossRef Medline
37. Robel S, Mori T, Zoubaa S, Schlegel J, Sirko S, Faissner A, Goebbels S, Dimou L, Götz M (2009) Conditional deletion of beta1-integrin in astroglia causes partial reactive gliosis. Glia 57:1630–1647. CrossRef Medline
38. Rurak J, Noel G, Lui L, Joshi B, Moukhles H (2007) Distribution of potassium ion and water permeable channels at perivascular glia in brain and retina of the Large(myd) mouse. J Neurochem 103:1940–1953. CrossRef Medline
39. Schulz M, Engelhardt B (2005) The circumventricular organs participate in the immunopathogenesis of experimental autoimmune encephalomyelitis. Cerebrospinal Fluid Res 2:8. CrossRef Medline
40. Shue EH, Carson-Walter EB, Liu Y, Winans BN, Ali ZS, Chen J, Walter KA (2008) Plasmalemmal vesicle associated protein-1 (PV-1) is a marker of blood– brain barrier disruption in rodent models. BMC Neurosci 9:29. CrossRef Medline
41. Sixt M, Engelhardt B, Pausch F, Hallmann R, Wendler O, Sorokin LM (2001) Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood– brain barrier in experimental autoimmune encephalomyelitis. J Cell Biol 153:933–946. CrossRef Medline
42. Sparks DL, Kuo YM, Roher A, Martin T, Lukas RJ (2000) Alterations of Alzheimer’s disease in the cholesterol-fed rabbit, including vascular inflammation: preliminary observations. Ann N Y Acad Sci 903:335–344. CrossRef Medline
43. Thyboll J, Kortesmaa J, Cao R, Soininen R, Wang L, Iivanainen A, Sorokin L, Risling M, Cao Y, Tryggvason K (2002) Deletion of the laminin alpha4 chain leads to impaired microvessel maturation. Mol Cell Biol 22:1194–1202. CrossRef Medline
44. Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schütz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103. CrossRef Medline
45. Vajda Z, Pedersen M, Füchtbauer EM, Wertz K, Stødkilde-Jørgensen H, Sulyok E, Dóczi T, Neely JD, Agre P, Frøkiaer J, Nielsen S (2002) Delayed onset of brain edema and mislocalization of aquaporin-4 in dystrophin-null transgenic mice. Proc Natl Acad Sci U S A 99:13131–13136. CrossRef Medline
46. Voisin MB, Probstl D, Nourshargh S (2010) Venular basement membranes ubiquitously express matrix protein low-expression regions: characterization in multiple tissues and remodeling during inflammation. J Pathol 176:482–495. CrossRef Medline
47. Wang S, Voisin MB, Larbi KY, Dangerfield J, Scheiermann C, Tran M, Maxwell PH, Sorokin L, Nourshargh S (2006) Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med 203:1519–1532. CrossRef Medline
48. Wu C, Ivars F, Anderson P, Hallmann R, Vestweber D, Nilsson P, Robenek H, Tryggvason K, Song J, Korpos E, Loser K, Beissert S, Georges-Labouesse E, Sorokin LM (2009) Endothelial basement membrane laminin alpha5 selectively inhibits T lymphocyte extravasation into the brain. Nat Med 15:519–527. CrossRef Medline
49. Yao Y, Chen ZL, Norris EH, Strickland S (2014) Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat Commun 5:3413. CrossRef Medline
50. Yoshioka M, Higuchi Y, Fujii T, Aiba H, Toda T (2008) Seizure– genotype relationship in Fukuyama-type congenital muscular dystrophy. Brain Dev 30:59–67. CrossRef Medline
51. Yousif LF, Di Russo J, Sorokin L (2013) Laminin isoforms in endothelial and perivascular basement membranes. Cell Adh Migr 7:101–110. CrossRef Medline
52. Yu D, Corbett B, Yan Y, Zhang GX, Reinhart P, Cho SJ, Chin J (2012) Early cerebrovascular inflammation in a transgenic mouse model of Alzheimer’s disease. Neurobiol Aging 33:2942–2947. CrossRef Medline
53. Zaccaria ML, Di Tommaso F, Brancaccio A, Paggi P, Petrucci TC (2001) Dystroglycan distribution in adult mouse brain: a light and electron microscopy study. Neuroscience 104:311–324. CrossRef Medline