The Bi-Functional Organization of Human Basement Membranes

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Halfter, Willi ^a   Monnier, Christophe ^b   Müller, David ^b   Oertle, Philipp ^b   Uechi, Guy ^c   Balasubramani, Manimalha ^c   Safi, Farhad ^c   Lim, Roderick ^b   Loparic, Marko ^b   Henrich, Paul Bernhard ^d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF PITTSBURGH   (United States)

^d UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 4; LAMININ; PROTEOGLYCAN;

ADULT; AGED; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; ATOMIC FORCE MICROSCOPY; BASEMENT MEMBRANE; BINDING AFFINITY; CELL ADHESION; CELL POLARITY; CHICK; CONTROLLED STUDY; DESCEMET MEMBRANE; EMBRYO; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; INNER LIMITING MEMBRANE; LENS CAPSULE; MOLECULAR WEIGHT; MORPHOLOGY; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALS; BASEMENT MEMBRANE; CELL ADHESION; CHICK EMBRYO; COLLAGEN; EXTRACELLULAR MATRIX; HUMANS; LAMININ; MICE; PROTEIN TRANSPORT; PROTEOGLYCANS;

METAZOA; MUS;

EID: 84879767137     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067660     Document Type: Article

References (61)

1. Yurchenco PD, Patton BL, (2009) Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des 15: 1277-1294.
2. Timpl R, (1996) Brown,JC (1996) Supramolecular assembly of basement membranes. Bioassays 18: 123-132.
3. Erickson AC, Couchman JR, (2000) Still more complexity in mammalian basement membranes. J Histochem and Cytochem 48: 1291-1306.
4. Stephens LE, Sutherland AE, Klimanskaya IV, Andrieux A, Meneses J, et al. (1995) Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality. Genes Dev 9: 1896-908.
5. Fassler R, Meyer M, (1995) Consequences of lack of β1 integrin gene expression in mice. Genes Dev 9: 1896-908.
6. Henry MD, Campbell KP, (1998) A role of dystroglycan in basement membrane assembly. Cell 95: 859-870.
7. Gautam M, Noakes PG, Moscovo L, Rupp F, Scheller RH, et al. (1996) Defective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85: 525-535.
8. Miner JH, Cunningham J, Sanes JR, (1998) Roles of laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J Cell Biol. 143: 1713-1723.
9. Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell, JR, Yamada Y, (1999) Perlecan is essential for cartilage and cephalic development. Nature Genetics 23: 354-358.
10. Smyth N, Vatansever HS, Murray P, Meyer M, Frie C, et al. (1999) Absence of basement membranes after targeting the LANC1 gene results in embryonic lethality due to failure of endoderm differentiation. J Cell Biol. 144: 151-160.
11. Costell M, Gustafsson E, Aszodi A, Moergelin M, Bloch E, et al. (1999) Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol. 147: 1109-1122.
12. Willem M, Miosge N, Halfter W, Smyth N, Janetti I, et al. (2001) Specific ablation of the nidogen binding site in the laminin γ1 chain interferes with kidney and lung development. Development 129: 2711-2722.
13. Fukai N, Eklund L, Marneros AG, Oh SP, Keene DR, et al. (2002) Lack of collagen XVIII/endostatin results in eye abnormalities. EMBO J 21: 1535-1544.
14. Pöschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, et al. (2004) Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131: 1619-1628.
15. Bader BL, Smyth N, Nedbal S, Miosge N, Baranowsky A, et al. (2005) Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol Cell Biol 25: 846-6856.
16. Gould DB, Phalan FC, Breedveld GJ, van Mil SE, Smith RS, et al. (2005) Mutations in Col4a1 cause perinatal cerebral hemorrhage and porencephaly. Science. 308: 1167-1171.
17. Lee J, Gross JM, (2007) Laminin beta1 and gamma1 containing laminins are essential for basement membrane integrity in zebra fish eye. Invest Ophthal Vis Sci 48: 2483-2490.
18. Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, et al. (1991) Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10: 3137-3146.
19. Timpl R, Wiedemannn H, vanDelden V, Furthmayr H, (1981) Kühn (1981) A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem 120: 203-211.
20. Candiello J, Cole GJ, Halfter W, (2010) Age-dependent changes in the structure, composition and biophysical properties of a human basement membrane. Matrix Biol. 29: 402-410.
21. Candiello J, Balasubramani M, Schreiber EM, Cole GJ, Mayer U, et al. (2007) Biomechanical properties of native basement membranes. Febs J 274: 2897-2908.
22. Balasubramani M, Schreiber ME, Candiello J, Balasubramani GK, Kurtz J, et al. (2010) Molecular interactions in the retinal basement membrane system: a proteomic approach. Matrix Biol. 29: 471-483.
23. Danysh BP, Czymmek KJ, Olurin PT, Sivak JG, Dunkan MK, (2008) Contributions of mouse genetic background and age on anterior lens capsule thickness. Anat Rec 291: 1819-1827.
24. Halfter W, von Boxberg Y, (1992) Axonal growth on solubilized and reconstituted matrix from the embryonic chicken retina inner limiting membrane. Eur J Neurosc 4: 840-852.
25. Halfter W, Reckhaus W, Kroeger S, (1987) Nondirected axonal growth on basal lamina from the embryonic avian retina. J of Neuroscience 7: 3712-3722.
26. Sado Y, Kagawa M, Kishiro Y, Sugihara K, Seyer JM, et al. (1995) Establishment by the rat lymph node method of epitope-defined monoclonal antibodies recognizing the six different α chains of human type IV collagen. Histochem Cell Biol. 104: 267-275.
27. SundarRaj N, Wilson J, (1982) Monoclonal antibody to human basement membrane collagen IV. Immunology 47: 133-140.
28. Henrich PB, Monnier CA, Halfter W, Haritoglu C, Strauss RW, et al. (2012) Nanoscale topographic and biomechanical studies of the human inner limiting membrane. Invest Ophthalmol Vis Sci 29: 2561-2570.
29. Chen J, Wong-Chong J, SundarRaj N, (2011) FGF-2 and TGF-ß1-induced downregulation of lumican and keratocan in activated corneal keratocytes by JNK signaling pathway. Invest Ophthal Vis Sci 21: 8957-8964.
30. Halfter W, Newgreen DF, Sauter J, Schwarz U, (1983) Oriented axon outgrowth from avian embryonic retinae in culture. Dev Biol 95: 56-64.
31. Libby RT, Champliaud M-F, Claudepierre T, Xu Y, Gibbons EP, et al. (2000) Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J Neurosci 20: 6517-6528.
32. Uechi G, Halfter W, Balasubramani M (2013) Proteomic analysis of human BMs. In preparation.
33. Hudson BG, Gunwar S, Chung AE, Burgeson RE (1995) Matrix components (type IV and VII collagen, entactin, and laminin) found in basement membranes. In: Extracellular Matrix. A practical approach. Eds. MA. Haralson and JR. Hassell. Oxford University Press.
34. Risteli J, Bächinger HP, Engel J, Furthmayr H, Timpl R, (1980) 7-S collagen: characterization of an unusual basement membrane structure. Eur J Biochem. 108: 239-250.
35. Dukes JD, Whitley P, Chalmers AD, (2011) The MDCK variety pack: choosing the right strain. BMC Cell Biol. 12: 43-46.
36. Behrens DT, Villone D, Koch M, Brunner G, Sorokin L, et al. (2012) The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem 287: 18700-18709.
37. Sarthy PV, Fu M, (1990) Localization of laminin B1 mRNA in retinal ganglion cells by in situ hybridization. J Cell Biol 110: 2099-2108.
38. Dong LJ, Chung AE, (1991) The expression of the genes for entactin, laminin A, laminin B1 and laminin B2 in murine lens morphogenesis and eye development. Differentiation 48: 157-172.
39. Sarthy V, (1993) Collagen IV mRNA expression during development of the mouse retina: an in situ hybridization study. Invest Ophthalmol Vis Sci 34: 145-152.
40. Dong S, Landfair J, Balasubramani M, Bier ME, Cole G, et al. (2002) Expression of basal lamina protein mRNA in the early embryonic chick eye. J Comp Neurol 447: 261-273.
41. Halfter W, Dong S, Dong A, Eller AW, Nischt R, (2008) Origin and turnover of ECM proteins from the inner limiting membrane and vitreous body. Eye 22: 1207-1213.
42. Yin Y, Kikkawa Y, Mudd J, Skarnes WC, Sanes JR, et al. (2003) Expression of laminin chains by central neurons: analysis with gene and protein trapping techniques. Genesis 36: 114-127.
43. Halfter W, Dong S, Schurer B, Ring C, Cole GJ, et al. (2005) Embryonic synthesis of the inner limiting membrane and vitreous body. Invest Ophthalmol Vis Sci 46: 2202-220.
44. Murphy C, Alvarado J, Juster R, (1984) Prenatal and postnatal growth of the human Descemet's membrane. Invest Ophthal Vis Sci 25: 1402-1415.
45. Danysh BP, Duncan MK, (2008) The lens capsule. Exp Eye Res 88: 151-164.
46. Vazquez F, Palacios S, Aleman N, Guerrero F, (1996) Changes in the basement membranes and type IV collagen in human skin during aging. Maturitas 25: 209-215.
47. Neuman KH, Kellner C, Kühn K, Stolte H, Schurek HJ, (2004) Age-dependent thickening of glomerular basement membrane has no major effect on glomerular hydraulic conductivity. Nephrol Dial Transpl 19: 805-811.
48. Kobosova A, Azar DT, Bannikov GA, Campbell KP, Durbeej M, et al. (2007) Compositional differences between infant and adult human corneal basement membranes. Invest Ophthalmol Vis Sci 48: 4989-4999.
49. Pulkinen L, Christiano AM, Airenne T, (1994) Mutations in the gamma2 chain gene (LAMC2) of Kalinin/laminin 5 in the junctional form of epidermolysis bullosa. Nat Genet 6: 293-297.
50. Aberdam D, Galliano MF, Vailly J, (1994) Herlitz's junctional epidermolysis bullosa is linked to mutations in the gene (LAMC2) for the gamma 2 subunit of nicein/kalinin (LAMININ-5). Nat Genet 6: 299-304.
51. Kivirikko S, McGrath JA, Baudoin C, (1995) A homozygous nonsense mutation in the alpha 3 chain gene laminin 5 (LAMA3) in lethal (Herlitz) junctional epidermolysis bullosa. Hum Mol Genet 4: 959-962.
52. Davis GE, Blaker SN, Engvall E, Varon S, Manthorpe M, et al. (1978) Human amnion membrane serves as a substratum for growing axons in vitro and in vivo. Science 236: 106-109.
53. Schlie K, Maisa A, Freiberg F, Groseth A, Strecker T, et al. (2010) Viral protein determinants of Lassa virus entry and release from polarized epithelial cells. J Virol 84: 3178-3188.
54. Hasenson S, Maattta M, Rousselle P, Kikkawa Y, Miner JH, et al. (2005) The immortalized human corneal epithelial cells adhere to laminin-10 by using the Lutheran glycoprotein and integrin a3b1. Exp Eye Res 81: 415-421.
55. Schoenenberger C-A, Zuk A, Zinkl GM, Kendall D, Matlin KS, (1994) Integrin expression and localization in normal MDCK cells and transformed MDCK cells lacking apical polarity. J Cell Sci 107: 527-541.
56. Cann GM, Bradshaw AD, Gervin DB, Hunter AW, Clegg DO, (1996) Widespread expression of b1 integrins in the developing chick retina: evidence for a role in migration of retinal ganglion cells. Dev Biol 180: 82-96.
57. Stepp MA, (2006) Corneal integrins and their functions. Exp Eye Res 83: 3-15.
58. Silva R, D'Amico G, Kairbaan MH-D, Reynolds LE, (2008) Integrins: the keys to unlocking angiogenesis. Artherioscler Thrombosis Vasc Bio 28: 1703-1713.
59. Hynes RO, (2012) The evolution of the extracellular matrix. J Cell Biol 195: 671-679.
60. Nayak BR, Spiro RG, (1991) Localization and structure of the asparagine-linked oligosaccharides of type IV collagen from glomerular basement membrane and lens capsule. J Biol Chem 266: 13978-13987.
61. Langeveld JPM, Noelken ME, Hard K, Todd P, Vliegenthart JF, et al. (1991) Bovine glomerular basement membrane. Location and structure of the asparagine-linked oligosaccharide units and their potential role in the assembly of the 7S collagen IV tetramer. J Biol Chem 266: 2622-2631.