Collagen IV Exploits a Cl- Step Gradient for Scaffold Assembly.
Basement membrane
Cl−
Collagen IV
Extracellular matrix
Kinetics
NC1 domain
Protein assembly
Journal
Advances in experimental medicine and biology
ISSN: 0065-2598
Titre abrégé: Adv Exp Med Biol
Pays: United States
ID NLM: 0121103
Informations de publication
Date de publication:
2021
2021
Historique:
pubmed:
27
9
2020
medline:
4
3
2021
entrez:
26
9
2020
Statut:
ppublish
Résumé
Collagen molecules are crucial extracellular players in animal tissue development and in functions ranging from ultrafiltration to organism locomotion. Among the 28 types of collagen found in human, type IV collagen stands out as a primordial type found in all species of the animal kingdom. Collagen IV forms smart scaffolds for basement membranes, sheet-like acellular structures that isolate, coordinate, and direct cells during morphogenesis. Collagen IV is also involved in multiple functions in developed tissues. As part of the basement membrane, collagen IV scaffolds provide mechanical strength, spatially tether extracellular macromolecules and directly signal to cells via receptor binding sites. Proper assembly and structure of the scaffolds are critical for development and function of multiple types of basement membranes. Within last 5 years it was established that Cl
Identifiants
pubmed: 32979156
doi: 10.1007/5584_2020_582
doi:
Substances chimiques
Collagen Type IV
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
129-141Subventions
Organisme : NIDDK NIH HHS
ID : R01 DK018381
Pays : United States
Références
Andersen O (2013) Cellular electrolyte metabolism. Encyclopedia of metalloproteins. Springer, New York
Armstrong CM (2003) The Na/K pump, Cl ion, and osmotic stabilization of cells. Proc Natl Acad Sci U S A 100(10):6257–6262. https://doi.org/10.1073/pnas.0931278100
doi: 10.1073/pnas.0931278100
pubmed: 12730376
pmcid: 156359
Bachinger HP, Fessler LI, Fessler JH (1982) Mouse procollagen IV. Characterization and supramolecular association. J Biol Chem 257(16):9796–9803
doi: 10.1016/S0021-9258(18)34142-5
Bhave G, Cummings CF, Vanacore RM, Kumagai-Cresse C, Ero-Tolliver IA, Rafi M, Kang JS, Pedchenko V, Fessler LI, Fessler JH, Hudson BG (2012) Peroxidasin forms sulfilimine chemical bonds using hypohalous acids in tissue genesis. Nat Chem Biol 8(9):784–790. https://doi.org/10.1038/nchembio.1038
doi: 10.1038/nchembio.1038
pubmed: 22842973
pmcid: 4128002
Borza DB, Bondar O, Ninomiya Y, Sado Y, Naito I, Todd P, Hudson BG (2001) The NC1 domain of collagen IV encodes a novel network composed of the alpha 1, alpha 2, alpha 5, and alpha 6 chains in smooth muscle basement membranes. J Biol Chem 276(30):28532–28540. https://doi.org/10.1074/jbc.M103690200
doi: 10.1074/jbc.M103690200
pubmed: 11375996
Boudko SP, Danylevych N, Hudson BG, Pedchenko VK (2018) Basement membrane collagen IV: isolation of functional domains. Methods Cell Biol 143:171–185. https://doi.org/10.1016/bs.mcb.2017.08.010
doi: 10.1016/bs.mcb.2017.08.010
pubmed: 29310777
Boutaud A, Borza DB, Bondar O, Gunwar S, Netzer KO, Singh N, Ninomiya Y, Sado Y, Noelken ME, Hudson BG (2000) Type IV collagen of the glomerular basement membrane. Evidence that the chain specificity of network assembly is encoded by the noncollagenous NC1 domains. J Biol Chem 275(39):30716–30724. https://doi.org/10.1074/jbc.M004569200
doi: 10.1074/jbc.M004569200
pubmed: 10896941
Brown KL, Cummings CF, Vanacore RM, Hudson BG (2017) Building collagen IV smart scaffolds on the outside of cells. Protein Sci 26(11):2151–2161. https://doi.org/10.1002/pro.3283
doi: 10.1002/pro.3283
pubmed: 28845540
pmcid: 5654846
Casino P, Gozalbo-Rovira R, Rodriguez-Diaz J, Banerjee S, Boutaud A, Rubio V, Hudson BG, Saus J, Cervera J, Marina A (2018) Structures of collagen IV globular domains: insight into associated pathologies, folding and network assembly. IUCr J 5(Pt 6):765–779. https://doi.org/10.1107/S2052252518012459
doi: 10.1107/S2052252518012459
Cosgrove D, Liu S (2017) Collagen IV diseases: a focus on the glomerular basement membrane in Alport syndrome. Matrix Biol 57-58:45–54. https://doi.org/10.1016/j.matbio.2016.08.005
doi: 10.1016/j.matbio.2016.08.005
pubmed: 27576055
Cummings CF, Pedchenko V, Brown KL, Colon S, Rafi M, Jones-Paris C, Pokydeshava E, Liu M, Pastor-Pareja JC, Stothers C, Ero-Tolliver IA, McCall AS, Vanacore R, Bhave G, Santoro S, Blackwell TS, Zent R, Pozzi A, Hudson BG (2016) Extracellular chloride signals collagen IV network assembly during basement membrane formation. J Cell Biol 213(4):479–494. https://doi.org/10.1083/jcb.201510065
doi: 10.1083/jcb.201510065
pubmed: 27216258
pmcid: 4878091
Fidler AL, Darris CE, Chetyrkin SV, Pedchenko VK, Boudko SP, Brown KL, Gray Jerome W, Hudson JK, Rokas A, Hudson BG (2017) Collagen IV and basement membrane at the evolutionary dawn of metazoan tissues. elife 6. https://doi.org/10.7554/eLife.24176
Gunwar S, Ballester F, Noelken ME, Sado Y, Ninomiya Y, Hudson BG (1998) Glomerular basement membrane. Identification of a novel disulfide-cross-linked network of alpha3, alpha4, and alpha5 chains of type IV collagen and its implications for the pathogenesis of Alport syndrome. J Biol Chem 273(15):8767–8775. https://doi.org/10.1074/jbc.273.15.8767
doi: 10.1074/jbc.273.15.8767
pubmed: 9535854
Hudson BG, Kalluri R, Gunwar S, Noelken ME (1994) Structure and organization of type IV collagen of renal glomerular basement membrane. Contrib Nephrol 107:163–167. https://doi.org/10.1159/000422975
doi: 10.1159/000422975
pubmed: 8004963
Hudson BG, Tryggvason K, Sundaramoorthy M, Neilson EG (2003) Alport’s syndrome, Goodpasture’s syndrome, and type IV collagen. N Engl J Med 348(25):2543–2556. https://doi.org/10.1056/NEJMra022296
doi: 10.1056/NEJMra022296
pubmed: 12815141
Jayadev R, Sherwood DR (2017) Basement membranes. Curr Biol 27(6):R207–R211. https://doi.org/10.1016/j.cub.2017.02.006
doi: 10.1016/j.cub.2017.02.006
pubmed: 28324731
Kahsai TZ, Enders GC, Gunwar S, Brunmark C, Wieslander J, Kalluri R, Zhou J, Noelken ME, Hudson BG (1997) Seminiferous tubule basement membrane. Composition and organization of type IV collagen chains, and the linkage of alpha3(IV) and alpha5(IV) chains. J Biol Chem 272(27):17023–17032. https://doi.org/10.1074/jbc.272.27.17023
doi: 10.1074/jbc.272.27.17023
pubmed: 9202017
Kefalides NA (1968) Isolation and characterization of the collagen from glomerular basement membrane. Biochemistry 7(9):3103–3112. https://doi.org/10.1021/bi00849a012
doi: 10.1021/bi00849a012
pubmed: 5684337
Lu JY, Mohammed TA, Donohue ST, Al-Ghoul KJ (2008) Distribution of basal membrane complex components in elongating lens fibers. Mol Vis 14:1187–1203
pubmed: 18596883
pmcid: 2442472
Luscher BP, Vachel L, Ohana E, Muallem S (2020) Cl(−) as a bona fide signaling ion. Am J Physiol Cell Physiol 318(1):C125–C136. https://doi.org/10.1152/ajpcell.00354.2019
doi: 10.1152/ajpcell.00354.2019
pubmed: 31693396
Meuwissen ME, Halley DJ, Smit LS, Lequin MH, Cobben JM, de Coo R, van Harssel J, Sallevelt S, Woldringh G, van der Knaap MS, de Vries LS, Mancini GM (2015) The expanding phenotype of COL4A1 and COL4A2 mutations: clinical data on 13 newly identified families and a review of the literature. Genet Med 17(11):843–853. https://doi.org/10.1038/gim.2014.210
doi: 10.1038/gim.2014.210
pubmed: 25719457
Morrissey MA, Sherwood DR (2015) An active role for basement membrane assembly and modification in tissue sculpting. J Cell Sci 128(9):1661–1668. https://doi.org/10.1242/jcs.168021
doi: 10.1242/jcs.168021
pubmed: 25717004
pmcid: 4446735
Pedchenko V, Bauer R, Pokidysheva EN, Al-Shaer A, Forde NR, Fidler AL, Hudson BG, Boudko SP (2019) A chloride ring is an ancient evolutionary innovation mediating the assembly of the collagen IV scaffold of basement membranes. J Biol Chem 294(20):7968–7981. https://doi.org/10.1074/jbc.RA119.007426
doi: 10.1074/jbc.RA119.007426
pubmed: 30923125
pmcid: 6527180
Risteli J, Bachinger HP, Engel J, Furthmayr H, Timpl R (1980) 7-S collagen: characterization of an unusual basement membrane structure. Eur J Biochem 108(1):239–250. https://doi.org/10.1111/j.1432-1033.1980.tb04717.x
doi: 10.1111/j.1432-1033.1980.tb04717.x
pubmed: 6250829
Soder S, Poschl E (2004) The NC1 domain of human collagen IV is necessary to initiate triple helix formation. Biochem Biophys Res Commun 325(1):276–280. https://doi.org/10.1016/j.bbrc.2004.10.034
doi: 10.1016/j.bbrc.2004.10.034
pubmed: 15522229
Spiro RG (1967) Studies on the renal glomerular basement membrane. Preparation and chemical composition. J Biol Chem 242(8):1915–1922
doi: 10.1016/S0021-9258(18)96088-6
Stokman MF, Renkema KY, Giles RH, Schaefer F, Knoers NV, van Eerde AM (2016) The expanding phenotypic spectra of kidney diseases: insights from genetic studies. Nat Rev Nephrol 12(8):472–483. https://doi.org/10.1038/nrneph.2016.87
doi: 10.1038/nrneph.2016.87
pubmed: 27374918
Sundaramoorthy M, Meiyappan M, Todd P, Hudson BG (2002) Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes. J Biol Chem 277(34):31142–31153. https://doi.org/10.1074/jbc.M201740200
doi: 10.1074/jbc.M201740200
pubmed: 11970952
Than ME, Henrich S, Huber R, Ries A, Mann K, Kuhn K, Timpl R, Bourenkov GP, Bartunik HD, Bode W (2002) The 1.9-A crystal structure of the noncollagenous (NC1) domain of human placenta collagen IV shows stabilization via a novel type of covalent Met-Lys cross-link. Proc Natl Acad Sci U S A 99(10):6607–6612. https://doi.org/10.1073/pnas.062183499
doi: 10.1073/pnas.062183499
pubmed: 12011424
pmcid: 124450
Timpl R, Risteli J, Bachinger HP (1979) Identification of a new basement membrane collagen by the aid of a large fragment resistant to bacterial collagenase. FEBS Lett 101(2):265–268. https://doi.org/10.1016/0014-5793(79)81022-4
doi: 10.1016/0014-5793(79)81022-4
pubmed: 87347
Timpl R, Wiedemann H, van Delden V, Furthmayr H, Kuhn K (1981) A network model for the organization of type IV collagen molecules in basement membranes. Eur J Biochem 120(2):203–211. https://doi.org/10.1111/j.1432-1033.1981.tb05690.x
doi: 10.1111/j.1432-1033.1981.tb05690.x
pubmed: 6274634
Vanacore RM, Shanmugasundararaj S, Friedman DB, Bondar O, Hudson BG, Sundaramoorthy M (2004) The alpha1.alpha2 network of collagen IV. Reinforced stabilization of the noncollagenous domain-1 by noncovalent forces and the absence of met-Lys cross-links. J Biol Chem 279(43):44723–44730. https://doi.org/10.1074/jbc.M406344200
doi: 10.1074/jbc.M406344200
pubmed: 15299013
Vanacore R, Ham AJ, Voehler M, Sanders CR, Conrads TP, Veenstra TD, Sharpless KB, Dawson PE, Hudson BG (2009) A sulfilimine bond identified in collagen IV. Science 325(5945):1230–1234. https://doi.org/10.1126/science.1176811
doi: 10.1126/science.1176811
pubmed: 19729652
pmcid: 2876822
Wang X, Li W, Wei K, Xiao R, Wang J, Ma H, Qin L, Shao W, Li C (2018) Missense mutations in COL4A5 or COL4A6 genes may cause cerebrovascular fibromuscular dysplasia: case report and literature review. Medicine (Baltimore) 97(30):e11538. https://doi.org/10.1097/MD.0000000000011538
doi: 10.1097/MD.0000000000011538
Weber S, Engel J, Wiedemann H, Glanville RW, Timpl R (1984) Subunit structure and assembly of the globular domain of basement-membrane collagen type IV. Eur J Biochem 139(2):401–410. https://doi.org/10.1111/j.1432-1033.1984.tb08019.x
doi: 10.1111/j.1432-1033.1984.tb08019.x
pubmed: 6698021