Structural elucidation of full-length nidogen and the laminin-nidogen complex in solution

Matrix Biology

Volumn 33, Issue , 2014, Pages 60-67

  Patel, Trushar R ^a   Bernards, Claudia ^b   Meier, Markus ^a   McEleney, Kevin ^a   Winzor, Donald J ^c   Koch, Manuel ^b   Stetefeld, Jörg ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Dynamic light scattering; Extracellular matrix proteins; Hydrodynamics; Laminin; Nidogen 1; Small angle X ray scattering

Indexed keywords

DYNAMIC LIGHT SCATTERING; EXTRACELLULAR MATRIX PROTEINS; HYDRODYNAMICS; LAMININ; NIDOGEN-1; SMALL ANGLE X-RAY SCATTERING;

ANIMALS; LAMININ; MEMBRANE GLYCOPROTEINS; MICE; MODELS, MOLECULAR; PARTICLE SIZE; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; SCATTERING, SMALL ANGLE; SOLUTIONS; X-RAY DIFFRACTION;

EID: 84894273331     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.07.009     Document Type: Article

References (53)

1. Ackley B.D., Kang S.H., Crew J.R., Suh C., Jin Y., Kramer J.M. The basement membrane components nidogen and type XVIII collagen regulate organization of neuromuscular junctions in Caenorhabditis elegans. J. Neurosci. 2003, 23:3577-3587.
2. Alstadt S.P., Hebda P.A., Chung A.E., Eaglstein W.H. Effect of basement membrane entactin on epidermal cell attachment and growth. J. Invest. Dermatol. 1987, 88:55-59.
3. Bader B.L., Smyth N., Nedbal S., Miosge N., Baranowsky A., Mokkapati S., Murshed M., Nischt R. Compound genetic ablation of nidogen 1 and 2 causes basement membrane defects and perinatal lethality in mice. Mol. Cell. Biol. 2005, 25:6846-6856.
4. Baumgartner R., Czisch M., Mayer U., Poschl E., Huber R., Timpl R., Holak T.A. Structure of the nidogen binding LE module of the laminin gamma1 chain in solution. J. Mol. Biol. 1996, 257:658-668.
5. Beck K., Hunter I., Engel J. Structure and function of laminin: anatomy of a multidomain glycoprotein. FASEB J. 1990, 4:148-160.
6. Bonnet F., Vivars D., Robert C., Colloc'h N. Interactions in solution and crystallization of Aspergillus flavus urate oxidase. J. Cryst. Growth 2001, 232:330-339.
7. Bose K., Nischt R., Page A., Bader B.L., Paulsson M., Smyth N. Loss of nidogen-1 and -2 results in syndactyly and changes in limb development. J. Biol. Chem. 2006, 281:39620-39629.
8. Carafoli F., Hussain S.A., Hohenester E. Crystal structures of the network-forming short-arm tips of the laminin beta1 and gamma1 chains. PLoS One 2012, 7:e42473.
9. Chung A.E., Durkin M.E. Entactin: structure and function. Am. J. Respir. Cell Mol. Biol. 1990, 3:275-282.
10. Colognato H., Yurchenco P.D. Form and function: the laminin family of heterotrimers. Dev. Dyn. 2000, 218:213-234.
11. Dedhar S., Jewell K., Rojiani M., Gray V. The receptor for the basement membrane glycoprotein entactin is the integrin alpha 3/beta 1. J. Biol. Chem. 1992, 267:18908-18914.
12. Dong L.J., Hsieh J.C., Chung A.E. Two distinct cell attachment sites in entactin are revealed by amino acid substitutions and deletion of the RGD sequence in the cysteine-rich epidermal growth factor repeat 2. J. Biol. Chem. 1995, 270:15838-15843.
13. Fox J.W., Mayer U., Nischt R., Aumailley M., Reinhardt D., Wiedemann H., Mann K., Timpl R., Krieg T., Engel J., et al. Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J. 1991, 10:3137-3146.
14. Franke D., Svergun D.I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 2009, 42:342-346.
15. Fujiwara S., Shinkai H., Mann K., Timpl R. Structure and localization of O- and N-linked oligosaccharide chains on basement membrane protein nidogen. Matrix 1993, 13:215-222.
16. García de la Torre J., Huertas M.L., Carrasco B. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 2000, 78:719-730.
17. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., Bairoch A. Protein identification and analysis tools on the ExPASy server. The Proteomics Protocols Handbook 2005, 571-607. Humana Press. J.M. Walker (Ed.).
18. Gerl M., Mann K., Aumailley M., Timpl R. Localization of a major nidogen-binding site to domain III of laminin B2 chain. Eur. J. Biochem. 1991, 202:167-174.
19. Ho M.S., Bose K., Mokkapati S., Nischt R., Smyth N. Nidogens - extracellular matrix linker molecules. Microsc. Res. Tech. 2008, 71:387-395.
20. Hsieh J.C., Wu C., Chung A.E. The binding of fibronectin to entactin is mediated through the 29kDa amino terminal fragment of fibronectin and the G2 domain of entactin. Biochem. Biophys. Res. Commun. 1994, 199:1509-1517.
21. Kohfeldt E., Sasaki T., Gohring W., Timpl R. Nidogen-2: a new basement membrane protein with diverse binding properties. J. Mol. Biol. 1998, 282:99-109.
22. Konarev P.V., Volkov V.V., Sokolova A.V., Koch M.H.J., Svergun D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 2003, 36:1277-1282.
23. Kvansakul M., Hopf M., Ries A., Timpl R., Hohenester E. Structural basis for the high-affinity interaction of nidogen-1 with immunoglobulin-like domain 3 of perlecan. EMBO J. 2001, 20:5342-5346.
24. Laue T.M., Shah B.D., Ridgeway T.M., Pelletier S.L. Computer-aided interpretation of analytical sedimentation data for proteins. Analytical Ultracentrifugation in Biochemistry and Polymer Science 1992, 90-125. Royal Society of Chemistry, Cambridge, United Kingdom. S.E. Harding, A.J. Rowe, J.C. Horton (Eds.).
25. Malmon A.G. Small-angle X-ray scattering functions for ellipsoids of revolution and right circular cylinders. Acta Crystallogr. 1957, 10:639-642.
26. Mayer U., Nischt R., Poschl E., Mann K., Fukuda K., Gerl M., Yamada Y., Timpl R. A single EGF-like motif of laminin is responsible for high affinity nidogen binding. EMBO J. 1993, 12:1879-1885.
27. Mercurio A.M., Rabinovitz I. Towards a mechanistic understanding of tumor invasion - Lessons from the oe±6oe≤4 integrin. Semin. Cancer Biol. 2001, 11:129-141.
28. Mokkapati S., Fleger-Weckmann A., Bechtel M., Koch M., Breitkreutz D., Mayer U., Smyth N., Nischt R. Basement membrane deposition of nidogen 1 but not nidogen 2 requires the nidogen binding module of the laminin gamma1 chain. J. Biol. Chem. 2011, 286:1911-1918.
29. Murshed M., Smyth N., Miosge N., Karolat J., Krieg T., Paulsson M., Nischt R. The absence of nidogen 1 does not affect murine basement membrane formation. Mol. Cell. Biol. 2000, 20:7007-7012.
30. Nischt R., Schmidt C., Mirancea N., Baranowsky A., Mokkapati S., Smyth N., Woenne E.C., Stark H.J., Boukamp P., Breitkreutz D. Lack of nidogen-1 and -2 prevents basement membrane assembly in skin-organotypic coculture. J. Invest. Dermatol. 2007, 127:545-554.
31. Patel T.R., Morris G.A., Zwolanek D., Koch M., Harding S.E., Stetefeld J. Nano-structure of the laminin gamma-1 short arm reveals an extended and curved multidomain assembly. Matrix Biol. 2010, 29:565-572.
32. Patel T.R., Besong T.M.D., Patel N., Meier M., Harding S.E., Winzor D.J., Stetefeld J. Evidence for self-association of a miniaturized version of agrin from hydrodynamic and small-angle X-ray scattering measurements. J. Phys. Chem. B 2011, 115:11286-11293.
33. Patel T.R., Reuten R., Xiong S., Meier M., Winzor D.J., Koch M., Stetefeld J. Determination of a molecular shape for netrin-4 from hydrodynamic and small angle X-ray scattering measurements. Matrix Biol. 2012, 31:135-140.
34. Paulsson M., Deutzmann R., Dziadek M., Nowack H., Timpl R., Weber S., Engel J. Purification and structural characterization of intact and fragmented nidogen obtained from a tumor basement membrane. Eur. J. Biochem. 1986, 156:467-478.
35. Paulsson M., Aumailley M., Deutzmann R., Timpl R., Beck K., Engel J. Laminin-nidogen complex. Extraction with chelating agents and structural characterization. Eur. J. Biochem. 1987, 166:11-19.
36. Poschl E., Fox J.W., Block D., Mayer U., Timpl R. Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif of the laminin gamma 1 chain. EMBO J. 1994, 13:3741-3747.
37. Pujuguet P., Simian M., Liaw J., Timpl R., Werb Z., Bissell M.J. Nidogen-1 regulates laminin-1-dependent mammary-specific gene expression. J. Cell Sci. 2000, 113:849-858.
38. Reinhardt D., Mann K., Nischt R., Fox J.W., Chu M.L., Krieg T., Timpl R. Mapping of nidogen binding sites for collagen type IV, heparan sulfate proteoglycan, and zinc. J. Biol. Chem. 1993, 268:10881-10887.
39. Sasaki T., Gohring W., Pan T.C., Chu M.L., Timpl R. Binding of mouse and human fibulin-2 to extracellular matrix ligands. J. Mol. Biol. 1995, 254:892-899.
40. Sasaki T., Kostka G., Gohring W., Wiedemann H., Mann K., Chu M.L., Timpl R. Structural characterization of two variants of fibulin-1 that differ in nidogen affinity. J. Mol. Biol. 1995, 245:241-250.
41. Schuck P. Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and lamm equation modeling. Biophys. J. 2000, 78:1606-1619.
42. Schymeinsky J., Nedbal S., Miosge N., Poschl E., Rao C., Beier D.R., Skarnes W.C., Timpl R., Bader B.L. Gene structure and functional analysis of the mouse nidogen-2 gene: nidogen-2 is not essential for basement membrane formation in mice. Mol. Cell. Biol. 2002, 22:6820-6830.
43. Scott D.J., Patel T.R., Besong D.M.T., Stetefeld J., Winzor D.J. Examination of the discrepancy between size estimates for ovalbumin from small-angle x-ray scattering and other physicochemical measurements. J. Phys. Chem. B 2011, 115:10725-10729.
44. Stetefeld J., Mayer U., Timpl R., Huber R. Crystal structure of three consecutive laminin-type epidermal growth factor-like (LE) modules of laminin [gamma]1 chain harboring the nidogen binding site. J. Mol. Biol. 1996, 257:644-657.
45. Svergun D. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 1992, 25:495-503.
46. Svergun D.I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 1999, 76:2879-2886.
47. Svergun D.I., Nierhaus K.H. A map of protein-rRNA distribution in the 70S Escherichia coli ribosome. J. Biol. Chem. 2000, 275:14432-14439.
48. Takagi J., Yang Y., Liu J.-h., Wang J.-h., Springer T.A. Complex between nidogen and laminin fragments reveals a paradigmatic [beta]-propeller interface. Nature 2003, 424:969-974.
49. Tsao T., Hsieh J.C., Durkin M.E., Wu C.Y., Chakravarti S., Dong L.J., Lewis M., Chung A.E. Characterization of the basement membrane glycoprotein entactin synthesized in a baculovirus expression system. J. Biol. Chem. 1990, 265:5188-5191.
50. Tzu J., Marinkovich M.P. Bridging structure with function: structural, regulatory, and developmental role of laminins. Int. J. Biochem. Cell Biol. 2008, 40:199-214.
51. Ulazzi L., Sabbioni S., Miotto E., Veronese A., Angusti A., Gafa R., Manfredini S., Farinati F., Sasaki T., Lanza G., Negrini M. Nidogen 1 and 2 gene promoters are aberrantly methylated in human gastrointestinal cancer. Mol. Cancer 2007, 6:17.
52. Volkov V.V., Svergun D.I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 2003, 36:860-864.
53. Yurchenco P.D., Schittny J.C. Molecular architecture of basement membranes. FASEB J. 1990, 4:1577-1590.