Structural study of cell attachment peptide derived from laminin by molecular dynamics simulation

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Yamada, Hironao ^a   Mori, Sakiko ^a   Miyakawa, Takeshi ^a   Morikawa, Ryota ^a   Katagiri, Fumihiko ^a   Hozumi, Kentaro ^a   Kikkawa, Yamato ^a   Nomizu, Motoyoshi ^a   Takasu, Masako ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTYLPHENYLALANYLALANYLTHREONYLVALYLGLUTAMINYLLEUCYLARGINYLASPARAGINYLGLYCYLPHENYLALANYLPROLYLTYROSYLPHENYLALANYLSERYLTYROSYLASPARTYLLEUCYLGLYCINE; ASPARTYLTYROSYLALANYLTHREONYLLEUCYLGLUTAMINYLLEUCYLGLUTAMINYLGLUTAMYLGLYCYLARGINYLLEUCYLHISTIDYLPHENYLALANYLMETHIONYLPHENYLALANYLASPARTYLLEUCYLGLYCINE; LAMININ; PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; CELL ADHESION; CELL SPREADING; CONTROLLED STUDY; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; PROTEIN STABILITY; PROTEIN STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; PROTEIN CONFORMATION; THERMODYNAMICS;

AMINO ACID SEQUENCE; CELL ADHESION; HYDROGEN BONDING; LAMININ; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN CONFORMATION; THERMODYNAMICS;

EID: 84960484028     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0149474     Document Type: Article

References (57)

1. Collier JH, Segura T. Evolving the use of peptides as components of biomaterials. Biomaterials. 2011; 32: 4198-4204. doi: 10.1016/j.biomaterials.2011.02.030 PMID: 21515167
2. Holmes TC Novel peptide-based biomaterial scaffolds fortissue engineering. Trends Biotechnol. 2002; 20: 16-21. PMID: 11742673
3. Hozumi K, Sasaki A, Yamada Y, Otagiri D, Kobayashi K, Fujimori C, et al. Reconstitution of laminin-111 biological activity using multiple peptide coupled to chitosan scaffolds. Biomaterials. 2012; 33: 4241-4250. doi: 10.1016/j.biomaterials.2012.02.055 PMID: 22436803
4. Sasaki T, Fassler R, Hohenester E. Laminin: the crux of basement membrane assembly. J Cell Biol. 2004; 164: 959-963. PMID: 15037599
5. Colognato H, Yurchenco PD. Form and function: the laminin family of heterotrimers. Dev Dyn. 2000; 218: 213-234. PMID: 10842354
6. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD. Molecular biology of the cell 5thed. Garland Publishing Inc. New York. 2007; pp 1167.
7. Li S, Edgar D, Flassler R, Wadsworth W, Yurchenco PD. The role of laminin in embryonic cell polarization and tissue organization. Dev Cell. 2003; 4: 613-624. PMID: 12737798
8. Miner JH, Yurchenco PD. Laminin functions in tissue morphogenesis. Annu Rev Cell Dev Biol. 2004; 20: 255-284. PMID: 15473841
9. Burgeson RE, Chiquet M, Deutzmann R, Ekblom P, Engel J, Kleinman HK, et al. A new nomenclature forthelaminins. Matrix Biol. 1994; 14: 209-211. PMID: 7921537
10. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, et al. The laminin α chains: expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins8-11, and cloning of a novel α3 isoform. J Cell Biol. 1997; 137: 685-701. PMID: 9151674
11. Iivanainen A, Morita T, Tryggvason K. Molecular cloning and tissue-specific expression of a novel murine laminin γ3 chain. J Biol Chem. 1999; 274: 14107-14111. PMID: 10318827
12. Libby RT, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, Koch M, et al. Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J Neurosci. 2000; 20: 6517-6528. PMID: 10964957
13. Aumailley M, Bruckner-Tuderman L, Cater WG, Deutzmann R, Edgar D, Ekblom P, et al. A simplified laminin nomenclature. Matrix Biol. 2005; 24: 326-332. PMID: 15979864
14. Ramadhani D, Tsukada T, Fujiwara K, Horiguchi K, Kikuchi M, Tashiro T. Laminin isoforms and laminin-producing cells in rat anterior pituitary. Acta Histochem Cytochem. 2012; 45: 309-315. doi: 10.1267/ahc.12028 PMID: 23209340
15. Hallmann R, Horn N, Selg M, Wendler O, Pausch F, Sorokin LM. Expression and function of laminins in the embryonic and mature vasculature. Physiol Rev. 2005; 85: 979-1000. PMID: 15987800
16. Durbeej M. Laminins. Cell Tisssue Res. 2010; 339: 259-268.
17. Yamada KM Adhesive recognition sequences. J Biol Chem. 1991; 266: 12809-12812. PMID: 2071570
18. Yamada Y, Kleinman HK. Functional domains of cell adhesion molecules. Curr Opin Cell Biol. 1992; 4: 819-823. PMID: 1419059
19. Powell SK, Kleinman HK. Neuronal laminins and their cellular receptors. Int J BiochemCell Biol. 1997; 29: 401-414. PMID: 9202420
20. Nomizu M, Kim WH, Yamamura K, Utani A, Song SY, Otaka A, et al. Identification of cell binding sites in the laminin alpha 1 chain carboxyl-terminal globular domain by systematic screening of synthetic peptides. J Biol Chem. 1995; 270: 20583-20590. PMID: 7657636
21. Nomizu M, Kuratomi Y, Song SY, Ponce ML, Hoffman MP, Powell SK, et al. Identification of cell binding sequences in mouse laminin gamma1 chain by systematic peptide screening. J Biol Chem. 1997; 272: 32198-32205. PMID: 9405421
22. Nomizu M, Kuratomi Y, Malinda KM, Song SY, Miyoshi K, Otaka A, et al. Cell binding sequences in mouse laminin alpha1 chain. J Biol Chem. 1998; 273: 32491-32499. PMID: 9829982
23. Nomizu M, Kuratomi Y, Ponce ML, Song SY, Miyoshi K, Otaka A, et al. Cell adhesive sequences in mouse laminin beta1 chain. Arch Biochem Biophys. 2000; 378: 311-320. PMID: 10860548
24. Utani A, Nomizu M, Matsuura H, Kato K, Kobayashi T, Takeda U, et al. A unique sequence of the laminin α3 G domain binds to heparin and promotes cell adhesion through syndecan-2 and -4. J Biol Chem. 2001; 276: 28779-28788. PMID: 11373281
25. Kato K, Utani A, Suzuki N, Mochizuki M, Yamada M, Nishi N, et al. Identification of neurite outgrowth promoting sites on the laminin α3 chain G domain. Biochemistry 2002; 41: 10747-10753. PMID: 12196012
26. Yamaguchi H, Yamashita H, Mori H, Okazaki I, Nomizu M, Beck K, et al. High and low affinity heparinbinding sites in the G domain of the mouse laminin α4 chain. J Biol Chem. 2000; 275: 29458-29465. PMID: 10893232
27. Makino M, Okazaki I, Kasai S, Nishi N, Bougaeva M, Weeks BS, et al. Identification of cell binding sites in the laminin α5-chain G domain. Exp Cell Res. 2002; 277: 95-106. PMID: 12061820
28. Nielsen PK, Gho YS, Hoffman MP, Watanabe H, Makino M, Nomizu M, et al. Identification of a major heparin and cell binding site in the LG4 module of the laminin α5 chain. J Biol Chem. 2000; 275: 14517-14523. PMID: 10799535
29. Okazaki I, Suzuki N, Nishi N, Utani A, Matsuura H, Shinkai H, et al. Identification of biologically active sequences in the laminin α4; chain G domain. J Biol Chem. 2002; 277: 37070-37078. PMID: 12130633
30. Hohenester E, Tisi D, Talts JF, Timple R. The crystal structure of a laminin G-like module reveals the molecular basis of odystroglycan binding to laminins, perlecan, and agrin. Mol Cell. 1999; 4: 783-792. PMID: 10619025
31. Suzuki N, Nakatsuka H, Mochizuki M, Nishi N, Kadoya Y, Utani A, et al. Biological activities of homologous loop regions in the laminin α chain G domains. J Biol Chem. 2003; 278: 45697-45705. PMID: 12933811
32. Harrison D, Hussain SA, Combs AC, Ervasti JM, Yurchenco PD, Hohenester E. Crystal structure and cell surface anchorage sites of laminin alpha1LG4-5. J Biol Chem. 2007; 282: 11573-11581. PMID: 17307732
33. Katagiri F, Hara T, Yamada Y, Hozumi K, Urushibata S, Kikkawa Y, et al. The biological activities of the homologous loop regions in the laminin α chain LG modules. Biochemistry. 2014; 53: 3699-3708. doi: 10.1021/bi5003822 PMID: 24850085
34. Tisi D, Talts J, Timple R, Hohenester E. Structure of the C-terminal laminin G-like domain pair of the laminin α2 chain harbouring binding sites for odystroglycan and heparin. EMBOJ. 2000; 19: 1432-1440. PMID: 10747011
35. Yamada H, Komatsu Y, Miyakawa T, Morikawa R, Katagiri F, Hozumi K, et al. Conformation analysis of loop region peptides in the laminin α; chain LG4 modules by molecular dynamics simulations. Peptide Science 2011, Jap Peptide Soc; 2012: 201-204.
36. Yamada H, Miyakawa T, Morikawa R, Katagiri F, Hozumi K, Kikkawa Y, et al. Molecular dynamics simulations of peptides derived from laminin α2 Chain. Peptide Science 2012, Jap Peptide Soc; 2013: 339-342.
37. Okabe T, Kawata M, Okamoto Y, Mikami M. Replica-exchange Monte Carlo method for the isobaric-isothermal ensemble. Chem Phys Lett. 2001; 335: 435-439.
38. Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P, Apostolov R, et al. GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics. 2013; 29: 845-854. doi: 10.1093/bioinformatics/btt055 PMID: 23407358
39. Lindorff-Larsen K, Piana S, Palmo K, Maragakis P, Klepeis JL, Dorr RO, et al. Improved side-chain torsion potentials for the AMBER ff99SB protein force field. PROTEINS. Struct Funct Gen. 2010; 78: 1950-1958.
40. Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML. Comparison of simple potential functions for simulating liquid water. J Chem Phys. 1983; 79: 926-935.
41. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. LINCS: A linear constraint solver for molecular simulations. J Comp Chem. 1997; 18: 1463-1472.
42. Darden T, York D, Pedersen L. Particle mesh Ewald: An N•log(N) method for Ewald sums in large systems. J Chem Phys. 1993; 98: 10089-10092.
43. Zimmerman K. All purpose molecular mechanics simulator and energy minimizer. J Comp Chem. 1991; 12: 310-319.
44. Zhang W, Wu C, Duan Y. Convergence of replica exchange molecular dyanmics. J. Chem. Phys. 2005; 123: 154105-154113. PMID: 16252940
45. Chodera JD, Swope WC, Pitera JW, Seok C, Dill KA. Use of the Weighted Histogram Analysis Method for the Analysis of Simulated and Parallel Tempering. J. Chem. Theory Comput. 2007; 3: 26-41. doi: 10.1021/ct0502864 PMID: 26627148
46. Kabsch W, Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogenbonded and geometrical features. Biopolymers. 1983; 22: 2577-2637. PMID: 6667333
47. Altis A, Otten M, Nguyen PH, Hegger R, Stock G. Construction of the free energy landscape of biomolecules via dihedral angle principal component analysis. J Chem Phys. 2008; 128: 245102-245111. doi: 10.1063/1.2945165 PMID: 18601386
48. Eisenhaber F, Lijnzaad P, Argos P, Sander C, Scharf M. The double cubic lattice method: Efficient approaches to numerical integration of surface area and volume and to dot surface contouring of molecular assemblies. J Comput Chem. 1995; 16: 273-284.
49. Umezawa K, Ikebe J, Nomizu M, Nakamura H, Higo J. Conformational requirement on peptides to exert laminin's activities and search for protein segments with laminin's activities. Biopolymers. 2009; 92: 124-131. doi: 10.1002/bip.21148 PMID: 19180521
50. Yamada H, Fukuda M, Miyakawa T, Morikawa R, Takasu M. Conformation analysis of peptides derived from laminin a1-2 chain using molecular dynamics simulation. JPSConf Proc. 2014; 1: 016016.
51. Hatfield MPD, Murphy RF, Lovas S. Molecular dynamics analysis of the conformations of a β-hairpin miniprotein. J Phys Chem B. 2010; 114: 3028-3037. doi: 10.1021/jp910465e PMID: 20148510
52. Csontos J, Murphy RF, Lovas S. The role of weakly polar and H-bonding interactions in the stabilization of theconformers of FGG, WGG, and YGG: an aqueous phase computational study. Biopolymers. 2008; 89: 1002-1011. doi: 10.1002/bip.21049 PMID: 18615659
53. Pande VS, Roshkar DS. Molecular dynamics simulations of unfolding and refolding of a β-hairpin fragment of protein G. Proc Natl Acad Sci USA. 1999; 96: 9062-9067. PMID: 10430895
54. Garcia AE, Sanbonmatsu KY. Exploring the energy landscape of a β-hairpin in explicit solvent. Proteins. 2001; 42: 345-354. PMID: 11151006
55. Zhou R, Berne BJ, Germain R. The free energy landscape for β-hairpin folding in explicit water. Proc Natl Acad Sci USA. 2001; 98: 14931-14936. PMID: 11752441
56. Zhou R. Exploring the protein folding free energy landscape: coupling replica exchange method with P3ME/RESPA algorithm. J Mol Graph Model. 2004; 22: 451-463. PMID: 15099840
57. Singh G, Brovchenko I, Oleinikova A, Winter R. Aggregation of fragments of the islet amyloid polypeptide as a phase transition: a cluster analysis. NIC series. 2007; 36: 275-278.