Enzymatically crosslinked collagen-mimetic dendrimers that promote integrin-targeted cell adhesion

Biomaterials

Volumn 29, Issue 20, 2008, Pages 3034-3045

  Khew, Shih Tak ^a   Yang, Qing Jun ^a   Tong, Yen Wah ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Biomimetic material; Cell adhesion; Collagen; Dendrimer; Enzymatic crosslinking; Hepatocyte

Indexed keywords

BIOMIMETIC MATERIALS; CELL ADHESION; COLLAGEN; CROSSLINKING; ENZYME ACTIVITY; TISSUE CULTURE;

DONOR SUBSTRATES; ENZYMATIC CROSSLINKING; HEPATOCYTE; TISSUE TRANSGLUTAMINASE;

DENDRIMERS;

BIOMIMETIC MATERIAL; COLLAGEN; DENDRIMER; FIBRILLIN 1; INTEGRIN; POLYAMIDOAMINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE ANTIBODY;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL ADHESION; CONFORMATIONAL TRANSITION; CONJUGATION; CONTROLLED STUDY; CROSS LINKING; HUMAN; HUMAN CELL; LIVER CELL; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; CELL ADHESION; COLLAGEN; DENDRIMERS; HUMANS; INTEGRINS; MICROFILAMENT PROTEINS; MOLECULAR MIMICRY;

EID: 42749083406     PISSN: 01429612     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2008.03.023     Document Type: Article

References (72)

1. Majoros I.J., Thomas T.P., Mehta C.B., and Baker Jr. J.R. Poly(amidoamine) dendrimer-based multifunctional engineered nanodevice for cancer therapy. J Med Chem 48 (2005) 5892-5899
2. Gilmartin B.P., McLaughlin R.L., and Williams M.E. Artificial tripeptide scaffolds for self-assembly of heteromultimetallic structures with tunable electronic and magnetic properties. Chem Mater 17 (2005) 5446-5454
3. Higashi N., Koga T., and Niwa M. Dendrimers with attached helical peptides. Adv Mater 12 (2000) 1373-1375
4. Kinberger G.A., Cai W., and Goodman M. Collagen mimetic dendrimers. J Am Chem Soc 124 (2002) 15162-15163
5. Kinberger G.A., Taulane J.P., and Goodman M. The design, synthesis, and characterization of a PAMAM-based triple helical collagen mimetic dendrimer. Tetrahedron 62 (2006) 5280-5286
6. 1-binding site containing an essential GER sequence. J Biol Chem 273 (1998) 33287-33294
7. 1 recognize the same specific amino acid sequence, GFOGER, in native (triple-helical) collagens. J Biol Chem 275 (2000) 35-40
8. Chelberg M.K., McCarthy J.B., Skubitz A.P.N., Furcht L.T., and Tsilibary E.C. Characterization of a synthetic peptide from type IV collagen that promotes melanoma cell adhesion, spreading, and motility. J Cell Biol 111 (1990) 261-270
9. 1(IV) 531-543. J Biol Chem 269 (1994) 30939-30945
10. 1 integrin in collagen. J Biol Chem 266 (1991) 7363-7367
11. 1 integrins. J Cell Biol 113 (1991) 1475-1483
12. Khew S.T., and Tong Y.W. Template-assembled triple-helical peptide molecules: mimicry of collagen by molecular architecture and integrin-specific cell adhesion. Biochemistry 47 (2008) 585-596
13. Khew S.T., and Tong Y.W. The specific recognition of a cell binding sequence derived from type I collagen by Hep3B and L929 cells. Biomacromolecules 8 (2007) 3153-3161
14. Khew S.T., Zhu X.H., and Tong Y.W. An integrin-specific collagen-mimetic peptide approach for optimizing Hep3B liver cell adhesion, proliferation, and cellular functions. Tissue Eng 13 (2007) 2451-2463
15. Engler A.J., Sen S., Sweeney H.L., and Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 126 (2006) 677-689
16. Greenberg C., Birckbichler P., and Rice R. Transglutaminases: multifunctional cross-linking enzymes that stabilize tissues. FASEB J 5 (1991) 3071-3077
17. Lorand L., and Graham R.M. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 4 (2003) 140-156
18. Aeschlimann D., Wetterwald A., Fleisch H., and Paulsson M. Expression of tissue transglutaminase in skeletal tissues correlates with events of terminal differentiation of chondrocytes. J Cell Biol 120 (1993) 1461-1470
19. Nakaoka H., Perez D.M., Baek K.J., Das T., Husain A., Misono K., et al. Gh: a GTP-binding protein with transglutaminase activity and receptor signaling function. Science 264 (1994) 1593-1596
20. Fesus L., Thomazy V., and Falus A. Induction and activation of tissue transglutaminase during programmed cell death. FEBS Lett 224 (1987) 104-108
21. Schittny J.C., Paulsson M., Vallan C., Burri P.H., Kedei N., and Aeschlimann D. Protein cross-linking mediated by tissue transglutaminase correlates with the maturation of extracellular matrices during lung development. Am J Respir Cell Mol Biol 17 (1997) 334-343
22. Griffin M., Casadio R., and Bergamini C.M. Transglutaminases: nature's biological glues. Biochem J 368 (2002) 377-396
23. Feng Y., Melacini G., Taulane J.P., and Goodman M. Collagen-based structures containing the peptoid residue Nleu - synthesis and biophysical studies of Gly-Pro-Nleu sequences by CD, UV absorbance and optical rotation. Biopolymers 39 (1996) 859-872
24. Kajiyama K., Tomiyama T., Uchiyama S., and Kobayashi Y. Phase transitions of sequenced polytripeptides observed by microcalorimetry. Chem Phys Lett 247 (1995) 299-303
25. Hohenadl C., Mann K., Mayer U., Timpl R., Paulsson M., and Aeschlimann D. Two adjacent N-terminal glutamines of BM-40 (osteonectin, SPARC) act as amine acceptor sites in transglutaminase-catalyzed modification. J Biol Chem 270 (1995) 23415-23420
26. 726 in nidogen as the amine acceptor in transglutaminase-catalyzed cross-linking of laminin-nidogen complexes. J Biol Chem 267 (1992) 11316-11321
27. Coussons P.J., Price N.C., Kelly S.M., Smith B., and Sawyer L. Factors that govern the specificity of transglutaminase-catalysed modification of proteins and peptides. Biochem J 282 (1992) 929-930
28. Groenen P.J., Grootjans J.J., Lubsen N.H., Bloemendal H., and de Jong W.W. Lys-17 is the amine-donor substrate site for transglutaminase in βA3-crystallin. J Biol Chem 269 (1994) 831-833
29. Porta R., Esposito C., Metafora S., Malorni A., Pucci P., Siciliano R., et al. Mass spectrometric identification of the amino donor and acceptor sites in a transglutaminase protein substrate secreted from rat seminal vesicles. Biochemistry 30 (1991) 3114-3120
30. Pucci P., Malorni A., Marino G., Metafora S., Esposito C., and Porta R. β-Endorphin modification by transglutaminase in vitro: identification by FAB/MS of glutamine-11 and lysine-29 as acyl donor and acceptor sites. Biochem Biophys Res Commun 154 (1988) 735-740
31. Ikura K., Takahata K., and Sasaki R. Cross-linking of a synthetic partial-length (1-28) peptide of the Alzheimer β/A4 amyloid protein by transglutaminase. FEBS Lett 326 (1993) 109-111
32. Merck K.B., Groenen P.J.T.A., Voorter C.E.M., de Haard-Hoekman W.A., Horwitz J., Bloemendal H., et al. Structural and functional similarities of bovine α-crystallin and mouse small heat-shock protein. A family of chaperones. J Biol Chem 268 (1993) 1046-1052
33. Mariniello L., Esposito C., Pierro P.D., Cozzolino A., Pucci P., and Porta R. Human-immunodeficiency-virus transmembrane glycoprotein gp41 is an amino acceptor and donor substrate for transglutaminase in vitro. Eur J Biochem 215 (1993) 99-104
34. Groenen P.J.T.A., Bloemendal H., and de Jong W.W. The carboxy-terminal lysine of αβ-crystallin is an amine-donor substrate for tissue transglutaminase. Eur J Biochem 205 (1992) 671-674
35. Lorand L., Valasco P.T., Murthy S.N.P., Wilson J., and Parameswaran K.N. Isolation of transglutaminase-reactive sequences from complex biological systems: a prominent lysine donor sequence in bovine lens. Proc Natl Acad Sci USA 89 (1992) 11161-11163
36. Mulders J.W.M., Hoekman W.A., Bloemendal H., and de Jong W.W. βB1 crystallin is an amine-donor substrate for tissue transglutaminase. Exp Cell Res 171 (1987) 296-305
37. Qian R., and Glanville R. Alignment of fibrillin molecules in elastic microfibrils is defined by transglutaminase-derived cross-links. Biochemistry 36 (1997) 15841-15847
38. Cain S.A., Morgan A., Sherratt M.J., Ball S.G., Shuttleworth C.A., and Kielty C.M. Proteomic analysis of fibrillin-rich microfibrils. Proteomics 6 (2006) 111-122
39. Rock M.J., Cain S.A., Freeman L.J., Morgan A., Mellody K., Marson A., et al. Molecular basis of elastic fiber formation: critical interactions and a tropoelastin fibrillin-1 cross-link. J Biol Chem 279 (2004) 23748-23758
40. Clarke A.W., Wise S.G., Cain S.A., Kielty C.M., and Weiss A.S. Coacervation is promoted by molecular interactions between the PF2 segment of fibrillin-1 and the domain 4 region of tropoelastin. Biochemistry 44 (2005) 10271-10281
41. Ritty T.M., Broekelmann T.J., Werneck C.C., and Mecham R.P. Fibrillin-1 and -2 contain heparin-binding sites important for matrix deposition and that support cell attachment. Biochem J 375 (2003) 425-432
42. Raghunath M., Putnam E.A., Ritty T., Hamstra D., Park E.S., Tschodrich-Rotter M., et al. Carboxy-terminal conversion of profibrillin to fibrillin at a basic site by PACE/furin-like activity required for incorporation in the matrix. J Cell Sci 112 (1999) 1093-1100
43. Jeitner T.M., Fuchsbauer H.-L., Blass J.P., and Cooper A.J.L. A sensitive fluorometric assay for tissue transglutaminase. Anal Biochem 292 (2001) 198-206
44. Zhang Z.Y., Shum P., Yates M., Messersmith P.B., and Thompson D.H. Formation of fibrinogen-based hydrogels using phototriggerable diplasmalogen liposomes. Bioconjugate Chem 13 (2002) 640-646
45. Brown F.R., Corato A.D., Lorenzi G.P., and Blout E.R. Synthesis and structural studies of two collagen analogues poly(-prolyl-seryl-glycyl) and poly(-prolyl-alanyl-glycyl). J Mol Biol 63 (1972) 85-99
46. 10, a synthetic polypeptide model of collagen. J Mol Biol 65 (1972) 371-372
47. Feng Y., Melacini G., Taulane J.P., and Goodman M. Acetyl-terminated and template-assembled collagen-based polypeptides composed of Gly-Pro-Hyp sequences. 2. Synthesis and conformational analysis by CD, UV absorbance and optical rotation. J Am Chem Soc 118 (1996) 10351-10358
48. Kwak J., Capua A.D., Locardi E., and Goodman M. TREN (Tris(2-aminoethyl)amine) - an effective scaffold for the assembly of triple helical collagen mimetic structures. J Am Chem Soc 124 (2002) 14085-14091
49. Jefferson E.A., Locardi E., and Goodman M. Incorporation of achiral peptoid-based trimeric sequences into collagen mimetics. J Am Chem Soc 120 (1998) 7420-7428
50. Bella J., Brodsky B., and Berman H.M. Hydration structure of a collagen peptide. Structure 3 (1995) 893-906
51. Bella J., Eaton M., Brodsky B., and Berman H.M. Crystal and molecular structure of a collagen-like peptide at 1.9 Å resolution. Science 266 (1994) 75-81
52. Feng Y., Melacini G., and Goodman M. Collagen-based structures containing the peptoid residue N-isobutylglycine (Nleu) - synthesis and biophysial studies of Gly-Nleu-Pro sequences by CD and optical rotation. Biochemistry 36 (1997) 8716-8724
53. Fesus L., Metsis M.L., Muszbek L., and Koteliansky V.E. Transglutaminase-sensitive glutamine residues of human plasma fibronectin revealed by studying its proteolytic fragments. Eur J Biochem 154 (1986) 371-374
54. Kleman J.P., Aeschlimann D., Paulsson M., and van de Rest M. Transglutaminase-catalyzed cross-linking of fibrils of collagen V/XI in A204 rhabdomyosarcoma cells. Biochemistry 34 (1995) 13768-13775
55. Bowness J., Folk J., and Timpl R. Identification of a substrate site for liver transglutaminase on the aminopropeptide of type III collagen. J Biol Chem 262 (1987) 1022-1024
56. Jelenska M.M., Fesus L., and Kopec M. The comparative ability of plasma and tissue transglutaminases to use collagen as a substrate. Biochim Biophys Acta 616 (1980) 167-178
57. Mosher D., Schad P., and Vann J. Cross-linking of collagen and fibronectin by factor XIIIa. Localization of participating glutaminyl residues to a tryptic fragment of fibronectin. J Biol Chem 255 (1980) 1181-1188
58. Mosher D.F., and Schad P.E. Cross-linking of fibronectin to collagen by blood coagulation factor XIIIa. J Clin Invest 64 (1979) 781-787
59. Koide T. Triple helical collagen-like peptides: engineering and applications in matrix biology. Connect Tissue Res 46 (2005) 131-141
60. Goodman M., Bhumralkar M., Jefferson E.A., Kwak J., and Locardi E. Collagen mimetics. Peptide Sci 47 (1998) 127-142
61. 1 integrins in adhesion and invasion of hepatocellular carcinoma cells. Hepatology 29 (1999) 68-74
62. Johnson G., Jenkins M., McLean K.M., Griesser H.J., Kwak J., Goodman M., et al. Peptoid-containing collagen mimetics with cell binding activity. J Biomed Mater Res 51 (2000) 612-624
63. Massia S., and Hubbell J. An RGD spacing of 440 nm is sufficient for integrin alpha v beta 3-mediated fibroblast spreading and 140 nm for focal contact and stress fiber formation. J Cell Biol 114 (1991) 1089-1100
64. 1 integrin recognizes the GFOGER sequence in interstitial collagens. J Biol Chem 278 (2003) 7270-7277
65. 1. J Biol Chem 275 (2000) 38981-38989
66. Siljander P.R.M., Hamaia S., Peachey A.R., Slatter D.A., Smethurst P.A., Ouwehand W.H., et al. Integrin activation state determines selectivity for novel recognition sites in fibrillar collagens. J Biol Chem 279 (2004) 47763-47772
67. Wozniak M.A., Modzelewska K., Kwong L., and Keely P.J. Focal adhesion regulation of cell behavior. Biochim Biophys Acta 1692 (2004) 103-119
68. Burridge K., Chrzanowska-Wodnicka M., and Zhong C. Focal adhesion assembly. Trends Cell Biol 7 (1997) 342-347
69. Bačáková L., Mareš V., Bottone M.G., Pellicciari C., Lisá V., and Švorčík V. Fluorine-ion-implanted polystyrene improves growth and viability of vascular smooth muscle cells in culture. J Biomed Mater Res 49 (2000) 369-379
70. Bačáková L., Walachová K., Švorčík V., and Hnatowicz V. Molecular mechanisms of improved adhesion and growth of an endothelial cell line cultured on polystyrene implanted with fluorine ions. Biomaterials 21 (2000) 1173-1179
71. Hynes R.O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69 (1992) 11-25
72. Fields C.G., Mickelson D.J., Drake S.L., McCarthy J.B., and Fields G.B. Melanoma cell adhesion and spreading activities of a synthetic 124-residue triple-helical "mini-collagen". J Biol Chem 268 (1993) 14153-14160