Review collagen-based biomaterials for wound healing

Sayani Chattopadhyay, Ronald T Raines, Sayani Chattopadhyay, Ronald T Raines

Abstract

With its wide distribution in soft and hard connective tissues, collagen is the most abundant of animal proteins. In vitro, natural collagen can be formed into highly organized, three-dimensional scaffolds that are intrinsically biocompatible, biodegradable, nontoxic upon exogenous application, and endowed with high tensile strength. These attributes make collagen the material of choice for wound healing and tissue engineering applications. In this article, we review the structure and molecular interactions of collagen in vivo; the recent use of natural collagen in sponges, injectables, films and membranes, dressings, and skin grafts; and the on-going development of synthetic collagen mimetic peptides as pylons to anchor cytoactive agents in wound beds.

Keywords: biocompatible; biodegradable; catgut; extracellular matrix; regenerative medicine.

© 2014 Wiley Periodicals, Inc.

Figures

Figure 1
Figure 1
Sir Joseph Lister (English) and Sir William Macewen (Scottish), pioneers in the use of exogenous collagen in medicine.,, The image of Lister is from an oil painting by Walter William Ouless (courtesy of the Wellcome Library, London); the image of Macewen is from an oil painting by Charles R. Dowell (courtesy of the Royal College of Physicians and Surgeons of Glasgow). The catgut in oil was prepared by Lister in 1875 (courtesy of King's College London).
Figure 2
Figure 2
Structure of triple-helical collagen. Hydrogen bonds, blue dashed lines; n→π* interactions, red dashed lines. Panel A is a cross-section from PDB entry 1v4f.
Figure 3
Figure 3
Biosynthetic route to collagen fibers. Size and complexity increase upon post-translational modification and self-assembly. The oxidation of lysine side chains leads to the spontaneous formation of hydroxylysyl pyridinoline and lysyl pyridinoline cross-links.
Figure 4
Figure 4
Pyrrolidine ring puckers preferred in the Xaa and Yaa positions of collagen strands, and natural and non-natural derivatives of proline with those preferences. The pyrrolidine rings actually prefer a twist rather than envelope conformation. As Cγ typically experiences the largest out-of-plane displacement in these twisted rings, we refer to pyrrolidine ring conformations simply as “Cγ-exo” and “Cγ-endo”.
Figure 5
Figure 5
Strategy for anchoring molecules in a wound bed. A natural strand (yellow) in weak or damaged collagen is displaced by a synthetic collagen mimetic peptide (CMP; red) that forms a hyperstable triple helix. A pendant dye enables wound assessment; a pendant growth factor expedites wound healing.

References

    1. Gibson T. Br J Surg. 1990;77:824–825.
    1. Macewen W. Br Med J. 1881;1:150–151.
    1. Lister J. Br Med J. 1881;1:183–185.
    1. Stenzel KH, Miyata T, Rubin AL. Annu Rev Biochem. 1974:231–253.
    1. Shoulders MD, Raines RT. Annu Rev Biochem. 2009;78:929–958.
    1. Parenteau-Bareil R, Gauvin R, Berthod F. Materials. 2010;3:1863–1887.
    1. Yu SM, Li Y, Kim D. Soft Matter. 2011;7:7927–7938.
    1. Aszódi A, Legate KR, Nakchbandi I, Fässler R. Annu Rev Cell Dev Biol. 2006;22:591–621.
    1. Fonseca JM, Alsina AM, Francesca R. Biochim Biophys Acta Biomembr. 1996;1279:259–265.
    1. Maeda M, Tani S, Sano A, Fujioka K. J Control Release. 1999;62:313–324.
    1. Söderhäll C, Marenholz I, Kerscher T, Rüschendorf F, Esparza-Gordillo J, Worm M, Gruber C, Mayr G, Albrecht M, Rohde K, Schulz H, Wahn U, Hubner N, Lee YA. PLoS Biol. 2007;5:1952–1961.
    1. Okuyama K, Hongo C, Fukushima R, Wu G, Narita H, Noguchi K, Tanaka Y, Nishino N. Biopolymers. 2004;76:367–377.
    1. Fischer E. Z Physiol Chem. 1901;33:151–176.
    1. Fischer E. Ber. 1902;35:2660–2665.
    1. Ramshaw JAM, Shah NK, Brodsky B. J Struct Biol. 1998;122:86–91.
    1. Timpl R. In: Extracellular Matrix Biochemistry. Piez KA, Reddi AH, editors. Elsevier; New York: 1984. pp. 159–190.
    1. Asara JM, Schweitzer MH, Freimark LM, Phillips M, Cantley LC. Science. 2007;316:280–285.
    1. Schweitzer MH, Zheng W, Organ CL, Avci R, Suo Z, Freimark LM, Lebleu VS, Duncan MB, Vander Heiden MG, Neveu JM, Lane WS, Cottrell JS, Horner JR, Cantley LC, Kalluri R, Asara JM. Science. 2009;324:626–631.
    1. Badylak SF. Transplant Immunol. 2004;12:367–377.
    1. Koide T. Phil Trans R Soc B: Biol Sci. 2007;362:1281–1291.
    1. Olsen D, Yang C, Bodo M, Chang R, Leigh S, Baez J, Carmichael D, Perälä M, Hämäläinen ER, Jarvinen M, Polarek J. Adv Drug Deliv Rev. 2003;55:1547–1567.
    1. Buechter DD, Paolella DN, Lelie BS, Brown MS, Mehos KA, Gruskin EA. J Biol Chem. 2003;278:645–650.
    1. Pinkas DM, Ding S, Raines RT, Barron AE. ACS Chem Biol. 2011;6:320–324.
    1. Orgel JP, San Antonio JD, Antipova O. Connect Tissue Res. 2011;52:2–17.
    1. Smethurst PA, Onley DJ, Jarvis GE, O'Connor MN, Knight CG, Herr AB, Ouwehand WH, Farndale RW. J Biol Chem. 2007;282:1296–1304.
    1. Fiedler LR, Schönherr E, Waddington R, Niland S, Seidler DG, Aeschlimann D, Eble JA. J Biol Chem. 2008;283:17406–17415.
    1. Fields GB. J Theor Biol. 1991;153:585–602.
    1. Aimes RT, Quigley JP. J Biol Chem. 1995;270:5872–5876.
    1. Ohuchi E, Imai K, Fujii Y, Sato H, Seiki M, Okada Y. J Biol Chem. 1997;272:2446–2451.
    1. Lauer-Fields JL, Juska D, Fields GB. Biopolymers. 2002;66:19–32.
    1. Allan JA, Hembry RM, Angal S, Reynolds JJ, Murphy G. J Cell Sci. 1991;99:789–795.
    1. Allan JA, Docherty AJ, Barker PJ, Huskisson NS, Reynolds JJ, Murphy G. Biochem J. 1995;309:299–306.
    1. Postlethwaite AE, Seyer JM, Kang AH. Proc Natl Acad Sci USA. 1978;75:871–875.
    1. Yannas I, Burke J, Orgill D, Skrabut E. Science. 1982;215:174–176.
    1. Weadock KS, Miller EJ, Keuffel EL, Dunn MG. J Biomed Mat Res. 1996;32:221–226.
    1. Ruderman RJ, Wade CWR, Shepard WD, Leonard F. J Biomat Med Res. 1973;7:263–265.
    1. Harriger MD, Supp AP, Warden GD, Boyce ST. J Biomed Mat Res. 1997;35:137–145.
    1. Wu X, Black L, Santacana-Laffitte G, Patrick CW. J Biomat Mat Res. 2007;81A:59–65.
    1. Powell HM, Boyce ST. Biomaterials. 2006;27:5821–5827.
    1. Powell HM, Boyce ST. Biomaterials. 2007;28:1084–1092.
    1. Tu R, Lu CL, Thyagarajan K, Wang E, Nguyen H, Shen S, Hata C, Quijano RC. J Biomed Mat Res. 1993;27:3–9.
    1. Petite H, Rault I, Huc A, Menasche P, Herbage D. J Biomed Mat Res. 1990;24:179–187.
    1. Zeugolis DI, Paul GR, Attenburrow G. J Biomed Mat Res. 2009;89A:895–908.
    1. Speer DP, Chvapil M, Eskelson CD, Ulreich J. J Biomed Mat Res. 1980;14:753–764.
    1. van Luyn MJA, van Wachem PB, Damink LHHO, Dijkstra PJ, Feijen J, Nieuwenhuis P. Biomaterials. 1992;13:1017–1024.
    1. Maa L, Gaoa C, Maoa Z, Zhoua J, Shena J, Hub X, Han C. Biomaterials. 2003;24:4833–4841.
    1. Weadock KS, Miller EJ, Bellincampi LD, Zawadsky JP, Dunn MG. J Biomed Mat Res. 1995;29:1373–1379.
    1. Gorham SD, Light ND, Diamond AM, Willins MJ, Bailey AJ, Wess TJ, Leslie NJ. Int J Biol Macromol. 1992;14:129–138.
    1. Khew ST, Yang QJ, Tong YW. Biomaterials. 2008;29:3034–3045.
    1. Gilbert TW, Sellaro TL, Badylak SF. Biomaterials. 2006;27:3675–3683.
    1. Buijtenhuijs P, Buttafoco L, Poot AA, Daamen WF, van Kuppevelt TH, Dijkstra PJ, de Vos RAI, Sterk LM, Geelkerken BRH, Feijen J, Vermes I. Biotechnol Appl Biochem. 2004;39:141–149.
    1. Ellis DL, Yannas IV. Biomaterials. 1996;17:291–299.
    1. Fielding AM. In: The Methodology of Connective Tissue Research. Hall DA, editor. Joynson–Bruvvers; Oxford, UK: 1976. pp. 9–12.
    1. Piez KA. In: Extracellular Matrix Biochemistry. Piez KA, Reddi AH, editors. Elsevier; New York: 1984. pp. 1–40.
    1. Piez KA. Encyclopedia of Polymer Science and Engineering. Wiley; New York, NY: 1985. pp. 699–727.
    1. Yannas IV. Angew Chem Int Ed. 1990;29:20–35.
    1. Geesin JC, Brown LJ, Liu Z, Berg RA. J Biomed Mat Res. 1996;33:1–8.
    1. Doillon CJ, Silver FH. Biomaterials. 1986;7:3–8.
    1. Lefebvre F, Gorecki S, Bareille R, Amedee J, Bordenave L, Rabaud M. Biomaterials. 1992;13:28–33.
    1. Carlson MA, Longaker MT. Wound Rep Regen. 2004;12:134–147.
    1. Chvapil M, Chvapil TA, Owen JA. J Surg Res. 1986;41:410–418.
    1. Boyce ST, Christianson DJ, Hansbrough JF. J Biomed Mat Res. 1988;22:939–957.
    1. Leipziger LS, Glushko V, DiBernardo B, Shafaie F, Noble J, Nichols J, Alvarez OM. J Am Acad Dermatol. 1985;12:409–419.
    1. McPherson JM, Sawamura S, Armstrong R. J Biomed Mat Res. 1986;20:93–107.
    1. Boyce ST, Stompro BE, Hansbrough JF. J Biomed Mat Res. 1992;26:547–553.
    1. Stompro BE, Hansbrough JF, Boyce ST. J Surg Res. 1989;46:413–421.
    1. Marks MG, Doillon C, Silvert FH. J Biomed Mat Res. 1991;25:683–696.
    1. Lepistö J, Kujari H, Niinikoski J, Laato M. Eur Surg Res. 1994;26:267–272.
    1. Wachol-Drewek Z, Pfeiffer M, Scholl E. Biomaterials. 1996;17:1733–1738.
    1. Vaneerdeweg W, Bresseleers T, Du Jardin P, Lauwers P, Pauli S, Thyssens K, Van Marck E, Elseviers M, Eyskens E. Eur J Surg. 1998;164:617–621.
    1. Stemberger A, Grimm H, Bader F, Rahn HD, Ascherl R. Eur J Surg. 1997;578:17–26.
    1. Fujisato T, Sajiki T, Liu Q, Ikada Y. Biomaterials. 1996;17:155–162.
    1. Toolan BC, Frenkel SR, Pachence JM, Yalowitz L, Alexander H. J Biomed Mat Res. 1996;31:273–280.
    1. van Wachem PB, van Luyn MJA, Ponte da Costa ML. J Biomed Mat Res. 1996;30:353–360.
    1. Paíno CL, Fernandez-Valle C, Bates ML, Bunge MB. J Neurocytol. 1994;23:433–452.
    1. Sung KE, Su G, Pehlke C, Trier SM, Eliceiri KW, Keely PJ, Friedl A, Beebe D. J Biomaterials. 2009;30:4833–4841.
    1. Cross VL, Zheng Y, Won Choi N, Verbridge SS, Sutermaster BA, Bonassar LJ, Fischbach C, Stroock AD. Biomaterials. 2010;31:8596–8607.
    1. Altman AM, Matthias N, Yan Y, Song YH, Bai X, Chiu ES, Slakey DP, Alt EU. Biomaterials. 2008;29:1431–1442.
    1. Trottier V, Marceau-Fortier G, Germain L, Vincent C, Fradette J. Stem Cells. 2008;26:2713–2723.
    1. Koide M, Osaki K, Konishi J, Oyamada K, Katakura T, Takahashi A, Yoshizato K. J Biomed Mat Res. 1993;27:79–87.
    1. Ponticiello MS, Schinagl RM, Kadiyala S, Barry FP. J Biomed Mat Res. 2000;52:246–255.
    1. Tanihara M, Kajiwara K, Ida K, Suzuki Y, Kamitakahara M, Ogata SI. J Biomed Mater Res A. 2007;85:133–139.
    1. Shibasaki Y, Hirohara S, Terada K, Ando T, Tanihara M. Biopolymers (Pept Sci) 2011;96:302–315.
    1. McPherson JM, Ledger PW, Sawamura S, Conti A, Wade S, Reihanian H, Wallace DG. J Biomed Mat Res. 1986;20:79–92.
    1. Wallace DG, Rhee W, Reihanian H, Ksander G, Lee R, Braun WB, Weiss BA, Pharriss BB. J Biomed Mat Res. 1989;23:931–945.
    1. Wallace DG, Reihanian H, Pharriss BB, Braun WG. US Pat 4803075. 1989
    1. Horáková Z, Krajícek M, Chvapil M, Boissier J. Therapie. 1967;22:1455–1460.
    1. Rosenblatt J, Rhee W, Wallace D. J Control Release. 1989;9:195–203.
    1. Slavin J, Nash JR, Kingsnorth AN. Br J Surg. 1992;79:69–72.
    1. Saltzman WM, Parkhurst MR, Parsons-Wingerter P, Zhu WH. Ann NY Acad Sci. 1992;665:259–273.
    1. Parkhurst MR, Saltzman WM. Biophys J. 1992;61:306–315.
    1. Parkhurst MR, Saltzman WM. Cell Immunol. 1994;156:77–94.
    1. Marchand R, Woerly S, Bertrand L, Valdes N. Brain Res Bull. 1993;30:415–422.
    1. Docherty R, Forrester JV, Lackie JM, Gregory DW. J Cell Sci. 1989;92:263–270.
    1. Joosten EAJ, Bär PR, Gispen WH. J Neurosci Res. 1995;41:481–490.
    1. Cascone MG, Sim B, Sandra D. Biomaterials. 1995;16:569–574.
    1. Uchio Y, Ochi M, Matsusaki M, Kurioka H, Katsube K. J Biomed Mat Res. 2000;50:138–143.
    1. Weiner AL, Carpenter-Green SS, Soehngen EC, Lenk RP, Popescu MC. J Pharm Sci. 1985;74:922–925.
    1. Pajean M, Herbage D. Int J Pharm. 1993;91:209–216.
    1. Yamahira Y, Fujioka K, Sato S, Yoshida N. Eur Pat EP0140255. 1985
    1. Rubin AL, Stenzel KH, Miyata T, White MJ, Dunn M. J Clin Pharmacol. 1973;13:309–312.
    1. Maeda M, Kadota K, Kajihara M, Sano A, Fujioka K. J Control Release. 2001;77:261–272.
    1. Song SZ, Morawiecki A, Pierce GF, Pitt CG. US Pat 5418222. 1995
    1. Rosenthal FM, Kohler G. Anticancer Res. 1997;17:1179–1186.
    1. Park JC, Hwang YS, Lee JE, Park KD, Matsumura K, Hyon SH, Suh H. J Biomed Mat Res. 2000;52:669–677.
    1. Yang C, Hillas PJ, Báez JA, Nokelainen M, Balan J, Tang J, Spiro R, Polarek JW. BioDrugs. 2004;18:103–119.
    1. Van der Laan JS, Lopez GP, van Wachem PB, Nieuwenhuis P, Ratner BD, Bleichrodt RP, Schakenraad JM. Int J Artif Organs. 1991;14:661–666.
    1. Sekine T, Nakamura T, Shimizu Y, Ueda H, Matsumoto K, Takimoto Y, Kiyotani T. J Biomed Mater Res. 2001;54:305–310.
    1. Peters WJ. Ann Plast Surg. 1980;4:133–137.
    1. Whitaker K, Barrow P, Feree K. Ostomy Wound Manage. 1992;38:36–44.
    1. Zitelli JA. Adv Dermatol. 1987;2:243.
    1. Smith DJ., Jr J Burn Care Res. 1995;16:317–320.
    1. Lal S, Barrow RE, Wolf SE, Chinkes DL, Hart DW, Heggers JP, Herndon DN. Shock. 2000;14:314–319.
    1. Rao KP. J Biomater Sci. 1996;7:623–645.
    1. Boyce S. Med Biol Eng Comput. 1998;36:791–800.
    1. Yannas IV, Lee E, Orgill DP, Skrabut EM, Murphy GF. Proc Natl Acad Sci USA. 1989;86:933–937.
    1. Orwin EJ, Hubel A. Tissue Eng. 2000;6:304–319.
    1. Griffith M, Jackson WB, Lagali N, Merrett K, Li F, Fagerholm P. Eye. 2009;23:1985–1989.
    1. Carrier P, Deschambeault A, Talbot M, Giasson CJ, Auger FA, Guérin SL, Germain L. Invest Ophthalmol Vis Sci. 2008;49:1376–1385.
    1. Boyce ST, Supp AP, Warden GD, Holder IA. Antimicrob Agents Chemother. 1993;37:1890–1895.
    1. Régnier M, Staquet MJ, Schmitt D, Schimdt R. J Invest Dermatol. 1997;109:510–512.
    1. Bechetoille N, Dezutter-Dambuyant C, Damour O, André V, Orly I, Perrier E. Tissue Eng. 2007;13:2667–2679.
    1. Supp AP, Wickett RR, Swope VB, Harriger MD, Hoath SB, Boyce ST. Wound Rep Regen. 1999;7:226–237.
    1. Boyce ST, Goretsky MJ, Greenhalgh DG, Kagan RJ, Rieman MT, Warden GD. Ann Surg. 1995;222:743–752.
    1. Lam PK, Chan ESY, Liew CT, Lau CH, Yen SC, King WWK. Ann Plast Surg. 1999;43:523–528.
    1. Suzuki S, Kawai K, Ashoori F, Morimoto N, Nishimura Y, Ikada Y. Br J Plast Surg. 2000;53:659–666.
    1. Koide T. Philos Trans R Soc, B. 2007;362:1281–1291.
    1. Woolfson DN. Biopolymers. 2010;94:118–127.
    1. Fields GB. Org Biomol Chem. 2010;8:1237–1258.
    1. Fallas JA, O'Leary LE, Hartgerink JD. Chem Soc Rev. 2010;39:3510–3527.
    1. Przybyla DE, Chmielewski J. Biochemistry. 2010;49:4411–4419.
    1. Siebler C, Erdmann RS, Wennemers H. Chimia. 2013;67:891–895.
    1. He L, Theato P. Eur Polym J. 2013;49:2986–2997.
    1. Hartgerink JD, Beniash E, Stupp SI. Science. 2001;294:1684–1688.
    1. Hartgerink JD, Beniash E, Stupp SI. Proc Natl Acad Sci USA. 2002;99:5133–5138.
    1. Zhang S. Nat Biotechnol. 2003;21:1171–1178.
    1. Marini DM, Hwang W, Lauffenburger DA, Zhang S, Kamm RD. Nano Lett. 2002;2:295–299.
    1. Kisiday J, Jin M, Kurz B, Hung H, Semino C, Zhang S, Grodzinsky AJ. Proc Natl Acad Sci USA. 2002;99:9996–10001.
    1. Paramonov SE, Gauba V, Hartgerink JD. Macromolecules. 2005;38:7555–7561.
    1. O'Leary LE, Fallas JA, Bakota EL, Kang MK, Hartgerink JD. Nat Chem. 2011;3:821–828.
    1. Fallas JA, Hartgerink JD. Nat Commun. 2011;3:1087.
    1. Rele S, Song Y, Apkarian RP, Qu Z, Conticello VP, Chaikof EL. J Am Chem Soc. 2007;129:14780–14787.
    1. Cejas MA, Kinney WA, Chen C, Vinter JG, Almond J, H R, Balss KM, Maryanoff CA, Schmidt U, Breslav M, Mahan A, Lacy E, Maryanoff BE. Proc Natl Acad Sci USA. 2008;105:8513–8518.
    1. Koide T, Homma DL, Asada S, Kitagawa K. Bioorg Med Chem Lett. 2005;15:5230–5233.
    1. Kotch FW, Raines RT. Proc Natl Acad Sci USA. 2006;103:3028–3033.
    1. Johnson G, Jenkins M, McLean KM, Griesser HJ, Kwak J, Goodman M, Steele JG. J Biomed Mat Res. 2000;51:612–624.
    1. Cejas MA, Chen C, Kinney WA, Maryanoff BE. Bioconjugate Chem. 2007;18:1025–1027.
    1. Laskin DL, Soltys RA, Berg RA, Riley DJ. Am J Respir Cell Mol Biol. 1990;2:463–470.
    1. Laskin DL, Soltys RA, Berg RA, Riley DJ. Am J Respir Cell Mol Biol. 1994;10:58–64.
    1. Inoue O, Suzuki-Inoue K, Shinoda D, Umeda Y, Uchino M, Takasaki Si, Ozaki Y. FEBS Lett. 2009;583:81–87.
    1. Hennessy KM, Pollot BE, Clem WC, Phipps MC, Sawyer AA, Culpepper BK, Bellis SL. Biomaterials. 2009;30:1898–1909.
    1. Wang AY, Mo X, Chen CS, Yu SM. J Am Chem Soc. 2005;127:4130–4131.
    1. Wang AY, Foss CA, Leong S, Mo X, Pomper MG, Yu SM. Biomacromolecules. 2008;9:1755–1763.
    1. Mo X, An Y, Yun CS, Yu SM. Angew Chem Int Ed. 2006;45:2267–2270.
    1. Li Y, Foss CA, Summerfield DD, Doyle JJ, Torok CM, Dietz HC, Pomper MG, Yu SM. Proc Natl Acad Sci USA. 2012;109:14767–14772.
    1. Holmgren SK, Taylor KM, Bretscher LE, Raines RT. Nature. 1998;392:666–667.
    1. Hodges JA, Raines RT. J Am Chem Soc. 2003;125:9262–9263.
    1. Malkar NB, Lauer-Fields JL, Borgia JA, Fields GB. Biochemistry. 2002;41:6054–6064.
    1. Eberhardt ES, Panasik N, Jr, Raines RT. J Am Chem Soc. 1996;118:12261–12266.
    1. Bretscher LE, Jenkins CL, Taylor KM, DeRider ML, Raines RT. J Am Chem Soc. 2001;123:777–778.
    1. Shoulders MD, Satyshur KA, Forest KT, Raines RT. Proc Natl Acad Sci USA. 2010;106:559–564.
    1. Hodges JA, Raines RT. J Am Chem Soc. 2005;127:15923–15932.
    1. Chattopadhyay S, Murphy CJ, McAnulty JF, Raines RT. Org Biomol Chem. 2012;10:5892–5897.
    1. Chattopadhyay S, Guthrie KM, Teixeira L, Murphy CJ, Dubielzig RR, McAnulty JF, Raines RT. J Tissue Eng Regen Med. 2014;8 doi: 10.1002/term.1886.

Source: PubMed

3
Suscribir