Research article Topical Sections

Effect of nordihydroguaiaretic acid cross-linking on fibrillar collagen: in vitro evaluation of fibroblast adhesion strength and migration

  • Received: 17 January 2017 Accepted: 29 March 2017 Published: 06 April 2017
  • Fixation is required to reinforce reconstituted collagen for orthopedic bioprostheses such as tendon or ligament replacements. Previous studies have demonstrated that collagen fibers cross-linked by the biocompatible dicatechol nordihydroguaiaretic acid (NDGA) have mechanical strength comparable to native tendons. This work focuses on investigating fibroblast behavior on fibrillar and NDGA cross-linked type I collagen to determine if NDGA modulates cell adhesion, morphology, and migration. A spinning disk device that applies a range of hydrodynamic forces under uniform chemical conditions was employed to sensitively quantify cell adhesion strength, and a radial barrier removal assay was used to measure cell migration on films suitable for these quantitative in vitro assays. The compaction of collagen films, mediated by the drying and cross-linking fabrication process, suggests a less open organization compared to native fibrillar collagen that likely allowed the collagen to form more inter-chain bonds and chemical links with NDGA polymers. Fibroblasts strongly adhered to and migrated on native and NDGA cross-linked fibrillar collagen; however, NDGA modestly reduced cell spreading, adhesion strength and migration rate. Thus, it is hypothesized that NDGA cross-linking masked some adhesion receptor binding sites either physically, chemically, or both, thereby modulating adhesion and migration. This alteration in the cell-material interface is considered a minimal trade-off for the superior mechanical and compatibility properties of NDGA cross-linked collagen compared to other fixation approaches.

    Citation: Ana Y. Rioja, Maritza Muniz-Maisonet, Thomas J. Koob, Nathan D. Gallant. Effect of nordihydroguaiaretic acid cross-linking on fibrillar collagen: in vitro evaluation of fibroblast adhesion strength and migration[J]. AIMS Bioengineering, 2017, 4(2): 300-317. doi: 10.3934/bioeng.2017.2.300

    Related Papers:

  • Fixation is required to reinforce reconstituted collagen for orthopedic bioprostheses such as tendon or ligament replacements. Previous studies have demonstrated that collagen fibers cross-linked by the biocompatible dicatechol nordihydroguaiaretic acid (NDGA) have mechanical strength comparable to native tendons. This work focuses on investigating fibroblast behavior on fibrillar and NDGA cross-linked type I collagen to determine if NDGA modulates cell adhesion, morphology, and migration. A spinning disk device that applies a range of hydrodynamic forces under uniform chemical conditions was employed to sensitively quantify cell adhesion strength, and a radial barrier removal assay was used to measure cell migration on films suitable for these quantitative in vitro assays. The compaction of collagen films, mediated by the drying and cross-linking fabrication process, suggests a less open organization compared to native fibrillar collagen that likely allowed the collagen to form more inter-chain bonds and chemical links with NDGA polymers. Fibroblasts strongly adhered to and migrated on native and NDGA cross-linked fibrillar collagen; however, NDGA modestly reduced cell spreading, adhesion strength and migration rate. Thus, it is hypothesized that NDGA cross-linking masked some adhesion receptor binding sites either physically, chemically, or both, thereby modulating adhesion and migration. This alteration in the cell-material interface is considered a minimal trade-off for the superior mechanical and compatibility properties of NDGA cross-linked collagen compared to other fixation approaches.


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    [1] Alberts B (2008) Molecular biology of the cell. New York: Garland Science.
    [2] Koob TJ (2004) Collagen fixation. Encyclopedia Biomater Biomed Eng 1: 335–347.
    [3] Koob TJ (2002) Biomimetic approaches to tendon repair. Comp Biochem Physiol A Mol Integr Physiol 133: 1171–1192. doi: 10.1016/S1095-6433(02)00247-7
    [4] McCarthy JB, Vachhani B, Iida J (1996) Cell adhesion to collagenous matrices. Biopolymers 40: 371–381. doi: 10.1002/(SICI)1097-0282(1996)40:4<371::AID-BIP3>3.0.CO;2-T
    [5] Rault I, Frei V, Herbage D, et al. (1996) Evaluation of different chemical methods for cros-linking collagen gel, films and sponges. J Mater Sci Mater M 7: 215–221.
    [6] Jayakrishnan A, Jameela SR (1996) Glutaraldehyde as a fixative in bioprostheses and drug delivery matrices. Biomaterials 17: 471–484. doi: 10.1016/0142-9612(96)82721-9
    [7] Zuhdi N, Hawley W, Voehl V, et al. (1974) Porcine aortic valves as replacements for human heart valves. Ann Thorac Surg 17: 479–491. doi: 10.1016/S0003-4975(10)65683-4
    [8] Bigi A, Cojazzi G, Panzavolta S, et al. (2001) Mechanical and thermal properties of gelatin films at different degrees of glutaraldehyde crosslinking. Biomaterials 22: 763–768. doi: 10.1016/S0142-9612(00)00236-2
    [9] Goldstein JD, Tria AJ, Zawadsky JP, et al. (1989) Development of a reconstituted collagen tendon prosthesis-a preliminary implantation study. J Bone Joint Surg Am 71: 1183–1191. doi: 10.2106/00004623-198971080-00010
    [10] Damink LHHO, Dijkstra PJ, Vanluyn MJA, et al. (1995) Glutaraldehyde as a cross-linking agent for collagen-based biomaterials. J Mater Sci Mater M 6: 460–472. doi: 10.1007/BF00123371
    [11] Speer DP, Chvapil M, Eskelson CD, et al. (1980) Biological effects of residual glutaraldehyde in glutaraldehyde-tanned collagen biomaterials. J Biomed Mater Res 14: 753–764. doi: 10.1002/jbm.820140607
    [12] Olde DLH, Dijkstra PJ, van Luyn MJ, et al. (1996) Cross-linking of dermal sheep collagen using a water-soluble carbodiimide. Biomaterials 17: 765–773. doi: 10.1016/0142-9612(96)81413-X
    [13] Kato YP, Christiansen DL, Hahn RA, et al. (1989) Mechanical-properties of collagen-fibers-a comparison of reconstituted and rat tail tendon fibers. Biomaterials 10: 38–41. doi: 10.1016/0142-9612(89)90007-0
    [14] Kato YP, Dunn MG, Zawadsky JP, et al. (1991) Regeneration of achilles-tendon with a collagen tendon prosthesis-results of a one-year implantation study. J Bone Joint Surg Am 73: 561–574. doi: 10.2106/00004623-199173040-00013
    [15] Everaerts F, Torrianni M, Hendriks M, et al. (2008) Biomechanical properties of carbodiimide crosslinked collagen: influence of the formation of ester crosslinks. J Biomed Mater Res A 85A: 547–555. doi: 10.1002/jbm.a.31524
    [16] Sung HW, Chang WH, Ma CY, et al. (2003) Crosslinking of biological tissues using genipin and/or carbodiimide. J Biomed Mater Res A 64: 427–438.
    [17] Chang Y, Tsai CC, Liang HC, et al. (2001) Reconstruction of the right ventricular outflow tract with a bovine jugular vein graft fixed with a naturally occurring crosslinking agent (genipin) in a canine model. J Thorac Cardiov Sur 122: 1208–1218. doi: 10.1067/mtc.2001.117624
    [18] Huang LLH, Sung HW, Tsai CC, et al. (1998) Biocompatibility study of a biological tissue fixed with a naturally occurring crosslinking reagent. J Biomed Mater Res 42: 568–576. doi: 10.1002/(SICI)1097-4636(19981215)42:4<568::AID-JBM13>3.0.CO;2-7
    [19] Sung HW, Huang RN, Huang LLH, et al. (1998) Feasibility study of a natural crosslinking reagent for biological tissue fixation. J Biomed Mater Res 42: 560–567. doi: 10.1002/(SICI)1097-4636(19981215)42:4<560::AID-JBM12>3.0.CO;2-I
    [20] Sung HW, Liang IL, Chen CN, et al. (2001) Stability of a biological tissue fixed with a naturally occurring crosslinking agent (genipin). J Biomed Mater Res 55: 538–546. doi: 10.1002/1097-4636(20010615)55:4<538::AID-JBM1047>3.0.CO;2-2
    [21] Hwang YJ, Larsen J, Krasieva TB, et al. (2011) Effect of genipin crosslinking on the optical spectral properties and structures of collagen hydrogels. ACS Appl Mater Inter 3: 2579–2584. doi: 10.1021/am200416h
    [22] Koob TJ, Hernandez DJ (2002) Material properties of polymerized NDGA-collagen composite fibers: development of biologically based tendon constructs. Biomaterials 23: 203–212. doi: 10.1016/S0142-9612(01)00096-5
    [23] Koob TJ, Hernandez DJ (2003) Mechanical and thermal properties of novel polymerized NDGA-gelatin hydrogels. Biomaterials 24: 1285–1292. doi: 10.1016/S0142-9612(02)00465-9
    [24] Koob TJ, Willis TA, Hernandez DJ (2001) Biocompatibility of NDGA-polymerized collagen fibers I. Evaluation of cytotoxicity with tendon fibroblasts in vitro. J Biomed Mater Res 56: 31–39.
    [25] Koob TJ, Willis TA, Qiu YS, et al. (2001) Biocompatibility of NDGA-polymerized collagen fibers II. Attachment, proliferation, and migration of tendon fibroblasts in vitro. J Biomed Mater Res 56: 40–48.
    [26] Qiu Y, Lei J, Koob TJ, et al. (2014) Cyclic tension promotes fibroblastic differentiation of human MSCs cultured on collagen-fibre scaffolds. J Tissue Eng Regen M 10: 989–999.
    [27] Lu JM, Nurko J, Weakley SM, et al. (2010) Molecular mechanisms and clinical applications of nordihydroguaiaretic acid (NDGA) and its derivatives: an update. Med Sci Monit 16: RA93–100.
    [28] Fisher AA, Labenski MT, Malladi S, et al. (2007) Quinone electrophiles selectively adduct "electrophile binding motifs" within cytochrome c†. Biochemistry 46: 11090–11100. doi: 10.1021/bi700613w
    [29] Labenski MT, Fisher AA, Lo HH, et al. (2009) Protein electrophile-binding motifs: lysine-rich proteins are preferential targets of quinones. Drug Metab Dispos 37: 1211–1218.
    [30] Moussy Y, Guegan E, Davis T, et al. (2007) Transport characteristics of a novel local drug delivery system using nordihydroguaiaretic acid (NDGA)-polymerized collagen fibers. Biotechnol Prog 23: 990–994. doi: 10.1002/bp0700509
    [31] Xu B, Chow MJ, Zhang Y (2011) Experimental and modeling study of collagen scaffolds with the effects of crosslinking and fiber alignment. Int J Biomater 2011: 172389–172400.
    [32] Ju YM, Yu B, Koob TJ, et al. (2008) A novel porous collagen scaffold around an implantable biosensor for improving biocompatibility I. In vitro/in vivo stability of the scaffold and in vitro sensitivity of the glucose sensor with scaffold. J Biomed Mater Res A 87: 136–146.
    [33] Baker BM, Mauck RL (2007) The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomaterials 28: 1967–1977. doi: 10.1016/j.biomaterials.2007.01.004
    [34] Elineni KK, Gallant ND (2011) Regulation of cell adhesion strength by peripheral focal adhesion distribution. Biophys J 101: 2903–2911. doi: 10.1016/j.bpj.2011.11.013
    [35] Gallant ND, Michael KE, Garcia AJ (2005) Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol Biol Cell 16: 4329–4340. doi: 10.1091/mbc.E05-02-0170
    [36] Garcia AJ, Gallant ND (2003) Stick and grip: measurement systems and quantitative analyses of integrin-mediated cell adhesion strength. Cell Biochem Biophys 39: 61–73. doi: 10.1385/CBB:39:1:61
    [37] Kennedy SB, Washburn NR, Simon CG Jr., et al. (2006) Combinatorial screen of the effect of surface energy on fibronectin-mediated osteoblast adhesion, spreading and proliferation. Biomaterials 27: 3817–3824. doi: 10.1016/j.biomaterials.2006.02.044
    [38] Elliott JT, Tona A, Plant AL (2003) Comparison of reagents for shape analysis of fixed cells by automated fluorescence microscopy. Cytometry A 52: 90–100.
    [39] Zohrabian VM, Forzani B, Chau ZL, et al. (2009) Rho/ROCK and MAPK Signaling pathways are involved in glioblastoma cell migration and proliferation. Anticancer Res 29: 119–123.
    [40] Berens ME, Beaudry C (2004) Radial monolayer cell migration assay. Methods Mol Med 88: 219–224.
    [41] Pratt BM, Harris AS, Morrow JS, et al. (1984) Mechanisms of cytoskeletal regulation. Modulation of aortic endothelial cell spectrin by the extracellular matrix. Am J pathol 117: 349–354.
    [42] Kondo H, Matsuda R, Yonezawa Y (1993) Autonomous migration of human fetal skin fibroblasts into a denuded area in a cell monolayer is mediated by basic fibroblast growth factor and collagen. In Vitro Cell Dev Biol Anim 29: 929–935. doi: 10.1007/BF02634231
    [43] Tomasz M (1995) Mitomycin C: small, fast and deadly (but very selective). Chem Biol 2: 575–579. doi: 10.1016/1074-5521(95)90120-5
    [44] Kark LR, Karp JM, Davies JE (2006) Platelet releasate increases the proliferation and migration of bone marrow-derived cells cultured under osteogenic conditions. Clin Oral Implants Res 17: 321–327. doi: 10.1111/j.1600-0501.2005.01189.x
    [45] Albarran G, Boggess W, Rassolov V, et al. (2010) Absorption spectrum, mass spectrometric properties, and electronic structure of 1,2-benzoquinone. J Phys Chem A 114: 7470–7478. doi: 10.1021/jp101723s
    [46] Hamann JN, Tuczek F (2014) New catalytic model systems of tyrosinase: fine tuning of the reactivity with pyrazole-based N-donor ligands. Chem Commun 50: 2298–2300. doi: 10.1039/c3cc47888b
    [47] Buxboim A, Rajagopal K, Brown AE, et al. (2010) How deeply cells feel: methods for thin gels. J Phys Condens Matter 22: 194116–194125. doi: 10.1088/0953-8984/22/19/194116
    [48] Engler A, Bacakova L, Newman C, et al. (2004) Substrate compliance versus ligand density in cell on gel responses. Biophys J 86: 617–628. doi: 10.1016/S0006-3495(04)74140-5
    [49] Engler AJ, Sen S, Sweeney HL, et al. (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677–689. doi: 10.1016/j.cell.2006.06.044
    [50] Lo CM, Wang HB, Dembo M, et al. (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79: 144–152.
    [51] Cavalcanti AEA, Volberg T, Micoulet A, et al. (2007) Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys J 92: 2964–2974. doi: 10.1529/biophysj.106.089730
    [52] Selhuber UC, Erdmann T, Lopez GM, et al. (2010) Cell adhesion strength is controlled by intermolecular spacing of adhesion receptors. Biophys J 98: 543–551. doi: 10.1016/j.bpj.2009.11.001
    [53] Maheshwari G, Brown G, Lauffenburger DA, et al. (2000) Cell adhesion and motility depend on nanoscale RGD clustering. J Cell Sci 113: 1677–1686.
    [54] Massia SP, Hubbell JA (1991) 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: 1089–1100. doi: 10.1083/jcb.114.5.1089
    [55] Reyes CD, Garcia AJ (2003) A centrifugation cell adhesion assay for high-throughput screening of biomaterial surfaces. J Biomed Mater Res 67: 328–333.
    [56] Garcia AJ, Huber F, Boettiger D (1998) Force required to break alpha5beta1 integrin-fibronectin bonds in intact adherent cells is sensitive to integrin activation state. J Biol Chem 273: 10988–10993. doi: 10.1074/jbc.273.18.10988
    [57] Grover CN, Gwynne JH, Pugh N, et al. (2012) Crosslinking and composition influence the surface properties, mechanical stiffness and cell reactivity of collagen-based films. Acta Biomater 8: 3080–3090. doi: 10.1016/j.actbio.2012.05.006
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