Hyaluronic acid: Evaluation as a potential delivery vehicle for vitronectin:growth factor complexes in wound healing applications

Journal of Controlled Release

Volumn 153, Issue 3, 2011, Pages 225-232

  Xie, Yan ^a   Upton, Zee ^a   Richards, Sean ^a   Rizzi, Simone C ^a,b   Leavesley, David I ^a  

^a QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^b EPFL   (Switzerland)

Author keywords

Delivery vehicle; Hyaluronic acid (HA); Skin wound healing; Vitronectin:growth factor (VN:GF)

Indexed keywords

BURN MODEL; CELL RESPONSE; CELL SURFACE RECEPTORS; CELLULAR RESPONSE; DELIVERY VEHICLE; ENHANCED ABSORPTION; GROWTH FACTOR; HUMAN FIBROBLAST; HUMAN SKIN; HYALURONIC ACIDS; KERATINOCYTES; MONOLAYER CELL CULTURE; PHYSICOCHEMICAL PROPERTY; RE-EPITHELIALIZATION; TOPICAL DELIVERY; VITRONECTIN; WOUND HEALING APPLICATIONS;

ANIMAL CELL CULTURE; CELL MEMBRANES; COMPLEXATION; ECOLOGY; MONOLAYERS; ORGANIC ACIDS; PEPTIDES; THREE DIMENSIONAL;

RHENIUM COMPOUNDS;

CELL SURFACE RECEPTOR; HYALURONIC ACID; HYBRID PROTEIN; UNCLASSIFIED DRUG; VITRONECTIN GROWTH FACTOR COMPLEX;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DEGRADATION; DERMIS; DRUG DELIVERY SYSTEM; EPIDERMIS; EPITHELIZATION; HUMAN; HUMAN CELL; KERATINOCYTE; MONOLAYER CULTURE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; SKIN FIBROBLAST; SUSTAINED DRUG RELEASE; THICKNESS; WOUND HEALING;

CELL CULTURE TECHNIQUES; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CULTURE MEDIA, SERUM-FREE; DRUG CARRIERS; FIBROBLASTS; HUMANS; HYALURONIC ACID; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KERATINOCYTES; MODELS, BIOLOGICAL; SKIN; VITRONECTIN; WOUND HEALING;

EID: 79960929750     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.03.021     Document Type: Article

References (78)

1. N.N. Nissen, P.J. Polverini, A.E. Koch, M.V. Volin, R.L. Gamelli, L.A. DiPietro, Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing, Am. J. Pathol. 152 (6) (1998) 1445-1452. (Pubitemid 28275003)
2. M. Shah, D.M. Foreman, M.W. Ferguson, Control of scarring in adult wounds by neutralising antibody to transforming growth factor beta, Lancet 339 (8787) (1992) 213-214.
3. J.M. Smiell, T.J. Wieman, D.L. Steed, B.H. Perry, A.R. Sampson, B.H. Schwab, Efficacy and safety of becaplermin (recombinant human platelet-derived growth factor-BB) in patients with nonhealing, lower extremity diabetic ulcers: a combined analysis of four randomized studies, Wound Repair Regen. 7 (5) (1999) 335-346. (Pubitemid 29523009)
4. K. Kawai, S. Suzuki, Y. Tabata, Y. Ikada, Y. Nishimura, Accelerated tissue regeneration through incorporation of basic fibroblast growth factor-impregnated gelatin microspheres into artificial dermis, Biomaterials 21 (5) (2000) 489-499. (Pubitemid 30067585)
5. R.M. Da Costa, F.M. Ribeiro Jesus, C. Aniceto, M. Mendes, Randomized, double-blind, placebo-controlled, dose- ranging study of granulocyte-macrophage colony stimulating factor in patients with chronic venous leg ulcers, Wound Repair Regen. 7 (1) (1999) 17-25. (Pubitemid 29159037)
6. V. Falanga, W.H. Eaglstein, B. Bucalo, M.H. Katz, B. Harris, P. Carson, Topical use of human recombinant epidermal growth factor (h-EGF) in venous ulcers, J. Dermatol. Surg. Oncol. 18 (7) (1992) 604-606.
7. F.G. Giancotti, E. Ruoslahti, Integrin signaling, Science. 285 (5430) (1999) 1028-1032.
8. B. Hollier, D.G. Harkin, D. Leavesley, Z. Upton, Responses of keratinocytes to substrate-bound vitronectin:growth factor complexes, Exp. Cell Res. 305 (1) (2005) 221-232. (Pubitemid 40380668)
9. Z. Upton, L. Cuttle, A. Noble, M. Kempf, G. Topping, J. Malda, Y. Xie, J. Mill, D.G. Harkin, O. Kravchuk, D.I. Leavesley, R.M. Kimble, Vitronectin:growth factor complexes hold potential as a wound therapy approach, J. Invest. Dermatol. 128 (6) (2008) 1535-1544. (Pubitemid 351693179)
10. T.C. Laurent, J.R. Fraser, Hyaluronan, FASEB J. 6 (7) (1992) 2397-2404.
11. T.J. Brown, D. Alcorn, J.R. Fraser, Absorption of hyaluronan applied to the surface of intact skin, J. Invest. Dermatol. 113 (5) (1999) 740-746.
12. R. Gurny, H. Ibrahim, A. Aebi, P. Buri, C.G. Wilson, N. Washington, P. Edman, O. Camber, Design and evaluation of controlled release systems for the eye, J. Control. Release 6 (1987) 367-373. (Pubitemid 18019091)
13. M.F. Saettone, P. Chetoni, M.T. Torracca, S. Burgalassi, B. Giannaccini, Evaluation of muco-adhesive properties and in vivo activity of ophthalmic vehicles based on hyaluronic acid, Int. J. Pharm. 51 (3) (1989) 203-212. (Pubitemid 19117685)
14. F. Castellano, G.Mautone, Decongestant activity of a new formulation of xylometazoline nasal spray: a double-blind, randomized versus placebo and reference drugs controlled, dose-effect study, Drugs Exp Clin Res. 28 (1) (2002) 27-35. (Pubitemid 34606213)
15. K. Morimoto, H. Yamaguchi, Y. Iwakura, K. Morisaka, Y. Ohashi, Y. Nakai, Effects of viscous hyaluronate-sodium solutions on the nasal absorption of vasopressin and an analogue, Pharm. Res. 8 (4) (1991) 471-474.
16. Y. Luo, G.D. Prestwich, Synthesis and selective cytotoxicity of a hyaluronic acid-antitumor bioconjugate, Bioconjug. Chem. 10 (5) (1999) 755-763. (Pubitemid 29456361)
17. K. Sakurai, K. Miyazaki, Y. Kodera, H. Nishimura, M. Shingu, Y. Inada, Anti-inflammatory activity of superoxide dismutase conjugated with sodium hyaluronate, Glycoconj. J. 14 (6) (1997) 723-728. (Pubitemid 27400103)
18. J.P. Chen, Y.L. Leu, C.L. Fang, C.H. Chen, J.Y. Fang, Thermosensitive hydrogels composed of hyaluronic acid and gelatin as carriers for the intravesical administration of cisplatin, J. Pharm. Sci. 100 (2) (2010) 655-666.
19. A.K. Yadav, P. Mishra, A.K. Mishra, P. Mishra, S. Jain, G.P. Agrawal, Development and characterization of hyaluronic acid-anchored PLGA nanoparticulate carriers of doxorubicin, Nanomedicine 3 (4) (2007) 246-257. (Pubitemid 350199644)
20. K. Surendrakumar, G.P. Martyn, E.C.M. Hodgers, M. Jansen, J.A. Blair, Sustained release of insulin from sodium hyaluronate based dry powder formulations after pulmonary delivery to beagle dogs, J. Control. Release 91 (3) (2003) 385-394. (Pubitemid 36980658)
21. D. Peer, A. Florentin, R. Margalit, Hyaluronan is a key component in cryoprotection and formulation of targeted unilamellar liposomes, Biochim. Biophys. Acta 1612 (1) (2003) 76-82. (Pubitemid 36555689)
22. Y. Luo, K.R. Kirker, G.D. Prestwich, Cross-linked hyaluronic acid hydrogel films: new biomaterials for drug delivery, J. Control. Release 69 (1) (2000) 169-184.
23. S.T. Lim, G.P. Martin, D.J. Berry, M.B. Brown, Preparation and evaluation of the in vitro drug release properties and mucoadhesion of novel microspheres of hyaluronic acid and chitosan, J. Control. Release 66 (2-3) (2000) 281-292. (Pubitemid 30160864)
24. A. Kim, D.M. Checkla, P. Dehazya, W. Chen, Characterization of DNA-hyaluronan matrix for sustained gene transfer, J. Control. Release 90 (1) (2003) 81-95. (Pubitemid 36588881)
25. N.J. Trengove, H. Bielefeldt-Ohmann, M.C. Stacey, Mitogenic activity and cytokine levels in non-healing and healing chronic leg ulcers, Wound Repair Regen. 8 (1) (2000) 13-25. (Pubitemid 30140796)
26. I. Hopkinson, Growth factors an extracellular matrix biosynthesis, J. Wound Care 1 (2) (1992) 47-50.
27. J.A. Kricker, C.L. Towne, S.M. Firth, A.C. Herington, Z. Upton, Structural and functional evidence for the interaction of insulin-like growth factors (IGFs) and IGF binding proteins with vitronectin, Endocrinology 144 (7) (2003) 2807-2815. (Pubitemid 36819880)
28. C. Hyde, B. Hollier, A. Anderson, D. Harkin, Z. Upton, Insulin-like growth factors (IGF) and IGF-binding proteins bound to vitronectin enhance keratinocyte protein synthesis and migration, J. Invest. Dermatol. 122 (2004) 1198-1206. (Pubitemid 38651095)
29. B.G. Hollier, J.A. Kricker, D.R. Van Lonkhuyzen, D.I. Leavesley, Z. Upton, Substrate-bound insulin-like growth factor (IGF)-I-IGF binding protein-vitronectin-stimulated breast cell migration is enhanced by coactivation of the phosphatidylinositide 3-Kinase/AKT pathway by alphav-integrins and the IGF-I receptor, Endocrinology 149 (3) (2008) 1075-1090. (Pubitemid 351397938)
30. D.I.M.S. Leavesley, M Rosenfeld and DA Cheresh Integrin beta 1-and beta 3-mediated endothelial cell migration is triggered through distinct signaling mechanisms, J. Cell Biol. 121 (1) (1993) 163-170.
31. Y. Xie, S. Rizzi, R. Dawson, E. Lynam, S. Richards, D. Leavesley, Z. Upton, Development of a 3-dimensional human skin equivalent wound model for investigating novel wound healing therapies, Tissue Eng C Methods. 16 (5) (2010) 1111-1123.
32. G. Topping, J. Malda, R. Dawson, Z. Upton, Development and characterisation of human skin equivalents and their potential application as a burn wound model, Australian Wound Management. 14 (1) (2006) 14.
33. T.L. Wood, Gene-targeting and transgenic approaches to IGF and IGF binding protein function, Am. J. Physiol. 269 (4 Pt 1) (1995) E613-E622.
34. W.S. Cohick, D.R. Clemmons, The insulin-like growth factors, Annu. Rev. Physiol. 55 (1993) 131-153. (Pubitemid 23102127)
35. W. Kiess, Y. Yang, U. Kessler, A. Hoeflich, Insulin-like growth factor II (IGF-II) and the IGF-II/mannose-6-phosphate receptor: the myth continues, Horm. Res. 41 (Suppl. 2) (1994) 66-73. (Pubitemid 24180897)
36. E. Wertheimer, M. Trebicz, T. Eldar, M. Gartsbein, S. Nofeh-Moses, T. Tennenbaum, Differential roles of insulin receptor and insulin-like growth factor-1 receptor in differentiation of murine skin keratinocytes, J. Invest. Dermatol. 115 (1) (2000) 24-29. (Pubitemid 30470187)
37. G. Schultz, D.S. Rotatori, W. Clark, EGF and TGF-alpha in wound healing and repair, J. Cell. Biochem. 45 (4) (1991) 346-352.
38. E. Kawahara, N. Nakada, T. Hikichi, J. Kobayashi, I. Nakanishi, EGF and beta1 integrin convergently regulate migration of A431 carcinoma cell through MAP kinase activation, Exp. Cell Res. 272 (1) (2002) 84-91.
39. K.S. Stenn, Epibolin: a protein of human plasma that supports epithelial cell movement, Proc Natl Acad Sci USA. 78 (11) (1981) 6907-6911. (Pubitemid 12216871)
40. C. Brown, K.S. Stenn, R.J. Falk, D.T. Woodley, E.J. O'Keefe, Vitronectin: effects on keratinocyte motility and inhibition of collagen-induced motility, J. Invest. Dermatol. 96 (5) (1991) 724-728.
41. K.T. Preissner, Structure and biological role of vitronectin, Annu. Rev. Cell Biol. 7 (1991) 275-310.
42. M. Schoppet, T. Chavakis, N. Al-Fakhri, S.M. Kanse, K.T. Preissner, Molecular interactions and functional interference between vitronectin and transforming growth factor-beta, Lab Invest. 82 (1) (2002) 37-46. (Pubitemid 34072644)
43. A. Stockmann, S. Hess, P. Declerck, R. Timpl, K.T. Preissner, Multimeric vitronectin. Identification and characterization of conformation-dependent self-association of the adhesive protein, J. Biol. Chem. 268 (30) (1993) 22874-22882. (Pubitemid 23318352)
44. D.M. Danilenko, B.D. Ring, J.Z. Lu, J.E. Tarpley, D. Chang, N. Liu, D. Wen, G.F. Pierce, Neu differentiation factor upregulates epidermal migration and integrin expression in excisional wounds, J. Clin. Invest. 95 (2) (1995) 842-851.
45. S.R. Baker, M.C. Stacey, Epidemiology of chronic leg ulcers in Australia, Aust. N. Z. J. Surg. 64 (4) (1994) 258-261. (Pubitemid 24270267)
46. J. Banks, J.W. Kreider, V.P. Bhavanandan, E.A. Davidson, Anionic polysaccharide production and tyrosinase activation in cultured human melanoma cells, Cancer Res. 36 (2 Pt 1) (1976) 424-431.
47. H.C. DeGrendele, P. Estess, M.H. Siegelman, Requirement for CD44 in activated T cell extravasation into an inflammatory site, Science. 278 (5338) (1997) 672-675. (Pubitemid 27464963)
48. C.L. Hall, C. Wang, L.A. Lange, E.A. Turley, Hyaluronan and the hyaluronan receptor RHAMM promote focal adhesion turnover and transient tyrosine kinase activity, J. Cell Biol. 126 (2) (1994) 575-588. (Pubitemid 24226272)
49. C.R. Kothapalli, A. Ramamurthi, Benefits of concurrent delivery of hyaluronan and IGF-1 cues to regeneration of crosslinked elastin matrices by adult rat vascular cells, J. Tissue Eng. Regen. Med. 2 (2-3) (2008) 106-116.
50. S. Rajapaksa, D. McIntosh, A. Cowin, D. Adams, P.J. Wormald, The effect of insulin-like growth factor 1 incorporated into a hyaluronic acid-based nasal pack on nasal mucosal healing in a healthy sheep model and a sheep model of chronic sinusitis, Am. J. Rhinol. 19 (3) (2005) 251-256. (Pubitemid 40936428)
51. Y. Matsumoto, Y. Kuroyanagi, Development of a wound dressing composed of hyaluronic acid sponge containing arginine and epidermal growth factor. J Biomater Sci Polym Ed. 21(6) (2010) 715-726.
52. P.S. Leventhal, E.L. Feldman, Insulin-like growth factors as regulators of cell motility signaling mechanisms, Trends Endocrinol. Metab. 8 (1) (1997) 1-6. (Pubitemid 27090225)
53. R.M. Greco, J.A. Iocono, H.P. Ehrlich, Hyaluronic acid stimulates human fibroblast proliferation within a collagen matrix, J. Cell. Physiol. 177 (3) (1998) 465-473. (Pubitemid 28524669)
54. S. Mohapatra, X. Yang, J.A. Wright, E.A. Turley, A.H. Greenberg, Soluble hyaluronan receptor RHAMM induces mitotic arrest by suppressing Cdc2 and cyclin B1 expression, J. Exp. Med. 183 (4) (1996) 1663-1668. (Pubitemid 26134308)
55. S. Zhang, M.C. Chang, D. Zylka, S. Turley, R. Harrison, E.A. Turley, The hyaluronan receptor RHAMM regulates extracellular-regulated kinase, J. Biol. Chem. 273 (18) (1998) 11342-11348. (Pubitemid 28204989)
56. A. Noble, In vitro examination of vitronectin, insulin-like growth factor, insulin-like growth factor binding protein complexes as treatments to accelerate the healing of diabetic ulcers, Life Science Queensland University of Technology Brisbane, 2008, pp. 74-80.
57. A. Birgersdotter, R. Sandberg, I. Ernberg, Gene expression perturbation in vitro-a growing case for three-dimensional (3D) culture systems, Semin. Cancer Biol. 15 (5) (2005) 405-412. (Pubitemid 41140308)
58. V.M. Weaver, O.W. Petersen, F. Wang, C.A. Larabell, P. Briand, C. Damsky, M.J. Bissell, Reversion of the malignant phenotype of human breast cells in three-dimensional culture and in vivo by integrin blocking antibodies, J. Cell Biol. 137 (1) (1997) 231-245. (Pubitemid 27167310)
59. M. Breetveld, C.D. Richters, T. Rustemeyer, R.J. Scheper, S. Gibbs, Comparison of wound closure after burn and cold injury in human skin equivalents, J. Invest. Dermatol. 126 (8) (2006) 1918-1921. (Pubitemid 44086530)
60. K.H. Chakrabarty, R.A. Dawson, P. Harris, C. Layton, M. Babu, L. Gould, J. Phillips, I. Leigh, C. Green, E. Freedlander, Development of autologous human dermal-epidermal composites based on sterilized human allodermis for clinical use, Br. J. Dermatol. 141 (5) (1999) 811-823.
61. L.Y.W. Bourguignon, P.A. Singleton, F. Diedrich, Hyaluronan-CD44 interaction with Rac1-dependent protein kinase N-γ promotes phospholipase cγ1 activation, Ca2+ signaling, and cortactin-cytoskeleton function leading to keratinocyte adhesion and differentiation, J. Biol. Chem. 279 (28) (2004) 29654-29669. (Pubitemid 38915849)
62. V.B. Lokeshwar, N. Iida, L.Y.W. Bourguignon, The cell adhesion molecule, GP116, is a new CD44 variant (ex14/v10) involved in hyaluronic acid binding and endothelial cell proliferation, J. Biol. Chem. 271 (39) (1996) 23853-23864. (Pubitemid 26327359)
63. A. Masellis-Smith, A.R. Belch, M.J. Mant, E.A. Turley, L.M. Pilarski, Hyaluronan-dependent motility of B cells and leukemic plasma cells in blood, but not of bone marrow plasma cells, in multiple myeloma: alternate use of receptor for hyaluronan-mediated motility (RHAMM) and CD44, Blood 87 (5) (1996) 1891-1899.
64. J. Ortonne, A controlled study of the activity of hyaluronic acid in the treatment of venous leg ulcers, J Dermatol Treat. 7 (2) (1996) 75-81. (Pubitemid 26235527)
65. S. Werner, T. Krieg, H. Smola, Keratinocyte-fibroblast interactions in wound healing, J. Invest. Dermatol. 127 (5) (2007) 998-1008. (Pubitemid 46625161)
66. S. Gariboldi, M. Palazzo, L. Zanobbio, S. Selleri, M. Sommariva, L. Sfondrini, S. Cavicchini, A. Balsari, C. Rumio, Low molecular weight hyaluronic acid increases the self-defense of skin epithelium by induction of beta-defensin 2 via TLR2 and TLR4, J. Immunol. 181 (3) (2008) 2103-2110.
67. G.F. Dusio, D. Cardani, L. Zanobbio, M. Mantovani, P. Luchini, L. Battini, V. Galli, A. Diana, A. Balsari, C. Rumio, Stimulation of TLRs by LMW-HA induces self-defense mechanisms in vaginal epithelium, Immunol. Cell Biol. (2010)8 (Epub ahead of print).
68. S. Matou-Nasri, J. Gaffney, S. Kumar, M. Slevin, Oligosaccharides of hyaluronan induce angiogenesis through distinct CD44 and RHAMM-mediated signalling pathways involving Cdc2 and gamma-adducin, Int. J. Oncol. 35 (4) (2009) 761-773.
69. M.M. Mascarenhas, R.M. Day, C.D. Ochoa, W.I. Choi, L. Yu, B. Ouyang, H.G. Garg, C.A. Hales, D.A. Quinn, Low molecular weight hyaluronan from stretched lung enhances interleukin-8 expression, Am. J. Respir. Cell Mol. Biol. 30 (1) (2004) 51-60. (Pubitemid 38085258)
70. M.B. Brown, B. Forbes, G.P. Martin, Hyaluronan: biomedical, medical and clinical aspects, in: G.O.P.J. Kennedy, P.A. Williams, V. Hascall (Eds.), Woodhead Publishers, Cambridge, 2002, pp. 249-256.
71. S.K. Amr, The effect of homogenised skin on the activity of licosamde antibiotics, Proc Millen Cong Pharma Sci. (2000) A80.
72. T. Nazir, G.P. Martin, M.B. Brown, Dermal delivery of cyclosporin A entrapped liposomal gels- preformulation Franz cell diffusion studies using silastic membranes, Pharm Sci. 3 (2001) 14298 (suppl.).
73. Y.H. Liao, S.A. Jones, B. Forbes, G.P. Martin, M.B. Brown, Hyaluronan: pharmaceutical characterization and drug delivery, Drug Deliv. 12 (6) (2005) 327-342. (Pubitemid 41572107)
74. A. Takagi, N. Yamashita, T. Yoshioka, Y. Takaishi, K. Nakanishi, S. Takemura, A. Maeda, K. Saito, Y. Takakura, M. Hashida, Incorporation into a biodegradable hyaluronic acid matrix enhances in vivo efficacy of recombinant human interleukin 11 (rhIL11), J. Control. Release 115 (2) (2006) 134-139. (Pubitemid 44537497)
75. T. Segura, B.C. Anderson, P.H. Chung, R.E. Webber, K.R. Shull, L.D. Shea, Crosslinked hyaluronic acid hydrogels: a strategy to functionalize and pattern, Biomaterials 26 (4) (2005) 359-371. (Pubitemid 38951103)
76. M.R. Kim, T.G. Park, Temperature-responsive and degradable hyaluronic acid/pluronic composite hydrogels for controlled release of human growth hormone, J. Control. Release 80 (1-3) (2002) 69-77. (Pubitemid 34273749)
77. F. Lee, J.E. Chung, M. Kurisawa, An injectable hyaluronic acid-tyramine hydrogel system for protein delivery, J. Control. Release 134 (3) (2009) 186-193.
78. A.K. Silva, C. Richard, M. Bessodes, D. Scherman, O.W. Merten, Growth factor delivery approaches in hydrogels, Biomacromolecules 10 (1) (2009) 9-18.