Evaluation of a highly skin permeable low-molecular-weight protamine conjugated epidermal growth factor for novel burn wound healing therapy

Journal of Pharmaceutical Sciences

Volumn 102, Issue 11, 2013, Pages 4109-4120

  Lee, Ji Hae ^a   Bae, Il Hong ^a   Choi, Jin Kyu ^b   Park, Jin Woo ^c  

^a AmorePacific Corporation   (South Korea)

^b Pacificpharma Corporation   (South Korea)

^c Mokpo National University   (South Korea)

Author keywords

Conjugation; Epithelial delivery permeability; Peptide delivery; Percutaneous; Permeability; Permeation enhancers; Protein delivery; Transdermal drug delivery; Wound healing

Indexed keywords

COLLAGEN; POLOXAMER; PROTAMINE; RECOMBINANT EPIDERMAL GROWTH FACTOR;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BURN SCAR; CELL PROLIFERATION; CONTROLLED STUDY; DRUG CONJUGATION; DRUG FORMULATION; DRUG PENETRATION; DRUG POTENTIATION; EPIDERMIS; EPITHELIUM CELL; FEMALE; HISTOPATHOLOGY; HYPERTROPHIC SCAR; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; SCAR FORMATION; SKIN IRRITATION; SKIN PENETRATION; SKIN PERMEABILITY; SKIN SENSITIZATION; WOUND HEALING;

CONJUGATION; EPITHELIAL DELIVERY/PERMEABILITY; PEPTIDE DELIVERY; PERCUTANEOUS; PERMEABILITY; PERMEATION ENHANCERS; PROTEIN DELIVERY; TRANSDERMAL DRUG DELIVERY; WOUND HEALING;

ANIMALS; BURNS; CELL PROLIFERATION; EPIDERMAL GROWTH FACTOR; FEMALE; HUMANS; MALE; MICE; MICE, INBRED BALB C; PROTAMINES; RABBITS; RECOMBINANT FUSION PROTEINS; SKIN; SKIN ABSORPTION; WOUND HEALING;

EID: 84885852187     PISSN: 00223549     EISSN: 15206017     Source Type: Journal    
DOI: 10.1002/jps.23725     Document Type: Article

References (60)

1. Jurjus A, Atiyeh BS, Abdallah IM, Jurjus RA, Hayek SN, Jaoude MA, Gerges A, Tohme RA. 2007. Pharmacological modulation of wound healing in experimental burns. Burns 33:892-907.
2. Tshukudu GM, van der Walt M, Wessels Q. 2010. Comparative in vitro study of honey based and silver based wound preparations on cell viability. Burns 36:1036-1041.
3. Jackson DM. 1953. The diagnosis of the depth of burning. Br J Surg 40:588-596.
4. Gillitzer R, Goebeler M. 2001. Chemokines in cutaneous wound healing. J Leukoc Biol 69:513-521.
5. Werner S, Grose R. 2003. Regulation of wound healing by growth factors and cytokines. Physiol Rev 83:835-870.
6. Goldman R. 2004. Growth factors and chronic wound healing: Past, present, and future. Adv Skin Wound Care 17:24-35.
7. Barrientos S, Stojadinovic O, Golinko MS, Brem H, Tomic-Canic M. 2008. Growth factors and cytokines in wound healing. Wound Repair Regen 16:585-601.
8. Behm B, Babilas P, Landthaler M, Schreml S. 2011. Cytokines, chemokines and growth factors in wound healing. J Eur Acad Dermatol Venereol 26:812-820.
9. Brown GL, Curtsinger LJ, White M, Mitchell RO, Pietsch J, Nordquist R, von Fraunhofer A, Schultz GS. 1988. Acceleration of tensile strength of incisions treated with EGF and TGF-β. Ann Surg 208:788-794.
10. Shah M, Foreman DM, Ferguson MW. 1992. Control of scarring in adult wounds by neutralizing antibody to transforming growth factor beta. Lancet 339:213-214.
11. Nissen NN, Polverini PJ, Koch AE, Volin MV, Gamelli RL, DiPietro LA. 1998. Vascular endothelial growth factor mediates angiogenic activity during the proliferative phase of wound healing. Am J Pathol 152:1445-1452.
12. Smiell JM, Wieman TJ, Steed DL, Perry BH, Sampson AR, Schwab BH. 1999. 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 7:335-346.
13. Kawai K, Suzuki S, Tabata Y, Ikada Y, Nishimura Y. 2000. Accelerated tissue regeneration through incorporation of basic fibroblast growth factor-impregnated gelatin microspheres into artificial dermis. Biomaterials 21:489-499.
14. Falanga V, Eaglstein WH, Bucalo B, Katz MH, Harris B, Carson P. 1992. Topical use of human recombinant epidermal growth factor (h-EGF) in venous ulcers. J Dermatol Surg Oncol 18:604-606.
15. Da Costa RM, Ribeiro Jesus FM, Aniceto C, Mendes M. 1999. Randomized, double-blind, placebo-controlled, dose-ranging study of granulocyte-macrophage colony stimulating factor in patients with chronic venous leg ulcers. Wound Repair Regen 7:17-25.
16. Møller S, Jensen M, Svensson P, Skakkebaek NE. 1991. Insulin-like growth factor 1 (IGF-1) in burn patients. Burns 17:279-281.
17. McCarthy DW, Downing MT, Brigstock DR, Luquette MH, Brown KD, Abad MS, Besner GE. 1996. Production of heparin-binding epidermal growth factor-like growth factor (Hb-EGF) at sites of thermal injury in pediatric patients. J Invest Dermatol 106:49-56.
18. Fu X, Shen Z, Chen Y, Xie J, Guo Z, Zhang M, Sheng Z. 1998. Randomised placebo-controlled trial of use of topical recombinant bovine basic fibroblast growth factor for second-degree burns. Lancet 352:1661-1664.
19. Cohen S, Carpenter G. 1975. Human epidermal growth factor: Isolation and chemical and biological properties. Proc Natl Acad Sci USA 72:1317.
20. Rheinwald JG, Green H. 1977. Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature 265:421.
21. Franklin JD, Lynch JB. 1979. Effects of topical applications of epidermal growth factor on wound healing. Plast Reconstr Surg 64:766-770.
22. Thornton JW, Hess CA, Cassingham V, Bartlett RH. 1981. Epidermal growth factor in the healing of second degree burns: A controlled animal study. Burns 8:156.
23. Niall M, Ryan GB, O'Brien BM. 1982. The effect of epidermal growth factor on wound healing in mice. J Surg Res 33:164-169.
24. Arturson G. 1984. Epidermal growth factor in the healing of corneal wounds, epidermal wounds and partial-thickness scalds. Scand J Plast Reconstr Surg 18:33-37.
25. Brown GL, Nanney LB, Griffen J, Cramer AB, Yancey JM, Curtsinger LJ 3rd, Holtzin L, Schultz GS, Jurkiewicz MJ, Lynch JB. 1989. Enhancement of wound healing by topical treatment of epidermal growth factor. N Engl J Med 321:76-79.
26. Chen RR, Mooney DJ. 2003. Polymeric growth factor delivery strategies for tissue engineering. Pharm Res 20:1103-1112.
27. Hardwicke J, Schmaljohann D, Boyce D, Thomas D. 2008. Epidermal growth factor therapy and wound healing-past, present and future perspectives. Surgeon 6:172-177.
28. Yang CH. 2008. Evaluation of the release rate of bioactive recombinant human epidermal growth factor from crosslinking collagen sponges. J Mater Sci Mater Med 19:1433-1440.
29. Buckley A, Davidson JM, Kamerath CD, Wolt TB, Woodward SC. 1985. Sustained release of epidermal growth factor accelerates wound repair. Proc Natl Acad Sci USA 82:7340-7344.
30. Alemdaroǧlu C, Deǧim Z, Celebi N, Zor F, Oztürk S, Erdoǧan D. 2006. An investigation on burn wound healing in rats with chitosan gel formulation containing epidermal growth factor. Burns 2006:319-327.
31. Choi JS, Leong KW, Yoo HS. 2008. In vivo wound healing of diabetic ulcers using eletrospun nanofibers immobilized with human epidermal growth factor (EGF). Biomaterials 29:587-596.
32. Ulubayram K, Nur Cakar A, Korkusuz P, Ertan C, Hasirci N. 2001. EGF containing gelatin-based wound dressing. Biomaterials 22:1345-1356.
33. Xie Y, Upton Z, Richards S, Rizzi SC, Leavesley DI. 2011. Hyaluronic acid: Evaluation as a potential delivery vehicle for vitronectin: Growth factor complexes in wound healing applications. J Control Release 153:225-232.
34. Johnson NR, Wang Y. 2013. Controlled delivery of heparin-biding EGF-like growth factor yields fast and comprehensive wound healing. J Control Release 166:124-129.
35. Cho Lee AR, Leem H, Lee J, Park KC. 2005. Reversal of silver sulfadiazine-impaired wound healing by epidermal growth factor. Biomaterials 26:4670-4676.
36. Breuing K, Andree C, Helo G, Slama J, Liu PY, Eriksson E. 1997. Growth factors in the repair of partial thickness porcine skin wounds. Plast Reconstr Surg 100:657-664.
37. Greaves MW. 1980. Lack of effect of topically applied epidermal growth factor (EGF) on epidermal growth in man in vivo. Clin Exp Dermatol 5:101-103.
38. Choi JK, Jang JH, Jang WH, Kim J, Bae IH, Bae J, Park YH, Kim BJ, Lim KM, Park JW. 2012. The effect of epidermal growth factor (EGF) conjugated with low-molecular-weight protamine (LMWP) on wound healing of the skin. Biomaterials 33:8579-8590.
39. Jiang CK, Magnaldo T, Ohtsuki M, Freedberg IM, Bernerd F, Blumenberg M. 1993. Epidermal growth factor and transforming growth factor α specifically induce the activation- and hyperproliferation-associated keratins 6 and 16. Proc Natl Acad Sci USA 90:6786-6790.
40. Kiyohara Y, Nishiguchi K, Komada F, Iwakawa S, Hirai M, Okumura K. 1993. Cytoprotective effects of epidermal growth factor (EGF) ointment containing nafamostat, a protease inhibitor, on tissue damage at burn site rats. Bio Pharm Bull 16:1146-1149.
41. Gönül B, Erdoǧan D, Ozoǧul C, Koz M, Babül A, Celebi N. 1995. Effect of EGF dosage forms on alkali burned corneal wound healing mice. Burns 21:7-10.
42. Hashimoto K, Higashiyama S, Asada H, Hashimura E, Kobayashi T, Sudo K, Nakagawa T, Damm D, Yoshikawa K, Taniguchi N. 1999. Heparin-binding epidermal growth factor-like growth factor is an autocrine growth factor for human keratinocytes. J Biol Chem 269:20060-20066.
43. Shirakata Y, Komurasaki T, Toyoda H, Hanakawa Y, Yamasaki K, Tokumaru S, Sayama K, Hashimoto K. 2000. Epiregulin, a novel member of the epidermal growth factor family, is an autocrine growth factor in normal human keratinocytes. J Biol Chem 275:5748-5753.
44. Ohtake K, Maeno T, Ueda H, Natsume H, Morimoto Y. 2003. Poly-l-arginine predominantly increases the paracellular permeability of hydrophilic macromolecules across rabbit nasal epithelium in vitro. Pharm Res 20:153-160.
45. Morita K, Myachi Y. 2003. Tight junctions in the skin. J Dermatol Sci 31:81-89.
46. Thorén PE, Persson D, Esbjörner EK, Goksör M, Lincoln P, Nordén B. 2004. Membrane binding and translocation of cell penetrating peptides. Biochemistry 43:3471-3489.
47. Sharma V, Stebe K, Murphy JC, Tung L. 1996. Poloxamer 188 decreases susceptibility of artificial lipid membranes to electroporation. Biophys J 71:3229-3241.
48. Curry DJ, Wright DA, Lee RC, Kang UJ, Frim DM. 2004. Surfactant poloxamer 188-related decreases in inflammation and tissue damage after experimental brain injury in rats. J Neurosurg 101:91-96.
49. Williams AC, Barry BW. 2004. Penetration enhancers. Adv Drug Deliv Rev 56:603-618.
50. Ward RS, Saffle JR. 1995. Topical agents in burn and wound care. Phys Ther 75:526-538.
51. Manafi A, Hashemlou A, Momeni P, Moghimi HR. 2008. Enhanced drugs absorption through third-degree burn wound eschar. Burns 34:698-702.
52. Rockwell WB, Cohen IK, Ehrlich HP. 1989. Keloids and hypertrophic scars: A comprehensive review. Plast Reconstr Surg 84:827-837.
53. Anderson RR, Parrish JA. 1981. The optics of human skin. J Invest Dermatol 77:13-19.
54. Amadeu T, Braune A, Mandarim-de-Lacerda C, Porto LC, Desmoulière A, Costa A. 2003. Vascularization pattern in hypertrophic scars and keloids: A stereological analysis. Pathol Res Pract 199:469-473.
55. Torkian BA, Yeh AT, Engel R, Sun CH, Tromberg BJ, Wong BJ. 2004. Modeling aberrant wound healing using tissue-engineered skin constructs and multiphoton microscopy. Arch Facial Plast Surg 6:180-187.
56. Laws RA, Finley EM, McCollough ML, Grabski WJ. 1998. Alabaster skin after carbon dioxide laser resurfacing with histologic correlation. Dermatol Surg 24:633-636.
57. Ayhan S, Baran CN, Yavuzer R, Latifoglu O, Cenetoglu S, Baran NK. 1998. Combined chemical peeling and dermabrasion for deep acne and posttraumatic scars as well as aging face. Plast Reconstr Surg 102:1238-1246.
58. Sadick NS. 2005. Combination radiofrequency and light energies: Electro-optical synergy technology in esthetic medicine. Dermatol Surg 31:1211-1217.
59. Aust MC, Fernandes D, Kolokythas P, Kaplan HM, Vogt PM. 2008. Percutaneous collagen induction therapy: An alternative treatment for scars, wrinkles, and skin laxity. Plast Reconstr Surg 121:1421-1429.
60. Aust MC, Knobloch K, Reimers K, Redeker J, Ipaktchi R, Altintas MA, Gohritz A, Schwaiger N, Vogt PM. 2010. Percutaneous collagen induction therapy: An alternative treatment for burn scars. Burns 36:836-843.