Bovine lactoferrin structures promoting corneal epithelial wound healing in vitro

Investigative Ophthalmology and Visual Science

Volumn 52, Issue 5, 2011, Pages 2719-2726

  Ashby, Ben ^a,b   Qian, Garrett ^a,b,c   Mark, Willcox ^a,b,c  

^a BRIEN HOLDEN VISION INSTITUTE   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c VISION COOPERATIVE RESEARCH CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALI; BOVINE LACTOFERRIN; GLYCOPROTEIN; IRON; ISOPROTEIN; LACTOFERRICIN B; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CHROMATOGRAPHY; CONTROLLED STUDY; CORNEA EPITHELIUM; CORNEA LESION; ENZYME ACTIVITY; ENZYME SUBSTRATE; GLYCOSYLATION; HUMAN; HUMAN CELL; HYDROLYSIS; IN VITRO STUDY; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN PURIFICATION; WOUND HEALING;

BURNS, CHEMICAL; CELL CULTURE TECHNIQUES; CELL SURVIVAL; EPITHELIUM, CORNEAL; EYE BURNS; GLYCOSYLATION; HUMANS; LACTOFERRIN; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; PROTEIN ISOFORMS; WOUND HEALING;

EID: 79955991518     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.10-6352     Document Type: Article

References (61)

1. Suzuki K, Saito J, Yanai R, et al. Cell-matrix and cell-cell interactions during corneal epithelial wound healing. Progr Retinal Eye Res. 2003;22:113-133.
2. Lu L, Reinach PS, Kao WW. Corneal epithelial wound healing. Exp Biol Med. 2001;226:653-664.
3. Merle H, Gerard M, Schrage N. Ocular burns. J Fr Ophthalmol. 2008;31:723-734.
4. Brodovsky SC, McCarty CA, Snibson G, et al. Management of alkali burns: an 11-year retrospective review. Ophthalmology. 2000;107: 1829-1835.
5. Wagoner MD. Chemical injuries of the eye: current concepts in pathophysiology and therapy. Surv Ophthalmol. 1997;41:275-313.
6. Pattamatta U, Willcox M, Stapleton F, Cole N, Garrett Q. Bovine lactoferrin stimulates human corneal epithelial alkali wound healing in vitro. Invest Ophthalmol Vis Sci. 2009;50:1636-1643.
7. Bullen JJ, Rogers HJ, Leigh L. Iron-binding proteins in milk and resistance to Escherichia coli infection in infants. Br Med J. 1972; 1:69-75.
8. Yoo YC, Watanabe S, Watanabe R, Hata K, Shimazaki K, Azuma I. Bovine lactoferrin and lactoferricin, a peptide derived from bovine lactoferrin, inhibit tumor metastasis in mice. Jpn J Cancer Res. 1997;88:184-190.
9. Legrand D, Elass E, Carpentier M, Mazurier J. Lactoferrin: a modulator of immune and inflammatory responses. Cell Mol Life Sci. 2005;62:2549-2559.
10. Baker EN, Baker HM. A structural framework for understanding the multifunctional character of lactoferrin. Biochimie (Paris). 2009; 91:3-10.
11. Nishida T, Nakamura M, Mishima H, Otori T. Interleukin 6 promotes epithelial migration by a fibronectin-dependent mechanism. J Cell Physiol. 1992;153:1-5.
12. Kamiyama K, Iguchi I, Wang X, Imanishi J. Effects of PDGF on the migration of rabbit corneal fibroblasts and epithelial cells. Cornea. 1998;17:315-325.
13. Hynes RO. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992;69:11-25.
14. Saika S, Shiraishi A, Liu CY, et al. Role of lumican in the corneal epithelium during wound healing. J Biol Chem. 2000;275:2607-2612.
15. Kao WW, Kao CW, Kaufman AH, et al. Healing of corneal epithelial defects in plasminogen-and fibrinogen-deficient mice. Invest Ophthalmol Vis Sci. 1998;39:502-508.
16. Hayashi K, Berman M, Smith D, el-Ghatit A, Pease S, Kenyon KR. Pathogenesis of corneal epithelial defects: role of plasminogen activator. Curr Eye Res. 1991;10:381-398.
17. Alio JL, Ayala MJ, Mulet ME, Artola A, Ruiz JM, Bellot J. Antioxidant therapy in the treatment of experimental acute corneal inflammation. Ophthalmic Res. 1995;27:136-143.
18. Massucci MT, Giansanti F, Di Nino G, et al. Proteolytic activity of bovine lactoferrin. Biometals. 2004;17:249-255.
19. Baldwin DA, Jenny ER, Aisen P. The effect of human serum transferrin and milk lactoferrin on hydroxyl radical formation from superoxide and hydrogen peroxide. J Biol Chem. 1984;259: 13391-13394.
20. Vogel HJ, Schibli DJ, Jing W, Lohmeier-Vogel EM, Epand RF, Epand RM. Towards a structure-function analysis of bovine lactoferricin and related tryptophan-and arginine-containing peptides. Biochem Cell Biol. 2002;80:49-63.
21. Damiens E, El Yazidi I, Mazurier J, et al. Role of heparan sulphate proteoglycans in the regulation of human lactoferrin binding and activity in the MDA-MB-231 breast cancer cell line. Eur J Cell Biol. 1998;77:344-351.
22. Davidson LA, Lonnerdal B. Specific binding of lactoferrin to brushborder membrane: ontogeny and effect of glycan chain. Am J Physiol. 1988;254:G580-G585.
23. Cornish J, Palmano K, Callon KE, et al. Lactoferrin and bone: structure-activity relationships. Biochem Cell Biol. 2006;84:297-302.
24. Takayama Y, Mizumachi K, Takezawa T. The bovine lactoferrin region responsible for promoting the collagen gel contractile activity of human fibroblasts. Biochem Biophys Res Commun. 2002; 299:813-817.
25. Legrand D, Mazurier J, Metz-Boutigue MH, et al. Characterization and localization of an iron-binding 18-kDa glycopeptide isolated from the N-terminal half of human lactotransferrin. Biochim Biophys Acta. 1984;787:90-96.
26. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.
27. Ly L, Wasinger VC. Peptide enrichment and protein fractionation using selective electrophoresis. Proteomics. 2008;8:4197-4208.
28. You J, Fitzgerald A, Cozzi PJ, et al. Post-translation modification of proteins in tears. Electrophoresis. 2010;31:1853-1861.
29. Searle BC. Scaffold: a bioinformatic tool for validating MS/MS-based proteomic studies. Proteomics. 2010;10:1265-1269.
30. Powers JC, Asgian JL, Ekici ÖD, James KE. Irreversible inhibitors of serine, cysteine, and threonine proteases. Chem Rev. 2002;102: 4639-4750.
31. Sojar HT, Bahl OP. A chemical method for the deglycosylation of proteins. Arch Biochem Biophys. 1987;259:52-57.
32. Masson PL, Heremans JF. Metal-combining properties of human lactoferrin (red milk protein), 1: the involvement of bicarbonate in the reaction. Eur J Biochem. 1968;6:579-584.
33. Bates GW, Schlabach MR. The reaction of ferric salts with transferrin. J Biol Chem. 1973;248:3228-3232.
34. Castellino FJ, Fish WW, Mann KG. Structural studies on bovine lactoferrin. J Biol Chem. 1970;245:4269-4275.
35. Gipson IK, Spurr-Michaud S, Argueso P, Tisdale A, Ng TF, Russo CL. Mucin gene expression in immortalized human corneal-limbal and conjunctival epithelial cell lines. Invest Ophthalmol Vis Sci. 2003;44:2496-2506.
36. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65:55-63.
37. Ramphal R, McNiece MT, Polack FM. Adherence of Pseudomonas aeruginosa to the injured cornea: a step in the pathogenesis of corneal infections. Ann Ophthalmol. 1981;13:421-425.
38. Pierce A, Colavizza D, Benaissa M, et al. Molecular cloning and sequence analysis of bovine lactotransferrin. Eur J Biochem. 1991; 196:177-184.
39. Bellamy W, Takase M, Yamauchi K, Wakabayashi H, Kawase K, Tomita M. Identification of the bactericidal domain of lactoferrin. Biochim Biophys Acta. 1992;1121:130-136.
40. Ziere GJ, Kruijt JK, Bijsterbosch MK, van Berkel TJ. Recognition of lactoferrin and aminopeptidase M-modified lactoferrin by the liver: involvement of proteoglycans and the remnant receptor. Biochem J. 1996;313(pt 1):289-295.
41. Yoo YC, Watanabe R, Koike Y, et al. Apoptosis in human leukemic cells induced by lactoferricin, a bovine milk protein-derived peptide: involvement of reactive oxygen species. Biochem Biophys Res Commun. 1997;237:624-628.
42. Eliassen LT, Berge G, Sveinbjornsson B, Svendsen JS, Vorland LH, Rekdal O. Evidence for a direct antitumor mechanism of action of bovine lactoferricin. Anticancer Res. 2002;22:2703-2710.
43. Cejkova J, Lojda Z, Dropcova S, Kadlecova D. The histochemical pattern of mechanically or chemically injured rabbit cornea after aprotinin treatment: relationships with the plasmin concentration of the tear fluid. Histochem J. 1993;25:438-445.
44. Romer J, Lund LR, Eriksen J, Pyke C, Kristensen P, Dano K. The receptor for urokinase-type plasminogen activator is expressed by keratinocytes at the leading edge during re-epithelialization of mouse skin wounds. J Invest Dermatol. 1994;102:519-522.
45. Morimoto K, Mishima H, Nishida T, Otori T. Role of urokinase type plasminogen activator (u-PA) in corneal epithelial migration. Thromb Haemost. 1993;69:387-391.
46. Tillett WS, Garner RL. The fibrinolytic activity of hemolytic streptococci. J Exp Med. 1933;58:485-502.
47. Daniels JT, Limb GA, Saarialho-Kere U, Murphy G, Khaw PT. Human corneal epithelial cells require MMP-1 for HGF-mediated migration on collagen I. Invest Ophthalmol Vis Sci. 2003;44:1048-1055.
48. Odekon LE, Blasi F, Rifkin DB. Requirement for receptor-bound urokinase in plasmin-dependent cellular conversion of latent TGFbeta to TGF-beta. J Cell Physiol. 1994;158:398-407.
49. Plaut AG, Qiu J, St. Geme JW. Human lactoferrin proteolytic activity: analysis of the cleaved region in the IgA protease of Haemophilus influenzae. Vaccine. 2000;19:S148-S152.
50. Qiu J, Hendrixson DR, Baker EN, Murphy TF, St Geme JW 3rd, Plaut AG. Human milk lactoferrin inactivates two putative colonization factors expressed by Haemophilus influenzae. Proc Natl Acad Sci USA. 1998;95:12641-12646.
51. Hendrixson DR, Qiu J, Shewry SC, et al. Human milk lactoferrin is a serine protease that cleaves Haemophilus surface proteins at arginine-rich sites. Mol Microbiol. 2003;47:607-617.
52. Goodman RE, Schanbacher FL. Bovine lactoferrin mRNA: sequence, analysis, and expression in the mammary gland. Biochem Biophys Res Commun. 1991;180:75-84.
53. Teuwissen B, Masson PL, Osinski P, Heremans JF. Metalcombining properties of human lactoferrin: the effect of nitration of lactoferrin with tetranitromethane. Eur J Biochem. 1973;35:366-371.
54. Grossmann JG, Neu M, Pantos E, et al. X-ray solution scattering reveals conformational changes upon iron uptake in lactoferrin, serum and ovo-transferrins. J Mol Biol. 1992;225:811-819.
55. Wei Z, Nishimura T, Yoshida S. Characterization of glycans in a lactoferrin isoform, lactoferrin-a. J Dairy Sci. 2001;84:2584-2590.
56. Wei Z, Nishimura T, Yoshida S. Presence of a glycan at a potential N-glycosylation site, Asn-281, of bovine lactoferrin. J Dairy Sci. 2000;83:683-689.
57. Yoshida S, Wei Z, Shinmura Y, Fukunaga N. Separation of lactoferrin-a and-b from bovine colostrum. J Dairy Sci. 2000;83:2211-2215.
58. Baker EN. Structure and reactivity of transferrins. Adv Inorg Chem. 1994:389-463.
59. Moore SA, Anderson BF, Groom CR, Haridas M, Baker EN. Threedimensional structure of diferric bovine lactoferrin at 2.8 A resolution. J Mol Biol. 1997;274:222-236.
60. Garrett Q, Simmons PA, Xu S, et al. Carboxymethylcellulose binds to human corneal epithelial cells and is a modulator of corneal epithelial wound healing. Invest Ophthalmol Vis Sci. 2007;48: 1559-1567.
61. Nakagawa S, Nishida T, Kodama Y, Itoi M. Spreading of cultured corneal epithelial cells on fibronectin and other extracellular matrices. Cornea. 1990;9:125-130.