Transgenic cows that produce recombinant human lactoferrin in milk are not protected from experimental Escherichia coli intramammary infection

Infection and Immunity

Volumn 74, Issue 11, 2006, Pages 6206-6212

  Hyvonen P ^a   Suojala, L ^b   Orro, T ^b   Haaranen, J ^a   Simola, O ^b   Rontved C ^c   Pyorala S ^b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c DANISH INSTITUTE OF AGRICULTURAL SCIENCES   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEIN; HAPTOGLOBIN; HYDROCORTISONE; LACTOFERRIN; LIPOPOLYSACCHARIDE; RECOMBINANT HUMAN LACTOFERRIN; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COUNT; BACTERIAL STRAIN; CONTROLLED STUDY; DAIRY CATTLE; ENTEROBACTER INFECTION; ESCHERICHIA COLI; GENETIC ENGINEERING; HYDROCORTISONE BLOOD LEVEL; IMMUNOMODULATION; INFLAMMATION; MASTITIS; MILK; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CATTLE; ESCHERICHIA COLI; ESCHERICHIA COLI INFECTIONS; FEMALE; HUMANS; MASTITIS, BOVINE; RECOMBINANT PROTEINS;

EID: 33750477003     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00238-06     Document Type: Article

References (58)

1. Alsemgeest, S. P., H. C. Kalsbeek, T. Wensing, J. P. Koeman, A. M. van Ederen, and E. Gruys. 1994. Concentrations of serum amyloid-A (SAA) and haptoglobin (HP) as parameters of inflammatory diseases in cattle. Vet. Q. 16:21-23.
2. Baker, H. M., and E. N. Baker. 2004. Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals 17:209-216.
3. Bannerman, D. D., M. J. Paape, J. W. Lee, X. Zhao, J. C. Hope, and P. Rainard. 2004. Escherichia coli and Staphylococcus aureus elicit differential innate immune responses following intramammary infection. Clin. Diagn. Lab. Immunol. 11:463-472.
4. Baumann, H., and J. Gauldie. 1994. The acute phase response. Immunol. Today 15:74-80.
5. Blum, J. W., H. Dosogne, D. Hoeben, F. Vangroenweghe, H. M. Hammon, R. M. Bruckmaier, and C. Burvenich. 2000. Tumor necrosis factor-alpha and nitrite/nitrate responses during acute mastitis induced by Escherichia coli infection and endotoxin in dairy cows. Domest. Anim. Endocrinol. 19:223-235.
6. Brink, M. F., M. D. Bishop, and F. R. Pieper. 2000. Developing efficient strategies for the generation of transgenic cattle which produce biopharmaceuticals in milk. Theriogenology 53:139-148.
7. Brock, J. H. 2002. The physiology of lactoferrin. Biochem. Cell Biol. 80:1-6.
8. Burvenich, C., V. Van Merris, J. Mehrzad, A. Diez-Fraile, and L. Duchateau. 2003. Severity of E. coli mastitis is mainly determined by cow factors. Vet. Res. 34:521-564.
9. Carstensen, L., C. M. Rontved, and J. P. Nielsen. 2005. Determination of tumor necrosis factor-alpha responsiveness in piglets around weaning using an ex vivo whole blood stimulation assay. Vet. Immunol. Immunopathol. 105:59-66.
10. Crouch, S. P., K. J. Slater, and J. Fletcher. 1992. Regulation of cytokine release from mononuclear cells by the iron-binding protein lactoferrin. Blood 80:235-240.
11. Diarra, M. S., D. Petitclerc, and P. Lacasse. 2002. Effect of lactoferrin in combination with penicillin on the morphology and the physiology of Staphylococcus aureus isolated from bovine mastitis. J. Dairy Sci. 85:1141-1149.
12. Dingwell, R. T., K. E. Leslie, Y. H. Schukken, J. M. Sargeant, L. L. Timms, T. F. Duffield, G. P. Keefe, D. F. Kelton, K. D. Lissemore, and J. Conklin. 2004. Association of cow and quarter-level factors at drying-off with new intramammary infections during the dry period. Prev. Vet. Med. 63:75-89.
13. Dionysius, D. A., P. A. Grieve, and J. M. Milne. 1993. Forms of lactoferrin: their antibacterial effect on enterotoxigenic Escherichia coli. J. Dairy Sci. 76:2597-2606.
14. Elass-Rochard, E., A. Roseanu, D. Legrand, M. Trif, V. Salmon, C. Motas, J. Montreuil, and G. Spik. 1995. Lactoferrin-lipopolysaccharide interaction: involvement of the 28-34 loop region of human lactoferrin in the high-affinity binding to Escherichia coli 055B5 lipopolysaccharide. Biochem. J. 312:839-845.
15. Farnaud, S., A. Patel, E. W. Odell, and R. W. Evans. 2004. Variation in antimicrobial activity of lactoferricin-derived peptides explained by structure modelling. FEMS Microbiol. Lett. 238:221-226.
16. Golodetz, C. L., and M. E. White. 1983. Prognosis for cows with severe clinical coliform mastitis. Vet. Rec. 112:402-403.
17. Hagiwara, S., K. Kawai, A. Ann, and H. Nagahata. 2003. Lactoferrin concentrations in milk from normal and subclinical mastitic cows. J. Vet. Med. Sci. 65:319-323.
18. Harmon, R. J., F. L. Schanbacher, L. C. Ferguson, and K. L. Smith. 1976. Changes in lactoferrin, immunoglobulin G, bovine serum albumin, and alpha-lactalbumin during acute experimental and natural coliform mastitis in cows. Infect. Immun. 13:533-542.
19. Haversen, L., B. G. Ohlsson, M. Hahn-Zoric, L. A. Hanson, and I. Mattsby-Baltzer. 2002. Lactoferrin down-regulates the LPS-induced cytokine production in monocytic cells via NF-kappa B. Cell. Immunol. 220:83-95.
20. Hirvonen, J., K. Eklund, A. M. Teppo, G. Huszenicza, M. Kulcsar, H. Saloniemi, and S. Pyorala. 1999. Acute phase response in dairy cows with experimentally induced Escherichia coli mastitis. Acta Vet. Scand. 40:35-46.
21. Hiss, S., M. Mielenz, R. M. Bruckmaier, and H. Sauerwein. 2004. Haptoglobin concentrations in blood and milk after endotoxin challenge and quantification of mammary Hp mRNA expression. J. Dairy Sci. 87:3778-3784.
22. Hyvönen, P., L. Suojala, J. Haaranen, A. von Wright, and S. Pyörälä. 2006. Human and bovine lactoferrins in the milk of recombinant human lactoferrin-transgenic dairy cows during lactation. Biotechnol. J. 1:410-412.
23. Jackson, J. A., D. E. Shuster, W. J. Silvia, and R. J. Harmon. 1990. Physiological responses to intramammary or intravenous treatment with endotoxin in lactating dairy cows. J. Dairy Sci. 73:627-632.
24. Kai, K., Y. Komine, K. Komine, K. Asai, T. Kuroishi, T. Kozutsumi, M. Itagaki, M. Ohta, and K. Kumagai. 2002. Effects of bovine lactoferrin by the intramammary infusion in cows with staphylococcal mastitis during the early non-lactating period. J. Vet. Med. Sci. 64:873-878.
25. Kawai, K., S. Hagiwara, A. Anri, and H. Nagahata. 1999. Lactoferrin concentration in milk of bovine clinical mastitis. Vet. Res. Commun. 23:391-398.
26. Kawai, K., H. Nagahata, N. Y. Lee, A. Anri, and K. Shimazaki. 2003. Effect of infusing lactoferrin hydrolysate into bovine mammary glands with subclinical mastitis. Vet. Res. Commun. 27:539-548.
27. Kerr, D. E., K. Plaut, A. J. Bramley, C. M. Williamson, A. J. Lax, K. Moore, K. D. Wells, and R. J. Wall. 2001. Lysostaphin expression in mammary glands confers protection against staphylococcal infection in transgenic mice. Nat. Biotechnol. 19:66-70.
28. Kitchen, B. J., G. Middleton, and M. Salmon. 1978. Bovine milk N-acetyl-beta-D-glucosaminidase and its significance in the detection of abnormal udder secretions. J. Dairy Res. 45:15-20.
29. Komine, K., Y. Komine, T. Kuroishi, J. Kobayashi, Y. Obara, and K. Kumagai. 2005. Small molecule lactoferrin with an inflammatory effect but no apparent antibacterial activity in mastitic mammary gland secretion. J. Vet. Med. Sci. 67:667-677.
30. Kossaibati, M. A., M. Hovi, and R. J. Esslemont. 1998. Incidence of clinical mastitis in dairy herds in England. Vet. Rec. 143:649-653.
31. Krimpenfort, P., A. Rademakers, W. Eyestone, A. van der Schans, S. van den Broek, P. Kooiman, E. Kootwijk, G. Platenburg, F. Pieper, and R. Strijker. 1991. Generation of transgenic dairy cattle using 'in vitro' embryo production. Biotechnology (New York) 9:844-847.
32. Kutila, T., S. Pyorala, H. Saloniemi, and L. Kaartinen. 2003. Antibacterial effect of bovine lactoferrin against udder pathogens. Acta Vet. Scand. 44:35-42.
33. Kutila, T., L. Suojala, T. Lehtolainen, H. Saloniemi, L. Kaartinen, M. Tahti, K. Seppala, and S. Pyorala. 2004. The efficacy of bovine lactoferrin in the treatment of cows with experimentally induced Escherichia coli mastitis. J. Vet. Pharmacol. Ther. 27:197-202.
34. Lee, N. Y., K. Kawai, I. Nakamura, T. Tanaka, H. Kumura, and K. Shimazaki. 2004. Susceptibilities against bovine lactoferrin with microorganisms isolated from mastitic milk. J. Vet. Med. Sci. 66:1267-1269.
35. Legrand, D., V. Salmon, B. Goddeville, M. Benaissa, Y. Plancke, and G. Spik. 1997. Structural determination of two N-linked glycans isolated from recombinant human lactoferrin expressed in BHK* cells, p. 111-117. In T. W. Hutchens and B. Lönnerdal (ed.), Lactoferrin. Interactions and biological functions. Humana Press, Totowa, NJ.
36. Legrand, D., E. Elass, M. Carpentier, and J. Mazurier. 2005. Lactoferrin: a modulator of immune and inflammatory responses. Cell Mol. Life Sci. 62:2549-2559.
37. Legrand, D., E. Elass, A. Pierce, and J. Mazurier. 2004. Lactoferrin and host defence: an overview of its immuno-modulating and anti-inflammatory properties. Biometals 17:225-229.
38. Lehtolainen, T., C. Rontved, and S. Pyorala. 2004. Serum amyloid A and TNF-α in serum and milk during experimental endotoxin mastitis. Vet. Res. 35:651-659.
39. Maga, E. A. 2005. Genetically engineered livestock: closer than we think? Trends Biotechnol. 23:533-535.
40. Makimura, S., and N. Suzuki. 1982. Quantitative determination of bovine serum haptoglobin and its elevation in some inflammatory diseases. Nippon Juigaku Zasshi 44:15-21.
41. Mattila, T., and M. Sandholm. 1985. Antitrypsin and N-acetyl-beta-D- glucosaminidase as markers of mastitis in a herd of Ayrshire cows. Am. J. Vet. Res. 46:2453-2456.
42. Molenaar, A. J., Y. M. Kuys, S. R. Davis, R. J. Wilkins, P. E. Mead, and J. W. Tweedie. 1996. Elevation of lactoferrin gene expression in developing, ductal, resting, and regressing parenchymal epithelium of the ruminant mammary gland. J. Dairy Sci. 79:1198-1208.
43. Na, Y. J., S. B. Han, J. S. Kang, Y. D. Yoon, S. K. Park, H. M. Kim, K. H. Yang, and C. O. Joe. 2004. Lactoferrin works as a new LPS-binding protein in inflammatory activation of macrophages. Int. Immunopharmacol. 4:1187-1199.
44. Nuijens, J. H. 1993. A strategy to increase resistance in dairy cows. IDF Mastitis News 134:16-18.
45. Nuijens, J. H, P. H. van Berkel, M. E. Geerts, P. P. Hartevelt, H. A. de Boer, H. A. van Veen, and F. R. Pieper. 1997. Characterization of recombinant human lactoferrin secreted in milk of transgenic mice. J. Biol. Chem. 272:8802-8807.
46. Prgomet, C., H. Sarikaya, R. M. Bruckmaier, and M. W. Pfaffl. 2005. Short-term effects on pro-inflammatory cytokine, lactoferrin and CD14 mRNA expression levels in bovine immunoseparated milk and blood cells treated by LPS. J. Vet. Med. A 52:317-324.
47. Pyorala, S., L. Kaartinen, H. Kack, and V. Rainio. 1994. Efficacy of two therapy regimens for treatment of experimentally induced Escherichia coli mastitis in cows. J. Dairy Sci. 77:453-461.
48. Sanchez, L., P. Aranda, M. D. Perez, and M. Calvo. 1988. Concentration of lactoferrin and transferrin throughout lactation in cow's colostrum and milk. Biol. Chem. Hoppe-Seyler 369:1005-1008.
49. Schanbacher, F. L., R. E. Goodman, and R. S. Talhouk. 1993. Bovine mammary lactoferrin: implications from messenger ribonucleic acid (mRNA) sequence and regulation contrary to other milk proteins. J. Dairy Sci. 76:3812-3831.
50. Schmitz, S., M. W. Pfaffl, H. H. Meyer, and R. M. Bruckmaier. 2004. Short-term changes of mRNA expression of various inflammatory factors and milk proteins in mammary tissue during LPS-induced mastitis. Domest. Anim. Endocrinol. 26:111-126.
51. Shpigel, N. Y., D. Levin, M. Winkler, A. Saran, G. Ziv, and A. Bottner. 1997. Efficacy of cefquinome for treatment of cows with mastitis experimentally induced using Escherichia coli. J. Dairy Sci. 80:318-323.
52. Sordillo, L. M., and K. L. Streicher. 2002. Mammary gland immunity and mastitis susceptibility. J. Mammary Gland Biol. Neoplasia 7:135-146.
53. Thomassen, E. A., H. A. van Veen, P. H. van Berkel, J. H. Nuijens, and J. P. Abrahams. 2005. The protein structure of recombinant human lactoferrin produced in the milk of transgenic cows closely matches the structure of human milk-derived lactoferrin. Transgenic Res. 14:397-405.
54. van Berkel, P. H., H. A. van Veen, M. E. Geerts, H. A. de Boer, and J. H. Nuijens. 1996. Heterogeneity in utilization of N-glycosylation sites Asn624 and Asn138 in human lactoferrin: a study with glycosylation-site mutants. Biochem. J. 319:117-122.
55. van Berkel, P. H., M. M. Welling, M. Geerts, H. A. van Veen, B. Ravensbergen, M. Salaheddine, E. K. Pauwels, F. Pieper, J. H. Nuyens, and P. H. Nibbering. 2002. Large scale production of recombinant human lactoferrin in the milk of transgenic cows. Nat. Biotechnol. 20:484-487.
56. Wall, R. J., A. M. Powell, M. J. Paape, D. E. Kerr, D. D. Bannerman, V. G. Pursel, K. D. Wells, N. Talbot, and H. W. Hawk. 2005. Genetically enhanced cows resist intramammary Staphylococcus aureus infection. Nat. Biotechnol. 23:445-451.
57. Ward, P. P., S. Uribe-Luna, and O. M. Conneely. 2002. Lactoferrin and host defense. Biochem. Cell Biol. 80:95-102.
58. Welty, F. K., K. L. Smith, and F. L. Schanbacher. 1976. Lactoferrin concentration during involution of the bovine mammary gland. J. Dairy Sci. 59:224-231.