[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Log in

Evaluation of the protective effect of bovine lactoferrin against lipopolysaccharides in a bovine mammary epithelial cell line

  • Original Article
  • Published:
Veterinary Research Communications Aims and scope Submit manuscript

Abstract

Lactoferrin (Lf) is a non-haem iron-binding glycoprotein with a molecular weight of about 80 kDa, synthesized by glandular epithelial cells and stored in the secondary granules of neutrophils. The physiological significance of Lf is related to non-specific immune defence against pathogens, immunomodulatory activity, iron homeostasis, antioxidant properties and regulation of cell growth. Lf is a bioactive component of the mammary secretions and its modulatory and defensive functions do affect the newborn and the mammary gland as well. In this work a bovine mammary epithelial cell line (BME-UV1) was used as an in vitro model of the bovine mammary epithelium to examine the protective role of exogenous bovine Lf (bLf) against the cytotoxic damage induced by bacterial lipopolysaccharides (LPS) and the endogenous bLf mRNA expression after LPS exposure. In the in vitro model used, exogenous bLf exerts a protective effect against endotoxin cytotoxicity, which could be mediated by the LPS-neutralizing capability of bLf. In addition, in BME-UV1 cells the response to LPS exposure does not involve bLf mRNA expression, suggesting that this cell line lack of functional LPS-responsive elements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Appelmelk BJ, An YQ, Geerts M, Thijs BG, de Boer HA, MacLaren DM, de Graaff J, Nuijens JH (1994) Lactoferrin is a lipid A-binding protein. Infect Immun 62: 2628–2632.

    CAS  PubMed  Google Scholar 

  • Baker EN, Baker HM (2005) Molecular structure, binding properties and dynamics of lactoferrin. Cell Mol Life Sci 62: 2531–2539. doi:10.1007/s00018-005-5368-9.

    Article  CAS  PubMed  Google Scholar 

  • Baldi A, Savoini G, Cheli F, Fantuz F, Senatore E, Bertocchi L, Politis I (1996) Changes in plasmin-plasminogen-plasminogen activator system in milk from italian Fresian herds. Int Dairy J 6: 1045–1053. doi:10.1016/0958-6946(95)00075-5.

    Article  CAS  Google Scholar 

  • Baldi A, Losio MN, Cheli F, Rebucci R, Sangalli L, Fusi E, Bertasi B, Pavoni E, Carli S, Politis I (2004) Evaluation of the protective effects of alpha-tocopherol and retinol against ochratoxin A cytotoxicity. Br J Nutr 91: 507–12. doi:10.1079/BJN20041092.

    Article  CAS  PubMed  Google Scholar 

  • Baldi A, Politis I, Pecorini C, Fusi E, Roubini C, Dell’Orto V (2005) Biological effects of milk proteins and their peptides with emphasis on those related to the gastrointestinal ecosystem. J Dairy Res 72: 66–72.

    Article  CAS  PubMed  Google Scholar 

  • Baumrucker CR, Gibson CA, Schanbacher FL (2003) Bovine lactoferrin binds to insulin-like growth factor-binding protein-3. Domest Anim Endocrinol 24: 287–303. doi:10.1016/S0739-7240(03)00014-6.

    Article  CAS  PubMed  Google Scholar 

  • Baveye S, Elass E, Mazurier J, Legrand D (2000) Lactoferrin inhibits the binding of lipopolysaccharides to L-selectin and subsequent production of reactive oxygen species by neutrophils. FEBS Lett 469: 5–8. doi:10.1016/S0014-5793(00)01243-6.

    Article  CAS  PubMed  Google Scholar 

  • Boudjellab N, Chan-Tang HS, Li X, Zhao X (1998) Interleukin 8 response by bovine mammary epithelial cells to lipopolysaccharide stimulation. Am J Vet Res 59: 1563–1567.

    CAS  PubMed  Google Scholar 

  • Buommino E, Morelli F, Metafora S, Rossano F, Perfetto B, Baroni A, Tufano MA (1999) Porin from Pseudomonas aeruginosa induces apoptosis in an epithelial cell line derived from rat seminal vesicles. Infect Immun 67: 4794–4800.

    CAS  PubMed  Google Scholar 

  • Cheli F, Zavizion B, Todoulou O, Politis I (1999) The effect of calcium on mammary epithelial cell proliferation and the plasminogen activating system. Can J Anim Sci 79: 277–283. doi:10.4141/A99-001.

    Article  CAS  Google Scholar 

  • Cheli F, Politis I, Rossi L, Fusi E, Baldi A (2003) Effects of retinoids on proliferation and plasminogen activator expression in a bovine mammary epithelial cell line. J Dairy Res 70: 367-372. doi:10.1017/S0022029903006496.

    Article  CAS  PubMed  Google Scholar 

  • Elass-Rochard E, Roseanu A, Legrand D, Trif M, Salmon V, Motas C, Montreuil J, Spik G (1995) Lactoferrin-lipopolysaccharides interaction: involvement of the 28–34 loop region of human lactoferrin in the high-affinity binding to E. coli O55:B5 lipopolysaccharide. Biochem J 312: 839–845.

    CAS  PubMed  Google Scholar 

  • Fillebeen C, Ruchoux MM, Mitchell V, Vincent S, Benaïssa M, Pierce A (2001) Lactoferrin is synthesized by activated microglia in the human substantia nigra and its synthesis by the human microglial CHME cell line is upregulated by tumor necrosis factor alpha or 1-methyl-4-phenylpyridinium treatment. Brain Res Mol Brain Res 96: 103–113. doi:10.1016/S0169-328X(01)00216-9.

    Article  CAS  PubMed  Google Scholar 

  • Fusi E, Rossi L, Sangalli L, Pinotti L, Rebucci R, Cheli F (2002) Espressione dell’attivatore del plasminogeno di tipo urochinasico in cellule epiteliali di ghiandola mammaria bovina in coltura. Proceedings of LVI S.I.S.Vet., Giardini Naxos, Italy, 26–28 September, 405–406.

  • Hirotani Y, Ikeda K, Kato R, Myotoku M, Umeda T, Ijiri Y, Tanaka K (2008) Protective effects of lactoferrin against intestinal mucosal damage induced by lipopolysaccharide in human intestinal Caco-2 cells. Yakugaku Zasshi 128: 1363–1368. doi:10.1248/yakushi.128.1363.

    Article  CAS  PubMed  Google Scholar 

  • Jenssen H, Hancock REW (2009) Antimicrobial properties of lactoferrin. Biochimie 91: 19–29. doi:10.1016/j.biochi.2008.05.015.

    Article  CAS  PubMed  Google Scholar 

  • Kruzel ML, Harari Y, Chen CY, Castro GA (2000) Lactoferrin protects gut mucosal integrity during endotoxemia induced by lipopolysaccharide in mice. Inflammation 24: 33–44. doi:10.1023/A:1006935908960.

    Article  CAS  PubMed  Google Scholar 

  • Kruzel ML, Actor JK, Radak Z, Bacsi A, Saavedra-Molina A, Boldogh I (2009) Lactoferrin decreases LPS-induced mitochondrial dysfunction in cultured cells and in animal endotoxemia model. Innate Immun. doi:10.1177/1753425909105317.

    PubMed  Google Scholar 

  • Lacasse P, Lauzon K, Diarra MS, Petitclerc D (2008) Utilization of lactoferrin to fight antibiotic-resistant mammary gland pathogens. J Anim Sci 86: 66–71. doi:10.2527/jas.2007-0216.

    CAS  PubMed  Google Scholar 

  • Lee WJ, Farmer JL, Hilty M, Kim YB (1998) The protective effects of lactoferrin feeding against endotoxin lethal shock in germfree piglets. Infect Immun 66: 1421–1426.

    CAS  PubMed  Google Scholar 

  • Legrand D, van Berkel PH, Salmon V, van Veen HA, Slomianny MC, Nuijens JH, Spik G (1997) The N-terminal Arg2, Arg3 and Arg4 of human lactoferrin interact with sulphated molecules but not with the receptor present on Jurkat human lymphoblastic T-cells. Biochem J 327: 841–846.

    CAS  PubMed  Google Scholar 

  • Legrand D, Elass E, Carpentier M, Mazurier J (2006) Interactions of lactoferrin with cells involved in immune function. Biochem Cell Biol 84: 282–290. doi:10.1139/O06-045.

    Article  CAS  PubMed  Google Scholar 

  • Legrand D, Pierce A, Elass E, Carpentier M, Mariller C, Mazurier J (2008) Lactoferrin structure and functions. Adv Exp Med Biol 606: 163–194. doi:10.1007/978-0-387-74087-4.

    Article  PubMed  Google Scholar 

  • Li Y, Limmon GV, Imani F, Teng C (2009) Induction of lactoferrin gene expression by innate immune stimuli in mouse mammary epithelial HC-11 cells. Biochimie 91: 58–67. doi:10.1016/j.biochi.2008.04.014.

    Article  CAS  PubMed  Google Scholar 

  • Masson PL, Heremans JF, Dive CH (1966) An iron-binding protein common to many external secretions. Clin Chim Acta 14: 735–739.

    Article  CAS  Google Scholar 

  • Masson PL, Heremans JF, Schonne E (1969) Lactoferrin, an iron-binding protein in neutrophilic leukocytes. J Exp Med 130: 643–658.

    Article  CAS  PubMed  Google Scholar 

  • Neville MC, Zhang P (2000) Lactoferrin secretion into milk: comparison between ruminant, murine, and human milk. J Anim Sci 78: 26–35.

    Google Scholar 

  • Nuijens JH, van Berkel PHC, Schanbacher FL (1996) Structure and biological actions of lactoferrin. J Mammary Gland Biol Neoplasia 1: 285–295. doi:10.1007/BF02018081.

    Article  CAS  PubMed  Google Scholar 

  • Okada H, Ito T, Ohtsuka H, Kirisawa R, Iwai H, Yamashita K, Yoshino T, Rosol TJ (1997) Detection of interleukin-1 and interleukin-6 on cryopreserved bovine mammary epithelial cells in vitro. J Vet Med Sci 59: 503–507.

    Article  CAS  PubMed  Google Scholar 

  • Paesano R, Pietropaoli M, Gessani S, Valenti P (2009) The influence of lactoferrin, orally administered, on systemic iron homeostasis in pregnant women suffering of iron deficiency and iron deficiency anaemia. Biochimie 91: 44–51. doi:10.1016/j.biochi.2008.06.004.

    Article  CAS  PubMed  Google Scholar 

  • Panella TJ, Liu Y, Huang AT, Teng CT (1991) Polymorphism and altered methylation of the lactoferrin gene in normal leukocytes, leukemic cells, and breast cancer. Cancer Res 51: 3037–3043.

    CAS  PubMed  Google Scholar 

  • Pecorini C, Savazzini F, Martino PA, Fusi E, Fogher C, Baldi A (2005) Heterologous expression of biologically active porcine lactoferrin in Pichia pastoris yeast. Vet Res Commmun 29 Suppl. 2: 379–382. doi:10.1007/s11259-005-0086-1.

    Article  Google Scholar 

  • Pecorini C, Cheli F, Ollivier-Bousquet M, Baldi A (2006) Evaluation of biological activity of lactoferrin using in vitro models of intestinal and mammary epithelia. Revista de Ciências Veterinárias 4 (Suppl. 1): 5.

    Google Scholar 

  • Pecorini C, Delpal S, Truchet S, Le Provost F, Baldi A, Ollivier-Bousquet M (2009) Lactoferrin at basal side of mouse mammary epithelium derives in part from stroma cells. Cell Tissue Res 338: 241–255. doi:10.1007/s00441-009-0873-z.

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW, Wittmann SL, Meyer HHD, Bruckmaier RM (2003) Gene expression of immunologically important factors in blood cells, milk cells, and mammary tissue of cows. J Dairy Sci 86: 538–545.

    Article  CAS  Google Scholar 

  • Politis I (1996) Plasminogen activator system: implications for mammary cell growth and involution. J Dairy Sci 79: 1097–1107.

    Article  CAS  PubMed  Google Scholar 

  • Puddu P, Latorre D, Valenti P, Gessani S (2010) Immunoregulatory role of lactoferrin-lipopolysaccharide interactions. Biometals doi:10.1007/s10534-010-9307-3.

    Google Scholar 

  • Rabot A, Wellnitz O, Meyer HHD, Bruckmaier RM (2007) Use and relevance of a bovine mammary gland explant model to study infection responses in bovine mammary tissue. J Dairy Res 74: 93–99. doi:10.1017/S0022029906002147.

    Article  CAS  PubMed  Google Scholar 

  • Rainard P, Riollet C (2006) Innate immunity of the bovine mammary gland. Vet Res 37: 369–400. doi:10.1051/vetres:2006007.

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ pp 365–386.

    Google Scholar 

  • SAS (2001) User’s Guide: Statistics, Version 9.1 SAS Institute Inc., Cary, NC, USA.

  • Schmitz S, Pfaffl MW, Meyer HHD, Bruckmaier RM (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. doi:10.1016/j.domaniend.2003.09.003.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki YA, Lopez V, Lönnerdal B (2005) Mammalian lactoferrin receptors: structure and function. Cell Mol Life Sci 62: 2560–2575. doi:10.1007/s00018-005-5371-1.

    Article  CAS  PubMed  Google Scholar 

  • Talukder MJ, Harada E (2007) Bovine lactoferrin protects lipopolysaccharide-induced diarrhea modulating nitric oxide and prostaglandin E2 in mice. Can J Physiol Pharmacol 85: 200–208. doi:10.1139/Y07-004.

    Article  CAS  PubMed  Google Scholar 

  • Tian H, Maddox IS, Ferguson LR, Shu Q (2010) Evaluation of the cytoprotective effects of bovine lactoferrin against intestinal toxins using cellular model systems. Biometals doi:10.1007/s10534-010-9301-9.

    Google Scholar 

  • Valenti P, Antonini G (2005) Lactoferrin: an important host defence against microbial and viral attack. Cell Mo Life Sci 62: 2576–2587. doi:10.1007/s00018-005-5372-0.

    Article  CAS  Google Scholar 

  • Ward PP, Paz E, Conneely OM (2005) Multifunctional roles of lactoferrin: a critical overview. Cell Mol Life Sci 62: 2540–2548. doi:10.1007/s00018-005-5369-8.

    Article  CAS  PubMed  Google Scholar 

  • Wellnitz O, Kerr DE (2004) Cryopreserved bovine mammary cells to model epithelial response to infection. Vet Immunol Immunopathol 101: 191–202. doi:10.1016/j.vetimm.2004.04.019.

    Article  CAS  PubMed  Google Scholar 

  • Zavizion B, van Duffelen M, Schaeffer W, Politis I (1996) Establishment and characterization of a bovine mammary epithelial cell line with unique properties. In Vitro Cell Dev Biol Anim 32: 138–148. doi:10.1007/BF02723679.

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Ather JL, Sonstegard TS, Kerr DE (2005) Characterization of the infection-responsive bovine lactoferrin promoter. Gene 353: 107–117. doi:10.1016/j.gene.2005.04.016.

    Article  CAS  PubMed  Google Scholar 

  • Zheng J, Watson AD, Kerr DE (2006) Genome-wide expression analysis of lipopolysaccharide-induced mastitis in a mouse model. Infect Immun 74: 1907–1915. doi:10.1128/IAI.74.3.1907-1915.2006.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgement

This work was supported by Italian University and Research Grant PRIN 2007.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chiara Pecorini.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pecorini, C., Sassera, D., Rebucci, R. et al. Evaluation of the protective effect of bovine lactoferrin against lipopolysaccharides in a bovine mammary epithelial cell line. Vet Res Commun 34, 267–276 (2010). https://doi.org/10.1007/s11259-010-9351-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11259-010-9351-z

Keywords

Navigation