Skip to main content

Advertisement

Log in

Antirotaviral potential of lactoferrin from different origin: effect of thermal and high pressure treatments

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Rotaviral gastroenteritis causes a high rate of infant mortality and severe healthcare implications worldwide. Several studies have pointed out that human milk and dairy fractions, such as whey and buttermilk, possess antirotaviral activity. This activity has been mainly associated with glycoproteins, among them lactoferrin (LF). Thermal treatments are necessary to provide microbiological safety and extend the shelf life of milk products, though they may diminish their biological value. High hydrostatic pressure (HHP) treatment is a non-thermal method that causes lower degradation of food components than other treatments. Thus, the main objective of this study was to prove the antirotaviral activity of LFs from different origin and to evaluate the effect of several thermal and HHP treatments on that activity. LF exerted a high antirotaviral activity, regardless of its origin. Native LFs from bovine, ovine, swine and camel milk, and the human recombinant forms, at 1 mg/mL, showed neutralizing values in the range 87.5–98.6%, while human LF neutralized 58.2%. Iron saturation of bovine LF did not modify its antirotaviral activity. Results revealed interspecies differences in LFs heat susceptibility. Thus, pasteurization at 63 °C for 30 min led to a decrease of 60.1, 44.5, 87.1, 3.8 and 8% of neutralizing activity for human, bovine, swine, ovine and camel LFs, respectively. Pasteurization at 75 °C for 20 s was less harmful to the activity of LFs, with losses ranging from 0 to 13.8%. HHP treatment at 600 MPa for 15 min did not cause any significant decrease in the neutralizing activity of LFs.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Arias CF, Romero P, Alvarez V, López S (1996) Trypsin activation pathway of rotavirus infectivity. J Virol 70:5832–5839

    PubMed  PubMed Central  CAS  Google Scholar 

  • Arias CF, Silva-Ayala D, Isa P et al (2016) Rotavirus attachment, internalization, and vesicular traffic. In: Svensson L, Desselberger U, Greenberg HB, Estes MK (eds) Viral gastroenteritis. Molecular epidemiology and pathogenesis. Academic Press, Cambridge, pp 103–119

    Google Scholar 

  • Arnold M, Patton JT, McDonald SM (2009) Culturing, storage, and quantification of rotaviruses. Curr Protoc Microbiol 15:15C.3.1–15C.3.24

    Article  Google Scholar 

  • Arslanoglu S, Bertino E, Tonetto P et al (2010) Guidelines for the establishment and operation of a donor human milk bank. J Matern Neonatal Med 23:1–20

    Article  Google Scholar 

  • Asensi MT, Martínez-Costa C, Buesa J (2006) Anti-rotavirus antibodies in human milk: quantification and neutralizing activity. J Pediatr Gastroenterol Nutr 42:560–567

    Article  PubMed  CAS  Google Scholar 

  • Berlutti F, Pantanella F, Natalizi T et al (2011) Antiviral properties of lactoferrin: a natural immunity molecule. Molecules 16:6992–7018

    Article  PubMed  CAS  Google Scholar 

  • Bojsen A, Buesa J, Montava R et al (2007) Inhibitory activities of bovine macromolecular whey proteins on rotavirus infections in vitro and in vivo. J Dairy Sci 90:66–74

    Article  PubMed  CAS  Google Scholar 

  • Chawla R, Patil GR, Singh AK (2011) High hydrostatic pressure technology in dairy processing: a review. J Food Sci Technol 48:260–268

    Article  PubMed  Google Scholar 

  • Claeys WL, Verraes C, Cardoen S et al (2014) Consumption of raw or heated milk from different species: an evaluation of the nutritional and potential health benefits. Food Control 42:188–201

    Article  Google Scholar 

  • Conesa C, Rota MC, Pérez MD et al (2008a) Antimicrobial activity of recombinant human lactoferrin from Aspergillus awamori, human milk lactoferrin and their hydrolysates. Eur Food Res Technol 228:205–211

    Article  CAS  Google Scholar 

  • Conesa C, Sánchez L, Rota C et al (2008b) Isolation of lactoferrin from milk of different species: calorimetric and antimicrobial studies. Comp Biochem Physiol 150:131–139

    Article  CAS  Google Scholar 

  • Das JK, Salam RA, Bhutta ZA (2014) Global burden of childhood diarrhea and interventions. Curr Opin Infect Dis 27:451–458

    Article  PubMed  Google Scholar 

  • Egashira M, Takayanagi T, Moriuchi M, Moriuchi H (2007) Does daily intake of bovine lactoferrin-containing products ameliorate rotaviral gastroenteritis? Acta Paediatr 96:1242–1244

    Article  PubMed  Google Scholar 

  • El Agamy ESI, Ruppanner R, Ismail A et al (1992) Antibacterial and antiviral activity of camel milk protective proteins. J Dairy Res 59:169–175

    Article  PubMed  Google Scholar 

  • El-Fakharany EM, Sánchez L, Al-Mehdar HA, Redwan EM (2013) Effectiveness of human, camel, bovine and sheep lactoferrin on the hepatitis C virus cellular infectivity: comparison study. Virol J 10:199–209

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Figueroa-Lozano S, Valk-Weeber RL, van Leeuwen SS et al (2018) Dietary N-glycans from bovine lactoferrin and TLR modulation. Mol Nutr Food Res 62:1–30

    Article  CAS  Google Scholar 

  • Franco I, Pérez MD, Conesa C et al (2018) Effect of technological treatments on bovine lactoferrin: an overview. Food Res Int 106:173–182

    Article  PubMed  CAS  Google Scholar 

  • García-Montoya IA, Cendón TS, Arévalo-Gallegos S, Rascón-Cruz Q (2012) Lactoferrin a multiple bioactive protein: an overview. Biochim Biophys Acta 1820:226–236

    Article  PubMed  CAS  Google Scholar 

  • Gianino P, Mastretta E, Longo P et al (2002) Incidence of nosocomial rotavirus infections, symptomatic and asymptomatic, in breast-fed and non-breast-fed infants. J Hosp Infect 50:13–17

    Article  PubMed  CAS  Google Scholar 

  • Holsinger VH, Rajkowski KT, Stabel JR (1997) Milk pasteurisation and safety: a brief history and update. Rev Sci Tech 16:441–451

    Article  PubMed  CAS  Google Scholar 

  • Inagaki M, Yamamoto M, Uchida K et al (2010) In vitro and in vivo evaluation of the efficacy of bovine colostrum against human rotavirus infection. Biosci Biotechnol Biochem 74:680–682

    Article  PubMed  CAS  Google Scholar 

  • Isa P, Arias CF, López S (2006) Role of sialic acids in rotavirus infection. Glycoconj J 23:27–37

    Article  PubMed  CAS  Google Scholar 

  • Karav S, German JB, Rouquié C et al (2017) Studying lactoferrin N-glycosylation. Int J Mol Sci 18:870–884

    Article  PubMed Central  Google Scholar 

  • Kvistgaard AS, Pallesen LT, Arias CF et al (2004) Inhibitory effects of human and bovine milk constituents on rotavirus infections. J Dairy Sci 87:4088–4096

    Article  PubMed  CAS  Google Scholar 

  • Marcotte H, Hammarström L (2016) Immunodeficiencies: significance for gastrointestinal disease. In: Svensson L, Desselberger U, Greenberg HB, Estes MK (eds) Viral gastroenteritis. Molecular epidemiology and pathogenesis. Academic Press, Kidlington, pp 47–72

    Google Scholar 

  • Mayayo C, Montserrat M, Ramos SJ et al (2014) Kinetic parameters for high-pressure-induced denaturation of lactoferrin in human milk. Int Dairy J 39:246–252

    Article  CAS  Google Scholar 

  • Mayeur S, Spahis S, Pouliot Y, Levy E (2016) Lactoferrin, a pleiotropic protein in health and disease. Antioxid Redox Signal 24:813–836

    Article  PubMed  CAS  Google Scholar 

  • Mazri C, Sánchez L, Ramos SJ et al (2012) Effect of high-pressure treatment on denaturation of bovine lactoferrin and lactoperoxidase. J Dairy Sci 95:549–557

    Article  PubMed  CAS  Google Scholar 

  • O’Riordan N, Kane M, Joshi L, Hickey RM (2014) Structural and functional characteristics of bovine milk protein glycosylation. Glycobiology 24:220–236

    Article  PubMed  CAS  Google Scholar 

  • Oria R, Sánchez L, Houston T et al (1995) Effect of nitric oxide on expression of transferrin receptor and ferritin and on cellular iron metabolism in K562 human erythroleukemia cells. Blood 85:2962–2966

    PubMed  CAS  Google Scholar 

  • Parrón JA, Ripollés D, Pérez MD et al (2016) Effect of heat treatment on antirotaviral activity of bovine and ovine whey. Int Dairy J 60:78–85

    Article  CAS  Google Scholar 

  • Parrón JA, Ripollés D, Pérez MD et al (2017) Antirotaviral activity of bovine and ovine dairy byproducts. J Agric Food Chem 65:4280–4288

    Article  PubMed  CAS  Google Scholar 

  • Peila C, Moro GE, Bertino E et al (2016) The Effect of holder pasteurization on nutrients and biologically-active components in donor human milk: a review. Nutrients 8:477–496

    Article  PubMed Central  Google Scholar 

  • Peila C, Emmerik NE, Giribaldi M et al (2017) Human milk processing: a systematic review of innovative techniques to ensure the safety and quality of donor milk. J Pediatr Gastroenterol Nutr 64:353–361

    Article  PubMed  Google Scholar 

  • Pesavento JB, Crawford SE, Estes MK, Prasad BVV (2006) Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 309:189–219

    PubMed  CAS  Google Scholar 

  • Peterson R, Cheah WY, Grinyer J, Packer N (2013) Glycoconjugates in human milk: protecting infants from disease. Glycobiology 23:1425–1438

    Article  PubMed  CAS  Google Scholar 

  • Prasad BVV, Shanker S, Hu L et al (2014) Structural basis of glycan interaction in gastroenteric viral pathogens. Curr Opin Virol 7:119–127

    Article  PubMed Central  CAS  Google Scholar 

  • Ripollés D, Harouna S, Parrón JA et al (2015) Antibacterial activity of bovine milk lactoferrin and its hydrolysates prepared with pepsin, chymosin and microbial rennet against foodborne pathogen Listeria monocytogenes. Int Dairy J 45:15–22

    Article  CAS  Google Scholar 

  • Rosa L, Cutone A, Lepanto MS et al (2017) Lactoferrin: a natural glycoprotein involved in iron and inflammatory homeostasis. Int J Mol Sci 18:1985–2011

    Article  PubMed Central  Google Scholar 

  • Sánchez L, Peiró JM, Castillo H et al (1992) Kinetic parameters for denaturation of bovine milk lactoferrin. J Food Sci 57:873–879

    Article  Google Scholar 

  • Siciliano R, Rega B, Marchetti M et al (1999) Bovine lactoferrin peptidic fragments involved in inhibition of herpes simplex virus type 1 infection. Biochem Biophys Res Commun 264:19–23

    Article  PubMed  CAS  Google Scholar 

  • Skibiel AL, Downing LM, Orr TJ, Hood WR (2013) The evolution of the nutrient composition of mammalian milks. J Anim Ecol 82:1254–1264

    Article  PubMed  Google Scholar 

  • Superti F, Ammendolia MG, Valenti P, Seganti L (1997) Antirotaviral activity of milk proteins: lactoferrin prevents rotavirus infection in the enterocyte-like cell line HT-29. Med Microbiol Immunol 186:83–91

    Article  PubMed  CAS  Google Scholar 

  • Superti F, Siciliano R, Rega B et al (2001) Involvement of bovine lactoferrin metal saturation, sialic acid and protein fragments in the inhibition of rotavirus infection. Biochim Biophys Acta 1528:107–115

    Article  PubMed  CAS  Google Scholar 

  • Tino De Franco M, Vieira PD, Santos SMR et al (2013) Neutralizing activity and secretory IgA antibodies reactive with rotavirus SA-11 (serotype G3) in colostrum and milk from Brazilian women. Paediatr Int Child Health 33:102–109

    Article  PubMed  CAS  Google Scholar 

  • Valenti P, Antonini G (2005) Lactoferrin: an important host defence against microbial and viral attack. Cell Mol Life Sci 62:2576–2587

    Article  PubMed  CAS  Google Scholar 

  • van Veen HA, Geerts MEJ, van Berkel PHC, Nuijens JH (2004) The role of N-linked glycosylation in the protection of human and bovine lactoferrin against tryptic proteolysis. Eur J Biochem 271:678–684

    Article  PubMed  CAS  Google Scholar 

  • Wang XY, Guo HY, Zhang W et al (2013) Effect of iron saturation level of lactoferrin on osteogenic activity in vitro and in vivo. J Dairy Sci 96:33–39

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The work described herein was supported by Spanish government under a FPU predoctoral grant and a CICYT project (AGL2010-20835), and by the European Social Fund.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lourdes Sánchez.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parrón, J.A., Ripollés, D., Ramos, S.J. et al. Antirotaviral potential of lactoferrin from different origin: effect of thermal and high pressure treatments. Biometals 31, 343–355 (2018). https://doi.org/10.1007/s10534-018-0088-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-018-0088-4

Keywords

Navigation