Antiviral properties of milk proteins and peptides

International Dairy Journal

Volumn 16, Issue 11, 2006, Pages 1252-1261

  Pan, Y ^a   Lee, A ^b   Wan, J ^b   Coventry, M J ^b   Michalski, W P ^b   Shiell, B ^b   Roginski, H ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b CSIRO   (Australia)

Author keywords

lactalbumin; lactoglobulin; Antiviral proteins and peptides; Chemically modified milk proteins; Lactoferricin; Lactoferrin

Indexed keywords

CELLS; CHEMICAL MODIFICATION; DAIRY PRODUCTS; DISEASES; POLYPEPTIDES; VIRUSES;

Α-LACTALBUMIN; Β-LACTOGLOBULIN; ANTIVIRAL PROTEINS AND PEPTIDES; CHEMICALLY MODIFIED MILK PROTEINS; LACTOFERRICIN; LACTOFERRIN;

PROTEINS;

BOS TAURUS;

EID: 33748450128     PISSN: 09586946     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.idairyj.2006.06.010     Document Type: Review

References (102)

1. Andersen J.H., Jenssen H., and Gutteberg T.J. Lactoferrin and lactoferricin inhibit herpes simplex 1 and 2 infection and exhibit synergy when combined with acyclovir. Antiviral Research 58 (2003) 209-215
2. Andersen J.H., Osbakk S.A., Vorland L.H., Traavik T., and Gutteberg T.J. Lactoferrin and cyclic lactoferricin inhibit the entry of human cytomegalovirus into human fibroblasts. Antiviral Research 51 (2001) 141-149
3. Arnold D., Di Biase A.M., Marchetti M., Pietrantoni A., Valenti P., Seganti L., et al. Antiadenovirus activity of milk proteins: Lactoferrin prevents viral infection. Antiviral Research 53 (2002) 153-158
4. Baba M., Pauwels R., Balzarini J., Arnout J., Desmyter J., and De Clercq E. Mechanism of inhibitory effect of dextran sulphate and heparin on replication of human immunodeficiency virus in vitro. Proceedings of the National Academy of Science USA 85 (1988) 6132-6136
5. Beaumont S.L., Maggs D.J., and Clarke H.E. Effects of bovine lactoferrin on in vitro replication of feline herpesvirus. Veterinary Ophthalmology 6 (2003) 245-250
6. Belding M.E., Klebanoff S.J., and Ray C.G. Peroxidase-mediated virucidal systems. Science 167 (1970) 195-196
7. Beljaars L., Van Der Strate B.W.A., Bakker H.I., Reker-Smit C., van Loenen-Weemaes A., Wiegmans F.C., et al. Inhibition of cytomegalovirus infection by lactoferrin in vitro and in vivo. Antiviral Research 63 (2004) 197-208
8. Berkhout B., Derksen G.C.H., Back N.K.T., Klaver B., de Kruif C.G., and Visser S. Structural and functional analysis of negatively charged milk proteins with anti-HIV activity. AIDS Research and Human Retroviruses 13 (1997) 1101-1107
9. Berkhout B., Floris R., Recio I., and Visser S. The antiviral activity of the milk protein lactoferrin against the human immunodeficiency virus type 1. Biometals 17 (2004) 291-294
10. Berkhout B., van Wamel J.L.B., Beljaars L., Meijer D.K.F., Visser S., and Floris R. Characterization of the anti-HIV effects of native lactoferrin and other milk proteins and protein-derived peptides. Antiviral Research 55 (2002) 341-355
11. Blacklow N.R., and Greenberg H.B. Viral gastroenteritis. New England Journal of Medicine 325 (1991) 252-264
12. Brüssow H., Hilpert H., Walther I., Sidoti J., Mietens C., and Bachmann P. Bovine milk immunoglobulins for passive immunity to infantile rotavirus gastroenteritis. Journal of Clinical Microbiology 25 (1987) 982-986
13. Chen L.T., Lu L., and Broxmeyer H.E. Effects of purified iron-saturated human lactoferrin on spleen morphology in mice infected with Friend virus complex. American Journal of Pathology 126 (1987) 285-292
14. Clarke N.M., and May J.T. Effect of antimicrobial factors in human milk on rhinoviruses and milk-borne cytomegalovirus in vitro. Journal of Medical Microbiology 49 (2000) 719-723
15. 2+. American Journal of Pathology 257 (1989) G930-G934
16. Dechecchi M.C., Melotti P., Bonizzato A., Santacatterina M., Chilosi M., and Cabrini G. Heparan sulphate glycosaminoglycans are receptors sufficient to mediate the initial binding of adenovirus types 2 and 5. Journal of Virology 75 (2001) 8772-8780
17. Dechecchi M.C., Tamanini A., Bonizzato A., and Cabrini G. Heparan sulfate glycosaminoglycans are involved in adenovirus type 5 and 2-host cell interactions. Virology 268 (2000) 382-390
18. Di Biase A.M., Pietrantoni A., Tinari A., Siciliano R., Valenti P., Antonini G., et al. Heparin-interacting sites of bovine lactoferrin are involved in anti-adenovirus activity. Journal of Medical Virology 69 (2003) 495-502
19. Dosako, S., Kusano, H., Deya, E., & Idota, T. (1992). Infection protectant. United States Patent 5,147,853.
20. Doultree J.C., Druce J.D., Birch C.J., Bowden D.S., and Marshall J.A. Inactivation of feline calicivirus, a Norwalk virus surrogate. Journal of Hospital Infection 41 (1999) 51-57
21. Downham M.A., Scott R., Sims D.G., Webb J.K., and Gardner P.S. Breast-feeding protects against respiratory syncytial virus infections. British Medical Journal 2 6030 (1976) 274-276
22. Drobni P., Näslund J., and Evander M. Lactoferrin inhibits human papillomavirus binding and uptake in vitro. Antiviral Research 64 (2004) 63-68
23. El Agamy E.I., Ruppanner R., Ismail A., Champagne C.P., and Assaf R. Antibacterial and antiviral activity of camel milk protective proteins. Journal of Dairy Research 59 (1992) 169-175
24. Fieldsteel A.H. Nonspecific antiviral substances in human milk active against arbovirus and murine leukemia virus. Cancer Research 34 (1974) 712-715
25. Fleet G.H., Heiskanen P., Reid I., and Buckle K.A. Foodborne viral illness status in Australia. International Journal of Food Microbiology 59 (2000) 127-136
26. Fujihara T., and Hayashi K. Lactoferrin inhibits herpes simplex virus type-1 (HSV-1) infection to mouse cornea. Archives of Virology 140 (1995) 1469-1472
27. Grover M., Giouzeppos O., Schnagl R.D., and May J.T. Effect of human milk prostaglandins and lactoferrin on respiratory syncytial virus and rotavirus. Acta Paediatrica 86 (1997) 315-316
28. Hale A. Foodborne viral infections: Most are caused by Norwalk-like viruses, but we need to know more about these. British Medical Journal 318 (1999) 1433-1434
29. Hammer J., Haaheim H., and Gutteberg T.J. Bovine lactoferrin is more efficient than bovine lactoferricin in inhibiting HSV-I/-II replication in vitro. In: Shimazaki K. (Ed). Lactoferrin: Structure functions and applications (2000), Elsevier Science, Amsterdam, The Netherlands 239-243
30. Hansen F.S. Bactericidal properties of milk. British Journal of Experimental Pathology 5 (1924) 271-280
31. Hara K., Ikeda M., Saito S., Matsumoto S., Numata K., Kato N., et al. Lactoferrin inhibits hepatitis B virus infection in cultured human hepatocytes. Hepatology Research 24 (2002) 228-235
32. Harmsen M.C., Swart P.J., de Béthune M.P., Pauwels R., De Clercq E., The T.H., et al. Antiviral effects of plasma and milk proteins: Lactoferrin shows a potent activity against both human immunodeficiency virus and human cytomegalovirus replication in vitro. The Journal of Infectious Diseases 172 (1995) 380-388
33. Hasegawa K., Motsuchi W., Tanaka S., and Dosako S. Inhibition with lactoferrin of in vitro infection with human herpes virus. Japanese Journal of Medical Science and Biology 47 (1994) 73-85
34. Ho G., Broze G.J., and Schwartz A.L. Role of heparan sulphate proteoglycans in the uptake and degradation of tissue factor pathway inhibition-coagulation factor Xa complexes. Journal of Biological Chemistry 272 (1997) 16838-16844
35. Ikeda M., Nozaki A., Sugiyama K., Tanaka T., Naganuma A., Tanaka K., et al. Characterization of antiviral activity of lactoferrin against hepatitis C virus infection in human cultured cells. Virus Research 66 (2000) 51-63
36. Ikeda M., Sugiyama K., Tanaka T., Tanaka K., Sekihara H., Shimotohno K., et al. Lactoferrin markedly inhibits hepatitis C virus infection in cultured human hepatocytes. Biochemical and Biophysical Research Communications 245 (1998) 549-553
37. Isaacs C.E., Thormar H., and Pessolano T. Membrane-disruptive effect of human milk: Inactivation of enveloped viruses. Journal of Infectious Diseases 154 (1986) 966-971
38. Ishii K., Takamura N., Shinohara M., Wakui N., Shin H., Sumino Y., et al. Long-term follow-up of chronic hepatitis C patients treated with oral lactoferrin for 12 months. Hepatology Research 25 (2003) 226-233
39. Jansen R.W., Molema G., Pauwels R., Schols D., De Clerq E., and Meijer D.K.F. Potent in vitro anti-human immunodeficiency virus-1 activity of modified human serum albumins. Molecular Pharmacology 39 (1991) 818-823
40. Jenssen H., Andersen J.H., Uhlin-Hansen L., Gutteberg T.J., and Rekdal Ø. Anti-HSV activity of lactoferricin analogues is only partly related to their affinity for heparan sulfate. Antiviral Research 61 (2004) 101-109
41. Jiang S., Lin K., Strick N., Li Y.-Y., and Neurath A.R. Chemically modified bovine β-lactoglobulin blocks uptake of HIV-1 by colon- and cervix-derived epithelial cell lines. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology 13 (1996) 461-462
42. Jiang X., Wang M., Wang K., and Estes M.K. Sequence and genomic organization of Norwalk virus. Virology 195 (1993) 51-61
43. Kanamaru Y., Etoh M., Song X.-G., Mikogami T., Hayasawa H., Ebina T., et al. A high-Mr glycoprotein fraction from cow's milk potent in inhibiting replication of human rotavirus in vitro. Bioscience, Biotechnology and Biochemistry 63 (1999) 246-249
44. Kawasaki Y., Isoda K., Shinmoto H., Tanimoto M., Dosako S., Idota T., et al. Inhibition of κ-casein glycomacropeptide and lactoferrin of influenza virus hemagglutination. Bioscience, Biotechnology and Biochemistry 57 (1993) 1214-1215
45. Kokuba H., Aurelian L., and Neurath A.R. 3-Hydroxyphthaloyl β-lactoglobulin, IV. Antiviral activity in the mouse model of genital herpesvirus infection. Antiviral Chemistry and Chemotherapy 9 (1998) 353-357
46. Kreutz L.C., Seal B.S., and Mengeling W.L. Early interaction of FCV with cells in culture. Archives of Virology 136 (1994) 443-448
47. Kuipers M.E., Swart P.J., Witvrouw M., Esté J.A., Reymen D., De Clercq E., et al. Anti-HIV-1 activity of combinations and covalent conjugates of negatively charged human serum albumins (NCAs) and AZT. Journal of Drug Target 6 (1999) 323-335
48. Lederman S., Gulick R., and Chess L. Dextran sulphate and heparin interact with CD4 molecules to inhibit the binding of coat protein (gp120) of HIV. Journal of Immunology 143 (1989) 1149-1154
49. Lu L., Hangoc G., Oliff A., Chen L., Shen R.N., and Broxmeyer H.E. Protective influence of lactoferrin on mice infected with the polythemia-inducing strain of Friend virus complex. Cancer Research 47 (1987) 4184-4188
50. Lüscher-Mattli M. Polyanions-A lost chance in the fight against HIV and other virus diseases?. Antiviral Chemistry and Chemotherapy 11 (2000) 249-259
51. Mann D.M., Romm E., and Migliorini V. Delineation of the glycosaminoglycan binding site in the human inflammatory response protein lactoferrin. Journal of Biological Chemistry 269 (1994) 23661-23667
52. Marchetti M., Longhi C., Conte M.P., Pisani S., Valenti P., and Seganti L. Lactoferrin inhibits herpes simplex virus type 1 adsorption to Vero cells. Antiviral Research 29 (1996) 221-231
53. Marchetti M., Pisani S., Antonini G., Valenti P., Seganti L., and Orsi N. Metal complexes of bovine lactoferrin inhibit in vitro replication of herpes simplex virus type 1 and 2. Biometals 11 (1998) 89-94
54. Marchetti M., Superti F., Ammendolia M.G., Rossi P., Valenti P., and Seganti L. Inhibition of poliovirus type 1 infection by iron-, manganese- and zinc-saturated lactoferrin. Medical Microbiology and Immunology 187 (1999) 199-204
55. Matthews T.H.J., Nair C.D.G., Lawrence M.K., and Tyrrel D.A.J. Antiviral activity in milk of possible clinical importance. Lancet 7 (1976) 1387-1389
56. Micke P., Beeh K.M., and Buhl R. Effects of long-term supplementation with whey proteins on plasma glutathione levels of HIV-infected patients. European Journal of Nutrition 41 (2002) 12-18
57. McCann K.B., Lee A., Wan J., Roginski H., and Coventry M.J. The effect of bovine lactoferrin and lactoferricin B on the ability of feline calicivirus (a norovirus surrogate) and poliovirus to infect cell cultures. Journal of Applied Microbiology 95 (2003) 1026-1033
58. Moreno Y.F., Sgarbieri V.C., da Silva M.N., Toro A.A.D.C., and Vilela M.M.S. Features of whey protein concentrate supplementation in children with rapidly progressive HIV infection. Journal of Tropical Pediatrics 52 (2006) 34-38
59. Murphy M.E., Kariwa H., Mizutani T., Yoshimatsu K., Arikawa J., and Takashima I. In vitro antiviral activity of lactoferrin and ribavirin upon hantavirus. Archives of Virology 145 (2000) 1571-1582
60. Neurath A.R., Debnath A.K., Strick N., Li Y.-Y., Lin K., and Jiang S. 3-Hydroxyphthaloyl-β-lactoglobulin. I. Optimization of production and comparison with other compounds considered for chemoprophylaxis of mucosally transmitted human immunodeficiency virus type 1. Antiviral Chemistry and Chemotherapy, 8 (1997) 131-139
61. Neurath A.R., Jiang S., Strick N., Lin K., Li Y.-Y., and Debnath A.K. Bovine β-lactoglobulin modified by 3-hydroxyphthalic anhydride blocks the CD4 cell receptor for HIV. Nature Medicine 2 (1996) 230-234
62. Neurath A.R., Strick N., and Li Y.-Y. 3-Hydroxyphthaloyl β-lactoglobulin. III. Antiviral activity against herpesviruses. Antiviral Chemistry and Chemotherapy, 9 (1998) 177-184
63. Newburg D.S., Peterson J.A., Ruiz-Palacios G.M., Matson D.O., Morrow A.L., Shults J., et al. Role of human-milk lactadherin in protection against symptomatic rotavirus infection. The Lancet 351 (1998) 1160-1164
64. Newburg D.S., Viscidi R.P., Ruff A., and Yolken R.H. A human milk factor inhibits binding of human immunodeficiency virus to the CD4 receptor. Pediatric Research 31 (1992) 22-28
65. Nozaki A., Tanaka K., Naganuma A., and Kato N. Recent advances of basic research and clinical application of lactoferrin as an antiviral reagent against chronic hepatitis C. Japanese Journal of Clinical Medicine 60 (2002) 819-829
66. Oevermann A., Engels M., Thomas U., and Pellegrini A. The antiviral activity of naturally occurring proteins and their peptide fragments after chemical modification. Antiviral Research 59 (2003) 23-33
67. Poole A.R. Proteoglycans in health and diseases: Structures and functions. Biochemical Journal 236 (1986) 1-14
68. Puddu P., Borghi P., Gessani S., Valenti P., Belardelli F., and Seganti L. Antiviral effect of bovine lactoferrin saturated with metal ions on early steps of human immunodeficiency virus type 1 infection. The International Journal of Biochemistry and Cell Biology 30 (1998) 1055-1062
69. Pullan C.R., Toms G.L., Martin A.J., Gardner P.S., Webb J.K., and Appleton D.R. Breast-feeding and respiratory syncytial virus infection. British Medical Journal 281 (1980) 1034-1036
70. Roderiquez G., Oravecz T., Yanagishita M., Bou-habib D.C., Mostowski H., and Norcross M.A. Mediation of human immunodeficiency virus type 1 binding by interaction of cell surface heparan sulfate proteoglycans with the V3 region of envelope gp 120-gp41. Journal of Virology 69 (1995) 2233-2239
71. Rostand K.S., and Esko J.D. Microbial adherence to and invasion through proteoglycans. Infection and Immunity 65 (1997) 1-8
72. Schoen P., Corver J., Meijer D.K.F., Wilschut J., and Swart P.J. Inhibition of influenza virus fusion by polyanionic proteins. Biochemical Pharmacology 53 (1997) 995-1003
73. Seganti L., Di Biase A.M., Marchetti M., Pietrantoni A., Tinari A., and Superti F. Antiviral activity of lactoferrin towards naked viruses. Biometals 17 (2004) 295-299
74. Shimizu K., Matsuzawa H., Okada K., Tazume S., Dosako S., Kawasaki Y., et al. Lactoferrin-mediated protection of the host from murine cytomegalovirus infection by a T-cell-dependent augmentation of natural killer cell activity. Archives of Virology 141 (1996) 1875-1889
75. Siciliano R., Rega B., Marchetti M., and Seganti L. Bovine lactoferrin peptidic fragments involved in inhibition of herpes simplex virus type 1 infection. Biochemical and Biophysical Research Communications 264 (1999) 19-23
76. Slomka M.J., and Appleton H. Feline calicivirus as a model system for heat inactivation studies of small round structured viruses in shellfish. Epidemiology and Infection 121 (1998) 401-407
77. Superti F., Ammendolia M.G., Valenti P., and Seganti L. Antirotaviral activity of milk proteins: lactoferrin prevents rotavirus infection in the enterocyte-like cell line HT-29. Medical Microbiology and Immunology 186 (1997) 83-91
78. Superti F., Siciliano R., Rega B., Giansanti F., Valenti P., and Antonini G. Involvement of bovine lactoferrin metal saturation, sialic acid and protein fragments in the inhibition of rotavirus infection. Biochimica et Biophysica Acta 1528 (2001) 107-115
79. Swart P.J., Beljaars L., Kuipers M.E., Smit C., Nieuwenhuis P., and Meijer D.K.F. Homing of negatively charged albumins to the lymphatic system. Biochemical Pharmacology 58 (1999) 1425-1435
80. Swart P.J., Harmsen M.C., De Béthune M.-P., Pauwels R., De Clercq E., The T.H., et al. Antiviral effects of plasma and milk proteins: Lactoferrin shows potent antiviral activity on both HIV and HCMV replication in vitro in the same concentration range. Antiviral Research 30 (1996) A35
81. Swart P.J., Harmsen M.C., Kuipers M.E., Van Dijk A.A., Van der Strate B.W.A., Van Berkel P.H.C., et al. Charge modification of plasma and milk proteins results in antiviral active compounds. Journal of Peptide Science 5 (1999) 563-576
82. Swart P.J., Kuipers M.E., Smit C., Pauwels R., De Béthune M.-P., De Clercq E., et al. Antiviral effects of milk proteins: Acylation results in polyanionic compounds with potent activity against human immunodeficiency virus types 1 and 2 in vitro. AIDS Research and Human Retroviruses 12 (1996) 769-775
83. Swart P.J., Kuipers M.E., Smit C., VanDerStrate B.W.A., Harmsen M.C., and Meijer D.K.F. Lactoferrin: Antiviral activity of lactoferrin. In: Spik G., Legrand D., Mazurier J., Pierce A., and Perraudin J.P. (Eds). Advances in lactoferrin research (1998), Plenum Press, New York, USA 205-213
84. Swart P.J., and Meijer D.K.F. Negatively charged albumins: A novel class of polyanionic proteins with a potent anti-HIV activity. Antiviral News 2 (1994) 69-71
85. Takami M., Sone T., Mizumoto K., Kino K., and Tsunoo H. Maleylated human serum albumin inhibits HIV-1 infection in vitro. Biochimica et Biophysica Acta 1180 (1992) 180-186
86. Tanaka T., Nakatani S., Xuan X., Kumura H., Igarashi I., and Shimazaki K. Antiviral activity of lactoferrin against canine herpesvirus. Antiviral Research 60 (2003) 193-199
87. Thormar H., Isaacs C.E., Brown H.R., Barshatzki M.R., and Pessolano T. Inactivation of enveloped viruses and killing of cells by fatty acids and monoglycerides. Antimicrobial Agents and Chemotherapy 31 (1987) 27-31
88. Tinari A., Pietrantoni A., Ammendolia M.G., Valenti P., and Superti F. Inhibitory activity of bovine lactoferrin against echovirus induced programmed cell death in vitro. International Journal of Antimicrobial Agents 25 (2005) 433-438
89. Ueno R., and Kuno S. Anti-HIV synergism between dextran sulphate and zidovudine. Lancet 2 (1987) 796-797
90. Valenti P., Marchetti M., Superti F., Amendolia M.G., Puddu P., Gessani S., et al. Antiviral activity of lactoferrin. In: Spik G., Legrand D., Mazurier J., Pierce A., and Perraudin J.P. (Eds). Advances in lactoferrin research (1998), Plenum Press, New York, USA 199-203
91. Van Der Strate B.W.A., Beljaars L., Molema G., Harmsen M.C., and Meijer D.K.F. Antiviral activities of lactoferrin. Antiviral Research 52 (2001) 225-239
92. Van Der Strate B.W.A., De Boer F.M., Bakker H.I., Meijer D.K.F., Molema G., and Harmsen M.C. Synergy of bovine lactoferrin with the anti-cytomegalovirus drug cidofovir in vitro. Antiviral Research 58 (2003) 159-165
93. van Hooijdonk A.C.M., Kussendrager K.D., and Steijns J.M. In vivo antimicrobial and antiviral activity of components in bovine milk and colostrum involved in non-specific defence. British Journal of Nutrition 84 (2000) S127-S134
94. Vorland L.H. Lactoferrin: A multifunctional glycoprotein. APMIS: Acta Pathologica, Microbiologica et Immunologica Scandinavica 107 (1999) 971-981
95. Waarts B., Aneke O.J.C., Smit J.M., Kimata K., Bittman R., Meijer D.K.F., et al. Antiviral activity of human lactoferrin: Inhibition of alphavirus interaction with heparan sulfate. Virology 333 (2005) 284-292
96. Watanabe A., Okada K., Shimizu Y., Wakabayashi H., Higuchi K., Niiya K., et al. Nutritional therapy of chronic hepatitis by whey protein (non-heated). Journal of Medicine 31 (2000) 283-302
97. Welsh J.K., Arsenakis M., Coelen R.J., and May J.T. Effect of antiviral lipids heat and freezing on the activity of viruses in human milk. The Journal of Infectious Diseases 140 (1979) 322-328
98. Wu H.F., Monroe D.M., and Church F.C. Characterization of the glycosaminoglycan-binding region of lactoferrin. Archives of Biochemistry and Biophysics 317 (1995) 85-92
99. WuDunn D., and Spear P.G. Initial interaction of herpes simplex virus with cells is binding to heparan sulphate. Journal of Virology 63 (1989) 52-58
100. Yi M., Kaneko S., Yu D.Y., and Murakami S. Hepatitis C virus envelope proteins bind lactoferrin. Journal of Virology 71 (1997) 5997-6002
101. Yolken R.H., Peterson J.A., Vonderfecht S.L., Fouts E.T., Midthun K., and Newburg D.S. Human milk mucin inhibits rotavirus replication and prevents experimental gastroenteritis. Journal of Clinical Investigation 90 (1992) 1984-1991
102. Zeder-Lutz G., Neurath A.R., and Van Regenmortel M.H.V. Kinetics of interaction between 3-hydroxyphthaloyl-β-lactoglobulin and CD4 molecules. Biologicals 27 (1999) 29-34