Bovine lactoferrin inhibits Influenza A virus induced programmed cell death in vitro

BioMetals

Volumn 23, Issue 3, 2010, Pages 465-475

  Pietrantoni, Agostina ^a   Dofrelli, Eleonora ^a   Tinari, Antonella ^a   Ammendolia, Maria Grazia ^a   Puzelli, Simona ^a   Fabiani, Concetta ^a   Donatelli, Isabella ^a   Superti, Fabiana ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Apoptosis; Bovine lactoferrin; Influenza virus; MDCK cells

Indexed keywords

CASPASE 3; IRON BINDING PROTEIN; LACTOFERRIN; RIBONUCLEOPROTEIN; ANTIVIRUS AGENT;

ANIMAL CELL; ANTIMICROBIAL ACTIVITY; ANTIVIRAL ACTIVITY; APOPTOSIS; CELL NUCLEUS; CELL STRAIN; CONFERENCE PAPER; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOMODULATION; IN VITRO STUDY; INFLUENZA A (H3N2); INFLUENZA VIRUS A H3N2; INHIBITION KINETICS; NONHUMAN; PLEIOTROPY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN TRANSPORT; ULTRAVIOLET SPECTROSCOPY; VIRUS ASSEMBLY; ANIMAL; BOVINAE; CELL PROLIFERATION; DOG; DOSE RESPONSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; INFLUENZA VIRUS A; MICROBIAL SENSITIVITY TEST; PATHOGENICITY; STRUCTURE ACTIVITY RELATION;

ANIMALS; ANTIVIRAL AGENTS; APOPTOSIS; CATTLE; CELL PROLIFERATION; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; INFLUENZA A VIRUS; LACTOFERRIN; MICROBIAL SENSITIVITY TESTS; STRUCTURE-ACTIVITY RELATIONSHIP;

BOVINAE; INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

EID: 77953287277     PISSN: 09660844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10534-010-9323-3     Document Type: Conference Paper

References (50)

1. MG Ammendolia A Tinari A Calcabrini F Superti 1999 Poliovirus infection induces apoptosis in CaCo-2 cells J Med Virol 59 122 129 10.1002/(SICI)1096- 9071(199909)59:1<122::AID-JMV20>3.0.CO;2-9 1:STN:280:DyaK1MznvFaktw%3D%3D 10440819 (Pubitemid 29362176)
2. MG Ammendolia M Marchetti F Superti 2007 Bovine lactoferrin prevents the entry and intercellular spread of herpes simplex virus type 1 in Green Monkey Kidney cells Antiviral Res 76 252 262 10.1016/j.antiviral.2007.07.005 1:CAS:528:DC%2BD2sXht1anurnN 17881064 (Pubitemid 47600359)
3. MG Ammendolia A Pietrantoni A Tinari P Valenti F Superti 2007 Bovine lactoferrin inhibits echovirus endocytic pathway by interacting with viral structural polypeptides Antiviral Res 73 151 160 10.1016/j.antiviral.2006.09.002 1:CAS:528:DC%2BD2sXitFOitLs%3D 17023058
4. JH Andersen SA Osbakk LH Vorland T Traavik TJ Gutteberg 2001 Lactoferrin and cyclic lactoferricin inhibit the entry of human cytomegalovirus into human fibroblasts Antiviral Res 51 141 149 10.1016/S0166-3542(01)00146-2 1:CAS:528:DC%2BD3MXks1OmurY%3D 11431038 (Pubitemid 32592502)
5. JH Andersen H Jenssen TJ Gutteberg 2003 Lactoferrin and lactoferricin inhibit Herpes simplex 1 and 2 infection and exhibit synergy when combined with acyclovir Antiviral Res 58 209 215 10.1016/S0166-3542(02)00214-0 1:CAS:528:DC%2BD3sXktFWksLc%3D 12767468 (Pubitemid 36589011)
6. E Anisimová E Tucková V Vonka H Závadová 1977 Ultrastructural changes induced by Influenza viruses in permissive and nonpermissive cells Virology 77 330 336 10.1016/0042-6822(77)90429-9
7. D Arnold AM Di Biase M Marchetti A Pietrantoni P Valenti L Seganti F Superti 2002 Antiadenovirus activity of milk proteins: lactoferrin prevents viral infection Antiviral Res 53 153 158 10.1016/S0166-3542(01)00197-8 1:CAS:528:DC%2BD3MXptFylsr8%3D 11750941 (Pubitemid 34062835)
8. NJ Dharan LV Gubareva JJ Meyer M Okomo-Adhiambo RC McClinton SA Marshall K St George S Epperson L Brammer AI Klimov JS Bresee AM Fry Oseltamivir- Resistance Working Group 2009 Infections with oseltamivir-resistant influenza A(H1N1) virus in the United States JAMA 30 1034 1041 10.1001/jama.2009.294
9. AM Di Biase A Pietrantoni A Tinari R Siciliano P Valenti G Antonini L Seganti F Superti 2003 Heparin-interacting sites of bovine lactoferrin are involved in anti-adenovirus activity J Med Virol 69 495 502 10.1002/jmv.10337 1:CAS:528:DC%2BD3sXisVOit78%3D 12601757 (Pubitemid 36249863)
10. P Drobni J Naslund M Evander 2004 Lactoferrin inhibits human papillomavirus binding and uptake in vitro Antiviral Res 6 63 68
11. AE Fiore DK Shay K Broder JK Iskander TM Uyeki G Mootrey JS Bresee NS Cox Centers for Disease Control, Prevention (CDC) Advisory Committee on Immunization Practices (ACIP) 2008 Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP) MMWR Recomm Rep 57 RR-7 1 60 18685555
12. ML Groves 1960 The isolation of a red protein from milk J Am Chem Soc 82 3345 3350 10.1021/ja01498a029 1:CAS:528:DyaF3MXhvVWqsA%3D%3D
13. LV Gubareva MN Matrosovich MK Brenner RC Bethell RG Webster 1998 Evidence for zanamivir resistance in an immunocompromised child infected with influenza B virus J Infect Dis 178 1257 1262 10.1086/314440 1:STN:280:DyaK1cvltlCnsg%3D%3D 9780244 (Pubitemid 28523261)
14. K Hara M Ikeda S Saito S Matsumoto K Numata N Kato K Tanaka H Sekihara 2002 Lactoferrin inhibits hepatitis B virus infection in cultured human hepatocytes Hepatol Res 24 228 235 10.1016/S1386-6346(02)00088-8 1:CAS:528:DC%2BD38XotVCgtLs%3D 12393024 (Pubitemid 35314579)
15. MC Harmsen PJ Swart MP de Béthune R Pawels E De Clercq TH The DKF Meijer 1995 Antiviral effects of plasma and milk proteins: lactoferrin shows a potent activity against both human immunodeficiency virus and human cytomegalovirus replication in vitro J Infect Dis 172 380 388 1:CAS:528:DyaK2MXnslSnt7o%3D 7622881
16. K Hasegawa W Motsuchi S Tanaka S Dosako 1994 Inhibition with lactoferrin of in vitro infection with human herpes virus Jpn J Med Sci Biol 47 73 85 1:CAS:528:DyaK2MXitFCltr4%3D 7853749
17. FG Hayden 2006 Antiviral resistance in influenza viruses-implications for management and pandemic response N Engl J Med 354 785 788 10.1056/NEJMp068030 1:CAS:528:DC%2BD28XhslOgtrY%3D 16495389 (Pubitemid 43290915)
18. FG Hayden JJ Treanor RS Fritz M Lobo RF Betts M Miller N Kinnersley RG Mills P Ward SE Straus 1999 Use of the oral neuraminidase inhibitor oseltamivir in experimental human influenza: randomized controlled trials for prevention and treatment JAMA 282 1240 1246 10.1001/jama.282.13.1240 1:CAS:528: DyaK1MXmvVWhtbo%3D 10517426 (Pubitemid 29468495)
19. VS Hinshaw CW Olsen N Dybdahl-Sissoko D Evans 1994 Apoptosis: a mechanism of cell killing by influenza A and B viruses J Virol 68 3667 3673 1:CAS:528:DyaK2cXjt1Snurw%3D 8189504
20. M Kiso K Mitamura Y Sakai-Tagawa K Shiraishi C Kawakami K Kimura FG Hayden N Sugaya Y Kawaoka 2004 Resistant influenza A viruses in children treated with oseltamivir: descriptive study Lancet 364 759 765 10.1016/S0140-6736(04) 16934-1 1:CAS:528:DC%2BD2cXntVOjt7Y%3D 15337401 (Pubitemid 39165094)
21. AH Koyama T Fukumori M Fujita H Irie A Adachi 2000 Physiological significance of apoptosis in animal virus infection Microbes Infect 2 1111 1117 10.1016/S1286-4579(00)01265-X 1:STN:280:DC%2BD3cvot1ahtA%3D%3D 10967291 (Pubitemid 30664225)
22. M Kurokawa H Ochiai K Nakajima S Niwayama 1990 Inhibitory effect of protein kinase C inhibitor on the replication of influenza type A virus J Gen Virol 71 2149 2155 10.1099/0022-1317-71-9-2149 1:CAS:528:DyaK3cXlvVChurs%3D 1698925
23. UK Laemmli 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 680 685 10.1038/227680a0 1:CAS:528:DC%2BD3MXlsFags7s%3D 5432063
24. PF Levay M Viljoen 1995 Lactoferrin: a general review Haematologica 80 252 267 1:CAS:528:DyaK2MXoslGrsb0%3D 7672721
25. G Longhi V Pietropaolo M Mischitelli C Longhi MP Conte M Marchetti A Tinari P Valenti AM Degener L Seganti F Superti 2006 Lactoferrin inhibits early steps of human BK polyomavirus infection Antiviral Res 72 145 152 10.1016/j.antiviral.2006.05.008 1:CAS:528:DC%2BD28Xptlyrt70%3D 16774792 (Pubitemid 44332569)
26. S Ludwig S Pleschka O Planz T Wolf 2006 Ringing the alarm bells: signalling and apoptosis in influenza virus infected cells Cell Microbiol 8 375 386 10.1111/j.1462-5822.2005.00678.x 1:CAS:528:DC%2BD28XivFKgtbg%3D 16469051 (Pubitemid 43356029)
27. M Marchetti F Superti MG Ammendolia P Rossi P Valenti L Seganti 1999 Inhibition of poliovirus type 1 infection by iron-, manganese- and zinc-saturated lactoferrin Med Microbiol Immunol 187 199 204 10.1007/s004300050093 1:CAS:528:DyaK1MXis1SnsL8%3D 10363676 (Pubitemid 29216755)
28. M Marchetti MG Ammendolia F Superti 2009 Glycosaminoglycans are not indispensable for the anti-herpes simplex virus type 2 activity of lactoferrin Biochimie 91 155 159 10.1016/j.biochi.2008.04.015 1:CAS:528: DC%2BD1MXktF2htQ%3D%3D 18534197
29. JT May 1988 Microbial contaminants and antimicrobial properties of human milk Microbiol Sci 5 42 46 1:STN:280:DyaK3czksVeksw%3D%3D 3079217
30. A Meijer A Lackenby O Hungnes B Lina S van der Werf B Schweiger M Opp J Paget J van de Kassteele A Hay M Zambon 2009 European Influenza Surveillance Scheme Oseltamivir-resistant influenza virus A (H1N1), Europe, 2007-08 season Emerg Infect Dis 15 552 560 10.3201/eid1504.081280 19331731
31. I Mori T Komatsu K Takeuchi K Nakakuki M Sudo Y Kimura 1995 In vivo induction of apoptosis by influenza virus J Gen Virol 76 2869 2873 10.1099/0022-1317-76-11-2869 1:CAS:528:DyaK2MXovFOrtbw%3D 7595397
32. ME Murphy H Kariwa T Mizutani K Yoshimatsu J Arikawa I Takashima 2000 In vitro antiviral activity of lactoferrin and ribavirin upon hantavirus Arch Virol 145 1571 1582 10.1007/s007050070077 1:CAS:528:DC%2BD3cXnt1Whtrc%3D 11003470
33. N Orsi 2004 The antimicrobial activity of lactoferrin: current status and perspectives Biometals 17 189 196 10.1023/B:BIOM.0000027691.86757.e2 1:CAS:528:DC%2BD2cXjvFaru7Y%3D 15222464 (Pubitemid 38987136)
34. R Paesano M Pietropaoli S Gessani P Valenti 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 10.1016/j.biochi.2008.06.004 1:CAS:528:DC%2BD1MXktF2gsQ%3D%3D 18601971
35. A Pietrantoni AM Di Biase A Tinari M Marchetti P Valenti L Seganti F Superti 2003 Bovine lactoferrin inhibits adenovirus infection by interacting with viral structural polypeptides Antimicrob Agents Chemother 47 2688 2691 10.1128/AAC.47.8.2688-2691.2003 1:CAS:528:DC%2BD3sXlvFClsLc%3D 12878543 (Pubitemid 36919483)
36. A Pietrantoni MG Ammendolia A Tinari R Siciliano P Valenti F Superti 2006 Bovine lactoferrin peptidic fragments involved in inhibition of Echovirus 6 in vitro infection Antiviral Res 69 98 106 10.1016/j.antiviral.2005.10.006 1:CAS:528:DC%2BD28XhtV2lsbg%3D 16386316 (Pubitemid 43152045)
37. GA Poland RM Jacobson IG Ovsyannikova 2009 Influenza virus resistance to antiviral agents: a plea for rational use Clin Infect Dis 48 1254 1256 10.1086/598989 19323631
38. P Puddu P Borghi S Gessani P Valenti F Belardelli L Seganti 1998 Antiviral effect of bovine lactoferrin saturated with metal ions on early steps of human immunodeficiency virus type 1 infection Int J Biochem Cell Biol 30 1055 1062 10.1016/S1357-2725(98)00066-1 1:CAS:528:DyaK1cXmsVGmsbc%3D 9785469 (Pubitemid 28484861)
39. AH Reid JK Taubenberger TG Fanning 2001 The 1918 Spanish influenza: integrating history and biology Microbes Infect 3 81 87 10.1016/S1286-4579(00) 01351-4 1:STN:280:DC%2BD3M3ksVertA%3D%3D 11226857 (Pubitemid 32172043)
40. H Sano K Nagai H Tsutsumi Y Kuroki 2003 Lactoferrin and surfactant protein A exhibit distinct binding specificity to F protein and differently modulate respiratory syncytial virus infection Eur J Immunol 33 2894 2902 10.1002/eji.200324218 1:CAS:528:DC%2BD3sXosFSjt78%3D 14515273 (Pubitemid 37337155)
41. L Seganti AM Di Biase M Marchetti A Pietrantoni A Tinari F Superti 2004 Antiviral activity of lactoferrin towards naked viruses Biometals 17 295 299 10.1023/B:BIOM.0000027708.27142.bc 1:CAS:528:DC%2BD2cXjvFarur4%3D 15222481 (Pubitemid 38987153)
42. F Superti MG Ammendolia P Valenti L Seganti 1997 Antirotaviral activity of milk proteins: lactoferrin prevents rotavirus infection in the enterocyte-like cell line HT-29 Med Microbiol Immunol 186 83 91 10.1007/s004300050049 1:CAS:528:DyaK2sXmvVOjuro%3D 9403835 (Pubitemid 27477875)
43. F Superti R Siciliano B Rega F Giansanti P Valenti G Antonini 2001 Involvement of bovine lactoferrin metal saturation, sialic acid and protein fragments in the inhibition of rotavirus infection Biochim Biophys Acta 1528 107 115 1:CAS:528:DC%2BD3MXnvFCku7g%3D 11687297
44. T Takizawa C Tatematsu K Ohashi Y Nakanishi 1999 Recruitment of apoptotic cysteine proteases (caspases) in influenza virus-induced cell death Microbiol Immunol 43 245 252 1:CAS:528:DyaK1MXis1Ghtbg%3D 10338194
45. K Tanaka M Ikeda A Nozaki N Kato H Tsuda S Saito H Sekihara 1999 Lactoferrin inhibits hepatitis C virus viremia in patients with chronic hepatitis C: a pilot study Jpn J Cancer Res 90 367 371 1:CAS:528: DyaK1MXislGrsbs%3D 10363572
46. NA Thornberry Y Lazebnik 1998 Caspases: enemies within Science 281 1312 1316 10.1126/science.281.5381.1312 1:CAS:528:DyaK1cXlvVegsLs%3D 9721091
47. A Tinari A Pietrantoni MG Ammendolia P Valenti F Superti 2005 Inhibitory activity of bovine lactoferrin against echovirus induced programmed cell death in vitro Int J Antimicrob Agents 25 433 438 10.1016/j.ijantimicag.2005.02.011 1:CAS:528:DC%2BD2MXjsVeht7k%3D 15848300 (Pubitemid 40558777)
48. P Valenti G Antonini 2005 Lactoferrin: an important host defence against microbial and viral attack Cell Mol Life Sci 62 2576 2587 10.1007/s00018-005- 5372-0 1:CAS:528:DC%2BD2MXhtlSms7vO 16261253 (Pubitemid 41721231)
49. BWA van der Strate FM De Boer HI Bakker DK Meijer G Molema MC Harmsen 2003 Synergy of bovine lactoferrin with the anti-cytomegalovirus drug cidofovir in vitro Antiviral Res 58 159 165 10.1016/S0166-3542(02)00211-5 12742576 (Pubitemid 36559610)
50. WJ Wurzer O Planz C Ehrhardt M Giner T Silberzahn S Pleschka S Ludwig 2003 Caspase 3 activation is essential for efficient influenza virus propagation EMBO J 22 2717 2728 10.1093/emboj/cdg279 1:CAS:528:DC%2BD3sXkt1Wrtb4%3D 12773387 (Pubitemid 36712368)