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Effect of bovine apo-lactoferrin on the growth and virulence of Actinobacillus pleuropneumoniae

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Abstract

Actinobacillus pleuropneumoniae (App) is a Gram-negative bacterium that causes porcine pleuropneumonia, leading to economic losses in the swine industry. Due to bacterial resistance to antibiotics, new treatments for this disease are currently being sought. Lactoferrin (Lf) is an innate immune system glycoprotein of mammals that is microbiostatic and microbicidal and affects several bacterial virulence factors. The aim of this study was to investigate whether bovine iron-free Lf (BapoLf) has an effect on the growth and virulence of App. Two serotype 1 strains (reference strain S4074 and the isolate BC52) and a serotype 7 reference strain (WF83) were analyzed. First, the ability of App to grow in iron-charged BLf was discarded because in vivo, BapoLf sequesters iron and could be a potential source of this element favoring the infection. The minimum inhibitory concentration of BapoLf was 14.62, 11.78 and 10.56 µM for the strain BC52, S4074 and WF83, respectively. A subinhibitory concentration (0.8 µM) was tested by assessing App adhesion to porcine buccal epithelial cells, biofilm production, and the secretion and function of toxins and proteases. Decrease in adhesion (24–42 %) was found in the serotype 1 strains. Biofilm production decreased (27 %) for only the strain 4074 of serotype 1. Interestingly, biofilm was decreased (60–70 %) in the three strains by BholoLf. Hemolysis of erythrocytes and toxicity towards HeLa cells were not affected by BapoLf. In contrast, proteolytic activity in all strains was suppressed in the presence of BapoLf. Finally, oxytetracycline produced synergistic effect with BapoLf against App. Our results suggest that BapoLf affects the growth and several of the virulence factors in App.

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References

  • Ammendolia MG, Bertuccini L, Iosi F, Minelli F, Berlutti F, Valenti P, Superti F (2010) Bovine lactoferrin interacts with cable pili of Burkholderia cenocepacia. Biometals 23:531–542. doi:10.1007/s10534-010-9333-1

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Archambault M, Harel J, Goure J, Tremblay YD, Jacques M (2012) Antimicrobial susceptibilities and resistance genes of Canadian isolates of Actinobacillus pleuropneumoniae. Microb Drug Resist 18:198–206. doi:10.1089/mdr.2011.0150

    Article  CAS  PubMed  Google Scholar 

  • Arslan SY, Leung KP, Wu CD (2009) The effect of lactoferrin on oral bacterial attachment. Oral Microbiol Immunol 24:411–416

    Article  CAS  PubMed  Google Scholar 

  • Baker HM, Baker EN (2004) Lactoferrin and iron: structural and dynamic aspects of binding and release. Biometals 17:209–216

    Article  CAS  PubMed  Google Scholar 

  • Blackall PJ, Klaasen HL, van den Bosch H, Kuhnert P, Frey J (2002) Proposal of a new serovar of Actinobacillus pleuropneumoniae: serovar 15. Vet Microbiol 84:47–52

    Article  CAS  PubMed  Google Scholar 

  • Boekema BK, Van Putten JP, Stockhofe-Zurwieden N, Smith HE (2004) Host cell contact-induced transcription of the type IV fimbria gene cluster of Actinobacillus pleuropneumoniae. Infect Immun 72:691–700

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Chen HL, Yen CC, Lu CY, Yu CH, Chen CM (2006) Synthetic porcine lactoferricin with a 20-residue peptide exhibits antimicrobial activity against Escherichia coli, Staphylococcus aureus, and Candida albicans. J Agric Food Chem 54:3277–3282. doi:10.1021/jf053031s

    Article  CAS  PubMed  Google Scholar 

  • Chiers K, De Waele T, Pasmans F, Ducatelle R, Haesebrouck F (2010) Virulence factors of Actinobacillus pleuropneumoniae involved in colonization, persistence and induction of lesions in its porcine host. Vet Res 41:65. doi:10.1051/vetres/2010037

    Article  PubMed Central  PubMed  Google Scholar 

  • Dashper SG, Pan Y, Veith PD, Chen YY, Toh EC, Liu SW, Cross KJ, Reynolds EC (2012) Lactoferrin inhibits Porphyromonas gingivalis proteinases and has sustained biofilm inhibitory activity. Antimicrob Agents Chemother 56:1548–1556

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deneer HG, Potter AA (1989) Effect of iron restriction on the outer membrane proteins of Actinobacillus (Haemophilus) pleuropneumoniae. Infect Immun 57:798–804

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dom P, Hommez J, Castryck F, Devriese LA, Haesebrouck F (1994) Serotyping and quantitative determination of in vitro antibiotic susceptibility of Actinobacillus pleuropneumoniae strains isolated in Belgium (July 1991–August 1992. Vet Q 16:10–13. doi:10.1080/01652176.1994.9694407

    Article  CAS  PubMed  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Drago-Serrano ME, de la Garza-Amaya M, Luna JS, Campos-Rodriguez R (2012) Lactoferrin-lipopolysaccharide (LPS) binding as key to antibacterial and antiendotoxic effects. Int Immunopharmacol 12:1–9. doi:10.1016/j.intimp.2011.11.002

    Article  CAS  PubMed  Google Scholar 

  • D’Silva CG, Archibald FS, Niven DF (1995) Comparative study of iron acquisition by biotype 1 and biotype 2 strains of Actinobacillus pleuropneumoniae. Vet Microbiol 44:11–23

    Article  PubMed  Google Scholar 

  • Dubin G, Koziel J, Pyrc K, Wladyka B, Potempa J (2013) Bacterial proteases in disease - role in intracellular survival, evasion of coagulation/fibrinolysis innate defenses, toxicoses and viral infections. Curr Pharm Des 19:1090–1113

    Article  CAS  PubMed  Google Scholar 

  • Ellison RT 3rd, Giehl TJ, LaForce FM (1988) Damage of the outer membrane of enteric Gram-negative bacteria by lactoferrin and transferrin. Infect Immun 56:2774–2781

    CAS  PubMed Central  PubMed  Google Scholar 

  • Enriquez-Verdugo I, Guerrero AL, Serrano JJ, Godinez D, Rosales JL, Tenorio V, de la Garza M (2004) Adherence of Actinobacillus pleuropneumoniae to swine-lung collagen. Microbiology 150:2391–2400. doi:10.1099/mic.0.27053-0

    Article  CAS  PubMed  Google Scholar 

  • Flores-Villasenor H, Canizalez-Roman A, de la Garza M, Nazmi K, Bolscher JG, Leon-Sicairos N (2012) Lactoferrin and lactoferrin chimera inhibit damage caused by enteropathogenic Escherichia coli in HEp-2 cells. Biochimie 94:1935–1942

    Article  CAS  PubMed  Google Scholar 

  • Frey J (2011) The role of RTX toxins in host specificity of animal pathogenic Pasteurellaceae. Vet Microbiol 153:51–58

    Article  CAS  PubMed  Google Scholar 

  • Frey J, Bosse JT, Chang YF, Cullen JM, Fenwick B, Gerlach GF, Gygi D, Haesebrouck F, Inzana TJ, Jansen R (1993) Actinobacillus pleuropneumoniae RTX-toxins: uniform designation of haemolysins, cytolysins, pleurotoxin and their genes. J Gen Microbiol 139:1723–1728

    Article  CAS  PubMed  Google Scholar 

  • Garcia Gonzalez O, de la Garza M, Vaca S, Paniagua GL, Mejia R, Tenorio VR, Negrete-Abascal E (2004) Actinobacillus pleuropneumoniae metalloprotease: cloning and in vivo expression. FEMS Microbiol Lett 234:81–86. doi:10.1016/j.femsle.2004.03.012

    Article  PubMed  Google Scholar 

  • Garcia-Cuellar C, Montanez C, Tenorio V, Reyes-Esparza J, Duran MJ, Negrete E, Guerrero A, de la Garza M (2000) A 24-kDa cloned zinc metalloprotease from Actinobacillus pleuropneumoniae is common to all serotypes and cleaves actin in vitro. Can J Vet Res 64:88–95

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gonzalez GC, Caamano DL, Schryvers AB (1990) Identification and characterization of a porcine-specific transferrin receptor in Actinobacillus pleuropneumoniae. Mol Microbiol 4:1173–1179

    Article  CAS  PubMed  Google Scholar 

  • Grasteau A, Tremblay YD, Labrie J, Jacques M (2011) Novel genes associated with biofilm formation of Actinobacillus pleuropneumoniae. Vet Microbiol 153:134–143

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez-Martin CB, del Blanco NG, Blanco M, Navas J, Rodriguez-Ferri EF (2006) Changes in antimicrobial susceptibility of Actinobacillus pleuropneumoniae isolated from pigs in Spain during the last decade. Vet Microbiol 115:218–222

    Article  CAS  PubMed  Google Scholar 

  • Hamer-Barrera R, Godinez D, Enrique VL, Vaca-Pacheco S, Matinez-Zuniga R, Tamás-Rohana P, Suarez-Guemez F, de la Garza M (2004) Adherence of Actinobacillus pleuropneumoniae serotype 1 to swine buccal epithelial cells involves fibronectin. Can J Vet Res 68:33–41

    CAS  PubMed Central  PubMed  Google Scholar 

  • Investigación Aplicada SA (2010). Acontecer porcino 86-87

  • Inzana TJ (1991) Virulence properties of Actinobacillus pleuropneumoniae. Microb Pathog 11:305–316

    Article  CAS  PubMed  Google Scholar 

  • Jacques M (2004) Surface polysaccharides and iron-uptake systems of Actinobacillus pleuropneumoniae. Can J Vet Res 68:81–85

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kamiya H, Ehara T, Matsumoto T (2012) Inhibitory effects of lactoferrin on biofilm formation in clinical isolates of Pseudomonas aeruginosa. J Infect Chemother 18:47–52. doi:10.1007/s10156-011-0287-1

    Article  CAS  PubMed  Google Scholar 

  • Kaplan JB, Mulks MH (2005) Biofilm formation is prevalent among field isolates of Actinobacillus pleuropneumoniae. Vet Microbiol 108:89–94

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki Y, Shimizu K, Matsuzawa H, Dosako S, Isoda H, Tsukiji M, Fujimura R, Muranaka Y, Isihida H (2000) Inhibitory effects of bovine lactoferrin on the adherence of enterotoxigenic Escherichia coli to host cells. Biosci Biotechnol Biochem 64:348–354

    Article  CAS  PubMed  Google Scholar 

  • Komine Y, Komine K, Kai K, Itagaki M, Kuroishi T, Aso H, Obara Y, Kumagai K (2006) Effect of combination therapy with lactoferrin and antibiotics against staphylococcal mastitis on drying cows. J Vet Med Sci 68:205–211

    Article  CAS  PubMed  Google Scholar 

  • Kutta H, Willer A, Steven P, Brauer L, Tsokos M, Paulsen F (2008) Distribution of mucins and antimicrobial substances lysozyme and lactoferrin in the laryngeal subglottic region. J Anat 213:473–481

    Article  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Lee TT, Chang CC, Juang RS, Chen RB, Yang HY, Chu LW, Wang SR, Tseng TH, Wang CS, Chen LJ, Yu B (2010) Porcine lactoferrin expression in transgenic rice and its effects as a feed additive on early weaned piglets. J Agric Food Chem 58:5166–5173. doi:10.1021/jf903904s

    Article  CAS  PubMed  Google Scholar 

  • Leitch EC, Willcox MD (1999) Elucidation of the antistaphylococcal action of lactoferrin and lysozyme. J Med Microbiol 48:867–871

    Article  CAS  PubMed  Google Scholar 

  • Leon-Sicairos N, Canizales-Roman A, de la Garza M, Reyes-Lopez M, Zazueta-Beltrán J, Nazmi K, Gomez-Gil B, Bolscher JG (2009) Bactericidal effect of lactoferrin and lactoferrin chimera against halophilic Vibrio parahaemolyticus. Biochimie 91:133–140

    Article  CAS  PubMed  Google Scholar 

  • Leon-Sicairos N, Lopez-Soto F, Reyes-Lopez M, Godinez-Vargas D, Ordaz-Pichardo C, de la Garza M (2006) Amoebicidal activity of milk, apo-lactoferrin, sIgA and lysozyme. Clin Med Res 4:106–113

  • Li L, Mou X, Nelson DR (2013) Characterization of Plp, a phosphatidylcholine-specific phospholipase and hemolysin of Vibrio anguillarum. BMC Microbiol 13:271

    Article  PubMed  Google Scholar 

  • Lloyd DH (2012) Alternatives to conventional antimicrobial drugs: a review of future prospects. Vet Dermatol 23(299–304):e259–e260. doi:10.1111/j.1365-3164.2012.01042.x

    Google Scholar 

  • López-Ruiz B, Vaca S, de la Garza M, Negrete-Abascal E (2013) Actinobacillus pleuropneumoniae secretes a metalloprotease that degrades porcine fibrinogen. Afr J Microbiol Res 7:2803–2807

    Google Scholar 

  • Morioka A, Asai T, Nitta H, Yamamoto K, Ogikubo Y, Takahashi T, Suzuki S (2008) Recent trends in antimicrobial susceptibility and the presence of the tetracycline resistance gene in Actinobacillus pleuropneumoniae isolates in Japan. J Vet Med Sci 70:1261–1264

    Article  PubMed  Google Scholar 

  • Mosquito S, Zegarra G, Villanueva C, Ruiz J, Ochoa TJ (2012) Effect of bovine lactoferrin on the minimum inhibitory concentrations of ampicillin and trimethoprim-sulfamethoxazole for clinical Shigella spp. strains. Biochem Cell Biol 90:412–416. doi:10.1139/o11-066

    Article  CAS  PubMed  Google Scholar 

  • Murdock CA, Cleveland J, Matthews KR, Chikindas ML (2007) The synergistic effect of nisin and lactoferrin on the inhibition of Listeria monocytogenes and Escherichia coli O157:H7. Lett Appl Microbiol 44:255–261

    Article  CAS  PubMed  Google Scholar 

  • Nedbalcova K, Satran P, Jaglic Z, Ondriasova R, Kucerova Z (2005) Monitoring of antibiotic resistance in isolates of Actinobacillus pleuropneumoniae in the Czech Republic between 2001 and 2003. Vet Med Czech 50:181–185

    CAS  Google Scholar 

  • Negrete-Abascal E, Tenorio VR, Serrano JJ, Garcia C, de la Garza M (1994) Secreted proteases from Actinobacillus pleuropneumoniae serotype 1 degrade porcine gelatin, hemoglobin and immunoglobulin A. Can J Vet Res 58:83–86

    CAS  PubMed Central  PubMed  Google Scholar 

  • Negrete-Abascal E, Tenorio VR, Guerrero AL, Garcia RM, Reyes ME, de la Garza M (1998) Purification and characterization of a protease from Actinobacillus pleuropneumoniae serotype 1, an antigen common to all the serotypes. Can J Vet Res 62:183–190

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ochoa TJ, Brown EL, Guion CE, Chen JZ, McMahon RJ, Cleary TG (2006) Effect of lactoferrin on enteroaggregative E. coli (EAEC). Biochem Cell Biol 84:369–376. doi:10.1139/o06-053

    Article  CAS  PubMed  Google Scholar 

  • Oho T, Mitoma M, Koga T (2002) Functional domain of bovine milk lactoferrin which inhibits the adherence of Streptococcus mutans cells to a salivary film. Infect Immun 70:5279–5282

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • O’May CY, Sanderson K, Roddam LF, Kirov SM, Reid DW (2009) Iron-binding compounds impair Pseudomonas aeruginosa biofilm formation, especially under anaerobic conditions. J Med Microbiol 58:765–773

    Article  PubMed  Google Scholar 

  • Orsi N (2004) The antimicrobial activity of lactoferrin: current status and perspectives. Biometals 17:189–196

    Article  CAS  PubMed  Google Scholar 

  • Plaut AG, Qiu J, St Geme JW 3rd (2000) Human lactoferrin proteolytic activity: analysis of the cleaved region in the IgA protease of Haemophilus influenzae. Vaccine 19(Suppl 1):S148–S152

    Article  CAS  PubMed  Google Scholar 

  • Pohl S, Bertschinger U, Frederiksen W, Mannheim W (1983) Transfer of Haemophilus pleuropneumoniae and the Pasteurella haemolytica-like organism causing porcine necrotic pleuropneumonia to the genus Actinobacillus (Actinobacillus pleuropneumoniae comb. Nov.) on the basis of phenotypic and deoxyribonucleic acid relatedness. Int J Syst Bacteriol 33:510–514

    Article  Google Scholar 

  • Qiu J, Hendrixson DR, Baker EN, Murphy TF, St Geme JW 3rd, Plaut AG (1998) Human milk lactoferrin inactivates two putative colonization factors expressed by Haemophilus influenzae. Proc Natl Acad Sci U S A 95:12641–12646

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ramos-Clamont G, Rodríguez-Franco D, Guzmán-Partida A, Acedo-Félix E, Vázquez-Moreno L (2010) Actividad antibacteriana de lactoferrina bovina y lactoferrina porcina sobre Escherichia coli K88 +. Rev Cient-Fac Cienc Vet 5:473–479

    Google Scholar 

  • Sanchez L, Aranda P, Perez MD, Calvo M (1988) Concentration of lactoferrin and transferrin throughout lactation in cow’s colostrum and milk. Biol Chem Hoppe Seyler 369:1005–1008

    Article  CAS  PubMed  Google Scholar 

  • Sandkvist M (2001) Type II secretion and pathogenesis Infect Immun 69:3523–3535. doi:10.1128/IAI.69.6.3523-3535.2001

    CAS  Google Scholar 

  • Schryvers AB (1989) Identification of the transferrin- and lactoferrin-binding proteins in Haemophilus influenzae. J Med Microbiol 29:121–130

    Article  CAS  PubMed  Google Scholar 

  • Schryvers AB, Morris LJ (1988) Identification and characterization of the transferrin receptor from Neisseria meningitidis. Mol Microbiol 2:281–288

    Article  CAS  PubMed  Google Scholar 

  • Shi Y, Kong W, Nakayama K (2000) Human lactoferrin binds and removes the hemoglobin receptor protein of the periodontopathogen Porphyromonas gingivalis. J Biol Chem 275:30002–30008. doi:10.1074/jbc.M001518200

    Article  CAS  PubMed  Google Scholar 

  • Singh PK, Tack BF, McCray PB Jr, Welsh MJ (2000) Synergistic and additive killing by antimicrobial factors found in human airway surface liquid. Am J Physiol Lung Cell Mol Physiol 279:L799–L805

    CAS  PubMed  Google Scholar 

  • Sojar HT, Hamada N, Genco RJ (1998) Structures involved in the interaction of Porphyromonas gingivalis fimbriae and human lactoferrin. FEBS Lett 422:205–208

    Article  CAS  PubMed  Google Scholar 

  • Teraguchi S, Shin K, Fukuwatari Y, Shimamura S (1996) Glycans of bovine lactoferrin function as receptors for the type 1 fimbrial lectin of Escherichia coli. Infect Immun 64:1075–1077

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tian H, Maddox IS, Ferguson LR, Shu Q (2010) Influence of bovine lactoferrin on selected probiotic bacteria and intestinal pathogens. Biometals 23:593–596. doi:10.1007/s10534-010-9318-0

    Article  CAS  PubMed  Google Scholar 

  • Van Meerloo J, Kaspers G, Cloos J (2011) Cell sensitivity assays: the MTT assay. In: Cree IA (ed) Cancer cell culture: methods and protocols, 2nd edn. Humana Press, New York, pp 237–245

    Chapter  Google Scholar 

  • Vanni M, Merenda M, Barigazzi G, Garbarino C, Luppi A, Tognetti R, Intorre L (2012) Antimicrobial resistance of Actinobacillus pleuropneumoniae isolated from swine. Vet Microbiol 156:172–177

    Article  CAS  PubMed  Google Scholar 

  • Vogel HJ (2012) Lactoferrin, a bird’s eye view. Biochem Cell Biol 90:233–244. doi:10.1139/o2012-016

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi H, Yamauchi K, Kobayashi T, Yaeshima T, Iwatsuki K, Yoshie H (2009) Inhibitory effects of lactoferrin on growth and biofilm formation of Porphyromonas gingivalis and Prevotella intermedia. Antimicrob Agents Chemother 53:3308–3316

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Williams J, Salazar-Fajardo M, Ramírez-Porras R, Mosqueda-Ara Z (2001) Sensibilidad in vitro de cepas de Actinobacillus pleuropneumoniae y Pasteurella multocida tipo “A” ante diferentes antimicrobianos. Rev Biomed 12:172–179

    Google Scholar 

  • Xiao L, Zhou L, Sun C, Feng X, Du C, Gao Y, Ji Q, Yang S, Wang Y, Han W, Langford PR, Lei L (2012) Apa is a trimeric autotransporter adhesin of Actinobacillus pleuropneumoniae responsible for autoagglutination and host cell adherence. J Basic Microbiol 52:598–607. doi:10.1002/jobm.201100365

    Article  CAS  PubMed  Google Scholar 

  • Yang TS, Wu SC, Wang SR (2000) Serum and milk lactoferrin concentration and the correlation with some blood components in lactating sows. Res Vet Sci 69:95–97. doi:10.1053/rvsc.2000.0393

    Article  CAS  PubMed  Google Scholar 

  • Yu RH, Schryvers AB (2002) Bacterial lactoferrin receptors: insights from characterizing the Moraxella bovis receptors. Biochem Cell Biol 80:81–90

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Ricardo Félix Grijalva for the HeLa cell line and Mr. Esteban Molina for his technical assistance. The first author received a scholarship from Conacyt, Mexico (Registration No. 201473).

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  1. Departamento de Biología Celular, Centro de Investigación y de Estudios Avanzados del IPN (CINVESTAV-IPN), Ave. IPN 2508, 07360, México DF, Mexico

    Sarahí Luna-Castro, Luisa Samaniego-Barrón, Delfino Godínez-Vargas & Mireya de la Garza

  2. Centro Nacional de Investigación Disciplinaria-Microbiología Animal, México DF, Mexico

    Francisco Aguilar-Romero

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  1. Sarahí Luna-Castro
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Luna-Castro, S., Aguilar-Romero, F., Samaniego-Barrón, L. et al. Effect of bovine apo-lactoferrin on the growth and virulence of Actinobacillus pleuropneumoniae . Biometals 27, 891–903 (2014). https://doi.org/10.1007/s10534-014-9752-5

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