LigB subunit vaccine confers sterile immunity against challenge in the hamster model of leptospirosis

PLoS Neglected Tropical Diseases

Volumn 11, Issue 3, 2017, Pages

  Conrad, Neida L ^a   Cruz McBride, Flávia W ^b   Souza, Jéssica D ^a   Silveira, Marcelle M ^a   Félix, Samuel ^a   Mendonça, Karla S ^a   Santos, Cleiton S ^c   Athanazio, Daniel A ^d   Medeiros, Marco A ^c   Reis, Mitermayer G ^c,d   Dellagostin, Odir A ^a   McBride, Alan J A ^a,c  

^a FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^b CATHOLIC UNIVERSITY OF PELOTAS   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

^d FEDERAL UNIVERSITY OF BAHIA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LEPTOSPIRAL IMMUNOGLOBULIN IKE PROTEIN; SUBUNIT VACCINE; UNCLASSIFIED DRUG; ALUMINUM HYDROXIDE; BACTERIAL ANTIGEN; BACTERIAL VACCINE; BACTERIUM ANTIBODY; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; IMMUNOLOGICAL ADJUVANT; LIGB-M PROTEIN, LEPTOSPIRA INTERROGANS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRIGHT FIELD MICROSCOPY; CONTROLLED STUDY; DRUG FORMULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPISTAXIS; FEMALE; FLUORESCENCE MICROSCOPY; HAMSTER; HAMSTER MODEL; HISTOPATHOLOGY; HUMORAL IMMUNITY; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; IMMUNOBLOTTING; LEPTOSPIROSIS; MALE; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; WEIGHT REDUCTION; ANIMAL; BLOOD; DISEASE MODEL; IMMUNOLOGY; LEPTOSPIRA; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ADJUVANTS, IMMUNOLOGIC; ALUMINUM HYDROXIDE; ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL VACCINES; CRICETINAE; DISEASE MODELS, ANIMAL; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LEPTOSPIRA; LEPTOSPIROSIS; SURVIVAL ANALYSIS; TREATMENT OUTCOME; VACCINES, SUBUNIT;

EID: 85016929984     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0005441     Document Type: Article

References (65)

1. Costa F, Hagan JE, Calcagno J, Kane M, Torgerson P, Martinez-Silveira MS, et al. Global Morbidity and Mortality of Leptospirosis: A Systematic Review. PLoS Negl Trop Dis. 2015;9(9):e0003898. doi: 10.1371/journal.pntd.0003898 26379143
2. Andre-Fontaine G, Aviat F, Thorin C, Waterborne Leptospirosis: Survival and Preservation of the Virulence of Pathogenic Leptospira spp. in Fresh Water. Curr Microbiol. 2015;71(1):136–42. doi: 10.1007/s00284-015-0836-4 26003629
3. Trueba G, Zapata S, Madrid K, Cullen P, Haake D, Cell aggregation: a mechanism of pathogenic Leptospira to survive in fresh water. Int Microbiol. 2004;7(1):35–40. 15179605
4. IGBE. [Population estimates for residents of Brazilian municipalities and federation units as of 01 of July 2016]. In: Ministério do Planejamento Orçamento e Gestão, editor.: Instituto Brasileiro de Geografia e Estatística (IBGE); 2016.
5. The World Bank. Poverty & Equity, Country Dashboard, Brazil Washington DC2016 [cited 2016 May]. http://povertydata.worldbank.org/poverty/country/BRA.
6. Adler B, Vaccines against leptospirosis. Curr Top Microbiol Immunol. 2015;387:251–72. doi: 10.1007/978-3-662-45059-8_10 25388138
7. Ellis WA, Animal leptospirosis. Curr Top Microbiol Immunol. 2015;387:99–137. doi: 10.1007/978-3-662-45059-8_6 25388134
8. Adler B, Faine S, The antibodies involved in the human immune response to leptospiral infection. J Med Microbiol. 1978;11(4):387–400. doi: 10.1099/00222615-11-4-387 722781
9. Jost BH, Adler B, Faine S, Experimental immunisation of hamsters with lipopolysaccharide antigens of Leptospira interrogans. J Med Microbiol. 1989;29(2):115–20. doi: 10.1099/00222615-29-2-115 2733021
10. Sonrier C, Branger C, Michel V, Ruvoen-Clouet N, Ganiere JP, Andre-Fontaine G, Evidence of cross-protection within Leptospira interrogans in an experimental model. Vaccine. 2000;19(1):86–94. Epub 2000/08/05. 10924790
11. Dellagostin OA, Grassmann AA, Hartwig DD, Felix SR, da Silva EF, McBride AJ, Recombinant vaccines against leptospirosis. Hum Vaccin. 2011;7(11):1215–24. Epub 2011/11/04. doi: 10.4161/hv.7.11.17944 22048111
12. Branger C, Sonrier C, Chatrenet B, Klonjkowski B, Ruvoen-Clouet N, Aubert A, et al. Identification of the hemolysis-associated protein 1 as a cross-protective immunogen of Leptospira interrogans by adenovirus-mediated vaccination. Infect Immun. 2001;69(11):6831–8. Epub 2001/10/13. doi: 10.1128/IAI.69.11.6831-6838.2001 11598056
13. Haake DA, Mazel MK, McCoy AM, Milward F, Chao G, Matsunaga J, et al. Leptospiral outer membrane proteins OmpL1 and LipL41 exhibit synergistic immunoprotection. Infect Immun. 1999;67(12):6572–82. 10569777
14. Branger C, Chatrenet B, Gauvrit A, Aviat F, Aubert A, Bach JM, et al. Protection against Leptospira interrogans sensu lato challenge by DNA immunization with the gene encoding hemolysin-associated protein 1. Infect Immun. 2005;73(7):4062–9. Epub 2005/06/24. doi: 10.1128/IAI.73.7.4062-4069.2005 15972494
15. Matsunaga J, Barocchi MA, Croda J, Young TA, Sanchez Y, Siqueira I, et al. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol Microbiol. 2003;49(4):929–45. doi: 10.1046/j.1365-2958.2003.03619.x 12890019
16. Palaniappan RU, Chang YF, Jusuf SS, Artiushin S, Timoney JF, McDonough SP, et al. Cloning and molecular characterization of an immunogenic LigA protein of Leptospira interrogans. Infect Immun. 2002;70(11):5924–30. doi: 10.1128/IAI.70.11.5924-5930.2002 12379666
17. Hamburger ZA, Brown MS, Isberg RR, Bjorkman PJ, Crystal structure of invasin: a bacterial integrin-binding protein. Science. 1999;286(5438):291–5. 10514372
18. Luo Y, Frey EA, Pfuetzner RA, Creagh AL, Knoechel DG, Haynes CA, et al. Crystal structure of enteropathogenic Escherichia coli intimin-receptor complex. Nature. 2000;405(6790):1073–7. doi: 10.1038/35016618 10890451
19. Koizumi N, Watanabe H, Leptospiral immunoglobulin-like proteins elicit protective immunity. Vaccine. 2004;22(11–12):1545–52. doi: 10.1016/j.vaccine.2003.10.007 15063580
20. Adler B, de la Pena Moctezuma A,. Leptospira and leptospirosis. Vet Microbiol. 2010;140(3–4):287–96. Epub 2009/04/07. doi: 10.1016/j.vetmic.2009.03.012 19345023
21. Palaniappan RU, McDonough SP, Divers TJ, Chen CS, Pan MJ, Matsumoto M, et al. Immunoprotection of recombinant leptospiral immunoglobulin-like protein A against Leptospira interrogans serovar Pomona infection. Infect Immun. 2006;74(3):1745–50. doi: 10.1128/IAI.74.3.1745-1750.2006 16495547
22. Silva EF, Medeiros MA, McBride AJ, Matsunaga J, Esteves GS, Ramos JG, et al. The terminal portion of leptospiral immunoglobulin-like protein LigA confers protective immunity against lethal infection in the hamster model of leptospirosis. Vaccine. 2007;25(33):6277–86. doi: 10.1016/j.vaccine.2007.05.053 17629368
23. Ko AI, Galvao Reis M, Ribeiro Dourado CM, Johnson WD, JrRiley LW, Urban epidemic of severe leptospirosis in Brazil. Salvador Leptospirosis Study Group. Lancet. 1999;354(9181):820–5. 10485724
24. Green MR, Sambrook J, Molecular Cloning: A Laboratory Manual. 4th ed. Cold Spring Harbor, New York, USA: Cold Spring Harbor Laboratory Press; 2012.
25. Coutinho ML, Choy HA, Kelley MM, Matsunaga J, Babbitt JT, Lewis MS, et al. A LigA three-domain region protects hamsters from lethal infection by Leptospira interrogans. PLoS Negl Trop Dis. 2011;5(12):e1422. Epub 2011/12/20. doi: 10.1371/journal.pntd.0001422 22180800
26. Reed LJ, Muench H, A simple method of estimating fifty percent endpoints. Am J Hyg. 1938;27:493–7.
27. WHOILSHuman leptospirosis: guidance for diagnosis, surveillance and control. Malta: World Health Organization; 2003.
28. Bandeira M, Santos CS, de Azevedo EC, Soares LM, Macedo JO, Marchi S, et al. Attenuated nephritis in inducible nitric oxide synthase knockout C57BL/6 mice and pulmonary hemorrhage in CB17 SCID and recombination activating gene 1 knockout C57BL/6 mice infected with Leptospira interrogans. Infect Immun. 2011;79(7):2936–40. Epub 2011/05/18. doi: 10.1128/IAI.05099-11 21576342
29. Crowther JR, ELISA. Theory and practice. Methods Mol Biol. 1995;42:1–218. 7655571
30. Chagas-Junior AD, da Silva CL, Soares LM, Santos CS, Silva CD, Athanazio DA, et al. Detection and quantification of Leptospira interrogans in hamster and rat kidney samples: immunofluorescent imprints versus real-time PCR. PLoS One. 2012;7(2):e32712. doi: 10.1371/journal.pone.0032712 22393440
31. Fouts DE, Matthias MA, Adhikarla H, Adler B, Amorim-Santos L, Berg DE, et al. What makes a bacterial species pathogenic?: Comparative genomic analysis of the genus Leptospira. PLoS Negl Trop Dis. 2016;10(2):e0004403. doi: 10.1371/journal.pntd.0004403 26890609
32. Cerqueira GM, McBride AJ, Hartskeerl RA, Ahmed N, Dellagostin OA, Eslabao MR, et al. Bioinformatics describes novel loci for high resolution discrimination of Leptospira isolates. PLoS One. 2010;5(10):e15335. Epub 2010/12/03. doi: 10.1371/journal.pone.0015335 21124728
33. McBride AJ, Cerqueira GM, Suchard MA, Moreira AN, Zuerner RL, Reis MG, et al. Genetic diversity of the leptospiral immunoglobulin-like (Lig) genes in pathogenic Leptospira spp. Infect Genet Evol. 2009;9(2):196–205. Epub 2008/11/26. doi: 10.1016/j.meegid.2008.10.012 19028604
34. Orenstein WA, Bernier RH, Dondero TJ, Hinman AR, Marks JS, Bart KJ, et al. Field evaluation of vaccine efficacy. Bull World Health Organ. 1985;63(6):1055–68. 3879673
35. Chagas-Junior AD, McBride AJ, Athanazio DA, Figueira CP, Medeiros MA, Reis MG, et al. An imprint method for detecting leptospires in the hamster model of vaccine-mediated immunity for leptospirosis. J Med Microbiol. 2009;58(Pt 12):1632–7. Epub 2009/08/15. doi: 10.1099/jmm.0.014050-0 19679685
36. Lourdault K, Wang LC, Vieira A, Matsunaga J, Melo R, Lewis MS, et al. Oral immunization with Escherichia coli expressing a lipidated form of LigA protects hamsters against challenge with Leptospira interrogans serovar Copenhageni. Infect Immun. 2014;82(2):893–902. doi: 10.1128/IAI.01533-13 24478102
37. Faisal SM, Yan W, McDonough SP, Chang YF, Leptospira immunoglobulin-like protein A variable region (LigAvar) incorporated in liposomes and PLGA microspheres produces a robust immune response correlating to protective immunity. Vaccine. 2009;27(3):378–87. Epub 2008/11/22. doi: 10.1016/j.vaccine.2008.10.089 19022317
38. Faisal SM, Yan W, Chen CS, Palaniappan RU, McDonough SP, Chang YF, Evaluation of protective immunity of Leptospira immunoglobulin like protein A (LigA) DNA vaccine against challenge in hamsters. Vaccine. 2008;26(2):277–87. doi: 10.1016/j.vaccine.2007.10.029 18055070
39. Bacelo KL, Hartwig DD, Seixas FK, Schuch R, Moreira Ada S, Amaral M, et al. Xanthan gum as an adjuvant in a subunit vaccine preparation against leptospirosis. BioMed research international. 2014;2014:636491. doi: 10.1155/2014/636491 24895594
40. Cerqueira GM, McBride AJ, Picardeau M, Ribeiro SG, Moreira AN, Morel V, et al. Distribution of the leptospiral immunoglobulin-like (lig) genes in pathogenic Leptospira species and application of ligB to typing leptospiral isolates. J Med Microbiol. 2009;58(Pt 9):1173–81. Epub 2009/06/17. doi: 10.1099/jmm.0.009175-0 19528180
41. Yan W, Faisal SM, McDonough SP, Divers TJ, Barr SC, Chang CF, et al. Immunogenicity and protective efficacy of recombinant Leptospira immunoglobulin-like protein B (rLigB) in a hamster challenge model. Microbes Infect. 2009;11(2):230–7. Epub 2008/12/17. doi: 10.1016/j.micinf.2008.11.008 19070678
42. Murray GL, Lo M, Bulach DM, Srikram A, Seemann T, Quinsey NS, et al. Evaluation of 238 antigens of Leptospira borgpetersenii serovar Hardjo for protection against kidney colonisation. Vaccine. 2013;31(3):495–9. doi: 10.1016/j.vaccine.2012.11.028 23176980
43. Srinivas GB, Walker A, Rippke B, USDA regulatory guidelines and practices for veterinary Leptospira vaccine potency testing. Biologicals: journal of the International Association of Biological Standardization. 2013;41(5):298–302.
44. Rawlins J, Portanova A, Zuckerman I, Loftis A, Ceccato P, Willingham AL, et al. Molecular detection of leptospiral DNA in environmental water on St. Kitts. Int J Environ Res Public Health. 2014;11(8):7953–60. doi: 10.3390/ijerph110807953 25105546
45. Vein J, Perrin A, Berny PJ, Benoit E, Leblond A, Kodjo A, Adaptation of a real-time PCR method for the detection and quantification of pathogenic leptospires in environmental water. Can J Microbiol. 2012;58(7):828–35. doi: 10.1139/w2012-060 22698616
46. Viau EJ, Boehm AB, Quantitative PCR-based detection of pathogenic Leptospira in Hawaiian coastal streams. J Water Health. 2011;9(4):637–46. Epub 2011/11/04. doi: 10.2166/wh.2011.064 22048423
47. Ganoza CA, Matthias MA, Collins-Richards D, Brouwer KC, Cunningham CB, Segura ER, et al. Determining risk for severe leptospirosis by molecular analysis of environmental surface waters for pathogenic Leptospira. PLoS Med. 2006;3(8):e308. doi: 10.1371/journal.pmed.0030308 16933963
48. Murphy KP, Janeway's Immunobiology. 8th ed. New York: Garland Science; 2012.
49. Coe JE, The immune response in the hamster. II. Studies on IgM. Immunology. 1970;18(2):223–36. 5416639
50. Coe JE, The immune response in the hamster. I. Definition of two 7 S globulin classes: 7 S-gamma-1 and 7 S-gamma-2. J Immunol. 1968;100(3):507–15. 4966837
51. Coe JE, Schell RF, Ross MJ, Immune response in the hamster: definition of a novel IgG not expressed in all hamster strains. Immunology. 1995;86(1):141–8. 7590875
52. McGuire KL, Duncan WR, Tucker PW, Phylogenetic conservation of immunoglobulin heavy chains: direct comparison of hamster and mouse Cmu genes. Nucleic Acids Res. 1985;13(15):5611–28. 2994005
53. Coe JE, Bell JF, Antibody response to rabies virus in Syrian hamsters. Infect Immun. 1977;16(3):915–9. 330398
54. Melby PC, Chandrasekar B, Zhao W, Coe JE, The hamster as a model of human visceral leishmaniasis: progressive disease and impaired generation of nitric oxide in the face of a prominent Th1-like cytokine response. J Immunol. 2001;166(3):1912–20. 11160239
55. Portis JL, Coe JE, Immune response in the hamster. VIII. Ig class differences in susceptibility to tolerance induction. J Immunol. 1976;117(3):835–40. 956656
56. He P, Zou Y, Hu Z, Advances in aluminum hydroxide-based adjuvant research and its mechanism. Hum Vaccin Immunother. 2015;11(2):477–88. doi: 10.1080/21645515.2014.1004026 25692535
57. Figueira CP, Croda J, Choy HA, Haake DA, Reis MG, Ko AI, et al. Heterologous expression of pathogen-specific genes ligA and ligB in the saprophyte Leptospira biflexa confers enhanced adhesion to cultured cells and fibronectin. BMC Microbiol. 2011;11:129. Epub 2011/06/11. doi: 10.1186/1471-2180-11-129 21658265
58. Lin YP, Chang YF, The C-terminal variable domain of LigB from Leptospira mediates binding to fibronectin. J Vet Sci. 2008;9(2):133–44. doi: 10.4142/jvs.2008.9.2.133 18487934
59. Choy HA, Kelley MM, Chen TL, Moller AK, Matsunaga J, Haake DA, Physiological osmotic induction of Leptospira interrogans adhesion: LigA and LigB bind extracellular matrix proteins and fibrinogen. Infect Immun. 2007;75(5):2441–50. doi: 10.1128/IAI.01635-06 17296754
60. Lin YP, Chang YF, A domain of the Leptospira LigB contributes to high affinity binding of fibronectin. Biochem Biophys Res Commun. 2007;362(2):443–8. doi: 10.1016/j.bbrc.2007.07.196 17707344
61. Castiblanco-Valencia MM, Fraga TR, Pagotto AH, Serrano SM, Abreu PA, Barbosa AS, et al. Plasmin cleaves fibrinogen and the human complement proteins C3b and C5 in the presence of Leptospira interrogans proteins: A new role of LigA and LigB in invasion and complement immune evasion. Immunobiology. 2016;221(5):679–89. doi: 10.1016/j.imbio.2016.01.001 26822552
62. Castiblanco-Valencia MM, Fraga TR, Silva LB, Monaris D, Abreu PA, Strobel S, et al. Leptospiral immunoglobulin-like proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP. J Infect Dis. 2012;205(6):995–1004. doi: 10.1093/infdis/jir875 22291192
63. Breda LC, Hsieh CL, Castiblanco Valencia MM, da Silva LB, Barbosa AS, Blom AM, et al. Fine Mapping of the Interaction between C4b-Binding Protein and Outer Membrane Proteins LigA and LigB of Pathogenic Leptospira interrogans. PLoS Negl Trop Dis. 2015;9(10):e0004192. doi: 10.1371/journal.pntd.0004192 26517116
64. Choy HA, Kelley MM, Croda J, Matsunaga J, Babbitt JT, Ko AI, et al. The multifunctional LigB adhesin binds homeostatic proteins with potential roles in cutaneous infection by pathogenic Leptospira interrogans. PLoS One. 2011;6(2):e16879. Epub 2011/02/25. doi: 10.1371/journal.pone.0016879 21347378
65. Choy HA, Multiple activities of LigB potentiate virulence of Leptospira interrogans: inhibition of alternative and classical pathways of complement. PLoS One. 2012;7(7):e41566. doi: 10.1371/journal.pone.0041566 22911815