Oral immunization with escherichia coli expressing a lipidated form of LigA protects hamsters against challenge with leptospira interrogans serovar Copenhageni

Infection and Immunity

Volumn 82, Issue 2, 2014, Pages 893-902

  Lourdault, Kristel ^a,b   Wang, Long Chieh ^a   Vieira, Ana ^c   Matsunaga, James ^a,b   Melo, Rita ^c   Lewis, Michael S ^a   Haake, David A ^a,b   Gomes Soleckie, Maria ^d  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d Biopeptides Corp   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN LIGA; IMMUNOGLOBULIN G; LIVE VACCINE; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; CELL SURVIVAL; CONTROLLED STUDY; DRUG DOSE; DRUG EFFICACY; DRUG SYNTHESIS; ESCHERICHIA COLI; FEMALE; HAMSTER; HAMSTER MODEL; HISTOPATHOLOGY; HUMAN; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; LEPTOSPIRA INTERROGANS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROTYPE;

ADMINISTRATION, ORAL; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; CRICETINAE; DISEASE MODELS, ANIMAL; DNA LIGASES; DRUG CARRIERS; ESCHERICHIA COLI; FEMALE; IMMUNIZATION; IMMUNOGLOBULIN G; LEPTOSPIRA INTERROGANS; LEPTOSPIROSIS; MESOCRICETUS; SURVIVAL ANALYSIS;

EID: 84892953246     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01533-13     Document Type: Article

References (44)

1. Levett PN. 2001. Leptospirosis. Clin. Microbiol. Rev. 14:296-326. http: //dx.doi.org/10.1128/CMR.14.2.296-326.2001.
2. Faine S, Adler B, Bolin C, Perolat P. 1999. Leptospira and leptospirosis, 2nd ed. MediSci, Melbourne, Australia.
3. Weil A. 1886. Ueber eine eigenthümliche, mit milztumor, icterus und nephritis einhergehende, acute infectionskrankheit. Dtsch. Arch. Klin. Med. 39:209.
4. McBride AJ, Athanazio DA, Reis MG, Ko AI. 2005. Leptospirosis. Curr. Opin. Infect. Dis. 18:376-386. http://dx.doi.org/10.1097/01.qco.0000178824 .05715.2c.
5. Hartskeerl RA, Collares-Pereira M, Ellis WA. 2011. Emergence, control and re-emerging leptospirosis: dynamics of infection in the changing world. Clin. Microbiol. Infect. 17:494-501. http://dx.doi.org/10.1111/j .1469-0691.2011.03474.x.
6. WHO. 2003. Human leptospirosis: guidance for diagnosis, surveillance and control. WHO, Geneva, Switzerland.
7. Ko AI, Galvao Reis M, Ribeiro Dourado CM, Johnson WD, Jr, Riley LW, Salvador Leptospirosis Study Group. 1999. Urban epidemic of severe leptospirosis in Brazil. Lancet 354:820-825. http://dx.doi.org/10 .1016/S0140-6736(99)80012-9.
8. Martínez Sanchez R, Obregon Fuentes AM, Perez Sierra A, Baly Gil A, Diaz Gonzalez M, Baro Suarez M, Menendez Capote R, Ruiz Perez A, Sierra Gonzalez G, Lopez Chavez AU. 1998. The reactogenicity and immunogenicity of the first Cuban vaccine against human leptospirosis. Rev. Cuba. Med. Trop. 50:159-166.
9. Baranton G. 1990. The human vaccine against Leptospirosis icterohaemorrhagiae. An effective vaccine which concerns only exposed subjects. Rev. Prat. Med. Gen. 93:17-19.
10. Koizumi N, Watanabe H. 2005. Leptospirosis vaccines: past, present, and future. J. Postgrad. Med. 51:210-214.
11. Lycke N. 2012. Recent progress in mucosal vaccine development: potential and limitations. Nat. Rev. Immunol. 12:592-605. http://dx.doi.org/10 .1038/nri3251.
12. del Rio B, Dattwyler RJ, Aroso M, Neves V, Meirelles L, Seegers JF, Gomes-Solecki MJ. 2008. Oral immunization with recombinant lactobacillus plantarum induces a protective immune response in mice with Lyme disease. Clin. Vaccine Immunol. 15:1429-1435. http://dx.doi.org/10.1128 /CVI.00169-08.
13. Holmgren J, Svennerholm AM. 2012. Vaccines against mucosal infections. Curr. Opin. Immunol. 24:343-353. http://dx.doi.org/10.1016/j.coi .2012.03.014.
14. Scheckelhoff MR, Telford SR, Hu LT. 2006. Protective efficacy of an oral vaccine to reduce carriage of Borrelia burgdorferi (strain N40) in mouse and tick reservoirs. Vaccine 24:1949-1957. http://dx.doi.org/10.1016/j .vaccine.2005.10.044.
15. Gomes-Solecki MJ, Brisson DR, Dattwyler RJ. 2006. Oral vaccine that breaks the transmission cycle of the Lyme disease spirochete can be delivered via bait. Vaccine 24:4440-4449. http://dx.doi.org/10.1016/j.vaccine .2005.08.089.
16. Erdile LF, Brandt MA, Warakomski DJ, Westrack GJ, Sadziene A, Barbour AG, Mays JP. 1993. Role of attached lipid in immunogenicity of Borrelia burgdorferi OspA. Infect. Immun. 61:81-90.
17. Erdile LF, Guy B. 1997. OspA lipoprotein of Borrelia burgdorferi is a mucosal immunogen and adjuvant. Vaccine 15:988-996. http://dx.doi .org/10.1016/S0264-410X(96)00295-2.
18. Weis JJ, Ma Y, Erdile LF. 1994. Biological activities of native and recombinant Borrelia burgdorferi outer surface protein A: dependence on lipid modification. Infect. Immun. 62:4632-4636.
19. del Rio B, Seegers JF, Gomes-Solecki MJ. 2010. Immune response to Lactobacillus plantarum expressing Borrelia burgdorferi OspA is modulated by the lipid modification of the antigen. PLoS One 5:e11199. http: //dx.doi.org/10.1371/journal.pone.0011199.
20. Haake DA, Matsunaga J. 2010. Leptospira: a spirochaete with a hybrid outer membrane. Mol. Microbiol. 77:805-814. http://dx.doi.org/10.1111 /j.1365-2958.2010.07262.x.
21. Nally JE, Whitelegge JP, Blanco SBDR, Lovett MA. 2007. Characterization of the outer membrane proteome of Leptospira interrogans expressed during acute lethal infection. Infect. Immun. 75:766-773. http://dx.doi .org/10.1128/IAI.00741-06.
22. Matsunaga J, Barocchi MA, Croda J, Young TA, Sanchez Y, Siqueira I, Bolin CA, Reis MG, Riley LW, Haake DA, Ko AI. 2003. Pathogenic Leptospira species express surface-exposed proteins belonging to the bacterial immunoglobulin superfamily. Mol. Microbiol. 49:929-945. http: //dx.doi.org/10.1046/j.1365-2958.2003.03619.x.
23. Matsunaga J, Medeiros MA, Sanchez Y, Werneid KF, Ko AI. 2007. Osmotic regulation of expression of two extracellular matrix-binding proteins and a haemolysin of Leptospira interrogans: differential effects on LigA and Sph2 extracellular release. Microbiology 153:3390-3398. http: //dx.doi.org/10.1099/mic.0.2007/007948-0.
24. Matsunaga J, Schlax PJ, Haake DA. 2013. Role for cis-acting RNA sequences in the temperature-dependent expression of the multiadhesive Lig proteins in Leptospira interrogans. J. Bacteriol. 195:5092-5101. http: //dx.doi.org/10.1128/JB.00663-13.
25. Croda J, Ramos JG, Matsunaga J, Queiroz A, Homma A, Riley LW, Haake DA, Reis MG, Ko AI. 2007. Leptospira immunoglobulin-like proteins as a serodiagnostic marker for acute leptospirosis. J. Clin. Microbiol. 45:1528-1534. http://dx.doi.org/10.1128/JCM.02344-06.
26. Silva EF, Medeiros MA, McBride AJ, Matsunaga J, Esteves GS, Ramos JB, Santos CS, Croda J, Homma A, Dellagostin OA, Haake DA, Reis MG, Ko AI. 2007. The terminal portion of leptospiral immunoglobulinlike protein LigA confers protective immunity against lethal infection in the hamster model of leptospirosis. Vaccine 25:6277-6286. http://dx.doi .org/10.1016/j.vaccine.2007.05.053.
27. Koizumi N, Watanabe H. 2004. Leptospiral immunoglobulin-like proteins elicit protective immunity. Vaccine 22:1545-1552. http://dx.doi.org /10.1016/j.vaccine.2003.10.007.
28. Palaniappan RU, McDonough SP, Divers TJ, Chen CS, Pan MJ, Matsumoto M, Chang YF. 2006. Immunoprotection of recombinant leptospiral immunoglobulin-like protein A against Leptospira interrogans serovar Pomona infection. Infect. Immun. 74:1745-1750. http://dx.doi.org/10 .1128/IAI.74.3.1745-1750.2006.
29. Faisal SM, Yan W, Chen CS, Palaniappan RU, McDonough SP, Chang YF. 2008. Evaluation of protective immunity of Leptospira immunoglob-ulin like protein A (LigA) DNA vaccine against challenge in hamsters. Vaccine 26:277-287. http://dx.doi.org/10.1016/j.vaccine.2007.10.029.
30. Coutinho ML, Choy HA, Haake D. 2011. A LigA three-domain region protects hamsters from lethal infection by Leptospira interrogans. PLoS Neg. Trop. Dis. 5:e1422. http://dx.doi.org/10.1371/journal.pntd.0001422.
31. Ellinghausen HC, McCullough WG. 1965. Nutrition of "Leptospira pomona" and growth of 13 other serotypes: fractionation of oleic albumin complex and a medium of bovine albumin and polysorbate 80. Am. J. Vet. Res. 26:45-51.
32. Johnson RC, Harris VG. 1967. Differentiation of pathogenic and saprophytic letospires. I. Growth at low temperatures. J. Bacteriol. 94:27-31.
33. Miller JN. 1971. Spirochetes in body fluids and tissues: manual of investigative methods. Charles C. Thomas Publisher, Springfield, IL.
34. Nascimento AL, Ko AI, Martins EA, Monteiro-Vitorello CB, Ho PL, Haake DA, Verjovski-Almeida S, Hartskeerl RA, Marques MV, Oliveira MC, Menck CF, Leite LC, Carrer H, Coutinho LL, Degrave WM, Dellagostin OA, El-Dorry H, Ferro ES, Ferro MI, Furlan LR, Gamberini M, Giglioti EA, Goes-Neto A, Goldman GH, Goldman MH, Harakava R, Jeronimo SM, Junqueira-de-Azevedo IL, Kimura ET, Kuramae EE, Lemos EG, Lemos MV, Marino CL, Nunes LR, de Oliveira RC, Pereira GG, Reis MS, Schriefer A, Siqueira WJ, Sommer P, Tsai SM, Simpson AJ, Ferro JA, Camargo LE, Kitajima JP, Setubal JC, Van Sluys MA. 2004. Comparative genomics of two Leptospira interrogans serovars reveals novel insights into physiology and pathogenesis. J. Bacteriol. 186: 2164-2172. http://dx.doi.org/10.1128/JB.186.7.2164-2172.2004.
35. Radolf JD, Chamberlain NR, Clausell A, Norgard MV. 1988. Identification and localization of integral membrane proteins of virulent Treponema pallidum subsp. pallidum by phase partitioning with the nonionic detergent triton X-114. Infect. Immun. 56:490-498.
36. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675. http://dx.doi.org/10 .1038/nmeth.2089.
37. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
38. Stoddard RA, Gee JE, Wilkins PP, McCaustland K, Hoffmaster AR. 2009. Detection of pathogenic Leptospira spp. through TaqMan polymerase chain reaction targeting the LipL32 gene. Diagn. Microbiol. Infect. Dis. 64:247-255. http://dx.doi.org/10.1016/j.diagmicrobio.2009.03.014.
39. Stavitsky AB. 1945. Studies on the pathogenesis of leptospirosis. J. Infect. Dis. 76:179-192. http://dx.doi.org/10.1093/infdis/76.3.179.
40. Lourdault K, Aviat F, Picardeau M. 2009. Use of quantitative real-time PCR for studying the dissemination of Leptospira interrogans in the guinea pig infection model of leptospirosis. J. Med. Microbiol. 58:648-655. http: //dx.doi.org/10.1099/jmm.0.008169-0.
41. Silva EF, Santos CS, Athanazio DA, Seyffert N, Seixas FK, Cerqueira GM, Fagundes MQ, Brod CS, Reis MG, Dellagostin OA, Ko AI. 2008. Characterization of virulence of Leptospira isolates in a hamster model. Vaccine 26:3892-3896. http://dx.doi.org/10.1016/j.vaccine.2008.04.085.
42. Ganoza CA, Matthias MA, Collins-Richards D, Brouwer KC, Cunningham CB, Segura ER, Gilman RH, Gotuzzo E, Vinetz JM. 2006. Determining risk for severe leptospirosis by molecular analysis of environmental surface waters for pathogenic Leptospira. PLoS Med. 3:e308. http://dx .doi.org/10.1371/journal.pmed.0030308.
43. Stoddard RA. 2013. Detection of pathogenic Leptospira spp. through realtime PCR (qPCR) targeting the LipL32 gene. Methods Mol. Biol. 943:257- 266. http://dx.doi.org/10.1007/978-1-60327-353-4_17.
44. Moss B. 1996. Genetically engineered poxviruses for recombinant gene expression, vaccination, and safety. Proc. Natl. Acad. Sci. U. S. A. 93: 11341-11348. http://dx.doi.org/10.1073/pnas.93.21.11341.