A Listeria monocytogenes-based vaccine that secretes sand fly salivary protein LJM11 confers long-term protection against vector-transmitted Leishmania major

Infection and Immunity

Volumn 82, Issue 7, 2014, Pages 2736-2745

  Abi Abdallah, Delbert S ^a   Bitar, Alan Pavinski ^a   Oliveira, Fabiano ^b   Meneses, Claudio ^b   Park, Justin J ^a   Mendez, Susana ^a,b   Kamhawi, Shaden ^b   Valenzuela, Jesus G ^b   Marquis, Hélène ^a  

^a Department of Microbiology and Immunology Cornell University ^*  (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 10; LJM11 PROTEIN; SALIVA PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FLOW CYTOMETRY; GENE EXPRESSION SYSTEM; LEISHMANIA MAJOR; LISTERIA MONOCYTOGENES; MOUSE; NONHUMAN; PARASITE CONTROL; PRIORITY JOURNAL; SCAR; SKIN LEISHMANIASIS; T LYMPHOCYTE;

ANIMALS; BITES AND STINGS; EAR, EXTERNAL; INSECT PROTEINS; INSECT VECTORS; LEISHMANIA MAJOR; LEISHMANIASIS VACCINES; LEISHMANIASIS, CUTANEOUS; LISTERIA MONOCYTOGENES; MICE; MICE, INBRED C57BL; PSYCHODIDAE; SALIVARY PROTEINS AND PEPTIDES; T-LYMPHOCYTES; VACCINES, SYNTHETIC;

EID: 84903168395     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01633-14     Document Type: Article

References (50)

1. Alvar J, Velez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, den Boer M. 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7:e35671. http://dx.doi.org/10.1371/journal.pone.0035671.
2. Gomes R, Oliveira F. 2012. The immune response to sand fly salivary proteins and its influence on Leishmania immunity. Front. Immunol. 3:110. http://dx.doi.org/10.3389/fimmu.2012.00110.
3. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, Rowton E, Ribeiro J, Sacks DL. 1998. Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J. Exp. Med. 188:1941-1953. http://dx.doi.org/10.1084/jem.188.10.1941.
4. Titus RG, Ribeiro JM. 1988. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239:1306-1308. http://dx.doi.org/10.1126/science.3344436.
5. Andrade BB, de Oliveira CI, Brodskyn CI, Barral A, Barral-Netto M. 2007. Role of sand fly saliva in human and experimental leishmaniasis: current insights. Scand. J. Immunol. 66:122-127. http://dx.doi.org/10.1111/j.1365-3083.2007.01964.x.
6. Kamhawi S, Belkaid Y, Modi G, Rowton E, Sacks D. 2000. Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290:1351-1354. http://dx.doi.org/10.1126/science.290.5495.1351.
7. Anderson JM, Samake S, Jaramillo-Gutierrez G, Sissoko I, Coulibaly CA, Traore B, Soucko C, Guindo B, Diarra D, Fay MP, Lawyer PG, Doumbia S, Valenzuela JG, Kamhawi S. 2011. Seasonality and prevalence of Leishmania major infection in Phlebotomus duboscqi Neveu-Lemaire from two neighboring villages in central Mali. PLoS Negl. Trop. Dis. 5:e1139. http://dx.doi.org/10.1371/journal.pntd.0001139.
8. Aronson SM. 2007. The Bagdad boil deploys to the United States. Med. Health R. I. 90:231.
9. Bhutto AM, Soomro RA, Nonaka S, Hashiguchi Y. 2003. Detection of new endemic areas of cutaneous leishmaniasis in Pakistan: a 6-year study. Int. J. Dermatol. 42:543-548. http://dx.doi.org/10.1046/j.1365-4362.2003.01818.x.
10. Jacobson RL. 2011. Leishmaniasis in an era of conflict in the Middle East. Vector Borne Zoonotic Dis. 11:247-258. http://dx.doi.org/10.1089/vbz.2010.0068.
11. Pavli A, Maltezou HC. 2010. Leishmaniasis, an emerging infection in travelers. Int. J. Infect. Dis. 14:e1032-1039. http://dx.doi.org/10.1016/j.ijid.2010.06.019.
12. Postigo JA. 2010. Leishmaniasis in the World Health Organization eastern Mediterranean region. Int. J. Antimicrob. Agents 36(Suppl 1):S62-S65. http://dx.doi.org/10.1016/j.ijantimicag.2010.06.023.
13. Reyburn H, Rowland M, Mohsen M, Khan B, Davies C. 2003. The prolonged epidemic of anthroponotic cutaneous leishmaniasis in Kabul, Afghanistan: "bringing down the neighbourhood." Trans. R. Soc. Trop. Med. Hyg. 97:170-176. http://dx.doi.org/10.1016/S0035-9203(03)90111-8.
14. van Thiel PP, Leenstra T, de Vries HJ, van der Sluis A, van Gool T, Krull AC, van Vugt M, de Vries PJ, Zeegelaar JE, Bart A, van der Meide WF, Schallig HD, Faber WR, Kager PA. 2010. Cutaneous leishmaniasis (Leishmania major infection) in Dutch troops deployed in northern Afghanistan: epidemiology, clinical aspects, and treatment. Am. J. Trop. Med. Hyg. 83:1295-1300. http://dx.doi.org/10.4269/ajtmh.2010.10-0143.
15. Yaghoobi-Ershadi MR, Jafari R, Hanafi-Bojd AA. 2004. A new epidemic focus of zoonotic cutaneous leishmaniasis in central Iran. Ann. Saudi Med. 24:98-101.
16. Gomes R, Oliveira F, Teixeira C, Meneses C, Gilmore DC, Elnaiem DE, Kamhawi S, Valenzuela JG. 2012. Immunity to sand fly salivary protein LJM11 modulates host response to vector-transmitted Leishmania conferring ulcer-free protection. J. Investig. Dermatol. 132:2735-2743. http://dx.doi.org/10.1038/jid.2012.205.
17. Gomes R, Teixeira C, Teixeira MJ, Oliveira F, Menezes MJ, Silva C, de Oliveira CI, Miranda JC, Elnaiem DE, Kamhawi S, Valenzuela JG, Brodskyn CI. 2008. Immunity to a salivary protein of a sand fly vector protects against the fatal outcome of visceral leishmaniasis in a hamster model. Proc. Natl. Acad. Sci. U. S. A. 105:7845-7850. http://dx.doi.org/10.1073/pnas.0712153105.
18. Oliveira F, Lawyer PG, Kamhawi S, Valenzuela JG. 2008. Immunity to distinct sand fly salivary proteins primes the anti-Leishmania immune response towards protection or exacerbation of disease. PLoS Negl. Trop. Dis. 2:e226. http://dx.doi.org/10.1371/journal.pntd.0000226.
19. Tavares NM, Silva RA, Costa DJ, Pitombo MA, Fukutani KF, Miranda JC, Valenzuela JG, Barral A, de Oliveira CI, Barral-Netto M, Brodskyn C. 2011. Lutzomyia longipalpis saliva or salivary protein LJM19 protects against Leishmania braziliensis and the saliva of its vector, Lutzomyia intermedia. PLoS Negl. Trop. Dis. 5:e1169. http://dx.doi.org/10.1371/journal.pntd.0001169.
20. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, Sacks D. 2000. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J. Immunol. 165:969-977.
21. Sacks D, Noben-Trauth N. 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2:845-858. http://dx.doi.org/10.1038/nri933.
22. Tilney LG, Portnoy DA. 1989. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes. J. Cell Biol. 109:1597-1608. http://dx.doi.org/10.1083/jcb.109.4.1597.
23. Mackaness GB. 1962. Cellular resistance to infection. J. Exp. Med. 116: 381-406. http://dx.doi.org/10.1084/jem.116.3.381.
24. Pamer EG. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4:812-823. http://dx.doi.org/10.1038/nri1461.
25. Brockstedt DG, Dubensky TW. 2008. Promises and challenges for the development of Listeria monocytogenes-based immunotherapies. Expert Rev. Vaccines 7:1069-1084. http://dx.doi.org/10.1586/14760584.7.7.1069.
26. Gravekamp C, Paterson Y. 2010. Harnessing Listeria monocytogenes to target tumors. Cancer Biol. Ther. 9:257-265. http://dx.doi.org/10.4161/cbt.9.4.11216.
27. Le DT, Dubenksy TW, Jr, Brockstedt DG. 2012. Clinical development of Listeria monocytogenes-based immunotherapies. Semin. Oncol. 39:311-322. http://dx.doi.org/10.1053/j.seminoncol.2012.02.008.
28. Brundage RA, Smith GA, Camilli A, Theriot JA, Portnoy DA. 1993. Expression and phosphorylation of the Listeria monocytogenes ActA protein in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 90:11890-11894. http://dx.doi.org/10.1073/pnas.90.24.11890.
29. Kocks C, Gouin E, Tabouret M, Berche P, Ohayon H, Cossart P. 1992. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 68:521-531.
30. Brockstedt DG, Giedlin MA, Leong ML, Bahjat KS, Gao Y, Luckett W, Liu W, Cook DN, Portnoy DA, Dubensky TW, Jr. 2004. Listeria-based cancer vaccines that segregate immunogenicity from toxicity. Proc. Natl. Acad. Sci. U. S. A. 101:13832-13837. http://dx.doi.org/10.1073/pnas.0406035101.
31. Crimmins GT, Herskovits AA, Rehder K, Sivick KE, Lauer P, Dubensky TW, Jr, Portnoy DA. 2008. Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc. Natl. Acad. Sci. U. S. A. 105:10191-10196. http://dx.doi.org/10.1073/pnas.0804170105.
32. Auerbuch V, Brockstedt DG, Meyer-Morse N, O'Riordan M, Portnoy DA. 2004. Mice lacking the type I interferon receptor are resistant to Listeria monocytogenes. J. Exp. Med. 200:527-533. http://dx.doi.org/10.1084/jem.20040976.
33. Rayamajhi M, Humann J, Penheiter K, Andreasen K, Lenz LL. 2010. Induction of IFN-alphabeta enables Listeria monocytogenes to suppress macrophage activation by IFN-gamma. J. Exp. Med. 207:327-337. http://dx.doi.org/10.1084/jem.20091746.
34. Camilli A, Tilney LG, Portnoy DA. 1993. Dual roles of plcA in Listeria monocytogenes pathogenesis. Mol. Microbiol. 8:143-157. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01211.x.
35. Snyder A, Marquis H. 2003. Restricted translocation across the cell wall regulates secretion of the broad-range phospholipase C of Listeria monocytogenes. J. Bacteriol. 185:5953-5958. http://dx.doi.org/10.1128/JB.185.20.5953-5958.2003.
36. Marquis H. 2006. Tissue culture cell assays used to analyze Listeria monocytogenes, p 9B.4.1-9B.4.24. In Downey T (ed), Current protocols in microbiology. John Wiley & Sons, Inc., Hoboken, NJ.
37. Mendez S, Gurunathan S, Kamhawi S, Belkaid Y, Moga MA, Skeiky YA, Campos-Neto A, Reed S, Seder RA, Sacks D. 2001. The potency and durability of DNA-and protein-based vaccines against Leishmania major evaluated using low-dose, intradermal challenge. J. Immunol. 166:5122-5128.
38. Abi Abdallah DS, Egan CE, Butcher BA, Denkers EY. 2011. Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int. Immunol. 23:317-326. http://dx.doi.org/10.1093/intimm/dxr007.
39. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
40. Anderson CF, Oukka M, Kuchroo VJ, Sacks D. 2007. CD4(+)CD25(-) Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204:285-297. http://dx.doi.org/10.1084/jem.20061886.
41. Darrah PA, Hegde ST, Patel DT, Lindsay RW, Chen L, Roederer M, Seder RA. 2010. IL-10 production differentially influences the magnitude, quality, and protective capacity of Th1 responses depending on the vaccine platform. J. Exp. Med. 207:1421-1433. http://dx.doi.org/10.1084/jem.20092532.
42. Stober CB, Lange UG, Roberts MT, Alcami A, Blackwell JM. 2005. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J. Immunol. 175:2517-2524.
43. Xu X, Oliveira F, Chang BW, Collin N, Gomes R, Teixeira C, Reynoso D, My Pham V, Elnaiem DE, Kamhawi S, Ribeiro JM, Valenzuela JG, Andersen JF. 2011. Structure and function of a "yellow" protein from saliva of the sand fly Lutzomyia longipalpis that confers protective immunity against Leishmania major infection. J. Biol. Chem. 286:32383-32393. http://dx.doi.org/10.1074/jbc.M111.268904.
44. Kupper TS. 2012. Old and new: recent innovations in vaccine biology and skin T cells. J. Investig. Dermatol. 132:829-834. http://dx.doi.org/10.1038/jid.2011.400.
45. Larregina AT, Falo LD, Jr. 2005. Changing paradigms in cutaneous immunology: adapting with dendritic cells. J. Investig. Dermatol. 124:1-12. http://dx.doi.org/10.1111/j.1523-1747.2004.23554.x.
46. Sigmundsdottir H, Butcher EC. 2008. Environmental cues, dendritic cells and the programming of tissue-selective lymphocyte trafficking. Nat. Immunol. 9:981-987. http://dx.doi.org/10.1038/ni.f.208.
47. Rogers ME. 2012. The role of Leishmania proteophosphoglycans in sand fly transmission and infection of the mammalian host. Front. Microbiol. 3:223. http://dx.doi.org/10.3389/fmicb.2012.00223.
48. McSorley S, Proudfoot L, O'Donnell CA, Liew FY. 1996. Immunology of murine leishmaniasis. Clin. Dermatol. 14:451-464. http://dx.doi.org/10.1016/0738-081X(96)00037-5.
49. Novais FO, Carvalho LP, Graff JW, Beiting DP, Ruthel G, Roos DS, Betts MR, Goldschmidt MH, Wilson ME, de Oliveira CI, Scott P. 2013. Cytotoxic T cells mediate pathology and metastasis in cutaneous leishmaniasis. PLoS Pathog. 9:e1003504. http://dx.doi.org/10.1371/journal.ppat.1003504.
50. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, Flynn BJ, Hoff ST, Andersen P, Reed SG, Morris SL, Roederer M, Seder RA. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850. http://dx.doi.org/10.1038/nm1592.