Coinjection with TLR2 Agonist Pam3CSK4 Reduces the Pathology of Leishmanization in Mice

PLoS Neglected Tropical Diseases

Volumn 9, Issue 3, 2015, Pages

  Huang, Lu ^a   Hinchman, Meleana ^a   Mendez, Susana ^a  

^a Department of Molecular Biology and Genetics   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 6; MESSENGER RNA; PAM3CSK4; TOLL LIKE RECEPTOR AGONIST; UNCLASSIFIED DRUG; CYTOKINE; LIPOPEPTIDE; PAM(3)CSK(4) PEPTIDE; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; LEISHMANIA MAJOR; MACROPHAGE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PARASITE LOAD; PROMASTIGOTE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; RNA EXTRACTION; SKIN LEISHMANIASIS; TH1 CELL; TH1 TH2 BALANCE; TH17 CELL; AGONISTS; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; C57BL MOUSE; DENDRITIC CELL; IMMUNOLOGY; INJECTION; LEISHMANIASIS, CUTANEOUS; PARASITOLOGY; PATHOLOGY;

ANIMALS; CYTOKINES; DENDRITIC CELLS; INJECTIONS; LEISHMANIASIS, CUTANEOUS; LIPOPEPTIDES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; TOLL-LIKE RECEPTOR 2;

EID: 84928788105     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003546     Document Type: Article

References (52)

1. Desjeux P, (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27: 305–318. 15225981
2. Antinori S, Gianelli E, Calattini S, Longhi E, Gramiccia M, et al. (2005) Cutaneous leishmaniasis: an increasing threat for travellers. Clin Microbiol Infect 11: 343–346. 15819858
3. Milon G, (2009) Perpetuation of Leishmania: some novel insight into elegant developmental programs. Vet Res 40: 38. doi: 10.1051/vetres/2009021 19379663
4. Khamesipour A, Rafati S, Davoudi N, Maboudi F, Modabber F, (2006) Leishmaniasis vaccine candidates for development: a global overview. Indian J Med Res 123: 423–438. 16778321
5. Tabbara KS, (2006) Progress towards a Leishmania vaccine. Saudi Med J 27: 942–950. 16830009
6. Khamesipour A, Dowlati Y, Asilian A, Hashemi-Fesharki R, Javadi A, et al. (2005) Leishmanization: use of an old method for evaluation of candidate vaccines against leishmaniasis. Vaccine 23: 3642–3648. 15882524
7. Janssens S, Beyaert R, (2003) Role of Toll-like receptors in pathogen recognition. Clin Microbiol Rev 16: 637–646. 14557290
8. Arevalo I, Ward B, Miller R, Meng TC, Najar E, et al. (2001) Successful treatment of drug-resistant cutaneous leishmaniasis in humans by use of imiquimod, an immunomodulator. Clin Infect Dis 33: 1847–1851. 11692295
9. Buates S, Matlashewski G, (1999) Treatment of experimental leishmaniasis with the immunomodulators imiquimod and S-28463: efficacy and mode of action. J Infect Dis 179: 1485–1494. 10228071
10. Zimmermann S, Heeg K, Dalpke A, (2003) Immunostimulatory DNA as adjuvant: efficacy of phosphodiester CpG oligonucleotides is enhanced by 3' sequence modifications. Vaccine 21: 990–995. 12547613
11. Zimmermann S, Egeter O, Hausmann S, Lipford GB, Rocken M, et al. (1998) CpG oligodeoxynucleotides trigger protective and curative Th1 responses in lethal murine leishmaniasis. Journal of immunology 160: 3627–3630. 9558060
12. Flynn B, Wang V, Sacks DL, Seder RA, Verthelyi D, (2005) Prevention and treatment of cutaneous leishmaniasis in primates by using synthetic type D/A oligodeoxynucleotides expressing CpG motifs. Infect Immun 73: 4948–4954. 16041009
13. Datta N, Mukherjee S, Das L, Das PK, (2003) Targeting of immunostimulatory DNA cures experimental visceral leishmaniasis through nitric oxide up-regulation and T cell activation. Eur J Immunol 33: 1508–1518. 12778468
14. Mendez S, Tabbara K, Belkaid Y, Bertholet S, Verthelyi D, et al. (2003) Coinjection with CpG-containing immunostimulatory oligodeoxynucleotides reduces the pathogenicity of a live vaccine against cutaneous Leishmaniasis but maintains its potency and durability. Infect Immun 71: 5121–5129. 12933855
15. Wu W, Weigand L, Belkaid Y, Mendez S, (2006) Immunomodulatory effects associated with a live vaccine against Leishmania major containing CpG oligodeoxynucleotides. Eur J Immunol 36: 3238–3247. 17109471
16. Laabs EM, Wu W, Mendez S, (2009) Vaccination with live Leishmania major and CpG DNA promotes interleukin-2 production by dermal dendritic cells and NK cell activation. Clin Vaccine Immunol 16: 1601–1606. doi: 10.1128/CVI.00249-09 19776191
17. Wu W, Huang L, Mendez S, (2010) A live Leishmania major vaccine containing CpG motifs induces the de novo generation of Th17 cells in C57BL/6 mice. Eur J Immunol 40: 2517–2527. doi: 10.1002/eji.201040484 20683901
18. Sakthianandeswaren A, Foote SJ, Handman E, (2009) The role of host genetics in leishmaniasis. Trends Parasitol 25: 383–391. doi: 10.1016/j.pt.2009.05.004 19617002
19. Tripathi P, Singh V, Naik S, (2007) Immune response to leishmania: paradox rather than paradigm. FEMS Immunol Med Microbiol 51: 229–242. 17714488
20. Liang S, Hosur KB, Nawar HF, Russell MW, Connell TD, et al. (2009) In vivo and in vitro adjuvant activities of the B subunit of Type IIb heat-labile enterotoxin (LT-IIb-B5) from Escherichia coli. Vaccine 27: 4302–4308. doi: 10.1016/j.vaccine.2009.05.027 19450646
21. Gallorini S, Berti F, Mancuso G, Cozzi R, Tortoli M, et al. (2009) Toll-like receptor 2 dependent immunogenicity of glycoconjugate vaccines containing chemically derived zwitterionic polysaccharides. Proc Natl Acad Sci U S A 106: 17481–17486. doi: 10.1073/pnas.0903313106 19805031
22. Bielinska AU, Gerber M, Blanco LP, Makidon PE, Janczak KW, et al. (2010) Induction of Th17 cellular immunity with a novel nanoemulsion adjuvant. Crit Rev Immunol 30: 189–199. 20370629
23. Spath GF, Beverley SM, (2001) A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp Parasitol 99: 97–103. 11748963
24. Mendez S, Gurunathan S, Kamhawi S, Belkaid Y, Moga MA, et al. (2001) The potency and durability of DNA- and protein-based vaccines against Leishmania major evaluated using low-dose, intradermal challenge. Journal of immunology 166: 5122–5128. 11290794
25. Harding CV, (2001) Choosing and preparing antigen-presenting cells. Curr Protoc Immunol Chapter 16: Unit 16 11.
26. Becker I, Salaiza N, Aguirre M, Delgado J, Carrillo-Carrasco N, et al. (2003) Leishmania lipophosphoglycan (LPG) activates NK cells through toll-like receptor-2. Mol Biochem Parasitol 130: 65–74. 12946842
27. de Veer MJ, Curtis JM, Baldwin TM, DiDonato JA, Sexton A, et al. (2003) MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur J Immunol 33: 2822–2831. 14515266
28. Kavoosi G, Ardestani SK, Kariminia A, (2009) The involvement of TLR2 in cytokine and reactive oxygen species (ROS) production by PBMCs in response to Leishmania major phosphoglycans (PGs). Parasitology 136: 1193–1199. doi: 10.1017/S0031182009990473 19631014
29. Lopez Kostka S, Dinges S, Griewank K, Iwakura Y, Udey MC, et al. (2009) IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice. Journal of immunology 182: 3039–3046. doi: 10.4049/jimmunol.0713598 19234200
30. Birnbaum R, Craft N, (2011) Innate immunity and Leishmania vaccination strategies. Dermatol Clin 29: 89–102. doi: 10.1016/j.det.2010.08.014 21095533
31. Shah JA, Darrah PA, Ambrozak DR, Turon TN, Mendez S, et al. (2003) Dendritic cells are responsible for the capacity of CpG oligodeoxynucleotides to act as an adjuvant for protective vaccine immunity against Leishmania major in mice. J Exp Med 198: 281–291. 12874261
32. Rhee EG, Mendez S, Shah JA, Wu CY, Kirman JR, et al. (2002) Vaccination with heat-killed leishmania antigen or recombinant leishmanial protein and CpG oligodeoxynucleotides induces long-term memory CD4+ and CD8+ T cell responses and protection against leishmania major infection. J Exp Med 195: 1565–1573. 12070284
33. Belkaid Y, Kamhawi S, Modi G, Valenzuela J, Noben-Trauth N, et al. (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. 9815271
34. Belkaid Y, Mendez S, Lira R, Kadambi N, Milon G, et al. (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. Journal of immunology 165: 969–977.
35. Mendez S, Reckling SK, Piccirillo CA, Sacks D, Belkaid Y, (2004) Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med 200: 201–210. 15263027
36. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL, (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502–507. 12466842
37. Tolouei S, Hejazi SH, Ghaedi K, Khamesipour A, Hasheminia SJ, (2013) TLR2 and TLR4 in cutaneous leishmaniasis caused by Leishmania major. Scandinavian journal of immunology 78: 478–484. doi: 10.1111/sji.12105 23980810
38. Liu T, Matsuguchi T, Tsuboi N, Yajima T, Yoshikai Y, (2002) Differences in expression of toll-like receptors and their reactivities in dendritic cells in BALB/c and C57BL/6 mice. Infect Immun 70: 6638–6645. 12438336
39. Pirmez C, Yamamura M, Uyemura K, Paes-Oliveira M, Conceicao-Silva F, et al. (1993) Cytokine patterns in the pathogenesis of human leishmaniasis. The Journal of clinical investigation 91: 1390–1395. 8473490
40. Pandey SP, Chandel HS, Srivastava S, Selvaraj S, Jha MK, et al. (2014) Pegylated Bisacycloxypropylcysteine, a Diacylated Lipopeptide Ligand of TLR6, Plays a Host-Protective Role against Experimental Leishmania major Infection. Journal of immunology doi: 10.4049/jimmunol.1400672
41. Mahmoudzadeh-Niknam H, Khalili G, Abrishami F, Najafy A, Khaze V, (2013) The route of Leishmania tropica infection determines disease outcome and protection against Leishmania major in BALB/c mice. The Korean journal of parasitology 51: 69–74. doi: 10.3347/kjp.2013.51.1.69 23467583
42. Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N, et al. (2008) In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 321: 970–974. doi: 10.1126/science.1159194 18703742
43. Tacchini-Cottier F, Zweifel C, Belkaid Y, Mukankundiye C, Vasei M, et al. (2000) An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. Journal of immunology 165: 2628–2636.
44. de Souza Carmo EV, Katz S, Barbieri CL, (2010) Neutrophils reduce the parasite burden in Leishmania (Leishmania) amazonensis-infected macrophages. PLoS One 5: e13815. doi: 10.1371/journal.pone.0013815 21082032
45. Sousa LM, Carneiro MB, Resende ME, Martins LS, Dos Santos LM, et al. (2014) Neutrophils have a protective role during early stages of Leishmania amazonensis infection in BALB/c mice. Parasite immunology 36: 13–31. doi: 10.1111/pim.12078 24102495
46. Novais FO, Santiago RC, Bafica A, Khouri R, Afonso L, et al. (2009) Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. Journal of immunology 183: 8088–8098. doi: 10.4049/jimmunol.0803720 19923470
47. Charmoy M, Megnekou R, Allenbach C, Zweifel C, Perez C, et al. (2007) Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. J Leukoc Biol 82: 288–299. 17449725
48. Pitta MG, Romano A, Cabantous S, Henri S, Hammad A, et al. (2009) IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. The Journal of clinical investigation 119: 2379–2387. doi: 10.1172/JCI38813 19620772
49. Taylor PR, Roy S, Leal SM, Jr.Sun Y, Howell SJ, et al. (2014) Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORgammat and dectin-2. Nature immunology 15: 143–151. doi: 10.1038/ni.2797 24362892
50. Jayakumar A, Castilho TM, Park E, Goldsmith-Pestana K, Blackwell JM, et al. (2011) TLR1/2 activation during heterologous prime-boost vaccination (DNA-MVA) enhances CD8+ T Cell responses providing protection against Leishmania (Viannia). PLoS neglected tropical diseases 5: e1204. doi: 10.1371/journal.pntd.0001204 21695103
51. Pakpour N, Zaph C, Scott P, (2008) The central memory CD4+ T cell population generated during Leishmania major infection requires IL-12 to produce IFN-gamma. Journal of immunology 180: 8299–8305. 18523296
52. Stobie L, Gurunathan S, Prussin C, Sacks DL, Glaichenhaus N, et al. (2000) The role of antigen and IL-12 in sustaining Th1 memory cells in vivo: IL-12 is required to maintain memory/effector Th1 cells sufficient to mediate protection to an infectious parasite challenge. Proc Natl Acad Sci U S A 97: 8427–8432. 10890924