Mechanisms of Immune Evasion in Leishmaniasis

Advances in Applied Microbiology

Volumn 82, Issue , 2013, Pages 155-184

  Gupta, Gaurav ^a   Oghumu, Steve ^a,b   Satoskar, Abhay R ^a,b  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Cell signaling; Complement system; Host immunity; Immune evasion; Leishmania; Macrophages; T cells

Indexed keywords

CHEMOKINE; CYTOKINE; TOLL LIKE RECEPTOR;

ADAPTIVE IMMUNITY; AMASTIGOTE; ANTIGEN PRESENTATION; ARTICLE; CELL MIGRATION; CELL SURVIVAL; CLINICAL RESEARCH; COMPLEMENT SYSTEM; CYTOKINE RELEASE; ENZYME ACTIVATION; HUMAN; IMMUNE EVASION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; IMMUNOTHERAPY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LEISHMANIA; LEISHMANIASIS; MACROPHAGE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; PHAGOSOME; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; SIGNAL TRANSDUCTION;

CYTOKINES; HUMANS; IMMUNE EVASION; LEISHMANIA; LEISHMANIASIS; SIGNAL TRANSDUCTION;

EID: 84874447687     PISSN: 00652164     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407679-2.00005-3     Document Type: Chapter

References (191)

1. Abu-Dayyeh I., Hassani K., Westra E.R., Mottram J.C., Olivier M. Comparative study of the ability of Leishmania mexicana promastigotes and amastigotes to alter macrophage signaling and functions. Infection and Immunity 2010, 78:2438-2445.
2. Abu-Dayyeh I., Shio M.T., Sato S., Akira S., Cousineau B., Olivier M. Leishmania-induced IRAK-1 inactivation is mediated by SHP-1 interacting with an evolutionarily conserved KTIM motif. PLoS Neglected Tropical Diseases 2008, 2:e305.
3. Aebischer T., Wolfram M., Patzer S.I., Ilg T., Wiese M., Overath P. Subunit vaccination of mice against new world cutaneous leishmaniasis: comparison of three proteins expressed in amastigotes and six adjuvants. Infection and Immunity 2000, 68:1328-1336.
4. Afonso L., Borges V.M., Cruz H., Ribeiro-Gomes F.L., DosReis G.A., Dutra A.N., et al. Interactions with apoptotic but not with necrotic neutrophils increase parasite burden in human macrophages infected with Leishmania amazonensis. Journal of Leukocyte Biology 2008, 84:389-396.
5. Alexander J., Satoskar A.R., Russell D.G. Leishmania species: models of intracellular parasitism. Journal of Cell Science 1999, 112(Pt 18):2993-3002.
6. Ali H.Z., Harding C.R., Denny P.W. Endocytosis and sphingolipid scavenging in Leishmania mexicana amastigotes. Biochemistry Research International 2012, 2012:691363.
7. Amprey J.L., Im J.S., Turco S.J., Murray H.W., Illarionov P.A., Besra G.S., et al. A subset of liver NK T cells is activated during Leishmania donovani infection by CD1d-bound lipophosphoglycan. Journal of Experimental Medicine 2004, 200:895-904.
8. Ato M., Stäger S., Engwerda C.R., Kaye P.M. Defective CCR7 expression on dendritic cells contributes to the development of visceral leishmaniasis. Nature Immunology 2002, 3:1185-1191.
9. Awasthi A., Mathur R., Khan A., Joshi B.N., Jain N., Sawant S., et al. CD40 signaling is impaired in L. major-infected macrophages and is rescued by a p38MAPK activator establishing a host-protective memory T cell response. Journal of Experimental Medicine 2003, 197:1037-1043.
10. Awasthi A., Mathur R.K., Saha B. Immune response to Leishmania infection. Indian Journal of Medical Research 2004, 119:238-258.
11. Bankoti R., Gupta K., Levchenko A., Stäger S. Marginal zone B cells regulate antigen-specific T cell responses during infection. Journal of Immunology 2012, 188:3961-3971.
12. Belkaid Y. The role of CD4(+)CD25(+) regulatory T cells in Leishmania infection. Expert Opinion on Biological Therapy 2003, 3:875-885.
13. Belkaid Y., Mendez S., Lira R., Kadambi N., Milon G., Sacks D. 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 2000, 165:969-977.
14. Belkaid Y., Piccirillo C.A., Mendez S., Shevach E.M., Sacks D.L. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002, 420:502-507.
15. Belkaid Y., Von Stebut E., Mendez S., Lira R., Caler E., Bertholet S., et al. CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. Journal of Immunology 2002, 168:3992-4000.
16. Bhardwaj N., Rosas L.E., Lafuse W.P., Satoskar A.R. Leishmania inhibits STAT1-mediated IFN-gamma signaling in macrophages: increased tyrosine phosphorylation of dominant negative STAT1beta by Leishmania mexicana. International Journal of Parasitology 2005, 35:75-82.
17. Bhattacharya P., Bhattacharjee S., Gupta G., Majumder S., Adhikari A., Mukherjee A., et al. Arabinosylated lipoarabinomannan-mediated protection in visceral leishmaniasis through up-regulation of toll-like receptor 2 signaling: an immunoprophylactic approach. Journal of Infectious Diseases 2010, 202:145-155.
18. Bhattacharyya S., Ghosh S., Jhonson P.L., Bhattacharya S.K., Majumdar S. Immunomodulatory role of interleukin-10 in visceral leishmaniasis: defective activation of protein kinase C-mediated signal transduction events. Infection and Immunity 2001, 69:1499-1507.
19. Bhattacharyya S., Ghosh S., Sen P., Roy S., Majumdar S. Selective impairment of protein kinase C isotypes in murine macrophage by Leishmania donovani. Molecular and Cellular Biochemistry 2001, 216:47-57.
20. Blackwell J.M., Ezekowitz R.A., Roberts M.B., Channon J.Y., Sim R.B., Gordon S. Macrophage complement and lectin-like receptors bind Leishmania in the absence of serum. Journal of Experimental Medicine 1985, 162:324-331.
21. Blanchette J., Abu-Dayyeh I., Hassani K., Whitcombe L., Olivier M. Regulation of macrophage nitric oxide production by the protein tyrosine phosphatase Src homology 2 domain phosphotyrosine phosphatase 1 (SHP-1). Immunology 2009, 127:123-133.
22. Blanchette J., Racette N., Faure R., Siminovitch K.A., Olivier M. Leishmania-induced increases in activation of macrophage SHP-1 tyrosine phosphatase are associated with impaired IFN-gamma-triggered JAK2 activation. European Journal of Immunology 1999, 29:3737-3744.
23. Bogdan C., Gessner A., Solbach W., Röllinghoff M. Invasion, control and persistence of Leishmania parasites. Current Opinion in Immunology 1996, 8:517-525.
24. Brittingham A., Morrison C.J., McMaster W.R., McGwire B.S., Chang K.P., Mosser D.M. Role of the Leishmania surface protease gp63 in complement fixation, cell adhesion, and resistance to complement-mediated lysis. Journal of Immunology 1995, 155:3102-3111.
25. Brown J.A., Greenwald R.J., Scott S., Schweitzer A.N., Satoskar A.R., Chung C., et al. T helper differentiation in resistant and susceptible B7-deficient mice infected with Leishmania major. European Journal of Immunology 2002, 32:1764-1772.
26. Calegari-Silva T.C., Pereira R.M., De-Melo L.D., Saraiva E.M., Soares D.C., Bellio M., et al. NF-kappaB-mediated repression of iNOS expression in Leishmania amazonensis macrophage infection. Immunology Letters 2009, 127:19-26.
27. Cameron P., McGachy A., Anderson M., Paul A., Coombs G.H., Mottram J.C., et al. Inhibition of lipopolysaccharide-induced macrophage IL-12 production by Leishmania mexicana amastigotes: the role of cysteine peptidases and the NF-kappaB signaling pathway. Journal of Immunology 2004, 173:3297-3304.
28. Campbell K.A., Ovendale P.J., Kennedy M.K., Fanslow W.C., Reed S.G., Maliszewski C.R. CD40 ligand is required for protective cell-mediated immunity to Leishmania major. Immunity 1996, 4:283-289.
29. Camussi G., Bussolino F., Salvidio G., Baglioni C. Tumor necrosis factor/cachectin stimulates peritoneal macrophages, polymorphonuclear neutrophils, and vascular endothelial cells to synthesize and release platelet-activating factor. Journal of Experimental Medicine 1987, 166:1390-1404.
30. Carrada G., Cañeda C., Salaiza N., Delgado J., Ruiz A., Sanchez B., et al. Monocyte cytokine and costimulatory molecule expression in patients infected with Leishmania mexicana. Parasite Immunology 2007, 29:117-126.
31. Carter C.R., Whitcomb J.P., Campbell J.A., Mukbel R.M., McDowell M.A. Complement receptor 3 deficiency influences lesion progression during Leishmania major infection in BALB/c mice. Infection and Immunity 2009, 77:5668-5675.
32. Chakkalath H.R., Theodos C.M., Markowitz J.S., Grusby M.J., Glimcher L.H., Titus R.G. Class II major histocompatibility complex-deficient mice initially control an infection with Leishmania major but succumb to the disease. Journal of Infectious Diseases 1995, 171:1302-1308.
33. Chakraborty D., Banerjee S., Sen A., Banerjee K.K., Das P., Roy S. Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. Journal of Immunology 2005, 175:3214-3224.
34. Chandra D., Naik S. Leishmania donovani infection down-regulates TLR2-stimulated IL-12p40 and activates IL-10 in cells of macrophage/monocytic lineage by modulating MAPK pathways through a contact-dependent mechanism. Clinical and Experimental Immunology 2008, 154:224-234.
35. Charmoy M., Megnekou R., Allenbach C., Zweifel C., Perez C., Monnat K., et al. Leishmania major induces distinct neutrophil phenotypes in mice that are resistant or susceptible to infection. Journal of Leukocyte Biology 2007, 82:288-299.
36. Chawla M., Vishwakarma R.A. Alkylacylglycerolipid domain of GPI molecules of Leishmania is responsible for inhibition of PKC-mediated c-fos expression. Journal of Lipid Research 2003, 44:594-600.
37. Cheekatla S.S., Aggarwal A., Naik S. mTOR signaling pathway regulates the IL-12/IL-10 axis in Leishmania donovani infection. Medical Microbiology and Immunology 2012, 201:37-46.
38. Coler R.N., Reed S.G. Second-generation vaccines against leishmaniasis. Trends in Parasitology 2005, 21:244-249.
39. Contreras I., Gómez M.A., Nguyen O., Shio M.T., McMaster R.W., Olivier M. Leishmania-induced inactivation of the macrophage transcription factor AP-1 is mediated by the parasite metalloprotease GP63. PLoS Pathogens 2010, 6:e1001148.
40. Courret N., Prina E., Mougneau E., Saraiva E.M., Sacks D.L., Glaichenhaus N., et al. Presentation of the Leishmania antigen LACK by infected macrophages is dependent upon the virulence of the phagocytosed parasites. European Journal of Immunology 1999, 29:762-773.
41. Culley F.J., Harris R.A., Kaye P.M., McAdam K.P., Raynes J.G. C-reactive protein binds to a novel ligand on Leishmania donovani and increases uptake into human macrophages. Journal of Immunology 1996, 156:4691-4696.
42. Cummings H.E., Barbi J., Reville P., Oghumu S., Zorko N., Sarkar A., et al. Critical role for phosphoinositide 3-kinase gamma in parasite invasion and disease progression of cutaneous leishmaniasis. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:1251-1256.
43. Da Silva R.P., Hall B.F., Joiner K.A., Sacks D.L. CR1, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. Journal of Immunology 1989, 143:617-622.
44. Das S., Pandey K., Kumar A., Sardar A.H., Purkait B., Kumar M., et al. TGF-β(1) re-programs TLR4 signaling in L. donovani infection: enhancement of SHP-1 and ubiquitin-editing enzyme A20. Immunology and Cell Biology 2012, 90:640-654.
45. De Leo F.R., Ulman K.V., Davis A.R., Jutila K.L., Quinn M.T. Assembly of the human neutrophil NADPH oxidase involves binding of p67phox and flavocytochrome b to a common functional domain in p47phox. Journal of Biological Chemistry 1996, 271:17013-17020.
46. De Souza Leao S., Lang T., Prina E., Hellio R., Antoine J.C. Intracellular Leishmania amazonensis amastigotes internalize and degrade MHC class II molecules of their host cells. Journal of Cell Science 1995, 108(Pt 10):3219-3231.
47. Delgado-Domínguez J., González-Aguilar H., Aguirre-García M., Gutiérrez-Kobeh L., Berzunza-Cruz M., Ruiz-Remigio A., et al. Leishmania mexicana lipophosphoglycan differentially regulates PKCalpha-induced oxidative burst in macrophages of BALB/c and C57BL/6 mice. Parasite Immunology 2010, 32:440-449.
48. Descoteaux A., Turco S.J. Glycoconjugates in Leishmania infectivity. Biochimica et Biophysica Acta 1999, 1455:341-352.
49. Desjeux P. Leishmaniasis: current situation and new perspectives. Comparative Immunology. Microbiology and Infectious Diseases 2004, 27:305-318.
50. Diefenbach A., Schindler H., Donhauser N., Lorenz E., Laskay T., MacMicking J., et al. Type 1 interferon (IFNalpha/beta) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 1998, 8:77-87.
51. Erb K., Blank C., Ritter U., Bluethmann H., Moll H. Leishmania major infection in major histocompatibility complex class II-deficient mice: CD8+ T cells do not mediate a protective immune response. Immunobiology 1996, 195:243-260.
52. Faria M.S., Reis F.C., Azevedo-Pereira R.L., Morrison L.S., Mottram J.C., Lima A.P. Leishmania inhibitor of serine peptidase 2 prevents TLR4 activation by neutrophil elastase promoting parasite survival in murine macrophages. Journal of Immunology 2011, 186:411-422.
53. Faria M.S., Reis F.C., Lima A.P. Toll-like receptors in Leishmania infections: guardians or promoters?. Journal of Parasitology Research 2012, 2012:930257.
54. Filardy A.A., Pires D.R., Nunes M.P., Takiya C.M., Freire-de-Lima C.G., Ribeiro-Gomes F.L., et al. Proinflammatory clearance of apoptotic neutrophils induces an IL-12(low)IL-10(high) regulatory phenotype in macrophages. Journal of Immunology 2010, 185:2044-2050.
55. Flandin J.F., Chano F., Descoteaux A. RNA interference reveals a role for TLR2 and TLR3 in the recognition of Leishmania donovani promastigotes by interferon-gamma-primed macrophages. European Journal of Immunology 2006, 36:411-420.
56. Forget G., Gregory D.J., Olivier M. Proteasome-mediated degradation of STAT1alpha following infection of macrophages with Leishmania donovani. Journal of Biological Chemistry 2005, 280:30542-30549.
57. Forget G., Gregory D.J., Whitcombe L.A., Olivier M. Role of host protein tyrosine phosphatase SHP-1 in Leishmania donovani-induced inhibition of nitric oxide production. Infection and Immunity 2006, 74:6272-6279.
58. de Freitas Balanco J.M., Moreira M.E., Bonomo A., Bozza P.T., Amarante-Mendes G., Pirmez C., et al. Apoptotic mimicry by an obligate intracellular parasite downregulates macrophage microbicidal activity. Current Biology 2001, 11:1870-1873.
59. Fruth U., Solioz N., Louis J.A. Leishmania major interferes with antigen presentation by infected macrophages. Journal of Immunology 1993, 150:1857-1864.
60. Ganguly S., Mukhopadhyay D., Das N.K., Chaduvula M., Sadhu S., Chatterjee U., et al. Enhanced lesional Foxp3 expression and peripheral anergic lymphocytes indicate a role for regulatory T cells in Indian post-kala-azar dermal leishmaniasis. Journal of Investigative Dermatology 2010, 130:1013-1022.
61. Gaur U., Roberts S.C., Dalvi R.P., Corraliza I., Ullman B., Wilson M.E. An effect of parasite-encoded arginase on the outcome of murine cutaneous leishmaniasis. Journal of Immunology 2007, 179:8446-8453.
62. Ghosh S., Bhattacharyya S., Das S., Raha S., Maulik N., Das D.K., et al. Generation of ceramide in murine macrophages infected with Leishmania donovani alters macrophage signaling events and aids intracellular parasitic survival. Molecular and Cellular Biochemistry 2001, 223:47-60.
63. Ghosh S., Bhattacharyya S., Sirkar M., Sa G.S., Das T., Majumdar D., et al. Leishmania donovani suppresses activated protein 1 and NF-kappaB activation in host macrophages via ceramide generation: involvement of extracellular signal-regulated kinase. Infection and Immunity 2002, 70:6828-6838.
64. Gomes-Pereira S., Rodrigues O.R., Rolão N., Almeida P.D., Santos-Gomes G.M. Hepatic cellular immune responses in mice with " cure" and " non-cure" phenotype to Leishmania infantum infection: importance of CD8+ T cells and TGF-beta production. FEMS Immunology and Medical Microbiology 2004, 41:59-68.
65. Gregory D.J., Godbout M., Contreras I., Forget G., Olivier M. A novel form of NF-kappaB is induced by Leishmania infection: involvement in macrophage gene expression. European Journal of Immunology 2008, 38:1071-1081.
66. Guimarães-Costa A.B., Nascimento M.T., Froment G.S., Soares R.P., Morgado F.N., Conceição-Silva F., et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:6748-6753.
67. Guizani-Tabbane L., Ben-Aissa K., Belghith M., Sassi A., Dellagi K. Leishmania major amastigotes induce p50/c-Rel NF-kappa B transcription factor in human macrophages: involvement in cytokine synthesis. Infection and Immunity 2004, 72:2582-2589.
68. Gupta G., Majumdar S., Adhikari A., Bhattacharya P., Mukherjee A.K., Majumdar S.B. Treatment with IP-10 induces host-protective immune response by regulating the T regulatory cell functioning in Leishmania donovani-infected mice. Medical Microbiology and Immunology 2011, 200:241-253.
69. Gupta S., Sane S.A., Shakya N., Vishwakarma P., Haq W. CpG oligodeoxynucleotide 2006 and miltefosine, a potential combination for treatment of experimental visceral leishmaniasis. Antimicrobial Agents and Chemotherapy 2011, 55:3461-3464.
70. Guy R.A., Belosevic M. Comparison of receptors required for entry of Leishmania major amastigotes into macrophages. Infection and Immunity 1993, 61:1553-1558.
71. Hartley M.A., Ronet C., Zangger H., Beverley S.M., Fasel N. Leishmania RNA virus: when the host pays the toll. Frontiers in Cellular and Infection Microbiology 2012, 2:99.
72. Hermoso T., Fishelson Z., Becker S.I., Hirschberg K., Jaffe C.L. Leishmanial protein kinases phosphorylate components of the complement system. EMBO Journal 1991, 10:4061-4067.
73. Holm A., Tejle K., Magnusson K.E., Descoteaux A., Rasmusson B. Leishmania donovani lipophosphoglycan causes periphagosomal actin accumulation: correlation with impaired translocation of PKCalpha and defective phagosome maturation. Cellular Microbiology 2001, 3:439-447.
74. Hoover D.L., Berger M., Nacy C.A., Hockmeyer W.T., Meltzer M.S. Killing of Leishmania tropica amastigotes by factors in normal human serum. Journal of Immunology 1984, 132:893-897.
75. Huber M., Timms E., Mak T.W., Röllinghoff M., Lohoff M. Effective and long-lasting immunity against the parasite Leishmania major in CD8-deficient mice. Infection and Immunity 1998, 66:3968-3970.
76. Huynh C., Andrews N.W. Iron acquisition within host cells and the pathogenicity of Leishmania. Cellular Microbiology 2008, 10:293-300.
77. Iniesta V., Gómez-Nieto L.C., Corraliza I. The inhibition of arginase by N(omega)-hydroxy-l-arginine controls the growth of Leishmania inside macrophages. Journal of Experimental Medicine 2001, 193:777-784.
78. Ishikawa H., Hisaeda H., Taniguchi M., Nakayama T., Sakai T., Maekawa Y., et al. CD4(+) v(alpha)14 NKT cells play a crucial role in an early stage of protective immunity against infection with Leishmania major. International Immunology 2000, 12:1267-1274.
79. Ives A., Ronet C., Prevel F., Ruzzante G., Fuertes-Marraco S., Schutz F., et al. Leishmania RNA virus controls the severity of mucocutaneous leishmaniasis. Science 2011, 331:775-778.
80. Jaramillo M., Gomez M.A., Larsson O., Shio M.T., Topisirovic I., Contreras I., et al. Leishmania repression of host translation through mTOR cleavage is required for parasite survival and infection. Cell Host and Microbe 2011, 9:331-341.
81. Kamanaka M., Yu P., Yasui T., Yoshida K., Kawabe T., Horii T., et al. Protective role of CD40 in Leishmania major infection at two distinct phases of cell-mediated immunity. Immunity 1996, 4:275-281.
82. Kamir D., Zierow S., Leng L., Cho Y., Diaz Y., Griffith J., et al. A Leishmania ortholog of macrophage migration inhibitory factor modulates host macrophage responses. Journal of Immunology 2008, 180:8250-8261.
83. Kane M.M., Mosser D.M. Leishmania parasites and their ploys to disrupt macrophage activation. Current Opinion in Hematology 2000, 7:26-31.
84. Karmakar S., Bhaumik S.K., Paul J., De T. TLR4 and NKT cell synergy in immunotherapy against visceral leishmaniasis. PLoS Pathogens 2012, 8:e1002646.
85. Karmakar S., Paul J., De T. Leishmania donovani glycosphingolipid facilitates antigen presentation by inducing relocation of CD1d into lipid rafts in infected macrophages. European Journal of Immunology 2011, 41:1376-1387.
86. Katara G.K., Ansari N.A., Verma S., Ramesh V., Salotra P. Foxp3 and IL-10 expression correlates with parasite burden in lesional tissues of post kala azar dermal leishmaniasis (PKDL) patients. PLoS Neglected Tropical Diseases 2011, 5:e1171.
87. Katzman S.D., Fowell D.J. Pathogen-imposed skewing of mouse chemokine and cytokine expression at the infected tissue site. Journal of Clinical Investigation 2008, 118:801-811.
88. Kautz-Neu K., Noordegraaf M., Dinges S., Bennett C.L., John D., Clausen B.E., et al. Langerhans cells are negative regulators of the anti-Leishmania response. Journal of Experimental Medicine 2011, 208:885-891.
89. Kavoosi G., Ardestani S.K., Kariminia A. The involvement of TLR2 in cytokine and reactive oxygen species (ROS) production by PBMCs in response to Leishmania major phosphoglycans (PGs). Parasitology 2009, 136:1193-1199.
90. Kavoosi G., Ardestani S.K., Kariminia A., Alimohammadian M.H. Leishmania major lipophosphoglycan: discrepancy in toll-like receptor signaling. Experimental Parasitology 2010, 124:214-218.
91. Kaye P., Scott P. Leishmaniasis: complexity at the host-pathogen interface. Nature Reviews Microbiology 2011, 9:604-615.
92. Khouri R., Bafica A., Silva M.a.P., Noronha A., Kolb J.P., Wietzerbin J., et al. IFN-beta impairs superoxide-dependent parasite killing in human macrophages: evidence for a deleterious role of SOD1 in cutaneous leishmaniasis. Journal of Immunology 2009, 182:2525-2531.
93. Kima P.E., Soong L., Chicharro C., Ruddle N.H., McMahon-Pratt D. Leishmania-infected macrophages sequester endogenously synthesized parasite antigens from presentation to CD4+ T cells. European Journal of Immunology 1996, 26:3163-3169.
94. Kirkpatrick C.E., Farrell J.P. Leishmaniasis in beige mice. Infection and Immunity 1982, 38:1208-1216.
95. Kopf M., Brombacher F., Kohler G., Kienzle G., Widmann K.H., Lefrang K., et al. IL-4-deficient Balb/c mice resist infection with Leishmania major. Journal of Experimental Medicine 1996, 184:1127-1136.
96. Kropf P., Freudenberg N., Kalis C., Modolell M., Herath S., Galanos C., et al. Infection of C57BL/10ScCr and C57BL/10ScNCr mice with Leishmania major reveals a role for toll-like receptor 4 in the control of parasite replication. Journal of Leukocyte Biology 2004, 76:48-57.
97. Kropf P., Freudenberg M.A., Modolell M., Price H.P., Herath S., Antoniazi S., et al. Toll-like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infection and Immunity 2004, 72:1920-1928.
98. Kropf P., Herath S., Weber V., Modolell M., Müller I. Factors influencing Leishmania major infection in IL-4-deficient BALB/c mice. Parasite Immunology 2003, 25:439-447.
99. Kushawaha P.K., Gupta R., Sundar S., Sahasrabuddhe A.A., Dube A. Elongation factor-2, a Th1 stimulatory protein of Leishmania donovani, generates strong IFN-γ and IL-12 response in cured Leishmania-infected patients/hamsters and protects hamsters against Leishmania challenge. Journal of Immunology 2011, 187:6417-6427.
100. Lang T., de Chastellier C., Frehel C., Hellio R., Metezeau P., Leao S.e.S., et al. Distribution of MHC class I and of MHC class II molecules in macrophages infected with Leishmania amazonensis. Journal of Cell Science 1994, 107(Pt 1):69-82.
101. Laskay T., Diefenbach A., Röllinghoff M., Solbach W. Early parasite containment is decisive for resistance to Leishmania major infection. European Journal of Immunology 1995, 25:2220-2227.
102. Lieke T., Nylén S., Eidsmo L., Schmetz C., Berg L., Akuffo H. The interplay between Leishmania promastigotes and human natural killer cells in vitro leads to direct lysis of Leishmania by NK cells and modulation of NK cell activity by Leishmania promastigotes. Parasitology 2011, 138:1898-1909.
103. Liu D., Zhang T., Marshall A.J., Okkenhaug K., Vanhaesebroeck B., Uzonna J.E. The p110delta isoform of phosphatidylinositol 3-kinase controls susceptibility to Leishmania major by regulating expansion and tissue homing of regulatory T cells. Journal of Immunology 2009, 183:1921-1933.
104. Llanos-Cuentas A., Calderon W., Cruz M., Ashman J.A., Alves F.P., Coler R.N., et al. A clinical trial to evaluate the safety and immunogenicity of the LEISH-F1+MPL-SE vaccine when used in combination with sodium stibogluconate for the treatment of mucosal leishmaniasis. Vaccine 2010, 28:7427-7435.
105. Lo S.K., Bovis L., Matura R., Zhu B., He S., Lum H., et al. Leishmania lipophosphoglycan reduces monocyte transendothelial migration: modulation of cell adhesion molecules, intercellular junctional proteins, and chemoattractants. Journal of Immunology 1998, 160:1857-1865.
106. Locksley R.M., Reiner S.L., Hatam F., Littman D.R., Killeen N. Helper T cells without CD4: control of leishmaniasis in CD4-deficient mice. Science 1993, 261:1448-1451.
107. Mannheimer S.B., Hariprashad J., Stoeckle M.Y., Murray H.W. Induction of macrophage antiprotozoal activity by monocyte chemotactic and activating factor. FEMS Immunology and Medical Microbiology 1996, 14:59-61.
108. Marth T., Kelsall B.L. Regulation of interleukin-12 by complement receptor 3 signaling. Journal of Experimental Medicine 1997, 185:1987-1995.
109. Martiny A., Meyer-Fernandes J.R., de Souza W., Vannier-Santos M.A. Altered tyrosine phosphorylation of ERK1 MAP kinase and other macrophage molecules caused by Leishmania amastigotes. Molecular and Biochemical Parasitology 1999, 102:1-12.
110. Mary C., Auriault V., Faugère B., Dessein A.J. Control of Leishmania infantum infection is associated with CD8(+) and gamma interferon- and interleukin-5-producing CD4(+) antigen-specific T cells. Infection and Immunity 1999, 67:5559-5566.
111. Mathur R.K., Awasthi A., Wadhone P., Ramanamurthy B., Saha B. Reciprocal CD40 signals through p38MAPK and ERK-1/2 induce counteracting immune responses. Nature Medicine 2004, 10:540-544.
112. Mattner J., Donhauser N., Werner-Felmayer G., Bogdan C. NKT cells mediate organ-specific resistance against Leishmania major infection. Microbes and Infection 2006, 8:354-362.
113. Mattner F., Magram J., Ferrante J., Launois P., Di Padova K., Behin R., et al. Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. European Journal of Immunology 1996, 26:1553-1559.
114. Mbow M.L., DeKrey G.K., Titus R.G. Leishmania major induces differential expression of costimulatory molecules on mouse epidermal cells. European Journal of Immunology 2001, 31:1400-1409.
115. McDowell M.A., Sacks D.L. Inhibition of host cell signal transduction by Leishmania: observations relevant to the selective impairment of IL-12 responses. Current Opinion in Microbiology 1999, 2:438-443.
116. Meddeb-Garnaoui A., Zrelli H., Dellagi K. Effects of tropism and virulence of Leishmania parasites on cytokine production by infected human monocytes. Clinical and Experimental Immunology 2009, 155:199-206.
117. Mendez S., Reckling S.K., Piccirillo C.A., Sacks D., Belkaid Y. Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. Journal of Experimental Medicine 2004, 200:201-210.
118. Mise-Omata S., Kuroda E., Sugiura T., Yamashita U., Obata Y., Doi T.S. The NF-kappaB RelA subunit confers resistance to Leishmania major by inducing nitric oxide synthase 2 and Fas expression but not Th1 differentiation. Journal of Immunology 2009, 182:4910-4916.
119. Mollinedo F., Janssen H., de la Iglesia-Vicente J., Villa-Pulgarin J.A., Calafat J. Selective fusion of azurophilic granules with Leishmania-containing phagosomes in human neutrophils. Journal of Biological Chemistry 2010, 285:34528-34536.
120. Moreno I., Molina R., Toraño A., Laurin E., García E., Domínguez M. Comparative real-time kinetic analysis of human complement killing of Leishmania infantum promastigotes derived from axenic culture or from Phlebotomus perniciosus. Microbes and Infection 2007, 9:1574-1580.
121. Mosser D.M., Edelson P.J. The mouse macrophage receptor for C3bi (CR3) is a major mechanism in the phagocytosis of Leishmania promastigotes. Journal of Immunology 1985, 135:2785-2789.
122. Müller K., van Zandbergen G., Hansen B., Laufs H., Jahnke N., Solbach W., et al. Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice. Medical Microbiology and Immunology 2001, 190:73-76.
123. Murphy M.L., Cotterell S.E., Gorak P.M., Engwerda C.R., Kaye P.M. Blockade of CTLA-4 enhances host resistance to the intracellular pathogen, Leishmania donovani. Journal of Immunology 1998, 161:4153-4160.
124. Murphy M.L., Engwerda C.R., Gorak P.M., Kaye P.M. B7-2 blockade enhances T cell responses to Leishmania donovani. Journal of Immunology 1997, 159:4460-4466.
125. Murray H.W., Nathan C.F. Macrophage microbicidal mechanisms in vivo: reactive nitrogen versus oxygen intermediates in the killing of intracellular visceral Leishmania donovani. Journal of Experimental Medicine 1999, 189:741-746.
126. Nandan D., Lo R., Reiner N.E. Activation of phosphotyrosine phosphatase activity attenuates mitogen-activated protein kinase signaling and inhibits c-FOS and nitric oxide synthase expression in macrophages infected with Leishmania donovani. Infection and Immunity 1999, 67:4055-4063.
127. Nandan D., Reiner N.E. Attenuation of gamma interferon-induced tyrosine phosphorylation in mononuclear phagocytes infected with Leishmania donovani: selective inhibition of signaling through Janus kinases and Stat1. Infection and Immunity 1995, 63:4495-4500.
128. Nateghi Rostami M., Keshavarz H., Edalat R., Sarrafnejad A., Shahrestani T., Mahboudi F., et al. CD8+ T cells as a source of IFN-γ production in human cutaneous leishmaniasis. PLoS Neglected Tropical Diseases 2010, 4:e845.
129. Novais F.O., Santiago R.C., Báfica A., Khouri R., Afonso L., Borges V.M., et al. Neutrophils and macrophages cooperate in host resistance against Leishmania braziliensis infection. Journal of Immunology 2009, 183:8088-8098.
130. Oghumu S., Lezama-Dávila C.M., Isaac-Márquez A.P., Satoskar A.R. Role of chemokines in regulation of immunity against leishmaniasis. Experimental Parasitology 2010, 126:389-396.
131. Olivier M., Atayde V.D., Isnard A., Hassani K., Shio M.T. Leishmania virulence factors: focus on the metalloprotease GP63. Microbes and Infection 2012, 14:1377-1389.
132. Olivier M., Brownsey R.W., Reiner N.E. Defective stimulus-response coupling in human monocytes infected with Leishmania donovani is associated with altered activation and translocation of protein kinase C. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:7481-7485.
133. Olivier M., Gregory D.J., Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clinical Microbiology Reviews 2005, 18:293-305.
134. Pearson R.D., Steigbigel R.T. Phagocytosis and killing of the protozoan Leishmania donovani by human polymorphonuclear leukocytes. Journal of Immunology 1981, 127:1438-1443.
135. Pereira L.I., Dorta M.L., Pereira A.J., Bastos R.P., Oliveira M.A., Pinto S.A., et al. Increase of NK cells and proinflammatory monocytes are associated with the clinical improvement of diffuse cutaneous leishmaniasis after immunochemotherapy with BCG/Leishmania antigens. American Journal of Tropical Medicine and Hygiene 2009, 81:378-383.
136. Pereira W.F., Ribeiro-Gomes F.L., Guillermo L.V., Vellozo N.S., Montalvão F., Dosreis G.A., et al. Myeloid-derived suppressor cells help protective immunity to Leishmania major infection despite suppressed T cell responses. Journal of Leukocyte Biology 2011, 90:1191-1197.
137. Peruhype-Magalhães V., Martins-Filho O.A., Prata A., Silva L.e.A., Rabello A., Teixeira-Carvalho A., et al. Immune response in human visceral leishmaniasis: analysis of the correlation between innate immunity cytokine profile and disease outcome. Scandinavian Journal of Immunology 2005, 62:487-495.
138. Peters N., Sacks D. Immune privilege in sites of chronic infection: leishmania and regulatory T cells. Immunological Reviews 2006, 213:159-179.
139. Pinheiro N.F., Hermida M.D., Macedo M.P., Mengel J., Bafica A., dos-Santos W.L. Leishmania infection impairs beta 1-integrin function and chemokine receptor expression in mononuclear phagocytes. Infection and Immunity 2006, 74:3912-3921.
140. Pompeu M.L., Freitas L.A., Santos M.L., Khouri M., Barral-Netto M. Granulocytes in the inflammatory process of BALB/c mice infected by Leishmania amazonensis. A quantitative approach. Acta Tropica 1991, 48:185-193.
141. Prajeeth C.K., Haeberlein S., Sebald H., Schleicher U., Bogdan C. Leishmania-infected macrophages are targets of NK cell-derived cytokines but not of NK cell cytotoxicity. Infection and Immunity 2011, 79:2699-2708.
142. Prina E., Lang T., Glaichenhaus N., Antoine J.C. Presentation of the protective parasite antigen LACK by Leishmania-infected macrophages. Journal of Immunology 1996, 156:4318-4327.
143. Privé C., Descoteaux A. Leishmania donovani promastigotes evade the activation of mitogen-activated protein kinases p38, c-Jun N-terminal kinase, and extracellular signal-regulated kinase-1/2 during infection of naive macrophages. European Journal of Immunology 2000, 30:2235-2244.
144. Puentes S.M., Da Silva R.P., Sacks D.L., Hammer C.H., Joiner K.A. Serum
145. Puentes S.M., Sacks D.L., da Silva R.P., Joiner K.A. Complement binding by two developmental stages of Leishmania major promastigotes varying in expression of a surface lipophosphoglycan. Journal of Experimental Medicine 1988, 167:887-902.
146. Rai A.K., Thakur C.P., Seth T., Mitra D.K. Enrichment of invariant natural killer T cells in the bone marrow of visceral leishmaniasis patients. Parasite Immunology 2011, 33:688-691.
147. Rai A.K., Thakur C.P., Singh A., Seth T., Srivastava S.K., Singh P., et al. Regulatory T cells suppress T cell activation at the pathologic site of human visceral leishmaniasis. PLoS One 2012, 7:e31551.
148. Raman V.S., Bhatia A., Picone A., Whittle J., Bailor H.R., O'Donnell J., et al. Applying TLR synergy in immunotherapy: implications in cutaneous leishmaniasis. Journal of Immunology 2010, 185:1701-1710.
149. Reguera R.M., Balaña-Fouce R., Showalter M., Hickerson S., Beverley S.M. Leishmania major lacking arginase (ARG) are auxotrophic for polyamines but retain infectivity to susceptible BALB/c mice. Molecular and Biochemical Parasitology 2009, 165:48-56.
150. Reiner S.L., Zheng S., Wang Z.E., Stowring L., Locksley R.M. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection. Journal of Experimental Medicine 1994, 179:447-456.
151. Rezai H.R., Sher S., Gettner S. Leishmania tropica, L. donovani, and L. enriettii: immune rabbit serum inhibitory in vitro. Experimental Parasitology 1969, 26:257-263.
152. Ribeiro-Gomes F.L., Moniz-de-Souza M.C., Alexandre-Moreira M.S., Dias W.B., Lopes M.F., Nunes M.P., et al. Neutrophils activate macrophages for intracellular killing of Leishmania major through recruitment of TLR4 by neutrophil elastase. Journal of Immunology 2007, 179:3988-3994.
153. Ribeiro-Gomes F.L., Otero A.C., Gomes N.A., Moniz-De-Souza M.C., Cysne-Finkelstein L., Arnholdt A.C., et al. Macrophage interactions with neutrophils regulate Leishmania major infection. Journal of Immunology 2004, 172:4454-4462.
154. Ritter U., Moll H., Laskay T., Bröcker E., Velazco O., Becker I., et al. Differential expression of chemokines in patients with localized and diffuse cutaneous American leishmaniasis. Journal of Infectious Diseases 1996, 173:699-709.
155. Sacks D.L., Pimenta P.F., McConville M.J., Schneider P., Turco S.J. Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. Journal of Experimental Medicine 1995, 181:685-697.
156. Saha B., Das G., Vohra H., Ganguly N.K., Mishra G.C. Macrophage-T cell interaction in experimental visceral leishmaniasis: failure to express costimulatory molecules on Leishmania-infected macrophages and its implication in the suppression of cell-mediated immunity. European Journal of Immunology 1995, 25:2492-2498.
157. Satoskar A.R., Stamm L.M., Zhang X., Okano M., David J.R., Terhorst C., et al. NK cell-deficient mice develop a Th1-like response but fail to mount an efficient antigen-specific IgG2a antibody response. Journal of Immunology 1999, 163:5298-5302.
158. Scharton T.M., Scott P. Natural killer cells are a source of interferon gamma that drives differentiation of CD4+ T cell subsets and induces early resistance to Leishmania major in mice. Journal of Experimental Medicine 1993, 178:567-577.
159. Scianimanico S., Desrosiers M., Dermine J.F., Méresse S., Descoteaux A., Desjardins M. Impaired recruitment of the small GTPase rab7 correlates with the inhibition of phagosome maturation by Leishmania donovani promastigotes. Cellular Microbiology 1999, 1:19-32.
160. Sen S., Roy K., Mukherjee S., Mukhopadhyay R., Roy S. Restoration of IFNγR subunit assembly, IFNγ signaling and parasite clearance in Leishmania donovani infected macrophages: role of membrane cholesterol. PLoS Pathogens 2011, 7:e1002229.
161. Shakya N., Sane S.A., Shankar S., Gupta S. Effect of Pam3Cys induced protection on the therapeutic efficacy of miltefosine against experimental visceral leishmaniasis. Peptides 2011, 32:2131-2133.
162. Shweash M., Adrienne McGachy H., Schroeder J., Neamatallah T., Bryant C.E., Millington O., et al. Leishmania mexicana promastigotes inhibit macrophage IL-12 production via TLR-4 dependent COX-2, iNOS and arginase-1 expression. Molecular Immunology 2011, 48:1800-1808.
163. Silva V.M., Larangeira D.F., Oliveira P.R., Sampaio R.B., Suzart P., Nihei J.S., et al. Enhancement of experimental cutaneous leishmaniasis by Leishmania molecules is dependent on interleukin-4, serine protease/esterase activity, and parasite and host genetic backgrounds. Infection and Immunity 2011, 79:1236-1243.
164. Smelt S.C., Cotterell S.E., Engwerda C.R., Kaye P.M. B cell-deficient mice are highly resistant to Leishmania donovani infection, but develop neutrophil-mediated tissue pathology. Journal of Immunology 2000, 164:3681-3688.
165. de Souza Carmo E.V., Katz S., Barbiéri C.L. Neutrophils reduce the parasite burden in Leishmania (Leishmania) amazonensis-infected macrophages. PLoS One 2010, 5:e13815.
166. Srivastava A., Singh N., Mishra M., Kumar V., Gour J.K., Bajpai S., et al. Identification of TLR inducing Th1-responsive Leishmania donovani amastigote-specific antigens. Molecular and Cellular Biochemistry 2012, 359:359-368.
167. Srivastava N., Sudan R., Saha B. CD40-modulated dual-specificity phosphatases MAPK phosphatase (MKP)-1 and MKP-3 reciprocally regulate Leishmania major infection. Journal of Immunology 2011, 186:5863-5872.
168. Srivastav S., Kar S., Chande A.G., Mukhopadhyaya R., Das P.K. Leishmania donovani exploits host deubiquitinating enzyme A20, a negative regulator of TLR signaling, to subvert host immune response. Journal of Immunology 2012, 189:924-934.
169. Stanley A.C., Zhou Y., Amante F.H., Randall L.M., Haque A., Pellicci D.G., et al. Activation of invariant NKT cells exacerbates experimental visceral leishmaniasis. PLoS Pathogens 2008, 4:e1000028.
170. Suffia I., Reckling S.K., Salay G., Belkaid Y. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. Journal of Immunology 2005, 174:5444-5455.
171. Suzuki E., Tanaka A.K., Toledo M.S., Takahashi H.K., Straus A.H. Role of beta-d-galactofuranose in Leishmania major macrophage invasion. Infection and Immunity 2002, 70:6592-6596.
172. Swihart K., Fruth U., Messmer N., Hug K., Behin R., Huang S., et al. Mice from a genetically resistant background lacking the interferon gamma receptor are susceptible to infection with Leishmania major but mount a polarized T helper cell 1-type CD4+ T cell response. Journal of Experimental Medicine 1995, 181:961-971.
173. Tabatabaee P.A., Abolhassani M., Mahdavi M., Nahrevanian H., Azadmanesh K. Leishmania major: secreted antigens of Leishmania major promastigotes shift the immune response of the C57BL/6 mice toward Th2 in vitro. Experimental Parasitology 2011, 127:46-51.
174. Tacchini-Cottier F., Zweifel C., Belkaid Y., Mukankundiye C., Vasei M., Launois P., et al. An immunomodulatory function for neutrophils during the induction of a CD4+ Th2 response in BALB/c mice infected with Leishmania major. Journal of Immunology 2000, 165:2628-2636.
175. Talamás-Rohana P., Wright S.D., Lennartz M.R., Russell D.G. Lipophosphoglycan from Leishmania mexicana promastigotes binds to members of the CR3, p150,95 and LFA-1 family of leukocyte integrins. Journal of Immunology 1990, 144:4817-4824.
176. Thalhofer C.J., Chen Y., Sudan B., Love-Homan L., Wilson M.E. Leukocytes infiltrate the skin and draining lymph nodes in response to the protozoan Leishmania infantum chagasi. Infection and Immunity 2011, 79:108-117.
177. Tsagozis P., Karagouni E., Dotsika E. Function of CD8+ T lymphocytes in a self-curing mouse model of visceral leishmaniasis. Parasitology International 2005, 54:139-146.
178. Turco S.J., Hull S.R., Orlandi P.A., Shepherd S.D., Homans S.W., Dwek R.A., et al. Structure of the major carbohydrate fragment of the Leishmania donovani lipophosphoglycan. Biochemistry 1987, 26:6233-6238.
179. Vargas-Inchaustegui D.A., Tai W., Xin L., Hogg A.E., Corry D.B., Soong L. Distinct roles for MyD88 and toll-like receptor 2 during Leishmania braziliensis infection in mice. Infection and Immunity 2009, 77:2948-2956.
180. de Veer M.J., Curtis J.M., Baldwin T.M., DiDonato J.A., Sexton A., McConville M.J., et al. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and toll-like receptor 2 signaling. European Journal of Immunology 2003, 33:2822-2831.
181. Vinet A.F., Fukuda M., Turco S.J., Descoteaux A. The Leishmania donovani lipophosphoglycan excludes the vesicular proton-ATPase from phagosomes by impairing the recruitment of synaptotagmin V. PLoS Pathogens 2009, 5:e1000628.
182. Vivarini A.e.C., Pereira R.e.M., Teixeira K.L., Calegari-Silva T.C., Bellio M., Laurenti M.D., et al. Human cutaneous leishmaniasis: interferon-dependent expression of double-stranded RNA-dependent protein kinase (PKR) via TLR2. FASEB Journal 2011, 25:4162-4173.
183. Weingartner A., Kemmer G., Muller F.D., Zampieri R.A., Gonzaga Dos Santos M., Schiller J., et al. Leishmania promastigotes lack phosphatidylserine but bind annexin V upon permeabilization or miltefosine treatment. PLoS One 2012, 7:e42070.
184. Weinheber N., Wolfram M., Harbecke D., Aebischer T. Phagocytosis of Leishmania mexicana amastigotes by macrophages leads to a sustained suppression of IL-12 production. European Journal of Immunology 1998, 28:2467-2477.
185. Whitaker S.M., Colmenares M., Pestana K.G., McMahon-Pratt D. Leishmania pifanoi proteoglycolipid complex P8 induces macrophage cytokine production through toll-like receptor 4. Infection and Immunity 2008, 76:2149-2156.
186. Wiethe C., Debus A., Mohrs M., Steinkasserer A., Lutz M., Gessner A. Dendritic cell differentiation state and their interaction with NKT cells determine Th1/Th2 differentiation in the murine model of Leishmania major infection. Journal of Immunology 2008, 180:4371-4381.
187. Wilson J., Huynh C., Kennedy K.A., Ward D.M., Kaplan J., Aderem A., et al. Control of parasitophorous vacuole expansion by LYST/Beige restricts the intracellular growth of Leishmania amazonensis. PLoS Pathogens 2008, 4:e1000179.
188. Wright S.D., Silverstein S.C. Receptors for C3b and C3bi promote phagocytosis but not the release of toxic oxygen from human phagocytes. Journal of Experimental Medicine 1983, 158:2016-2023.
189. Yang Z., Mosser D.M., Zhang X. Activation of the MAPK, ERK, following Leishmania amazonensis infection of macrophages. Journal of Immunology 2007, 178:1077-1085.
190. Yurchenko E., Tritt M., Hay V., Shevach E.M., Belkaid Y., Piccirillo C.A. CCR5-dependent homing of naturally occurring CD4+ regulatory T cells to sites of Leishmania major infection favors pathogen persistence. Journal of Experimental Medicine 2006, 203:2451-2460.
191. van Zandbergen G., Hermann N., Laufs H., Solbach W., Laskay T. Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin-8 release but inhibit gamma interferon-inducible protein 10 production by neutrophil granulocytes. Infection and Immunity 2002, 70:4177-4184.