Class II MHC/peptide interaction in Leishmania donovani infection: Implications in vaccine design

Journal of Immunology

Volumn 192, Issue 12, 2014, Pages 5873-5880

  Roy, Koushik ^a   Naskar, Kshudiram ^a   Ghosh, Moumita ^a   Roy, Syamal ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

2 (1 ADAMANTYL)ETHANOL; ALCOHOL DERIVATIVE; LACK PEPTIDE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CELL EXPANSION; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; IN VITRO STUDY; LEISHMANIASIS; MACROPHAGE; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SPLEEN CELL; T LYMPHOCYTE ACTIVATION;

ANIMALS; ANTIGENS, PROTOZOAN; HISTOCOMPATIBILITY ANTIGENS CLASS II; LEISHMANIA DONOVANI; LEISHMANIASIS VACCINES; LEISHMANIASIS, VISCERAL; LYMPHOCYTE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; PEPTIDES; PROTOZOAN PROTEINS; T-LYMPHOCYTES;

EID: 84902174395     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302970     Document Type: Article

References (57)

1. Basak, S. K., B. Saha, A. Bhattacharya, and S. Roy. 1992. Immunobiological studies on experimental visceral leishmaniasis. II. Adherent cell-mediated downregulation of delayed-type hypersensitivity response and up-regulation of B cell activation. Eur. J. Immunol. 22:2041-2045.
2. Decuypere, S., M. Vanaerschot, K. Brunker, H. Imamura, S. Muller, B. Khanal, S. Rijal, J. C. Dujardin, and G. H. Coombs. 2012. Molecular mechanisms of drug resistance in natural Leishmania populations vary with genetic background. PLoS Negl. Trop. Dis. 6:e1514.
3. Nylén, S., and S. Gautam. 2010. Immunological perspectives of leishmaniasis. J. Glob. Infect. Dis. 2:135-146.
4. Kaye, P. M., M. Svensson, M. Ato, A. Maroof, R. Polley, S. Stager, S. Zubairi, and C. R. Engwerda. 2004. The immunopathology of experimental visceral leishmaniasis. Immunol. Rev. 201:239-253.
5. Muraille, E., P. Gounon, J. Cazareth, J. Hoebeke, C. Lippuner, A. Davalos-Misslitz, T. Aebischer, S. Muller, N. Glaichenhaus, and E. Mougneau. 2010. Direct visualization of peptide/MHC complexes at the surface and in the intracellular compartments of cells infected in vivo by Leishmania major. PLoS Pathog. 6:e1001154.
6. Belkaid, Y., E. Von Stebut, S. Mendez, R. Lira, E. Caler, S. Bertholet, M. C. Udey, and D. Sacks. 2002. CD8+ T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J. Immunol. 168:3992-4000.
7. Uzonna, J. E., K. L. Joyce, and P. Scott. 2004. Low dose Leishmania major promotes a transient T helper cell type 2 response that is down-regulated by interferon gamma-producing CD8+ T cells. J. Exp. Med. 199:1559-1566.
8. Murray, H. W. 2005. Prevention of relapse after chemotherapy in a chronic intracellular infection: mechanisms in experimental visceral leishmaniasis. J. Immunol. 174:4916-4923.
9. Bold, T. D., and J. D. Ernst. 2012. CD4+ T cell-dependent IFN-γ production by CD8+ effector T cells in Mycobacterium tuberculosis infection. J. Immunol. 189:2530-2536.
10. Singh, O. P., C. B. Stober, A. K. Singh, J. M. Blackwell, and S. Sundar. 2012. Cytokine responses to novel antigens in an Indian population living in an area endemic for visceral leishmaniasis. PLoS. Negl. Trop. Dis. 6:e1874.
11. Naundorf, S., M. Schröder, C. Höflich, N. Suman, H. D. Volk, and G. Grütz. 2009. IL-10 interferes directly with TCR-induced IFN-gamma but not IL-17 production in memory T cells. Eur. J. Immunol. 39:1066-1077.
12. Oswald, I. P., T. A. Wynn, A. Sher, and S. L. James. 1992. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor alpha required as a costimulatory factor for interferon gamma-induced activation. Proc. Natl. Acad. Sci. USA 89:8676-8680.
13. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
14. Sen, S., K. Roy, S. Mukherjee, R. Mukhopadhyay, and S. Roy. 2011. Restoration of IFNγR subunit assembly, IFNγ signaling and parasite clearance in Leishmania donovani infected macrophages: role of membrane cholesterol. PLoS Pathog. 7:e1002229.
15. Rohtagi, A., S. K. Agarwal, M. Bose, D. Chattopadhya, and K. Saha. 1996. Blood, bone marrow and splenic lymphocyte subset profiles in Indian visceral leishmaniasis. Trans. R. Soc. Trop. Med. Hyg. 90:431-434.
16. Beattie, L., A. Peltan, A. Maroof, A. Kirby, N. Brown, M. Coles, D. F. Smith, and P. M. Kaye. 2010. Dynamic imaging of experimental Leishmania donovaniinduced hepatic granulomas detects Kupffer cell-restricted antigen presentation to antigen-specific CD8 T cells. PLoS Pathog. 6:e1000805.
17. Huber, M., E. Timms, T. W. Mak, M. Röllinghoff, and M. Lohoff. 1998. Effective and long-lasting immunity against the parasite Leishmania major in CD8-deficient mice. Infect. Immun. 66:3968-3970.
18. Locksley, R. M., S. L. Reiner, F. Hatam, D. R. Littman, and N. Killeen. 1993. Helper T cells without CD4: control of leishmaniasis in CD4-deficient mice. Science 261:1448-1451.
19. Hofstetter, A. R., M. L. Ford, L. C. Sullivan, J. J. Wilson, A. Hadley, A. G. Brooks, and A. E. Lukacher. 2012. MHC class Ib-restricted CD8 T cells differ in dependence on CD4 T cell help and CD28 costimulation over the course of mouse polyomavirus infection. J. Immunol. 188:3071-3079.
20. Janssen, E. M., E. E. Lemmens, T. Wolfe, U. Christen, M. G. Von Herrath, and S. P. Schoenberger. 2003. CD4+ T cells are required for secondary expansion and memory in CD8+ T lymphocytes. Nature 421:852-856.
21. Khanolkar, A., M. J. Fuller, and A. J. Zajac. 2004. CD4 T cell-dependent CD8 T cell maturation. J. Immunol. 172:2834-2844.
22. Salkowitz, J. R., S. F. Sieg, C. V. Harding, and M. M. Lederman. 2004. In vitro human memory CD8 T cell expansion in response to cytomegalovirus requires CD4+ T cell help. J. Infect. Dis. 189:971-983.
23. Shi, M., and J. Xiang. 2006. CD4+ T cell-independent maintenance and expansion of memory CD8+ T cells derived from in vitro dendritic cell activation. Int. Immunol. 18:887-895.
24. Prina, E., C. Jouanne, S. De Souza Lão, A. Szabo, J. G. Guillet, and J. C. Antoine. 1993. Antigen presentation capacity of murine macrophages infected with Leishmania amazonensis amastigotes. J. Immunol. 151:2050-2061.
25. Sijts, A. J., and E. G. Pamer. 1997. Enhanced intracellular dissociation of major histocompatibility complex class I-associated peptides: a mechanism for optimizing the spectrum of cell surface-presented cytotoxic T lymphocyte epitopes. J. Exp. Med. 185:1403-1411.
26. Lazaro, E., C. Kadie, P. Stamegna, S. C. Zhang, P. Gourdain, N. Y. Lai, M. Zhang, S. A. Martinez, D. Heckerman, and S. Le Gall. 2011. Variable HIV peptide stability in human cytosol is critical to epitope presentation and immune escape. J. Clin. Invest. 121:2480-2492.
27. Gerlier, D., M. C. Trescol-Biémont, L. Ettouati, J. Paris, and C. Rabourdin-Combe. 1998. An accessory peptide binding site with allosteric effect on the formation of peptide-MHC-II complexes? C. R. Acad. Sci. III 321:19-24.
28. Baumgartner, C. K., A. Ferrante, M. Nagaoka, J. Gorski, and L. P. Malherbe. 2010. Peptide-MHC class II complex stability governs CD4 T cell clonal selection. J. Immunol. 184:573-581.
29. Constant, S. L., and K. Bottomly. 1997. Induction of Th1 and Th2 CD4+ T cell responses: the alternative approaches. Annu. Rev. Immunol. 15:297-322.
30. Lazarski, C. A., F. A. Chaves, S. A. Jenks, S. Wu, K. A. Richards, J. M. Weaver, and A. J. Sant. 2005. The kinetic stability of MHC class II: peptide complexes is a key parameter that dictates immunodominance. Immunity 23:29-40.
31. Ghosh, M., A. K. Solanki, K. Roy, R. R. Dhoke, Ashish, and S. Roy. 2013. Carrier protein influences immunodominance of a known epitope: implication in peptide vaccine design. Vaccine 31:4682-4688.
32. Haldar, A. K., V. Yadav, E. Singhal, K. K. Bisht, A. Singh, S. Bhaumik, R. Basu, P. Sen, and S. Roy. 2010. Leishmania donovani isolates with antimony-resistant but not-sensitive phenotype inhibit sodium antimony gluconate-induced dendritic cell activation. PLoS Pathog. 6:e1000907.
33. Chakraborty, D., S. Banerjee, A. Sen, K. K. Banerjee, P. Das, and S. Roy. 2005. Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J. Immunol. 175:3214-3224.
34. Roy, K., M. Ghosh, T. K. Pal, S. Chakrabarti, and S. Roy. 2013. Cholesterol lowering drug may influence cellular immune response by altering MHC II function. J. Lipid Res. 54:3106-3115.
35. Blome, M. C., K. A. Petro, and C. L. Schengrund. 2010. Surface plasmon resonance analysis of ricin binding to plasma membranes isolated from NIH 3T3 cells. Anal. Biochem. 396:212-216.
36. Cho, S., J. H. Park, J. Yu, Y. K. Lee, Y. Byun, H. Chung, I. C. Kwon, and S. Y. Jeong. 2004. Preparation and characterization of reconstructed small intestinal brush border membranes for surface plasmon resonance analysis. Pharm. Res. 21:55-60.
37. Kalipatnapu, S., and A. Chattopadhyay. 2007. Membrane organization of the serotonin 1A receptor monitored by a detergent-free approach. Cell. Mol. Neurobiol. 27:463-474.
38. Busch, R., and J. B. Rothbard. 1990. Detection of peptide-MHC class II complexes on the surface of intact cells. J. Immunol. Methods 134:1-22.
39. Chaves, F. A., and A. J. Sant. 2007. Measurement of peptide dissociation from MHC class II molecules. Curr. Protoc. Immunol. Chapter 18: Unit 18.14.
40. Vacchino, J. F., and H. M. McConnell. 2001. Peptide binding to active class II MHC protein on the cell surface. J. Immunol. 166:6680-6685.
41. Höpner, S., K. Dickhaut, M. Hofstätter, H. Krämer, D. Rückerl, J. A. Söderhäll, S. Gupta, V. Marin-Esteban, R. Kühne, C. Freund, et al. 2006. Small organic compounds enhance antigen loading of class II major histocompatibility complex proteins by targeting the polymorphic P1 pocket. J. Biol. Chem. 281:38535-38542.
42. Falo, L. D., Jr., K. Sullivan, B. Benacerraf, M. F. Mescher, and K. L. Rock. 1985. Analysis of antigen presentation by metabolically inactive accessory cells and their isolated membranes. Proc. Natl. Acad. Sci. USA 82:6647-6651.
43. Jensen, P. E. 1989. Stable association of processed antigen with antigenpresenting cell membranes. J. Immunol. 143:420-425.
44. Busch, R., G. Strang, K. Howland, and J. B. Rothbard. 1990. Degenerate binding of immunogenic peptides to HLA-DR proteins on B cell surfaces. Int. Immunol. 2:443-451.
45. Roy, S., M. T. Scherer, T. J. Briner, J. A. Smith, and M. L. Gefter. 1989. Murine MHC polymorphism and T cell specificities. Science 244:572-575.
46. Bender, V., M. Ali, M. Amon, E. Diefenbach, and N. Manolios. 2004. T cell antigen receptor peptide-lipid membrane interactions using surface plasmon resonance. J. Biol. Chem. 279:54002-54007.
47. Lee, J. M., C. M. Kay, and T. H. Watts. 1992. Conformational changes in mouse MHC class II proteins at acidic pH. Int. Immunol. 4:889-897.
48. Da-Cruz, A. M., F. Conceição-Silva, A. L. Bertho, and S. G. Coutinho. 1994. Leishmania-reactive CD4+ and CD8+ T cells associated with cure of human cutaneous leishmaniasis. Infect. Immun. 62:2614-2618.
49. Wolfram, M., M. Fuchs, M. Wiese, Y. D. Stierhof, and P. Overath. 1996. Antigen presentation by Leishmania mexicana-infected macrophages: activation of helper T cells by a model parasite antigen secreted into the parasitophorous vacuole or expressed on the amastigote surface. Eur. J. Immunol. 26:3153-3162.
50. Mirshahidi, S., L. C. Ferris, and S. Sadegh-Nasseri. 2004. The magnitude of TCR engagement is a critical predictor of T cell anergy or activation. J. Immunol. 172:5346-5355.
51. Ganguly, S., D. Mukhopadhyay, N. K. Das, M. Chaduvula, S. Sadhu, U. Chatterjee, M. Rahman, R. P. Goswami, S. K. Guha, D. Modak, et al. 2010. Enhanced lesional Foxp3 expression and peripheral anergic lymphocytes indicate a role for regulatory T cells in Indian post-kala-azar dermal leishmaniasis. J. Invest. Dermatol. 130:1013-1022.
52. Mukherjee, P., P. C. Sen, and A. C. Ghose. 2006. Lymph node cells from BALB/c mice with chronic visceral leishmaniasis exhibiting cellular anergy and apoptosis: involvement of Ser/Thr phosphatase. Apoptosis 11:2013-2029.
53. Antoine, J. C., E. Prina, T. Lang, and N. Courret. 1998. The biogenesis and properties of the parasitophorous vacuoles that harbour Leishmania in murine macrophages. Trends Microbiol. 6:392-401.
54. De Kroon, A. I., and H. M. McConnell. 1994. Kinetics and specificity of peptide-MHC class II complex displacement reactions. J. Immunol. 152:609-619.
55. Dickhaut, K., S. Hoepner, J. Eckhard, K. H. Wiesmueller, L. Schindler, G. Jung, K. Falk, and O. Roetzschke. 2009. Enhancement of tumour-specific immune responses in vivo by 'MHC loading-enhancer' (MLE). PLoS ONE 4:e6811.
56. Banerjee, S., J. Ghosh, S. Sen, R. Guha, R. Dhar, M. Ghosh, S. Datta, B. Raychaudhury, K. Naskar, A. K. Haldar, et al. 2009. Designing therapies against experimental visceral leishmaniasis by modulating the membrane fluidity of antigen-presenting cells. Infect. Immun. 77:2330-2342.
57. Diaz Granados, C. A., A. J. Dunning, E. Jordanov, V. Landolfi, M. Denis, and H. K. Talbot. 2013. High-dose trivalent influenza vaccine compared to standard dose vaccine in elderly adults: safety, immunogenicity and relative efficacy during the 2009-2010 season. Vaccine 31:861-866