Depletion of regulatory T cells augments a vaccine-induced T effector cell response against the liver-stage of malaria but fails to increase memory

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Espinoza Mora, Maria Del Rosario ^a,b   Steeg, Christiane ^a   Tartz, Susanne ^a   Heussler, Volker ^a   Sparwasser, Tim ^c   Link, Andreas ^b   Fleischer, Bernhard ^a   Jacobs, Thomas ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

^c INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE TOXIN; CIRCUMSPOROZOITE PROTEIN; DIPHTHERIA TOXIN; ENHANCED GREEN FLUORESCENT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MALARIA VACCINE; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BORDETELLA; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; IMMUNOLOGICAL MEMORY; MALARIA; MALE; MOUSE; NONHUMAN; PARASITE LOAD; PARASITEMIA; PLASMODIUM BERGHEI INFECTION; REGULATORY T LYMPHOCYTE; SPOROZOITE; T CELL DEPLETION; TRANSGENIC MOUSE; ANIMAL; DISEASE MODEL; IMMUNIZATION; IMMUNOLOGY; LIVER; LYMPHOCYTE DEPLETION; PARASITOLOGY; PLASMODIUM BERGHEI; T LYMPHOCYTE SUBPOPULATION;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNIZATION; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; LIVER; LYMPHOCYTE DEPLETION; MALARIA; MALARIA VACCINES; MALE; MICE; PLASMODIUM BERGHEI; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84905842689     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104627     Document Type: Article

References (45)

1. Good MF, Doolan DL (1999) Immune effector mechanisms in malaria. Current opinion in immunology 11: 412-419. (Pubitemid 29377908)
2. Balam S, Romero JF, Bongfen SE, Guillaume P, Corradin G (2012) CSP - a model for in vivo presentation of Plasmodium berghei sporozoite antigens by hepatocytes. PloS one 7: e51875.
3. Nussenzweig RS, Vanderberg J, Most H, Orton C (1967) Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature 216: 160-162.
4. Schofield L, Villaquiran J, Ferreira A, Schellekens H, Nussenzweig R, et al. (1987) Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330: 664-666. (Pubitemid 18005584)
5. Krzych U, Dalai S, Zarling S, Pichugin A (2012) Memory CD8 T cells specific for plasmodia liver-stage antigens maintain protracted protection against malaria. Front Immunol 3: 370.
6. Jobe O, Lumsden J, Mueller AK, Williams J, Silva-Rivera H, et al. (2007) Genetically attenuated Plasmodium berghei liver stages induce sterile protracted protection that is mediated by major histocompatibility complex Class Idependent interferon-gamma-producing CD8+ T cells. The Journal of infectious diseases 196: 599-607. (Pubitemid 47206108)
7. Trimnell A, Takagi A, Gupta M, Richie TL, Kappe SH, et al. (2009) Genetically attenuated parasite vaccines induce contact-dependent CD8+ T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. Journal of immunology 183: 5870-5878.
8. Plebanski M, Gilbert SC, Schneider J, Hannan CM, Layton G, et al. (1998) Protection from Plasmodium berghei infection by priming and boosting T cells to a single class I-restricted epitope with recombinant carriers suitable for human use. European journal of immunology 28: 4345-4355. (Pubitemid 28558665)
9. Tartz S, Kamanova J, Simsova M, Sebo P, Bolte S, et al. (2006) Immunization with a circumsporozoite epitope fused to Bordetella pertussis adenylate cyclase in conjunction with cytotoxic T-lymphocyte-associated antigen 4 blockade confers protection against Plasmodium berghei liver-stage malaria. Infection and immunity 74: 2277-2285.
10. Allsopp CE, Plebanski M, Gilbert S, Sinden RE, Harris S, et al. (1996) Comparison of numerous delivery systems for the induction of cytotoxic T lymphocytes by immunization. European journal of immunology 26: 1951-1959. (Pubitemid 26283174)
11. Schneider J, Gilbert SC, Hannan CM, Degano P, Prieur E, et al. (1999) Induction of CD8+ T cells using heterologous prime-boost immunisation strategies. Immunological reviews 170: 29-38. (Pubitemid 29490742)
12. Simsova M, Sebo P, Leclerc C (2004) The adenylate cyclase toxin from Bordetella pertussis-a novel promising vehicle for antigen delivery to dendritic cells. International journal of medical microbiology: IJMM 293: 571-576. (Pubitemid 38667581)
13. Tartz S, Russmann H, Kamanova J, Sebo P, Sturm A, et al. (2008) Complete protection against P. berghei malaria upon heterologous prime/boost immunization against circumsporozoite protein employing Salmonella type III secretion system and Bordetella adenylate cyclase toxoid. Vaccine 26: 5935-5943.
14. Nie CQ, Bernard NJ, Schofield L, Hansen DS (2007) CD4+ CD25+ regulatory T cells suppress CD4 + T-cell function and inhibit the development of Plasmodium berghei-specific TH1 responses involved in cerebral malaria pathogenesis. Infection and immunity 75: 2275-2282. (Pubitemid 46744315)
15. Haque A, Best SE, Amante FH, Mustafah S, Desbarrieres L, et al. (2010) CD4+ natural regulatory T cells prevent experimental cerebral malaria via CTLA-4 when expanded in vivo. PLoS pathogens 6: e1001221.
16. Moore AC, Gallimore A, Draper SJ, Watkins KR, Gilbert SC, et al. (2005) Anti-CD25 antibody enhancement of vaccine-induced immunogenicity: increased durable cellular immunity with reduced immunodominance. Journal of immunology 175: 7264-7273. (Pubitemid 41713421)
17. Lahl K, Sparwasser T (2011) In vivo depletion of FoxP3+ Tregs using the DEREG mouse model. Methods in molecular biology 707: 157-172.
18. Steeg C, Adler G, Sparwasser T, Fleischer B, Jacobs T (2009) Limited role of CD4+Foxp3+ regulatory T cells in the control of experimental cerebral malaria. Journal of immunology 183: 7014-7022.
19. Witney AA, Doolan DL, Anthony RM, Weiss WR, Hoffman SL, et al. (2001) Determining liver stage parasite burden by real time quantitative PCR as a method for evaluating pre-erythrocytic malaria vaccine efficacy. Molecular and Biochemical Parasitology 118: 233-245. (Pubitemid 34001686)
20. Sakaguchi S (2011) Regulatory T cells: history and perspective. Methods in molecular biology 707: 3-17.
21. Hansen W, Westendorf AM, Buer J (2008) Regulatory T cells as targets for immunotherapy of autoimmunity and inflammation. Inflammation & allergy drug targets 7: 217-223.
22. Miyara M, Gorochov G, Ehrenstein M, Musset L, Sakaguchi S, et al. (2011) Human FoxP3 + regulatory T cells in systemic autoimmune diseases. Autoimmunity reviews 10: 744-755.
23. Rech AJ, Vonderheide RH (2009) Clinical use of anti-CD25 antibody daclizumab to enhance immune responses to tumor antigen vaccination by targeting regulatory T cells. Annals of the New York Academy of Sciences 1174: 99-106.
24. Rouse BT, Sarangi PP, Suvas S (2006) Regulatory T cells in virus infections. Immunological reviews 212: 272-286. (Pubitemid 44116714)
25. Rad R, Brenner L, Bauer S, Schwendy S, Layland L, et al. (2006) CD25+/Foxp3 + T cells regulate gastric inflammation and Helicobacter pylori colonization in vivo. Gastroenterology 131: 525-537. (Pubitemid 44142446)
26. Taylor MD, van der Werf N, Harris A, Graham AL, Bain O, et al. (2009) Early recruitment of natural CD4 + Foxp3+ Treg cells by infective larvae determines the outcome of filarial infection. European journal of immunology 39: 192-206.
27. D'Elia R, Behnke JM, Bradley JE, Else KJ (2009) Regulatory T cells: a role in the control of helminth-driven intestinal pathology and worm survival. Journal of immunology 182: 2340-2348.
28. Furuichi Y, Tokuyama H, Ueha S, Kurachi M, Moriyasu F, et al. (2005) Depletion of CD25+CD4+T cells (Tregs) enhances the HBV-specific CD8+ T cell response primed by DNA immunization. World journal of gastroenterology: WJG 11: 3772-3777. (Pubitemid 41149280)
29. Chuang C-M, Hoory T, Monie A, Wu A, Wang M-C, et al. (2009) Enhancing therapeutic HPV DNA vaccine potency through depletion of CD4+CD25+ T regulatory cells. Vaccine 27: 684-689.
30. Couper KN, Lanthier PA, Perona-Wright G, Kummer LW, Chen W, et al. (2009) Anti-CD25 antibody-mediated depletion of effector T cell populations enhances susceptibility of mice to acute but not chronic Toxoplasma gondii infection. Journal of immunology 182: 3985-3994.
31. Couper KN, Blount DG, de Souza JB, Suffia I, Belkaid Y, et al. (2007) Incomplete depletion and rapid regeneration of Foxp3 + regulatory T cells following anti-CD25 treatment in malaria-infected mice. Journal of immunology 178: 4136-4146. (Pubitemid 46492363)
32. Mauduit M, Tewari R, Depinay N, Kayibanda M, Lallemand E, et al. (2010) Minimal role for the circumsporozoite protein in the induction of sterile immunity by vaccination with live rodent malaria sporozoites. Infection and immunity 78: 2182-2188.
33. Gruner AC, Mauduit M, Tewari R, Romero JF, Depinay N, et al. (2007) Sterile protection against malaria is independent of immune responses to the circumsporozoite protein. PloS one 2: e1371.
34. Mahnke K, Ring S, Bedke T, Karakhanova S, Enk AH (2008) Interaction of regulatory T cells with antigen-presenting cells in health and disease. Chemical immunology and allergy 94: 29-39.
35. Tang Q, Krummel MF (2006) Imaging the function of regulatory T cells in vivo. Current opinion in immunology 18: 496-502. (Pubitemid 43947578)
36. Schildknecht A, Brauer S, Brenner C, Lahl K, Schild H, et al. (2010) FoxP3+ regulatory T cells essentially contribute to peripheral CD8+ T-cell tolerance induced by steady-state dendritic cells. Proceedings of the National Academy of Sciences of the United States of America 107: 199-203.
37. Piccirillo CA, d'Hennezel E, Sgouroudis E, Yurchenko E (2008) CD4+Foxp3+ regulatory T cells in the control of autoimmunity: in vivo veritas. Current opinion in immunology 20: 655-662.
38. Nakamura K, Kitani A, Strober W (2001) Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. The Journal of experimental medicine 194: 629-644. (Pubitemid 32844773)
39. Kearley J, Robinson DS, Lloyd CM (2008) CD4+ CD25+ regulatory T cells reverse established allergic airway inflammation and prevent airway remodeling. The Journal of allergy and clinical immunology 122: 617-624 e616.
40. Chaturvedi V, Collison LW, Guy CS, Workman CJ, Vignali DAA (2011) Cutting Edge: Human Regulatory T Cells Require IL-35 To Mediate Suppression and Infectious Tolerance. The Journal of Immunology 186: 6661-6666.
41. Collison LW, Pillai MR, Chaturvedi V, Vignali DA (2009) Regulatory T cell suppression is potentiated by target T cells in a cell contact, IL-35- and IL-10-dependent manner. Journal of immunology 182: 6121-6128.
42. Vignali DA (2012) Mechanisms of Treg suppression: still a long way to go. Frontiers in Immunology 3.
43. Schmidt NW, Podyminogin RL, Butler NS, Badovinac VP, Tucker BJ, et al. (2008) Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proceedings of the National Academy of Sciences of the United States of America 105: 14017-14022.
44. Butler NS, Schmidt NW, Harty JT (2010) Differential effector pathways regulate memory CD8 T cell immunity against Plasmodium berghei versus P. yoelii sporozoites. Journal of immunology 184: 2528-2538.
45. Shanker A (2010) Adaptive control of innate immunity. Immunology letters 131: 107-112.