Priming of CD8+ T cell responses to liver stage malaria parasite antigens

Frontiers in Immunology

Volumn 5, Issue NOV, 2014, Pages

  Corradin, Giampietro ^a   Levitskaya, Jelena ^b  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Antigen presentation to T cells; Dendritic and liver cells as APC; Liver stage antigens; Malaria; Plasmodium

Indexed keywords

GAMMA INTERFERON; LIVER ANTIGEN;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL PROLIFERATION; CELLULAR IMMUNITY; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; MALARIA; PLASMODIUM; REVIEW; T LYMPHOCYTE ACTIVATION;

EID: 84919437154     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00527     Document Type: Review

References (65)

1. Zhang N, Bevan MJ. CD8(+) T cells: foot soldiers of the immune system. Immunity (2011) 35:161-8. doi: 10.1016/j.immuni.2011.07.010
2. Hickman HD, Takeda K, Skon CN, Murray FR, Hensley SE, Loomis J, et al. Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat Immunol (2008) 9:155-65. doi:10.1038/ni1557
3. John B, Harris TH, Tait ED, Wilson EH, Gregg B, Ng LG, et al. Dynamic Imaging of CD8(+) T cells and dendritic cells during infection with Toxoplasma gondii. PLoS Pathog (2009) 5:e1000505. doi:10.1371/journal.ppat.1000505
4. Mueller SN, Hosiawa-Meagher KA, Konieczny BT, Sullivan BM, Bachmann MF, Locksley RM, et al. Regulation of homeostatic chemokine expression and cell trafficking during immune responses. Science (2007) 317:670-4. doi:10.1126/science.1144830
5. Kuka M, Iannacone M. The role of lymph node sinus macrophages in host defense. Ann N Y Acad Sci (2014) 1319:38-46. doi:10.1111/nyas.12387
6. Wei J, Waithman J, Xiao K, Oveissi S, Chen W. Optimal conditions required for influenza A infection-enhanced cross-priming of CD8(+) T cells specific to cell-associated antigens. Immunol Cell Biol (2013) 91:576-82. doi:10.1038/icb.2013.46
7. Helft J, Manicassamy B, Guermonprez P, Hashimoto D, Silvin A, Agudo J, et al. Cross-presenting CD103+ dendritic cells are protected from influenza virus infection. J Clin Invest (2012) 122:4037-47. doi:10.1172/JCI60659
8. Reinicke AT, Omilusik KD, Basha G, Jefferies WA. Dendritic cell cross-priming is essential for immune responses to Listeria monocytogenes. PLoS One (2009) 4:e7210. doi:10.1371/journal.pone.0007210
9. Munz C. Dendritic cells during Epstein Barr virus infection. Front Microbiol (2014) 5:308. doi:10.3389/fmicb.2014.00308
10. Parish IA, Kaech SM. Diversity in CD8(+) T cell differentiation. Curr Opin Immunol (2009) 21:291-7. doi:10.1016/j.coi.2009.05.008
11. Mescher MF, Curtsinger JM, Agarwal P, Casey KA, Gerner M, Hammerbeck CD, et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev (2006) 211:81-92. doi:10.1111/j.0105-2896.2006.00382.x
12. Joshi NS, Cui W, Chandele A, Lee HK, Urso DR, Hagman J, et al. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity (2007) 27:281-95. doi:10.1016/j.immuni.2007.07.010
13. Smith-Garvin JE, Burns JC, Gohil M, Zou T, Kim JS, Maltzman JS, et al. T-cell receptor signals direct the composition and function of the memory CD8+ T-cell pool. Blood (2010) 116:5548-59. doi:10.1182/blood-2010-06-292748
14. Chang JT, Ciocca ML, Kinjyo I, Palanivel VR, McClurkin CE, Dejong CS, et al. Asymmetric proteasome segregation as a mechanism for unequal partitioning of the transcription factor T-bet during T lymphocyte division. Immunity (2011) 34:492-504. doi:10.1016/j.immuni.2011.03.017
15. Buller RM, Holmes KL, Hugin A, Frederickson TN, Morse HC III. Induction of cytotoxic T-cell responses in vivo in the absence of CD4 helper cells. Nature (1987) 328:77-9. doi:10.1038/328077a0
16. 4. Nature (1991) 353:180-4. doi:10.1038/353180a0
17. 4+ T-cell help in CD8+ T-cell responses. Curr Biol (1994) 4:499-505. doi:10.1016/S0960-9822(00)00110-X
18. 4+ T-helper and a T-killer cell. Nature (1998) 393:474-8. doi:10.1038/30989
19. Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, Heath WR. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature (1998) 393:478-80. doi:10.1038/30996
20. Yamauchi LM, Coppi A, Snounou G, Sinnis P. Plasmodium sporozoites trickle out of the injection site. Cell Microbiol (2007) 9:1215-22. doi:10.1111/j.1462-5822.2006.00861.x
21. Chakravarty S, Cockburn IA, Kuk S, Overstreet MG, Sacci JB, Zavala F. CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat Med (2007) 13:1035-41. doi:10.1038/nm1628
22. Krzych U, Schwenk R, Guebre-Xabier M, Sun P, Palmer D, White K, et al. The role of intrahepatic lymphocytes in mediating protective immunity induced by attenuated Plasmodium berghei sporozoites. Immunol Rev (2000) 174:123-34. doi:10.1034/j.1600-0528.2002.00013h.x
23. 4+ T cells modulate expansion and survival but not functional properties of effector and memory CD8+ T cells induced by malaria sporozoites. PLoS One (2011) 6:e15948. doi:10.1371/journal.pone.0015948
24. Tse SW, Cockburn IA, Zhang H, Scott AL, Zavala F. Unique transcriptional profile of liver-resident memory CD8+ T cells induced by immunization with malaria sporozoites. Genes Immun (2013) 14:302-9. doi:10.1038/gene.2013.20
25. Bongfen SE, Torgler R, Romero JF, Renia L, Corradin G. Plasmodium berghei-infected primary hepatocytes process and present the circumsporozoite protein to specific CD8+ T cells in vitro. J Immunol (2007) 178:7054-63. doi:10.4049/jimmunol.178.11.7054
26. Obeid M, Franetich JF, Lorthiois A, Gego A, Grüner AC, Tefit M, et al. Skin-draining lymph node priming is sufficient to induce sterile immunity against pre-erythrocytic malaria. EMBO Mol Med (2013) 5:250-63. doi:10.1002/emmm.201201677
27. Sano G, Hafalla JC, Morrot A, Abe R, Lafaille JJ, Zavala F. Swift development of protective effector functions in naive CD8(+) T cells against malaria liver stages. J Exp Med (2001) 194:173-80. doi:10.1084/jem.194.2.173
28. Brinkmann V, Cyster JG, Hla T. FTY720: sphingosine 1-phosphate receptor-1 in the control of lymphocyte egress and endothelial barrier function. Am J Transplant (2004) 4:1019-25. doi:10.1111/j.1600-6143.2004.00476.x
29. Pinschewer DD, Ochsenbein AF, Odermatt B, Brinkmann V, Hengartner H, Zinkernagel RM. FTY720 immunosuppression impairs effector T cell peripheral homing without affecting induction, expansion, and memory. J Immunol (2000) 164:5761-70. doi:10.4049/jimmunol.164.11.5761
30. Massberg S, von Andrian UH. Fingolimod and sphingosine-1-phosphate - modifiers of lymphocyte migration. N Engl J Med (2006) 355:1088-91. doi:10.1056/NEJMp068159
31. Mempel TR, Henrickson SE, Von Andrian UH. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature (2004) 427:154-9. doi:10.1038/nature02238
32. Henrickson SE, von Andrian UH. Single-cell dynamics of T-cell priming. Curr Opin Immunol (2007) 19:249-58. doi:10.1016/j.coi.2007.04.013
33. Renia L, Rodrigues MM, Nussenzweig V. Intrasplenic immunization with infected hepatocytes: a mouse model for studying protective immunity against malaria pre-erythrocytic stage. Immunology (1994) 82:164-8.
34. Leiriao P, Mota MM, Rodriguez A. Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells. J Infect Dis (2005) 191:1576-81. doi:10.1086/429635
35. Renia L, Maranon C, Hosmalin A, Gruner AC, Silvie O, Snounou G. Do apoptotic Plasmodium-infected hepatocytes initiate protective immune responses? J Infect Dis (2006) 193:163-4. doi:10.1086/498536
36. Marañón C, Desoutter JF, Hoeffel G, Cohen W, Hanau D, Hosmalin A. Dendritic cells cross-present HIV antigens from live as well as apoptotic infected CD4+ T lymphocytes. Proc Natl Acad Sci U S A (2004) 101:6092-7. doi:10.1073/pnas.0304860101
37. Harshyne LA, Watkins SC, Gambotto A, Barratt-Boyes SM. Dendritic cells acquire antigens from live cells for cross-presentation to CTL. J Immunol (2001) 166:3717-23. doi:10.4049/jimmunol.166.6.3717
38. Jung S, Unutmaz D, Wong P, Sano G, De LosSantosK, Sparwasser T, et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity (2002) 17:211-20. doi:10.1016/S1074-7613(02)00365-5
39. Balam S, Romero JF, Bongfen SE, Guillaume P, Corradin G. CSP - a model for in vivo presentation of Plasmodium berghei sporozoite antigens by hepatocytes. PLoS One (2012) 7:e51875. doi:10.1371/journal.pone.0051875
40. Ma J, Trop S, Baer S, Rakhmanaliev E, Arany Z, Dumoulin P, et al. Dynamics of the major histocompatibility complex class I processing and presentation pathway in the course of malaria parasite development in human hepatocytes: implications for vaccine development. PLoS One (2013) 8:e75321. doi:10.1371/journal.pone.0075321
41. Bertolino P, Trescol-Biemont MC, Rabourdin-Combe C. Hepatocytes induce functional activation of naive CD8+ T lymphocytes but fail to promote survival. Eur J Immunol (1998) 28:221-36. doi:10.1002/(SICI)1521-4141(199801)28:01<221::AID-IMMU221>3.3.CO;2-6
42. Bertolino P, Bowen DG, McCaughan GW, Fazekas De St Groth B. Antigen-specific primary activation of CD8+ T cells within the liver. J Immunol (2001) 166:5430-8. doi:10.4049/jimmunol.166.9.5430
43. Bertolino P, McCaughan GW, Bowen DG. Role of primary intrahepatic T-cell activation in the 'liver tolerance effect'. Immunol Cell Biol (2002) 80:84-92. doi:10.1046/j.0818-9641.2001.01048.x
44. Bertolino P, Heath WR, Hardy CL, Morahan G, Miller JF. Peripheral deletion of autoreactive CD8+ T cells in transgenic mice expressing H-2Kb in the liver. Eur J Immunol (1995) 25:1932-42. doi:10.1002/eji.1830250721
45. Bertolino P, Trescol-Biémont MC, Thomas J, Fazekas De St Groth B, Pihlgren M, Marvel J, et al. Death by neglect as a deletional mechanism of peripheral tolerance. Int Immunol (1999) 11:1225-38. doi:10.1093/intimm/11.8.1225
46. Crispe IN. Liver antigen-presenting cells. J Hepatol (2011) 54:357-65. doi:10.1016/j.jhep.2010.10.005
47. Crispe IN. Immune tolerance in liver disease. Hepatology (2014). doi:10.1002/hep.27254
48. Isogawa M, Chung J, Murata Y, Kakimi K, Chisari FV. CD40 activation rescues antiviral CD8(+) T cells from PD-1-mediated exhaustion. PLoS Pathog (2013) 9:e1003490. doi:10.1371/journal.ppat.1003490
49. Gehring AJ, Haniffa M, Kennedy PT, Ho ZZ, Boni C, Shin A, et al. Mobilizing monocytes to cross-present circulating viral antigen in chronic infection. J Clin Invest (2013) 123:3766-76. doi:10.1172/JCI66043
50. Albuquerque SS, Carret C, Grosso AR, Tarun AS, Peng X, Kappe SH, et al. Host cell transcriptional profiling during malaria liver stage infection reveals a coordinated and sequential set of biological events. BMC Genomics (2009) 10:270. doi:10.1186/1471-2164-10-270
51. Chattopadhyay R, de la Vega P, Paik SH, Murata Y, Ferguson EW, Richie TL, et al. Early transcriptional responses of HepG2-A16 liver cells to infection by Plasmodium falciparum sporozoites. J Biol Chem (2011) 286:26396-405. doi:10.1074/jbc. M111.240879
52. Nganou-Makamdop K, Sauerwein RW. Liver or blood-stage arrest during malaria sporozoite immunization: the later the better? Trends Parasitol (2013) 29:304-10. doi:10.1016/j.pt.2013.03.008
53. Ouédraogo AL, de VlasSJ, Nébié I, Ilboudo-Sanogo E, Bousema JT, Ouattara AS, et al. Seasonal patterns of Plasmodium falciparum gametocyte prevalence and density in a rural population of Burkina Faso. Acta Trop (2008) 105:28-34. doi:10.1016/j.actatropica.2007.09.003
54. Beier JC, Oster CN, Onyango FK, Bales JD, Sherwood JA, Perkins PV, et al. Plasmodium falciparum incidence relative to entomologic inoculation rates at a site proposed for testing malaria vaccines in western Kenya. Am J Trop Med Hyg (1994) 50:529-36.
55. Collins FH, Zavala F, Graves PM, Cochrane AH, Gwadz RW, Akoh J, et al. First field trial of an immunoradiometric assay for the detection of malaria sporozoites in mosquitoes. Am J Trop Med Hyg (1984) 33:538-43.
56. ShiffCJ, Minjas JN, Hall T, Hunt RH, Lyimo S, Davis JR. Malaria infection potential of anopheline mosquitoes sampled by light trapping indoors in coastal Tanzanian villages. Med Vet Entomol (1995) 9:256-62. doi:10.1111/j.1365-2915.1995.tb00131.x
57. Valenzuela JG, Pham VM, Garfield MK, Francischetti IM, Ribeiro JM. Toward a description of the sialome of the adult female mosquito Aedes aegypti. Insect Biochem Mol Biol (2002) 32:1101-22. doi:10.1016/S0965-1748(02)00047-4
58. Bissonnette EY, Rossignol PA, Befus AD. Extracts of mosquito salivary gland inhibit tumour necrosis factor alpha release from mast cells. Parasite Immunol (1993) 15:27-33. doi:10.1111/j.1365-3024.1993.tb00569.x
59. Cross ML, Cupp EW, Enriquez FJ. Differential modulation of murine cellular immune responses by salivary gland extract of Aedes aegypti. Am J Trop Med Hyg (1994) 51:690-6.
60. Zeidner NS, Higgs S, Happ CM, Beaty BJ, Miller BR. Mosquito feeding modulates Th1 and Th2 cytokines in flavivirus susceptible mice: an effect mimicked by injection of sialokinins, but not demonstrated in flavivirus resistant mice. Parasite Immunol (1999) 21:35-44. doi:10.1046/j.1365-3024.1999.00199.x
61. Wanasen N, Nussenzveig RH, Champagne DE, Soong L, Higgs S. Differential modulation of murine host immune response by salivary gland extracts from the mosquitoes Aedes aegypti and Culex quinquefasciatus. Med Vet Entomol (2004) 18:191-9. doi:10.1111/j.1365-2915.2004.00498.x
62. Wasserman HA, Singh S, Champagne DE. Saliva of the yellow fever mosquito, Aedes aegypti, modulates murine lymphocyte function. Parasite Immunol (2004) 26:295-306. doi:10.1111/j.0141-9838.2004.00712.x
63. Depinay N, Hacini F, Beghdadi W, Peronet R, Mecheri S. Mast cell-dependent down-regulation of antigen-specific immune responses by mosquito bites. J Immunol (2006) 176:4141-6. doi:10.4049/jimmunol.176.7.4141
64. Schneider BS, Soong L, Zeidner NS, Higgs S. Aedes aegypti salivary gland extracts modulate anti-viral and TH1/TH2 cytokine responses to sindbis virus infection. Viral Immunol (2004) 17:565-73. doi:10.1089/vim.2004.17.565
65. Bonelo A, Valmori D, Triponez F, Tiercy JM, Mentha G, Oberholzer J, et al. Generation and characterization of malaria-specific human CD8(+) lymphocyte clones: effect of natural polymorphism on T cell recognition and endogenous cognate antigen presentation by liver cells. Eur J Immunol (2000) 30:3079-88. doi:10.1002/1521-4141(200011)30:11<3079::AID-IMMU3079>3.0.CO;2-7