Control of Toxoplasma reactivation by rescue of dysfunctional CD8 + T-cell response via PD-1-PDL-1 blockade

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 22, 2011, Pages 9196-9201

  Bhadra, Rajarshi ^a   Gigley, Jason P ^a   Weiss, Louis M ^b   Khan, Imtiaz A ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Adaptive immunity; Recrudescence; Toxoplasma gondii

Indexed keywords

ANTIBODY; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; INFECTION CONTROL; LYMPHOID TISSUE; MICROBIOLOGICAL PHENOMENA AND FUNCTIONS; MORTALITY; MOUSE; NONHUMAN; PARASITE CONTROL; PARASITE DEVELOPMENT; PATHOGENESIS; PRIORITY JOURNAL; TOXOPLASMA GONDII; TOXOPLASMA REACTIVATION; TOXOPLASMOSIS;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, CD80; ANTIGENS, DIFFERENTIATION; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; HUMANS; LYMPHOCYTE ACTIVATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; PEPTIDES; RECEPTORS, IMMUNOLOGIC; TOXOPLASMA; TOXOPLASMOSIS;

ANIMALIA; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 79959357729     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1015298108     Document Type: Article

References (57)

1. Luft BJ, Remington JS (1992) Toxoplasmic encephalitis in AIDS. Clin Infect Dis 15: 211-222.
2. Grant IH, Gold JW, Rosenblum M, Niedzwiecki D, Armstrong D (1990) Toxoplasma gondii serology in HIV-infected patients: The development of central nervous system toxoplasmosis in AIDS. AIDS 4:519-521. (Pubitemid 20215021)
3. Zangerle R, Allerberger F, Pohl P, Fritsch P, Dierich MP (1991) High risk of developing toxoplasmic encephalitis in AIDS patients seropositive to Toxoplasma gondii. Med Microbiol Immunol (Berl) 180:59-66.
4. Jones JL, et al. (1999) Surveillance for AIDS-defining opportunistic illnesses, 1992- 1997. MMWR CDC Surveill Summ 48:1-22.
5. Vidal JE, et al. (2005) Cerebral toxoplasmosis in HIV-positive patients in Brazil: Clinical features and predictors of treatment response in the HAART era. AIDS Patient Care STDS 19:626-634. (Pubitemid 41527673)
6. Lyons RE, McLeod R, Roberts CW (2002) Toxoplasma gondii tachyzoite-bradyzoite interconversion. Trends Parasitol 18:198-201. (Pubitemid 34442589)
7. Scharton-Kersten TM, Yap G, Magram J, Sher A (1997) Inducible nitric oxide is essential for host control of persistent but not acute infection with the intracellular pathogen Toxoplasma gondii. J Exp Med 185:1261-1273. (Pubitemid 27172907)
8. Deckert-Schlüter M, et al. (1994) Toxoplasma encephalitis in congenic B10 and BALB mice: Impact of genetic factors on the immune response. Infect Immun 62:221-228. (Pubitemid 24011963)
9. Gazzinelli R, Xu Y, Hieny S, Cheever A, Sher A (1992) Simultaneous depletion of CD4+ and CD8+ T lymphocytes is required to reactivate chronic infection with Toxoplasma gondii. J Immunol 149:175-180.
10. Gallimore A, et al. (1998) Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J Exp Med 187:1383-1393. (Pubitemid 28215398)
11. Su C, et al. (2003) Recent expansion of Toxoplasma through enhanced oral transmission. Science 299:414-416. (Pubitemid 36120048)
12. Hughes HP, Kasper LH, Little J, Dubey JP (1988) Absence of a role for natural killer cells in the control of acute infection by Toxoplasma gondii oocysts. Clin Exp Immunol 72:394-399.
13. Ferguson DJ, Huskinson-Mark J, Araujo FG, Remington JS (1994) A morphological study of chronic cerebral toxoplasmosis in mice: Comparison of four different strains of Toxoplasma gondii. Parasitol Res 80:493-501. (Pubitemid 24261787)
14. Sibley LD, Khan A, Ajioka JW, Rosenthal BM (2009) Genetic diversity of Toxoplasma gondii in animals and humans. Philos Trans R Soc Lond B Biol Sci 364:2749-2761.
15. Fleige T, Fischer K, Ferguson DJ, Gross U, Bohne W (2007) Carbohydrate metabolism in the Toxoplasma gondii apicoplast: Localization of three glycolytic isoenzymes, the single pyruvate dehydrogenase complex, and a plastid phosphate translocator. Eukaryot Cell 6:984-996. (Pubitemid 46983298)
16. Dzierszinski F, Mortuaire M, Dendouga N, Popescu O, Tomavo S (2001) Differential expression of two plant-like enolases with distinct enzymatic and antigenic properties during stage conversion of the protozoan parasite Toxoplasma gondii. J Mol Biol 309: 1017-1027. (Pubitemid 32623305)
17. Fux B, et al. (2007) Toxoplasma gondii strains defective in oral transmission are also defective in developmental stage differentiation. Infect Immun 75:2580-2590. (Pubitemid 46744350)
18. Tait ED, et al. (2010) Virulence of Toxoplasma gondii is associated with distinct dendritic cell responses and reduced numbers of activated CD8+ T cells. J Immunol 185:1502-1512.
19. Torre D, et al.; Italian Collaborative Study Group (1998) Randomized trial of trimethoprim-sulfamethoxazole versus pyrimethamine-sulfadiazine for therapy of toxoplasmic encephalitis in patients with AIDS. Antimicrob Agents Chemother 42: 1346-1349.
20. Weiss LM, et al. (1995) A cell culture system for study of the development of Toxoplasma gondii bradyzoites. J Eukaryot Microbiol 42:150-157.
21. Ferguson DJ, Hutchison WM (1987) The host-parasite relationship of Toxoplasma gondii in the brains of chronically infected mice. Virchows Arch A Pathol Anat Histopathol 411:39-43. (Pubitemid 17064419)
22. Courret N, et al. (2006) CD11c- and CD11b-expressing mouse leukocytes transport single Toxoplasma gondii tachyzoites to the brain. Blood 107:309-316. (Pubitemid 43053557)
23. Zammit DJ, Cauley LS, Pham QM, Lefrançois L (2005) Dendritic cells maximize the memory CD8 T cell response to infection. Immunity 22:561-570. (Pubitemid 40719192)
24. Langhorne J, Ndungu FM, Sponaas AM, Marsh K (2008) Immunity to malaria: More questions than answers. Nat Immunol 9:725-732. (Pubitemid 351859155)
25. Bustamante JM, Bixby LM, Tarleton RL (2008) Drug-induced cure drives conversion to a stable and protective CD8+ T central memory response in chronic Chagas disease. Nat Med 14:542-550. (Pubitemid 351655210)
26. Wilson EH, et al. (2009) Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 30: 300-311.
27. Barber DL, et al. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682-687. (Pubitemid 43237609)
28. Janumyan YM, et al. (2003) Bcl-xL/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry. EMBO J 22:5459-5470. (Pubitemid 37279955)
29. Andersen JL, et al. (2006) HIV-1 Vpr-induced apoptosis is cell cycle dependent and requires Bax but not ANT. PLoS Pathog 2:e127.
30. Galea I, et al. (2007) An antigen-specific pathway for CD8 T cells across the blood-brain barrier. J Exp Med 204:2023-2030. (Pubitemid 47360864)
31. Joshi NS, et al. (2007) Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295. (Pubitemid 47284924)
32. Chang JT, et al. (2007) Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science 315:1687-1691. (Pubitemid 46515618)
33. Dias P, et al. (2010) CD4 T-cell help programs a change in CD8 T-cell function enabling effective long-term control of murine gammaherpesvirus 68: Role of PD-1-PD-L1 interactions. J Virol 84:8241-8249.
34. Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988) Interferon-gamma: The major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
35. Hakim FT, et al. (1991) CD8+ T cells from mice vaccinated against Toxoplasma gondii are cytotoxic for parasite-infected or antigen-pulsed host cells. J Immunol 147: 2310-2316.
36. Lamoril J, et al. (1996) Detection by PCR of Toxoplasma gondii in blood in the diagnosis of cerebral toxoplasmosis in patients with AIDS. J Clin Pathol 49:89-92. (Pubitemid 26034156)
37. Glimcher LH, Townsend MJ, Sullivan BM, Lord GM (2004) Recent developments in the transcriptional regulation of cytolytic effector cells. Nat Rev Immunol 4:900-911. (Pubitemid 39490765)
38. Intlekofer AM, et al. (2005) Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6:1236-1244. (Pubitemid 43045635)
39. Pearce EL, et al. (2003) Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302:1041-1043. (Pubitemid 37386196)
40. Cruz-Guilloty F, et al. (2009) Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J Exp Med 206:51-59.
41. Sanjabi S, Mosaheb MM, Flavell RA (2009) Opposing effects of TGF-beta and IL-15 cytokines control the number of short-lived effector CD8+ T cells. Immunity 31: 131-144.
42. Mueller SN, Ahmed R (2009) High antigen levels are the cause of T cell exhaustion during chronic viral infection. Proc Natl Acad Sci USA 106:8623-8628.
43. Shin H, Wherry EJ (2007) CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol 19:408-415. (Pubitemid 47284857)
44. Snyder CM, et al. (2008) Memory inflation during chronic viral infection is maintained by continuous production of short-lived, functional T cells. Immunity 29:650-659.
45. Zhu J, et al. (2007) Virus-specific CD8+ T cells accumulate near sensory nerve endings in genital skin during subclinical HSV-2 reactivation. J Exp Med 204:595-603. (Pubitemid 46457082)
46. Wherry EJ, Blattman JN, Ahmed R (2005) Low CD8 T-cell proliferative potential and high viral load limit the effectiveness of therapeutic vaccination. J Virol 79:8960-8968. (Pubitemid 40934807)
47. Fuller MJ, Zajac AJ (2003) Ablation of CD8 and CD4 T cell responses by high viral loads. J Immunol 170:477-486. (Pubitemid 36026174)
48. Wherry EJ, Blattman JN, Murali-Krishna K, van der Most R, Ahmed R (2003) Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J Virol 77:4911-4927. (Pubitemid 36402840)
49. Gazzinelli RT, Eltoum I, Wynn TA, Sher A (1993) Acute cerebral toxoplasmosis is induced by in vivo neutralization of TNF-alpha and correlates with the downregulated expression of inducible nitric oxide synthase and other markers of macrophage activation. J Immunol 151:3672-3681. (Pubitemid 23282679)
50. Mordue DG, Monroy F, La Regina M, Dinarello CA, Sibley LD (2001) Acute toxoplasmosis leads to lethal overproduction of Th1 cytokines. J Immunol 167: 4574-4584. (Pubitemid 32954337)
51. Brooks DG, Lee AM, Elsaesser H, McGavern DB, Oldstone MB (2008) IL-10 blockade facilitates DNA vaccine-induced T cell responses and enhances clearance of persistent virus infection. J Exp Med 205:533-541. (Pubitemid 351439301)
52. Jankovic D, et al. (2007) Conventional T-bet(+)Foxp3(-) Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J Exp Med 204:273-283. (Pubitemid 46294544)
53. Teixeiro E, et al. (2009) Different T cell receptor signals determine CD8+ memory versus effector development. Science 323:502-505.
54. Almeida JR, et al. (2009) Antigen sensitivity is a major determinant of CD8+ T-cell polyfunctionality and HIV-suppressive activity. Blood 113:6351-6360.
55. Sheppard KA, et al. (2004) PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett 574:37-41.
56. Reichmann G, Villegas EN, Craig L, Peach R, Hunter CA (1999) The CD28/B7 interaction is not required for resistance to Toxoplasma gondii in the brain but contributes to the development of immunopathology. J Immunol 163:3354-3362. (Pubitemid 29431837)
57. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.