CD73-generated adenosine facilitates Toxoplasma gondii differentiation to long-lived tissue cysts in the central nervous system

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

Volumn 109, Issue 40, 2012, Pages 16312-16317

  Mahamed, Deeqa A ^a   Mills, Jeffrey H ^a   Egan, Charlotte E ^a   Denkers, Eric Y ^a   Bynoe, Margaret S ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE 5' (N ETHYLCARBOXAMIDE); ADENOSINE RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BRADYZOITE; BRAIN CYST; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; FIBROBLAST; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TACHYZOITE; TOXOPLASMA GONDII; TOXOPLASMOSIS; WILD TYPE;

5'-NUCLEOTIDASE; ADENOSINE; ANALYSIS OF VARIANCE; ANIMALS; CENTRAL NERVOUS SYSTEM; CYSTS; DEXAMETHASONE; DNA PRIMERS; FEMALE; FLOW CYTOMETRY; KINETICS; LIFE CYCLE STAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; POLYMERASE CHAIN REACTION; TOXOPLASMA; TOXOPLASMOSIS;

MUS; PROTOZOA; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 84867052003     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1205589109     Document Type: Article

References (45)

1. Kim K, Weiss LM (2004) Toxoplasma gondii: The model apicomplexan. Int J Parasitol 34:423-432. (Pubitemid 38299191)
2. Holland GN, et al. (1988) Ocular toxoplasmosis in patients with the acquired immunodeficiency syndrome. Am J Ophthalmol 106:653-667. (Pubitemid 19009919)
3. Falangola MF, Petito CK (1993) Choroid plexus infection in cerebral toxoplasmosis in AIDS patients. Neurology 43:2035-2040. (Pubitemid 23318875)
4. Lambert H, Barragan A (2010) Modelling parasite dissemination: Host cell subversion and immune evasion by Toxoplasma gondii. Cell Microbiol 12:292-300.
5. 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)
6. Däubener W, Hadding U (1997) Cellular immune reactions directed against Toxoplasma gondii with special emphasis on the central nervous system. Med Microbiol Immunol (Berl) 185:195-206.
7. Gavrilescu LC, Denkers EY (2001) IFN-gamma overproduction and high level apoptosis are associated with high but not low virulence Toxoplasma gondii infection. J Immunol 167:902-909. (Pubitemid 32660846)
8. Wang X, Kang H, Kikuchi T, Suzuki Y (2004) Gamma interferon production, but not perforin-mediated cytolytic activity, of T cells is required for prevention of toxoplasmic encephalitis in BALB/c mice genetically resistant to the disease. Infect Immun 72:4432-4438. (Pubitemid 38989299)
9. Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783:673-694.
10. Schetinger MR, Morsch VM, Bonan CD, Wyse AT (2007) NTPDase and 5′-nucleotidase activities in physiological and disease conditions: New perspectives for human health. Biofactors 31:77-98.
11. Thompson LF, et al. (2004) Crucial role for ecto-5′-nucleotidase (CD73) in vascular leakage during hypoxia. J Exp Med 200:1395-1405. (Pubitemid 39657287)
12. Haskó G, Cronstein BN (2004) Adenosine: An endogenous regulator of innate immunity. Trends Immunol 25:33-39. (Pubitemid 38032805)
13. Okusa MD, et al. (2000) A(2A) adenosine receptor-mediated inhibition of renal injury and neutrophil adhesion. Am J Physiol Renal Physiol 279:F809-F818.
14. Haskó G, Németh ZH, Vizi ES, Salzman AL, Szabó C (1998) An agonist of adenosine A3 receptors decreases interleukin-12 and interferon-gamma production and prevents lethality in endotoxemic mice. Eur J Pharmacol 358:261-268.
15. Linden J (2001) Molecular approach to adenosine receptors: Receptor-mediated mechanisms of tissue protection. Annu Rev Pharmacol Toxicol 41:775-787.
16. Grenz A, et al. (2007) Protective role of ecto-5′-nucleotidase (CD73) in renal ischemia. J Am Soc Nephrol 18:833 -845.
17. Mills JH, et al. (2008) CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 105:9325-9330.
18. Carman AJ, Mills JH, Krenz A, Kim DG, Bynoe MS (2011) Adenosine receptor signaling modulates permeability of the blood-brain barrier. J Neurosci 31:13272-13280.
19. Blader IJ, Manger ID, Boothroyd JC (2001) Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J Biol Chem 276: 24223-24231.
20. Schwartzman JD, Pfefferkorn ER (1982) Toxoplasma gondii: Purine synthesis and salvage in mutant host cells and parasites. Exp Parasitol 53:77-86. (Pubitemid 12148209)
21. Chaudhary K, et al. (2004) Purine salvage pathways in the apicomplexan parasite Toxoplasma gondii. J Biol Chem 279:31221-31227. (Pubitemid 39037787)
22. Krug EC, Marr JJ, Berens RL (1989) Purine metabolism in Toxoplasma gondii. J Biol Chem 264:10601-10607. (Pubitemid 19161629)
23. Denkers EY, Caspar P, Hieny S, Sher A (1996) Toxoplasma gondii infection induces specific nonresponsiveness in lymphocytes bearing the V beta 5 chain of the mouse T cell receptor. J Immunol 156:1089-1094. (Pubitemid 26048102)
24. Conley FK, Jenkins KA (1981) Immunohistological study of the anatomic relationship of toxoplasma antigens to the inflammatory response in the brains of mice chronically infected with Toxoplasma gondii. Infect Immun 31:1184-1192. (Pubitemid 11155486)
25. Suzuki Y, Orellana MA, Schreiber RD, Remington JS (1988) Interferon-gamma: The major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
26. Sher A, Denkers EY, Gazzinelli RT (1995) Induction and regulation of host cell-mediated immunity by Toxoplasma gondii. Ciba Found Symp 195:95-104, discussion 104-109.
27. Scharton-Kersten TM, et al. (1996) In the absence of endogenous IFN-gamma, mice develop unimpaired IL-12 responses to Toxoplasma gondii while failing to control acute infection. J Immunol 157:4045-4054. (Pubitemid 126449315)
28. Suzuki Y, Sa Q, Gehman M, Ochiai E (2011) Interferon-gamma- and perforin-mediated immune responses for resistance against Toxoplasma gondii in the brain. Expert Rev Mol Med 13:e31.
29. Suzuki Y (2002) Host resistance in the brain against Toxoplasma gondii. J Infect Dis 185(Suppl 1):S58-S65.
30. 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)
31. Sibley LD, Adams LB, Fukutomi Y, Krahenbuhl JL (1991) Tumor necrosis factor-alpha triggers antitoxoplasmal activity of IFN-gamma primed macrophages. J Immunol 147: 2340-2345.
32. Pfefferkorn ER, Pfefferkorn LC (1977) Specific labeling of intracellular Toxoplasma gondii with uracil. J Protozool 24:449-453. (Pubitemid 8237138)
33. Soete M, Fortier B, Camus D, Dubremetz JF (1993) Toxoplasma gondii: Kinetics of bradyzoite-tachyzoite interconversion in vitro. Exp Parasitol 76:259-264. (Pubitemid 23196029)
34. Bohne W, Gross U, Ferguson DJ, Heesemann J (1995) Cloning and characterization of a bradyzoite-specifically expressed gene (hsp30/bag1) of Toxoplasma gondii, related to genes encoding small heat-shock proteins of plants. Mol Microbiol 16:1221-1230.
35. Ferguson DJ (2004) Use of molecular and ultrastructural markers to evaluate stage conversion of Toxoplasma gondii in both the intermediate and definitive host. Int J Parasitol 34:347-360.
36. Djurković-Djaković O (2001) Murine model of drug-induced reactivation of Toxoplasma gondii. Acta Protozool 40:99.
37. SoêteM, Camus D, Dubremetz JF (1994) Experimental induction of bradyzoite-specific antigen expression and cyst formation by the RH strain of Toxoplasma gondii in vitro. Exp Parasitol 78:361-370. (Pubitemid 24231290)
38. Sullivan WJ, Jr., Jeffers V (2012) Mechanisms of Toxoplasma gondii persistence and latency. FEMS Microbiol Rev 36:717-733.
39. Camus D, Zalis MG, Vannier-Santos MA, Banic DM (1995) The art of parasite survival. Braz J Med Biol Res 28:399-413.
40. Suzuki Y, et al. (2010) Removal of Toxoplasma gondii cysts from the brain by perforin-mediated activity of CD8+ T cells. Am J Pathol 176:1607-1613.
41. Deussen A, Stappert M, Schäfer S, Kelm M (1999) Quantification of extracellular and intracellular adenosine production: Understanding the transmembranous concentration gradient. Circulation 99:2041-2047. (Pubitemid 29183903)
42. Schwab JC, Afifi Afifi M, Pizzorno G, Handschumacher RE, Joiner KA (1995) Toxoplasma gondii tachyzoites possess an unusual plasma membrane adenosine transporter. Mol Biochem Parasitol 70:59-69.
43. Chiang CW, et al. (1999) The adenosine transporter of Toxoplasma gondii. Identification by insertional mutagenesis, cloning, and recombinant expression. J Biol Chem 274:35255-35261.
44. De Koning HP, Al-Salabi MI, Cohen AM, Coombs GH, Wastling JM (2003) Identification and characterisation of high affinity nucleoside and nucleobase transporters in Toxoplasma gondii. Int J Parasitol 33:821-831. (Pubitemid 36831006)
45. Aloisi F, Agresti C, Levi G (1988) Establishment, characterization, and evolution of cultures enriched in type-2 astrocytes. J Neurosci Res 21:188-198. (Pubitemid 19031344)