Toxoplasma gondii is dependent on glutamine and alters migratory profile of infected host bone marrow derived immune cells through SNAT2 and CXCR4 pathways

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Lee, I Ping ^a   Evans, Andrew K ^a   Yang, Cissy ^a   Works, Melissa G ^a   Kumar, Vineet ^b   De Miguel, Zurine ^a   Manley, Nathan C ^a,c   Sapolsky, Robert M ^a,c  

^a STANFORD UNIVERSITY   (United States)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; B7 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; GLUTAMINE; LIPOPOLYSACCHARIDE; PHOSPHATIDYLINOSITOL 3 KINASE; RHO KINASE; SODIUM DEPENDENT NEUTRAL AMINO ACID TRANSPORTER 2; STROMAL CELL DERIVED FACTOR 1ALPHA; UNCLASSIFIED DRUG; CXCL12 PROTEIN, RAT; CXCR4 PROTEIN, RAT; LUCIFERASE; SNAT2 PROTEIN, RAT; STROMAL CELL DERIVED FACTOR 1;

AMINO ACID TRANSPORT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CELL DAMAGE; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; HOST CELL; IMMUNOCOMPETENT CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; NONHUMAN; PARASITE CULTIVATION; PARASITE VIABILITY; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; TOXOPLASMA GONDII; TOXOPLASMOSIS; WESTERN BLOTTING; ANIMAL; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MOTION; DRUG EFFECTS; FIBROBLAST; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; NEWBORN; PARASITOLOGY; PATHOLOGY; PRIMARY CELL CULTURE; REPORTER GENE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TOXOPLASMA; TRANSGENIC ORGANISM;

TOXOPLASMA GONDII;

AMINO ACID TRANSPORT SYSTEMS; ANIMALS; ANIMALS, NEWBORN; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL MOVEMENT; CHEMOKINE CXCL12; DENDRITIC CELLS; FIBROBLASTS; GENE EXPRESSION REGULATION; GENES, REPORTER; GLUTAMINE; HOST-PATHOGEN INTERACTIONS; HUMANS; LIPOPOLYSACCHARIDES; LUCIFERASES; ORGANISMS, GENETICALLY MODIFIED; PRIMARY CELL CULTURE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; TOXOPLASMA;

EID: 84907841896     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109803     Document Type: Article

References (53)

1. MacRae JI, Dixon MW, Dearnley MK, Chua HH, Chambers JM, et al. (2013) Mitochondrial metabolism of sexual and asexual blood stages of the malaria parasite Plasmodium falciparum. BMC Biol 11:67.
2. MacRae JI, Sheiner L, Nahid A, Tonkin C, Striepen B, et al. (2012) Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of Toxoplasma gondii. Cell Host Microbe 12:682-692.
3. Blume M, Rodriguez-Contreras D, Landfear S, Fleige T, Soldati-Favre D, et al. (2009) Host-derived glucose and its transporter in the obligate intracellular pathogen Toxoplasma gondii are dispensable by glutaminolysis. Proc Natl Acad Sci U S A 106:12998-13003.
4. Sheiner L, Vaidya AB, McFadden GI (2013) The metabolic roles of the endosymbiotic organelles of Toxoplasma and Plasmodium spp. Curr Opin Microbiol 16:452-458.
5. Broer S, Brookes N (2001) Transfer of glutamine between astrocytes and neurons. J Neurochem 77:705-719.
6. Kalloniatis M, Tomisich G (1999) Amino acid neurochemistry of the vertebrate retina. Prog Retin Eye Res 18:811-866.
7. Tjader I, Berg A, Wernerman J (2007) Exogenous glutaminecompensating a shortage? Crit Care Med 35:S553-S556.
8. Tanhoffer RA, Yamazaki RK, Nunes EA, Pchevozniki AI, Pchevozniki AM, et al. (2007) Glutamine concentration and immune response of spinal cordinjured rats. J Spinal Cord Med 30:140-146.
9. Albrecht J, Sidoryk-Wegrzynowicz M, Zielinska M, Aschner M (2010) Roles of glutamine in neurotransmission. Neuron Glia Biol 6:263-276.
10. Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A (2006) Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol 8:1611-1623.
11. Lambert H, Vutova PP, Adams WC, Lore K, Barragan A (2009) The Toxoplasma gondii-shuttling function of dendritic cells is linked to the parasite genotype. Infect Immun 77:1679-1688.
12. Procko E, McColl SR (2005) Leukocytes on the move with phosphoinositide 3-kinase and its downstream effectors. Bioessays 27:153-163.
13. Cain RJ, Ridley AJ (2009) Phosphoinositide 3-kinases in cell migration. Biol Cell 101:13-29.
14. Hyde R, Cwiklinski EL, MacAulay K, Taylor PM, Hundal HS (2007) Distinct sensor pathways in the hierarchical control of SNAT2, a putative amino acid transceptor, by amino acid availability. J Biol Chem 282:19788-19798.
15. Evans K, Nasim Z, Brown J, Clapp E, Amin A, et al. (2008) Inhibition of SNAT2 by metabolic acidosis enhances proteolysis in skeletal muscle. J Am Soc Nephrol 19:2119-2129.
16. Mackenzie B, Erickson JD (2004) Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflugers Arch 447:784-795.
17. Li P, Yin YL, Li D, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237-252.
18. Newsholme P (2001) Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? J Nutr 131:2515S-2522S.
19. Saeij JP, Boyle JP, Boothroyd JC (2005) Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol 21:476-481.
20. Darde ML (2004) Genetic analysis of the diversity in Toxoplasma gondii. Ann Ist Super Sanita 40:57-63.
21. Saeij JP, Boyle JP, Grigg ME, Arrizabalaga G, Boothroyd JC (2005) Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains. Infect Immun 73:695-702.
22. Boothroyd JC, Grigg ME (2002) Population biology of Toxoplasma gondii and its relevance to human infection: do different strains cause different disease? Curr Opin Microbiol 5:438-442.
23. Vyas A, Kim SK, Giacomini N, Boothroyd JC, Sapolsky RM (2007) Behavioral changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odors. Proc Natl Acad Sci U S A 104:6442-6447.
24. Vyas A (2013) Parasite-augmented mate choice and reduction in innate fear in rats infected by Toxoplasma gondii. J Exp Biol 216:120-126.
25. Maroni BJ, Karapanos G, Mitch WE (1986) System A amino acid transport in incubated muscle: effects of insulin and acute uremia. Am J Physiol 251:F74-F80.
26. Rae C, Hare N, Bubb WA, McEwan SR, Broer A, et al. (2003) Inhibition of glutamine transport depletes glutamate and GABA neurotransmitter pools: further evidence for metabolic compartmentation. J Neurochem 85:503-514.
27. Song C, Li G (2011) CXCR4 and matrix metalloproteinase-2 are involved in mesenchymal stromal cell homing and engraftment to tumors. Cytotherapy 13:549-561.
28. Lee JY, Buzney CD, Poznansky MC, Sackstein R (2009) Dynamic alterations in chemokine gradients induce transendothelial shuttling of human T cells under physiologic shear conditions. J Leukoc Biol 86:1285-1294.
29. Badillo AT, Zhang L, Liechty KW (2008) Stromal progenitor cells promote leukocyte migration through production of stromal-derived growth factor 1alpha: a potential mechanism for stromal progenitor cell-mediated enhancement of cellular recruitment to wounds. J Pediatr Surg 43:1128-1133.
30. Kraemer BF, Borst O, Gehring EM, Schoenberger T, Urban B, et al. (2010) PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). J Mol Med (Berl) 88:1277-1288.
31. Fuks JM, Arrighi RB, Weidner JM, Kumar MS, Jin Z, et al. (2012) GABAergic signaling is linked to a hypermigratory phenotype in dendritic cells infected by Toxoplasma gondii. PLoS Pathog 8:e1003051.
32. Lambert H, Barragan A (2010) Modelling parasite dissemination: host cell subversion and immune evasion by Toxoplasma gondii. Cell Microbiol 12:292-300.
33. Gupta R, Chattopadhyay D (2009) Glutamate is the chemotaxis-inducing factor in placental extracts. Amino Acids 37:359-366.
34. Gupta R, Palchaudhuri S, Chattopadhyay D (2013) Glutamate induces neutrophil cell migration by activating class I metabotropic glutamate receptors. Amino Acids 44:757-767.
35. Rot A, von Andrian UH (2004) Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu Rev Immunol 22:891-928.
36. Tan W, Martin D, Gutkind JS (2006) The Galpha13-Rho signaling axis is required for SDF-1-induced migration through CXCR4. J Biol Chem 281:39542-39549.
37. Fricker SP, Anastassov V, Cox J, Darkes MC, Grujic O, et al. (2006) Characterization of the molecular pharmacology of AMD3100: a specific antagonist of the G-protein coupled chemokine receptor, CXCR4. Biochem Pharmacol 72:588-596.
38. Hatse S, Princen K, Bridger G, De CE, Schols D (2002) Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett 527:255-262.
39. Evans K, Nasim Z, Brown J, Butler H, Kauser S, et al. (2007) Acidosis-sensing glutamine pump SNAT2 determines amino acid levels and mammalian target of rapamycin signalling to protein synthesis in L6 muscle cells. J Am Soc Nephrol 18:1426-1436.
40. Gazzola RF, Sala R, Bussolati O, Visigalli R, Dall'Asta V, et al. (2001) The adaptive regulation of amino acid transport system A is associated to changes in ATA2 expression. FEBS Lett 490:11-14.
41. Hyde R, Christie GR, Litherland GJ, Hajduch E, Taylor PM, et al. (2001) Subcellular localization and adaptive up-regulation of the System A (SAT2) amino acid transporter in skeletal-muscle cells and adipocytes. Biochem J 355:563-568.
42. Jones HN, Ashworth CJ, Page KR, McArdle HJ (2006) Expression and adaptive regulation of amino acid transport system A in a placental cell line under amino acid restriction. Reproduction 131:951-960.
43. Ling R, Bridges CC, Sugawara M, Fujita T, Leibach FH, et al. (2001) Involvement of transporter recruitment as well as gene expression in the substrate-induced adaptive regulation of amino acid transport system A. Biochim Biophys Acta 1512:15-21.
44. Pinilla J, Aledo JC, Cwiklinski E, Hyde R, Taylor PM, et al. (2011) SNAT2 transceptor signalling via mTOR: a role in cell growth and proliferation? Front Biosci (Elite Ed) 3:1289-1299.
45. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18:1926-1945.
46. Tokunaga C, Yoshino K, Yonezawa K (2004) mTOR integrates amino acidand energy-sensing pathways. Biochem Biophys Res Commun 313:443-446.
47. Hundal HS, Taylor PM (2009) Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am J Physiol Endocrinol Metab 296:E603-E613.
48. Boothroyd JC, Dubremetz JF (2008) Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat Rev Microbiol 6:79-88.
49. Bougdour A, Tardieux I, Hakimi MA (2013) Toxoplasma exports dense granule proteins beyond the vacuole to the host cell nucleus and rewires the host genome expression. Cell Microbiol.
50. Persat F, Mercier C, Ficheux D, Colomb E, Trouillet S, et al. (2012) A synthetic peptide derived from the parasite Toxoplasma gondii triggers human dendritic cells' migration. J Leukoc Biol 92:1241-1250.
51. Fleckenstein MC, Reese ML, Konen-Waisman S, Boothroyd JC, Howard JC, et al. (2012) A Toxoplasma gondii pseudokinase inhibits host IRG resistance proteins. PLoS Biol 10:e1001358.
52. Hunter CA, Sibley LD (2012) Modulation of innate immunity by Toxoplasma gondii virulence effectors. Nat Rev Microbiol 10:766-778.
53. Manley NC, Caso JR, Works MG, Cutler AB, Zemlyak I, et al. (2013) Derivation of injury-responsive dendritic cells for acute brain targeting and therapeutic protein delivery in the stroke-injured rat. PLoS One 8:e61789.