Lack of a functioning P2X7 receptor leads to increased susceptibility to toxoplasmic ileitis

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Miller, Catherine M ^a   Zakrzewski, Alana M ^b   Robinson, Dionne P ^c   Fuller, Stephen J ^d   Walker, Robert A ^a   Ikin, Rowan J ^b   Bao, Shisan J ^e   Grigg, Michael E ^c   Wiley, James S ^f   Smith, Nicholas C ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d UNIVERSITY OF SYDNEY   (Australia)

^e UNIVERSITY OF SYDNEY   (Australia)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

MUS; PROTOZOA; TOXOPLASMA GONDII;

AUTACOID; CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PURINERGIC P2X7 RECEPTOR; REACTIVE NITROGEN SPECIES;

ANIMAL; ANIMAL TOXOPLASMOSIS; DEFICIENCY; DISEASE COURSE; DISEASE MODEL; DISEASE PREDISPOSITION; GENETICS; ILEITIS; KNOCKOUT MOUSE; MALE; METABOLISM; MOUSE; PARASITOLOGY; PATHOLOGY; SIGNAL TRANSDUCTION; TOXOPLASMA;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DISEASE SUSCEPTIBILITY; ILEITIS; INFLAMMATION MEDIATORS; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NF-KAPPA B; REACTIVE NITROGEN SPECIES; RECEPTORS, PURINERGIC P2X7; TOXOPLASMA; TOXOPLASMOSIS, ANIMAL;

EID: 84936805476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129048     Document Type: Article

References (62)

1. Miller CMD, Boulter NR, Ikin RJ, Smith NC. The immunobiology of the innate response to Toxoplasma gondii. Int. J. Parasitol. 2009; 39: 23-39. doi: 10.1016/j.ijpara.2008.08.002 PMID: 18775432
2. Egan CE, Cohen SB, Denkers EY. Insights into inflammatory bowel disease using Toxoplasma gondii as an infectious trigger. Immunol. Cell. Biol. 2012; 90: 668-675. doi: 10.1038/icb.2011.93 PMID: 22064707
3. Combe CL, Moretto MM, Schwartzman JD, Gigley JP, Bzik DJ, Khan IA.Lack of IL-15 results in the suboptimal priming of CD4+ T cell response against an intracellular parasite. Proc. Natl. Acad. Sci. USA 2006; 103: 6635-6640. PMID: 16614074
4. Kelly MN, Kolls JK, Happel K, Schwartzman JD, Schwarzenburger P, Combe C, et al. Interleukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection. Infect. Immun. 2005; 73: 617-621. PMID: 15618203
5. Liesenfeld O, Kang OH, Park D, Nguyen TA, Parkhe CV, Watanabe H, et al. TNF-α, nitric oxide and IFN-γ are all critical for development of necrosis in the small intestine and early mortality in genetically susceptible mice infected perorally with Toxoplasma gondii. Parasite Immunol. 1999; 21: 365-376. PMID: 10417671
6. Vossenka¨mper A, Struck D, Alvarado-Esquivel C, Went T, Takeda K, Akira S, et al. Both IL-12 and IL-18 contribute to small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii, but IL-12 is dominant over IL-18 in parasite control. Eur. J. Immunol. 2004; 34: 3197-3207. PMID: 15368276
7. Muñoz M, Heimesaat MM, Danker K, Struck D, Lohmann U, Plickert R, et al. Interleukin 23 mediates Toxoplasma gondii-induced immunopathology in the gut via matrixmetalloproteinase-2 and IL-22 but independent of IL-17. J. Exp. Med. 2009; 206: 3047-3059. doi: 10.1084/jem.20090900 PMID: 19995958
8. Khan IA, Schwartzman JD, Matsuura T, Kasper LH.A dichotomous role for nitric oxide during acute Toxoplasma gondii infection in mice. Proc. Natl. Acad. Sci. USA 1997; 94: 13955-13960. PMID: 9391134
9. Buzoni-Gatel D, Debbabi H, Mennechet FJ, Martin V, Lepage AC, Schwartzman JD, et al. Murine ileitis after intracellular parasite infection is controlled by TGF-β producing intraepithelia lymphocytes. Gastroenterology 2001; 120: 914-924. PMID: 11231945
10. Mennechet FJ, Kasper LH, Rachinel N, Minns LA, Luangsay S, Vandewalle A, et al. Intestinal intraepithelial lymphocytes prevent pathogen-driven inflammation and regulate the Smad/T-bet pathway of lamina propria CD4+ T cells. Eur. J. Immunol. 2004; 34: 1059-1067. PMID: 15048716
11. Suzuki Y, Sher A, Yap G, Park D, Neyer LE, Liesenfeld O, et al. IL-10 is required for prevention of necrosis in the small intestine and mortality in both genetically resistant BALB/c and susceptible C57BL/6 mice following peroral infection with Toxoplasma. J. Immunol. 2000; 164: 5375-5382. PMID: 10799901
12. Miller CM, Boulter NR, Fuller SJ, Zakrzewski AM, Lees MP, Saunders B, et al. The role of P2X7 receptors in infectious diseases. PLoS Pathogens 2011; 7: e1002212. doi: 10.1371/journal.ppat.1002212 PMID: 22102807
13. Lees MP, Fuller S, McLeod R, Boulter NR, Miller CM, Zakrzewski AM, et al. P2X7 receptor-mediated killing of an intracellular parasite, Toxoplasma gondii by human and mouse macrophages. J. Immunol. 2010; 184: 7040-7046. doi: 10.4049/jimmunol.1000012 PMID: 20488797
14. Cesaro A, Brest P, Hofman V, Hébuterne X, Wildman S, Ferrua B, et al. Amplification loop of the inflammatory process is induced by P2X7R activation in intestinal epithelial cells in response to neutrophil transepithelial migration. Am. J. Physiol. Gastrointest.Liver Physiol. 2010; 299: G32-G42. doi: 10.1152/ajpgi.00282.2009 PMID: 20185692
15. de Campos NE, Marques-da-Silva C, Corrêa G, Castelo-Branco MT, de Souza HS, Countinho-Silva R. Characterizing the presence and sensitivity of the P2X7 receptor in different compartments of the gut. J. Innate Immun. 2012; 4: 529-541. doi: 10.1159/000336628 PMID: 22508425
16. Gulbransen BD, Bashashati M, Hirota SA, Gui X, Roberts JA, MacDonald JA, et al. Activation of neuronal P2X7 receptor-pannexin-1 mediates death of enteric neurons during colitis. Nature Med. 2012; 4: 600-605. doi: 10.1038/nm.2679 PMID: 22426419
17. Kurashima Y, Amiya T, Nochi T, Fujisawa K, Haraguchi T, Iba H, et al. Extracellular ATP mediates mast cell-dependent intestinal inflammation through P2X7 purinoreceptors. Nature Comm. 2012; 3: 1034.
18. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, et al. Disruption of the P2X7 purinoreceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 2005; 114: 386-396. PMID: 15777864
19. Friedle SA, Brautigam VM, Nikodemova M, Wright ML, Watters JJ.The P2X7-Egr pathway regulates nucleotide-dependent inflammatory gene expression in microglia. GLIA 2011; 59: 1-13. doi: 10.1002/glia.21071 PMID: 20878769
20. Miller CM, Zakrzewski AM, Ikin RJ, Boulter NR, Katrib M, Lees MP, et al. Dysregulation of the inflammatory response to the parasite, Toxoplasma gondii, in P2X7 receptor-deficient mice. Int. J. Parasitol. 2011; 41: 301-308. doi: 10.1016/j.ijpara.2010.10.001 PMID: 21044631
21. Jamieson SE, Peixoto-Rangel AL, Hargrave AC, Roubaix LA, Mui EJ, Boulter NR, et al. Evidence for associations between the purinergic receptor P2X7 [P2RX7] and toxoplasmosis. Genes and Immunity 2010; 11: 374-383. doi: 10.1038/gene.2010.31 PMID: 20535134
22. Heiss K, Ja¨nner N, Ma¨hnss B, Schumacher V, Koch-Nolte F, Haag F, et al. High sensitivity of intestinal CD8+ T cells to nucleotides indicates P2X7 as a regulator for intestinal T cell responses. J. Immunol. 2008; 181: 3861-3869. PMID: 18768840
23. Atarashi K, Nishimura J, Shima T, Umesaki Y, Yamamoto M, Onoue M, et al. ATP drives lamina propria TH17 cell differentiation. Nature 2008; 455: 808-812. doi: 10.1038/nature07240 PMID: 18716618
24. Hofman P, Cherfils-Vicini J, Bazin M, Ilie M, Hébuterne X, Gilson E, et al. Genetic and pharmacological inactivation of the purinergic P2RX7 receptor dampens inflammation but increases tumor incidence in a mouse model of colitis-associated cancer. Cancer Res. 2015; 75:835-45. doi: 10.1158/0008-5472.CAN-14-1778 PMID: 25564520
25. Haas SL, Ruether A, Singer MV, Schreiber S, Böcker U. Functional P2X7 receptor polymorphisms (His155Tyr, Arg307Gln, Glu496Ala) in patients with Crohn's Disease. Scand. J. Immunol. 2006; 65: 166-170.
26. Sibley LD, Adams LB, Fukutomi Y, Krahenbuhl JL. Tumor necrosis factor-alpha triggers antitoxoplasmal activity of IFN-gamma primed macrophages. J. Immunol, 1991; 147: 2340-5. PMID: 1918966
27. Gazzinelli RT, Brezin A, Li Q, Nussenblatt RB, Chan CC. Toxoplasma gondii: acquired ocular toxoplasmosis in the murine model, protective role of TNF-alpha and IFN-gamma. Exp. Parasitol, 1994; 78: 217-29. PMID: 8119376
28. Vossenka¨mper A, Struck D, Alvarado-Esquivel C, Went T, Takeda K, Akira S, et al. Both IL-12 and IL-18 contribute to small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii, but IL-12 is dominant over IL-18 in parasite control. Eur. J. Immunol, 2004; 34: 3197-207. PMID: 15368276
29. Gaddi PJ, Yap GS.Cytokine regulation of immunopathology in toxoplasmosis. Immunol Cell Biol, 2007; 85: 155-9. PMID: 17228318
30. Ewald SE, Chavarria-Smith J, Boothroyd JC.NLRP1 is an inflammasome sensor for Toxoplasma gondii. Infect. Immun. 2014; 82: 460-468. doi: 10.1128/IAI.01170-13 PMID: 24218483
31. Chardes T, Velge-Roussel F, Mevelec P, Mevelec MN, Buzoni-Gatel D, Bout D.Mucosal and systemic cellular immune responses induced by Toxoplasma gondii antigens in cyst orally infected mice. Immunology 1993; 78: 421-429. PMID: 8478024
32. Brenier-Pinchart MP, Pelloux H, Simon J, Ricard J, Bosson JL, Ambroise-Thomas P.Toxoplasma gondii induces the secretion of monocyte chemotactic protein-1 in human fibroblasts, in vitro. Mol Cell Biochem, 2000; 209: 79-87. PMID: 10942204
33. Gorfu G, Cirelli KM, Melo MB, Mayer-Narber K, Crown D, Koller BH, et al. Dual role for inflammasome sensors NLRP1 and NLRP3 in murine resistance to Toxoplasma gondii. mBio 2014; 5: e01117-13. doi: 10.1128/mBio.01117-14 PMID: 24865556
34. Johnson RM, Kerr MS, Slaven JE.Plac8-dependent and inducible NO synthase-dependent mechanisms clear Chlamydia muridarum infections from the genital tract. J. Immunol. 2012; 188: 1896-1904. doi: 10.4049/jimmunol.1102764 PMID: 22238459
35. Amrouche-Mekkioui I, Djerdjouri B.N-acetylcysteine improves redox status, mitochondrial dysfunction, mucin-depleted crypts and epithelial hyperplasia in dextran sulfate sodium-induced oxidative colitis in mice. Eur. J. Pharmacol. 2012; 691: 2019-217.
36. Zhong H, May MJ, Jimi E, Ghosh S.The phosphorylation status of nuclear NFκB determines its association with CBP/p300 or HDAC-1. Molecular Cell 2002; 9: 625-636. PMID: 11931769
37. Viatour P, Merville M-P, Bours V, Chariot A.Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends in Biochemical Sciences 2005; 30: 43-52 PMID: 15653325
38. Lenertz LY, Gavala ML, Hill LM, Bertics PJ.Cell signaling via the P2X[7] nucleotide receptor: linkage to ROS production, gene transcription, and receptor trafficking. Purinergic Signal 2009; 5: 175-87. doi: 10.1007/s11302-009-9133-7 PMID: 19263245
39. Gregg B, Taylor BC, Beena J, Tait-Wojno ED, Girgis NM, Miller N, et al. Replication and distribution of Toxoplasma gondii in the small intestine after oral infection with tissue cysts. Infect. Immun. 2013; 81: 1635-1643. doi: 10.1128/IAI.01126-12 PMID: 23460516
40. Boyle JP, Saeij JPJ, Boothroyd JC.Toxoplasma gondii: inconsistent dissemination patterns following oral infection in mice. Exp. Parasitol. 2007; 116: 302-305. PMID: 17335814
41. Correa G, Marques da Silva C, De Abreu Moreira-Souza AC, Vommaro RC, Coutinho-Silva R.Activation of the P2X(7) receptor triggers the elimination of Toxoplasma gondii tachyzoites from infected macrophages. Microbes Infect. 2010; 12: 497-504. doi: 10.1016/j.micinf.2010.03.004 PMID: 20298798
42. Craven M, Egan CE, Dowd SE, McDonough SP, Dogan B, Denkers EY, et al. Inflammation drives dysbiosis and bacterial invasion in murine models of ileal Crohn's disease. PLoS ONE 2012 7: e41594. doi: 10.1371/journal.pone.0041594 PMID: 22848538
43. Heimesaat MM, Bereswill S, Fischer A, Fuchs D, Struck D, Niebergall J, et al. Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology. J. Immunol. 2006; 177: 8785-8795. PMID: 17142781
44. Hand TW, Dos Santos LM, Bouladoux N, Molloy MJ, Pagán AJ, Pepper M, et al. Acute gastrointestinal infection induces long-lived microbiota-specific T cell responses. Science 2012; 337: 1553-1556. PMID: 22923434
45. Egan CE, Sukhumavasi W, Butcher BA, and Denkers EY. Functional aspects of TLR-MyD88 signaling during protozoan infection: focus on Toxoplasma gondii. Clin. Exp. Immunol. 2009; 156: 17-24. doi: 10.1111/j.1365-2249.2009.03876.x PMID: 19161444
46. Ferrari D, Chiozzi P, Falzoni S, Dal Susino M, Melchiorri L, Baricordi OR, et al. Extracellular ATP triggers IL-1 beta release by activating the purinergic P2Z receptor of human macrophages. J. Immunol. 1997; 159: 1451-1458. PMID: 9233643
47. Solle M, Labasi L, Perregaux DG, Stam E, Petrushova N, Koller BH, et al. Altered cytokine production in mice lacking P2X(7) receptors. J. Biol. Chem. 2001; 276: 125-132. PMID: 11016935
48. Sluyter R, Shemon AN, Wiley JS. Glu496 to Ala polymorphism in the P2X7 receptor impairs ATP-induced IL-1 beta release from human monocytes. J. Immunol. 2004; 172: 3399-3405. PMID: 15004138
49. Sluyter R, Dalitz JG, Wiley JS. P2X7 receptor polymorphism impairs extracellular adenosine 5′-triphosphate-induced interleukin-18 release from human monocytes. Genes Immun. 2004; 5: 588-591. PMID: 15306849
50. Wiley JS, Sluyter R, Gu BJ, Stokes L, Fuller SJ. The human P2X7 receptor and its role in innate immunity. Tissue Antigens 2011; 78: 321-332. doi: 10.1111/j.1399-0039.2011.01780.x PMID: 21988719
51. Trabanelli S, Ocadlikova D, Gulinelli S, Curti A, Salvestrini V, Vieira RP, et al. Extracellular ATP exerts opposite effects on activated and regulatory CD4+ T cells via purinergic P2 receptor activation. J. Immunol. 2012; 189: 1303-1310. doi: 10.4049/jimmunol.1103800 PMID: 22753942
52. Oldenhove G, Bouladoux N, Wohlfert EA, Hall JA, Chou D, Dos Santos L, et al. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 2009; 31: 772-786. doi: 10.1016/j.immuni.2009.10.001 PMID: 19896394
53. Brautigam VM, Frasier C, Nikodemova M, Watters JJ. Purinergic receptor modulation of BV-2 microglial cell activity: potential involvement of p38 MAP kinase and CREB. J. Neuroimmunol, 2005; 166: 113-25. PMID: 15979729
54. Gavala ML, Pfeiffer ZA, Bertics PJ. The nucleotide receptor P2RX7 mediates ATP-induced CREB activation in human and murine monocytic cells. J. Leukoc. Biol, 2008; 84: 1159-71. doi: 10.1189/jlb.0907612 PMID: 18625910
55. Wen AY, Sakamoto KM, Miller LS. The role of the transcription factor CREB in immune function. J. Immunol, 2010; 185: 6413-6419. doi: 10.4049/jimmunol.1001829 PMID: 21084670
56. Bachstetter AD, Van Eldik LJ. The p38 MAP kinase family as regulators of proinflammatory cytokine production in degenerative diseases of the CNS. Aging Dis. 2010; 1: 199-211. PMID: 22720195
57. Gorska MM, Liang Q, Stafford SJ, Goplen N, Dharajiya N, Guo L, et al. MK2 controls the level of negative feedback in the NF-kappaB pathway and is essential for vascular permeability and airway inflammation. J. Exp. Med. 2007; 204: 1637-1652. PMID: 17576778
58. Ananieva O, Darragh J, Johansen C, Carr M, McIlrath J, Park JM, et al. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signalling. Nat. Immunol. 2008; 9: 1028-1036. doi: 10.1038/ni.1644 PMID: 18690222
59. Adriouch S, Dox C, Welge V, Seman M, Koch-Nolte F, Haag F. Cutting Edge: A Natural P451L Mutation in the Cytoplasmic Domain Impairs the Function of the Mouse P2X7 Receptor. J. Immunol. 2002; 169: 4108-4112. PMID: 12370338
60. Melgar S, Karlsson A, Michaelsson E. Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am. J. Physiol. Gastrointest. Liver Physiol, 2005; 288: G1328-38. PMID: 15637179
61. Buffet PA, Sulahian A, Garin YJF, Nassar N, Derouin F. Culture microtitration: a sensitive method for quantifying Leishmania infantum in tissues of infected mice. Antimicrob. Agents Chemother. 1995; 39: 2167-2168. PMID: 8540741
62. Pfefferkorn ER, Pfefferkorn LC. Toxoplasma gondii: isolation and preliminary characterization of temperature-sensitive mutants. Exp. Parasitol, 1976; 39: 365-76. PMID: 1269580