Trichinella spiralis secreted enzymes regulate nucleotide-induced mast cell activation and release of mouse mast cell protease

Infection and Immunity

Volumn 80, Issue 11, 2012, Pages 3761-3767

  Afferson, Holly C ^a   Eleftheriou, Emily ^a   Selkirk, Murray E ^a   Gounaris, Kleoniki ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CHYMASE; MAST CELL PROTEASE 1; NUCLEOTIDE; PURINERGIC RECEPTOR; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; URIDINE TRIPHOSPHATE;

ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CELL ACTIVATION; CELL FUNCTION; ENZYME RELEASE; INNATE IMMUNITY; MAST CELL; MOUSE; MUCOSA CELL; NONHUMAN; PRIORITY JOURNAL; TRICHINELLA SPIRALIS;

ANIMALS; CELLS, CULTURED; CHYMASES; CYTOKINES; INTESTINAL DISEASES, PARASITIC; INTESTINAL MUCOSA; MAST CELLS; MICE; NUCLEOTIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRICHINELLA SPIRALIS; TRICHINELLOSIS;

EID: 84867617543     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00411-12     Document Type: Article

References (52)

1. Arden SR, et al. 1997. Identification of serine/threonine protein kinases secreted by Trichinella spiralis infective larvae. Mol. Biochem. Parasitol. 90:111-119.
2. Boyer JL, Adams M, Ravi RG, Jacobson KA, Harden TK. 2002. 2-Chloro N(6)-methyl-(N)-methanocarba-2=-deoxyadenosine-3=,5=-bisphosphate is a selective high affinity P2Y(1) receptor antagonist. Br. J. Pharmacol. 135:2004-2010.
3. Brown JK, Knight PA, Wright SH, Thornton EM, Miller HR. 2003. Constitutive secretion of the granule chymase mouse mast cell protease-1 and the chemokine, CCL2, by mucosal mast cell homologues. Clin. Exp. Allergy 33:132-146.
4. Bruce AF, Gares MP, Selkirk ME, Gounaris K. 2006. Functional characterisation of a nematode secreted GM2-activator protein. Mol. Biochem. Parasitol. 147:224 -229.
5. Bulanova E, Bulfone-Paus S. 2010. P2 receptor-mediated signaling in mast cell biology. Purinergic Signal. 6:3-17.
6. Ciana P, et al. 2006. The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J. 25:4615-4627.
7. Cockcroft S, Gomperts BD. 1979. Activation and inhibition of calciumdependent histamine secretion by ATP ions applied to rat mast cells. J. Physiol. 296:229 -243.
8. De Jonge F, et al. 2004. In vitro activation of murine DRG neurons by CGRP-mediated mucosal mast cell degranulation. Am. J. Physiol. Gastrointest. Liver Physiol. 287:G178-G191.
9. Feoktistov I, Ryzhov S, Goldstein AE, Biaggioni I. 2003. Mast cellmediated stimulation of angiogenesis: cooperative interaction between A2B and A3 adenosine receptors. Circ. Res. 92:485-492.
10. Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN, Linden J. 2001. International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol. Rev. 53:527-552.
11. Gallucci S, Matzinger P. 2001. Danger signals: SOS to the immune system. Curr. Opin. Immunol. 13:114-119.
12. Gao ZG, Ding Y, Jacobson KA. 2010. UDP-glucose acting at P2Y14 receptors is a mediator of mast cell degranulation. Biochem. Pharmacol. 79:873-879.
13. Ge ZD, et al. 2006. Cl-IB-MECA [2-chloro-N6-(3-iodobenzyl)adenosine-5=-N-methylcarboxamide] reduces ischemia/reperfusion injury in mice by activating the A3 adenosine receptor. J. Pharmacol. Exp. Ther. 319:1200 -1210.
14. Gordon JL. 1986. Extracellular ATP: effects, sources and fate. Biochem. J. 233:309 -319.
15. Gounaris K. 2002. Nucleotidase cascades are catalyzed by secreted proteins of the parasitic nematode Trichinella spiralis. Infect. Immun. 70: 4917-4924.
16. Gounaris K, Selkirk ME. 2005. Parasite nucleotide-metabolizing enzymes and host purinergic signalling. Trends Parasitol. 21:17-21.
17. Gounaris K, Selkirk ME, Sadeghi SJ. 2004. A nucleotidase with unique catalytic properties is secreted by Trichinella spiralis. Mol. Biochem. Parasitol. 136:257-264.
18. Gounaris K, Thomas S, Najarro P, Selkirk ME. 2001. Secreted variant of nucleoside diphosphate kinase from the intracellular parasitic nematode Trichinella spiralis. Infect. Immun. 69:3658 -3662.
19. Grencis RK. 1997. Th2-mediated host protective immunity to intestinal nematode infections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 352:1377-1384.
20. Harnett W, Harnett MM. 2010. Helminth-derived immunomodulators: can understanding the worm produce the pill? Nat. Rev. Immunol. 10: 278-284.
21. Hasko G, et al. 2000. Inosine inhibits inflammatory cytokine production by a posttranscriptional mechanism and protects against endotoxininduced shock. J. Immunol. 164:1013-1019.
22. Jin X, Shepherd RK, Duling BR, Linden J. 1997. Inosine binds to A3 adenosine receptors and stimulates mast cell degranulation. J. Clin. Invest. 100:2849 -2857.
23. Khan WI, Collins SM. 2004. Immune-mediated alteration in gut physiology and its role in host defence in nematode infection. Parasite Immunol. 26:319 -326.
24. Knight PA, Wright SH, Lawrence CE, Paterson YY, Miller HR. 2000. Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. J. Exp. Med. 192:1849 -1856.
25. Kumar V, Sharma A. 2009. Adenosine: an endogenous modulator of innate immune system with therapeutic potential. Eur. J. Pharmacol. 616: 7-15.
26. Lawrence CE, Paterson YY, Wright SH, Knight PA, Miller HR. 2004. Mouse mast cell protease-1 is required for the enteropathy induced by gastrointestinal helminth infection in the mouse. Gastroenterology 127: 155-165.
27. Lazarowski ER, Boucher RC. 2001. UTP as an extracellular signaling molecule. News Physiol.Sci. 16:1-5.
28. Maizels RM, Yazdanbakhsh M. 2008. T-cell regulation in helminth parasite infections: implications for inflammatory diseases. Chem. Immunol. Allergy 94:112-123.
29. McDermott JR, et al. 2003. Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc. Natl. Acad. Sci. U. S. A. 100: 7761-7766.
30. Melendez AJ, et al. 2007. Inhibition of Fc epsilon RI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nat. Med. 13:1375-1381.
31. Mellor EA, Austen KF, Boyce JA. 2002. Cysteinyl leukotrienes and uridine diphosphate induce cytokine generation by human mast cells through an interleukin 4-regulated pathway that is inhibited by leukotriene receptor antagonists. J. Exp. Med. 195:583-592.
32. Mellor EA, Maekawa A, Austen KF, Boyce JA. 2001. Cysteinyl leukotriene receptor 1 is also a pyrimidinergic receptor and is expressed by human mast cells. Proc. Natl. Acad. Sci. U. S. A. 98:7964 -7969.
33. Miller HR. 1996. Mucosal mast cells and the allergic response against nematode parasites. Vet. Immunol. Immunopathol. 54:331-336.
34. Miller HR, Wright SH, Knight PA, Thornton EM. 1999. A novel function for transforming growth factor-beta1: upregulation of the expression and the IgE-independent extracellular release of a mucosal mast cell granule-specific beta-chymase, mouse mast cell protease-1. Blood 93:3473-3486.
35. Murray M, Smith WD, Waddell AH, Jarrett WF. 1971. Nippostrongylus brasiliensis: histamine and 5-hydroxytryptamine inhibition and worm expulsion. Exp. Parasitol. 30:58-63.
36. Newlands GF, et al. 1991. Heterogeneity of murine bone marrow-derived mast cells: analysis of their proteinase content. Immunology 72:434-439.
37. North RA, Surprenant A. 2000. Pharmacology of cloned P2X receptors. Annu. Rev. Pharmacol. Toxicol. 40:563-580.
38. Onah DN, et al. 2000. Mucosal defense against gastrointestinal nematodes: responses of mucosal mast cells and mouse mast cell protease 1 during primary Strongyloides venezuelensis infection in FcRgammaknockout mice. Infect. Immun. 68:4968-4971.
39. Pfefferkorn JA, et al. 2008. P2Y1 receptor antagonists as novel antithrombotic agents. Bioorg. Med. Chem. Lett. 18:3338 -3343.
40. Ramkumar V, Stiles GL, Beaven MA, Ali H. 1993. The A3 adenosine receptor is the unique adenosine receptor which facilitates release of allergic mediators in mast cells. J. Biol. Chem. 268:16887-16890.
41. Rittiner JE, et al. 2012. AMP is an adenosine A1 receptor agonist. J. Biol. Chem. 287:5301-5309.
42. Saito H, et al. 1991. Extracellular ATP stimulates interleukin-dependent cultured mast cells and eosinophils through calcium mobilization. Int. Arch. Allergy Appl. Immunol. 94:68 -70.
43. Scudamore CL, Thornton EM, McMillan L, Newlands GF, Miller HR. 1995. Release of the mucosal mast cell granule chymase, rat mast cell protease-II, during anaphylaxis is associated with the rapid development of paracellular permeability to macromolecules in rat jejunum. J. Exp. Med. 182:1871-1881.
44. Smith VP, Selkirk ME, Gounaris K. 2000. A reversible protein phosphorylation system is present at the surface of infective larvae of the parasitic nematode Trichinella spiralis. FEBS Lett. 483:104 -108.
45. Spicuzza L, Bonfiglio C, Polosa R. 2003. Research applications and implications of adenosine in diseased airways. Trends Pharmacol. Sci. 24:409-413.
46. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. 1994. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76:519 -529.
47. Tilley SL, Wagoner VA, Salvatore CA, Jacobson MA, Koller BH. 2000. Adenosine and inosine increase cutaneous vasopermeability by activating A(3) receptors on mast cells. J. Clin. Invest. 105:361-367.
48. von Kugelgen I. 2006. Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 110:415-432.
49. von Kugelgen I, Wetter A. 2000. Molecular pharmacology of P2Yreceptors. Naunyn Schmiedebergs Arch. Pharmacol. 362:310 -323.
50. Wang CH. 1997. Study of biological properties of Trichinella spiralis newborn larvae and the antiparasitic mucosal immunity of the host. Front. Biosci. 2:d317-d330.
51. Wright SH, et al. 2002. Transforming growth factor-beta1 mediates coexpression of the integrin subunit alphaE and the chymase mouse mast cell protease-1 during the early differentiation of bone marrow-derived mucosal mast cell homologues. Clin. Exp. Allergy 32:315-324.
52. Yip KH, Wong LL, Lau HY. 2009. Adenosine: roles of different receptor subtypes in mediating histamine release from human and rodent mast cells. Inflamm. Res. 58(Suppl 1):17-19.