A Lucilia cuprina excretory-secretory protein inhibits the early phase of lymphocyte activation and subsequent proliferation

Parasite Immunology

Volumn 31, Issue 12, 2009, Pages 750-765

  Elkington, R A ^a   Humphries, M ^a   Commins, M ^a   Maugeri, N ^a   Tierney, T ^a   Mahony, T J ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Immunosuppression; Lucilia cuprina; Proliferation; T lymphocyte

Indexed keywords

BLOWFLY LARVAL IMMUNOSUPPRESSIVE PROTEIN; CONCANAVALIN A; GAMMA INTERFERON; INSECT PROTEIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; IONOMYCIN; MESSENGER RNA; MYRISTIC ACID DERIVATIVE; PROTEIN KINASE C; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CELL CYCLE PHASE; CELL DIVISION; CELL STIMULATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; ENZYME ACTIVATION; FLY; GENE EXPRESSION REGULATION; GROWTH INHIBITION; IMMUNE DEFICIENCY; IMMUNOMODULATION; LARVAL STAGE; LUCILIA CUPRINA; LYMPHOCYTE PROLIFERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SYNTHESIS INHIBITION; SHEEP; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION;

ADAPTIVE IMMUNITY; AMINO ACID SEQUENCE; ANIMALS; CELL PROLIFERATION; CYTOKINES; DIPTERA; GENE EXPRESSION REGULATION; INSECT PROTEINS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LARVA; LYMPHOCYTE ACTIVATION; MOLECULAR SEQUENCE DATA; MYIASIS; PROTEIN BINDING; SEQUENCE ALIGNMENT; SHEEP; SHEEP DISEASES; T-LYMPHOCYTES;

LUCILIA CUPRINA; OVIS; OVIS ARIES;

EID: 71049168813     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2009.01154.x     Document Type: Article

References (44)

1. Sackett D, Holmes P, Abbott K, Jephcott S Barber M. Assessing the Economic Cost of Endemic Disease on the Profitability of Australian Beef Cattle and Sheep Producers. Sydney, Australia, Meat and Livestock Australia, 2006. ISBN 1741910021, AHW.087 http://www.mla.com.au/TopicHierarchy/InformationCentre/ PublicationsDatabase/PublicationDetailsCommerce.htm?pubID=2799.
2. Australian Wool Innovation Limited. Meeting the insecticide resistance challenge. 2008. http://www.wool.com.au/Publications/Beyond-the-Bale/Battling- the-Blowfly-supplement/page--7325.aspx.
3. Guerrini VH, Bell MA Murphy GM. Lucilia cuprina induced hyperammonaemia and alkalosis associated with pathology in sheep. J S Afr Vet Assoc 1988 59 : 73 76.
4. Elkington RA Mahony TJ. A blowfly strike vaccine requires an understanding of host-pathogen interactions. Vaccine 2007 25 : 5133 5145.
5. Maizels RM Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003 3 : 733 744.
6. Kerlin RL East IJ. Potent immunosuppression by secretory/excretory products of larvae from the sheep blowfly Lucilia cuprina. Parasite Immunol 1992 14 : 595 604.
7. Dalton JP, Neill SO, Stack C, et al. Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. Int J Parasitol 2003 9/30 33 : 1173 1181.
8. Pruett JH Jr. Proteolytic cleavage of bovine IgG by hypodermin A, a serine protease of Hypoderma lineatum (Diptera: Oestridae). J Parasitol 1993 79 : 829 833.
9. Temeyer KB, Pruett JH, Kuhn I Files J. Recombinant vaccine development: a novel approach to ectoparasite control. A review of development of a recombinant vaccine for hypodermosis based on hypodermin A. SAAS Bull Biochem Biotechnol 1993 6 : 31 35.
10. Cordoba OL, Linskens SB, Dacci E Santome JA. 'In gel' cleavage with cyanogen bromide for protein internal sequencing. J Biochem Biophys Methods 1997 35 : 1 10.
11. Altschul SF, Gish W, Miller W, Myers EW Lipman DJ. Basic local alignment search tool. J Mol Biol 1990 215 : 403 410.
12. Reddy M, Eirikis E, Davis C, Davis HM Prabhakar U. Comparative analysis of lymphocyte activation marker expression and cytokine secretion profile in stimulated human peripheral blood mononuclear cell cultures: an in vitro model to monitor cellular immune function. J Immunol Methods 2004 293 : 127 142.
13. Schmittgen TD Livak KJ. Analyzing real-time PCR data by the comparative Ct method. Nat Protoc 2008 3 : 1101 1108.
14. Sacks D Sher A. Evasion of innate immunity by parasitic protozoa. Nat Immunol 2002 3 : 1041 1047.
15. Belkaid Y, Sun CM Bouladoux N. Parasites and immunoregulatory T cells. Curr Opin Immunol 2006 18 : 406 412.
16. Allen JE MacDonald AS. Profound suppression of cellular proliferation mediated by the secretions of nematodes. Parasite Immunol 1998 20 : 241 247.
17. Yazdanbakhsh M. Common features of T cell reactivity in persistent helminth infections: lymphatic filariasis and schistosomiasis. Immunol Lett 1999 65 : 109 115.
18. Maizels RM, Gomez-Escobar N, Gregory WF, Murray J Zang X. Immune evasion genes from filarial nematodes. Int J Parasitol 2001 31 : 889 898.
19. Prowse RK, Chaplin P, Robinson HC Spithill TW. Fasciola hepatica cathepsin L suppresses sheep lymphocyte proliferation in vitro and modulates surface CD4 expression on human and ovine T cells. Parasite Immunol 2002 24 : 57 66.
20. Gomez-Munoz MT, Canals-Caballero A, Almeria S, Pasquali P, Zarlenga DS Gasbarre LC. Inhibition of bovine T lymphocyte responses by extracts of the stomach worm Ostertagia ostertagi. Vet Parasitol 2004 120 : 199 214.
21. Carrell RW, Aulak KS Owen MC. The molecular pathology of the serpins. Mol Biol Med 1989 6 : 35 42.
22. Carrell RW. How serpins are shaping up. Science 1999 285 : 1861.
23. Yenbutr P Scott AL. Molecular cloning of a serine proteinase inhibitor from Brugia malayi. Infect Immun 1995 63 : 1745 1753.
24. Zang X, Atmadja AK, Gray P, et al. The serpin secreted by Brugia malayi microfilariae, Bm-SPN-2, elicits strong, but short-lived, immune responses in mice and humans. J Immunol 2000 165 : 5161 5169.
25. Zang X Maizels RM. Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends Biochem Sci 2001 26 : 191 197.
26. Mulenga A, Sugino M, Nakajima M, Sugimoto C Onuma M. Tick-Encoded serine proteinase inhibitors (serpins); potential target antigens for tick vaccine development. J Vet Med Sci 2001 63 : 1063 1069.
27. Imamura S, Namangala B, Tajima T, et al. Two serine protease inhibitors (serpins) that induce a bovine protective immune response against Rhipicephalus appendiculatus ticks. Vaccine 2006 24 : 2230 2237.
28. Casu RE, Eisemann CH, Vuocolo T Tellam RL. The major excretory/secretory protease from Lucilia cuprina larvae is also a gut digestive protease. Int J Parasitol 1996 26 : 623 628.
29. Ruhul Amin ARM, Uddin Biswas MH, Senga T, et al. A role for SHPS-1/SIRP{alpha} in Concanavalin A-dependent production of MMP-9. Genes Cells 2007 12 : 1023 1033.
30. Truneh A, Albert F, Golstein P Schmitt-Verhulst A. Early steps of lymphocyte activation bypassed by synergy between calcium ionophores and phorbol ester. Nature 1985 313 : 318 320.
31. De Boer R, Ganusov V, Milutinovic D, Hodgkin P Perelson A. Estimating lymphocyte division and death rates from CFSE data. Bull Math Biol 2006 68 : 1011 1031. [Epub 2006 May 16].
32. Baine Y, Stankunas BM, Miller P, et al. Functional characterization of novel IL-2 transcriptional inhibitors. J Immunol 1995 154 : 3667 3677.
33. Lipkowitz S, Greene WC, Rubin AL, Novogrodsky A Stenzel KH. Expression of receptors for interleukin 2: role in the commitment of T lymphocytes to proliferate. J Immunol 1984 132 : 31 37.
34. Cantrell DA Smith KA. The interleukin-2 T-cell systems: a new cell growth model. Science 1984 224 : 1312.
35. Deenick EK, Gett AV Hodgkin PD. Stochastic model of T cell proliferation: a calculus revealing IL-2 regulation of precursor frequencies, cell cycle time, and survival. J Immunol 2003 170 : 4963 4972.
36. Smith KA. Interleukin-2: inception, impact, and implications. Science 1988 240 : 1169 1176.
37. Egan PJ, Kimpton W, Seow H-F, Bowles VM, Brandon MR Nash AD. Inflammation-induced changes in the phenotype and cytokine profile of cells migrating through skin and afferent lymph. Immunology 1996 89 : 539 546.
38. Chen C-H, Seguin-Devaux C, Burke NA, et al. Transforming growth factor {beta} blocks Tec kinase phosphorylation, Ca2+ influx, and NFATc translocation causing inhibition of T cell differentiation. J Exp Med 2003 197 : 1689 1699.
39. O'Donnell IJ, Green PE, Connell JA Hopkins PS. Immunoglobulin G antibodies to the antigens of Lucilia cuprina in the sera of fly-struck sheep. Aust J Biol Sci 1980 33 : 27 34.
40. O'Donnell IJ, Green PE, Connell JA Hopkins PS. Immunization of sheep with larval antigens of Lucilia cuprina. Aust J Biol Sci 1981 34 : 411 417.
41. Bowles VM, Carnegie PR Sandeman RM. Immunization of sheep against infection with larvae of the blowfly Lucilia cuprina. Int J Parasitol 1987 17 : 753 758.
42. Bowles VM, Meeusen EN, Young AR, Andrews AE, Nash AD Brandon MR. Vaccination of sheep against larvae of the sheep blowfly (Lucilia cuprina). Vaccine 1996 14 : 1347 1352.
43. Hawkins ED, Hommel M, Turner ML, Battye FL, Markham JF Hodgkin PD. Measuring lymphocyte proliferation, survival and differentiation using CFSE time-series data. Nat Protoc 2007 2 : 2057 2067.
44. Villarino AV, Tato CM, Stumhofer JS, et al. Helper T cell IL-2 production is limited by negative feedback and STAT-dependent cytokine signals. J Exp Med 2007 204 : 65 71.