Glyceraldehyde-3-phosphate dehydrogenase of the parasitic nematode Haemonchus contortus binds to complement C3 and inhibits its activity

Parasite Immunology

Volumn 35, Issue 12, 2013, Pages 457-467

  Sahoo, S ^a   Murugavel, S ^a   Devi, I K ^a   Vedamurthy, G V ^a   Gupta, S C ^a   Singh, B P ^a   Joshi, P ^a  

^a INDIAN VETERINARY RESEARCH INSTITUTE   (India)

Author keywords

Complement activity; GAPDH; H. contortus; H.c C3BP; Immunomodulation; MAC

Indexed keywords

ANTISERUM; BINDING PROTEIN; COMPLEMENT; COMPLEMENT C3 BINDING PROTEIN; COMPLEMENT COMPONENT C3; COMPLEMENT MEMBRANE ATTACK COMPLEX; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; PROTEIN; SEPHAROSE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; COMPLEMENT ACTIVATION; COMPLEMENT HEMOLYSIS TEST; COMPLEMENT SYSTEM; CONTROLLED STUDY; ENZYME ACTIVITY; ESCHERICHIA COLI; GROWTH INHIBITION; HAEMONCHUS CONTORTUS; IMMUNOMODULATION; MASS SPECTROMETRY; MOLECULAR BIOLOGY; MOLECULE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SECRETION; SEQUENCE ANALYSIS;

COMPLEMENT ACTIVITY; GAPDH; H.C-C3BP; H. CONTORTUS; IMMUNOMODULATION; MAC;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, HELMINTH; COMPLEMENT ACTIVATION; COMPLEMENT C3; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GOAT DISEASES; GOATS; HAEMONCHIASIS; HAEMONCHUS; HELMINTH PROTEINS; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; RECOMBINANT PROTEINS; SHEEP;

EID: 84887162687     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/pim.12058     Document Type: Article

References (42)

1. Sood ML. Haemonchus in India. Parasitology 1981; 83: 639-650.
2. McLeod RS. The economic impact of worm infections in small ruminants in Southeast Asia, India and Australia. In Sani RA, Gray GD, Baker RL (eds): Worm Control for Small Ruminants in Tropical Asia, ACIAR Monograph 2004: 23-33.
3. Fox MT. Pathophysiology of infection with gastrointestinal nematodes in domestic ruminants: recent developments. Vet Parasitol 1997; 72: 285-308.
4. Waller PJ. The development of anthelmintic resistance in ruminant livestock. Acta Trop 1994; 56: 233-243.
5. Balic A, Bowles VM & Meeusen EN. Cellular profiles in the abomasal mucosa and lymph node during primary infection with Haemonchus contortus in sheep. Vet Immunol Immunopathol 2000; 75: 109-120.
6. Williamson AL, Brindley PJ, Knox DP, Hotez PJ & Loukas A. Digestive proteases of blood-feeding nematodes. Trends Parasitol 2003; 19: 417-423.
7. Mulcahy G, O'neill S, Donnelly S & Dalton JP. Helminths at mucosal barriers-interaction with the immune system. Adv Drug Deliv Rev 2004; 56: 853-868.
8. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD & Allen JE. Helminth parasites-masters of regulation. Immunol Rev 2004; 201: 89-116.
9. Schallig HDFH, van Leeuwen MAW & Hendrikk WML. Immune responses of Texel sheep to excretory/secretory products of adult Haemonchus contortus. Parasitology 1994; 108: 351-357.
10. Suchitra S & Joshi P. Characterization of Haemonchus contortus calreticulin suggests its role in feeding and immune evasion by the parasite. Biochim Biophys Acta 2005; 1722: 293-303.
11. Suchitra S, Anbu KA, Rathore DK, Mahawar M, Singh BP & Joshi P. Haemonchus contortus calreticulin binds to C-reactive of its host, a novel survival strategy of the parasite. Parasite Immunol 2008; 30: 371-374.
12. Goldsby RA, Kindt TJ, Osborne BA & Kuby J (eds). The complement system. In Immunology. New York, Freeman and Co, 2003: 299-318.
13. Burman JD, Leung E, Atkins KL, et al. Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein: indications of a novel mechanism of complement evasion by Staphylococcus aureus. J Biol Chem 2008; 283: 17579-17593.
14. Norris KA, Bradt B, Cooper NR & So M. Characterization of a Trypanosoma cruzi C3 binding protein with functional and genetic similarities to the human complement regulatory protein, decay-accelerating factor. J Immunol 1991; 147: 2240-2247.
15. Jeffrey SB & John FT. Inhibition of C3 Deposition on Streptococcus equi subsp. equi by M Protein: a mechanism for survival in equine blood. Infect Immun 1994; 62: 3515-3520.
16. Mohan J, Saini M & Joshi P. Isolation of a spermatozoa motility inhibiting factor from chicken seminal plasma with antibacterial property. Biochim Biophys Acta 1995; 1245: 407-413.
17. Naresha S, Suryawanshi A, Agarwal M, Singh BP & Joshi P. Mapping the complement C1q binding site in Haemonchus contortus calreticulin. Mol Biochem Parasitol 2009; 166: 42-46.
18. Zwirner J, Felber E, Reite C & Reithmuller G, Feucht HE. Deposition of complement activation products on plastic-adsorbed immunoglobulins. A simple ELISA technique for the detection of defined complement deficiencies. J Immunol Methods 1989; 124: 121-129.
19. Beutler E (ed). Red cell metabolism. In A Manual of Biochemical Methods. New York, Grune and Stratton, 1984: 51-52.
20. Moreno-Indias I, Dodds AW, Argüello A, Castro N & Sim RB. The complement system of the goat: haemolytic assays and isolation of major proteins. BMC Vet Res 2012; 8: 91-100.
21. Allison WS & Kaplan NO. The comparative enzymology of triosephosphate dehydrogenase. J Biol Chem 1964; 239: 2140-2152.
22. +-dependent glyceraldehyde-3-phosphate dehydrogenase of adult Haemonchus contortus. J Helminthol 2011; 85: 421-429.
23. Yatsuda AP, Krijgsveld J, Cornelissen AWCA, Heck AJR & De vries E. Comprehensive analysis of the secreted proteins of the parasite Haemonchus contortus reveals extensive sequence variation and differential immune recognition. J Biol Chem 2003; 278: 16941-16951.
24. Lindahl G, Sjobring U & Johnsson E. Human complement regulators: a major target for pathogenic microorganisms. Curr Opin Immunol 2000; 12: 44-51.
25. Duthy TG, Ormsby RJ, Giannakis E, et al. The human complement regulator factor H binds pneumococcal surface protein PspC via short consensus repeats 13 to 15. Infect Immun 2002; 70: 5604-5611.
26. Garcia BL, Ramyar KX, Tzekou A, et al. Molecular basis for complement recognition and inhibition determined by crystallographic studies of the staphylococcal complement inhibitor (SCIN) bound to C3c and C3b. J Mol Biol 2010; 402: 17-29.
27. Lee LY, Höök M, Haviland D, et al. Inhibition of complement activation by a secreted Staphylococcus aureus protein. J Infect Dis 2004; 190: 571-579.
28. Hammel M, Sfyroera G, Pyrpassopoulos S, et al. Characterization of Ehp, a secreted complement inhibitory protein from Staphylococcus aureus. J Biol Chem 2007; 282: 30051-30061.
29. Yutaka T, Masaya Y, Shigeyuki H & Shigetada K. Multifunctional glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pyogenes is essential for evasion from neutrophils. J Biol Chem 2006; 281: 14215-14223.
30. Pancholi V & Fischetti VA. A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med 1992; 176: 415-426.
31. Skelly PJ. Intravascular schistosomes and complement. Trends Parasitol 2004; 20: 370-374.
32. Inal J. Complement C2 receptor inhibitor trispanning: from man to schistosome. Springer Semin Immunopathol 2006; 27: 509-510.
33. Deng J, Gold D, LoVerde PT & Fishelson Z. Inhibition of the complement membrane attack complex by Schistosoma mansoni paramyosin. Infect Immun 2003; 71: 6402-6410.
34. Skelly PJ, Wilson RA, Baker JR, Muller R & Rollinson D. Making sense of the Schistosome surface. In Molyneux DH (ed): Advances in Parasitology. UK, Academic Press, 2006: 185-284.
35. Keating JH, Wilson RA & Skelly PJ. No overt cellular inflammation around intravascular schistosomes in vivo. J Parasitol 2006; 92: 1365-1369.
36. Pearce EJ, Hall BF & Sher A. Host-specific evasion of the alternative complement pathway by schistosomes correlates with the presence of a phospholipase C-sensitive surface molecule resembling human decay accelerating factor. J Immunol 1990; 144: 2751-2756.
37. Braschi S & Wilson RA. Proteins exposed at the adult schistosome surface revealed by biotinylation. Mol Cell Proteomics 2006; 5: 347-356.
38. Zheng L, Roeder RG & Luo Y. S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 2003; 114: 255-266.
39. Hara MR, Agrawal N, Kim SF, et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 2005; 7: 665-674.
40. Tarze A, Deniaud A, Le BM, et al. GAPDH, a novel regulator of the pro-apoptotic mitochondrial membrane permeabilization. Oncogene 2007; 26: 2606-2620.
41. Terrasse R, Delorme PT, Moriscot C, et al. Human and Pneumococcal cell surface glyceraldehydes-3-phosphate dehydrogenase (GAPDH) proteins are both ligands of human C1q protein. J Biol Chem 2012; 267: 42620-42633.
42. Schallig HDFH. Immunological responses of sheep to Haemonchus contortus. Parasitology 2000; 120: S63-S72.