Probing of a human proteome microarray with a recombinant pathogen protein reveals a novel mechanism by which hookworms suppress B-cell receptor signaling

Journal of Infectious Diseases

Volumn 211, Issue 3, 2015, Pages 416-425

  Tribolet, Leon ^a   Cantacessi, Cinzia ^a,e   Pickering, Darren A ^a   Navarro, Severine ^a   Doolan, Denise L ^b   Trieu, Angela ^b   Fei, Huang ^f   Chao, Yang ^f   Hofmann, Andreas ^c   Gasser, Robin B ^d   Giacomin, Paul R ^a   Loukas, Alex ^a  

^a JAMES COOK UNIVERSITY   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c GRIFFITH UNIVERSITY   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f BGI SHENZHEN   (China)

Author keywords

antigen receptor; B cell; CD79A; hookworm; host'pathogen interaction; Na ASP 2; Necator americanus; protein microarray; SCP TAPS

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD79A ANTIGEN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE LYN; PROTEIN NA ASP 2; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; CD79 ANTIGEN; HELMINTH PROTEIN; LYN PROTEIN-TYROSINE KINASE; PARASITE ANTIGEN; PRE B CELL RECEPTOR; PROTEIN TYROSINE KINASE; PROTEOME;

ADULT; ARTICLE; B LYMPHOCYTE; CAUCASIAN; DOWN REGULATION; ENZYME MECHANISM; EX VIVO STUDY; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOMODULATION; LYN GENE; NECATOR AMERICANUS; NONHUMAN; NORMAL HUMAN; PI3K GENE; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; UPREGULATION; ANIMAL; CELL CULTURE; GENETIC TRANSCRIPTION; GENETICS; HOOKWORM; HOOKWORM INFECTION; IMMUNOLOGY; MIDDLE AGED; MONONUCLEAR CELL; PROCEDURES;

ADULT; ANCYLOSTOMATOIDEA; ANIMALS; ANTIGENS, CD79; ANTIGENS, HELMINTH; B-LYMPHOCYTES; CELLS, CULTURED; DOWN-REGULATION; HELMINTH PROTEINS; HOOKWORM INFECTIONS; HOST-PATHOGEN INTERACTIONS; HUMANS; LEUKOCYTES, MONONUCLEAR; MIDDLE AGED; PHOSPHATIDYLINOSITOL 3-KINASES; PRE-B CELL RECEPTORS; PROTEIN ARRAY ANALYSIS; PROTEOME; RECOMBINANT PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84922572833     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu451     Document Type: Article

References (50)

1. Hotez PJ, Bethony JM, Diemert DJ, Pearson M, Loukas A. Developing vaccines to combat hookworm infection and intestinal schistosomiasis. Nat Rev Microbiol 2010; 8:814-26.
2. Palmer ED. Course of egg output over a 15 year period in a case of experimentally induced necatoriasis americanus, in the absence of hyper-infection. Am J Trop Med Hyg 1955; 4:756-7.
3. Albonico M, Smith PG, Ercole E, et al. Rate of reinfection with intestinal nematodes after treatment of children with mebendazole or alben-dazole in a highly endemic area. Trans R Soc Trop Med Hyg 1995; 89:538-41.
4. Loukas A, Bethony J, Brooker S, Hotez P. Hookworm vaccines: past, present, and future. Lancet Infect Dis 2006; 6:733-41.
5. Fujiwara RT, Loukas A, Mendez S, et al. Vaccination with irradiated Ancylostoma caninum third stage larvae induces a Th2 protective response in dogs. Vaccine 2006; 24:501-9.
6. Bethony J, LoukasA, Smout M, et al. Antibodies against a secreted protein from hookworm larvae reduce the intensity of hookworm infection in humans and vaccinated laboratory animals. FASEB J 2005; 19:1743-5.
7. Bethony JM, Simon G, Diemert DJ, et al. Randomized, placebo-controlled, double-blind trial of the Na-ASP-2 hookworm vaccine in unexposed adults. Vaccine 2008; 26:2408-17.
8. Diemert DJ, Pinto AG, Freire J, et al. Generalized urticaria induced by the Na-ASP-2 hookworm vaccine: implications for the development of vaccines against helminths. J Allerg Clin Immunol 2012; 130:169-76 e6.
9. Zhan B, Santiago H, Keegan B, et al. Fusion of Na-ASP-2 with human immunoglobulin Fcgamma abrogates histamine release from baso-phils sensitized with anti-Na-ASP-2 IgE. Parasite Immunol 2012; 34:404-11.
10. Hazebrouck S, Guillon B, Drumare MF, Paty E, Wal JM, Bernard H. Trypsin resistance of the major peanut allergen Ara h 6 and allergenicity of the digestion products are abolished after selective disruption of disulfide bonds. Mol Nutr Food Res 2012; 56:548-57.
11. Koyanagi S, Murakami T, Maeda T, et al. Production-scale purification of the recombinant major house dust mite allergen Der f 2 mutant C8/119S. J Biosci Bioeng 2010; 110:597-601.
12. Winkler B, Bolwig C, Seppala U, Spangfort MD, Ebner C, Wiedermann U. Allergen-specific immunosuppression by mucosal treatment with recombinant Ves v 5, a major allergen of Vespula vulgaris venom, in a murine model of wasp venom allergy. Immunology 2003; 110:376-85.
13. Bungiro R, Cappello M. Twenty-first century progress toward the global control of human hookworm infection. Curr Infect Dis Rep 2011; 13:210-7.
14. Hotez PJ, Hawdon JM, Cappello M, et al. Molecular approaches to vaccinating against hookworm disease. Pediatr Res 1996; 40:515-21.
15. Bower MA, Constant SL, Mendez S. Necator americanus: the Na-ASP-2 protein secreted by the infective larvae induces neutrophil recruitment in vivo and in vitro. Exp Parasitol 2008; 118:569-75.
16. Osman A, Wang CK, Winter A, et al. Hookworm SCP/TAPS protein structure-A key to understanding host-parasite interactions and developing new interventions. Biotech Adv 2012; 30:652-7.
17. Asojo OA, Goud G, Dhar K, et al. X-ray structure of Na-ASP-2, a path-ogenesis-related-1 protein from the nematode parasite, Necator ameri-canus, and a vaccine antigen for human hookworm infection. J Mol Biol 2005; 346:801-14.
18. Rieu P, Ueda T, Haruta I, Sharma CP, Arnaout MA. The A-domain of beta 2 integrin CR3 (CD11b/CD18) is a receptor for the hookworm-derived neutrophil adhesion inhibitor NIF. J Cell Biol 1994; 127:2081-91.
19. Goud GN, Bottazzi ME, Zhan B, et al. Expression of the Necator amer-icanus hookworm larval antigen Na-ASP-2 in Pichia pastoris and purification of the recombinant protein for use in human clinical trials. Vaccine 2005; 23:4754-64.
20. Wang CK, Broder U, Weeratunga SK, Gasser RB, Loukas A, Hofmann A. SBAL: a practical tool to generate and edit structure-based amino acid sequence alignments. Bioinformatics 2012; 28:1026-7.
21. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 1993; 234:779-815.
22. Radaev S, Zou Z, Tolar P, et al. Structural and functional studies of Igal-phabeta and its assembly with the B cell antigen receptor. Structure 2010; 18:934-43.
23. Ritchie DW, Kozakov D, Vajda S. Accelerating and focusing protein-protein docking correlations using multi-dimensional rotational FFT generating functions. Bioinformatics 2008; 24:1865-73.
24. The PyMOL Molecular Graphics System, Version 1.5.0.4 Schrödinger, LLC.
25. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25.
26. Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and iso-form switching during cell differentiation. Nat Biotechnol 2010; 28: 511-5.
27. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 2008; 5:621-8.
28. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res 1997; 7:986-95.
29. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001; 125:279-84.
30. Boyle EI, Weng S, Gollub J, et al. GO:TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinfor-matics 2004; 20:3710-5.
31. Mason L, Tribolet L, Simon A, et al. Probing the equatorial groove of the hookworm protein and vaccine candidate antigen, Na-ASP-2. Int J Bio-chem Cell Biol 2014; 50:146-55.
32. Bird DM, Opperman CH. The secret(ion) life of worms. Genome Biol 2009; 10:205.
33. Doyle S. Fungal proteomics: from identification to function. FEMS Microbiol Lett 2011; 321:1-9.
34. Tang YT, Gao X, Rosa BA, et al. Genome of the human hookworm Necator americanus. Nat Genet 2014; 46:261-9.
35. Bethony J, Brooker S, Albonico M, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet 2006; 367: 1521-32.
36. Loukas A, Constant SL, Bethony JM. Immunobiology of hookworm infection. FEMS Immunol Med Microbiol 2005; 43:115-24.
37. McSorley HJ, Loukas A. The immunology of human hookworm infections. Parasite Immunol 2010; 32:549-59.
38. Gaze S, McSorley HJ, Daveson J, et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Path 2012; 8:e1002520.
39. Ferreira I, Smyth D, Gaze S, et al. Hookworm excretory/secretory products induce interleukin-4 (IL-4)+ IL-10+ CD4+ T cell responses and suppress pathology in a mouse model of colitis. Infect Immun 2013; 81:2104-11.
40. Navarro S, Ferreira I, Loukas A. The hookworm pharmacopoeia for inflammatory diseases. Int J Parasitol 2013; 43:225-31.
41. Yang CW, Strong BS, Miller MJ, Unanue ER. Neutrophils influence the level of antigen presentation during the immune response to protein antigens in adjuvants. J Immunol 2010; 185:2927-34.
42. Yang X, Gao X. Role of dendritic cells: a step forward for the hygiene hypothesis. Cell Mol Immunol 2011; 8:12-8.
43. Treanor B. B-cell receptor: from resting state to activate. Immunology 2012; 136:21-7.
44. O'Neill SK, Getahun A, Gauld SB, et al. Monophosphorylation of CD79a and CD79b ITAM motifs initiates a SHIP-1 phosphatase-medi-ated inhibitory signaling cascade required for B cell anergy. Immunity 2011; 35:746-56.
45. Browne CD, Del Nagro CJ, Cato MH, Dengler HS, Rickert RC. Suppression of phosphatidylinositol 3, 4, 5-trisphosphate production is a key determinant of B cell anergy. Immunity 2009; 31:749-60.
46. Fujiwara RT, Cancado GG, Freitas PA, et al. Necator americanus infection: a possible cause of altered dendritic cell differentiation and eosin-ophil profile in chronically infected individuals. PLoS Negl Trop Dis 2009; 3:e399.
47. Mortimer K, Brown A, Feary J, et al. Dose-ranging study for therapeutic infection with Necator americanus in humans. Am J Trop Med Hyg 2006; 75:914-20.
48. Croese J, Giacomin PR, Navarro S, et al. Trace gluten consumption following experimental hookworm infection restores gluten tolerance in celiac disease. J Allergy Clin Immunol 2014; in press.
49. Hardy IR, Anceriz N, Rousseau F, et al. Anti-CD79 antibody induces B cell anergy that protects against autoimmunity. J Immunol 2014; 192:1641-50.
50. Li Y, Chen F, Putt M, et al. B cell depletion with anti-CD79 mAbs ameliorates autoimmune disease in MRL/lpr mice. J Immunol 2008; 181:2961-72.