AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system

PLoS Biology

Volumn 4, Issue 7, 2006, Pages 1137-1146

  Dong, Yuemei ^a   Taylor, Harry E ^a,b   Dimopoulos, George ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; IMMUNOGLOBULIN; INSECT PROTEIN; PATTERN RECOGNITION RECEPTOR;

AGDSCAM GENE; ANOPHELES GAMBIAE; ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; DISEASE CARRIER; EXON; GENE FUNCTION; GENOME ANALYSIS; IMMUNOGLOBULIN GENE; INFECTION RESISTANCE; INNATE IMMUNITY; MALARIA; NONHUMAN; PATHOGENESIS; PHAGOCYTOSIS; PLASMODIUM; PROTEIN DOMAIN; ALTERNATIVE RNA SPLICING; ANIMAL; BACTERIUM; CHEMISTRY; FEMALE; GENETICS; GENOME; IMMUNOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; PARASITOLOGY; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE;

ANOPHELES GAMBIAE; INSECTA;

ALTERNATIVE SPLICING; ANIMALS; ANOPHELES GAMBIAE; BACTERIA; EXONS; FEMALE; GENOME, INSECT; IMMUNITY, NATURAL; IMMUNOGLOBULINS; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PHAGOCYTOSIS; PLASMODIUM; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, PATTERN RECOGNITION; RNA INTERFERENCE;

EID: 33745874084     PISSN: 15457885     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.0040229     Document Type: Article

References (62)

1. Govind S, Nehm RH (2004) Innate immunity in fruit flies: A textbook example of genomic recycling. PLoS Biol 2: e276. DOI: 10.1371/journal.pbio. 0020276
2. Hultmark D (2003) Drosophila immunity: Paths and patterns. Curr Opin Immunol 15: 12-19.
3. Meister M (2004) Blood cells of Drosophila: Cell lineages and role in host defense. Curr Opin Immunol 16: 10-15.
4. Dimopoulos G (2003) Insect immunity and its implication in mosquito-malaria interactions. Cell Microbiol 5: 3-14.
5. Hoffmann JA (2003) The immune response of Drosophila. Nature 426: 33-38.
6. De Gregorio E, Spellman PT, Tzou P, Rubin GM, Lemaitre B (2002) The Toll and Imd pathways are the major regulators of the immune response in Drosophila. Embo J 21: 2568-2579.
7. Theopold U, Schmidt O, Soderhall K, Dushay MS (2004) Coagulation in arthropods: Defense, wound closure, and healing. Trends Immunol 25: 289-294.
8. Brennan CA, Anderson KV (2004) Drosophila: The genetics of innate immune recognition and response. Annu Rev Immunol 22: 457-483.
9. Faulhaber LM, Karp RD (1992) A diphasic immune response against bacteria in the American cockroach. Immunology 75: 378-381.
10. Sequeira T, Tavares D, Arala-Chaves M (1996) Evidence for circulating hemocyte proliferation in the shrimp Penaeus japonicus. Dev Comp Immunol 20: 97-104.
11. Moret Y, Siva-Jothy MT (2003) Adaptive innate immunity? Responsivemode prophylaxis in the mealworm beetle, Tenebrio molitor. Proc Biol Sci 270: 2475-2480.
12. Schmid-Hempel P (2005) Natural insect host-parasite systems show immune priming and specificity: Puzzles to be solved. Bioessays 27: 1026-1034.
13. Kurtz J (2004) Memory in the innate and adaptive immune systems. Microbes Infect 6: 1410-1417.
14. Hoffmann JA, Reichhart JM (2002) Drosophila innate immunity: An evolutionary perspective. Nat Immunol 3: 121-126.
15. Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, et al. (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298: 159-165.
16. Vogel C, Teichmann SA, Chothia C (2003) The immunoglobulin superfamily in Drosophila melanogaster and Caenorhabditis elegans and the evolution of complexity. Development 130: 6317-6328.
17. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, et al. (2000) Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101: 671-684.
18. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, et al. (2005) Extensive diversity of Ig superfamily proteins in the immune system of insects. Science 309: 1874-1878.
19. Graveley BR (2005) Mutually exclusive splicing of the insect Dscam prem-RNA directed by competing intronic RNA secondary structures. Cell 123: 65-73.
20. Zhu H, Hummel T, Clemens JC, Berdnik D, Zipursky SL, et al. (2006) Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat Neurosci 9: 349-355.
21. Schmucker D, Flanagan JG (2004) Generation of recognition diversity in the nervous system. Neuron 44: 219-222.
22. Celotto AM, Graveley BR (2001) Alternative splicing of the Drosophila Dscam pre-mRNA is both temporally and spatially regulated. Genetics 159: 599-608.
23. Neves G, Zucker J, Daly M, Chess A (2004) Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nat Genet 36: 240-246.
24. Barlow GM, Micales B, Chen XN, Lyons GE, Korenberg JR (2002) Mammalian DSCAMs: Roles in the development of the spinal cord, cortex, and cerebellum? Biochem Biophys Res Commun 293: 881-891.
25. Agarwala KL, Ganesh S, Tsutsumi Y, Suzuki T, Amano K, et al. (2001) Cloning and functional characterization of DSCAML1, a novel DSCAM-like cell adhesion molecule that mediates homophilic intercellular adhesion. Biochem Biophys Res Commun 285: 760-772.
26. Yimlamai D, Konnikova L, Moss LG, Jay DG (2005) The zebrafish down syndrome cell adhesion molecule is involved in cell movement during embryogenesis. Dev Biol 279: 44-57.
27. Graveley BR, Kaur A, Gunning D, Zipursky SL, Rowen L, et al. (2004) The organization and evolution of the dipteran and hymenopteran Down syndrome cell adhesion molecule (Dscam) genes. RNA 10: 1499-1506.
28. Dimopoulos G, Christophides GK, Meister S, Schultz J, White KP, et al. (2002) Genome expression analysis of Anopheles gambiae: Responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci U S A 99: 8814-8819.
29. Lundquist EA, Reddien PW, Hartwieg E, Horvitz HR, Bargmann CI (2001) Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration, and apoptotic cell phagocytosis. Development 128: 4475-4488.
30. Muller HM, Dimopoulos G, Blass C, Kafatos FC (1999) A hemocyte-like cell line established from the malaria vector Anopheles gambiae expresses six prophenoloxidase genes. J Biol Chem 274: 11727-11735.
31. Leulier F, Parquet C, Pili-Floury S, Ryu JH, Caroff M, et al. (2003) The Drosophila immune system detects bacteria through specific peptidoglycan recognition. Nat Immunol 4: 478-484.
32. Meister S, Kanzok SM, Zheng XL, Luna C, Li TR, et al. (2005) Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 102: 11420-11425.
33. Du Pasquier L (2005) Immunology: Insects diversify one molecule to serve two systems. Science 309: 1826-1827.
34. Dimopoulos G, Richman A, Muller HM, Kafatos FC (1997) Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci U S A 94: 11508-11513.
35. Manfruelli P, Reichhart JM, Steward R, Hoffmann JA, Lemaitre B (1999) A mosaic analysis in Drosophila fat body cells of the control of antimicrobial peptide genes by the Rel proteins Dorsal and DIF. Embo J 18: 3380-3391.
36. Han YS, Thompson J, Kafatos FC, Barillas-Mury C (2000) Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: The time bomb theory of ookinete invasion of mosquitoes. Embo J 19: 6030-6040.
37. Tahar R, Boudin C, Thiery I, Bourgouin C (2002) Immune response of Anopheles gambiae to the early sporogonic stages of the human malaria parasite Plasmodium falciparum. Embo J 21: 6673-6680.
38. Werner T, Liu G, Kang D, Ekengren S, Steiner H, et al. (2000) A family of peptidoglycan recognition proteins in the fruit fly Drosophila melanogaster. Proc Natl Acad Sci U S A 97: 13772-13777.
39. Choe KM, Werner T, Stoven S, Hultmark D, Anderson KV (2002) Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296: 359-362.
40. Werner T, Borge-Renberg K, Mellroth P, Steiner H, Hultmark D (2003) Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J Biol Chem 278: 26319-26322.
41. Nair SV, Del Valle H, Gross PS, Terwilliger DP, Smith LC (2005) Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiol Genomics 22: 33-47.
42. Foley E, O'Farrell PH (2004) Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol 2: e203. DOI: 10.1371/journal.pbio.0020203
43. Blandin S, Moita LF, Kocher T, Wilm M, Kafatos FC, et al. (2002) Reverse genetics in the mosquito Anopheles gambiae: Targeted disruption of the Defensin gene. EMBO Rep 3: 852-856.
44. Blandin S, Shiao SH, Moita LF, Janse CJ, Waters AP, et al. (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116: 661-670.
45. Vizioli J, Bulet P, Hoffmann JA, Kafatos FC, Muller HM, et al. (2001) Gambicin: A novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc Natl Acad Sci U S A 98: 12630-12635.
46. Vlachou D, Schlegelmilch T, Christophides GK, Kafatos FC (2005) Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 15: 1185-1195.
47. Franke-Fayard B, Trueman H, Ramesar J, Mendoza J, van der Keur M, et al. (2004) A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137: 23-33.
48. Beier MS, Pumpuni CB, Beier JC, Davis JR (1994) Effects of para-aminobenzoic acid, insulin, and gentamicin on Plasmodium falciparum development in anopheline mosquitoes (Diptera: Culicidae). J Med Entomol 31: 561-565.
49. Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, et al. (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104: 709-718.
50. Weiner OD, Rentel MC, Ott A, Brown GE, Jedrychowski M, et al. (2006) Hem-1 complexes are essential for Rac activation, actin polymerization, and myosin regulation during neutrophil chemotaxis. PLoS Biol 4: e38. DOI: 10.1371/journal.pbio.0040038
51. Lee WJ, Lee JD, Kravchenko VV, Ulevitch RJ, Brey PT (1996) Purification and molecular cloning of an inducible gram-negative bacteria-binding protein from the silkworm, Bombyx mori. Proc Natl Acad Sci U S A 93: 7888-7893.
52. Wojtowicz WM, Flanagan JJ, Millard SS, Zipursky SL, Clemens JC (2004) Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 118: 619-633.
53. Celotto AM, Lee JW, Graveley BR (2005) Exon-specific RNA interference: A tool to determine the functional relevance of proteins encoded by alternatively spliced mRNAs. Methods Mol Biol 309: 273-282.
54. Crayton ME III, Powell BC, Vision TJ, Giddings MC (2006) Tracking the evolution of alternatively spliced exons within the Dscam family. BMC Evol Biol 6: 16.
55. Boulanger LM, Huh GS, Shatz CJ (2001) Neuronal plasticity and cellular immunity: Shared molecular mechanisms. Curr Opin Neurobiol 11: 568-578.
56. Boulanger LM, Shatz CJ (2004) Immune signaling in neural development, synaptic plasticity, and disease. Nat Rev Neurosci 5: 521-531.
57. Benedict MQ (1997) Care and maintenance of anopheline mosquitoes. In: Crampton JM, Beard CB, Louis C, editors. The molecular biology of disease vectors: A methods manual. London: Champman and Hall. pp. 3-12.
58. Richman AM, Dimopoulos G, Seeley D, Kafatos FC (1997) Plasmodium activates the innate immune response of Anopheles gambiae mosquitoes. Embo J 16: 6114-6119.
59. Carter R, Ranford-Cartwright L, Alano P (1993) The culture and preparation of gametocytes of Plasmodium falciparum for immunochemical, molecular, and mosquito infectivity studies. Methods Mol Biol 21: 67-88.
60. Drevets DA, Campbell PA (1991) Macrophage phagocytosis: Use of fluorescence microscopy to distinguish between extracellular and intracellular bacteria. J Immunol Methods 142: 31-38.
61. Lane D J (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M, editors. Nucleic acid techniques in bacterial systematics. New York: John Wiley and Sons. pp. 115-175.
62. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.