Sequence-structure-function relations of the mosquito leucine-rich repeat immune proteins

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Waterhouse, Robert M ^a,b   Povelones, Michael ^c   Christophides, George K ^c  

^a UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES PLASMODIUM RESPONSIVE LEUCINE RICH REPEAT 1C; CYSTEINE; LEUCINE RICH REPEAT IMMUNE PROTEIN 1; MEMBRANE PROTEIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; DISULFIDE; INSECT PROTEIN; LEUCINE RICH REPEAT PROTEINS; LEUCINE-RICH REPEAT PROTEINS; PROTEIN;

AEDES AEGYPTI; AMINO ACID SEQUENCE; ANOPHELES GAMBIAE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CULEX QUINQUEFASCIATUS; GENE IDENTIFICATION; GENOME ANALYSIS; GENOME SIZE; INNATE IMMUNITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; ANIMAL; CHEMISTRY; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENETICS; GENOME; HEMOLYMPH; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE;

AEDES AEGYPTI; ANOPHELES GAMBIAE; CULEX PIPIENS QUINQUEFASCIATUS; HEXAPODA; MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; CLUSTER ANALYSIS; CYSTEINE; DISULFIDES; GENE EXPRESSION REGULATION; GENOME, INSECT; HEMOLYMPH; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; SEQUENCE ANALYSIS, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 77957205331     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-531     Document Type: Article

References (49)

1. Waterhouse R, Kriventseva E, Meister S, Xi Z, Alvarez K, Bartholomay L, Barillas-Mury C, Bian G, Blandin S, Christensen B, et al. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316(5832):1738-1743. 10.1126/science.1139862, 2042107, 17588928.
2. Fraiture M, Baxter R, Steinert S, Chelliah Y, Frolet C, Quispe-Tintaya W, Hoffmann J, Blandin S, Levashina E. Two mosquito LRR proteins function as complement control factors in the TEP1-mediated killing of Plasmodium. Cell Host Microbe 2009, 5(3):273-284. 10.1016/j.chom.2009.01.005, 19286136.
3. Povelones M, Waterhouse R, Kafatos F, Christophides G. Leucine-rich repeat protein complex activates mosquito complement in defense against Plasmodium parasites. Science 2009, 324(5924):258-261. 10.1126/science.1171400, 2790318, 19264986.
4. Dimopoulos G, Christophides G, Meister S, Schultz J, White K, Barillas-Mury C, Kafatos F. Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc Natl Acad Sci USA 2002, 99(13):8814-8819. 10.1073/pnas.092274999, 124381, 12077297.
5. Osta M, Christophides G, Kafatos F. Effects of mosquito genes on Plasmodium development. Science 2004, 303(5666):2030-2032. 10.1126/science.1091789, 15044804.
6. Riehle M, Markianos K, Niaré O, Xu J, Li J, Touré A, Podiougou B, Oduol F, Diawara S, Diallo M, et al. Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 2006, 312(5773):577-579. 10.1126/science.1124153, 16645095.
7. Blandin S, Shiao S, Moita L, Janse C, Waters A, Kafatos F, Levashina E. Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 2004, 116(5):661-670. 10.1016/S0092-8674(04)00173-4, 15006349.
8. Levashina E, Moita L, Blandin S, Vriend G, Lagueux M, Kafatos F. Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 2001, 104(5):709-718. 10.1016/S0092-8674(01)00267-7, 11257225.
9. Moita L, Wang-Sattler R, Michel K, Zimmermann T, Blandin S, Levashina E, Kafatos F. In vivo identification of novel regulators and conserved pathways of phagocytosis in A. gambiae. Immunity 2005, 23(1):65-73. 10.1016/j.immuni.2005.05.006, 16039580.
10. Habtewold T, Povelones M, Blagborough A, Christophides G. Transmission blocking immunity in the malaria non-vector mosquito Anopheles quadriannulatus species A. PLoS Pathog 2008, 4(5):e1000070. 10.1371/journal.ppat.1000070, 2374904, 18497855.
11. Jaramillo-Gutierrez G, Rodrigues J, Ndikuyeze G, Povelones M, Molina-Cruz A, Barillas-Mury C. Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes. BMC Microbiol 2009, 9:154. 10.1186/1471-2180-9-154, 2782267, 19643026.
12. Riehle M, Xu J, Lazzaro B, Rottschaefer S, Coulibaly B, Sacko M, Niare O, Morlais I, Traore S, Vernick K. Anopheles gambiae APL1 is a family of variable LRR proteins required for Rel1-mediated protection from the malaria parasite, Plasmodium berghei. PLoS One 2008, 3(11):e3672. 10.1371/journal.pone.0003672, 2577063, 18989366.
13. Mitri C, Jacques J, Thiery I, Riehle M, Xu J, Bischoff E, Morlais I, Nsango S, Vernick K, Bourgouin C. Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog 2009, 5(9):e1000576. 10.1371/journal.ppat.1000576, 2734057, 19750215.
14. Little T, Cobbe N. The evolution of immune-related genes from disease carrying mosquitoes: diversity in a peptidoglycan-and a thioester-recognizing protein. Insect Mol Biol 2005, 14(6):599-605. 10.1111/j.1365-2583.2005.00588.x, 16313560.
15. Obbard D, Callister D, Jiggins F, Soares D, Yan G, Little T. The evolution of TEP1, an exceptionally polymorphic immunity gene in Anopheles gambiae. BMC Evol Biol 2008, 8:274. 10.1186/1471-2148-8-274, 2576239, 18840262.
16. Blandin S, Levashina E. Thioester-containing proteins and insect immunity. Mol Immunol 2004, 40(12):903-908. 10.1016/j.molimm.2003.10.010, 14698229.
17. Baxter R, Chang C, Chelliah Y, Blandin S, Levashina E, Deisenhofer J. Structural basis for conserved complement factor-like function in the antimalarial protein TEP1. Proc Natl Acad Sci USA 2007, 104(28):11615-11620. 10.1073/pnas.0704967104, 1905922, 17606907.
18. Bell J, Botos I, Hall P, Askins J, Shiloach J, Segal D, Davies D. The molecular structure of the Toll-like receptor 3 ligand-binding domain. Proc Natl Acad Sci USA 2005, 102(31):10976-10980. 10.1073/pnas.0505077102, 1182468, 16043704.
19. Choe J, Kelker M, Wilson I. Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 2005, 309(5734):581-585. 10.1126/science.1115253, 15961631.
20. Waterhouse R, Wyder S, Zdobnov E. The Aedes aegypti genome: a comparative perspective. Insect Mol Biol 2008, 17(1):1-8. 10.1111/j.1365-2583.2008.00772.x, 18237279.
21. Dong Y, Aguilar R, Xi Z, Warr E, Mongin E, Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog 2006, 2(6):e52. 10.1371/journal.ppat.0020052, 1475661,1475661, 16789837.
22. Aguilar R, Jedlicka A, Mintz M, Mahairaki V, Scott A, Dimopoulos G. Global gene expression analysis of Anopheles gambiae responses to microbial challenge. Insect Biochem Mol Biol 2005, 35(7):709-719. 10.1016/j.ibmb.2005.02.019, 15894188.
23. Kambris Z, Cook P, Phuc H, Sinkins S. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 2009, 326(5949):134-136. 10.1126/science.1177531, 2867033, 19797660.
24. Vlachou D, Schlegelmilch T, Christophides G, Kafatos F. Functional genomic analysis of midgut epithelial responses in Anopheles during Plasmodium invasion. Curr Biol 2005, 15(13):1185-1195. 10.1016/j.cub.2005.06.044, 16005290.
25. Marinotti O, Nguyen Q, Calvo E, James A, Ribeiro J. Microarray analysis of genes showing variable expression following a blood meal in Anopheles gambiae. Insect Mol Biol 2005, 14(4):365-373. 10.1111/j.1365-2583.2005.00567.x, 16033430.
26. Matsushima N, Tanaka T, Enkhbayar P, Mikami T, Taga M, Yamada K, Kuroki Y. Comparative sequence analysis of leucine-rich repeats (LRRs) within vertebrate toll-like receptors. BMC Genomics 2007, 8:124. 10.1186/1471-2164-8-124, 1899181, 17517123.
27. Bella J, Hindle K, McEwan P, Lovell S. The leucine-rich repeat structure. Cell Mol Life Sci 2008, 65(15):2307-2333. 10.1007/s00018-008-8019-0, 18408889.
28. Wen D, Wildes C, Silvian L, Walus L, Mi S, Lee D, Meier W, Pepinsky R. Disulfide structure of the leucine-rich repeat C-terminal cap and C-terminal stalk region of Nogo-66 receptor. Biochemistry 2005, 44(50):16491-16501. 10.1021/bi0517483, 16342940.
29. Nishitani C, Mitsuzawa H, Sano H, Shimizu T, Matsushima N, Kuroki Y. Toll-like receptor 4 region Glu24-Lys47 is a site for MD-2 binding: importance of CYS29 and CYS40. J Biol Chem 2006, 281(50):38322-38329. 10.1074/jbc.M606904200, 17056597.
30. Grigoryan G, Keating A. Structural specificity in coiled-coil interactions. Curr Opin Struct Biol 2008, 18(4):477-483. 10.1016/j.sbi.2008.04.008, 2567808, 18555680.
31. Bent A, Mackey D. Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu Rev Phytopathol 2007, 45:399-436. 10.1146/annurev.phyto.45.062806.094427, 17506648.
32. Ye Z, Ting J. NLR, the nucleotide-binding domain leucine-rich repeat containing gene family. Curr Opin Immunol 2008, 20(1):3-9.
33. Leulier F, Lemaitre B. Toll-like receptors--taking an evolutionary approach. Nat Rev Genet 2008, 9(3):165-178. 10.1038/nrg2303, 18227810.
34. Pancer Z, Amemiya C, Ehrhardt G, Ceitlin J, Gartland G, Cooper M. Somatic diversification of variable lymphocyte receptors in the agnathan sea lamprey. Nature 2004, 430(6996):174-180. 10.1038/nature02740, 15241406.
35. Herrin B, Alder M, Roux K, Sina C, Ehrhardt G, Boydston J, Turnbough CJ, Cooper M. Structure and specificity of lamprey monoclonal antibodies. Proc Natl Acad Sci USA 2008, 105(6):2040-2045. 10.1073/pnas.0711619105, 2542867, 18238899.
36. Alder M, Herrin B, Sadlonova A, Stockard C, Grizzle W, Gartland L, Gartland G, Boydston J, Turnbough CJ, Cooper M. Antibody responses of variable lymphocyte receptors in the lamprey. Nat Immunol 2008, 9(3):319-327. 10.1038/ni1562, 18246071.
37. Kobe B, Kajava A. The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 2001, 11(6):725-732. 10.1016/S0959-440X(01)00266-4, 11751054.
38. Sutton R, Fasshauer D, Jahn R, Brunger A. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 1998, 395(6700):347-353. 10.1038/26412, 9759724.
39. Zdobnov E, Apweiler R. InterProScan--an integration platform for the signature-recognition methods in InterPro. Bioinformatics 2001, 17(9):847-848. 10.1093/bioinformatics/17.9.847, 11590104.
40. Andrade M, Ponting C, Gibson T, Bork P. Homology-based method for identification of protein repeats using statistical significance estimates. J Mol Biol 2000, 298(3):521-537. 10.1006/jmbi.2000.3684, 10772867.
41. Lupas A, Van Dyke M, Stock J. Predicting coiled coils from protein sequences. Science 1991, 252(5010):1162-1164.
42. Delorenzi M, Speed T. An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 2002, 18(4):617-625. 10.1093/bioinformatics/18.4.617, 12016059.
43. Bendtsen J, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 2004, 340(4):783-795. 10.1016/j.jmb.2004.05.028, 15223320.
44. Edgar R. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32(5):1792-1797. 10.1093/nar/gkh340, 390337, 15034147.
45. Do C, Mahabhashyam M, Brudno M, Batzoglou S. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res 2005, 15(2):330-340. 10.1101/gr.2821705, 546535, 15687296.
46. Thompson J, Higgins D, Gibson T. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994, 22(22):4673-4680. 10.1093/nar/22.22.4673, 308517, 7984417.
47. Kriventseva E, Rahman N, Espinosa O, Zdobnov E. OrthoDB: the hierarchical catalog of eukaryotic orthologs. Nucleic Acids Res 2008, (36 Database):D271-275. 2238902, 17947323.
48. Crooks G, Hon G, Chandonia J, Brenner S. WebLogo: a sequence logo generator. Genome Res 2004, 14(6):1188-1190. 10.1101/gr.849004, 419797, 15173120.
49. Lawson D, Arensburger P, Atkinson P, Besansky N, Bruggner R, Butler R, Campbell K, Christophides G, Christley S, Dialynas E, et al. VectorBase: a data resource for invertebrate vector genomics. Nucleic Acids Res 2009, (37 Database):D583-587. 10.1093/nar/gkn857, 2686483, 19028744.