Molecular evolution of immune genes in the malaria mosquito Anopheles gambiae

PLoS ONE

Volumn 4, Issue 2, 2009, Pages

  Lehmann, Tovi ^a,b,c   Hume, Jen C C ^c   Licht, Monica ^a,b   Burns, Christopher S ^a,b   Wollenberg, Kurt ^c   Simard, Fred ^d   Ribeiro, Jose M C ^c  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b EMORY UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d Institut de Recherche Pour le Developpement   (Cameroon)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; DEFENSIN; GAMBICIN; GRAM NEGATIVE BACTERIA BINDING PROTEIN; INSECT PROTEIN; SERINE PROTEINASE; SERINE PROTEINASE 14D1; UNCLASSIFIED DRUG;

ANOPHELES; ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; ANOPHELES QUADRIANNULATUS; ARTICLE; CODON; CONTROLLED STUDY; GENETIC HETEROGENEITY; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; IMMUNE RESPONSE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; SPECIES DIFFERENCE; TAXONOMY;

ANOPHELES ARABIENSIS; ANOPHELES GAMBIAE; CULICIDAE;

EID: 84887212580     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0004549     Document Type: Article

References (73)

1. Hughes AL, Hughes MK (1995) Natural selection on the peptide-binding regions of major histocompatibility complex molecules. Immunogenetics 42: 233-243.
2. Paterson S (1998) Evidence for balancing selection at the major histocompatibility complex in a free-living ruminant. J Hered 89: 289-294.
3. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167-170.
4. Tiffin P, Moeller DA (2006) Molecular evolution of plant immune system genes. Trends Genet 22: 662-670.
5. Gilbert SC, Plebanski M, Gupta S, Morris J, Cox M, et al. (1998) Association of malaria parasite population structure, HLA, and immunological antagonism. Science 279: 1173-1177.
6. Stahl EA, Dwyer G, Mauricio R, Kreitman M, Bergelson J (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667-671.
7. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc Lond B Biol Sci 205: 489-511.
8. Kreitman M (2000) Methods to detect selection in populations with applications to the human. Annu Rev Genomics Hum Genet 1: 539-559.
9. Sawyer SL, Wu LI, Emerman M, Malik HS (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102: 2832-2837.
10. Endo T, Ikeo K, Gojobori T (1996) Large-scale search for genes on which positive selection may operate. Mol Biol Evol 13: 685-690.
11. Lehmann T, Blackston CR, Parmley SF, Remington JS, Dubey JP (2000) Strain typing of Toxoplasma gondii: comparison of antigen-coding and housekeeping genes. J Parasitol 86: 960-971.
12. Clark AG, Wang L (1997) Molecular population genetics of Drosophila immune system genes. Genetics 147: 713-724.
13. Jiggins FM, Hurst GD (2003) The evolution of parasite recognition genes in the innate immune system: purifying selection on Drosophila melanogaster peptidoglycan recognition proteins. J Mol Evol 57: 598-605.
14. Lazzaro BP, Clark AG (2003) Molecular population genetics of inducible antibacterial peptide genes in Drosophila melanogaster. Mol Biol Evol 20: 914-923.
15. Simard F, Licht M, Besansky NJ, Lehmann T (2007) Polymorphism at the defensin gene in the Anopheles gambiae complex: testing different selection hypotheses. Infect Genet Evol 7: 285-292.
16. Little TJ, Cobbe N (2005) The evolution of immune-related genes from disease carrying mosquitoes: diversity in a peptidoglycan- and a thioester-recognizing protein. Insect Mol Biol 14: 599-605.
17. Obbard DJ, Linton YM, Jiggins FM, Yan G, Little TJ (2007) Population genetics of plasmodium resistance genes in Anopheles gambiae: no evidence for strong selection. Molecular Ecology 16: 3497-3510.
18. Slotman MA, Parmakelis A, Marshall JC, Awono-Ambene PH, Antonio-Nkondjo C, et al. (2007) Patterns of selection in anti-malarial immune genes in malaria vectors: evidence for adaptive evolution in LRIM1 in Anopheles arabiensis. PLoS ONE 2: e793.
19. Grenfell BT, Pybus OG, Gog JR, Wood JL, Daly JM, et al. (2004) Unifying the epidemiological and evolutionary dynamics of pathogens. Science 303: 327-332.
20. Fritz RS, Simms EL (1992) Plant resistance to herbivores and pathogens. Chicago: University of Chicago Press.
21. May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B Biol Sci 219: 281-313.
22. Lambrechts L, Fellous S, Koella JC (2006) Coevolutionary interactions between host and parasite genotypes. Trends Parasitol 22: 12-16.
23. Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301: 472-475.
24. Hoffmann JA, Kafatos FC, Janeway CA, Ezekowitz RA (1999) Phylogenetic perspectives in innate immunity. Science 284: 1313-1318.
25. Medzhitov R, Janeway CA Jr (2002) Decoding the patterns of self and nonself by the innate immune system. Science 296: 298-300.
26. Dimopoulos G, Casavant TL, Chang S, Scheetz T, Roberts C, et al. (2000) Anopheles gambiae pilot gene discovery project: identification of mosquito innate immunity genes from expressed sequence tags generated from immune-competent cell lines. Proc Natl Acad Sci U S A 97: 6619-6624.
27. Riehle MM, Markianos K, Niare O, Xu J, Li J, et al. (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312: 577-579.
28. Blandin S, Levashina EA (2004) Thioester-containing proteins and insect immunity. Mol Immunol 40: 903-908.
29. Barillas-Mury C, Wizel B, Han YS (2000) Mosquito immune responses and malaria transmission: lessons from insect model systems and implications for vertebrate innate immunity and vaccine development. Insect Biochem Mol Biol 30: 429-442.
30. Lehmann T, Licht M, Elissa N, Maega BT, Chimumbwa JM, et al. (2003) Population Structure of Anopheles gambiae in Africa. J Hered 94: 133-147.
31. Beier JC, Perkins PV, Onyango FK, Gargan TP, Oster CN, et al. (1990) Characterization of malaria transmission by Anopheles (Diptera: Culicidae) in western Kenya in preparation for malaria vaccine trials. J Med Entomol 27: 570-577.
32. Mbogo CN, Snow RW, Kabiru EW, Ouma JH, Githure JI, et al. (1993) Low-level Plasmodium falciparum transmission and the incidence of severe malaria infections on the Kenyan coast. Am J Trop Med Hyg 49: 245-253.
33. Lenhart A, Eigege A, Kal A, Pam D, Miri ES, et al. (2007) Contributions of different mosquito species to the transmission of lymphatic filariasis in central Nigeria: Implications for monitoring infection by PCR in mosquito pools. Filaria J 6: 14.
34. Mukoko DA, Pedersen EM, Masese NN, Estambale BB, Ouma JH (2004) Bancroftian filariasis in 12 villages in Kwale district, Coast province, Kenya - variation in clinical and parasitological patterns. Ann Trop Med Parasitol 98: 801-815.
35. Collins FH, et al. (1988) Comparison of dna-probe and isoenzyme methods for differentiating Anopheles gambiae and Anopheles arabiensis (Diptera:Culicidae). J Med Entomol 25: 116-120.
36. Scott JA, Brogdon WG, Collins FH (1993) Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction. Am J Trop Med Hyg 49: 520-529.
37. Favia G, della Torre A, Bagayoko M, Lanfrancotti A, Sagnon N, et al. (1997) Molecular identification of sympatric chromosomal forms of Anopheles gambiae and further evidence of their reproductive isolation. Insect Mol Biol 6: 377-383.
38. Rozas J, Rozas R (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
39. Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W (1995) The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140: 783-796.
40. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
41. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163.
42. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116: 153-159.
43. Wright S (1978) Evolution and the genetics of populations Variability Within and Among Natural Populations. Chicago: University of Chicago Press.
44. Hudson RR, Slatkin M, Maddison WP (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132: 583-589.
45. SAS (1990) SAS language: references, Version 6. version 6 ed: Cary, NC: SAS Institute.
46. Besansky NJ, Krzywinski J, Lehmann T, Simard F, Kern M, et al. (2003) Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: Evidence from multilocus DNA sequence variation. Proc Natl Acad Sci U S A 100: 10818-10823.
47. Besansky NJ, Lehmann T, Fahey GT, Fontenille D, Braack LE, et al. (1997) Patterns of mitochondrial variation within and between African malaria vectors, Anopheles gambiae and An. arabiensis, suggest extensive gene flow. Genetics 147: 1817-1828.
48. Donnelly MJ, Pinto J, Girod R, Besansky NJ, Lehmann T (2004) Revisiting the role of introgression vs shared ancestral polymorphisms as key processes shaping genetic diversity in the recently separated sibling species of the Anopheles gambiae complex. Heredity 92: 61-68.
49. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
50. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
51. Felsenstein J (1989) PHYLIP - Phylogeny Inference Package (Version 3.2). Cladistics. pp 164-166.
52. McDonald GH (1994) Detecting natural selection by comparing geographic variation in protein and DNA polymorphisms. In: Golding B, ed. Non-Neutral Evolution. New York: Chapman & Hall. pp 88-100.
53. Krzywinski J, Grushko OG, Besansky NJ (2006) Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution. Mol Phylogenet Evol 39: 417-423.
54. Collins FH, et al. (1986) Genetic selection of a Plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234: 607-610.
55. Huff CG (1951) Observations on the pre-erythrocytic stages of Plasmodium relictum, Plasmodium cathemerium, and Plasmodium gallinaceum in various birds. J Infect Dis 88: 17-26.
56. Huff CG (1965) Susceptibility of Mosquitoes to Avian Malaria. Exp Parasitol 16: 107-132.
57. Lazzaro BP, Sceurman BK, Clark AG (2004) Genetic basis of natural variation in D. melanogaster antibacterial immunity. Science 303: 1873-1876.
58. Schlenke TA, Begun DJ (2003) Natural selection drives Drosophila immune system evolution. Genetics 164: 1471-1480.
59. Jiggins FM, Kim KW (2005) The evolution of antifungal peptides in Drosophila. Genetics 171: 1847-1859.
60. Levine MT, Begun DJ (2007) Comparative population genetics of the immunity gene, Relish: is adaptive evolution idiosyncratic? PLoS ONE 2: e442.
61. Krzywinski J, Besansky NJ (2003) Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol 48: 111-139.
62. Lambrechts L, Halbert J, Durand P, Gouagna LC, Koella JC (2005) Host genotype by parasite genotype interactions underlying the resistance of anopheline mosquitoes to Plasmodium falciparum. Malar J 4: 3.
63. Chun J, McMaster J, Han Y, Schwartz A, Paskewitz SM (2000) Two-dimensional gel analysis of haemolymph proteins from Plasmodium- melanizing and -non-melanizing strains of Anopheles gambiae. Insect Mol Biol 9: 39-45.
64. Zheng L, Cornel AJ, Wang R, Erfle H, Voss H, et al. (1997) Quantitative trait loci for refractoriness of Anopheles gambiae to Plasmodium cynomolgi B. Science 276: 425-428.
65. Gorman MJ, Paskewitz SM (2001) Serine proteases as mediators of mosquito immune responses. Insect Biochem Mol Biol 31: 257-262.
66. 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.
67. Richman AM, Bulet P, Hetru C, Barillas-Mury C, Hoffmann JA, et al. (1996) Inducible immune factors of the vector mosquito Anopheles gambiae: biochemical purification of a defensin antibacterial peptide and molecular cloning of preprodefensin cDNA. Insect Mol Biol 5: 203-210.
68. 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.
69. Shahabuddin M, Fields I, Bulet P, Hoffmann JA, Miller LH (1998) Plasmodium gallinaceum: differential killing of some mosquito stages of the parasite by insect defensin. Exp Parasitol 89: 103-112.
70. Dia I, Diop T, Rakotoarivony I, Kengne P, Fonetenille D (2003) Bionomics of Anopehles gambiae Giles, An. arabiensis Patton, An. funestus Giles, and An. nili (Theobald) (Diptera: Culicidae) and transmission of Plasmodium falciparum in a Sudano-Guinean zone (Ngari, Senegal). J Med Entomol 40: 279-283.
71. White GB (1974) Anopheles gambiae complex and disease transmission in Africa. Trans. Roy Soc Trop Med Hyg 68: 278-298.
72. Githeko AK, Service MW, Mbogo CM, Atieli FK, Juma FO (1994) Origin of blood meals in indoor and outdoor resting malaria vectors in western Kenya. Acta Trop 58: 307-16.
73. Killeen GF, McKenzie FE, Foy BD, Schieffelin C, Billingsley PF, Beier JC (2000) A simplified model for predicting malaria entomologic inoculation rates based on entomologic and parasitologic parameters relevant to control. Am J Trop Med Hyg 62: 535-44.