Analysis of expression in the Anopheles gambiae developing testes reveals rapidly evolving lineage-specific genes in mosquitoes

BMC Genomics

Volumn 10, Issue , 2009, Pages

  Krzywinska, Elzbieta ^a   Krzywinski, Jaroslaw ^a,b  

^a UNIVERSITY OF TEXAS AT ARLINGTON   (United States)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DAZ INTERACTING PROTEIN 1 LIKE PROTEIN; INSECT PROTEIN; PROTEIN AMS; PROTEIN MTS; ROPPORIN 1 LIKE PROTEIN; UNCLASSIFIED DRUG;

ANOPHELES GAMBIAE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE ISOLATION; GENE SEQUENCE; IN SITU HYBRIDIZATION; INSECT GENOME; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; SPECIES COMPARISON; SPERMATID; SPERMATOGENESIS; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; TESTIS DEVELOPMENT; AMINO ACID SEQUENCE; ANIMAL; COMPARATIVE GENOMIC HYBRIDIZATION; DNA SEQUENCE; GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; TESTIS;

ANOPHELES GAMBIAE;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, COMPLEMENTARY; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; MALE; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPERMATOGENESIS; TESTIS;

EID: 67651230764     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-10-300     Document Type: Article

References (64)

1. Hill CA Kafatos FC Stansfield SK Collins FH Arthropod-borne diseases: vector control in the genomics era Nat Rev Microbiol 2005 3 3 262 268 10.1038/nrmicro1101 15703759
2. Breman JG Egan A Keusch GT The intolerable burden of malaria: A new look at the numbers Am J Trop Med Hyg 2001, 64(1-2 Suppl):iV-vii. 11425185
3. Mackenzie JS Gubler DJ Petersen LR Emerging flaviviruses: The spread and resurgence of Japanese encephalitis, West Nile and dengue viruses Nat Med 2004, 10(12 Suppl):S98-109. 10.1038/nm1144 15577938
4. Holt RA Subramanian GM Halpern A Sutton GG Charlab R Nusskern DR Wincker P Clark AG Ribeiro JM Wides R et al The genome sequence of the malaria mosquito Anopheles gambiae Science 2002, 298(5591):129-149. 10.1126/ science.1076181 12364791
5. Nene V Wortman JR Lawson D Haas B Kodira C Tu ZJ Loftus B Xi Z Megy K Grabherr M et al Genome sequence of Aedes aegypti, a major arbovirus vector Science 2007, 316(5832):1718-1723. 10.1126/science.1138878 17510324
6. Catteruccia F Malaria vector control in the third millennium: Progress and perspectives of molecular approaches Pest Manag Sci 2007, 63(7):634-640. 10.1002/ps.1324 17373671
7. Haerty W Jagadeeshan S Kulathinal RJ Wong A Ravi Ram K Sirot LK Levesque L Artieri CG Wolfner MF Civetta A et al Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila Genetics 2007, 177(3):1321-1335. 2147986 18039869 10.1534/genetics.107.078865
8. Clark AG Eisen MB Smith DR Bergman CM Oliver B Markow TA Kaufman TC Kellis M Gelbart W Iyer VN et al Evolution of genes and genomes on the Drosophila phylogeny Nature 2007, 450(7167):203-218. 10.1038/nature06341 17994087
9. Dorus S Freeman ZN Parker ER Heath BD Karr TL Recent origins of sperm genes in Drosophila Mol Biol Evol 2008, 25(10):2157-2166. 10.1093/molbev/ msn162 18653731
10. Sinkins SP Gould F Gene drive systems for insect disease vectors Nat Rev Genet 2006, 7(6):427-435. 10.1038/nrg1870 16682981
11. Windbichler N Papathanos PA Crisanti A Targeting the X chromosome during spermatogenesis induces Y chromosome transmission ratio distortion and early dominant embryo lethality in Anopheles gambiae PLoS Genet 2008, 4(12):e1000291. 2585807 19057670 10.1371/journal.pgen.1000291
12. Calvo E Walter M Adelman ZN Jimenez A Onal S Marinotti O James AA Nanos (nos) genes of the vector mosquitoes, Anopheles gambiae, Anopheles stephensi and Aedes aegypti Insect Biochem Mol Biol 2005, 35(7):789-798. 10.1016/j.ibmb.2005.02.007 15894194
13. Juhn J James AA oskar gene expression in the vector mosquitoes, Anopheles gambiae and Aedes aegypti Insect Mol Biol 2006, 15(3):363-372. 10.1111/j.1365-2583.2006.00655.x 16756555
14. Adelman ZN Jasinskiene N Onal S Juhn J Ashikyan A Salampessy M MacCauley T James AA nanos gene control DNA mediates developmentally regulated transposition in the yellow fever mosquito Aedes aegypti Proc Natl Acad Sci USA 2007, 104(24):9970-9975. 1891237 17548819 10.1073/pnas.0701515104
15. Windbichler N Papathanos PA Catteruccia F Ranson H Burt A Crisanti A Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos Nucleic Acids Res 2007, 35:5922-5933. 2034484 17726053 10.1093/nar/gkm632
16. Handler AM Allen ML Skoda SR Development and utilization of transgenic New World screwworm, Cochliomyia hominivorax Med Vet Entomol 2009, 23(Suppl 1):98-105. 10.1111/j.1365-2915.2008.00773.x 19335836
17. Hahn MW Lanzaro GC Female-biased gene expression in the malaria mosquito Anopheles gambiae Curr Biol 2005, 15(6):R192-193. 10.1016/ j.cub.2005.03.005 15797007
18. Koutsos AC Blass C Meister S Schmidt S Maccallum RM Soares MB Collins FH Benes V Zdobnov E Kafatos FC et al Life cycle transcriptome of the malaria mosquito Anopheles gambiae and comparison with the fruitfly Drosophila melanogaster Proc Natl Acad Sci USA 2007, 104(27):11304-11309. 2040894 17563388 10.1073/pnas.0703988104
19. Marinotti O Nguyen QK Calvo E James AA Ribeiro JM 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
20. Dottorini T Nicolaides L Ranson H Rogers DW Crisanti A Catteruccia F A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior Proc Natl Acad Sci USA 2007, 104(41):16215-16220. 2042187 17901209 10.1073/ pnas.0703904104
21. Kemphues KJ Raff EC Kaufman TC Genetic analysis of B2t, the structural gene for a testis-specific beta-tubulin subunit in Drosophila melanogaster Genetics 1983, 105(2):345-356. 1202161 6414882
22. Smith RC Walter MF Hice RH O'Brochta DA Atkinson PW Testis-specific expression of the beta2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker Insect Mol Biol 2007, 16(1):61-71. 10.1111/j.1365-2583.2006.00701.x 17257209
23. Catteruccia F Benton JP Crisanti A An Anopheles transgenic sexing strain for vector control Nat Biotechnol 2005, 23(11):1414-1417. 10.1038/ nbt1152 16244659
24. Miller D Ostermeier GC Towards a better understanding of RNA carriage by ejaculate spermatozoa Hum Reprod Update 2006, 12(6):757-767. 10.1093/ humupd/dml037 16882702
25. Clements AN The Biology of Mosquitoes Development, Nutrition and Reproduction London: Chapman & Hall 1992. 1
26. Cadeddu MG Laudani U Testis maturation in Anopheles atroparvus van Thiel Boll Zool 1974, 41:39-42.
27. Mahmood F Reisen WK Anopheles culicifacies: Effects of age on the male reproductive system and mating ability of virgin adult mosquitoes Med Vet Entomol 1994, 8(1):31-37. 10.1111/j.1365-2915.1994.tb00380.x 8161841
28. Huho BJ Ng'habi KR Killeen GF Nkwengulila G Knols BG Ferguson HM A reliable morphological method to assess the age of male Anopheles gambiae Malar J 2006, 5:62. 1570359 16872516 10.1186/1475-2875-5-62
29. MahmooC F Reisen WK Anopheles stephensi (Diptera: Culicidae): changes in male mating competence and reproductive system morphology associated with aging and mating J Med Entomol 1982, 19(5):573-588. 7143380
30. Ponlawat A Harrington LC Age and body size influence male sperm capacity of the dengue vector Aedes aegypti (Diptera: Culicidae) J Med Entomol 2007, 44(3):422-426. 10.1603/0022-2585(2007)44[422:AABSIM]2.0.CO;2 17547226
31. Barreau C Benson E Gudmannsdottir E Newton F White-Cooper H Post-meiotic transcription in Drosophila testes Development 2008, 135(11):1897-1902. 10.1242/dev.021949 18434411
32. Sieglaff DH Dunn WA Xie XS Megy K Marinotti O James AA Comparative genomics allows the discovery of cis-regulatory elements in mosquitoes Proc Natl Acad Sci USA 2009, 106(9):3053-3058. 2640218 19211788 10.1073/ pnas.0813264106
33. Meiklejohn CD Parsch J Ranz JM Hartl DL Rapid evolution of male-biased gene expression in Drosophila Proc Natl Acad Sci USA 2003, 100(17):9894-9899. 188344 12907700 10.1073/pnas.1630690100
34. Ranz JM Castillo-Davis CI Meiklejohn CD Hartl DL Sex-dependent gene expression and evolution of the Drosophila transcriptome Science 2003, 300(5626):1742-1745. 10.1126/science.1085881 12805547
35. Carr DW Fujita A Stentz CL Liberty GA Olson GE Narumiya S Identification of sperm-specific proteins that interact with A-kinase anchoring proteins in a manner similar to the type II regulatory subunit of PKA J Biol Chem 2001, 276(20):17332-17338. 10.1074/jbc.M011252200 11278869
36. Wong W Scott JD AKAP signalling complexes: Focal points in space and time Nat Rev Mol Cell Biol 2004, 5(12):959-970. 10.1038/nrm1527 15573134
37. Dell'Acqua ML Scott JD Protein kinase A anchoring J Biol Chem 1997, 272(20):12881-12884. 10.1074/jbc.272.20.12881 9190362
38. Carr DW Newell AE The role of A-kinase anchoring proteins (AKaps) in regulating sperm function Soc Reprod Fertil Suppl 2007, 63:135-141. 17566268
39. Yang C Yang P The flagellar motility of Chlamydomonas pf25 mutant lacking an AKAP-binding protein is overtly sensitive to medium conditions Mol Biol Cell 2006, 17(1):227-238. 1345661 16267272 10.1091/ mbc.E05-07-0630
40. Ward S Hogan E Nelson GA The initiation of spermiogenesis in the nematode Caenorhabditis elegans Dev Biol 1983, 98(1):70-79. 10.1016/ 0012-1606(83)90336-6 6345236
41. Inglis PN Ou G Leroux MR Scholey JM The sensory cilia of Caenorhabditis elegans The C. elegans Research Community, WormBook WormBook 2007 http://www.wormbook.org
42. Moore FL Jaruzelska J Dorfman DM Reijo-Pera RA Identification of a novel gene, DZIP (DAZ-interacting protein), that encodes a protein that interacts with DAZ (deleted in azoospermia) and is expressed in embryonic stem cells and germ cells Genomics 2004, 83(5):834-843. 10.1016/j.ygeno.2003.11.005 15081113
43. Berg JM Godwin HA Lessons from zinc-binding peptides Annu Rev Biophys Biomol Struct 1997, 26:357-371. 10.1146/annurev.biophys.26.1.357 9241423
44. Iuchi S Three classes of C2H2 zinc finger proteins Cell Mol Life Sci 2001, 58(4);625-635. 10.1007/PL00000885 11361095
45. Omichinski JG Pedone PV Felsenfeld G Gronenborn AM Clore GM The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode Nat Struct Biol 1997, 4(2):122-132. 10.1038/nsb0297-122 9033593
46. Dathan N Zaccaro L Esposito S Isernia C Omichinski JG Riccio A Pedone C Di Blasio B Fattorusso R Pedone PV The Arabidopsis SUPERMAN protein is able to specifically bind DNA through its single Cys2-His2 zinc finger motif Nucleic Acids Res 2002, 30(22):4945-4951. 137161 12433998 10.1093/ nar/gkf613
47. McGlincy NJ Smith CW Alternative splicing resulting in nonsense-mediated mRNA decay: What is the meaning of nonsense? Trends Biochem Sci 2008, 33(8):385-393. 10.1016/j.tibs.2008.06.001 18621535
48. Burkhard P Stetefeld J Strelkov SV Coiled coils: A highly versatile protein folding motif Trends Cell Biol 2001, 11(2):82-88. 10.1016/ S0962-8924(00)01898-5 11166216
49. Brendel V Karlin S Too many leucine zippers? Nature 1989, 341(6243):574-575. 10.1038/341574a0 2797188
50. Tanaka H Baba T Gene expression in spermiogenesis Cell Mol Life Sci 2005, 62(3):344-354. 10.1007/s00018-004-4394-y 15723169
51. Braun RE Packaging paternal chromosomes with protamine Nat Genet 2001, 28(1):10-12. 10.1038/88194 11326265
52. Fuller MT Spermatogenesis The development of Drosophila melanogaster Cold Spring Harbor, N.Y.: Cold Spring Harbor Laboratory Press; Bate M, Martinez-Arias A 1993, 71-147.
53. Rathke C Baarends WM Jayaramaiah-Raja S Bartkuhn M Renkawitz R Renkawitz-Pohl R Transition from a nucleosome-based to a protamine-based chromatin configuration during spermiogenesis in Drosophila J Cell Sci 2007, 120(Pt 9):1689-1700. 10.1242/jcs.004663 17452629
54. Hempel LU Rathke C Raja SJ Renkawitz-Pohl R In Drosophila, don juan and don juan like encode proteins of the spermatid nucleus and the flagellum and both are regulated at the transcriptional level by the TAF II80 cannonball while translational repression is achieved by distinct elements Dev Dyn 2006, 235(4):1053-1064. 10.1002/dvdy.20698 16477641
55. Krzywinski J Grushko OG Besansky NJ 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 2006, 39(2):417-423. 10.1016/ j.ympev.2006.01.006 16473530
56. Benedict MQ Care and maintenance of Anopheline mosquito colonies The Molecular Biology of Insect Disease Vectors London: Chapman & Hall Crampton JM, Beard CB, Louis C 1997, 3-12.
57. Munstermann L Care and maintenance of Aedes mosquito colonies The Molecular Biology of Insect Disease Vectors London: Chapman & Hall Crampton JM, Beard CB, Louis C 1997, 13-20.
58. Mori A Romero-Severson J Severson DW Genetic basis for reproductive diapause is correlated with life history traits within the Culex pipiens complex Insect Mol Biol 2007, 16(5):515-524. 17635616
59. Krzywinski J Nusskern DR Kern MK Besansky NJ Isolation and characterization of Y chromosome sequences from the African malaria mosquito Anopheles gambiae Genetics 2004, 166(3):1291-1302. 1470776 15082548 10.1534/genetics.166.3.1291
60. Bertucci LA Noor MA Single fly total RNA preparations for RT-PCR Dros Inf Serv 2001, 84:166-168.
61. Altschul SF Gish W Miller W Myers EW Lipman DJ Basic local alignment search tool J Mol Biol 1990, 215(3):403-410. 2231712
62. van Helden J Andre B Collado-Vides J Extracting regulatory sites from the upstream region of yeast genes by computational analysis of oligonucleotide frequencies J Mol Biol 1998, 281(5):827-842. 10.1006/ jmbi.1998.1947 9719638
63. Thompson JD Gibson TJ Plewniak F Jeanmougin F Higgins DG The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res 1997, 25(24):4876-4882. 147148 9396791 10.1093/nar/25.24.4876
64. Walter MF Biessmann H Expression of the telomeric retrotransposon HeT-A in Drosophila melanogaster is correlated with cell proliferation Dev Genes Evol 2004, 214(5):211-219. 10.1007/s00427-004-0400-x 15069641