An ancient immunity gene duplication in Daphnia magna: RNA expression and sequence analysis of two nitric oxide synthase genes

Developmental and Comparative Immunology

Volumn 33, Issue 9, 2009, Pages 1000-1010

  Labbé, Pierrick ^a   McTaggart, Seanna J ^a   Little, Tom J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Innate immunity; Invertebrate immunity; Nitric oxide synthase; Parasite; Pasteuria ramosa; Pathogen

Indexed keywords

ARGININE; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) NITROARGININE METHYL ESTER; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; DAPHNIA; GENE DUPLICATION; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HOST RESISTANCE; IMMUNE RESPONSE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPECIES DIFFERENTIATION;

ARTHROPODA; BACTERIA (MICROORGANISMS); CRUSTACEA; DAPHNIA; DAPHNIA MAGNA; HEXAPODA; INVERTEBRATA; PASTEURIA; PASTEURIA RAMOSA;

EID: 67349249742     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.04.006     Document Type: Article

References (56)

1. Tripathi P., Tripathi P., Kashyap L., and Singh V. The role of nitric oxide in inflammatory reactions. FEMS Immunology & Medical Microbiology 51 3 (2007) 443-452
2. Rivero A. Nitric oxide: an antiparasitic molecule of invertebrates. Trends in Parasitology 22 5 (2006) 219-225
3. Bogdan C., Röllinghoff M., and Diefenbach A. The role of nitric oxide in innate immunity. Immunological Reviews 173 1 (2000) 17-26
4. Bogdan C., Röllinghoff M., and Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Current Opinion in Immunology 12 1 (2000) 64-76
5. Krishnan N., Hyrsl P., and Simek V. Nitric oxide production by hemocytes of larva and pharate prepupa of Galleria mellonella in response to bacterial lipopolysaccharide: cytoprotective or cytotoxic?. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 142 1/2 (2006) 103-110
6. Kurtz J. Memory in the innate and adaptive immune systems. Microbes and Infection 6 15 (2004) 1410-1417
7. Dimopoulos G., Seeley D., Wolf A., and Kafatos F.C. Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO Journal 17 21 (1998) 6115-6123
8. Imamura M., Yang J., and Yamakawa M. cDNA cloning, characterization and gene expression of nitric oxide synthase from the silkworm, Bombyx mori. Insect Molecular Biology 11 3 (2002) 257-265
9. Kim H.W., Batista L.A., Hoppes J.L., Lee K.J., and Mykles D.L. A crustacean nitric oxide synthase expressed in nerve ganglia, Y-organ, gill and gonad of the tropical land crab, Gecarcinus lateralis. Journal of Experimental Biology 207 16 (2004) 2845-2857
10. Luckhart S., and Rosenberg R. Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene 232 1 (1999) 25-34
11. Luckhart S., Vodovotz Y., Cui L.W., and Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proceedings of the National Academy of Sciences of the United States of America 95 10 (1998) 5700-5705
12. McTaggart S.J., Conlon C., Colbourne J.K., Blaxter M.L., and Little T.J. The components of the Daphnia pulex immune system as revealed by complete genome sequencing. BMC Genomics 10 (2009) 175
13. Hahn U.K., Bender R.C., and Bayne C.J. Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata. Journal of Parasitology 87 4 (2001) 778-785
14. Nappi A.J., Vass E., Frey F., and Carton Y. Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4 4 (2000) 423-430
15. Ascenzi P., and Gradoni L. Nitric oxide limits parasite development in vectors and in invertebrate intermediate hosts. IUBMB Life 53 2 (2002) 121-123
16. Foley E., and O'Farrell P.H. Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Development 17 1 (2003) 115-125
17. Herrera-Ortíz A., Lanz-Mendoza H., Martínez-Barnetche J., Hernández-Martínez S., Villarreal-Treviño C., Aguilar-Marcelino L., et al. Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro. Insect Biochemistry and Molecular Biology 34 9 (2004) 893-901
18. Lim J., Gowda D.C., Krishnegowda G., and Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infection and Immunity 73 5 (2005) 2778-2789
19. Whitten M., Sun F., Tew I., Schaub G., Soukou C., Nappi A., et al. Differential modulation of Rhodnius prolixus nitric oxide activities following challenge with Trypanosoma rangeli. T. cruzi and bacterial cell wall components. Insect Biochemistry and Molecular Biology 37 5 (2007) 440-452
20. Yeh F.-C., Wu S.-H., Lai C.-Y., and Lee C.-Y. Demonstration of nitric oxide synthase activity in crustacean hemocytes and anti-microbial activity of hemocyte-derived nitric oxide. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 144 1 (2006) 11-17
21. Ebert D. Host-parasite coevolution: insights from the Daphnia-parasite model system. Current Opinion in Microbiology 11 3 (2008) 290-301
22. Ebert D. Ecology, epidemiology, and evolution of parasitism in Daphnia (2005), National Library of Medicine (US), National Center for Biotechnology Information, Bethesda, MD
23. Duncan A.B., and Little T.J. Parasite-driven genetic change in a natural population of Daphnia. Evolution 61 4 (2007) 796-803
24. Little T.J., and Ebert D. Associations between parasitism and host genotype in natural populations of Daphnia (Crustacea: Cladocera). Journal of Animal Ecology 68 1 (1999) 134-149
25. Little T.J., Watt K., and Ebert D. Parasite-host specificity: experimental studies on the basis of parasite adaptation. Evolution 60 1 (2006) 31-38
26. Labbé P., and Little T.J. ProPhenolOxidase in Daphnia magna: cDNA sequencing and expression in relation to resistance to pathogens. Developmental & Comparative Immunology 33 (2009) 674-680
27. Carius H.J., Little T.J., and Ebert D. Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55 6 (2001) 1136-1145
28. Little T.J., and Ebert D. The cause of parasitic infection in natural populations of Daphnia (Crustacea: Cladocera): the role of host genetics. Proceedings of the Royal Society of London Series B-Biological Sciences 267 1457 (2000) 2037-2042
29. Mitchell S.E., and Read A.F. Poor maternal environment enhances offspring disease resistance in an invertebrate. Proceedings of the Royal Society B-Biological Sciences 272 1581 (2005) 2601-2607
30. Mitchell S.E., Rogers E.S., Little T.J., and Read A.F. Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59 1 (2005) 70-80
31. Vale P.F., Stjernman M., and Little T.J. Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions. Journal of Evolutionary Biology 21 5 (2008) 1418-1427
32. Luckhart S., Li K.Y., Dunton R., Lewis E.E., Crampton A.L., Ryan J.R., et al. Anopheles gambiae immune gene variants associated with natural Plasmodium infection. Molecular and Biochemical Parasitology 128 1 (2003) 83-86
33. Drummond A, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Thierer T, Wilson A. Geneious v4.5.4, http://www.geneious.com 2008.
34. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Computer Applications in BioSciences 13 (1997) 555-556
35. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Research 16 (1988) 10881-10890
36. Heckmann L.-H., Connon R., Hutchinson T., Maund S., Sibly R., and Callaghan A. Expression of target and reference genes in Daphnia magna exposed to ibuprofen. BMC Genomics 7 1 (2006) 175
37. Crawley M.J. The R book (2007), John Wiley & Sons Ltd., Chichester, UK
38. Klüttgen B., Dülmer U., Engels M., and Ratte H.T. ADaM, an artificial freshwater for the culture of zooplankton. Water Research 28 3 (1994) 743-746
39. Gillespie J.P., Kanost M.R., and Trenczek T. Biological mediators of insect immunity. Annual Review of Entomology 42 (1997) 611-643
40. Rolff J., and Siva-Jothy M.T. Invertebrate ecological immunology. Science 301 5632 (2003) 472-475
41. Cerenius L., Lee B.L., and Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends in Immunology 29 6 (2008) 263-271
42. Ferrandon D., Imler J.-L., Hetru C., and Hoffmann J.A. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nature Review Immunology 7 11 (2007) 862-874
43. Cox R.L., Mariano T., Heck D.E., Laskin J.D., and Stegeman J.J. Nitric oxide synthase sequences in the marine fish Stenotomus chrysops and the sea urchin Arbacia punctulata, and phylogenetic analysis of nitric oxide synthase calmodulin-binding domains. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 130 4 (2001) 479-491
44. Haag C.R., McTaggart S.J., and Didier A. Little TJ, Charlesworth D. Nucleotide polymorphism and within-gene recombination in Daphnia magna and Daphnia pulex, two cyclical parthenogens. Genetics 182 (2009) 313-323
45. Colbourne J.K., and Hebert P.D.N. The systematics of North American Daphnia (Crustacea: Anomopoda): a molecular phylogenetic approach. Philosophical Transactions of the Royal Society B: Biological Sciences 351 1337 (1996) 349-360
46. Schlenke T.A., and Begun D.J. Natural selection drives Drosophila immune system evolution. Genetics 164 4 (2003) 1471-1480
47. Little T.J., Colbourne J.K., and Crease T.J. Molecular evolution of Daphnia immunity genes: polymorphism in a gram-negative binding protein gene and an alpha-2-macroglobulin gene. Journal of Molecular Evolution 59 4 (2004) 498-506
48. Hurst L.D., and Smith N.G.C. Do essential genes evolve slowly?. Current Biology 9 14 (1999) 747-750
49. Obbard D.J., Jiggins F.M., Halligan D.L., and Little T.J. Natural selection drives extremely rapid evolution in antiviral RNAi genes. Current Biology 16 6 (2006) 580-585
50. Ohno S. Evolution by gene duplication (1970), Springer-Verlag, Berlin
51. Lynch M., and Conery J.S. The evolutionary fate and consequences of duplicate genes. Science 290 5494 (2000) 1151-1155
52. Lynch M., and Katju V. The altered evolutionary trajectories of gene duplicates. Trends in Genetics 20 11 (2004) 544-549
53. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.-l., and Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 4 (1999) 1531-1545
54. Hughes M.K., and Hughes A.L. Evolution of duplicate genes in a tetraploid animal, Xenopus laevis. Molecular Biology and Evolution 10 6 (1993) 1360-1369
55. Labbé P., Berthomieu A., Berticat C., Alout H., Raymond M., Lenormand T., et al. Independent duplications of the acetylcholinesterase gene conferring insecticide resistance in the mosquito Culex pipiens. Molecular Biology and Evolution 24 4 (2007) 1056-1067
56. Emanuelsson O., Brunak S., von Heijne G., and Nielsen H. Locating proteins in the cell using TargetP, SignalP and related tools. Nature Protocols 2 4 (2007) 953-971