Semaphorin-1a is required for Aedes aegypti embryonic nerve cord development

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Haugen, Morgan ^a   Flannery, Ellen ^b   Tomchaney, Michael ^a,b   Mori, Akio ^b   Behura, Susanta K ^b   Severson, David W ^a,b   Duman Scheel, Molly ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSECT PROTEIN; PLEXIN A RECEPTOR; SEMAPHORIN 1A; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; SEMAPHORIN;

AEDES AEGYPTI; ANOPHELES GAMBIAE; ARTICLE; BRAIN COMMISSURE; CONTROLLED STUDY; DISEASE CARRIER; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; LOSS OF FUNCTION MUTATION; NERVE CORD DEVELOPMENT; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; VENTRAL ROOT; AEDES; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVOUS TISSUE; PHYSIOLOGY; PRENATAL DEVELOPMENT;

AEDES AEGYPTI; ANOPHELES GAMBIAE; DIPTERA; DROSOPHILA MELANOGASTER; HEXAPODA;

AEDES; ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; NERVE TISSUE; SEMAPHORINS;

EID: 79959599801     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021694     Document Type: Article

References (56)

1. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, et al. (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298: 129-149.
2. Nene V, Wortman JR, Lawson D, Haas B, Kodira C, et al. (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316: 1718-1723.
3. Arensburger P, Megy K, Waterhouse RM, Abrudan J, Amedeo P, et al. (2010) Sequencing of Culex quinquefasciatus establishes a platform for mosquito comparative genomics. Science 330: 86-88.
4. Clemons A, Haugen M, Flannery E, Tomchaney M, Kast K, et al. (2010) Aedes aegypti: an emerging model for vector mosquito development. Cold Spring Harb Protoc 2010: pdb emo141.
5. Chen XG, Mathur G, James AA, (2008) Gene expression studies in mosquitoes. Adv Genet 64: 19-50.
6. Raminani LN, Cupp EW, (1975) Early embryology of Aedes aegypti (L.) (Diptera: Culicdae). Int J Insect Morphol Embryol 4: 517-528.
7. Raminani LNCE, (1978) Embryology of Aedes aegypti (L.) (Diptera: Culicidae): organogenesis. Int J Insect Morphol & Embryol 7: 273-296.
8. Goltsev Y, Hsiong W, Lanzaro G, Levine M, (2004) Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev Biol 275: 435-446.
9. Calvo E, Walter M, Adelman ZN, Jimenez A, Onal S, et al. (2005) Nanos (nos) genes of the vector mosquitoes, Anopheles gambiae, Anopheles stephensi and Aedes aegypti. Insect Biochem Mol Biol 35: 789-798.
10. Juhn J, James AA, (2006) oskar gene expression in the vector mosquitoes, Anopheles gambiae and Aedes aegypti. Insect Mol Biol 15: 363-372.
11. Juhn J, Marinotti O, Calvo E, James AA, (2008) Gene structure and expression of nanos (nos) and oskar (osk) orthologues of the vector mosquito, Culex quinquefasciatus. Insect Mol Biol 17: 545-552.
12. Adelman ZN, Jasinskiene N, Onal S, Juhn J, Ashikyan A, et al. (2007) nanos gene control DNA mediates developmentally regulated transposition in the yellow fever mosquito Aedes aegypti. Proc Natl Acad Sci U S A 104: 9970-9975.
13. Goltsev Y, Fuse N, Frasch M, Zinzen RP, Lanzaro G, et al. (2007) Evolution of the dorsal-ventral patterning network in the mosquito, Anopheles gambiae. Development 134: 2415-2424.
14. Goltsev Y, Rezende GL, Vranizan K, Lanzaro G, Valle D, et al. (2009) Developmental and evolutionary basis for drought tolerance of the Anopheles gambiae embryo. Dev Biol 330: 462-470.
15. Simanton W, Clark S, Clemons A, Jacowski C, Farrell-VanZomeren A, et al. (2009) Conservation of arthropod midline netrin accumulation revealed with a cross-reactive antibody provides evidence for midline cell homology. Evol Dev 11: 260-268.
16. Clemons A, Haugen M, Le C, Mori A, Tomchaney M, et al. siRNA-mediated gene targeting in Aedes aegypti embryos reveals that frazzled regulates vector mosquito CNS development. PLoS One 6 (1): e16730.
17. Severson DW, DeBruyn B, Lovin DD, Brown SE, Knudson DL, et al. (2004) Comparative genome analysis of the yellow fever mosquito Aedes aegypti with Drosophila melanogaster and the malaria vector mosquito Anopheles gambiae. J Hered 95: 103-113.
18. Clemons A, Flannery E, Kast K, Severson D, Duman-Scheel M, (2010) Immunohistochemical analysis of protein expression during Aedes aegypti development. Cold Spring Harb Protoc 2010: pdb prot5510.
19. Clemons A, Haugen M, Flannery E, Kast K, Jacowski C, et al. (2010) Fixation and preparation of developing tissues from Aedes aegypti. Cold Spring Harb Protoc 2010: pdb prot5508.
20. Clemons A, Haugen M, Severson D, Duman-Scheel M, (2010) Functional analysis of genes in Aedes aegypti embryos. Cold Spring Harb Protoc 2010: pdb prot5511.
21. Clemons A, Mori A, Haugen M, Severson DW, Duman-Scheel M, (2010) Culturing and egg collection of Aedes aegypti. Cold Spring Harb Protoc 2010: pdb prot5507.
22. Haugen M, Tomchaney M, Kast K, Flannery E, Clemons A, et al. (2010) Whole-mount in situ hybridization for analysis of gene expression during Aedes aegypti development. Cold Spring Harbor Protoc 2010: pdb prot5509.
23. Duman-Scheel M, Clark SM, Grunow ET, Hasley AO, Hill BL, et al. (2007) Delayed onset of midline netrin expression in Artemia franciscana coincides with commissural axon growth and provides evidence for homology of midline cells in distantly related arthropods. Evol Dev 9: 131-140.
24. Kolodkin AL, Matthes DJ, Goodman CS, (1993) The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75: 1389-1399.
25. Flannery E, Duman-Scheel M, (2009) Semaphorins at the interface of development and cancer. Curr Drug Targets 10: 611-619.
26. Yu HH, Araj HH, Ralls SA, Kolodkin AL, (1998) The transmembrane Semaphorin Sema I is required in Drosophila for embryonic motor and CNS axon guidance. Neuron 20: 207-220.
27. Winberg ML, Noordermeer JN, Tamagnone L, Comoglio PM, Spriggs MK, et al. (1998) Plexin A is a neuronal semaphorin receptor that controls axon guidance. Cell 95: 903-916.
28. Ayoob JC, Terman JR, Kolodkin AL, (2006) Drosophila Plexin B is a Sema-2a receptor required for axon guidance. Development 133: 2125-2135.
29. Sweeney LB, Couto A, Chou YH, Berdnik D, Dickson BJ, et al. (2007) Temporal target restriction of olfactory receptor neurons by Semaphorin-1a/PlexinA-mediated axon-axon interactions. Neuron 53: 185-200.
30. Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo L, (2007) Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128: 399-410.
31. Yu L, Zhou Y, Cheng S, Rao Y, (2010) Plexin a-semaphorin-1a reverse signaling regulates photoreceptor axon guidance in Drosophila. J Neurosci 30: 12151-12156.
32. Flannery E, VanZomeren-Dohm A, Beach P, Holland WS, Duman-Scheel M, (2010) Induction of cellular growth by the axon guidance regulators netrin A and semaphorin-1a. Dev Neurobiol 70: 473-484.
33. Tessier-Lavigne M, Goodman CS, (1996) The molecular biology of axon guidance. Science 274: 1123-1133.
34. Kaprielian Z, Runko E, Imondi R, (2001) Axon guidance at the midline choice point. Dev Dyn 221: 154-181.
35. Patel NH, (1994) Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol 44: 445-487.
36. Mitchell KJ, Doyle JL, Serafini T, Kennedy TE, Tessier-Lavigne M, et al. (1996) Genetic analysis of Netrin genes in Drosophila: Netrins guide CNS commissural axons and peripheral motor axons. Neuron 17: 203-215.
37. Harris R, Sabatelli LM, Seeger MA, (1996) Guidance cues at the Drosophila CNS midline: identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17: 217-228.
38. Kolodziej PA, Timpe LC, Mitchell KJ, Fried SR, Goodman CS, et al. (1996) frazzled encodes a Drosophila member of the DCC immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87: 197-204.
39. Yu HH, Huang AS, Kolodkin AL, (2000) Semaphorin-1a acts in concert with the cell adhesion molecules fasciclin II and connectin to regulate axon fasciculation in Drosophila. Genetics 156: 723-731.
40. Zlatic M, Li F, Strigini M, Grueber W, Bate M, (2009) Positional cues in the Drosophila nerve cord: semaphorins pattern the dorso-ventral axis. PLoS Biol 7: e1000135.
41. Thomas JB, Bastiani MJ, Bate M, Goodman CS, (1984) From grasshopper to Drosophila: a common plan for neuronal development. Nature 310: 203-207.
42. Duman-Scheel M, Patel NH, (1999) Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126: 2327-2334.
43. Benedict MQ, (1997) The Molecular Biology of Insect Vectors of Disease. In: Crampton JM, Beard CB, Louis C, editors. London Chapman and Hall pp. 3-12.
44. Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucl Acids Res 37: D555-D559.
45. Patel N, (1996) In situ hybridization to whole mount Drosophila embryos. In: Krieg PA, editors. New York Wiley-Liss pp. 357-370.
46. Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, et al. (2009) VectorBase: a data resource for invertebrate vector genomics. Nucl Acids Res 37: D583-D587.
47. Morlais I, Mori A, Schneider JR, Severson DW, (2003) A targeted approach to the identification of candidate genes determining susceptibility to Plasmodium gallinaceum in Aedes aegypti. Mol Genet Genomics 269: 753-764.
48. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
49. Kriventseva EV, Rahman N, Espinosa O, Zdobnov EM, (2008) OrthoDB: the hierarchical catalog of eukaryotic orthologs. Nucleic Acids Res 36: D271-275.
50. Smedley D, Haider S, Ballester B, Holland R, London D, et al. (2009) BioMart-biological queries made easy. BMC Genomics 10: 22.
51. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, et al. (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
52. Saitou N, Nei M, (1987) The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4: 406-425.
53. Felsenstein J, (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783-791.
54. Takezaki N, Rzhetsky A, Nei M, (2004) Phylogenetic test of the molecular clock and linearized trees. Molecular Biology and Evolution 12: 823-833.
55. Zuckerkandl E, Pauling L, (1965) Evolutionary divergence and convergence in proteins. In: Bryson V, Vogel HJ, editors. New York Academic Press pp. 97-166.
56. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596-1599.