期刊论文详细信息
EvoDevo
Functional genetic characterization of salivary gland development in Aedes aegypti
Molly Duman-Scheel1  David W Severson3  Anthony Clemons2  Zeinab Annan3  Longhua Sun2  Christy Le3  Emily Andrews3  Chilinh Nguyen3 
[1] Indiana University School of Medicine, Raclin-Carmichael Hall, 1234 Notre Dame Avenue, South Bend, IN 46617, USA;University of Notre Dame, Notre Dame, Eck Institute for Global Health and Department of Biological Sciences, Notre Dame, IN 46556, USA;Department of Medical and Molecular Genetics, Indiana University School of Medicine, South Bend, IN 46617, USA
关键词: Vector;    siRNA;    Salivary gland;    Mosquito;    Drosophila melanogaster;    Development;    CrebA;    Aedes aegypti;   
Others  :  806815
DOI  :  10.1186/2041-9139-4-9
 received in 2012-09-27, accepted in 2012-12-07,  发布年份 2013
PDF
【 摘 要 】

Background

Despite the devastating global impact of mosquito-borne illnesses on human health, very little is known about mosquito developmental biology. In this investigation, functional genetic analysis of embryonic salivary gland development was performed in Aedes aegypti, the dengue and yellow fever vector and an emerging model for vector mosquito development. Although embryonic salivary gland development has been well studied in Drosophila melanogaster, little is known about this process in mosquitoes or other arthropods.

Results

Mosquitoes possess orthologs of many genes that regulate Drosophila melanogaster embryonic salivary gland development. The expression patterns of a large subset of these genes were assessed during Ae. aegypti development. These studies identified a set of molecular genetic markers for the developing mosquito salivary gland. Analysis of marker expression allowed for tracking of the progression of Ae. aegypti salivary gland development in embryos. In Drosophila, the salivary glands develop from placodes located in the ventral neuroectoderm. However, in Ae. aegypti, salivary marker genes are not expressed in placode-like patterns in the ventral neuroectoderm. Instead, marker gene expression is detected in salivary gland rudiments adjacent to the proventriculus. These observations highlighted the need for functional genetic characterization of mosquito salivary gland development. An siRNA- mediated knockdown strategy was therefore employed to investigate the role of one of the marker genes, cyclic-AMP response element binding protein A (Aae crebA), during Ae. aegypti salivary gland development. These experiments revealed that Aae crebA encodes a key transcriptional regulator of the secretory pathway in the developing Ae. aegypti salivary gland.

Conclusions

The results of this investigation indicated that the initiation of salivary gland development in Ae. aegypti significantly differs from that of D. melanogaster. Despite these differences, some elements of salivary gland development, including the ability of CrebA to regulate secretory gene expression, are conserved between the two species. These studies underscore the need for further analysis of mosquito developmental genetics and may foster comparative studies of salivary gland development in additional insect species.

【 授权许可】

   
2013 Nguyen et al; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140708100515490.pdf 3565KB PDF download
Figure 5. 184KB Image download
Figure 4. 106KB Image download
Figure 3. 145KB Image download
Figure 2. 124KB Image download
Figure 1. 102KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】
  • [1]Raminani LN, Cupp EW: Early embryology of Aedes aegypti (L.) (Diptera: Culicdae). Int J Insect Morphol Embryol 1975, 4:517-528.
  • [2]Raminani LN, Cupp EW: Embryology of Aedes aegypti (L.) (Diptera: Culicidae): organogenesis. Int J Insect Morphol Embryol 1978, 7:273-296.
  • [3]Clemons A, Haugen M, Flannery E, Tomchaney M, Kast K, Jacowski C, Le C, Mori A, Simanton Holland W, Sarro J, Severson DW, Duman-Scheel M: Aedes aegypti: an emerging model for vector mosquito development. Cold Spring Harb Protoc 2010, 2010(10):pdb.emo141.
  • [4]Clemons A, Mori A, Haugen M, Severson DW, Duman-Scheel M: Culturing and egg collection of Aedes aegypti. Cold Spring Harb Protoc 2010, 2010(10):pdb.prot5507.
  • [5]Clemons A, Haugen M, Flannery E, Kast K, Jacowski C, Severson D, Duman-Scheel M: Fixation and preparation of developing tissues from Aedes aegypti. Cold Spring Harb Protoc 2010, 2010(10):pdb.prot5508.
  • [6]Clemons A, Flannery E, Kast K, Severson D, Duman-Scheel M: Immunohistochemical analysis of protein expression during Aedes aegypti development. Cold Spring Harb Protoc 2010, 2010(10):pdb prot5510.
  • [7]Clemons A, Haugen M, Severson D, Duman-Scheel M: Functional analysis of genes in Aedes aegypti embryos. Cold Spring Harb Protoc 2010, 2010(10):pdb prot5511.
  • [8]Haugen M, Tomchaney M, Kast K, Flannery E, Clemons A, Jacowski C, Simanton Holland W, Le C, Severson D, Duman-Scheel M: Whole-mount in situ hybridization for analysis of gene expression during Aedes aegypti development. Cold Spring Harb Protoc 2010, 2010(10):pdb prot5509.
  • [9]Clemons A, Haugen M, Le C, Mori A, Tomchaney M, Severson DW, Duman-Scheel M: siRNA-mediated gene targeting in Aedes aegypti embryos reveals that frazzled regulates vector mosquito CNS development. PLoS One 2011, 6:e16730.
  • [10]Haugen M, Flannery E, Tomchaney M, Mori A, Behura SK, Severson DW, Duman-Scheel M: Semaphorin-1a is required for Aedes aegypti embryonic nerve cord development. PLoS One 2011, 6:e21694.
  • [11]Behura SK, Haugen M, Flannery E, Sarro J, Tessier CR, Severson DW, Duman-Scheel M: Comparative genomic analysis of Drosophila melanogaster and vector mosquito developmental genes. PLoS One 2011, 6:e21504.
  • [12]Goltsev Y, Hsiong W, Lanzaro G, Levine M: Different combinations of gap repressors for common stripes in Anopheles and Drosophila embryos. Dev Biol 2004, 275:435-446.
  • [13]Juhn J, Juhn J, James AA: oskar gene expression in the vector mosquitoes, Anopheles gambiae and Aedes aegypti. Insect Mol Biol 2006, 15:363-372.
  • [14]Ribeiro JM: Blood-feeding arthropods: live syringes or invertebrate pharmacologists? Infect Agents Dis 1995, 4:143-152.
  • [15]Valenzuela JG: High-throughput approaches to study salivary proteins and genes from vectors of disease. Insect Biochem Mol Biol 2002, 32:1199-1209.
  • [16]Andrew DJ, Henderson KD, Seshaiah P: Salivary gland development in Drosophila melanogaster. Mech Dev 2000, 92:5-17.
  • [17]Abrams EW, Vining MS, Andrew DJ: Constructing an organ: the Drosophila salivary gland as a model for tube formation. Trends Cell Biol 2003, 13:247-254.
  • [18]Horsfall WFH, Morettia L, Larsen J: Bionomics and Embryology of the Inland Floodwater Mosquito Aedes vexans. Urbana, IL: University of Illinois Press; 1973.
  • [19]Christophers SR: Aedes aegypti, The Yellow Fever Mosquito: Its Life History, Bionomics, and Structure. Cambridge, UK: Cambridge University Press; 1960.
  • [20]Patel NH: Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Meth Cell Biol 1994, 44:445-487.
  • [21]Kumar S, Konikoff C, Van Emden B, Busick C, Davis KT, Ji S, Wu LW, Ramos H, Brody T, Panchanathan S, Ye J, Karr TL, Gerold K, McCutchan M, Newfeld SJ: FlyExpress: visual mining of spatiotemporal patterns for genes and publications in Drosophila embryogenesis. Bioinformatics 2011, 27:3319-3320.
  • [22]Konikoff CE, Karr TL, McCutchan M, Newfeld SJ, Kumar S: Comparison of embryonic expression within multigene families using the FlyExpress discovery platform reveals more spatial than temporal divergence. Dev Dyn 2012, 241:150-160.
  • [23]Smedley D, Haider S, Ballester B, Holland R, London D, Thorisson G, Kasprzyk A: BioMart–biological queries made easy. BMC Genom 2009, 10:22. BioMed Central Full Text
  • [24]Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, Butler R, Campbell KS, Christophides GK, Christley S, Dialynas E, Hammond M, Hill CA, Konopinski N, Lobo NF, MacCallum RM, Madey G, Megy K, Meyer J, Redmond S, Severson DW, Stinson EO, Topalis P, Birney E, Gelbart WM, Kafatos FC, Louis C, Collins FH: VectorBase: a data resource for invertebrate vector genomics. Nucleic Acids Res 2009, 37:D583-D587.
  • [25]Abrams EW, Andrew DJ: CrebA regulates secretory activity in the Drosophila salivary gland and epidermis. Development 2005, 132:2743-2758.
  • [26]Patel N: In Situ Hybridization to Whole Mount Drosophila Embryos. New York: Wiley-Liss; 1996.
  • [27]Davis C: A comparative study of larval embryogenesis in the mosquito Culex fatigans wiedemann (diptera: culicidae) and the sheep-fly Lucilia sericata meigen (diptera: calliphoridae). Aust J Zool 1967, 15:547-579.
  • [28]Parthasarathy R, Gopinathan KP: Comparative analysis of the development of the mandibular salivary glands and the labial silk glands in the mulberry silkworm, Bombyx mori. Gene Expr Patterns 2005, 5:323-339.
  • [29]Kokubo H, Ueno K, Amanai K, Suzuki Y: Involvement of the Bombyx Scr gene in development of the embryonic silk gland. Dev Biol 1997, 186:46-57.
  • [30]Duman-Scheel M, Patel NH: Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 1999, 126:2327-2334.
  • [31]Duman-Scheel M, Clark SM, Grunow ET, Hasley AO, Hill BL, Simanton WL: 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 2007, 9:131-140.
  • [32]Simanton W, Clark S, Clemons A, Jacowski C, Farrell-VanZomeren A, Beach P, Browne WE, Duman-Scheel M: Conservation of arthropod midline netrin accumulation revealed with a cross-reactive antibody provides evidence for midline cell homology. Evol Dev 2009, 11:260-268.
  • [33]Kokoza VA, Raikhel AS: Targeted gene expression in the transgenic Aedes aegypti using the binary Gal4-UAS system. Insect Biochem Mol Biol 2011, 41:637-644.
  • [34]Lynd A, Lycett GJ: Development of the bi-partite Gal4-UAS system in the African malaria mosquito, Anopheles gambiae. PLoS One 2012, 7:e31552.
  文献评价指标  
  下载次数:50次 浏览次数:29次