| BMC Developmental Biology | |
| Integrated proteomic and transcriptomic analysis of the Aedes aegypti eggshell | |
| Anthony A James2  Paul D Gershon3  Zhijian Tu1  Marika F Walter4  Xiaofang Jiang1  Pedro N Marinotti3  Rebeca Carballar-Lejarazú3  Jennifer Juhn3  Brian Nguyen3  Shao-Pei Chou5  Bianca B Kojin3  Tuan Ngo3  Osvaldo Marinotti3  | |
| [1] Department of Biochemistry, Virginia Tech, Blacksburg, VA 24061, USA;Department of Microbiology and Molecular Genetics, University of California, Irvine, CA 92697, USA;Department of Molecular Biology and Biochemistry, University of California, Irvine, CA 92697, USA;Department of Biological Chemistry, School of Medicine, University of California, Irvine, CA 92697, USA;Department of Molecular Biology and Genetics, Cornell University, Cornell, NY 14850, USA | |
| 关键词: Mosquito; Oogenesis; Estivation; Vitelline membrane; Chorion; Eggshell; Aedes aegypti; | |
| Others : 1084996 DOI : 10.1186/1471-213X-14-15 |
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| received in 2013-12-09, accepted in 2014-03-31, 发布年份 2014 | |
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【 摘 要 】
Background
Mosquito eggshells show remarkable diversity in physical properties and structure consistent with adaptations to the wide variety of environments exploited by these insects. We applied proteomic, transcriptomic, and hybridization in situ techniques to identify gene products and pathways that participate in the assembly of the Aedes aegypti eggshell. Aedes aegypti population density is low during cold and dry seasons and increases immediately after rainfall. The survival of embryos through unfavorable periods is a key factor in the persistence of their populations. The work described here supports integrated vector control approaches that target eggshell formation and result in Ae. aegypti drought-intolerant phenotypes for public health initiatives directed to reduce mosquito-borne diseases.
Results
A total of 130 proteins were identified from the combined mass spectrometric analyses of eggshell preparations.
Conclusions
Classification of proteins according to their known and putative functions revealed the complexity of the eggshell structure. Three novel Ae. aegypti vitelline membrane proteins were discovered. Odorant-binding and cysteine-rich proteins that may be structural components of the eggshell were identified. Enzymes with peroxidase, laccase and phenoloxidase activities also were identified, and their likely involvements in cross-linking reactions that stabilize the eggshell structure are discussed.
【 授权许可】
2014 Marinotti et al.; licensee BioMed Central Ltd.
【 预 览 】
| Files | Size | Format | View |
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| 20150113165857691.pdf | 2699KB | ||
| Figure 5. | 143KB | Image | |
| Figure 4. | 102KB | Image | |
| Figure 3. | 176KB | Image | |
| Figure 2. | 40KB | Image | |
| Figure 1. | 77KB | Image |
【 图 表 】
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【 参考文献 】
- [1]Margaritis LH: Structure And Physiology Of The Eggshell. In Comprehensive Insect Physiology, Biochemistry and Pharmacology. Volume I Embryogenesis and Reproduction. Edited by Kerkut GA, Gilbert LI. Oxford: Pergamon Press; 1985:153-230.
- [2]Waring GL: Morphogenesis of the eggshell in Drosophila. Int Rev Cytol 2000, 198:67-108.
- [3]Cavaliere V, Bernardi F, Romani P, Duchi S, Gargiulo G: Building up the Drosophila eggshell: first of all the eggshell genes must be transcribed. Dev Dyn 2008, 237:2061-2072.
- [4]Jagadeeshan S, Singh RS: Rapid evolution of outer egg membrane proteins in the Drosophila melanogaster subgroup: a case of ecologically driven evolution of female reproductive traits. Mol Biol Evol 2007, 24:929-938.
- [5]Suman DS, Shrivastava AR, Parashar BD, Pant SC, Agrawal OP, Prakash S: Variation in morphology and morphometrics of eggs of Culex quinquefasciatus mosquitoes from different ecological regions of India. J Vector Ecol 2009, 34:191-199.
- [6]Sahlén G: Eggshell ultrastructure in four mosquito genera (Diptera, culicidae). J Am Mosq Control Assoc 1996, 12:263-270.
- [7]Christophers SR: Aedes Aegypti. The Yellow Fever Mosquito. Its Life History, Bionomics And Structure. London: Cambridge University Press; 1960.
- [8]Sota T, Mogi M: Survival time and resistance to desiccation of diapause and non-diapause eggs of temperate Aedes (Stegomyia) mosquitoes. Entomol Exp Appl 1992, 63:155-161.
- [9]Deane MP, Causey OR: Viability of Anopheles gambiae eggs and morphology of unusual types found in Brazil. Am J Trop Med Hyg 1943, 23:95-102.
- [10]Beier JC, Copeland R, Oyaro C, Masinya A, Odago WO, Oduor S, Koech DK, Roberts CR: Anopheles gambiae complex egg-stage survival in dry soil from larval development sites in western Kenya. J Am Mosq Control Assoc 1990, 6:105-109.
- [11]Lin Y, Hamblin MT, Edwards MJ, Barillas-Mury C, Kanost MR, Knipple DC, Wolfner MF, Hagedorn HH: Structure, expression, and hormonal control of genes from the mosquito, Aedes aegypti, which encode proteins similar to the vitelline membrane proteins of Drosophila melanogaster. Dev Biol 1993, 155:558-568.
- [12]Li J: Egg chorion tanning in Aedes aegypti mosquito. Comp Biochem Physiol 1994, 109A:835-843.
- [13]Ferdig MT, Li J, Severson DW, Christensen BM: Mosquito dopa decarboxylase cDNA characterization and blood-meal-induced ovarian expression. Insect Mol Biol 1996, 5:119-126.
- [14]Li J, Hodgeman BA, Christensen BM: Involvement of peroxidase in chorion hardening in Aedes aegypti. Insect Biochem Mol Biol 1996, 26:309-317.
- [15]Edwards MJ, Severson DW, Hagedorn HH: Vitelline envelope genes of the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 1998, 28:915-925.
- [16]Han Q, Li G, Li J: Purification and characterization of chorion peroxidase from Aedes aegypti eggs. Arch Biochem Biophys 2000, 378:107-115.
- [17]Yao R, Li J: Towards global analysis of mosquito chorion proteins through sequential extraction, two-dimensional electrophoresis and mass spectrometry. Proteomics 2003, 3:2036-2043.
- [18]Li J, Kim SR, Li J: Molecular characterization of a novel peroxidase involved in Aedes aegypti chorion protein crosslinking. Insect Biochem Mol Biol 2004, 34:1195-1203.
- [19]Kim SR, Yao Y, Han Q, Christensen BM, Li J: Identification and molecular characterization of a prophenoloxidase involved in Aedes aegypti chorion melanization. Insect Mol Biol 2005, 14:185-194.
- [20]Li JS, Li J: Major chorion proteins and their crosslinking during chorion hardening in Aedes aegypti mosquitoes. Insect Biochem Mol Biol 2006, 36:1195-1203.
- [21]Biedler JK, Hu W, Tae H, Tu Z: Identification of early zygotic genes in the yellow fever mosquito Aedes aegypti and discovery of a motif involved in early zygotic genome activation. PLoS One 2012, 7:e33933.
- [22]Jaeger J, Manu , Reinitz J: Drosophila blastoderm patterning. Curr Opin Genet Dev 2012, 22:533-541.
- [23]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, 35:789-798.
- [24]Juhn J, James AA: Oskar gene expression in the vector mosquitoes, Anopheles gambiae and Aedes aegypti. Insect Molec Biol 2006, 15:363-372.
- [25]Dissanayake SN, Ribeiro JM, Wang MH, Dunn WA, Yan G, James AA, Marinotti O: aeGEPUCI: a database of gene expression in the dengue vector mosquito, Aedes aegypti. BMC Res Notes 2010, 3:248. BioMed Central Full Text
- [26]Akbari OS, Antoshechkin I, Amrhein H, Williams B, Diloreto R, Sandler J, Hay BA: The developmental transcriptome of the mosquito Aedes aegypti, an invasive species and major arbovirus vector. G3 (Bethesda) 2013, 3:1493-1509.
- [27]Anderson WA, Spielman A: Incorporation of RNA and protein precursors by ovarian follicles of Aedes aegypti mosquitoes. J Submicrosc Cytol 1973, 5:181-198.
- [28]Mathew G, Rai KS: The structure and formation of egg membranes in Aedes aegypti. Internat J Insect Morphol Embryol 1975, 4:369-380.
- [29]Raikhel AS, Lea AO: Control of follicular epithelium development and vitelline envelope formation in the mosquito; role of juvenile hormone and 20-hydroxyecdysone. Tissue Cell 1991, 23:577-5791.
- [30]Gigliotti S, Graziani F, De Ponti L, Rafti F, Manzi A, Lavorgna G, Gargiulo G, Malva C: Sex-, tissue-, and stage-specific expression of a vitelline membrane protein gene from region 32 of the second chromosome of Drosophila melanogaster. Dev Genet 1989, 10:33-41.
- [31]Andrenacci D, Cernilogar FM, Taddel C, Rotoli D, Cavaliere V, Graziani F, Gargiulo G: Specific domains drive VM32E protein distribution and integration in Drosophila eggshell layers. J Cell Sci 2001, 114:2819-2829.
- [32]Merzendorfer H, Zimoch L: Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 2003, 206:4393-4412.
- [33]Moreira MF, Dos Santos AS, Marotta HR, Mansur JF, Ramos IB, Machado EA, Souza GH, Eberlin MN, Kaiser CR, Kramer KJ, Muthukrishnan S, Vasconcellos AM: A chitin-like component in Aedes aegypti eggshells, eggs and ovaries. Insect Biochem Mol Biol 2007, 37:1249-61.
- [34]Cohen E: Chitin synthesis and inhibition: a revisit. Pest Manag Sci 2001, 57:946-950.
- [35]Arnold K, Brydon LJ, Chappell LH, Gooday GW: Chitinolytic activities in Heligmosomoides polygyrus and their role in egg hatching. Mol Biochem Parasitol 1993, 58:317-323.
- [36]Biessmann H, Walter MF, Dimitratos S, Woods D: Isolation of cDNA clones encoding putative odourant binding proteins from the antennae of the malaria-transmitting mosquito, Anopheles gambiae. Insect Mol Biol 2002, 11:123-132.
- [37]Calvo E, Mans BJ, Ribeiro JM, Andersen JF: Multifunctionality and mechanism of ligand binding in a mosquito anti-inflammatory protein. Proc Natl Acad Sci 2009, 106:3728-3733.
- [38]Rothemund S, Liou YC, Davies PL, Krause E, Sönnichsen FD: A new class of hexahelical insect proteins revealed as putative carriers of small hydrophobic ligands. Structure 1999, 15:1325-1332.
- [39]Manoharan M, Ng Fuk Chong M, Vaïtinadapoulé A, Frumence E, Sowdhamini R, Offmann B: Comparative genomics of odorant binding proteins in Anopheles gambiae, Aedes aegypti, and Culex quinquefasciatus. Genome Biol Evol 2013, 5:163-80.
- [40]Vieira FG, Rozas J: Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system. Genome Biol Evol 2011, 3:476-490.
- [41]Amenya DA, Chou W, Li J, Yan G, Gershon PD, James AA, Marinotti O: Proteomics reveals novel components of the Anopheles gambiae eggshell. J Insect Physiol 2010, 56:1414-1419.
- [42]Fukuda N, Yomogida K, Okabe M, Touhara K: Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J Cell Sci 2004, 15:5835-5845.
- [43]da Silva AL C, Kojin BB, Marinotti O, James AA, Capurro ML: Expression and accumulation of the two-domain odorant binding protein AaegOBP45 in the ovaries of blood-fed Aedes aegypti. Parasites and Vectors 2013, 6:364. BioMed Central Full Text
- [44]Gaunt MW, Miles MA: An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographical landmarks. Mol Biol Evol 2002, 19:748-761.
- [45]Han Q, Li G, Li J: Chorion peroxidase-mediated NADH/O(2) oxidoreduction cooperated by chorion malate dehydrogenase-catalyzed NADH production: a feasible pathway leading to H(2)O(2) formation during chorion hardening in Aedes aegypti mosquitoes. Biochim Biophys Acta 2000, 1523:246-253.
- [46]Pan C, Zhou Y, Mo J: The clone of laccase gene and its potential function in cuticular penetration resistance of Culex pipiens pallens to fenvalerate. Pestic Biochem Physiol 2009, 93:105-111.
- [47]Wu X, Zhan X, Gan M, Zhang D, Zhang M, Zheng X, Wu Y, Li Z, He A: Laccase2 is required for sclerotization and pigmentation of Aedes albopictus eggshell. Parasitol Res 2013, 112:1929-1934.
- [48]Shibata T, Ariki S, Shinzawa N, Miyaji R, Suyama H, Sako M, Inomata N, Koshiba T, Kanuka H, Kawabata S: Protein crosslinking by transglutaminase controls cuticle morphogenesis in Drosophila. PLoS One 2010, 5:e13477.
- [49]Claycomb JM, Benasutti M, Bosco G, Fenger DD, Orr-Weaver TL: Gene amplification as a developmental strategy: isolation of two developmental amplicons in Drosophila. Dev Cell 2004, 6:145-155.
- [50]Fakhouri M, Elalayli M, Sherling D, Hall JD, Miller E, Sun X, Wells L, LeMosy EK: Minor proteins and enzymes of the Drosophila eggshell matrix. Dev Biol 2006, 293:127-141.
- [51]Fischer S, Alem IS, De Majo MS, Campos RE, Schweigmann N: Cold season mortality and hatching behavior of Aedes aegypti L. (Diptera: Culicidae) eggs in Buenos Aires City, Argentina. J Vector Ecol 2011, 36:94-99.
- [52]Keramaris KE, Margaritis LH, Zografou EN, Tsiropoulos GJ: Egg laying suppression in Drosophila melanogaster (Diptera:Drosophilidae) and Dacus (Bractocera) oleae (Diptera: Tephritidae) by phloroglucinol, a peroxidase inhibitor. Bull Entomol Res 1996, 86:369-375.
- [53]Willardsen JA, Dudley DA, Cody WL, Chi L, McClanahan TB, Mertz TE, Potoczak RE, Narasimhan LS, Holland DR, Rapundalo ST, Edmunds JJ: Design, synthesis, and biological activity of potent and selective inhibitors of blood coagulation factor Xa. J Med Chem 2004, 47:4089-4099.
- [54]Huang P, Ramphal J, Wei J, Liang C, Jallal B, McMahon G, Tang C: Structure-based design and discovery of novel inhibitors of protein tyrosine phosphatases. Bioorg Med Chem 2003, 11:1835-1849.
- [55]Meola RW, Dean SR, Meola SM, Sittertz-Bhatkar H, Schenker R: Effect of lufenuron on chorionic and cuticular structure of unhatched larval Ctenocephalides felis (Siphonaptera: Pulicidae). J Med Entomol 1999, 36:92-100.
- [56]Terenius O, Marinotti O, Sieglaff D, James AA: Molecular genetic manipulation of vector mosquitoes. Cell Host Microbe 2008, 4:417-423.
- [57]O’Brochta DA, Handler AM: Perspectives on the state of insect transgenics. Adv Exp Med Biol 2008, 627:1-18.
- [58]Fu G, Lees RS, Nimmo D, Aw D, Jin L, Gray P, Berendonk TU, White-Cooper H, Scaife S, Kim Phuc H, Marinotti O, Jasinskiene N, James AA, Alphey L: Female-specific flightless phenotype for mosquito control. Proc Natl Acad Sci U S A 2010, 107:4550-4554.
- [59]Robert MA, Okamoto K, Lloyd AL, Gould F: A reduce and replace strategy for suppressing vector-borne diseases: insights from a deterministic model. PLoS One 2013, 8:e73233.
- [60]Wiśniewski JR, Zougman A, Nagaraj N, Mann M: Universal sample preparation method for proteome analysis. Nat Methods 2009, 6:359-362.
- [61]Rappsilber J, Mann M, Ishihama Y: Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat Protoc 2007, 2:1896-1906.
- [62]Bonizzoni M, Dunn WA, Campbell CL, Olson KE, Marinotti O, James AA: Strain variation in the transcriptome of the dengue fever vector, Aedes aegypti. G3 (Bethesda) 2012, 2:103-114.
- [63]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10:R25. BioMed Central Full Text
- [64]Schmittgen TD, Livak KJ: Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1118.
- [65]Bailey TL, Bodén M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS: MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 2009, 37:W202-W208.
- [66]Simossis VA, Heringa J: PRALINE: a multiple sequence alignment toolbox that integrates homology-extended and secondary structure information. Nucleic Acids Res 2005, 33:W289-W294.
- [67]Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A: Protein Identification and Analysis Tools on the ExPASy Server. In The Proteomics Protocols Handbook. Edited by Walker JM. Totowa, New Jersey: Humana Press; 2005:571-607.
- [68]Kyte J, Doolittle R: A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982, 157:105-132.
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