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Brain Development in the Yellow Fever Mosquito Aedes Aegypti: a Comparative Immunocytochemical Analysis Using Cross-Reacting Antibodies from Drosophila Melanogaster

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Brain Development in the Yellow Fever Mosquito Aedes Aegypti: a Comparative Immunocytochemical Analysis Using Cross-Reacting Antibodies from Drosophila Melanogaster Dev Genes Evol (2011) 221:281–296 DOI 10.1007/s00427-011-0376-2 ORIGINAL ARTICLE Brain development in the yellow fever mosquito Aedes aegypti: a comparative immunocytochemical analysis using cross-reacting antibodies from Drosophila melanogaster Keshava Mysore & Susanne Flister & Pie Müller & Veronica Rodrigues & Heinrich Reichert Received: 1 April 2011 /Accepted: 14 September 2011 /Published online: 30 September 2011 # Springer-Verlag 2011 Abstract Considerable effort has been directed towards model system, Drosophila melanogaster, in larval, pupal, understanding the organization and function of peripheral and adult stages. Furthermore, we use immunolabeling to and central nervous system of disease vector mosquitoes such document the development of specific components of the as Aedes aegypti. To date, all of these investigations have Aedes brain, namely the optic lobes, the subesophageal been carried out on adults but none of the studies addressed neuropil, and serotonergic system of the subesophageal the development of the nervous system during the larval and neuropil in more detail. Our study reveals prominent differ- pupal stages in mosquitoes. Here, we first screen a set of 30 ences in the developing brain in the larval stage as compared antibodies, which have been used to study brain develop- to the pupal (and adult) stage of Aedes. The results also ment in Drosophila, and identify 13 of them cross-reacting uncover interesting similarities and marked differences in and labeling epitopes in the developing brain of Aedes.We brain development of Aedes as compared to Drosophila. then use the identified antibodies in immunolabeling studies Taken together, this investigation forms the basis for future to characterize general neuroanatomical features of the cellular and molecular investigations of brain development in developing brain and compare them with the well-studied this important disease vector. Communicated by V. Hartenstein Keywords Aedes aegypti . Fruitfly. Brain development . Electronic supplementary material The online version of this article Optic lobes . Subesophageal ganglion (doi:10.1007/s00427-011-0376-2) contains supplementary material, which is available to authorized users. : : K. Mysore S. Flister H. Reichert (*) Introduction Biozentrum, University of Basel, Klinglebergstrasse 50, Mosquitoes are vectors for major parasitic diseases and CH-4056 Basel, Switzerland e-mail: [email protected] viral infections such as malaria, dengue, yellow fever, and encephalitis by feeding on blood from infected individuals P. Müller and transferring the disease agents to naïve hosts; hence, Swiss Tropical and Public Health Institute, control of the mosquito vectors is an important goal for Socinstrasse 57, CH-4002 Basel, Switzerland global health (Feachem et al. 2010). Host-seeking behavior in mosquitoes is based on chemosensation involving the P. Müller peripheral olfactory and gustatory sense organs as well as University of Basel, the central olfactory and gustatory circuitry of the brain. Petersplatz 1, CH-4003 Basel, Switzerland Since basic knowledge about the organization, function, and development of olfactory and gustatory systems in V. Rodrigues mosquitoes may improve the design of existing and allows National Centre for Biological Sciences, Tata Institute for to design novel disease control strategies (e.g., repellents, Fundamental Research, GKVK Campus, Bellary Road, traps), there has been considerable effort directed towards Bangalore 560065, India understanding the organization and function of the periph- 282 Dev Genes Evol (2011) 221:281–296 eral and central nervous system in mosquitoes (Anton et al. view of this molecular genetic similarity, it seems likely that 2003; Ignell et al. 2005; Ignell and Hansson 2005; Kwon et many of the antibody tools that were generated and used in al. 2006; Ghaninia et al. 2007a, b; Lu et al. 2007; Siju et al. the study of the development of the nervous system in 2008; Wang et al. 2010; Carey et al. 2010). These structural Drosophila might cross-react with the corresponding and functional studies of the nervous system have been epitopes and, thus, be useful molecular labels for investi- complemented by molecular analyses of the mosquito gating mosquito brains. Indeed, in two cases, antibodies olfactory and gustatory receptor molecules and, in more generated/used in Drosophila have been shown to cross- general terms, by the sequencing of the genomes of several react in adult mosquito nervous systems, and they have mosquito species (Fox et al. 2001; Hill et al. 2002; Melo et been utilized to understand the general neuroanatomy of the al. 2004; Bohbot et al. 2007; Lu et al. 2007; Arensburger et adult brain as well as specific types of neurons in the adult al. 2010). While a wealth of studies has investigated the chemosensory system of mosquitoes (Ignell et al. 2005; adult’s olfactory system, studies elucidating the develop- Ghaninia et al. 2007a, b; Siju et al. 2008). Taken together, ment of the sensory receptors or the central nervous these findings suggest that antibodies generated in Dro- circuitry involved in mosquito chemosensation during the sophila might be very helpful tools for understanding the larval stages are critically absent. As a consequence, development of the mosquito brain. virtually nothing is known about the development of the To obtain a suite of antibody markers that can be chemosensory system in mosquitoes. used to understand the various processes involved in In other insects such as the fruit fly, Drosophila the development of the mosquito brain in general (and melanogaster, the hawk moth, Manduca sexta, as well as the olfactory system in particular), we analyzed a set of in social insects such as ants and bees, molecular tools (e.g., 30 antibodies, which have been used to study brain antibodies) have been very useful for understanding the development in Drosophila, for cross-reactivity in the development of peripheral and central chemosensory developing brains of mosquito Aedes aegypti. Here, we systems (Oland and Tolbert 1996; Rodrigues and Hummel identify 13 of these antibodies that cross-react and label 2008; Groh and Rössler 2008; Mysore et al. 2010). epitopes in the developing mosquito brain. We then Notably, in the genetic model Drosophila, a wealth of characterize the general neuroanatomical features of the monoclonal and polyclonal antibodies generated against mosquitobrainrevealedbyeachofthesecross-reacting numerous molecular antigens involved in nervous system antibodies in immunolabeling studies in larval, pupal and development and function are currently available and have the adult mosquitoes and compare these features with been used extensively to understand the various aspects of those of fruit fly brains labeled with same antibodies. peripheral and central nervous system development, includ- Moreover, using these antibodies, we analyze the devel- ing olfactory system development (reviewed by Rodrigues opment of specific components of the brain (optic lobes, and Hummel 2008). In neuroanatomical respects, a major subesophageal neuropil, and serotonergic system of finding in Drosophila brain development is the fact that an subesophageal neuropil) in Aedes. Our analysis reveals identified set of neuroblasts generates all of the neurons in prominent differences in the neuroanatomy of the brain in the central brain in a lineage-specific manner. Most of the the larval stage as compared to the pupal and the adult lineally related neurons that derive from a given neuroblast stages. Our findings also document remarkable similari- have comparable morphological features and their axons ties and major differences in brain development of Aedes come together to form coherent fascicles that project as compared to Drosophila. Taken together, these find- together. Since a given lineage of neurons has a common ings form a basis for subsequent cellular and molecular projection trajectory, lineages therefore form “units of studies of brain development in the important disease projection” that underlie connectivity in the brain (Larsen vector Aedes. et al. 2009; Pereanu et al. 2011). An important open question is whether this lineage-based organizational principle also holds for other Dipteran insects. Material and methods Although fruitflies and mosquitoes are Dipteran insects, the two insect groups diverged about 250 million years ago Mosquito rearing and, thus, manifest considerable differences reflecting adaptation associated with different ecological niches and Eggs of A. aegypti Rockefeller strain were collected from a life strategies (Yeates and Wiegmann 1999; Gaunt and stock cage were reared at 27°C with about 70% humidity. Miles 2002). Nevertheless, it has been suggested that more The hatchlings were collected and reared separately at same than half of the genes in their genomes (Drosophila versus conditions and were fed with TetraMin® Baby (Tetra Anopheles) are putative orthologs with an average sequence GmbH, Melle, Germany) fish food. For the dissections identity of approximately 56% (Zdobnov et al. 2002). In and antibody cross-reactivity assays, mosquitoes were Dev Genes Evol (2011) 221:281–296 283 collected as fourth instar larvae, pupae (24 h after puparium The following antibodies were screened for cross-reactivity formation (APF)) pupae and 1-day-old adults. against the mosquito CNS: mouse anti-SYNORF 1 (1:10, DSHB); mouse BP 102 (1:5, DSHB); mouse 7E8A10 (1:10, Fly strains DSHB); mouse 8D12 (1:10, DSHB); mouse nc82 (1:100, Pielage
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