Characterization of fat body cells at different developmental stages of Culex pipiens
Introduction
The fat body is often described as a tissue consisting of layers or ribbons of a few cell thicknesses. It possesses mesodermal origin and shows high biosynthetic activity (Resh and Cardé, 2009; Arrese and Soulages, 2010; Martins et al., 2011a; Chapman, 2013; Assis et al., 2014). Fat body, which is a storage and secretory organ, has many metabolic functions, which change as the embryonic development of the insect progresses. It plays an important role in the intermediate metabolism and in the metabolism of macromolecules (proteins, lipids and carbohydrates) (Wigglesworth, 1942; Feitosa et al., 2006; Alves et al., 2010; Chapman, 2013; Park et al., 2013; Zhang and Xi, 2014; Nation, 2016), which provide energy to insects for reproduction and movement (Arrese and Soulages, 2010; Roma et al., 2010; Martins et al., 2011b; Pascini et al., 2011; Furtado et al., 2013; Assis et al., 2014; Li et al., 2019). Due to its metabolic functions, the fat body is often described as equivalent to vertebrate liver (Chapman, 2013; Azeez et al., 2014; Zhang and Xi, 2014; Li et al., 2019). It is involved in synthesis, absorption and storage of nutrients from hemolymph (Roma et al., 2010). In addition to these functions; some studies showed that the fat body is also responsible for the production of immunological system components, antibacterial compounds and blood clotting proteins (Vilmos and Kurucz, 1998; Feitosa et al., 2006; Araújo et al., 2008; Martins and Pimenta, 2008; Azeez et al., 2014), and is a major endocrine organ of insects as it secretes insect growth factors (IDGFs, ADGFs) and has a key role in the synthesis of the insect molting hormone, 20-hydrocydysone (20E). Furthermore, it has an important role in ensuring proper energy homeostasis (Resh and Cardé, 2009; Chapman, 2013).
Even though the fat body is usually found intensively in the abdomen of the insects, it shows distribution throughout the body cavity (Imms, 1908; Snodgrass, 1935; Dean et al., 1985; Aguila et al., 2007; Martins and Pimenta, 2008; Pascini et al., 2011; Park et al., 2013; Assis et al., 2014). In several holometabolous insects, it is divided into two types with respect to its location in the body cavity: peripheral (subcuticular, parietal) fat body and perivisceral (visceral, abdominal) fat body. The peripheral fat body is located just beneath the integument and in the vicinity of the muscle system. On the other hand, the perivisceral fat body is found around the organs, especially the digestive tract (Haunerland and Shirk, 1995; Martins and Pimenta, 2008; Roma et al., 2010; Chapman, 2013; Klowden, 2013; Assis et al., 2014).
The trophocytes, the basic cells of the fat body, are round or polygonal in shape and have large irregular nucleus (Richards and Davies, 1977; Resh and Cardé, 2009; Roma et al., 2010). The other fat body cell types are mycetocytes, urate cells, hemoglobin cells, and chromatocytes (Snodgrass, 1935; Haunerland and Shirk, 1995; Clements, 2000; Gillott, 2005; Arrese and Soulages, 2010; Chapman, 2013; Furtado et al., 2013; Nation, 2016). There are also oenocytes associated with fat body. The oenocytes are of ectodermal origin and their location, size and number varies with species (Snodgrass, 1935; Arrese and Soulages, 2010; Roma et al., 2010; Martins and Ramalho-Ortigão, 2012; Furtado et al., 2013; Assis et al., 2014; Makki et al., 2014).
A recent review indicates that there are more than 2000 peer reviewed papers published on the biology of the fat body within the last decade. This sharp increase in the interest on fat body is partially due to the recent findings on comparative genomics studies revealing about 65% homology between the disease causing genes in humans and their functional homologs in insects. This, in turn, led to the use of insect model organisms for their fat body tissue in studying human metabolic disorders and immune diseases. There are few insects species used as model organisms for their fat bodies; like, Drosophila melanogaster, Bombyx mori, Helicoverpa armigera, Aedes aegypti, Locusta migratoria, and Blatta germanica (Li et al., 2019 and the references therein). Before using the fat body tissue as a model for human health studies, it must first be well characterized. Apart from these model organism studies; there are some histological studies on characterization and distribution of the fat body in some insects [like A. aegypti (Diptera) (Martins et al., 2011c), A. maculipennis (Diptera) (Imms, 1908; Martins and Ramalho-Ortigão, 2012), L. longipalpis (Diptera) and P. papatasi (Diptera) (Assis et al., 2014), M. quadrifasciata (Hymenoptera) (Furtado et al., 2013), P. americana (Blattoptera) (Park et al., 2013), T. theobaldi (Diptera) (Pascini et al., 2011)] at different developmental stages in order to understand its physiology and its roles in metabolic activities. Moreover, there are some studies on the effects of different feeding behaviors on the fat body tissue (Martins and Pimenta, 2008; Martins et al., 2011c). These comparative histological and histochemical studies are invaluable in understanding the fat body biology, physiology and its role in insect metabolic pathways.
Culex pipiens, a holometabolous insect species, is an important threat to public health as they can spread diseases in the world. Understanding their physiology at different stages of their life cycles may contribute to develop effective strategies managing the C. pipiens populations and spread of the diseases. However, there is no comparative study in the literature on the characterization and distribution of the fat body tissue across different stages of C. pipiens species. In this study, it is aimed at; (i) determining the cell types contained in the fat body of C. pipiens, and (ii) identifying the macromolecules (lipids, proteins and carbohydrates) contained in each of these cell types by using different histochemical techniques during different developmental stages.
Section snippets
Materials and methods
A population of Culex pipiens (L.) was established in our laboratory, in September 2000, using individuals collected from Menemen Region, İzmir, Turkey. The population has been maintained since then. For the experiments, the C. pipiens larvae were fed on chicken liver and adults were fed on cotton soaked with 10% sucrose solution. Meanwhile, the insects were maintained at 25 °C, 65–70% humidity with a 12 h/12 h daily light/dark cycle, respectively.
The histological study was conducted on the
Results
The histological preparations were compared based on some particular features in order to minimize any possible miscomparison between the different stages. These features were; (i) head, thorax, both end of the abdomen for the 4th stage larvae, (ii) cephalothorax (thorax part), both ends of the abdomen for the early and late pupae, (iii) head, thorax, both end of the abdomen for the adults. In all stages, each region of the sample was examined carefully. The trophocytes and the oenocytes were
Presence and distribution of fat body at different stages
Among all the possible cell types that can be found in fat body, only spherical-shaped trophocytes and oenocytes were observed in Culex pipiens (Diptera) samples of different developmental stages in the present study. These results were in parallel to the findings on Aedes aegypti (Diptera), another mosquito species, in which only the same two cell types were found in its fat body (Martins and Pimenta, 2008; Martins et al., 2011a, 2011b; 2011c). There are other fat body cells that were observed
Funding
This research was funded by the Ege University Scientific Research Fund (18 FEN 021).
Acknowledgements
We are sincerely grateful to Dr. Mehmet Salih Yıkılmaz for his endless support in providing the samples and his help in the laboratory analyses. We also would like to thank Dr. Evren Koban Baştanlar for critical reading and to Youchahou Poutougnigni for proofreading. Last but not least, we would like to express our gratitude to our two anonymous peer reviewers for their constructive comments on our manusript.
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