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On the Morphology of the Drosophila Heart

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On the Morphology of the Drosophila Heart Journal of Cardiovascular Development and Disease Review On the Morphology of the Drosophila Heart Barbara Rotstein and Achim Paululat * Department of Zoology/Developmental Biology, University of Osnabrück, Osnabrück 49069, Germany; [email protected] * Correspondence: [email protected]; Tel.: +49-541-969-2861; Fax: +49-541-969-2587 Academic Editors: Rolf Bodmer and Georg Vogler Received: 25 January 2016; Accepted: 29 March 2016; Published: 12 April 2016 Abstract: The circulatory system of Drosophila melanogaster represents an easily amenable genetic model whose analysis at different levels, i.e., from single molecules up to functional anatomy, has provided new insights into general aspects of cardiogenesis, heart physiology and cardiac aging, to name a few examples. In recent years, the Drosophila heart has also attracted the attention of researchers in the field of biomedicine. This development is mainly due to the fact that several genes causing human heart disease are also present in Drosophila, where they play the same or similar roles in heart development, maintenance or physiology as their respective counterparts in humans. This review will attempt to briefly introduce the anatomy of the Drosophila circulatory system and then focus on the different cell types and non-cellular tissue that constitute the heart. Keywords: Drosophila melanogaster; cardiovascular system; heart; dorsal vessel; circulatory system 1. The Circulatory System of Flies Studying organogenesis and organ functionality requires basic knowledge of the functional anatomy of the organ itself. Herein, we will provide an introduction to Drosophila heart anatomy that will guide the reader through the very basic principles of Drosophila heart function and the cell types that constitute the cardiovascular system of the fly. Our review is especially aimed toward researchers who do not work primarily with the Drosophila model system. Therefore, we will not discuss the histology and morphogenesis of the heart in detail; instead, we will present a general overview, with selected histological data illustrating the Drosophila heart architecture. Moreover, the pictures shown were chosen as representatives of the available imaging methods that are widely used in the Drosophila system and that have been developed over the years since the seminal anatomical studies of Miller and Rizki [1,2]. 2. Low and High Hydrostatic Pressure Circulatory Systems: The Main Difference between Insects and Mammals In the animal kingdom there are two main types of circulatory systems that are in concordance with the metabolic requirements of their host, suggesting that each kind of circuit offers specific advantages (Figure1). Humans and other vertebrates, on the one hand, have a closed circulatory system, meaning that the blood is limited to vessels, never leaving the network of arteries, veins and capillaries, and is distinct from the interstitial fluid. Due to the elevated pressure that the blood generates inside the complex ramified network, this type of circulation is also called a high hydrostatic pressure system. It is a very efficient circuit that allows animals with high metabolic rates to stay active. Lower hydrostatic pressure systems, on the other hand, such as those found in many mollusks and all arthropods, are commonly associated with open circulatory systems that require less energy to be built and maintained. Drosophila melanogaster displays such an open circulatory system, with a simple tube-like heart that pumps the hemolymph from the posterior body region towards the anterior. J. Cardiovasc. Dev. Dis. 2016, 3, 15; doi:10.3390/jcdd3020015 www.mdpi.com/journal/jcdd J. Cardiovasc. Dev. Dis. 2016, 3, 15 2 of 13 J.simple Cardiovasc. tube-like Dev. Dis. heart2016, 3 ,that 15 pumps the hemolymph from the posterior body region towards2 ofthe 14 anterior. The hemolymph represents the interstitial fluid and is often called the insect “blood”, Thealthough hemolymph it lacks representsthe presence the of interstitial oxygen-transporting fluid and is oftenblood called cells. theIt directly insect “blood”, supplies although the organs it lackswith thenutrients, presence signal of oxygen-transporting peptides, and all kind blood of cells.metabolites, It directly hormones supplies and the organsmacrophages with nutrients, responsible signal for peptides,wound healing. and all kindIn addition, of metabolites, the hemolymph hormones contai and macrophagesns hemocytes responsible that secrete for extracellular wound healing. matrix In addition,(ECM) proteins the hemolymph [3,4] and also contains contribute hemocytes to the thatinsect secrete′s immune extracellular system. matrixGas exchange (ECM) and proteins transport [3,4] andis not also the contribute purpose of to the the heart, insect since1s immune insects system. harbor Gasa dedicated exchange tubular and transport network, is the not tracheal the purpose system, of thefor heart,this purpose. since insects harbor a dedicated tubular network, the tracheal system, for this purpose. FigureFigure 1.1. Comparison ofof thethe circulatorycirculatory systemsystem inin DrosophilaDrosophila andand humans.humans. 3.3. Histology Histology of of the the Fly Fly Heart Heart TheThe heartheart ofofDrosophila Drosophila, also, also known known as as the the dorsal dorsal vessel vessel due due to itsto spatialits spatial position position underneath underneath the dorsalthe dorsal epidermis epidermis (Figure (Figure2(A1,A2)), 2A1,A2), is built is early built during early embryogenesisduring embryogenesis by cardiomyocytes by cardiomyocytes arranged inarranged two opposing in two opposing rows of cells rows that of cells form that a luminal form a spaceluminal in space between in between (Figure3 )[(Figure5]. At 3) the[5]. endAt the of embryogenesis,end of embryogenesis, the heart beginsthe heart beating. begins Contraction beating. of Contraction cardiomyocytes of cardiomyocytes pumps the hemolymph pumps from the thehemolymph posterior from heart the chamber posterior into heart the aorta, chamber where into it leavesthe aorta, the heartwhere tube it leaves to spread the heart into thetube open to spread body cavity.into the During open body larval cavity. development, During thelarval animal developm growsent, dramatically the animal and grows increases dramatically in length and from increases 0.5 mm (embryo/firstin length from instar 0.5 mm larva) (embryo/first to approximately instar larva) 3–4 mm to (thirdapproximately instar wandering 3–4 mm larva).(third Atinstar the wandering same time, thelarva). heart At tube the elongatessame time, exclusively the heart tube through elongate cell growths exclusively and not through through cell cell growth proliferation, and not implying through thatcell theproliferation, larval heart implying tube harbors that the the same larval number heart of tube cells harbors as the embryonic the same heart number (Figure of2 (B1,B2))cells as [the6]. Nevertheless,embryonic heart during (Figure larval 2B1,B2) growth [6]. Nevertheless, a few new features during arise: larval the growth luminal a few heart new diameter features arise: expands the dramatically,luminal heart thediameter cardiomyocytes expands dramatically, grow in size the as mentionedcardiomyocytes above, grow and in many size as of mentioned the cells that above, are closelyand many associated of the withcells thethat embryonic are closely heart associated (pericardial with cells,the embryonic see below) heart disappear (pericardial [7–9]. Thecells, adult see heartbelow) (Figure disappear2(C1,C2)) [7–9]. differs The inadult several heart anatomical (Figure and2C1,C2) histological differs aspects in several from theanatomical larval heart and duehistological to specific aspects differentiation from the larval processes heart taking due to place specific during differentiation metamorphosis processes [1,2,10 taking]. These place processes during include,metamorphosis e.g., the formation[1,2,10]. These of new processes incurrent include, openings e.g., (ostia) the [formation11,12], the differentiationof new incurrent of additional openings intracardiac(ostia) [11,12], valves the [differentiation6,8], the differentiation of additional of the ventralintracardiac longitudinal valves muscle[6,8], the (VLM) differentiation layer underneath of the theventral heart longitudinal tube [13,14], muscle the remodeling (VLM) layer of the underneath terminal heart the heart chamber, tube and[13,14], the formationthe remodeling of neuronal of the innervationsterminal heart [15 chamber,,16]. and the formation of neuronal innervations [15,16]. J. Cardiovasc. Dev. Dis. 2016, 3, 15 3 of 14 J. Cardiovasc. Dev. Dis. 2016, 3, 15 3 of 13 Figure 2.Figure The 2.DrosophilaThe Drosophila heartheart at different at different developmental developmental stages: stages: (A1 ()A1 and) and (A2) show(A2) dorsoventralshow dorsoventral views ofviews late wild-type of late wild-type embryonic embryonic hearts. hearts. Figure Figure (A1)) shows shows an an immunostained immunostained embryo embryo with three with three different organ systems labeled. Heart cells were visualized with an anti-GFP antibody to detect GFP different organ systems labeled. Heart cells were visualized with an anti-GFP antibody to detect GFP expressed under the control of hand-GFP (green channel); somatic muscles were visualized with an expressedantibody under recognizing the controlβ3Tubulin of hand (red-GFP channel); (green and channel); the central somatic nervous systemmuscles
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