Abstract
We have followed the normal development of the different cell types associated with the Drosophila dorsal vessel, i.e. cardioblasts, pericardial cells, alary muscles, lymph gland and ring gland, by using several tissue-specific markers and transmission electron microscopy. Precursors of pericardial cells and cardioblasts split as two longitudinal rows of cells from the lateral mesoderm of segments T2-A7 (“cardiogenic region”) during stage 12. The lymph gland and dorsal part of the ring gland (corpus allatum) originate from clusters of lateral mesodermal cells located in T3 and T1/dorsal ridge, respectively. Cardioblast precursors are strictly segmentally organized; each of T2-A6 gives rise to six cardioblasts. While moving dorsally during the stages leading up to dorsal closure, cardioblast precursors become flattened, polarized cells aligned in a regular longitudinal row. At dorsal closure, the leading edges of the cardioblast precursors meet their contralateral counterparts. The lumen of the dorsal vessel is formed when the trailing edges of the cardioblast precursors of either side bend around and contact each other. The amnioserosa invaginates during dorsal closure and is transiently attached to the cardioblasts; however, it does not contribute to the cells associated with the dorsal vessel and degenerates during late embryogenesis. We describe ultrastructural characteristics of cardioblast differentiation and discuss similarities between cardioblast development and capillary differentiation in vertebrates.
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Ashburner M (1989) Drosophila. A laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor
Beer J, Technau GM, Campos-Ortega JA (1987) Lineage analysis of transplanted individual cells. IV. Commitment and proliferative capabilities of mesodermal cells. Roux's Arch Dev Biol 196:222–230
Bier E, Vaessin H, Shepherd S, Lee K, McCall K, Barbel S, Ackerman L, Carretto R, Uemura T, Grell E, Jan LY, Jan YN (1989) Searching for pattern and mutation in the Drosophila genome with a P-IacZ vector. Genes Dev 3:1273–1287
Bogaert T, Brown N, Wilcox M (1987) The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments. Cell 51:929–940
Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York
Corbin V, Michelson AM, Abmayr SM, Neel B, Alcamo E, Maniatis T, Young MW (1991) A role for the Drosophila neurogenic genes in mesoderm differentiation. Cell 67:311–323
Crossley AC (1985) Nephrocytes and pericardial cells. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry, and pharmacology, vol 3. Pergamon Press, Oxford
Dejana E, Colella S, Abbadini M, Gaboli M, Marchisio PC (1988) Fibronectin and vitronectin regulate the organization of their respective Arg-Gly-Asp adhesion receptors in cultured human endothelial cells. J Cell Biol 107:1215–1223
Edwards GA, Challice CE (1960) The ultrastructure of the heart of the cockroach, Blatella germanica. Ann Entomol Soc Amer 53:369–383
Fessler LL, Campbell AG, Duncan KG, Fessler JH (1987) Drosophila laminin: characterization and distribution. J Cell Biol 105:2383–2391
Folkman J, Haudenschild C (1980) Angiogenesis in vitro. Nature 288:551–556
Franke WW, Cowin P, Grund C, Kuhn C, Kapprell HP (1988) The endothelial junction. The plaque and its components. In: Simionescu N, Simionesu M (eds) Endothelial cell biology in health and disease. New York, Plenum
Furcht LT (1986) Critical factors controlling angiogenesis: cell products, cell matrix, and growth factors. Lab Invest 55:505–509
Grant DS, Kleinman HK, Martin GR (1989a) The role of basement membranes in vascular development. NY Acad Sci 588:61–72
Grant DS, Tashiro K, Segui-Real B, Yamada Y, Martin GR, Kleinman HK (1989b) Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell 58:933–943
Grant DS, Lelkes PI, Fukuda K, Kleinman H (1991) Intracellular mechanisms involved in basement membrane induced blood vessel differentiation in vitro. Dev Biol 27A:327–336
Hama C, Ali Z, Kornberg TB (1990) Region-specific recombination and expression are directed by portions of the Drosophila engrailed promoter. Genes Dev 4:1079–1093
Hartenstein V, Jan YN (1992) Studying Drosophila embryogenesis with P-lacZ enhancer trap lines. Roux's Arch Dev Biol 201:194–220
Hartenstein AY, Rugendorff AE, Tepass U, Hartenstein V (1992) The function of the neurogenic genes during epithelial development in the Drosophila embryo. Development 116:1203–1220
Ingber DE, Folkman J (1989) Mechanochemical switching between growth and differentiation during Fibroblast Growth Factor-stimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol 109:317–330
Ingham PW, Martinez-Arias A (1992) Boundaries and fields in early embryos. Cell 68:221–235
Jensen H (1977) Ultrastructure of the myocardial cell and its membrane systems in the adult fly Calliphora erythrocephala (Insecta: Diptera). Cell Tissue Res 180:293–302
Jones JC (1977) The circulatory system of insects. C.C. Thomas, Springfield
Kessel RG (1960) Electron microscope observations on the submicroscopic vesicular component of the subesophageal body and pericardial cells of the grasshopper, Melanoplus differentialis differentialis (Thomas). Exp Cell Res 22:108–119
Kiehart DP, Feghali R (1986) Cytoplasmic myosin from Drosophila melanogaster. J Cell Biol 103:1517–1525
King RC, Aggarwal SK, Bodenstein D (1966) The comparative submicroscopic morphology of the ring gland of Drosophila melanogaster during the second and third larval instars. Z Zellforsch 73:272–285
Kleinman HK, Klebe RJ, Martin GR (1981) Role of collagenous matrices in the adhesion and growth of cells. J Cell Biol 88:473–485
Korotnier A (1883) Entwicklung des Herzens bei Gryllotalpa. Zool Anz 6 [cited in Schroeder C (ed) (1925) Handbuch der Entomologie, vol 1. Gustav Fischer, Jena, pp 788–796]
Kowalevsky A (1892) Sur les organs excreteurs chez les Arthropodes terrestres. Congr Int Zool (2) Moscow 1:187–234
Kubota Y, Kleinman HK, Martin GR, Lawley TJ (1988) Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J Cell Biol 107:1589–1598
Lane NJ, Flores V (1990) The role of cytoskeletal components in the maintenance of intercellular junctions in an insect. Cell Tissue Res 262:373–385
Leptin M, Bogaert T, Lehmann R, Wilcox M (1989) The function of PS Integrins during Drosophila embryogenesis. Cell 56:401–408
Lunstrum GP, Baechinger HP, Fessler LL, Duncan KG, Nelson RE, Fessler JH (1988) Drosophila basement membrane procollagen IV. I. Protein characterization and distribution. J Biol Chem 263:18318–18327
Maciag T, Kadish J, Wilkins L, Stemerman MB, Weinstein R (1982) Organizational behavior of human umbilical vein endothelial cells. J Cell Biol 94:511–520
Montell DJ, Goodman CS (1989) Drosophila laminin: sequence of B2 subunit and expression of all three subunits during embryogenesis. J Cell Biol 109:2441–2453
Myklebust R (1975) The ultrastructure of the myocardial cell in the dragonfly Aeschna juncea (L.). Norw J Zool 23:17–36
Poulson DF (1950) Histogenesis, organogenesis, and differentiation in the embryo of Drosophila melanogaster (Meigen). In: Demerec M (ed) Biology of Drosophila. Wiley, New York, pp 168–274
Ray RP, Arora K, Nüsslein-Volhard C, Gelbart WM (1991) The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development 113:35–54
Rizki TM (1978) The circulatory system and associated cells and tissues. In: Ashburner M, Wright TRF (eds) Genetics and biology of Drosophila, vol 2b. Academic Press, New York, pp 397–452
Rothberg JM, Jacobs JR, Goodman CS, Artavanis-Tsakonas S (1990) slit: an extracellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev 4:2169–2187
Schroeder C (1925) Handbuch der Entomologie, vol 1. Gustav Fischer, Jena, pp 788–796
Sedlak BJ, Whitten J (1976) Changes in heart ultrastructure during development of the flesh fly Sarcophaga bullata. Dev Biol 54:308–313
Snodgrass RE (1935) Principles of insect morphology. McGraw-Hill, New York, pp 311–315
Tadkowski TM, McCann FV (1980a) Embryonic development of an insect myocardium. Experientia 36:105–107
Tadkowski TM, McCann FV (1980b) Ultrastructure and electrical activity in developing heart cells (Insect). Dev Biol 74:387–400
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Correspondence to: V. Hartenstein
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Rugendorff, A., Younossi-Hartenstein, A. & Hartenstein, V. Embryonic origin and differentiation of the Drosophila heart. Roux's Arch Dev Biol 203, 266–280 (1994). https://doi.org/10.1007/BF00360522
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DOI: https://doi.org/10.1007/BF00360522