Abstract
Acetylcholinesterase (AChE) activity was topographically investigated in the presumptive cardiac conduction tissue regions visualized by HNK-1 immunoreactivity in rat embryos, and AChE-positive cells were examined with the electron microscope. On embryonic day (ED) 14.5, when HNK-1 was most intensely visualized, AChE activity could not be detected enzyme-histochemically in the conduction tissue regions, except in the ventricular trabeculae and part of the AV node. On ED 16.5, however, the AChE activity was clearly demonstrated in some parts of the developing conduction tissue. One exception was the AV node region, where an AChE-positive area was in close proximity to an area showing HNK-1 immunoreactivity but did not overlap. Furthermore, AChE activity was demonstrated predominantly in the ventricular trabeculae, including cardiac myocytes, but was rather weak in the atrium. With the electron microscope, AChE reaction products were observed predominantly intracellulary in both developing conduction tissue cells and developing ordinary myocytes, and no reactivity was found in neuronal components. From ED 18.5 until birth, both AChE activity and HNK-1 immunoreactivity faded away in the conduction tissue. Thus, transient AChE activity in the embryonic heart seems to be different from the developing adult form and may be related to a morphogenetic function in embryonic tissues, as proposed by other authors.
Similar content being viewed by others
References
Abo T, Balch CM (1981) A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1). J Immunol 127:1024–1029
Coraboeuf E, Obrecht-Coutris G, Le Douarin G (1970) Acetylcholine and the embryonic heart. Am J Cardiol 25:285–291
De Groot IJM, Sanders E, Visser SD, Lamers WH, De Jong F, Los JA, Moorman AFM (1987) Isomyosin expression in developing chicken atria: a marker for the development of conductive tissue? Anat Embryol 176:515–523
Drews U (1975) Cholinesterase in embryonic development. Prog Histochem Cytochem 7:1–52
Figueredo Da Silva J, Hosokawa T, Okada T, Kobayashi T, Seguchi H (1993) Localization of acetylcholinesterase activity in the mouse heart. Acta Histochem Cytochem 26:197–202
Finlay M, Anderson RH (1974) The development of cholinesterase activity in the rat heart. J Anat 117:239–248
Forsgren S, Carlsson E, Strehler E, Thornell L-E (1982) Ultrastructural identification of human fetal Purkinje fibres — a comparative immunocytochemical and electron microscopic study of composition and structure of myofibrillar M-regions. J Mol Cell Cardiol 14:437–449
Gomez H (1958) The development of the innervation of the heart in the rat embryo. Anat Rec 130:53–71
Gorza L, Schiaffino S, Vitadello M (1988) Heart conduction system: a neural crest derivative? Brain Res 457:360–366
Gyevai A (1969) Comparative histochemical investigations concerning prenatal and postnatal cholinesterase activity in the heart of chickens and rats. Acta Biol Acad Sci Hung 20:253–262
Hall EK (1951) Intrinsic contractility in the embryonic rat heart. Anat Rec 111:381–399
Hall EK (1957) Acetylcholine and epinephrine effects on the embryonic rat heart. J Cell Comp Physiol 49:187–200
Ikeda T, Iwasaki K, Shimokawa I, Sakai H, Ito H, Matsuo T (1990) Leu-7 immunoreactivity in human and rat embryonic hearts, with special reference to the development of the conduction tissue. Anat Embryol 182:553–562
Ito H, Iwasaki K, Ikeda T, Sakai H, Shimokawa I, Matsuo T (1992) HNK-1 expression pattern in normal and bis-diamine-induced malformed developing rat heart; three-dimensional reconstruction analysis using computer graphics. Anat Embryol 186:327–334
Kaehn K, Jacob HJ, Christ B, Hinrichsen K, Poelmann RE (1988) The onset of myotome formation in the chick. Anat Embryol 177:191–201
Karnovsky MJ, Roots L (1964) A “direct-coloring” thiocholine method for cholinesterase. J Histochem Cytochem 12:219–221
Lamers WH, Kortschot AT, Los JA, Moorman AFM (1987) Acetylcholinesterase in prenatal rat heart: a marker for the early development of the cardiac conductive tissue? Anat Rec 217:361–370
Lamers WH, Geerts WJC, Moorman AFM (1990) Distribution pattern of acetylcholinesterase in early embryonic chicken hearts. Anat Rec 228:297–305
Luider TM, Bravenboer N, Meijers C, Van der Kamp AWM, Tibboel D, Poelmann RE (1993) The distribution and characterization of HNK-1 antigens in the developing avian heart. Anat Embryol 188:307–316
Nakagawa M, Thompson RP, Terracio L, Borg TK (1993) Developmental anatomy of HNK-1 immunoreactivity in the embryonic rat heart: co-distribution with early conduction tissue. Anat Embryol 187:445–460
Navaratnam V (1965) The ontogenesis of cholinesterase activity within the heart and cardiac ganglia in man, rat, rabbit and guinea-pig. J Anat 99:459–467
Oettling G, Schmidt H, Drews U (1989) An embryonic Ca+ mobilizing muscarinic system in the chick embryo heart. J Dev Physiol 12:85–94
Owman CH, Sjoberg NO, Swedin G (1971) Histochemical and chemical studies on preand postnatal development of the different systems of “short” and “long” adrenergic neurons in peripheral-organs of the rat. Z Zellforsch Mikrosk Anat 116:319–341
Paff GH, Boucek RJ, Glander TP (1966) Acetylcholine-steraseacetylcholine, an enzyme system essential to rhythmicity in the preneural embryonic chick heart. Anat Rec 154:675–684
Sakai H, Ikeda T, Ito H, Nakamura T, Shimokawa I, Matsuo T (1994) Immunoelectron microscopic localization of HNK-1 in the embryonic rat heart. Anat Embryol 190:13–20
Sissman NJ (1970) Developmental landmarks in cardiac morphogenesis: comparative chronology. Am J Cardiol 25:141–148
Small DH (1990) Non-cholinergic actions of acetylcholinesterases: proteases regulating cell growth and development? Trends Biochem Sci 15:213–216
Tago H, Kimura H. Maeda T (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J Histochem Cytochem 34:1431–1438
Umezu Y, Yoshizuka M, Ueda H, Ogata H, Fujimoto S (1990) Acetylcholinesterase activity of developing muscles in the lower limb of the rat. Acta Anat 138:332–340
Vanittanakom P, Drews U (1985) Ultrastructural localization of cholinesterase during chondrogenesis and myogenesis in the chick limb bud. Anat Embryol 172:83–194
Viragh SZ, Challice CE (1983) The development of the early atrioventricular conduction system in the embryonic heart. Can J Physiol Pharmacol 61:775–792
Vitadello M, Matteoli M, Gorza L (1990) Neurofilament proteins are co-expressed with desmin in heart conduction system myocytes. J Cell Sci 97:11–21
Walker D (1975) Functional development of the autonomic innervation of the human fetal heart. Biol Neonate 25:31–43
Watanabe M, Timm M, Fallah-Najmabadi H (1992) Cardiac expression of polysialylated NCAM in the chicken embryo: correlation with the ventricular conduction system. Dev Dyn 194:128–141
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nakamura, T., Ikeda, T., Shimokawa, I. et al. Distribution of acetylcholinesterase activity in the rat embryonic heart with reference to HNK-1 immunoreactivity in the conduction tissue. Anat Embryol 190, 367–373 (1994). https://doi.org/10.1007/BF00187294
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00187294