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Fine structure of the intercalated disc and cardiac junctions in the black widow spider Latrodectus mactans

  • Yan Sun (Department of Biological Sciences, Dankook University) ;
  • Seung-Min Lee (Department of Biological Sciences, Dankook University) ;
  • Bon-Jin Ku (Department of Biological Sciences, Dankook University) ;
  • Myung-Jin Moon (Department of Biological Sciences, Dankook University)
  • Received : 2020.08.07
  • Accepted : 2020.09.15
  • Published : 2020.12.31

Abstract

Arthropods have an open circulatory system with a simple tubular heart, so it has been estimated that the contractile pumping structure of the cardiac muscle will be less efficient than that of vertebrates. Nevertheless, certain arthropods are known to have far superior properties and characteristics than vertebrates, so we investigated the fine structural features of intercalated discs and cardiac junctions of cardiac muscle cells in the black widow spider Latrodectus mactans. Characteristically, the spider cardiac muscle has typical striated features and represents a functional syncytium that supports multiple connections to adjacent cells by intercalated discs. Histologically, the boundary lamina of each sarcolemma connects to the basement membrane to form an elastic sheath, and the extracellular matrix allows the cells to be anchored to other tissues. Since the intercalated disc is also part of sarcolemma, it contains gap junctions for depolarization and desmosomes that keep the fibers together during cardiac muscle contraction. Furthermore, fascia adherens and macula adherens (desmosomes) were also identified as cell junctions in both sarcolemma and intercalated discs. To enable the coordinated heartbeat of the cardiac muscle, the muscle fibers have neuronal innervations by multiple axons from the motor ganglion.

Keywords

Acknowledgement

This work was partly supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (NRF-2019R1I1A3A01062105).

References

  1. R.H. Adams, A. Schwartz, Comparative mechanisms for contraction of cardiac and skeletal muscle. Chest 78, 123-139 (1980)
  2. P.M. Bennett, Riding the waves of the intercalated disc of the heart. Biophys. Rev. 10, 955-959 (2018)
  3. C.M. Borrmann, C. Grund, C. Kuhn, I. Hofmann, S. Pieperhoff, W.W. Franke, The area composita of adhering junctions connecting heart muscle cells of vertebrates. II. Colocalizations of desmosomal and fascia adherens molecules in the intercalated disk. Eur. J. Cell Biol. 85, 469-485 (2006)
  4. C.R. Bursey, R.G. Sherman, Spider cardiac physiology. I. Structure and function of the cardiac ganglion. Comp. Gen. Pharmacol. 1, 160-170 (1970)
  5. R. Craig, J.L. Woodhead, Structure and function of myosin filaments. Curr. Opin. Struct. Biol. 16, 204-212 (2006)
  6. E. Delva, D.K. Tucker, A.P. Kowalczyk, The desmosome. Cold Spring Harb. Perspect. Biol. 1, a002543 (2009)
  7. M. Dewey, in Comparative Physilogy of the Heart: Current Trends, ed. by F. V. McCann. The structure and function of the intercalated disc in vertebrate cardiac muscle (Basel, Springer, 1969), pp. 10-28
  8. E. Ehler, Cardiac cytoarchitecture - why the "hardware" is important for heart function! Biochim. Biophys. Acta 1863, 1857-1863 (2016)
  9. D.W. Fawcett, N.S. McNutt, The ultrastructure of the cat myocardium. I. Ventricular papillary muscle. J. Cell Biol. 42, 1-45 (1969)
  10. R.F. Foelix, Biology of Spiders, 3rd edn. (Oxford University Press, Oxford, 2011)
  11. M.S. Forbes, N. Sperelakis, Intercalated discs of mammalian heart: a review of structure and function. Tiss. Cell 17, 605-648 (1985)
  12. W.W. Franke, C.M. Borrmann, C. Grund, S. Pieperhoff, The area composita of adhering junctions connecting heart muscle cells of vertebrates (I) molecular definition in intercalated disks of cardiomyocytes by immunoelectron microscopy of desmosomal proteins. Eur. J. Cell Biol. 85, 69-82 (2006)
  13. D. Garrod, C. Martyn, Desmosome structure, composition and function. Biochimica et Biophysica Acta 1778, 572-587 (2008)
  14. D.A. Goodenough, D.L. Paul, Gap junction. Cold Spring Harb. Perspect. Biol. 1, a002576 (2009)
  15. S. Goossens, B. Janssens, S. Bonne, R. de Rycke, F. Braet, J. van Hengel, F. van Roy, A unique and specific interaction between αT-catenin and plakophilin-2 in the area composita, the mixed-type junctional structure of cardiac intercalated discs. J. Cell Sci. 120, 2126-2136 (2007)
  16. A.M. Gordon, E. Homsher, M. Regnier, Regulation of contraction in striated muscle. Physiol. Rev. 80, 853-924 (2000)
  17. R.G. Gourdie, C.R. Green, N.J. Severs, Gap junction distribution in adult mammalian myocardium revealed by an anti-peptide antibody and laser scanning confocal microscopy. J. Cell Sci. 99, 41-55 (1991)
  18. D.E. Gutstein, F. Liu, M.B. Meyers, A. Choo, G.I. Fishman, The organization of adherens junctions and desmosomes at the cardiac intercalated disc is independent of gap junctions. J. Cell Sci. 116, 875-885 (2003)
  19. A. Hartsock, W. James, Nelson, Adherens and tight junctions: Structure, function and connections to the actin cytoskeleton. Biochem. Biophys. Acta 1778, 660-669 (2007)
  20. G. Hoyle, Comparative aspects of muscle. Annu. Rev. Physiol. 31, 43-84 (1969)
  21. G.K. Isbister, M.R. Gray, Latrodectism: a prospective cohort study of bites by formally identified redback spiders. Med. J. Aust. 179, 88-91 (2003)
  22. S. Kawaguti, Electron microscopic study on the cardiac muscle of the horseshoe crab (Tachypleus tridentatus leach). Biol. J. Okayama Univ. 9, 11-26 (1963)
  23. H. Kim, M.J. Moon, Fine structure of cardiac sarcomeres in the black widow spider Latrodectus mactans. Ent. Res. 48, 429-438 (2018)
  24. Y.S. Lee, T.S. Hsu, Relationship between reestablishment of sarcolemmaglycocalyx ultrastructures and restoration of transmembrane potentials in cultured rat heart cells. J. Electrocardiol. 20, 303-311 (1987)
  25. R.A. Leyton, E.H. Sonnenblick, Cardiac muscle of the horseshoe crab, Limulus polyphemus (I) ultrastructure. J. Cell Biol. 48, 101-119 (1971)
  26. Z. Maretic, in Ecophysiology of Spiders, ed. by W. Nentwig. Spider venom and their effect (Berlin, Springer-Verlag, 1987), pp. 142-159
  27. N.S. McNutt, Ultrastructure of the myocardial sarcolemma. Circul. Res. 37, 1-13 (1975)
  28. W. Meng, M. Takeichi, Adherens junction: Molecular architecture and regulation. Cold Spring Harb. Perspect. Biol. 1, a002899 (2009)
  29. M.J. Moon, Fine structure of the aggregate silk nodules in the orb-web spider Nephila clavata. Anim. Cells Sys. 22, 421-428 (2018)
  30. M.J. Moon, E.K. Tillinghast, Immunoreactivity of glutamic acid decarboxylase (GAD) isoforms in the central nervous system of the barn spider, Araneus cavaticus. Ent. Res. 43, 47-54 (2013)
  31. H.S. Moss, L.S. Binder, A retrospective review of black widow spider envenomation. Ann. Emerg. Med. 16, 188-192 (1987)
  32. R. Paniagua, M. Royuela, R.M. Garcia-Anchuelo, B. Fraile, Ultrastructure of invertebrate muscle cell types. Histol. Histopathol. 11, 181-201 (1996)
  33. M.E. Peterson, Black widow spider envenomation. Clin. Tech. Small Anim. Pract. 21, 187-190 (2006)
  34. M. Pruna, E. Ehler, The intercalated disc: A mechanosensing signalling node in cardiomyopathy. Biophys. Rev. (2020). https://doi.org/10.1007/s12551-020-00737-x
  35. N.J. Severs, Gap junction shape and orientation at the cardiac intercalated disk. Circul. Res. 65, 1458-1465 (1989)
  36. R.G. Sherman, in Neurobiology of Arachnids, ed. by F. G. Barth. Neural control of the heartbeat and skeletal muscle in spiders and scorpions (Berlin, Springer-Verlag, 1987), pp. 319-336
  37. R.G. Sherman, R.A. Pax, The heartbeat of the spider Geolycosa missouriensis. Comp. Biochem. Physiol. 26, 529-536 (1968)
  38. T. Shimada, H. Kawazato, A. Yasuda, N. Ono, K. Sueda, Cytoarchitecture and intercalated disks of the working myocardium and the conduction system in the mammalian heart. Anat Rec A Discov Mol Cell Evol Biol 280, 940-951 (2004)
  39. J.R. Sommer, R.A. Waugh, Ultrastructure of heart muscle. Environ. Health Persp. 26, 159-167 (1978)
  40. R.J. Stenger, D. Spiro, The ultrastructure of mammalian cardiac muscle. J. Biophy. Biochem. Cytol. 9, 325-351 (1961)
  41. Y. Sun, H.J. Kim, M.J. Moon, Fine structure of the cardiac muscle cells in the orb-web spider Nephila clavata. Appl. Microsc. (2020). https://doi.org/10.1186/s42649-020-00030-x
  42. P.K. Timms, R.B. Gibbons, Latrodectism - effects of the black widow spider bite. West J. Med 144, 315-317 (1986)
  43. J. Ude, K. Richter, The submicroscopic morphology of the heart ganglion of the spider Tegenaria atrica (C.L. Koch) and its neuroendocrine relations to the myocard. Comp. Biochem. Physiol. 48A, 301-308 (1974)
  44. J.H. van Weerd, V.M. Christoffels, The formation and function of the cardiac conduction system. Development 143, 197-210 (2016)
  45. R. Veeraraghavan, S. Poelzing, R.G. Gourdie, Intercellular electrical communication in the heart: A new, active role for the intercalated disk. Cell Commun. Adhes. 21, 161-167 (2014)
  46. R.S. Vetter, G.K. Isbister, Medical aspects of spider bites. Annu. Rev. Entomol. 53, 409-429 (2008)
  47. R.S. Wilson, The heartbeat of the spider Heteropoda venatoria. J. Insect Physiol. 13, 1309-1326 (1967)
  48. C.S. Wirkner, Richter, evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). Cladistics 26, 143-167 (2010)
  49. C.S. Wirkner, M. Toegel, G. Pass, in Arthropod Biology and Evolution: Molecules, Development, Morphology, ed. by A. Minelli et al.. The arthropod circulatory system (Heidelberg, Springer, 2013), pp. 343-391
  50. G. Zhao, Y. Qiu, H.M. Zhang, et al., Intercalated discs: Cellular adhesion and signaling in heart health and diseases. Heart Fail. Rev. 24, 115-132 (2019)