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Some ultrastructural features of the myocardial cells in the hypertrophied human papillary muscle

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Summary

An ultrastructural study using various electron microscopical techniques has been conducted on biopsy material from the hypertrophied papillary muscle of the human heart. About 75% of the myocardial cells were classified as hypertrophic with diameters ranging from 15 εm to 53 εm. The increased cell diameter appeared to be the result of an elevated amount of mitochondria and contractile material. The hypertrophied myocytes displayed a general ultrastructural organization in many ways similar to that of the normal sized myocytes. However, the former cells were characterized by focal deposits of excess laminar coat material and abnormal Z-band patterns as well as of multiple intercalated discs. The preferential sites for the production of new sarcomere elements appeared to be in the subsarcolemmal and intercalated disc regions. Adjacent myocardial cells were interconnected by collagen bundles, and, by an elaborate collagen-fibril-microthread-granule lattice. The surface folds were linked to each other by surface cables, which probably constituted a separate category of extracellular material of unknown function. Intramembranous particles were abundant in the sarcolemma proper but scarce in the membranes of the sarcoplasmic vesicles. Such particles were also observed in the lipofuscin granular membrane and in the membranes surrounding the lipid droplets. A framework of transverse cytoskeletal filaments interconnected the Z-bands of adjacent myofibrils and anchored the contractile material to the sarcolemma as well as to the nucleus. A large and lobulated nucleus containing well developed nucleoli together with an abundance of sarcoplasmic free and membrane-attached ribosomes, were interpreted as morphological signs of enhanced synthetic activity in the hypertrophied cell. Degenerative phenomena on the other hand were confined to lysosomal degeneration of worn-out cell constituents that were manifested by the numerous lysosomes and aggregates of lipofuscin granules. Abnormal Z-band patterns as seen in the present material were interpreted as an initial stage in the formation of new contractile elements.

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References

  1. Adomian GE, Laks MM, Morady F, Swan HJC (1974) Significance of the multiple intercalated disc in the hypertrophied canine heart. J Molec Cell Cardiol 6:105–109

  2. Behnke O (1967) Some possible practical implications of the lability of blood platelet microtubules. Vox Sang 13:502–507

  3. Bishop SP, Cole CR (1969) Ultrastructural changes in the canine myocardium with right ventricular hypertrophy and congestive heart failure. Lab Invest 20:219–229

  4. Borg TK, Caulfield JB (1979) Collagen in the heart. Texas Rep Biol Med 39:321–333

  5. Borg TK, Sullivan T, Ivy J (1982) Functional arrangement of connective tissue in striated muscle with emphasis on cardiac muscle. Scan Electr Microsc IV:1775–1784

  6. Boyde A (1978) Pros and cons of critical point drying and freeze drying for SEM. Scan Electr Microsc II:303–314

  7. Breisch EA (1982) Myocardial lysosomes in pressure-overload hypertrophy. Cell Tissue Res 223:615–625

  8. Breisch EA, White FC, Bloor CM (1984) Myocardial characteristics of pressure overload hypertrophy. A structural and functional study. Lab Invest 51:333–342

  9. Caceci T, Orenstein JM, Bloom S (1981) Surface cables of vertebrate muscle cells. Scan Electr Microsc III:115–123

  10. Carrascal E, Leon L, Alexandre C (1981) Caveolae system in the myocardium of the rat. Morphol Normal y Patol Sec A 5:121–128

  11. Caulfield JB, Borg TK (1979) The collagen network of the heart. Lab Invest 40:364–372

  12. Colborn GL, Carsey jr E (1972) Electron microscopy of the sinoatrial node of the squirrel monkey Saimiri sciureus. J Molec Cell Cardiol 4:525–536

  13. Cluzeaud F, Perrenec J, De Amoral E, Willenium M, Hatt PY (1984) Myocardial cell nucleus in cardiac overloading in the rat. Eur Heart J 5 (Suppl. F):271–280

  14. Dalen H (1987) An ultrastructural study of myocardial cell mitochondria in the hypertrophied human papillary muscle. Virchows Archiv [Pathol Anat] (submitted)

  15. Dalen H, Myklebust R, Sætersdal TS (1978) Cryofracture of paraffin-embedded heart muscle cells. J Microsc 112:139–151

  16. Dalen H, Scheie P, Myklebust R, Sætersdal T (1983) An ultrastructural study of cryofractured myocardial cells with special attention to the relationship between mitochondria and sarcoplasmic reticulum. J Microsc 131:35–46

  17. Dalen H, Ødegården S, Sæterdal TS (1987) The application of various electron microscopic techniques for ultrastructural characterization of the human papillary heart muscle cell in biopsy material. Virchows Arch [Pathol Anat] 410:265–279

  18. Ericsson JLE, Brunk UT, Arborgh B (1978) Fixation. In: Johannessen JV (ed) Electron Microscopy in Human Medicine, vol 1, McGraw-Hill International Book Company, New York, p. 99

  19. Ferrans VJ, Maron BJ, Buja LM, Ali N, Roberts WC (1975) Intranuclear glycogen deposists in human cardiac muscle cells: Ultrastructure and cytochemistry. J Molec Cell Cardiol 7:373–386

  20. Ferrans VJ, Morrow AG, Roberts WC (1972) Myocardial ultrastructure in idiopathic hypertrophic subaortic stenosis. A study of operatively exised left ventricular outflow tract muscle in 14 patients. Circulation 45:769–792

  21. Ferrans VJ, Roberts WC (1973) Intermyofibrillar and nuclear-myofibrillar connections in human and canine myocardium. An ultrastructural study. J Mole Cell Cardiol 5:247–257

  22. Forbes MS, Sperelakis N (1976) The presence of transverse and axial tubules in the ventricular myocardium of embryonic and neonatal guinea pigs. Cell Tissue Res 166:83–90

  23. Forbes MS, Sperelakis N (1980) Structures located at the levels of the Z-bands in mouse ventricular myocardial cells. Tissue & Cell 12:467–489

  24. Forbes MS, Sperelakis N (1983) The membrane systems and cytoskeletal elements of mammalian myocardial cells. In: Dowben RM, Shay JW (eds) Cell and Muscle Mobility, vol. 3. Plenum Press, New York, p. 89

  25. Forbes MS, Sperelakis N (1984) Ultrastructure of the mammalian cardiac muscle. In: Sperelakis N (ed) Function of the Heart in Normal and Pathological States. Martinus Nijhoff, The Hague, p. 3

  26. Gabella G (1978) Inpocketings of the cell membrane (caveolae) in the rat myocardium. J Ultrastruct Res 65:135–147

  27. Goldstein MA, Entman ML (1979) Microtubules in mammalian heart muscle. J Cell Biol 80:183–195

  28. Goldstein MA, Sordahl LA, Schwartz A (1974) Ultrastructural analysis of left ventricular hypertrophy in rabbits. J Mol Cell Cardiol 6:265–273

  29. Jones M, Ferrans VJ (1979) Myocardial ultrastructure in children and adults with congenital heart disease. In: Roberts WC (ed) Congenital Heart Disease in Adults. F.A. Davis Company, Philadelphia, p. 501

  30. Kajihara H, Taguchi K, Hara H, Iijima S (1973) Electron microscopic observation of human hypertrophied myocardium. Acta Pathol Jpn 23:335–347

  31. Kawamura K (1982) Cardiac hypertrophy. Scanned architecture, ultrastructure and cytochemistry of myocardial cells. Jpn Circ J 46:1012–1030

  32. Koobs DH, Schultz RL, Jutzy RV (1978) Origin of lipofuscin and possible consequences to myocardium. Arch Pathol Lab Med 102:66–68

  33. Laks MM, Morady F, Adomian GE, Swan HJC (1970) Presence of widened and multiple intercalated discs in the hypertrophied canine heart. Circ Res 27:391–402

  34. Lazarides E (1980) Intermediate filaments as mechanical integrators of cellular space. Nature 283:249–256

  35. Legato MJ (1970) Sarcomerogenesis in human myocardium. J Mol Cell Cardiol 1:425–437

  36. Legato MJ, Mulieri LA, Alpert NR (1984) The ultrastructure of myocardial hypertrophy: Why does the compensated heart fail? Eur Heart J 5 (Suppl. F):251–269

  37. Levin KR, Page E (1980) Quantitative studies on plasmalemmal folds and caveola of rabbit ventricular myocardial cells. Circ Res 46:244–255

  38. Luftig RB, McMillan PN, Weatherbee JA, Weihing RR (1977) Increased visualization of microtubules by an improved fixation procedure. J Histochem Cytochem 25:175–187

  39. Maron BJ, Ferrans VJ (1973) Significance of multiple intercalated discs in hypertrophied human myocardium. Am J Pathol 73:81–96

  40. Maron BJ, Ferrans VJ (1974) Aggregates of tubules in human cardiac muscle cells. J Molec Cell Cardiol 6:249–264

  41. Maron BJ, Ferrans VJ (1978) Ultrastructural features of hypertrophied human ventricular myocardium. Prog Cardiovasc Dis 21:207–238

  42. Maron BJ, Ferrans VJ, Roberts WC (1975a) Myocardial ultrastructure in patients with chronic aortic valve disease. Am J Cardiol 35:725–739

  43. Maron BJ, Ferrans VJ, Roberts WC (1975b) Ultrastructural features of degenerated cardiac muscle cells in patients with cardiac hypertrophy. Am J Pathol 79:387–434

  44. Orenstein J, Hogan D, Bloom S (1980) Surface cables of cardiac myocytes. J Molec Cell Cardiol 12:771–780

  45. Prescott L, Brightman MW (1976) The sarcolemma of Aplysia smooth muscle in freeze-fracture preparations. Tissue & Cell 8:241–258

  46. Robinson TF, Cohen-Gould L, Factor SM (1983) Skeletal framework in mammalian heart muscle. Arrangement of inter- and pericellular connective tissue structures. Lab Invest 49:482–498

  47. Robinson TF, Winegrad S (1981) A variety of intercellular connections in heart muscle. J Molec Cell Cardiol 13:185–195

  48. Roth LE (1967) Electron microscopy of mitosis in amebae. III. Cold and urea treatments: A basis for tests of direct effects of mitotic inhibitors on microtubule formation. J Cell Biol 34:47–59

  49. Schaper J, Schwarz F, Hehrlein F (1981) Ultrastrukturelle Veränderungen im menschlichen Myocard bei Hypertrophie durch Aortenklappenfehler und deren Beziehung zur links-ventrikulären Masse und Auswurffraktion. Herz 6:217–225

  50. Sommer JR, Johnson EA (1979) Ultrastructure of the cardiac muscle. In: Berne RM, Sperelakis N, Geiger SR (eds) Handbook of Physiology. Section 2: The Cardiovascular System, vol. I: The Heart American Physiological Society, Bethesda, p 113

  51. Sætersdal TS, Myklebust R, Skagseth E, Engedal H (1976) Ultrastructural studies on the growth of filaments and sarcomeres in mechanically overloaded human hearts. Virch Arch [Cell Pathol] 21:91–112

  52. Thiéry G, Bergeron M (1976) Morphologie spatiale des mitochondries des tubes proximaux et distaux du néphron. Rev Can Biol 35:211–216

  53. Tilney LG, Porter KR (1967) Studies on the microtubules in heliozea. II. The effect of low temperature on these structures in the formation and maintance of the axopodia. J Cell Biol 34:327–343

  54. Travis DF, Travis A (1972) Ultrastructural changes in the left ventricular rat myocardial cells with age. J Ultrastruct Res 39:124–148

  55. Van Noorden S, Olsen EGJ, Pearse AGE (1971) Hypertrophic obstructive cardiomyopathy, a histological, histochemical, and ultrastructural study of biopsy material. Cardiovasc Res 5:118–131

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Correspondence to Helge Dalen.

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Dalen, H., Sætersdal, T. & Ødegården, S. Some ultrastructural features of the myocardial cells in the hypertrophied human papillary muscle. Vichows Archiv A Pathol Anat 410, 281–294 (1987). https://doi.org/10.1007/BF00711285

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Key words

  • Human heart
  • Papillary muscle
  • Myocardial hypertrophy
  • Ultrastructure