Two subcompartments of the smooth endoplasmic reticulum in perisynaptic astrocytic processes: ultrastructure and distribution in hippocampal and neocortical synapses

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Perisynaptic astrocytic processes involved in the tripartite synapse functioning respond to its activation by local depolarization with calcium release from the intracellular stores inside nodes of astrocytic processes and develop local and generalized calcium events. However, based on the first electron microscopy studies a point of view was formed that terminal astrocytic lamellae are devoid of any organelles, including the main astrocytic calcium store - the cisternae of the smooth endoplasmic reticulum. Indeed, analysis of smooth endoplasmic reticulum cisternae could be limited by their weak electron contrast, the studying of astrocytic processes on single sections, and insufficient optical resolution of the equipment used. Here, by using serial section transmission electron microscopy and 3D reconstructions, we analyzed astrocytic processes in murine hippocampal and cortical synapses. As a result of unit membranes contrast enhancement, it was shown for the first time that perisynaptic processes of astrocytes with a morphology of thin branchlets contain two types of smooth endoplasmic reticulum cisternae and microvesicles. Unlike branchlets, membrane organelles inside terminal lamellae were comprised by only short fragments of thin smooth endoplasmic reticulum cister-nae and microvesicles, whose groups tend to be located in close proximity to active zones of the most active synapses. We speculate both on reliability of the alternative methods in electron microscopy while studying astrocytic microenvironment of synapses and structure-function aspects of smooth endoplasmic reticulum cisternae compartmentalization inside the perisynaptic processes of astrocytes.

About the authors

E. A Shishkova

Institute of Cell Biophysics, Russian Academy of Sciences

Pushchino, Moscow Region, Russia

V. V Rogachevsky

Institute of Cell Biophysics, Russian Academy of Sciences

Email: ckpem.icb.ras@gmail.com
Pushchino, Moscow Region, Russia

References

  1. A. Reichenbach, A. Derouiche, and F. Kirchhoff, Brain Res. Rev., 63, 11 (2010).
  2. B. S. Khakh and M. V. Sofroniew, Nature Neuroscience, 18, 942 (2015).
  3. M. Arizono, V. V. G. K. Inavalli, A. Panatier, et al., Nature Commun., 11, 1906 (2020).
  4. M. Armbruster, S. Naskar, J. P. Garcia, et al., Nature Neurosci., 25, 607 (2022).
  5. J. SpaCek and A. R. Lieberman, J. Cell Sci., 46, 129 (1980).
  6. J. SpaCek and K. M. Harris, J. Neurosci., 17, 190 (1997).
  7. Y. Wu, C. Whiteus, C. S. Xue, et al., Proc. Natl. Acad. Sci. USA, 114,E4859 (2017).
  8. J. SpaCek, Anat. Embryol., 171, 235 (1985).
  9. J. SpaCek and K. M. Harris, J.Comp. Neurol., 393, 58 (1998).
  10. R. Ventura and K. M. Harris, J. Neurosci., 19, 6897 (1999).
  11. M. A. Xu-Friedman, K. M. Harris, and W. G. Regehr, J. Neurosci., 21, 6666 (2001).
  12. C. Genoud, C. Quairiaux, and P. Steiner, PLoS Biol., 4, e343 (2006).
  13. M. R. Witcher, S. A. Kirov, and K. M. Harris, Glia, 55, 13 (2007).
  14. K. Chounlamountry and J.-P. Kessler, Glia, 59, 655 (2011).
  15. M. Bellesi, L. de Vivo, G. Tononi, et al., BMC Biol., 13, 66 (2015).
  16. P. Bezzi, V. Gundersen, J. L. Galbete, et al., Nature Neurosci., 7, 613 (2004).
  17. L. H. Bergersen, C. Morland, L. Ormel, et al., Cereb Cortex, 22, 1690(2012).
  18. I. Patrushev, N. Gavrilov, V. Turlapov, et al., Cell Calcium, 54, 343 (2013).
  19. M. J. Karnovsky, In Abstr. Book of the 11th Annual Meet. of the American Society for Cell Biology, Abstracts 284, 146 (1971).
  20. A. M. Seligman, H. L. Wasserkrug, and J. S. Hanker, J. Cell Biol., 30, 424 (1966).
  21. B. Fernandez, I. Suarez, and G. Gonzalez, Anat. Anz., 156, 31 (1984).
  22. A. Semyanov and A. Verkhratsky, Trends Neurosci., 44, 781 (2021).
  23. Y. Oe, O. Baba, H. Ashida, et al., Glia, 64, 1532 (2016).
  24. N. Benmeradi, B. Payre, and S. L. Goodman, Microsc. Microanal. 21 (Suppl. 3), 721 (2015).
  25. T. Hanaichi, T. Sato, T. Iwamoto, et al., J. Electron Microsc. (Tokyo), 35, 304 (1986).
  26. S. Saalfeld, R. Fetter, A. Cardona, et al., Nature Methods, 9, 717 (2012).
  27. J. C. Fiala, K. M. Harris, J. Microsc., 202, Pt 3, 468 (2001).
  28. J. C. Fiala, J. Microsc., 218 (Pt 1), 52 (2005).
  29. W. C. De Bruijn, J. Ultrastruct. Res., 42, 29 (1973).
  30. L. A. Langford and R. E. Coggeshall, Anat. Rec., 197, 297 (1980).
  31. E. A. Shishkova, I. V. Kraev, and V. V. Rogachevsky, Biophysics, 67, 5, 752 (2022).
  32. P. Drochmans, J. Ultrastruct. Res., 6, 141 (1962).
  33. J. P. Revel, J. Histochem. Cytochem., 12, 104 (1964).
  34. L.-E. Thornell, J. Ultrastruct. Res., 49, 157 (1974).
  35. C. Prats, T. E. Graham, and J. Shearer, J. Biol. Chem., 293, 19, 7089 (2018).
  36. K. K. Rybicka, Tissue Cell, 28, 3, 253 (1996).
  37. M. L. Entman, S. S. Keslensky, A. Chu, et al., J. Biol. Chem., 255, 13, 6245 (1980).
  38. Y. Hirata, M. Atsumi, Y. Ohizumi, et al., Biochem. J., 371, 81 (2003).
  39. C. Lavoie, L. Roy, J. Lanoix, et al., Prog Histochem Cytochem., 46, 1 (2011).
  40. M. S. Muller, R. Fox, A. Schousboe, et al., Glia, 62, 526 (2014).
  41. S. P. J. Brooks, B. J. Lampi, and C. G. Bihun, Contemp. Top. Lab. Anim. Sci., 38, 19 (1999).
  42. C. W. Scouten, R. O'Connor, and M. Cunningham, J. Microsc. Today, 14, 3, 26 (2006).
  43. R. Kasukurthi, M. J. Brenner, Amy M. Moore, et al., J. Neurosci. Methods, 184, 303 (2009).
  44. S. R. Nelson, D. W. Schulz, J V. Passonneau, et al., J. Neurochem., 15, 1271 (1968).
  45. F D. Morgenthaler, D. M. Koski, R. Kraftsik, et al., Neurochem.Int., 48, 616 (2006).
  46. L. F. Obel, M. S. Muller, A. B. Walls, et al., Front. Neuroenergetics, 4, 3, 1 (2012).
  47. J. S. Coggan, D. Keller, C. Calo, et al., PLoS Comput. Biol., 14, 8, e1006392 (2018).
  48. O. H. Lowry, J. V. Passonneau, F. X. Hasselberger, et al., J. Biol. Chem., 239, 18 (1964).
  49. H. Watanabe and J. V. Passonneau, Brain Res., 66, 147 (1974).
  50. R. A. Swanson, S. M. Sagar, and F R. Sharp, Neurol. Res., 11, 24 (1989).
  51. R. A. Swanson, M. M. Morton, S. M. Sagar, et al., Neuroscience, 51, 2, 451 (1992).
  52. T. Matsui, T. Ishikawa, H. Ito, et al., J. Physiol., 590, 607 (2012).
  53. M. K. Brewer and M. S. Gentry, in Advances in Neurobiology, 23: Brain Glycogen Metabolism (Springer Nature Switzerl and AG, 2019), pp. 17-81.
  54. J. Hirrlinger, S. Hulsmann, and F Kirchhoff, Eur. J. Neurosci., 20, 2235 (2004).
  55. Y. Bernardinelli, J. Randall, E. Janettet al., Curr. Biol., 24, 1679 (2014).
  56. G. R. Login and A. M. Dvorak, Histochem. J., 20, 373 (1988).
  57. G. R. Login and A. M. Dvorak, The Microwave Tool Book (Beth Israel Hospital, 1994).
  58. F.E. Jensen and K.M. Harris, J. Neurosci. Methods, 29, 217 (1989).
  59. M. A. Sullivan, S. T. N. Aroney, S. Li, et al., Biomacromolecules, 15, 660 (2014).
  60. T. Satoh, C. A. Ross, A. Villa, et al., J. Cell Biol., 111, 615 (1990).
  61. N. Holbro, A. Grunditz, and T. G. Oertner, Proc. Natl. Acad. Sci. USA, 106, 15055 (2009).
  62. P. Jedlicka, A. Vlachos, S. W. Schwarzacher, et al., Behav. Brain Res., 192, 12 (2008).
  63. K. Takei, H. Stukenbrok, A. Metcalf, et al., J. Neurosci., 12, 489 (1992).
  64. A. H. Sharp, P. S. McPherson, T. M. Dawson, et al., J. Neurosci., 13, 3051 (1993).
  65. H. Shimizu, M. Fukaya, and M. Yamasaki, Proc. Natl. Acad. Sci. USA, 105, 11998 (2008).
  66. R. Barzan, F. Pfeiffer, and M. Kukley, Front. Neurosci., 10, 135 (2016).
  67. J.-P. Mothet, L. Pollegioni, G. Ouanounou, et al., Proc. Natl. Acad. Sci. USA, 102, 5606 (2005).
  68. Y. Du, S. Ferro-Novick, and P. Novick, J. Cell Sci., 117,2871 (2004).
  69. J. Espadas, D. Pendin, R. Bocanegra, et al., Nature Commun., 10, 5327 (2019).
  70. S. Wang, H. Tukachinsky, F. B. Romano, et al., eLife, 5, e18605 (2016).
  71. J. D. Lindsey and M. H. Ellisman, J. Neurosci., 5, 12, 3135 (1985).
  72. N. Rismanchi, C. Soderblom, J. Stadler, et al., Hum. Mol. Genet., 17, 11, 1591 (2008).
  73. X. Hu and F. Wu, Prot. Cell, 6, 4, 307 (2015).
  74. M. Krzisch, S. G. Temprana, L. A. Mongiat, et al., Brain Struct. Funct., 220, 4, 2027 (2015).
  75. G. Mattews, Neuron, 44, 223 (2004).
  76. R. G. Parton and K. Simons, Nat. Rev. Mol. Cell Biol., 8, 185 (2007).
  77. N. J. Willmott, K. Wong, and A. J. Strong, J. Neurosci., 20, 5, 1767 (2000).
  78. X. Hua, E. B. Malarkey, V. Sunjara, et al., J. Neurosci. Res., 76, 86 (2004).
  79. M. W. Sherwood, M. Arizono, C. Hisatsune, et al., Glia, 65, 3, 502 (2017).
  80. E. Shigetomi, S. Patel, and B. S. Khakh, Trends Cell Biol., 26, 4, 300 (2016).
  81. J. Meldolesi and T. Pozzan, J. Cell Biol., 21, 142, 1395 (1998).
  82. Y. Takumi, V. Ramirez-Leon, P. Laake, et al., Nature Neurosci., 2, 7, 618 (1999).
  83. M. G. Stewart, N. I. Medvedev, V. I. Popov, et al., Eur. J. Neurosci., 21, 3368 (2005).
  84. V. I. Popov, N. I. Medvedev, I. V. Patrushev, et al., Neuroscience, 149, 549 (2007).
  85. A. Plata, A. Lebedeva, P. Denisov, et al., Front. Mol. Neurosci., 11, 215 (2018).
  86. A. Matus, Curr. Opin. Neurobiol., 15, 76 (2005).
  87. A. J. G. D. Holtmaat, J. T. Trachtenberg, L. Wilbrecht, et al., Neuron, 45, 279 (2005).
  88. A. H. Cornell-Bell, P. G. Thomas, and S. J. Smith, Glia, 3, 322 (1990).
  89. M. E. Brown and P. C. Bridgman, J. Neurobiol., 58, 1, 118 (2004).
  90. S. J. Stachelek, R. A. Tuft, L. M. Lifschitz, J. Biol. Chem., 276, 35652 (2001).
  91. C. Cali, J. Baghabra, D.J. Boges, et al., J.Comp. Neurol., 524, 23 (2016).
  92. M. Bellesi, L. de Vivo, S. Koebe, et al., Front. Cell Neurosci., 12, 308 (2018).

Copyright (c) 2023 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies