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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2010; 56(5): 95-105


Spontaniously active ion cannelsof the nuclear envelope membrane

O.A. Fedorenko, S.M. Marchenko.

    O.O. Bogomoletz Institute of Physiology, National Academyof Science of Ukraine, Kyiv


Abstract

The genetic apparatus of the eukaryotic cells is enclosed by the nuclear envelope, which consists of two membranes, the inner and the outer ones, and can be regarded as the specific part of the endoplasmatic reticulum of the cell. There are nuclear pores in the nuclear membranes – complexes, which provide the highly selective transport of macromolecules and passive transport of ions and small molecules. Besides, ion channels selective to cations and anions were described in the inner and the outer nuclear membranes. The physiological significance of these channels is not still clear because of the difficulty of access for the direct electrophysiological investigation, but we can suppose that they can play an important role in the ion balance between the cytoplasm/nucleoplasm and the nuclear lumen. In this review we gathered and analyzed data about spontaneously active ion channels which were found in the membranes of the nuclear envelope from cells of different types and tried to propose their functional meaning.

Keywords: ion channels, nuclear envelope, nuclear pore,intracellular signaling, calcium signal, Ca2+ store of the cell.

References

  1. Akey C.W. Structural plasticity of the nuclear pore complex // J.Mol. Biol. - 1995. - 248. - P. 273-293.
  2. Allen T.D., Cronshaw J.M., Bagley S., Kiseleva E., Goldberg M.W. The nuclear pore complex: mediator of translocation between nucleus and cytoplasm // J. Cell Sci. - 2000. - 113. - P. 1651-1659.
  3. Assandri R., Mazzanti M. Ionic permeability on iso­lated mouse liver nuclei: influence of ATP and Ca2+ // J. Membr. Biol. - 1997. - 157, № 3. - P. 301-309.
  4. Badminton M.N., Campbell A.K., Rembold CM. Dif­ferential regulation of nuclear and cytosolic Ca2+ in HeLa cells // J. Biol. Chemistry. - 1996. - 271, № 49. -P.31210-31214.
  5. Baumann O., Walz B. Endoplasmic reticulum of ani­mal cells and its organization into structural and func­tional domains // Int. Rev. Cytol. - 2001. -205. -P. 149-214.
  6. Berridge M.J. The endoplasmic reticulum: a multifunc­tional signal organelle // Cell Calcium. - 2002. - 32,№ 5-6. - P. 235-249.
  7. Bortner CD., Cidlowski J.A. Uncoupling cell shrinkage from apoptosis reveals that Na+ influx is required for volume loss during programmed cell death // J. Biol. Chem. - 2003. - 278. - P. 39176-39184.
  8. Burke B., Stewart C.L. Life at the edge: the nuclear envelope and human disease // Nature. - 2002. - 3. -P. 575-585.
  9. 9. Bustamante J.O., Liepins A., Hanover J.A. Nuclear pore complex ion channels // Mol. Membr. Biol. - 1994. -11, №3. - P. 141-150.
  10. 10. Bustamante J.O., Hanover J.A., Liepins A. The ion channel behaviour of the nuclear pore complex // J. Membr. Biol. - 1995. - 146, №3. -P. 239-251.
  11. Bustamante J.O., Varanda W.A. Patch-clamp detec­tion of macromolecular translocation along nuclear pores // Braz. J. Med. Biol. Res. - 1998. - 31, № 3. -P.333-354.
  12. Bustamante J.O. Current concepts in nuclear pore elec-trophysiology // Can. J. Physiol. Pharmacol. - 2006. -84, №3-4. - P. 347-365.
  13. Danker T., H. Oberleithner. Nuclear pore function viewed with atomic force microscopy // Pflug. Arch. -Eur. J. Physiol. - 2000. - 439. - P. 671-681.
  14. Debska G., Kicinska A., Skalska J., Szewczyk A. In­tracellular potassium and chloride channels: an update // ABP. - 2001. - 48. - P. 137-144.
  15. Draguhn A., Borner G., Beckmann R., Buchber K., Heinemann U., Hucho F. Large-conductance cation channels in te envelope of nuclei from rat cerebral cortex // J. Membr. Biol. - 1997. - 158, № 2. - 159-166.
  16. Fedorenko O.A., Volkova T.M., Marchenko S.M. New cation channel of the T-lymphocyte nuclear membrane // Фізіол. журн. - 2006. - 52, № 1. - P. 17-21.
  17. Fedorenko O.A., Duzhyy D.E., Marchenko S.M. Spontaneous active ion channels of the nuclear envelope membranes of pyramidal hippocampal neurons // Neurophysiology. - 2007. - 39, № 1. - P. 3-8.
  18. Fedorenko O.A., Duzhyy D.E., Marchenko S.M. Nyclear ionic channels of the granule cells from the dentate gyrus // Фізіол. журн. - 2007. - 53, № 3. - P. 9-15.
  19. 19. Fedorenko O.A., Duzhyy D.E., Marchenko S.M. Cationic large conductance channels of the nuclear envelope of Purkinje neurons of cerebellum // Neurophysiology. - 2007. - 39, № 2. - P. 13-18.
  20. 20. Feldherr C.M., Akin D., Cohen R.J. Regulation of functional nuclear pore size in fibroblasts // J. Cell Sci. -2000. - 114. - P. 4621-4627.
  21. Franco-Obergon A., Wang H., Clapham D.E. Distinct ion channel classes are expressed on the outer nuclear envelope of T- and B-lymphocyte cell lines // Biophys. J. -2000. - 79. - P. 202-214.
  22. Gant T.M., Wilson K.L. Nuclear assembly // Annu. Rev. Cell Dev. Biol. - 1997. - 13. - P. 669-695. 23.Garcia-Segura L.M., Lafarga M., Berciano M.T., Hernandez P., Andrez M.A. Distribution of nuclear pores and chromatin organization in neurons and glial cells of the rat cerebellar cortex // J. Comp. Neurol. -1989. - 290, №3. - P. 440-450.
  23. Gerasimenko O.V., Gerasimenko J.V., Tepikin A.V., Petersen O.H. ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca2+ from the nuclear envelope // Cell. -1995. - 80, №3. - P. 439-444.
  24. Guihard G., Proteau S., Payet M.D., Eskande D., Rousseau E. Patch-clamp study of liver nuclear ionic channels reconstituted into giant proteoliposomes // FEBS Lett. - 2000. - 476. - P. 234-241.
  25. Goldberg M.W., Allen T.D. The nuclear pore complex and lamina: three-dimensional structures and inter­actions determined by field emission in-lens scanning electron microscopy // J. Mol. Biol. - 1996. - 257. -P. 848-865.
  26. Goldberg M.W., Wiese C, Allen T.D., Wilson K.L. Dimples, pores, star-rings, and thin rings on growing nuclear envelopes: evidence for structural intermediates in nuclear pore complex assembly // J. Cell Sci. - 1997. -110. - P. 409-420.
  27. Innocenti B., Mazzanti M. Identification of a nucleo-cytoplasmic ionic pathway by osmotic shock in isolated mouse liver nuclei // J. Membr. Biol. - 1993. -131, №2. - P. 137-142.
  28. 29. Jaggi R.D., Franco-Obergon A., Ensslin K. Quantative topographical analysis of nuclear pore complex function using scanning force microscopy // Biophys.J. - 2003. -85. – P. 4093-4098.
  29. 30. Jentsch T.J., Stein V., Weinreich F., Zdebik A.A. Molecular structure and physiological function of chloride channels // Physiol. Rev. - 2001. - 82. -P.503-568.
  30. Keminer O., Peters R. Permeability of single nuclear pore //Biophys. J. - 1999. - 77, № 1. - P. 217-228.
  31. Lanini L., Bachs O., Carafoli E. The calcium pump of the liver nuclear membrane is identical to that of endoplasmic reticulum // J. Biol. Chem. - 1992. - 267, №16. - P.11548-11552.
  32. Leite M.F., Thrower E.C., Echivarria W., Koulen P., Bennett A.M., Ehrlich B.E., Nathanson M.H. Nuclear and cytosolic calcium are regulated independently // PNAS. - 2003. - 100, № 5. - P. 2975-2980.
  33. Lenart P., Ellenberg J. Monitoring the permeability of the nuclear envelope during the cell cycle // Methods. -2006. - 38, №1. - P. 17-24.
  34. Marelli M., Lusk C.P., Chan H., Aitchison J.D., Wozniak R.W. A link between the synthesis of nucleoporins and the biogenesis of the nuclear envelope // J. Cell Biol. - 2001. - 153, № 4. - P. 709-724.
  35. Marchenko S.M., Yarotskyy V.V., Kovalenko T.N., Kostyuk P.G., Thomas R.C Spontaneously active and InsP -activated ion channels in cell nuclei from rat cerebellar Purkinje and granule neurones // J. Physiol.- 2005. - 15,№565. - P.897-910.
  36. Matzke M., Aufsatz W., Gregor W., van Der Winden J., Papp I., Matzake A.J. Ion transporters in the nucleus? // Plant Physiol. - 2001. - 127. - P. 10-13.
  37. Mazzanti M., DeFelice L.J., Cohn J., Malter H. Ion channels in the nuclear envelope // Nature. - 1990. -22, № 343(6260). - P. 764-767.
  38. 39. Mazzanti M., Bustamante J.O., Oberleithner H. Electrical dimension of the nuclear envelope // Physiol. Rev. - 2001. - 81, № 1. - P. 1-19.
  39. 40. Minn A.J., Velez P., Schendel S.L., Liang H., Muchmore S.W., Fesik S.W., Fill M., Thompson C.B. Bcl-x(L) forms an ion channel in synthetic lipid membranes // Nature. - 1997. - 23, № 385(6614). - P. 353-357.
  40. Nagasawa M., Kanzaki M., Lino Y., Morishita Y., Kojima I. Identification of a novel chloride channel expressed in the endoplasmic reticulum, Golgi apparatus and nucleus // J. Biol. Chem. - 2001. - 276, №23. - P. 20413-20418.
  41. Nicotera P., Orrenius S., Nilsson T., Berggren P.O. An inositol 1,4,5-trisphosphate-sensitive Ca2+ pool in liver nuclei // Proc. Natl. Acad. Sci. USA. - 1990. - 87, № 17. - P. 6858-6862.
  42. Pante N., Aebi U. Molecular dissection of the nuclear pore complex // Crit. Rev. Biochem. Mol. Biol. - 1996. -31. - P. 153-199.
  43. Petersen O.H., Gerasimenko O.V., Gerasimenko J.V., Mogami H., Tepikin A.V. The calcium store in the nuclear envelope // Cell Calcium. - 1998. - 23, № 2-3. - P.87-90.
  44. Picard L., Cote K., Teijeira J., Greentree D., Rousseau E. Sarcoplasmic reticulum K(+) channels from human and sheep atrial cells display a specific electro-pharmacological profile// J. Mol. Cell Cardiol. - 2002. – 34. - P. 1163-1172.
  45. Pozzan T., Rizzuto R., Volpe P., Meldolesi J. Molecular and cellular physiology if intracellular calcium stores / / Physiol. Rev. - 1994. - 73, №3. - P. 595-636.
  46. Quesada I., Rovira J.M., Martin F., Roche E., Nadal A., Soria B. Nuclear K channels trigger nuclear Ca2+ transients that modulate nuclear function // PNAS. -2002. - 99, № 14. - P. 9544-9549.
  47. Rousseau E., Michaud C, Lefebvre D., Proteau S., Decrouy A. Reconstitution of ionic channels from inner and outer membranes of mammalian cardiac nuclei // Biophys. J. - 1996. - 70, № 2. - P. 703-714.
  48. 49. Rout M. P., Aitchison J. D., Suprapto A., Hjertaas K., Zhao Y, Chait B.T. The yeast nuclear pore complex: composition, architecture and transport mechanism // J. Cell Biol. - 2000. - 148. - P. 635-651.
  49. 50. Ryan K.J., Wente S.R. The nuclear complex: a protein machine bridging the nucleus and cytoplasm // Curr. Opin. Cell Biol. - 2000. - 12. - P. 361-371.
  50. Santella L., Garafoli E. Calcium signaling in the cell nucleus // FASEB J. - 1997. - 11. - P. 1091-1109.
  51. Shahin V., Danker T., Enss K., Ossig R., Oberleithner H. Evidence for Ca2+- and ATP-sensitive peripheral channels in nuclear pore complexes // FASEB J. - 2001. -15, № 11. - P. 1895-1901.
  52. Shumaker D.K., Kuczmarski E.R., Goldman R.D. The nucleoskeleton: lamins and actin are major players in essential nuclear functions // Curr. Opin. Cell Biology. -2003. - 15, № 3. - P. 358-366.
  53. Stehno-Bittel L., Perez-Terzic C, Clapham D.E. Diffusion across the nuclear envelope inhibited by depletion of the nuclear Ca2+ store // Science. - 1995. -270. - P. 1835-1838.
  54. Tonini R., Grohovaz F., Laporta C.A., Mazzanti M. Gating mechanism of the nuclear pore complex channel in isolated neonatal and adult mouse liver nuclei // FASEB J. - 1999. - 13, № 11. -P. 1395-1403.
  55. Tonini R., Ferroni A., Valenzuela S.M., Warton K., Campbell T.J., Breit S.N., Mazzanti M. Functional characterization of the NCC27 nuclear protein in stable transfected CHO-K1 cells // FASEB J. - 2000. - 14, №(9). - P. 1171-1178.
  56. Walther T.C., Pickersgill H.S., Cordes V.C., Goldberg M.W., Allen T.D., Mattaj I.W., Fornerod M. The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import //J. Cell Biol. - 2002. - 158. - P.63-77.
  57. Wei X., Henke V.G., Strubing G., Brown E.B., Clapham D.E. Real-time imaging of nuclear permeation by EGFP in single intact cells // Biophys. J. - 2003. - 84. -P.1317-1327.
  58. 59. Wente S.R. Gatekeepers of the nucleus // Science. -2000. - 288. - P.1374-1377.
  59. 60. Worman H.J., Courvalin J.C. The inner nuclear membrane // J. Membr. Biol. - 2000. - 177. - P. 1-11.
  60. Worman H.J. Components of the nuclear envelope and their role in human disease // Novartis Found Symp. - 2005. - 264, №35. - P. 227-230.
  61. Worman H.J., Courvalin J.C. Nuclear envelope, nuclear lamina, and inherited disease // Int. Rev. Cytol. - 2005. -246. - P. 231-279.
  62. Yamashita M., Sugioka M., Ogawa Y Voltage- and Ca2+-activated potassium channels in Ca2+ store control Ca2+ release // FEBS Journal - 2006. - 273. -P.3585-3597.
  63. Yamashita M. ‘Quantal’ Ca2+ release reassessed - a clue to oscillation and synchronization // FEBS Lett. - 2006. - 580. - P. 4979-4983.

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