Українська Русский English

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

Spontaneously active ion channels of the nuclear envelope membrane

Fedorenko OA, Marchenko SM

    O.O. Bogomoletz Institute of Physiology, National Academyof Science of Ukraine, Kyiv, Ukraine
DOI: https://doi.org/10.15407/fz56.05.095

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.

Full text: (PDF, in Ukrainian)

References

  1. Akey C.W. Structural plasticity of the nuclear pore complex . J.Mol. Biol. 1995. 248. P. 273-293. CrossRef  
  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.  
  3. Assandri R., Mazzanti M. Ionic permeability on iso­lated mouse liver nuclei: influence of ATP and Ca2+ . J. Membr. Biol. 1997. 157, N 3. P. 301-309. CrossRef PubMed
    4.  
  4. Badminton M.N., Campbell A.K., Rembold CM. Dif­ferential regulation of nuclear and cytosolic Ca2+ in HeLa cells . J. Biol. Chemistry. 1996. 271, N 49. P.31210-31214. CrossRef PubMed
    5.  
  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. CrossRef  
  6. Berridge M.J. The endoplasmic reticulum: a multifunc­tional signal organelle . Cell Calcium. 2002. 32,N 5-6. P. 235-249. CrossRef PubMed
    7.  
  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. CrossRef PubMed
    8.  
  8. Burke B., Stewart C.L. Life at the edge: the nuclear envelope and human disease . Nature. 2002. 3. P. 575-585. CrossRef PubMed
    9.  
  9. Bustamante J.O., Liepins A., Hanover J.A. Nuclear pore complex ion channels . Mol. Membr. Biol. 1994. 11, N 3. P. 141-150. CrossRef PubMed
    10.  
  10. Bustamante J.O., Hanover J.A., Liepins A. The ion channel behaviour of the nuclear pore complex . J. Membr. Biol. 1995. 146, N 3. P. 239-251. CrossRef  
  11. Bustamante J.O., Varanda W.A. Patch-clamp detec­tion of macromolecular translocation along nuclear pores . Braz. J. Med. Biol. Res. 1998. 31, N 3. P.333-354. CrossRef PubMed
    12.  
  12. Bustamante J.O. Current concepts in nuclear pore elec-trophysiology . Can. J. Physiol. Pharmacol. 2006. 84, N 3-4. P. 347-365. CrossRef PubMed
    13.  
  13. Danker T., H. Oberleithner. Nuclear pore function viewed with atomic force microscopy . Pflug. Arch. Eur. J. Physiol. 2000. 439. P. 671-681. CrossRef PubMed
    14.  
  14. Debska G., Kicinska A., Skalska J., Szewczyk A. In­tracellular potassium and chloride channels: an update . ABP. 2001. 48. P. 137-144.
    15.  
  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, N 2. 159-166. CrossRef PubMed
    16.  
  16. Fedorenko O.A., Volkova T.M., Marchenko S.M. New cation channel of the T-lymphocyte nuclear membrane . Fiziol. zhurn. 2006. 52, N 1. P. 17-21.
    17.  
  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, N 1. P. 3-8. CrossRef  
  18. Fedorenko O.A., Duzhyy D.E., Marchenko S.M. Nyclear ionic channels of the granule cells from the dentate gyrus . Fiziol. zhurn. 2007. 53, N 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, N 2. P. 13-18. CrossRef  
  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.  
  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. CrossRef  
  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, N 3. P. 440-450. CrossRef PubMed
    23.  
  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, N 3. P. 439-444. CrossRef  
  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. CrossRef  
  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. CrossRef PubMed
    26.  
  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.  
  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, N 2. P. 137-142. CrossRef PubMed
    28.  
  28. 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. CrossRef  
  29. 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. CrossRef PubMed
    30.  
  30. Keminer O., Peters R. Permeability of single nuclear pore .Biophys. J. 1999. 77, N 1. P. 217-228. CrossRef  
  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, N 16. P.11548-11552.
    32.  
  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, N 5. P. 2975-2980. CrossRef PubMed PubMedCentral
    33.  
  33. Lenart P., Ellenberg J. Monitoring the permeability of the nuclear envelope during the cell cycle . Methods. 2006. 38, N 1. P. 17-24. CrossRef PubMed
    34.  
  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, N 4. P. 709-724. CrossRef PubMed PubMedCentral
    35.  
  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,N 565. P.897-910. CrossRef PubMed PubMedCentral
    36.  
  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. CrossRef PubMed PubMedCentral
    37.  
  37. Mazzanti M., DeFelice L.J., Cohn J., Malter H. Ion channels in the nuclear envelope . Nature. 1990. 22, N 343(6260). P. 764-767. CrossRef PubMed
    38.  
  38. Mazzanti M., Bustamante J.O., Oberleithner H. Electrical dimension of the nuclear envelope . Physiol. Rev. 2001. 81, N 1. P. 1-19. CrossRef PubMed
    39.  
  39. 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, N 385(6614). P. 353-357. CrossRef PubMed
    40.  
  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, N 23. P. 20413-20418. CrossRef PubMed
    41.  
  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, N 17. P. 6858-6862. CrossRef PubMed PubMedCentral
    42.  
  42. Pante N., Aebi U. Molecular dissection of the nuclear pore complex . Crit. Rev. Biochem. Mol. Biol. 1996. 31. P. 153-199. CrossRef PubMed
    43.  
  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, N 2-3. P.87-90. CrossRef  
  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. CrossRef PubMed
    45.  
  45. Pozzan T., Rizzuto R., Volpe P., Meldolesi J. Molecular and cellular physiology if intracellular calcium stores . . Physiol. Rev. 1994. 73, N 3. P. 595-636. CrossRef PubMed
    46.  
  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, N 14. P. 9544-9549. CrossRef PubMed PubMedCentral
    47.  
  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, N 2. P. 703-714. CrossRef  
  48. 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. CrossRef PubMed PubMedCentral
    49.  
  49. 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. CrossRef  
  50. Santella L., Garafoli E. Calcium signaling in the cell nucleus . FASEB J. 1997. 11. P. 1091-1109. CrossRef PubMed
    51.  
  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, N 11. P. 1895-1901. CrossRef PubMed
    52.  
  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, N 3. P. 358-366. CrossRef  
  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. CrossRef PubMed
    54.  
  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, N 11. P. 1395-1403. CrossRef PubMed
    55.  
  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, N (9). P. 1171-1178. CrossRef PubMed
    56.  
  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. CrossRef PubMed PubMedCentral
    57.  
  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. CrossRef  
  58. Wente S.R. Gatekeepers of the nucleus . Science. 2000. 288. P.1374-1377. CrossRef PubMed
    59.  
  59. Worman H.J., Courvalin J.C. The inner nuclear membrane . J. Membr. Biol. 2000. 177. P. 1-11. CrossRef PubMed
    60.  
  60. Worman H.J. Components of the nuclear envelope and their role in human disease . Novartis Found Symp. 2005. 264, N 35. P. 227-230.
    61.  
  61. Worman H.J., Courvalin J.C. Nuclear envelope, nuclear lamina, and inherited disease . Int. Rev. Cytol. 2005. 246. P. 231-279. CrossRef  
  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. CrossRef PubMed
    63.  
  63. Yamashita M. 'Quantal' Ca2+ release reassessed a clue to oscillation and synchronization . FEBS Lett. 2006. 580. P. 4979-4983. CrossRef PubMed
    64.  

© National Academy of Sciences of Ukraine, Bogomoletz Institute of Physiology, 2014-2019.