Calcium regulation of nucleocytoplasmic transport

Protein and Cell

Volumn 2, Issue 4, 2011, Pages 291-302

  Sarma, Ashapurna ^a   Yang, Weidong ^a  

^a BOWLING GREEN STATE UNIVERSITY   (United States)

Author keywords

calcium stores; nuclear envelope; nuclear pore complex; nucleocytoplasmic transport; single molecule fluorescence microscopy

Indexed keywords

CALCIUM ION; CARRIER PROTEIN; EXPORTIN; KARYOPHERIN; KARYOPHERIN BETA; NUCLEOPORIN; RAN PROTEIN; UNCLASSIFIED DRUG; CALCIUM;

CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CYTOPLASM; DIFFUSION; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; FLUORESCENCE MICROSCOPY; HUMAN; MOLECULAR MECHANICS; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; NUCLEAR PORE COMPLEX; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN TRANSPORT; REVIEW; ACTIVE TRANSPORT; ANIMAL; CHEMISTRY; CONFORMATION; CYTOLOGY; ION TRANSPORT; METABOLISM; NUCLEAR PORE; OOCYTE; PHYSIOLOGY; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

EUKARYOTA;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CALCIUM; CELL NUCLEUS; CYTOPLASM; DIFFUSION; ENDOPLASMIC RETICULUM; EUKARYOTIC CELLS; HUMANS; ION TRANSPORT; MICROSCOPY, FLUORESCENCE; MOLECULAR CONFORMATION; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; OOCYTES; SIGNAL TRANSDUCTION; XENOPUS LAEVIS;

EID: 80052786289     PISSN: 1674800X     EISSN: 16748018     Source Type: Journal    
DOI: 10.1007/s13238-011-1038-x     Document Type: Review

References (90)

1. Bayliss, R., Littlewood, T., and Stewart, M. (2000). Structural basis for the interaction between FxFG nucleoporin repeats and importinbeta in nuclear trafficking. Cell 102, 99-108.
2. Beck, M., Förster, F., Ecke, M., Plitzko, J. M., Melchior, F., Gerisch, G., Baumeister, W., and Medalia, O. (2004). Nuclear pore complex structure and dynamics revealed by cryoelectron tomography. Science 306, 1387-1390.
3. Bednenko, J., Cingolani, G., and Gerace, L. (2003). Importin β contains a COOH-terminal nucleoporin binding region important for nuclear transport. J Cell Biol 162, 391-401.
4. Betzig, E. (1995). Proposed method for molecular optical imaging. Opt Lett 20, 237-239.
5. Bischoff, F. R., and Görlich, D. (1997). RanBP1 is crucial for the release of RanGTP from importin β-related nuclear transport factors. FEBS Lett 419, 249-254.
6. Bischoff, F. R., Klebe, C., Kretschmer, J., Wittinghofer, A., and Ponstingl, H. (1994). RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc Natl Acad Sci U S A 91, 2587-2591.
7. Bootman, M. D., Fearnley, C., Smyrnias, I., MacDonald, F., and Roderick, H. L. (2009). An update on nuclear calcium signalling. J Cell Sci 122, 2337-2350.
8. Brohawn, S. G., Partridge, J. R., Whittle, J. R. R., and Schwartz, T. U. (2009). Nuclear pore complex has entered the atomic age. Structure 17, 1156-1168.
9. Bustamante, C., Bryant, Z., and Smith, S. B. (2003). Ten years of tension: single-molecule DNA mechanics. Nature 421, 423-427.
10. Cardarelli, F., and Gratton, E. (2010). In vivo imaging of singlemolecule translocation through nuclear pore complexes by pair correlation functions. PLoS One 5, e10475.
11. Carmen, P. T., Marisa, J., and David, E. C. (1997). Nuclear calcium and the regulation of the nuclear pore complex. BioEssays 19, 787-792.
12. Cook, A., Bono, F., Jinek, M., and Conti, E. (2007). Structural biology of nucleocytoplasmic transport. Annu Rev Biochem 76, 647-671.
13. Corbett, A. H., and Silver, P. A. (1997). Nucleocytoplasmic transport of macromolecules. Microbiol Mol Biol Rev 61, 193-211.
14. Coutavas, E., Ren, M., Oppenheim, J. D., D'Eustachio, P., and Rush, M. G. (1993). Characterization of proteins that interact with the cellcycle regulatory protein Ran/TC4. Nature 366, 585-587.
15. Cronshaw, J. M., Krutchinsky, A. N., Zhang, W., Chait, B. T., and Matunis, M. J. (2002). Proteomic analysis of the mammalian nuclear pore complex. J Cell Biol 158, 915-927.
16. Dange, T., Grünwald, D., Grünwald, A., Peters, R., and Kubitscheck, U. (2008). Autonomy and robustness of translocation through the nuclear pore complex: a single-molecule study. J Cell Biol 183, 77-86.
17. Danker, T. and Oberleithner, H. (2000). Nuclear pore function viewed with atomic force microscopy. Pflügers Arch 439, 671-681.
18. Denning, D. P., Patel, S. S., Uversky, V., Fink, A. L., and Rexach, M. (2003). Disorder in the nuclear pore complex: the FG repeat regions of nucleoporins are natively unfolded. Proc Natl Acad Sci U S A 100, 2450-2455.
19. Erickson, E. S., Mooren, O. L., Moore, D., Krogmeier, J. R., and Dunn, R. C. (2006). The role of nuclear envelope calciumin modifying nuclear pore complex structure. Can J Physiol Pharmacol 84, 309-318.
20. Erickson, E. S., Mooren, O. L., Moore-Nichols, D., and Dunn, R. C. (2004). Activation of ryanodine receptors in the nuclear envelope alters the conformation of the nuclear pore complex. Biophys Chem 112, 1-7.
21. Fahrenkrog, B., and Aebi, U. (2003). The nuclear pore complex: nucleocytoplasmic transport and beyond. Nat Rev Mol Cell Biol 4, 757-766.
22. Fernández-Suárez, M., and Ting, A. Y. (2008). Fluorescent probes for super-resolution imaging in living cells. Nat Rev Mol Cell Biol 9, 929-943.
23. Frey, N., McKinsey, T. A., and Olson, E. N. (2000). Decoding calcium signals involved in cardiac growth and function. Nat Med 6, 1221-1227.
24. Fried, H., and Kutay, U. (2003). Nucleocytoplasmic transport: taking an inventory. Cell Mol Life Sci 60, 1659-1688.
25. Gensburger, C., Freyermuth, S., Klein, C., and Malviya, A. N. (2003). In vivo nuclear Ca2+-ATPase phosphorylation triggers intermediate size molecular transport to the nucleus. Biochem Biophys Res Commun 303, 1225-1228.
26. Gerasimenko, J., Maruyama, Y., Tepikin, A., Petersen, O. H., and Gerasimenko, O. (2003). Calcium signalling in and around the nuclear envelope. Biochem Soc Trans 31, 76-78.
27. Greber, U. F., and Gerace, L. (1992). Nuclear protein import is inhibited by an antibody to a lumenal epitope of a nuclear pore complex glycoprotein. J Cell Biol 116, 15-30.
28. Greber, U. F., and Gerace, L. (1995). Depletion of calcium from the lumen of endoplasmic reticulum reversibly inhibits passive diffusion and signal-mediated transport into the nucleus. J Cell Biol 128, 5-14.
29. Greber, U. F., Senior, A., and Gerace, L. (1990). A major glycoprotein of the nuclear pore complex is a membrane-spanning polypeptide with a large lumenal domain and a small cytoplasmic tail. EMBO J 9, 1495-1502.
30. Hess, H. F., Betzig, E., Harris, T. D., Pfeiffer, L. N., and West, K. W. (1994). Near-field spectroscopy of the quantum constituents of a luminescent system. Science 264, 1740-1745.
31. Isgro, T. A., and Schulten, K. (2005). Binding dynamics of isolated nucleoporin repeat regions to importin-beta. Structure 13, 1869-1879.
32. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I. W., and Görlich, D. (1997). The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J 16, 6535-6547.
33. Jäggi, R. D., Franco-Obregón, A., Mühlhäusser, P., Thomas, F., Kutay, U., and Ensslin, K. (2003). Modulation of nuclear pore topology by transport modifiers. Biophys J 84, 665-670.
34. Kahms, M., Lehrich, P., Hüve, J., Sanetra, N., and Peters, R. (2009). Binding site distribution of nuclear transport receptors and transport complexes in single nuclear pore complexes. Traffic 10, 1228-1242.
35. Kass, G. E., and Orrenius, S. (1999). Calcium signaling and cytotoxicity. Environ Health Perspect 107, 25-35.
36. Kau, T. R., Way, J. C., and Silver, P. A.(2004). Nuclear transport and cancer: from mechanism to intervention. Nat Rev Cancer 4, 106-117.
37. Kramer, A., Ludwig, Y., Shahin, V., and Oberleithner, H. (2007). A pathway separate from the central channel through the nuclear pore complex for inorganic ions and small macromolecules. J Biol Chem 282, 31437-31443.
38. Kubitscheck, U., Grünwald, D., Hoekstra, A., Rohleder, D., Kues, T., Siebrasse, J. P., and Peters, R. (2005). Nuclear transport of single molecules: dwell times at the nuclear pore complex. J Cell Biol 168, 233-243.
39. Lee, M. A., Dunn, R. C., Clapham, D. E., and Stehno-Bittel, L. (1998). Calcium regulation of nuclear pore permeability. Cell Calcium 23, 91-101.
40. Lee, S. J., Matsuura, Y., Liu, S. M., and Stewart, M. (2005). Structural basis for nuclear import complex dissociation by RanGTP. Nature 435, 693-696.
41. Lim, R., Aebi, U., and Fahrenkrog, B. (2008). Towards reconciling structure and function in the nuclear pore complex. Histoche Cell Biol 129, 105-116.
42. Lim, R. Y. H., Fahrenkrog, B., Köser, J., Schwarz-Herion, K., Deng, J., and Aebi, U. (2007). Nanomechanical Basis of Selective Gating by the Nuclear Pore Complex. Science 318, 640-643.
43. Lippincott-Schwartz, J., and Patterson, G. H. (2009). Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol 19, 555-565.
44. Liu, S. M., and Stewart, M. (2005). Structural basis for the high-affinity binding of nucleoporin Nup1p to the Saccharomyces cerevisiae importin-beta homologue, Kap95p. J Mol Biol 349, 515-525.
45. Lyman, S. K., Guan, T., Bednenko, J., Wodrich, H., and Gerace, L. (2002). Influence of cargo size on Ran and energy requirements for nuclear protein import. J Cell Biol 159, 55-67.
46. Ma, J., and Yang, W. (2010). Three-dimensional distribution of transient interactions in the nuclear pore complex obtained from single-molecule snapshots. Proc Natl Acad Sci U S A 107, 7305-7310.
47. Malviya, A. N., and Klein, C. (2006). Mechanism regulating nuclear calcium signaling. Can J Physiol Pharmacol 84, 403-422.
48. Mattson, M. P., LaFerla, F. M., Chan, S. L., Leissring, M. A., Shepel, P. N., and Geiger, J. D. (2000). Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci 23, 222-229.
49. Miao, L., and Schulten, K. (2009). Transport-related structures and processes of the nuclear pore complex studied through molecular dynamics. Structure 17, 449-459.
50. Moore, M. S., and Blobel, G. (1993). The GTP-binding protein Ran/TC4 is required for protein import into the nucleus. Nature 365, 661-663.
51. Moore-Nichols, D., Arnott, A., and Dunn, R. C. (2002). Regulation of nuclear pore complex conformation by IP(3) receptor activation. Biophys J 83, 1421-1428.
52. Mooren, O. L., Erickson, E. S., Moore-Nichols, D., and Dunn, R. C. (2004). Nuclear side conformational changes in the nuclear pore complex following calcium release from the nuclear membrane. Phys Biol 1, 125-134.
53. O'Brien, E. M., Gomes, D. A., Sehgal, S., and Nathanson, M. H. (2007). Hormonal Regulation of Nuclear Permeability. J Biol Chem 282, 4210-4217.
54. Patel, S. S., Belmont, B. J., Sante, J. M., and Rexach, M. F. (2007). Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex. Cell 129, 83-96.
55. Patterson, G. H., and Lippincott-Schwartz, J. (2002). A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297, 1873-1877.
56. Paulillo, S. M., Powers, M. A., Ullman, K. S., and Fahrenkrog, B. (2006). Changes in nucleoporin domain topology in response to chemical effectors. J Mol Biol 363, 39-50.
57. Perez-Terzic, C., Gacy, A. M., Bortolon, R., Dzeja, P. P., Puceat, M., Jaconi, M., Prendergast, F. G., and Terzic, A. (1999). Structural plasticity of the cardiac nuclear pore complex in response to regulators of nuclear import. Circ Res 84, 1292-1301.
58. Perez-Terzic, C., Jaconi, M., and Clapham, D. E. (1997). Nuclear calcium and the regulation of the nuclear pore complex. BioEssays 19, 787-792.
59. 2+ stores. Science 273, 1875-1877.
60. Peters, R. (2009). Translocation through the nuclear pore: Kaps pave the way. Bioessays 31, 466-477.
61. Rakowska, A., Danker, T., Schneider, S. W., and Oberleithner, H. (1998). ATP-Induced shape change of nuclear pores visualized with the atomic force microscope. J Membr Biol 163, 129-136.
62. Rexach, M., and Blobel, G. (1995). Protein import into nuclei: association and dissociation reactions involving transport substrate, transport factors, and nucleoporins. Cell 83, 683-692.
63. Rizzuto, R., and Pozzan, T. (2003). When calcium goes wrong: genetic alterations of a ubiquitous signaling route. Nat Genet 34, 135-141.
64. Rout, M. P., and Aitchison, J. D. (2001). The nuclear pore complex as a transport machine. J Biol Chem 276, 16593-16596.
65. Rout, M. P., Aitchison, J. D., Magnasco, M. O., and Chait, B. T. (2003). Virtual gating and nuclear transport: the hole picture. Trends Cell Biol 13, 622-628.
66. Rout, M. P., Aitchison, J. D., Suprapto, A., Hjertaas, K., Zhao, Y., and Chait, B. T. (2000). The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148, 635-651.
67. Rout, M. P., and Blobel, G. (1993). Isolation of the yeast nuclear pore complex. J Cell Biol 123, 771-783.
68. Rout, M. P., and Wente, S. R. (1994). Pores for thought: nuclear pore complex proteins. Trends Cell Biol 4, 357-365.
69. Stehno-Bittel, L., Lückhoff, A., and Clapham, D. E. (1995a). Calcium release from the nucleus by InsP3 receptor channels. Neuron 14, 163-167.
70. Stehno-Bittel, L., Perez-Terzic, C., and Clapham, D. E. (1995b). Diffusion across the nuclear envelope inhibited by depletion of the nuclear Ca2 + store. Science 270, 1835-1838.
71. Stewart, M. (2007). Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8, 195-208.
72. Stoffler, D., Feja, B., Fahrenkrog, B., Walz, J., Typke, D., and Aebi, U. (2003). Cryo-electron tomography provides novel insights into nuclear pore architecture: implications for nucleocytoplasmic transport. J Mol Biol 328, 119-130.
73. Stoffler, D., Goldie, K. N., Feja, B., and Aebi, U. (1999). Calciummediated structural changes of native nuclear pore complexes monitored by time-lapse atomic force microscopy. J Mol Biol 287, 741-752.
74. Stoffler, D., Schwarz-Herion, K., Aebi, U., and Fahrenkrog, B. (2006). Getting across the nuclear pore complex: new insights into nucleocytoplasmic transport. Can J Physiol Pharmacol 84, 499-507.
75. Strawn, L. A., Shen, T., Shulga, N., Goldfarb, D. S., and Wente, S. R. (2004). Minimal nuclear pore complexes define FG repeat domains essential for transport. Nat Cell Biol 6, 197-206.
76. Strübing, C., and Clapham, D. E. (1999). Active nuclear import and export is independent of lumenal Ca2+ stores in intact mammalian cells. J Gen Physiol 113, 239-248.
77. Suntharalingam, M., and Wente, S. R. (2003). Peering through the pore: nuclear pore complex structure, assembly, and function. Dev Cell 4, 775-789.
78. Thompson, R. E., Larson, D. R., and Webb, W. W. (2002). Precise nanometer localization analysis for individual fluorescent probes. Biophys J 82, 2775-2783.
79. Walther, T. C., Pickersgill, H. S., Cordes, V. C., Goldberg, M. W., Allen, T. D., Mattaj, I. W., and Fornerod, M. (2002). The cytoplasmic filaments of the nuclear pore complex are dispensable for selective nuclear protein import. J Cell Biol 158, 63-77.
80. Wang, H., and Clapham, D. E. (1999). Conformational changes of the in situ nuclear pore complex. Biophys J 77, 241-247.
81. Wei, X., Henke, V. G., Strübing, C., Brown, E. B., and Clapham, D. E. (2003). Real-time imaging of nuclear permeation by EGFP in single intact cells. Biophys J 84, 1317-1327.
82. Weis, K. (2003). Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell 112, 441-451.
83. Wozniak, R. W., Rout, M. P., and Aitchison, J. D. (1998). Karyopherins and kissing cousins. Trends Cell Biol 8, 184-188.
84. Yang, W., Gelles, J., and Musser, S. M. (2004). Imaging of singlemolecule translocation through nuclear pore complexes. Proc Natl Acad Sci U S A 101, 12887-12892.
85. Yang, W., and Musser, S. M. (2006a). Nuclear import time and transport efficiency depend on importin β concentration. J Cell Biol 1174, 951-961.
86. Yang, W., and Musser, S. M. (2006b). Visualizing single molecules interacting with nuclear pore complexes by narrow-field epifluorescence microscopy. Methods 39, 316-328.
87. Yildiz, A., Forkey, J. N., McKinney, S. A., Ha, T., Goldman, Y. E., and Selvin, P. R. (2003). Myosin V walks hand-over-hand: single fluorophore imaging with 1. 5-nm localization. Science 300, 2061-2065.
88. Yildiz, A., Tomishige, M., Vale, R. D., and Selvin, P. R. (2004). Kinesin walks hand-over-hand. Science 303, 676-678.
89. Yokoyama, N., Hayashi, N., Seki, T., Panté, N., Ohba, T., Nishii, K., Kuma, K., Hayashida, T., Miyata, T., Aebi, U., et al. (1995). A giant nucleopore protein that binds Ran/TC4. Nature 376, 184-188.
90. Zhuang, X. (2005). Single-molecule RNA science. Annu Rev Biophys Biomol Struct 34, 399-414.