Importins and beyond: Non-conventional nuclear transport mechanisms

Traffic

Volumn 10, Issue 9, 2009, Pages 1188-1198

  Wagstaff, Kylie M ^a   Jans, David A ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Calmodulin; Importin; Microtubule dependent transport; Nuclear import; Nuclear localization signal; Nucleoporin

Indexed keywords

CALCIUM; CALMODULIN; CALRETICULIN; KARYOPHERIN; NUCLEOPORIN;

CELL FUNCTION; CELL NUCLEUS MEMBRANE; CELL TRANSPORT; CYTOSKELETON; MICROTUBULE; NUCLEAR IMPORT; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; TARGET CELL;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CYTOPLASM; HUMANS; KARYOPHERINS; NUCLEAR LOCALIZATION SIGNALS; NUCLEAR PORE COMPLEX PROTEINS;

EID: 68549085409     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2009.00937.x     Document Type: Review

References (107)

1. Poon IK, Jans DA. Regulation of nuclear transport: Central role in development and transformation? Traffic 2005;6:173-186.
2. Goldfarb DS, Corbett AH, Mason DA, Harreman MT, Adam SA. Importin alpha: a multipurpose nuclear-transport receptor. Trends Cell Biol 2004;14:505-514.
3. Azuma Y, Dasso M. The role of Ran in nuclear function. Curr Opin Cell Biol 2000;12:302-307.
4. Stochaj U, Rother KI. Nucleocytoplasmic trafficking of proteins: With or without Ran? Bioessays 1999;21:579-589.
5. Pouton CW, Wagstaff KM, Roth DM, Moseley GW, Jans DA. Targeted delivery to the nucleus. Adv Drug Deliv Rev 2007;59:698-717.
6. Campbell EM, Hope TJ. Role of the cytoskeleton in nuclear import. Adv Drug Deliv Rev 2003;55:761-771.
7. Dohner K, Nagel CH, Sodeik B. Viral stop-and-go along microtubules: taking a ride with dynein and kinesins. Trends Microbiol 2005;13:320-327.
8. Giannakakou P, Sackett DL, Ward Y, Webster KR, Blagosklonny MV, Fojo T. p53 is associated with cellular microtubules and is transported to the nucleus by dynein. [see comment]. Nat Cell Biol 2000;2:709-717.
9. Lam MH, Thomas RJ, Loveland KL, Schilders S, Gu M, Martin TJ, Gillespie MT, Jans DA. Nuclear transport of parathyroid hormone (PTH)-related protein is dependent on microtubules. Mol Endocrinol 2002;16:390-401.
10. Salman H, Abu-Arish A, Oliel S, Loyter A, Klafter J, Granek R, Elbaum M. Nuclear localization signal peptides induce molecular delivery along microtubules. Biophys J 2005;89:2134-2145.
11. Digard P, Elton D, Bishop K, Medcalf E, Weeds A, Pope B. Modulation of nuclear localization of the influenza virus nucleoprotein through interaction with actin filaments. J Virol 1999;73:2222-2231.
12. Sodeik B, Ebersold MW, Helenius A. Microtubule-mediated transport of incoming herpes simplex virus 1 capsids to the nucleus. J Cell Biol 1997;136:1007-1021.
13. McDonald D, Vodicka MA, Lucero G, Svitkina TM, Borisy GG, Emerman M, Hope TJ. Visualization of the intracellular behavior of HIV in living cells. [see comment]. J Cell Biol 2002;159:441-452.
14. Lakadamyali M, Rust MJ, Babcock HP, Zhuang X. Visualizing infection of individual influenza viruses. Proc Natl Acad Sci U S A 2003;100:9280-9285.
15. Funk A, Mhamdi M, Lin L, Will H, Sirma H. Itinerary of hepatitis B viruses: Delineation of restriction points critical for infectious entry. J Virol 2004;78:8289-8300.
16. Roth DM, Moseley GW, Glover D, Pouton CW, Jans DA. A microtubule-facilitated nuclear import pathway for cancer regulatory proteins. Traffic 2007;8:673-686.
17. Moseley GW, Roth DM, DeJesus MA, Leyton DL, Filmer RP, Pouton CW, Jans DA. Dynein light chain association sequences can facilitate nuclear protein import. Mol Biol Cell 2007;18:3204-3213.
18. Gleason EL, Hogan JC, Stephens JM. Stabilization, not polymerization, of microtubules inhibits the nuclear translocation of STATs in adipocytes. Biochem Biophys Res Commun 2004;325:716-718.
19. Lopez-Perez M, Salazar EP. A role for the cytoskeleton in STAT5 activation in MCF7 human breast cancer cells stimulated with EGF. Int J Biochem Cell Biol 2006;38:1716-1728.
20. Phung-Koskas T, Pilon A, Pous C, Betzina C, Sturm M, Bourguet-Kondracki ML, Durand G, Drechou A. STAT5B-mediated growth hormone signaling is organized by highly dynamic microtubules in hepatic cells. J Biol Chem 2005;280:1123-1131.
21. Fagerlund R, Kinnunen L, Kohler M, Julkunen I, Melen K. NF-κB is transported into the nucleus by importin α3 and importin α4. J Biol Chem 2005;280:15942-15951.
22. Fazal F, Minhajuddin M, Bijli KM, McGrath JL, Rahman A. Evidence for actin cytoskeleton-dependent and -independent pathways for RelA/p65 nuclear translocation in endothelial cells. J Biol Chem 2007;282:3940-3950.
23. Sweitzer TD, Hanover JA. Calmodulin activates nuclear protein import: A link between signal transduction and nuclear transport. Proc Natl Acad Sci U S A 1996;93:14574-14579.
24. Hanover JA, Love DC, Prinz WA. Calmodulin-driven nuclear entry: Trigger for sex determination and terminal differentiation. J Biol Chem 2009;12593-12597.
25. Vogel HJ. The Merck Frosst Award Lecture 1994. Calmodulin: A versatile calcium mediator protein. Biochem Cell Biol 1994;72:357-376.
26. Gilchrist JS, Czubryt MP, Pierce GN. Calcium and calcium-binding proteins in the nucleus. Mol Cell Biochem 1994;135:79-88.
27. Taules M, Rius E, Talaya D, Lopez-Girona A, Bachs O, Agell N. Calmodulin is essential for cyclin-dependent kinase 4 (Cdk4) activity and nuclear accumulation of cyclin D1-Cdk4 during G1. J Biol Chem 1998;273:33279-33286.
28. Argentaro A, Sim H, Kelly S, Preiss S, Clayton A, Jans DA, Harley VR. A SOX9 defect of calmodulin-dependent nuclear import in campomelic dysplasia/autosomal sex reversal. J Biol Chem 2003;278:33839-33847.
29. Forwood JK, Kaur G, Jans DA. Nuclear import properties of the sex-determining factor SRY. Methods Mol Biol 2007;390:83-97.
30. Hanover JA, Love DC, DeAngelis N, O'Kane ME, Lima-Miranda R, Schulz T, Yen YM, Johnson RC, Prinz WA. The High Mobility Group Box Transcription Factor Nhp6Ap enters the nucleus by a calmodulin-dependent, Ran-independent pathway. J Biol Chem 2007;282:33743-33751.
31. Sim H, Rimmer K, Kelly S, Ludbrook LM, Clayton AH, Harley VR. Defective calmodulin-mediated nuclear transport of the sex-determining region of the Y chromosome (SRY) in XY sex reversal. Mol Endocrinol 2005;19:1884-1892.
32. Sim H, Argentaro A, Harley VR. Boys, girls and shuttling of SRY and SOX9. Trends Endocrinol Metab 2008;19:213-222.
33. Harley VR, Layfield S, Mitchell CL, Forwood JK, John AP, Briggs LJ, McDowall SG, Jans DA. Defective importin beta recognition and nuclear import of the sex-determining factor SRY are associated with XY sex-reversing mutations. Proc Natl Acad Sci U S A 2003;100:7045-7050.
34. Li B, Zhang W, Chan G, Jancso-Radek A, Liu S, Weiss MA. Human sex reversal due to impaired nuclear localization of SRY. A clinical correlation. J Biol Chem 2001;276:46480-46484.
35. Smith JM, Koopman PA. The ins and outs of transcriptional control: nucleocytoplasmic shuttling in development and disease. Trends Genet 2004;20:4-8.
36. Pruschy M, Ju Y, Spitz L, Carafoli E, Goldfarb DS. Facilitated nuclear transport of calmodulin in tissue culture cells. J Cell Biol 1994;127:1527-1536.
37. Antonsson A, Hughes K, Edin S, Grundstrom T. Regulation of c-Rel nuclear localization by binding of Ca2+/calmodulin. Mol Cell Biol 2003;23:1418-1427.
38. Corneliussen B, Holm M, Waltersson Y, Onions J, Hallberg B, Thornell A, Grundstrom T. Calcium/calmodulin inhibition of basic-helix-loop-helix transcription factor domains. Nature 1994;368:760-764.
39. Hauser J, Saarikettu J, Grundstrom T. Calcium regulation of myogenesis by differential calmodulin inhibition of basic helix-loop-helix transcription factors. Mol Biol Cell 2008;19:2509-2519.
40. Hermann S, Saarikettu J, Onions J, Hughes K, Grundstrom T. Calcium regulation of basic helix-loop-helix transcription factors. Cell Calcium 1998;23:135-142.
41. Onions J, Hermann S, Grundstrom T. Basic helix-loop-helix protein sequences determining differential inhibition by calmodulin and S-100 proteins. J Biol Chem 1997;272:23930-23937.
42. Onions J, Hermann S, Grundstrom T. A novel type of calmodulin interaction in the inhibition of basic helix-loop-helix transcription factors. Biochemistry (Mosc) 2000;39:4366-4374.
43. Saarikettu J, Sveshnikova N, Grundstrom T. Calcium/calmodulin inhibition of transcriptional activity of E-proteins by prevention of their binding to DNA. J Biol Chem 2004;279:41004-41011.
44. Holaska JM, Black BE, Love DC, Hanover JA, Leszyk J, Paschal BM. Calreticulin is a receptor for nuclear export. J Cell Biol 2001;152:127-140.
45. Liu J, DeFranco DB. Protracted nuclear export of glucocorticoid receptor limits its turnover and does not require the exportin 1/CRM1-directed nuclear export pathway. Mol Endocrinol 2000;14:40-51.
46. Holaska JM, Black BE, Rastinejad F, Paschal BM. Ca2+-dependent nuclear export mediated by calreticulin. Mol Cell Biol 2002;22:6286-6297.
47. Black BE, Holaska JM, Rastinejad F, Paschal BM. DNA binding domains in diverse nuclear receptors function as nuclear export signals. Curr Biol 2001;11:1749-1758.
48. Walther RF, Lamprecht C, Ridsdale A, Groulx I, Lee S, Lefebvre YA, Hache RJ. Nuclear export of the glucocorticoid receptor is accelerated by cell fusion-dependent release of calreticulin. J Biol Chem 2003;278:37858-37864.
49. Bunn CF, Neidig JA, Freidinger KE, Stankiewicz TA, Weaver BS, McGrew J, Allison LA. Nucleocytoplasmic shuttling of the thyroid hormone receptor alpha. Mol Endocrinol 2001;15:512-533.
50. Grespin ME, Bonamy GM, Roggero VR, Cameron NG, Adam LE, Atchison AP, Fratto VM, Allison LA. Thyroid hormone receptor alpha1 follows a cooperative CRM1/calreticulin-mediated nuclear export pathway. J Biol Chem 2008;283:25576-25588.
51. Alefantis T, Flaig KE, Wigdahl B, Jain P. Interaction of HTLV-1 Tax protein with calreticulin: Implications for Tax nuclear export and secretion. Biomed Pharmacother 2007;61:194-200.
52. Ghildyal R, Ho A, Wagstaff KM, Dias MM, Barton CL, Jans P, Bardin P, Jans DA. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry (Mosc) 2005;44:12887-12895.
53. Hearps AC, Jans DA. HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism. Biochem J 2006;398:475-484.
54. Briggs LJ, Johnstone RW, Elliot RM, Xiao CY, Dawson M, Trapani JA, Jans DA. Novel properties of the protein kinase CK2-site-regulated nuclear- localization sequence of the interferon-induced nuclear factor IFI 16. Biochem J 2001;353:69-77.
55. Lixin R, Efthymiadis A, Henderson B, Jans DA. Novel properties of the nucleolar targeting signal of human angiogenin. Biochem Biophys Res Commun 2001;284:185-193.
56. Kose S, Imamoto N, Tachibana T, Shimamoto T, Yoneda Y. Ran-unassisted nuclear migration of a 97-kD component of nuclear pore-targeting complex. J Cell Biol 1997;139:841-849.
57. Nakielny S, Dreyfuss G. Import and export of the nuclear protein import receptor transportin by a mechanism independent of GTP hydrolysis. Curr Biol 1998;8:89-95.
58. Kehlenbach RH, Dickmanns A, Gerace L. Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT In vitro. J Cell Biol 1998;141:863-874.
59. Kutay U, Lipowsky G, Izaurralde E, Bischoff FR, Schwarzmaier P, Hartmann E, Gorlich D. Identification of a tRNA-specific nuclear export receptor. Mol Cell 1998;1:359-369.
60. Nelson WJ, Nusse R. Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004;303:1483-1487.
61. Polakis P. Wnt signaling and cancer. Genes Dev 2000;14:1837-1851.
62. Huber O, Korn R, McLaughlin J, Ohsugi M, Herrmann BG, Kemler R. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev 1996;59:3-10.
63. Kim K, Hay ED. New evidence that nuclear import of endogenous beta-catenin is LEF-1 dependent, while LEF-1 independent import of exogenous beta-catenin leads to nuclear abnormalities. Cell Biol Int 2001;25:1149-1161.
64. Fagotto F, Gluck U, Gumbiner BM. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of beta-catenin. Curr Biol 1998;8:181-190.
65. Yokoya F, Imamoto N, Tachibana T, Yoneda Y. beta-catenin can be transported into the nucleus in a Ran-unassisted manner. Mol Biol Cell 1999;10:1119-1131.
66. Asally M, Yoneda Y. Beta-catenin can act as a nuclear import receptor for its partner transcription factor, lymphocyte enhancer factor-1 (LEF-1). Exp Cell Res 2005;308:357-363.
67. Peifer M, Berg S, Reynolds AB. A repeating amino acid motif shared by proteins with diverse cellular roles. Cell 1994;76:789-791.
68. Suh EK, Gumbiner BM. Translocation of beta-catenin into the nucleus independent of interactions with FG-rich nucleoporins. Exp Cell Res 2003;290:447-456.
69. Koike M, Kose S, Furuta M, Taniguchi N, Yokoya F, Yoneda Y, Imamoto N. beta-Catenin shows an overlapping sequence requirement but distinct molecular interactions for its bidirectional passage through nuclear pores. J Biol Chem 2004;279:34038-34047.
70. Tsuji T, Sheehy N, Gautier VW, Hayakawa H, Sawa H, Hall WW. The nuclear import of the human T lymphotropic virus type I (HTLV-1) tax protein is carrier- and energy-independent. J Biol Chem 2007;282:13875-13883.
71. Shi Y, Massague J. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
72. Xu L, Alarcon C, Col S, Massague J. Distinct domain utilization by Smad3 and Smad4 for nucleoporin interaction and nuclear import. J Biol Chem 2003;278:42569-42577.
73. Xiao Z, Latek R, Lodish HF. An extended bipartite nuclear localization signal in Smad4 is required for its nuclear import and transcriptional activity. Oncogene 2003;22:1057-1069.
74. Zhong H, Takeda A, Nazari R, Shio H, Blobel G, Yaseen NR. Carrier-independent nuclear import of the transcription factor PU.1 via RanGTP-stimulated binding to Nup153. J Biol Chem 2005;280:10675-10682.
75. Tam WF, Lee LH, Davis L, Sen R. Cytoplasmic sequestration of rel proteins by IkappaBalpha requires CRM1-dependent nuclear export. Mol Cell Biol 2000;20:2269-2284.
76. Lee SH, Hannink M. The N-terminal nuclear export sequence of IkappaBalpha is required for RanGTP-dependent binding to CRM1. J Biol Chem 2001;276:23599-23606.
77. Turpin P, Hay RT, Dargemont C. Characterization of IkappaBalpha nuclear import pathway. J Biol Chem 1999;274:6804-6812.
78. Sachdev S, Bagchi S, Zhang DD, Mings AC, Hannink M. Nuclear import of IkappaBalpha is accomplished by a ran-independent transport pathway. Mol Cell Biol 2000;20:1571-1582.
79. Lee SH, Hannink M. Characterization of the nuclear import and export functions of Ikappa B(epsilon). J Biol Chem 2002;277:23358-23366.
80. Weil R, Sirma H, Giannini C, Kremsdorf D, Bessia C, Dargemont C, Brechot C, Israel A. Direct association and nuclear import of the hepatitis B virus X protein with the NF-kappaB inhibitor IkappaBalpha. Mol Cell Biol 1999;19:6345-6354.
81. Rudt F, Pieler T. Cytosolic import factor- and Ran-independent nuclear transport of ribosomal protein L5. Eur J Cell Biol 2001;80:661-668.
82. La Boissiere S, Hughes T, O'Hare P. HCF-dependent nuclear import of VP16. EMBO J 1999;18:480-489.
83. Schmalz D, Hucho F, Buchner K. Nuclear import of protein kinase C occurs by a mechanism distinct from the mechanism used by proteins with a classical nuclear localization signal. J Cell Sci 1998;111:1823-1830.
84. Hetzer M, Mattaj IW. An ATP-dependent, Ran-independent mechanism for nuclear import of the U1A and U2B" spliceosome proteins. J Cell Biol 2000;148:293-303.
85. Duverger E, Roche AC, Monsigny M. N-acetylglucosamine-dependent nuclear import of neoglycoproteins. Glycobiology 1996;6:381-386.
86. Monsigny M, Rondanino C, Duverger E, Fajac I, Roche AC. Glyco-dependent nuclear import of glycoproteins, glycoplexes and glycosylated plasmids. Biochim Biophys Acta 2004;1673:94-103.
87. Duverger E, Carpentier V, Roche AC, Monsigny M. Sugar-dependent nuclear import of glycoconjugates from the cytosol. Exp Cell Res 1993;207:197-201.
88. Rondanino C, Bousser MT, Monsigny M, Roche AC. Sugar-dependent nuclear import of glycosylated proteins in living cells. Glycobiology 2003;13:509-519.
89. Kampinga HH, Brunsting JF, Stege GJ, Burgman PW, Konings AW. Thermal protein denaturation and protein aggregation in cells made thermotolerant by various chemicals: Role of heat shock proteins. Exp Cell Res 1995;219:536-546.
90. Czubryt MP, Austria JA, Pierce GN. Hydrogen peroxide inhibition of nuclear protein import is mediated by the mitogen-activated protein kinase, ERK2. J Cell Biol 2000;148:7-16.
91. Dean DA, Dean BS, Muller S, Smith LC. Sequence requirements for plasmid nuclear import. Exp Cell Res 1999;253:713-722.
92. Dean DA, Byrd JN Jr, Dean BS. Nuclear targeting of plasmid DNA in human corneal cells. Curr Eye Res 1999;19:66-75.
93. Dean DA, Strong DD, Zimmer WE. Nuclear entry of nonviral vectors. Gene Ther 2005;12:881-890.
94. Wilson GL, Dean BS, Wang G, Dean DA. Nuclear import of plasmid DNA in digitonin-permeabilized cells requires both cytoplasmic factors and specific DNA sequences. J Biol Chem 1999;274:22025-22032.
95. Vacik J, Dean BS, Zimmer WE, Dean DA. Cell-specific nuclear import of plasmid DNA. Gene Ther 1999;6:1006-1014.
96. Miller AM, Dean DA. Cell-specific nuclear import of plasmid DNA in smooth muscle requires tissue-specific transcription factors and DNA sequences. Gene Ther 2008;15:1107-1115.
97. Chan CK, Hubner S, Hu W, Jans DA. Mutual exclusivity of DNA binding and nuclear localization signal recognition by the yeast transcription factor GAL4: Implications for nonviral DNA delivery. Gene Ther 1998;5:1204-1212.
98. Cohen S, Behzad AR, Carroll JB, Pante N. Parvoviral nuclear import: bypassing the host nuclear-transport machinery. J Gen Virol 2006;87:3209-3213.
99. Cohen S, Pante N. Pushing the envelope: Microinjection of Minute virus of mice into Xenopus oocytes causes damage to the nuclear envelope. J Gen Virol 2005;86:3243-3252.
100. Hansen J, Qing K, Srivastava A. Infection of purified nuclei by adeno-associated virus 2. Mol Ther 2001;4:289-296.
101. Gustin KE, Sarnow P. Effects of poliovirus infection on nucleo-cytoplasmic trafficking and nuclear pore complex composition. EMBO J 2001;20:240-249.
102. Gustin KE, Sarnow P. Inhibition of nuclear import and alteration of nuclear pore complex composition by rhinovirus. J Virol 2002;76:8787-8796.
103. Belov GA, Evstafieva AG, Rubtsov YP, Mikitas OV, Vartapetian AB, Agol VI. Early alteration of nucleocytoplasmic traffic induced by some RNA viruses. Virology 2000;275:244-248.
104. Belov GA, Lidsky PV, Mikitas OV, Egger D, Lukyanov KA, Bienz K, Agol VI. Bidirectional increase in permeability of nuclear envelope upon poliovirus infection and accompanying alterations of nuclear pores. J Virol 2004;78:10166-10177.
105. Yao X, Chen X, Cottonham C, Xu L. Preferential utilization of Imp7/8 in nuclear import of Smads. J Biol Chem 2008;283:22867-22874.
106. Lam MH, Briggs LJ, Hu W, Martin TJ, Gillespie MT, Jans DA. Importin beta recognizes parathyroid hormone-related protein with high affinity and mediates its nuclear import in the absence of importin alpha. J Biol Chem 1999;274:7391-7398.
107. Liang SH, Clarke MF. The nuclear import of p53 is determined by the presence of a basic domain and its relative position to the nuclear localization signal. Oncogene 1999;18:2163-2166.