Nuclear transport factors: Global regulation of mitosis

Current Opinion in Cell Biology

Volumn 35, Issue , 2015, Pages 78-90

  Forbes, Douglass J ^a   Travesa, Anna ^a   Nord, Matthew S ^a   Bernis, Cyril ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; KARYOPHERIN BETA; RAN PROTEIN; ACTIN;

CELL CYCLE; CELL NUCLEUS; CENTROMERE; COMPLEX FORMATION; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SPINDLE CELL; ACTIVE TRANSPORT; ANIMAL; CYTOSKELETON; HUMAN; METABOLISM;

VERTEBRATA;

ACTINS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; CYTOSKELETON; HUMANS; MITOSIS; RAN GTP-BINDING PROTEIN;

EID: 84938684565     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2015.04.012     Document Type: Review

References (115)

1. Maresca T.J., Heald R. Methods for studying spindle assembly and chromosome condensation in Xenopus egg extracts. Methods Mol Biol 2006, 322:459-474.
2. Kalab P., Pu R.T., Dasso M. The ran GTPase regulates mitotic spindle assembly. Curr Biol 1999, 9:481-484.
3. Zhang C., Hughes M., Clarke P.R. Ran-GTP stabilises microtubule asters and inhibits nuclear assembly in Xenopus egg extracts. J Cell Sci 1999, 112(Pt 14):2453-2461.
4. Nachury M.V., Maresca T.J., Salmon W.C., Waterman-Storer C.M., Heald R., Weis K. Importin beta is a mitotic target of the small GTPase Ran in spindle assembly. Cell 2001, 104:95-106.
5. Wiese C., Wilde A., Moore M.S., Adam S.A., Merdes A., Zheng Y. Role of importin-beta in coupling Ran to downstream targets in microtubule assembly. Science 2001, 291:653-656.
6. Gruss O.J., Carazo-Salas R.E., Schatz C.A., Guarguaglini G., Kast J., Wilm M., Le Bot N., Vernos I., Karsenti E., Mattaj I.W. Ran induces spindle assembly by reversing the inhibitory effect of importin alpha on TPX2 activity. Cell 2001, 104:83-93.
7. Kufer T.A., Sillje H.H., Korner R., Gruss O.J., Meraldi P., Nigg E.A. Human TPX2 is required for targeting Aurora-A kinase to the spindle. J Cell Biol 2002, 158:617-623.
8. Quimby B.B., Dasso M. The small GTPase Ran: interpreting the signs. Curr Opin Cell Biol 2003, 15:338-344.
9. Kalab P., Heald R. The RanGTP gradient - a GPS for the mitotic spindle. J Cell Sci 2008, 121:1577-1586.
10. Harel A., Forbes D.J. Importin beta: conducting a much larger cellular symphony. Mol Cell 2004, 16:319-330.
11. Ohtsubo M., Okazaki H., Nishimoto T. The RCC1 protein, a regulator for the onset of chromosome condensation locates in the nucleus and binds to DNA. J Cell Biol 1989, 109:1389-1397.
12. Lohka M.J., Maller J.L. Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts. J Cell Biol 1985, 101:518-523.
13. Newport J. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell 1987, 48:205-217.
14. Newport J., Spann T. Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes. Cell 1987, 48:219-230.
15. Chan R.C., Forbes D.I. In vitro study of nuclear assembly and nuclear import using Xenopus egg extracts. Methods Mol Biol 2006, 322:289-300.
16. Bernis C., Forbes D.J. Analysis of nuclear reconstitution, nuclear envelope assembly, and nuclear pore assembly using Xenopus in vitro assays. Methods Cell Biol 2014, 122:165-191.
17. Yokoyama H., Gruss O.J., Rybina S., Caudron Mw, Schelder M., Wilm M., Mattaj I.W., Karsenti E. Cdk11 is a RanGTP-dependent microtubule stabilization factor that regulates spindle assembly rate. J Cell Biol 2008, 180:867-875.
18. Arnaoutov A., Azuma Y., Ribbeck K., Joseph J., Boyarchuk Y., Karpova T., McNally J., Dasso M. Crm1 is a mitotic effector of Ran-GTP in somatic cells. Nat Cell Biol 2005, 7:626-632.
19. Zhang M.S., Arnaoutov A., Dasso M. RanBP1 governs spindle assembly by defining mitotic Ran-GTP production. Dev Cell 2014, 31:393-404.
20. Blower M.D., Nachury M., Heald R., Weis K. A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly. Cell 2005, 121:223-234.
21. Tsai M.Y., Wang S., Heidinger J.M., Shumaker D.K., Adam S.A., Goldman R.D., Zheng Y. A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 2006, 311:1887-1893.
22. Schweizer N., Weiss M., Maiato H. The dynamic spindle matrix. Curr Opin Cell Biol 2014, 28:1-7.
23. Dikovskaya D., Li Z., Newton I.P., Davidson I., Hutchins J.R., Kalab P., Clarke P.R., Nathke I.S. Microtubule assembly by the Apc protein is regulated by importin-beta--RanGTP. J Cell Sci 2010, 123:736-746.
24. Yokoyama H., Nakos K., Santarella-Mellwig R., Rybina S., Krijgsveld J., Koffa M.D., Mattaj I.W. CHD4 is a RanGTP-dependent MAP that stabilizes microtubules and regulates bipolar spindle formation. Curr Biol 2013, 23:2443-2451.
25. Yokoyama H., Rybina S., Santarella-Mellwig R., Mattaj I.W., Karsenti E. ISWI is a RanGTP-dependent MAP required for chromosome segregation. J Cell Biol 2009, 187:813-829.
26. Meunier S., Vernos I. K-fibre minus ends are stabilized by a RanGTP-dependent mechanism essential for functional spindle assembly. Nat Cell Biol 2011, 13:1406-1414.
27. Wozniak R., Burke B., Doye V. Nuclear transport and the mitotic apparatus: an evolving relationship. Cell Mol Life Sci 2010, 67:2215-2230.
28. Chatel G., Fahrenkrog B. Nucleoporins: Leaving the nuclear pore complex for a successful mitosis. Cell Signal 2011, 23:1555-1562.
29. Imamoto N., Funakoshi T. Nuclear pore dynamics during the cell cycle. Curr Opin Cell Biol 2012, 24:453-459.
30. Sood V., Brickner J.H. Nuclear pore interactions with the genome. Curr Opin Genet Dev 2014, 25:43-49.
31. Pascual-Garcia P., Capelson M. Nuclear pores as versatile platforms for gene regulation. Curr Opin Genet Dev 2014, 25:110-117.
32. Mitchison T.J. Mechanism and function of poleward flux in Xenopus extract meiotic spindles. Philos Trans R Soc Lond B Biol Sci 2005, 360:623-629.
33. Dumont S., Mitchison T.J. Force and length in the mitotic spindle. Curr Biol 2009, 19:R749-R761.
34. Torosantucci L., De Luca M., Guarguaglini G., Lavia P., Degrassi F. Localized RanGTP accumulation promotes microtubule nucleation at kinetochores in somatic mammalian cells. Mol Biol Cell 2008, 19:1873-1882.
35. Helmke K.J., Heald R., Wilbur J.D. Interplay between spindle architecture and function. Int Rev Cell Mol Biol 2013, 306:83-125.
36. Ciciarello M., Mangiacasale R., Lavia P. Spatial control of mitosis by the GTPase Ran. Cell Mol Life Sci 2007, 64:1891-1914.
37. Belgareh N., Rabut G., Bai S.W., van Overbeek M., Beaudouin J., Daigle N., Zatsepina O.V., Pasteau F., Labas V., Fromont-Racine M., et al. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J Cell Biol 2001, 154:1147-1160.
38. Orjalo A.V., Arnaoutov A., Shen Z., Boyarchuk Y., Zeitlin S.G., Fontoura B., Briggs S., Dasso M., Forbes D.J. The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol Biol Cell 2006, 17:3806-3818.
39. Rasala B.A., Orjalo A.V., Shen Z., Briggs S., Forbes D.J. ELYS is a dual nucleoporin/kinetochore protein required for nuclear pore assembly and proper cell division. Proc Natl Acad Sci 2006, 103:17801-17806.
40. Rasala B.A., Ramos C., Harel A., Forbes D.J. Capture of AT-rich chromatin by ELYS recruits POM121 and NDC1 to initiate nuclear pore assembly. Mol Biol Cell 2008, 19:3982-3996.
41. Loiodice I., Alves A., Rabut G., Van Overbeek M., Ellenberg J., Sibarita J.B., Doye V. The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol Biol Cell 2004, 15:3333-3344.
42. Mishra R.K., Chakraborty P., Arnaoutov A., Fontoura B.M., Dasso M. The Nup107-160 complex and gamma-TuRC regulate microtubule polymerization at kinetochores. Nat Cell Biol 2010, 12:164-169.
43. Franz C., Walczak R., Yavuz S., Santarella R., Gentzel M., Askjaer P., Galy V., Hetzer M., Mattaj I.W., Antonin W. MEL-28/ELYS is required for the recruitment of nucleoporins to chromatin and postmitotic nuclear pore complex assembly. EMBO Rep 2007, 8:165-172.
44. Yokoyama H., Koch B., Walczak R., Ciray-Duygu F., Gonzalez-Sanchez J.C., Devos D.P., Mattaj I.W., Gruss O.J. The nucleoporin MEL-28 promotes RanGTP-dependent gamma-tubulin recruitment and microtubule nucleation in mitotic spindle formation. Nat Commun 2014, 5:3270.
45. Scrofani J., Sardon T., Meunier S., Vernos I. Microtubule nucleation in mitosis by a RanGTP-dependent protein complex. Curr Biol 2015, 25:131-140.
46. Di Fiore B., Ciciarello M., Lavia P. Mitotic functions of the Ran GTPase network: the importance of being in the right place at the right time. Cell Cycle 2004, 3:305-313.
47. Pinyol R., Scrofani J., Vernos I. The role of NEDD1 phosphorylation by Aurora A in chromosomal microtubule nucleation and spindle function. Curr Biol 2013, 23:143-149.
48. Shaulov L., Gruber R., Cohen I., Harel A. A dominant-negative form of POM121 binds chromatin and disrupts the two separate modes of nuclear pore assembly. J Cell Sci 2011, 124:3822-3834.
49. Lau C.K., Delmar V.A., Chan R.C., Phung Q., Bernis C., Fichtman B., Rasala B.A., Forbes D.J. Transportin regulates major mitotic assembly events: from spindle to nuclear pore assembly. Mol Biol Cell 2009, 20:4043-4058.
50. Rotem A., Gruber R., Shorer H., Shaulov L., Klein E., Harel A. Importin beta regulates the seeding of chromatin with initiation sites for nuclear pore assembly. Mol Biol Cell 2009, 20:4031-4042.
51. Galy V., Askjaer P., Franz C., Lopez-Iglesias C., Mattaj I.W. MEL-28, a novel nuclear-envelope and kinetochore protein essential for zygotic nuclear-envelope assembly in C. elegans. Curr Biol 2006, 16:1748-1756.
52. Bernis C., Swift-Taylor B., Nord M., Carmona S., Chook Y.M., Forbes D.J. Transportin acts to regulate mitotic assembly events by target binding rather than Ran sequestration. Mol Biol Cell 2014, 25:992-1009.
53. Petry S., Groen A.C., Ishihara K., Mitchison T.J., Vale R.D. Branching microtubule nucleation in Xenopus egg extracts mediated by augmin and TPX2. Cell 2013, 152:768-777.
54. Zheng Y., Iglesias P.A. Nucleating new branches from old. Cell 2013, 152:669-670.
55. Petry S., Pugieux C., Nedelec F.J., Vale R.D. Augmin promotes meiotic spindle formation and bipolarity in Xenopus egg extracts. Proc Natl Acad Sci U S A 2011, 108:14473-14478.
56. Petry S., Vale R.D. A new cap for kinetochore fibre minus ends. Nat Cell Biol 2011, 13:1389-1391.
57. Cross M.K., Powers M.A. Nup98 regulates bipolar spindle assembly through association with microtubules and opposition of MCAK. Mol Biol Cell 2011, 22:661-672.
58. Ryan K.J., McCaffery J.M., Wente S.R. The Ran GTPase cycle is required for yeast nuclear pore complex assembly. J Cell Biol 2003, 160:1041-1053.
59. Kee H.L., Dishinger J.F., Blasius T.L., Liu C.J., Margolis B., Verhey K.J. A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 2012, 14:431-437. See annotation to Ref. [60].
60. Fan S., Whiteman E.L., Hurd T.W., McIntyre J.C., Dishinger J.F., Liu C.J., Martens J.R., Verhey K.J., Sajjan U., Margolis B. Induction of Ran GTP drives ciliogenesis. Mol Biol Cell 2011, 22:4539-4548.
61. Arnaoutov A., Dasso M. The Ran GTPase regulates kinetochore function. Developmental Cell 2003, 5:99-111.
62. Hutchins J.R., Moore W.J., Hood F.E., Wilson J.S., Andrews P.D., Swedlow J.R., Clarke P.R. Phosphorylation regulates the dynamic interaction of RCC1 with chromosomes during mitosis. Curr Biol 2004, 14:1099-1104.
63. Halpin D., Kalab P., Wang J., Weis K., Heald R. Mitotic spindle assembly around RCC1-coated beads in Xenopus egg extracts. PLoS Biol 2011, 9:e1001225.
64. Kalab P., Solc P., Motlik J. The role of RanGTP gradient in vertebrate oocyte maturation. Results Probl Cell Differ 2011, 53:235-267.
65. Helmke K.J., Heald R. TPX2 levels modulate meiotic spindle size and architecture in Xenopus egg extracts. J Cell Biol 2014, 206:385-393.
66. Hazel J., Krutkramelis K., Mooney P., Tomschik M., Gerow K., Oakey J., Gatlin J.C. Changes in cytoplasmic volume are sufficient to drive spindle scaling. Science 2013, 342:853-856.
67. Kiyomitsu T., Cheeseman I.M. Chromosome- and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat Cell Biol 2012, 14:311-317. See annotation to Ref. [111].
68. Zhang C., Clarke P.R. Chromatin-independent nuclear envelope assembly induced by Ran GTPase in Xenopus egg extracts. Science 2000, 288:1429-1432.
69. Harel A., Chan R.C., Lachish-Zalait A., Zimmerman E., Elbaum M., Forbes D.J. Importin beta negatively regulates nuclear membrane fusion and nuclear pore complex assembly. Mol Biol Cell 2003, 14:4387-4396.
70. Hachet V., Kocher T., Wilm M., Mattaj I.W. Importin alpha associates with membranes and participates in nuclear envelope assembly in vitro. EMBO J 2004, 23:1526-1535.
71. Walther T.C., Askjaer P., Gentzel M., Habermann A., Griffiths G., Wilm M., Mattaj I.W., Hetzer M. RanGTP mediates nuclear pore complex assembly. Nature 2003, 424:689-694.
72. Hetzer M., Gruss O.J., Mattaj I.W. The Ran GTPase as a marker of chromosome position in spindle formation and nuclear envelope assembly. Nat Cell Biol 2002, 4:E177-E184.
73. Lu X., Shi Y., Lu Q., Ma Y., Luo J., Wang Q., Ji J., Jiang Q., Zhang C. Requirement for lamin B receptor and its regulation by importin {beta} and phosphorylation in nuclear envelope assembly during mitotic exit. J Biol Chem 2010, 285:33281-33293.
74. Delmar V.A., Chan R.C., Forbes D.J. Xenopus importin beta validates human importin beta as a cell cycle negative regulator. BMC Cell Biol 2008, 9:14.
75. Doucet C.M., Talamas J.A., Hetzer M.W. Cell cycle-dependent differences in nuclear pore complex assembly in metazoa. Cell 2010, 141:1030-1041.
76. Funakoshi T., Clever M., Watanabe A., Imamoto N. Localization of Pom121 to the inner nuclear membrane is required for an early step of interphase nuclear pore complex assembly. Mol Biol Cell 2011, 22:1058-1069.
77. Wandke C., Kutay U. Enclosing chromatin: reassembly of the nucleus after open mitosis. Cell 2013, 152:1222-1225.
78. D'Angelo M.A., Hetzer M.W. Structure, dynamics and function of nuclear pore complexes. Trends Cell Biol 2008, 18:456-466.
79. Gorlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Dev Biol 1999, 15:607-660.
80. Lee B.J., Cansizoglu A.E., Suel K.E., Louis T.H., Zhang Z., Chook Y.M. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 2006, 126:543-558.
81. Cansizoglu A.E., Lee B.J., Zhang Z.C., Fontoura B.M., Chook Y.M. Structure-based design of a pathway-specific nuclear import inhibitor. Nat Struct Mol Biol 2007, 14:452-454.
82. Chook Y.M., Suel K.E. Nuclear import by karyopherin-betas: recognition and inhibition. Biochim Biophys Acta 2011, 1813:1593-1606.
83. Kimura M., Kose S., Okumura N., Imai K., Furuta M., Sakiyama N., Tomii K., Horton P., Takao T., Imamoto N. Identification of cargo proteins specific for the nucleocytoplasmic transport carrier transportin by combination of an in vitro transport system and stable isotope labeling by amino acids in cell culture (SILAC)-based quantitative proteomics. Mol Cell Proteomics 2013, 12:145-157.
84. Twyffels L., Gueydan C., Kruys V. Transportin-1 and Transportin-2: protein nuclear import and beyond. FEBS Lett 2014, 588:1857-1868.
85. Zuccolo M., Alves A., Galy V., Bolhy S., Formstecher E., Racine V., Sibarita J.B., Fukagawa T., Shiekhattar R., Yen T., et al. The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO J 2007, 26:1853-1864.
86. Bischoff F.R., Gorlich D. RanBP1 is crucial for the release of RanGTP from importin beta-related nuclear transport factors. FEBS Lett 1997, 419:249-254.
87. Arnaoutov A., Dasso M. Ran-GTP regulates kinetochore attachment in somatic cells. Cell Cycle 2005, 4:1161-1165.
88. Clarke P.R. The Crm de la creme of mitosis. Nat Cell Biol 2005, 7:551-552.
89. Knauer S.K., Bier C., Habtemichael N., Stauber R.H. The Survivin-Crm1 interaction is essential for chromosomal passenger complex localization and function. EMBO Rep 2006, 7:1259-1265.
90. Roscioli E., Di Francesco L., Bolognesi A., Giubettini M., Orlando S., Harel A., Schinina M.E., Lavia P. Importin-beta negatively regulates multiple aspects of mitosis including RANGAP1 recruitment to kinetochores. J Cell Biol 2012, 196:435-450.
91. Liu Q., Jiang Q., Zhang C. A fraction of Crm1 locates at centrosomes by its CRIME domain and regulates the centrosomal localization of pericentrin. Biochem Biophys Res Commun 2009, 384:383-388.
92. Wu Z., Jiang Q., Clarke P.R., Zhang C. Phosphorylation of Crm1 by CDK1-cyclin-B promotes Ran-dependent mitotic spindle assembly. J Cell Sci 2013, 126:3417-3428.
93. Brodie K.M., Henderson B.R. Characterization of BRCA1 protein targeting, dynamics, and function at the centrosome: a role for the nuclear export signal, CRM1, and Aurora A kinase. J Biol Chem 2012, 287:7701-7716.
94. Brodie K.M., Mok M.T., Henderson B.R. Characterization of BARD1 targeting and dynamics at the centrosome: the role of CRM1, BRCA1 and the Q564H mutation. Cell Signal 2012, 24:451-459.
95. Rousselet A. Inhibiting Crm1 causes the formation of excess acentriolar spindle poles containing NuMA and B23, but does not affect centrosome numbers. Biol Cell 2009, 101:679-693.
96. Mor A., White M.A., Fontoura B.M. Nuclear trafficking in health and disease. Curr Opin Cell Biol 2014, 28:28-35. See annotation to Ref. [98].
97. Senapedis W.T., Baloglu E., Landesman Y. Clinical translation of nuclear export inhibitors in cancer. Semin Cancer Biol 2014, 27:74-86. See annotation to Ref. [98].
98. Tan D.S., Bedard P.L., Kuruvilla J., Siu L.L., Razak A.R. Promising SINEs for embargoing nuclear-cytoplasmic export as an anticancer strategy. Cancer Discov 2014, 4:527-537.
99. Kalab P., Pralle A., Isacoff E.Y., Heald R., Weis K. Analysis of a RanGTP-regulated gradient in mitotic somatic cells. Nature 2006, 440:697-701.
100. Soderholm J.F., Bird S.L., Kalab P., Sampathkumar Y., Hasegawa K., Uehara-Bingen M., Weis K., Heald R. Importazole, a small molecule inhibitor of the transport receptor importin-beta. ACS Chem Biol 2011, 6:700-708.
101. Lee Y.P., Wong C.H., Chan K.S., Lai S.K., Koh C.G., Li H.Y. In vivo FRET imaging revealed a regulatory role of RanGTP in kinetochore-microtubule attachments via Aurora B kinase. PLoS One 2012, 7:e45836.
102. Kalab P., Weis K., Heald R. Visualization of a Ran-GTP gradient in interphase and mitotic Xenopus egg extracts. Science 2002, 295:2452-2456.
103. Dumont J., Verlhac M.H. Using FRET to study RanGTP gradients in live mouse oocytes. Methods Mol Biol 2013, 957:107-120.
104. Roscioli E., Bolognesi A., Guarguaglini G., Lavia P. Ran control of mitosis in human cells: gradients and local signals. Biochem Soc Trans 2010, 38:1709-1714.
105. Hasegawa K., Ryu S.J., Kalab P. Chromosomal gain promotes formation of a steep RanGTP gradient that drives mitosis in aneuploid cells. J Cell Biol 2013, 200:151-161.
106. Kutay U., Izaurralde E., Bischoff F.R., Mattaj I.W., Gorlich D. Dominant-negative mutants of importin-beta block multiple pathways of import and export through the nuclear pore complex. EMBO J 1997, 16:1153-1163.
107. Song L., Rape M. Regulated degradation of spindle assembly factors by the anaphase-promoting complex. Mol Cell 2010, 38:369-382. See annotation to Ref. [108™].
108. Song L., Craney A., Rape M. Microtubule-dependent regulation of mitotic protein degradation. Mol Cell 2014, 53:179-192.
109. Vaites L.L., Harper J.W. Spindle assembly factor protection. Mol Cell 2014, 53:165-166.
110. Wrighton K.H. Mitosis: Microtubules protect spindle assembly factors. Nat Rev Mol Cell Biol 2014, 15:150-151.
111. Bird S.L., Heald R., Weis K. RanGTP and CLASP1 cooperate to position the mitotic spindle. Mol Biol Cell 2013, 24:2506-2514.
112. McNally F.J. Mechanisms of spindle positioning. J Cell Biol 2013, 200:131-140.
113. Samwer M., Dehne H.J., Spira F., Kollmar M., Gerlich D.W., Urlaub H., Gorlich D. The nuclear F-actin interactome of Xenopus oocytes reveals an actin-bundling kinesin that is essential for meiotic cytokinesis. EMBO J 2013, 32:1886-1902.
114. Hanz S., Perlson E., Willis D., Zheng J.Q., Massarwa R., Huerta J.J., Koltzenburg M., Kohler M., van-Minnen J., Twiss J.L., et al. Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 2003, 40:1095-1104.
115. Panayotis N., Karpova A., Kreutz M.R., Fainzilber M. Macromolecular transport in synapse to nucleus communication. Trends Neurosci 2015, 38:108-116.