Nucleocytoplasmic shuttling of the Duchenne muscular dystrophy gene product dystrophin Dp71d is dependent on the importin α/β and CRM1 nuclear transporters and microtubule motor dynein

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 5, 2014, Pages 985-1001

  Suarez Sanchez R ^a,b   Aguilar, A ^a   Wagstaff, K M ^c   Velez, G ^a   Azuara Medina, P M ^a   Gomez, P ^a   Vasquez Limeta A ^a   Hernandez Hernandez O ^b   Lieu, K G ^c   Jans, D A ^c   Cisneros, B ^a  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b INSTITUTO NACIONAL DE REHABILITACIÓN   (Mexico)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Dynein; Dystrophin Dp71; Emerin; Exportin Crm1; Importins; ZZ domain

Indexed keywords

DYNEIN; DYSTROPHIN DP71; EMERIN; EXPORTIN CRM1; IMPORTINS; ZZ DOMAIN;

ALPHA KARYOPHERINS; ANIMALS; BASE SEQUENCE; BETA KARYOPHERINS; CELL LINE; CELL NUCLEUS; DNA PRIMERS; DYNEINS; DYSTROPHIN; KARYOPHERINS; MICE; MICROTUBULES; MUSCULAR DYSTROPHY, DUCHENNE; PROTEIN TRANSPORT; RATS; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84894424369     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.01.027     Document Type: Article

References (80)

1. Blake D.J., Weir A., Newey S.E., Davies K.E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 2002, 82:291-329.
2. Koenig M., Hoffman E.P., Bertelson C.J., Monaco A.P., Feener C., Kunkel L.M. Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 1987, 50:509-517.
3. Boyce F.M., Beggs A.H., Feener C., Kunkel L.M. Dystrophin is transcribed in brain from a distant upstream promoter. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:1276-1280.
4. Holder E., Maeda M., Bies R.D. Expression and regulation of the dystrophin Purkinje promoter in human skeletal muscle, heart, and brain. Hum. Genet. 1996, 97:232-239.
5. Klamut H.J., Gangopadhyay S.B., Worton R.G., Ray P.N. Molecular and functional analysis of the muscle-specific promoter region of the Duchenne muscular dystrophy gene. Mol. Cell. Biol. 1990, 10:193-205.
6. Lidov H.G., Selig S., Kunkel L.M. Dp140: a novel 140kDa CNS transcript from the dystrophin locus. Hum. Mol. Genet. 1995, 4:329-335.
7. Hugnot J.P., Gilgenkrantz H., Vincent N., Chafey P., Morris G.E., Monaco A.P., Berwald-Netter Y., Koulakoff A., Kaplan J.C., Kahn A., et al. Distal transcript of the dystrophin gene initiated from an alternative first exon and encoding a 75-kDa protein widely distributed in nonmuscle tissues. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:7506-7510.
8. Byers T.J., Lidov H.G., Kunkel L.M. An alternative dystrophin transcript specific to peripheral nerve. Nat. Genet. 1993, 4:77-81.
9. D'Souza V.N., Nguyen T.M., Morris G.E., Karges W., Pillers D.A., Ray P.N. A novel dystrophin isoform is required for normal retinal electrophysiology. Hum. Mol. Genet. 1995, 4:837-842.
10. Bar S., Barnea E., Levy Z., Neuman S., Yaffe D., Nudel U. A novel product of the Duchenne muscular dystrophy gene which greatly differs from the known isoforms in its structure and tissue distribution. Biochem. J. 1990, 272:557-560.
11. Blake D.J., Love D.R., Tinsley J., Morris G.E., Turley H., Gatter K., Dickson G., Edwards Y.H., Davies K.E. Characterization of a 4.8kb transcript from the Duchenne muscular dystrophy locus expressed in Schwannoma cells. Hum. Mol. Genet. 1992, 1:103-109.
12. Morales-Lazaro S.L., Gonzalez-Ramirez R., Gomez P., Tapia-Ramirez V., de Leon M.B., Cisneros B. Induction of dystrophin Dp71 expression during neuronal differentiation: opposite roles of Sp1 and AP2alpha in Dp71 promoter activity. J. Neurochem. 2010, 112:474-485.
13. de Leon M.B., Montanez C., Gomez P., Morales-Lazaro S.L., Tapia-Ramirez V., Valadez-Graham V., Recillas-Targa F., Yaffe D., Nudel U., Cisneros B. Dystrophin Dp71 expression is down-regulated during myogenesis: role of Sp1 and Sp3 on the Dp71 promoter activity. J. Biol. Chem. 2005, 280:5290-5299.
14. Lederfein D., Levy Z., Augier N., Mornet D., Morris G., Fuchs O., Yaffe D., Nudel U. A 71-kilodalton protein is a major product of the Duchenne muscular dystrophy gene in brain and other nonmuscle tissues. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:5346-5350.
15. Daoud F., Angeard N., Demerre B., Martie I., Benyaou R., Leturcq F., Cossee M., Deburgrave N., Saillour Y., Tuffery S., Urtizberea A., Toutain A., Echenne B., Frischman M., Mayer M., Desguerre I., Estournet B., Reveillere C., Penisson B., Cuisset J.M., Kaplan J.C., Heron D., Rivier F., Chelly J. Analysis of Dp71 contribution in the severity of mental retardation through comparison of Duchenne and Becker patients differing by mutation consequences on Dp71 expression. Hum. Mol. Genet. 2009, 18:3779-3794.
16. Moizard M.P., Toutain A., Fournier D., Berret F., Raynaud M., Billard C., Andres C., Moraine C. Severe cognitive impairment in DMD: obvious clinical indication for Dp71 isoform point mutation screening. Eur. J. Hum. Genet. 2000, 8:552-556.
17. Tadayoni R., Rendon A., Soria-Jasso L.E., Cisneros B. Dystrophin dp71: the smallest but multifunctional product of the Duchenne muscular dystrophy gene. Mol. Neurobiol. 2012, 45:43-60.
18. Dalloz C., Sarig R., Fort P., Yaffe D., Bordais A., Pannicke T., Grosche J., Mornet D., Reichenbach A., Sahel J., Nudel U., Rendon A. Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mouse retina. Hum. Mol. Genet. 2003, 12:1543-1554.
19. Fort P.E., Sene A., Pannicke T., Roux M.J., Forster V., Mornet D., Nudel U., Yaffe D., Reichenbach A., Sahel J.A., Rendon A. Kir4.1 and AQP4 associate with Dp71- and utrophin-DAPs complexes in specific and defined microdomains of Muller retinal glial cell membrane. Glia 2008, 56:597-610.
20. Cerna J., Osuna-Castro J.A., Muniz J., Mornet D., Garcia-Sierra F., Cisneros B. Dystrophin Dp71f associates with components of the beta1-integrin adhesion complex in PC12 cell neurites. Acta Neurol. Belg. 2009, 109:132-135.
21. Enriquez-Aragon J.A., Cerna-Cortes J., Bermudez de Leon M., Garcia-Sierra F., Gonzalez E., Mornet D., Cisneros B. Dystrophin Dp71 in PC12 cell adhesion. Neuroreport 2005, 16:235-238.
22. Cerna J., Cerecedo D., Ortega A., Garcia-Sierra F., Centeno F., Garrido E., Mornet D., Cisneros B. Dystrophin Dp71f associates with the beta1-integrin adhesion complex to modulate PC12 cell adhesion. J. Mol. Biol. 2006, 362:954-965.
23. Villarreal-Silva M., Centeno-Cruz F., Suarez-Sanchez R., Garrido E., Cisneros B. Knockdown of dystrophin Dp71 impairs PC12 cells cycle: localization in the spindle and cytokinesis structures implies a role for Dp71 in cell division. PLoS One 2011, 6:e23504.
24. Fuentes-Mera L., Rodriguez-Munoz R., Gonzalez-Ramirez R., Garcia-Sierra F., Gonzalez E., Mornet D., Cisneros B. Characterization of a novel Dp71 dystrophin-associated protein complex (DAPC) present in the nucleus of HeLa cells: members of the nuclear DAPC associate with the nuclear matrix. Exp. Cell Res. 2006, 312:3023-3035.
25. Gonzalez-Ramirez R., Morales-Lazaro S.L., Tapia-Ramirez V., Mornet D., Cisneros B. Nuclear and nuclear envelope localization of dystrophin Dp71 and dystrophin-associated proteins (DAPs) in the C2C12 muscle cells: DAPs nuclear localization is modulated during myogenesis. J. Cell. Biochem. 2008, 105:735-745.
26. Aleman V., Osorio B., Chavez O., Rendon A., Mornet D., Martinez D. Subcellular localization of Dp71 dystrophin isoforms in cultured hippocampal neurons and forebrain astrocytes. Histochem. Cell Biol. 2001, 115:243-254.
27. Villarreal-Silva M., Suarez-Sanchez R., Rodriguez-Munoz R., Mornet D., Cisneros B. Dystrophin Dp71 is critical for stability of the DAPs in the nucleus of PC12 cells. Neurochem. Res. 2010, 35:366-373.
28. Acosta R., Montanez C., Fuentes-Mera L., Gonzalez E., Gomez P., Quintero-Mora L., Mornet D., Alvarez-Salas L.M., Cisneros B. Dystrophin Dp71 is required for neurite outgrowth in PC12 cells. Exp. Cell Res. 2004, 296:265-275.
29. Gonzalez E., Montanez C., Ray P.N., Howard P.L., Garcia-Sierra F., Mornet D., Cisneros B. Alternative splicing regulates the nuclear or cytoplasmic localization of dystrophin Dp71. FEBS Lett. 2000, 482:209-214.
30. Marquez F.G., Cisneros B., Garcia F., Ceja V., Velazquez F., Depardon F., Cervantes L., Rendon A., Mornet D., Rosas-vargas H., Mustre M., Montanez C. Differential expression and subcellular distribution of dystrophin Dp71 isoforms during differentiation process. Neuroscience 2003, 118:957-966.
31. Jans D.A., Xiao C.Y., Lam M.H. Nuclear targeting signal recognition: a key control point in nuclear transport?. Bioessays 2000, 22:532-544.
32. Pemberton L.F., Paschal B.M. Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 2005, 6:187-198.
33. Austin R.C., Howard P.L., D'Souza V.N., Klamut H.J., Ray P.N. Cloning and characterization of alternatively spliced isoforms of Dp71. Hum. Mol. Genet. 1995, 4:1475-1483.
34. Beetz C., Brodhun M., Moutzouris K., Kiehntopf M., Berndt A., Lehnert D., Deufel T., Bastmeyer M., Schickel J. Identification of nuclear localisation sequences in spastin (SPG4) using a novel Tetra-GFP reporter system. Biochem. Biophys. Res. Commun. 2004, 318:1079-1084.
35. Hubner S., Xiao C.Y., Jans D.A. The protein kinase CK2 site (Ser111/112) enhances recognition of the simian virus 40 large T-antigen nuclear localization sequence by importin. J. Biol. Chem. 1997, 272:17191-17195.
36. Baliga B.C., Colussi P.A., Read S.H., Dias M.M., Jans D.A., Kumar S. Role of prodomain in importin-mediated nuclear localization and activation of caspase-2. J. Biol. Chem. 2003, 278:4899-4905.
37. Heilman D.W., Teodoro J.G., Green M.R. Apoptin nucleocytoplasmic shuttling is required for cell type-specific localization, apoptosis, and recruitment of the anaphase-promoting complex/cyclosome to PML bodies. J. Virol. 2006, 80:7535-7545.
38. Garcia-Tovar C.G., Perez A., Luna J., Mena R., Osorio B., Aleman V., Mondragon R., Mornet D., Rendon A., Hernandez J.M. Biochemical and histochemical analysis of 71kDa dystrophin isoform (Dp71f) in rat brain. Acta Histochem. 2001, 103:209-224.
39. Jans D.A., Moll T., Nasmyth K., Jans P. Cyclin-dependent kinase site-regulated signal-dependent nuclear localization of the SW15 yeast transcription factor in mammalian cells. J. Biol. Chem. 1995, 270:17064-17067.
40. Argentaro A., Sim H., Kelly S., Preiss S., Clayton A., Jans D.A., Harley V.R. A SOX9 defect of calmodulin-dependent nuclear import in campomelic dysplasia/autosomal sex reversal. J. Biol. Chem. 2003, 278:33839-33847.
41. Lara-Chacon B., de Leon M.B., Leocadio D., Gomez P., Fuentes-Mera L., Martinez-Vieyra I., Ortega A., Jans D.A., Cisneros B. Characterization of an Importin alpha/beta-recognized nuclear localization signal in beta-dystroglycan. J. Cell. Biochem. 2010, 110:706-717.
42. Ghildyal R., Ho A., Wagstaff K.M., Dias M.M., Barton C.L., Jans P., Bardin P., Jans D.A. Nuclear import of the respiratory syncytial virus matrix protein is mediated by importin beta1 independent of importin alpha. Biochemistry 2005, 44:12887-12895.
43. Wagstaff K.M., Jans D.A. Intramolecular masking of nuclear localization signals: analysis of importin binding using a novel AlphaScreen-based method. Anal. Biochem. 2006, 348:49-56.
44. Hearps A.C., Jans D.A. HIV-1 integrase is capable of targeting DNA to the nucleus via an importin alpha/beta-dependent mechanism. Biochem. J. 2006, 398:475-484.
45. Efthymiadis A., Briggs L.J., Jans D.A. The HIV-1 Tat nuclear localization sequence confers novel nuclear import properties. J. Biol. Chem. 1998, 273:1623-1628.
46. Forwood J.K., Harley V., Jans D.A. The C-terminal nuclear localization signal of the sex-determining region Y (SRY) high mobility group domain mediates nuclear import through importin beta 1. J. Biol. Chem. 2001, 276:46575-46582.
47. Lixin R., Efthymiadis A., Henderson B., Jans D.A. Novel properties of the nucleolar targeting signal of human angiogenin. Biochem. Biophys. Res. Commun. 2001, 284:185-193.
48. Bruening W., Moffett P., Chia S., Heinrich G., Pelletier J. Identification of nuclear localization signals within the zinc fingers of the WT1 tumor suppressor gene product. FEBS Lett. 1996, 393:41-47.
49. Yamasaki H., Sekimoto T., Ohkubo T., Douchi T., Nagata Y., Ozawa M., Yoneda Y. Zinc finger domain of Snail functions as a nuclear localization signal for importin beta-mediated nuclear import pathway. Genes Cells 2005, 10:455-464.
50. Pandya K., Townes T.M. Basic residues within the Kruppel zinc finger DNA binding domains are the critical nuclear localization determinants of EKLF/KLF-1. J. Biol. Chem. 2002, 277:16304-16312.
51. Saijou E., Itoh T., Kim K.W., Iemura S., Natsume T., Miyajima A. Nucleocytoplasmic shuttling of the zinc finger protein EZI Is mediated by importin-7-dependent nuclear import and CRM1-independent export mechanisms. J. Biol. Chem. 2007, 282:32327-32337.
52. Ito T., Azumano M., Uwatoko C., Itoh K., Kuwahara J. Role of zinc finger structure in nuclear localization of transcription factor Sp1. Biochem. Biophys. Res. Commun. 2009, 380:28-32.
53. Hnia K., Zouiten D., Cantel S., Chazalette D., Hugon G., Fehrentz J.A., Masmoudi A., Diment A., Bramham J., Mornet D., Winder S.J. ZZ domain of dystrophin and utrophin: topology and mapping of a beta-dystroglycan interaction site. Biochem. J. 2007, 401:667-677.
54. Pokorska A., Drevet C., Scazzocchio C. The analysis of the transcriptional activator PrnA reveals a tripartite nuclear localisation sequence. J. Mol. Biol. 2000, 298:585-596.
55. Hatayama M., Tomizawa T., Sakai-Kato K., Bouvagnet P., Kose S., Imamoto N., Yokoyama S., Utsunomiya-Tate N., Mikoshiba K., Kigawa T., Aruga J. Functional and structural basis of the nuclear localization signal in the ZIC3 zinc finger domain. Hum. Mol. Genet. 2008, 17:3459-3473.
56. Yu L.G., Fernig D.G., White M.R., Spiller D.G., Appleton P., Evans R.C., Grierson I., Smith J.A., Davies H., Gerasimenko O.V., Petersen O.H., Milton J.D., Rhodes J.M. Edible mushroom (Agaricus bisporus) lectin, which reversibly inhibits epithelial cell proliferation, blocks nuclear localization sequence-dependent nuclear protein import. J. Biol. Chem. 1999, 274:4890-4899.
57. Sorokin A.V., Kim E.R., Ovchinnikov L.P. Nucleocytoplasmic transport of proteins. Biochemistry (Mosc) 2007, 72:1439-1457.
58. Wente S.R., Rout M.P. The nuclear pore complex and nuclear transport. Cold Spring Harb. Perspect. Biol. 2010, 2:a000562.
59. Efthymiadis A., Shao H., Hubner S., Jans D.A. Kinetic characterization of the human retinoblastoma protein bipartite nuclear localization sequence (NLS) in vivo and in vitro. A comparison with the SV40 large T-antigen NLS. J. Biol. Chem. 1997, 272:22134-22139.
60. Roth D.M., Moseley G.W., Glover D., Pouton C.W., Jans D.A. A microtubule-facilitated nuclear import pathway for cancer regulatory proteins. Traffic 2007, 8:673-686.
61. Roth D.M., Moseley G.W., Pouton C.W., Jans D.A. Mechanism of microtubule-facilitated "fast track" nuclear import. J. Biol. Chem. 2011, 286:14335-14351.
62. Gong X., Ming X., Deng P., Jiang Y. Mechanisms regulating the nuclear translocation of p38 MAP kinase. J. Cell. Biochem. 2010, 110:1420-1429.
63. Mikenberg I., Widera D., Kaus A., Kaltschmidt B., Kaltschmidt C. Transcription factor NF-kappaB is transported to the nucleus via cytoplasmic dynein/dynactin motor complex in hippocampal neurons. PLoS One 2007, 2:e589.
64. Moseley G.W., Roth D.M., DeJesus M.A., Leyton D.L., Filmer R.P., Pouton C.W., Jans D.A. Dynein light chain association sequences can facilitate nuclear protein import. Mol. Biol. Cell 2007, 18:3204-3213.
65. Berk J.M., Tifft K.E., Wilson K.L. The nuclear envelope LEM-domain protein emerin. Nucleus 2013, 4:1-17.
66. Martinez-Vieyra I.A., Vasquez-Limeta A., Gonzalez-Ramirez R., Morales-Lazaro S.L., Mondragon M., Mondragon R., Ortega A., Winder S.J., Cisneros B. A role for beta-dystroglycan in the organization and structure of the nucleus in myoblasts. Biochim. Biophys. Acta 2013, 1833:698-711.
67. Yu Z., Lee C.H., Chinpaisal C., Wei L.N. A constitutive nuclear localization signal from the second zinc-finger of orphan nuclear receptor TR2. J. Endocrinol. 1998, 159:53-60.
68. Yang M., May W.S., Ito T. JAZ requires the double-stranded RNA-binding zinc finger motifs for nuclear localization. J. Biol. Chem. 1999, 274:27399-27406.
69. Matheny C., Day M.L., Milbrandt J. The nuclear localization signal of NGFI-A is located within the zinc finger DNA binding domain. J. Biol. Chem. 1994, 269:8176-8181.
70. Pouton C.W., Wagstaff K.M., Roth D.M., Moseley G.W., Jans D.A. Targeted delivery to the nucleus. Adv. Drug Deliv. Rev. 2007, 59:698-717.
71. Calderilla-Barbosa L., Ortega A., Cisneros B. Phosphorylation of dystrophin Dp71d by Ca2+/calmodulin-dependent protein kinase II modulates the Dp71d nuclear localization in PC12 cells. J. Neurochem. 2006, 98:713-722.
72. Kaffman A., O'Shea E.K. Regulation of nuclear localization: a key to a door. Annu. Rev. Cell Dev. Biol. 1999, 15:291-339.
73. Kau T.R., Way J.C., Silver P.A. Nuclear transport and cancer: from mechanism to intervention. Nat. Rev. Cancer 2004, 4:106-117.
74. Romo-Yanez J., Ceja V., Ilarraza-Lomeli R., Coral-Vazquez R., Velazquez F., Mornet D., Rendon A., Montanez C. Dp71ab/DAPs complex composition changes during the differentiation process in PC12 cells. J. Cell. Biochem. 2007, 102:82-97.
75. Blake D.J., Hawkes R., Benson M.A., Beesley P.W. Different dystrophin-like complexes are expressed in neurons and glia. J. Cell Biol. 1999, 147:645-658.
76. Claudepierre T., Dalloz C., Mornet D., Matsumura K., Sahel J., Rendon A. Characterization of the intermolecular associations of the dystrophin-associated glycoprotein complex in retinal Muller glial cells. J. Cell Sci. 2000, 113(Pt 19):3409-3417.
77. Haenggi T., Soontornmalai A., Schaub M.C., Fritschy J.M. The role of utrophin and Dp71 for assembly of different dystrophin-associated protein complexes (DPCs) in the choroid plexus and microvasculature of the brain. Neuroscience 2004, 129:403-413.
78. Cerecedo D., Cisneros B., Gomez P., Galvan I.J. Distribution of dystrophin- and utrophin-associated protein complexes during activation of human neutrophils. Exp. Hematol. 2010, 38:618-628. (e613).
79. Rodriguez-Munoz R., Villarreal-Silva M., Gonzalez-Ramirez R., Garcia-Sierra F., Mondragon M., Mondragon R., Cerna J., Cisneros B. Neuronal differentiation modulates the dystrophin Dp71d binding to the nuclear matrix. Biochem. Biophys. Res. Commun. 2008, 375:303-307.
80. Rivier F., Robert A., Hugon G., Bonet-Kerrache A., Nigro V., Fehrentz J.A., Martinez J., Mornet D. Dystrophin and utrophin complexed with different associated proteins in cardiac Purkinje fibres. Histochem. J. 1999, 31:425-432.