Developmental regulation of linkers of the nucleoskeleton to the cytoskeleton during mouse postnatal retinogenesis

Nucleus (United States)

Volumn 4, Issue 5, 2013, Pages

  Razafsky, David S ^a   Ward, Candace L ^a   Kolb, Thorsten ^b   Hodzic, Didier ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

KASH domain; Lamins; Nesprins; Nuclear envelope; Retinogenesis; Sun proteins

Indexed keywords

LAMIN A; LAMIN B; NESPRIN1; NESPRIN2; PEPTIDES AND PROTEINS; PROTEIN SUN1; PROTEIN SUN2; UNCLASSIFIED DRUG; LAMIN; MEMBRANE PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; SUN1 PROTEIN, MOUSE; SUN2 PROTEIN, MOUSE; SYNE1 PROTEIN, MOUSE; SYNE2 PROTEIN, MOUSE; TELOMERE BINDING PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; GENE TRANSLOCATION; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MASS SPECTROMETRY; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINA DEVELOPMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; CELL NUCLEUS MATRIX; CELL NUCLEUS MEMBRANE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; KASH DOMAIN; METABOLISM; MOLECULAR GENETICS; NESPRINS; RETINA; RETINOGENESIS; SUN PROTEINS;

KASH DOMAIN; LAMINS; NESPRINS; NUCLEAR ENVELOPE; RETINOGENESIS; SUN PROTEINS;

AMINO ACID SEQUENCE; ANIMALS; CYTOSKELETON; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NUCLEAR MATRIX; NUCLEAR PROTEINS; RETINA; TELOMERE-BINDING PROTEINS;

EID: 84883750041     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.26244     Document Type: Article

References (57)

1. Baye LM, Link BA. Nuclear migration during retinal development. Brain Res 2008; 1192:29-36; PMID:17560964; http://dx.doi.org/10.1016/j. brainres.2007.05.021
2. Swaroop A, Kim D, Forrest D. Transcriptional regulation of photoreceptor development and homeostasis in the mammalian retina. Nat Rev Neurosci 2010; 11:563-76; PMID:20648062; http://dx.doi. org/10.1038/nrn2880
3. Miyata T. Development of three-dimensional architecture of the neuroepithelium: role of pseudostratification and cellular 'community'. Dev Growth Differ 2008; 50(Suppl 1):S105-12; PMID:18070110; http:// dx.doi.org/10.1111/j.1440-169X.2007.00980.x
4. Spear PC, Erickson CA. Interkinetic nuclear migration: a mysterious process in search of a function. Dev Growth Differ 2012; 54:306-16; PMID:22524603; http://dx.doi.org/10.1111/j.1440-169X.2012.01342.x
5. Kosodo Y. Interkinetic nuclear migration: beyond a hallmark of neurogenesis. Cell Mol Life Sci 2012; 69:2727-38; PMID:22415322; http://dx.doi. org/10.1007/s00018-012-0952-2
6. Ghashghaei HT, Lai C, Anton ES. Neuronal migration in the adult brain: are we there yet? Nat Rev Neurosci 2007; 8:141-51; PMID:17237805; http:// dx.doi.org/10.1038/nrn2074
7. Kato M, Dobyns WB. Lissencephaly and the molecular basis of neuronal migration. Hum Mol Genet 2003; 12(Spec No 1):R89-96; PMID:12668601; http:// dx.doi.org/10.1093/hmg/ddg086
8. Nabi NU, Mezer E, Blaser SI, Levin AA, Buncic JR. Ocular findings in lissencephaly. J AAPOS 2003; 7:178-84; PMID:12825057; http://dx.doi. org/10.1016/S1091-8531(02)42005-8
9. Rich KA, Zhan Y, Blanks JC. Migration and synaptogenesis of cone photoreceptors in the developing mouse retina. J Comp Neurol 1997; 388:47-63; PMID:9364238; http://dx.doi.org/10.1002/ (SICI)1096-9861(19971110)388:1<47::AIDCNE4> 3.0.CO;2-O
10. Poché RA, Reese BE. Retinal horizontal cells: challenging paradigms of neural development and cancer biology. Development 2009; 136:2141-51; PMID:19502480; http://dx.doi.org/10.1242/ dev.033175
11. Poché RA, Kwan KM, Raven MA, Furuta Y, Reese BE, Behringer RR. Lim1 is essential for the correct laminar positioning of retinal horizontal cells. J Neurosci 2007; 27:14099-107; PMID:18094249; http://dx.doi. org/10.1523/JNEUROSCI.4046-07.2007
12. Edqvist PH, Hallböök F. Newborn horizontal cells migrate bi-directionally across the neuroepithelium during retinal development. Development 2004; 131:1343-51; PMID:14973293; http://dx.doi. org/10.1242/dev.01018
13. Razafsky D, Blecher N, Markov A, Stewart-Hutchinson PJ, Hodzic D. LINC complexes mediate the positioning of cone photoreceptor nuclei in mouse retina. PLoS One 2012; 7:e47180; PMID:23071752; http://dx.doi. org/10.1371/journal.pone.0047180
14. Yu J, Lei K, Zhou M, Craft CM, Xu G, Xu T, Zhuang Y, Xu R, Han M. KASH protein Syne-2/Nesprin-2 and SUN proteins SUN1/2 mediate nuclear migration during mammalian retinal development. Hum Mol Genet 2011; 20:1061-73; PMID:21177258; http://dx.doi. org/10.1093/hmg/ddq549
15. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, Xu R, Han M. SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 2009; 64:173-87; PMID:19874786; http://dx.doi. org/10.1016/j.neuron.2009.08.018
16. Lei K, Zhang X, Ding X, Guo X, Chen M, Zhu B, Xu T, Zhuang Y, Xu R, Han M. SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc Natl Acad Sci U S A 2009; 106:10207-12; PMID:19509342; http://dx.doi.org/10.1073/pnas.0812037106
17. Stuurman N, Heins S, Aebi U. Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 1998; 122:42-66; PMID:9724605; http://dx.doi. org/10.1006/jsbi.1998.3987
18. Hutchison CJ. Lamins: building blocks or regulators of gene expression? Nat Rev Mol Cell Biol 2002; 3:848-58; PMID:12415302; http://dx.doi.org/10.1038/ nrm950
19. Burke B, Roux KJ. Nuclei take a position: managing nuclear location. Dev Cell 2009; 17:587-97; PMID:19922864; http://dx.doi.org/10.1016/j.devcel. 2009.10.018
20. Starr DA, Fridolfsson HN. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu Rev Cell Dev Biol 2010; 26:421-44; PMID:20507227; http://dx.doi. org/10.1146/annurev-cellbio-100109-104037
21. Razafsky D, Hodzic D. Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J Cell Biol 2009; 186:461-72; PMID:19687252; http://dx.doi.org/10.1083/jcb.200906068
22. Hodzic DM, Yeater DB, Bengtsson L, Otto H, Stahl PD. Sun2 is a novel mammalian inner nuclear membrane protein. J Biol Chem 2004; 279:25805-12; PMID:15082709; http://dx.doi.org/10.1074/jbc. M313157200
23. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, Fry AM, Trembath RC, Shackleton S. SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 2006; 26:3738-51; PMID:16648470; http://dx.doi. org/10.1128/MCB.26.10.3738-3751.2006
24. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, Burke B, Stahl PD, Hodzic D. Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 2006; 172:41-53; PMID:16380439; http://dx.doi. org/10.1083/jcb.200509124
25. Wilhelmsen K, Litjens SH, Kuikman I, Tshimbalanga N, Janssen H, van den Bout I, Raymond K, Sonnenberg A. Nesprin-3, a novel outer nuclear membrane protein, associates with the cytoskeletal linker protein plectin. J Cell Biol 2005; 171:799-810; PMID:16330710; http://dx.doi.org/10.1083/jcb.200506083
26. Roux KJ, Crisp ML, Liu Q, Kim D, Kozlov S, Stewart CL, Burke B. Nesprin 4 is an outer nuclear membrane protein that can induce kinesin-mediated cell polarization. Proc Natl Acad Sci U S A 2009; 106:2194-9; PMID:19164528; http://dx.doi.org/10.1073/ pnas.0808602106
27. Padmakumar VC, Abraham S, Braune S, Noegel AA, Tunggal B, Karakesisoglou I, Korenbaum E. Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp Cell Res 2004; 295:330-9; PMID:15093733; http://dx.doi. org/10.1016/j.yexcr.2004.01.014
28. Meyerzon M, Fridolfsson HN, Ly N, McNally FJ, Starr DA. UNC-83 is a nuclear-specific cargo adaptor for kinesin-1-mediated nuclear migration. Development 2009; 136:2725-33; PMID:19605495; http://dx.doi. org/10.1242/dev.038596
29. Fridolfsson HN, Starr DA. Kinesin-1 and dynein at the nuclear envelope mediate the bidirectional migrations of nuclei. J Cell Biol 2010; 191:115-28; PMID:20921138; http://dx.doi.org/10.1083/ jcb.201004118
30. Patterson K, Molofsky AB, Robinson C, Acosta S, Cater C, Fischer JA. The functions of Klarsicht and nuclear lamin in developmentally regulated nuclear migrations of photoreceptor cells in the Drosophila eye. Mol Biol Cell 2004; 15:600-10; PMID:14617811; http://dx.doi.org/10.1091/mbc.E03-06-0374
31. Mosley-Bishop KL, Li Q, Patterson L, Fischer JA. Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr Biol 1999; 9:1211-20; PMID:10556085; http://dx.doi.org/10.1016/S0960-9822(99)80501-6
32. Kracklauer MP, Banks SM, Xie X, Wu Y, Fischer JA. Drosophila klaroid encodes a SUN domain protein required for Klarsicht localization to the nuclear envelope and nuclear migration in the eye. Fly (Austin) 2007; 1:75-85; PMID:18820457
33. Fan SS, Ready DF. Glued participates in distinct microtubule-based activities in Drosophila eye development. Development 1997; 124:1497-507; PMID:9108366
34. Tsujikawa M, Omori Y, Biyanwila J, Malicki J. Mechanism of positioning the cell nucleus in vertebrate photoreceptors. Proc Natl Acad Sci U S A 2007; 104:14819-24; PMID:17785424; http://dx.doi. org/10.1073/pnas.0700178104
35. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, Stewart CL, Burke B. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 1999; 147:913-20; PMID:10579712; http://dx.doi. org/10.1083/jcb.147.5.913
36. Jahn D, Schramm S, Schnölzer M, Heilmann CJ, de Koster CG, Schütz W, Benavente R, Alsheimer M. A truncated lamin A in the Lmna-/-mouse line: implications for the understanding of laminopathies. Nucleus 2012; 3:463-74; PMID:22895093; http:// dx.doi.org/10.4161/nucl.21676
37. Röber RA, Weber K, Osborn M. Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 1989; 105:365-78; PMID:2680424
38. Young SG, Jung HJ, Coffinier C, Fong LG. Understanding the roles of nuclear A-and B-type lamins in brain development. J Biol Chem 2012; 287:16103-10; PMID:22416132; http://dx.doi. org/10.1074/jbc.R112.354407
39. Göb E, Meyer-Natus E, Benavente R, Alsheimer M. Expression of individual mammalian Sun1 isoforms depends on the cell type. Commun Integr Biol 2011; 4:440-2; PMID:21966565
40. Zhang J, Felder A, Liu Y, Guo LT, Lange S, Dalton ND, Gu Y, Peterson KL, Mizisin AP, Shelton GD, et al. Nesprin 1 is critical for nuclear positioning and anchorage. Hum Mol Genet 2010; 19:329-41; PMID:19864491; http://dx.doi.org/10.1093/hmg/ ddp499
41. Zhang Q, Skepper JN, Yang F, Davies JD, Hegyi L, Roberts RG, Weissberg PL, Ellis JA, Shanahan CM. Nesprins: a novel family of spectrin-repeat-containing proteins that localize to the nuclear membrane in multiple tissues. J Cell Sci 2001; 114:4485-98; PMID:11792814
42. Rajgor D, Mellad JA, Autore F, Zhang Q, Shanahan CM. Multiple novel nesprin-1 and nesprin-2 variants act as versatile tissue-specific intracellular scaffolds. PLoS One 2012; 7:e40098; PMID:22768332; http:// dx.doi.org/10.1371/journal.pone.0040098
43. Young SG, Jung HJ, Coffinier C, Fong LG. Understanding the roles of nuclear A-and B-type lamins in brain development. J Biol Chem 2012; 287:16103-10; PMID:22416132; http://dx.doi. org/10.1074/jbc.R112.354407
44. Broers JL, Ramaekers FC, Bonne G, Yaou RB, Hutchison CJ. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 2006; 86:967-1008; PMID:16816143; http://dx.doi.org/10.1152/ physrev.00047.2005
45. Wakabayashi T, Mori T, Hirahara Y, Koike T, Kubota Y, Takamori Y, Yamada H. Nuclear lamins are differentially expressed in retinal neurons of the adult rat retina. Histochem Cell Biol 2011; 136:427-36; PMID:21842415; http://dx.doi.org/10.1007/s00418-011-0853-8
46. Solovei I, Wang AS, Thanisch K, Schmidt CS, Krebs S, Zwerger M, Cohen TV, Devys D, Foisner R, Peichl L, et al. LBR and lamin A/C sequentially tether peripheral heterochromatin and inversely regulate differentiation. Cell 2013; 152:584-98; PMID:23374351; http:// dx.doi.org/10.1016/j.cell.2013.01.009
47. Yoon BC, Jung H, Dwivedy A, O'Hare CM, Zivraj KH, Holt CE. Local translation of extranuclear lamin B promotes axon maintenance. Cell 2012; 148:752-64; PMID:22341447; http://dx.doi.org/10.1016/j. cell.2011.11.064
48. Göb E, Schmitt J, Benavente R, Alsheimer M. Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One 2010; 5:e12072; PMID:20711465; http://dx.doi. org/10.1371/journal.pone.0012072
49. Randles KN, Lam T, Sewry CA, Puckelwartz M, Furling D, Wehnert M, McNally EM, Morris GE. Nesprins, but not sun proteins, switch isoforms at the nuclear envelope during muscle development. Dev Dyn 2010; 239:998-1009; PMID:20108321; http:// dx.doi.org/10.1002/dvdy.22229
50. Zhang J, Felder A, Liu Y, Guo LT, Lange S, Dalton ND, Gu Y, Peterson KL, Mizisin AP, Shelton GD, et al. Nesprin 1 is critical for nuclear positioning and anchorage. Hum Mol Genet 2010; 19:329-41; PMID:19864491; http://dx.doi.org/10.1093/hmg/ ddp499
51. Guo Y, Jangi S, Welte MA. Organelle-specific control of intracellular transport: distinctly targeted isoforms of the regulator Klar. Mol Biol Cell 2005; 16:1406-16; PMID:15647372; http://dx.doi.org/10.1091/mbc. E04-10-0920
52. Yu YV, Li Z, Rizzo NP, Einstein J, Welte MA. Targeting the motor regulator Klar to lipid droplets. BMC Cell Biol 2011; 12:9; PMID:21349165; http://dx.doi. org/10.1186/1471-2121-12-9
53. Gros-Louis F, Dupré N, Dion P, Fox MA, Laurent S, Verreault S, Sanes JR, Bouchard JP, Rouleau GA. Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat Genet 2007; 39:80-5; PMID:17159980; http://dx.doi. org/10.1038/ng1927
54. Ding X, Xu R, Yu J, Xu T, Zhuang Y, Han M. SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 2007; 12:863-72; PMID:17543860; http://dx.doi.org/10.1016/j. devcel.2007.03.018
55. Kolb T, Maass K, Hergt M, Aebi U, Herrmann H. Lamin A and lamin C form homodimers and coexist in higher complex forms both in the nucleoplasmic fraction and in the lamina of cultured human cells. Nucleus 2011; 2:425-33; PMID:22033280; http:// dx.doi.org/10.4161/nucl.2.5.17765
56. Khatau SB, Bloom RJ, Bajpai S, Razafsky D, Zang S, Giri A, Wu PH, Marchand J, Celedon A, Hale CM, et al. The distinct roles of the nucleus and nucleuscytoskeleton connections in three-dimensional cell migration. Sci Rep 2012; 2:488; PMID:22761994; http://dx.doi.org/10.1038/srep00488
57. Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, Xu T, Zhuang Y, Han M. Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 2007; 134:901-8; PMID:17267447; http://dx.doi.org/10.1242/ dev.02783