LINCing lamin B2 to neuronal migration, growing evidence for cell-specific roles of B-types lamins

Nucleus

Volumn 1, Issue 5, 2010, Pages

  Coffinier, Catherine ^a   Fong, Loren G ^a   Young, Stephen G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cortical neurons; Lamin B2; LINC complex; Lissencephaly; Nesprin; Neuronal migration; Nuclear envelope; Nuclear lamina; Nuclear translocation; SUN

Indexed keywords

LAMIN B; LAMIN B1; LAMIN B2; UNCLASSIFIED DRUG;

AGYRIA; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CARDIOMYOPATHY; CELL MIGRATION; CELL NUCLEUS; CELL STRUCTURE; CEREBELLUM; FAMILIAL PARTIAL LIPODYSTROPHY; FLY; FOREBRAIN; GENE MAPPING; GENE MUTATION; GENETIC ASSOCIATION; HIPPOCAMPUS; HUMAN; MORPHOGENESIS; MUSCULAR DYSTROPHY; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEAR LAMINA; PERIPHERAL NEUROPATHY; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ANIMAL; CELL MOTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE; MOUSE MUTANT; MUTATION; NERVOUS SYSTEM DEVELOPMENT; NUCLEAR PORE; PHYSIOLOGY;

MUS;

ANIMALS; CELL MOVEMENT; CEREBELLUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIPPOCAMPUS; LAMIN TYPE B; MICE; MICE, KNOCKOUT; MUTATION; NEUROGENESIS; NEURONS; NUCLEAR LAMINA; NUCLEAR PORE;

EID: 77957670627     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Stewart CL, Roux KJ, Burke B. Blurring the boundary: The nuclear envelope extends its reach. Science 2007; 318:1408-12.
2. Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar D, Barkan R, et al. Nuclear lamins: Key regulators of nuclear structure and activities. J Cell Mol Med 2009; 13:1059-85.
3. Gerace L, Blum A, Blobel G. Immunocytochemical localization of the major polypeptides of the nuclear pore complex-lamina fraction. Interphase and mitotic distribution. J Cell Biol 1978; 79:546-66.
4. Aebi U, Cohn J, Buhle L, Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 1986; 323:560-4.
5. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, et al. Nuclear lamins: Major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008; 22:832-53.
6. Hutchison CJ. Lamins: Building blocks or regulators of gene expression? Nat Rev Mol Cell Biol 2002; 3:848-58.
7. Worman HJ, Fong LG, Muchir A, Young SG. Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest 2009; 119:1825-36.
8. Dauer WT, Worman HJ. The nuclear envelope as a signaling node in development and disease. Dev Cell 2009; 17:626-38.
9. Burke B, Stewart CL. Life at the edge: The nuclear envelope and human disease. Nat Rev Mol Cell Biol 2002; 3:575-85.
10. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, et al. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 2003; 423:293-8.
11. de Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, Boccaccio I, et al. Lamin A truncation in Hutchinson-Gilford progeria. Science 2003; 300:2055.
12. Wilson KL, Zastrow MS, Lee KK. Lamins and disease: Insights into nuclear infrastructure. Cell 2001; 104:647-50.
13. Hutchison CJ, Alvarez-Reyes M, Vaughan OA. Lamins in disease: Why do ubiquitously expressed nuclear envelope proteins give rise to tissue-specific disease phenotypes? J Cell Sci 2001; 114:9-19.
14. Misteli T, Scaffidi P. Genome instability in progeria: When repair gets old. Nat Med 2005; 11:718-9.
15. Bonne G, Di Barletta MR, Varnous S, Bécane HM, Hammouda EH, Merlini L, et al. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 1999; 21:285-8.
16. Muchir A, Medioni J, Laluc M, Massart C, Arimura T, van der Kooi AJ, et al. Nuclear envelope alterations in fibroblasts from patients with muscular dystrophy, cardiomyopathy and partial lipodystrophy carrying lamin A/C gene mutations. Muscle Nerve 2004; 30:444-50.
17. Dahl KN, Scaffidi P, Islam MF, Yodh AG, Wilson KL, Misteli T. Distinct structural and mechanical properties of the nuclear lamina in Hutchinson- Gilford progeria syndrome. Proc Natl Acad Sci USA 2006; 103:10271-6.
18. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, et al. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 2004; 113:370-8.
19. Broers JL, Peeters EA, Kuijpers HJ, Endert J, Bouten CV, Oomens CW, et al. Decreased mechanical stiffness in LMNA-/- cells is caused by defective nucleo-cytoskeletal integrity: Implications for the development of laminopathies. Hum Mol Genet 2004; 13:2567-80.
20. Padiath QS, Saigoh K, Schiffmann R, Asahara H, Yamada T, Koeppen A, et al. Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet 2006; 38:1114-23.
21. Meijer I, Simoes-Lopes A, Laurent S, Katz T, St-Onge J, Verlaan D, et al. A novel duplication confirms the involvement of 5q23.2 in autosomal dominant leukodystrophy. Arch Neurol 2008; 65:1496-501.
22. Brussino A, Vaula G, Cagnoli C, Mauro A, Pradotto L, Daniele D, et al. A novel family with Lamin B1 duplication associated with adult-onset leucoencephalopathy. J Neurol Neurosurg Psychiatry 2009; 80:237-40.
23. Hegele RA, Cao H, Liu DM, Costain GA, Charlton-Menys V, Rodger NW, et al. Sequencing of the reannotated LMNB2 gene reveals novel mutations in patients with acquired partial lipodystrophy. Am J Hum Genet 2006; 79:383-9.
24. Vergnes L, Peterfy M, Bergo MO, Young SG, Reue K. Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci USA 2004; 101:10428-33.
25. Coffinier C, Chang SY, Nobumori C, Tu Y, Farber EA, Toth JI, et al. Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA 2010; 107:5076-81.
26. Gupta A, Tsai LH, Wynshaw-Boris A. Life is a journey: A genetic look at neocortical development. Nat Rev Genet 2002; 3:342-55.
27. Wynshaw-Boris A. Lissencephaly and LIS1: Insights into the molecular mechanisms of neuronal migration and development. Clin Genet 2007; 72:296-304.
28. Bielas S, Higginbotham H, Koizumi H, Tanaka T, Gleeson JG. Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu Rev Cell Dev Biol 2004; 20:593-618.
29. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, Nagashima K, et al. Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 1999; 147:913-9.
30. Wolf CM, Wang L, Alcalai R, Pizard A, Burgon PG, Ahmad F, et al. Lamin A/C haploinsufficiency causes dilated cardiomyopathy and apoptosis-triggered cardiac conduction system disease. J Mol Cell Cardiol 2008; 44:293-303.
31. 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.
32. Broers JL, Machiels BM, Kuijpers HJ, Smedts F, van den Kieboom R, Raymond Y, et al. A- and B-type lamins are differentially expressed in normal human tissues. Histochem Cell Biol 1997; 107:505-17.
33. Takamori Y, Tamura Y, Kataoka Y, Cui Y, Seo S, Kanazawa T, et al. Differential expression of nuclear lamin, the major component of nuclear lamina, during neurogenesis in two germinal regions of adult rat brain. Eur J Neurosci 2007; 25:1653-62.
34. Solecki DJ, Govek EE, Tomoda T, Hatten ME. Neuronal polarity in CNS development. Genes Dev 2006; 20:2639-47.
35. Wynshaw-Boris A, Gambello MJ. LIS1 and dynein motor function in neuronal migration and development. Genes Dev 2001; 15:639-51.
36. Vallee RB, Tsai JW. The cellular roles of the lissencephaly gene LIS1 and what they tell us about brain development. Genes Dev 2006; 20:1384-93.
37. Méjat A, Misteli T. LINC complexes in health and disease. Nucleus 2010; 1:40-52.
38. Fridkin A, Penkner A, Jantsch V, Gruenbaum Y. SUN-domain and KASH-domain proteins during development, meiosis and disease. Cell Mol Life Sci 2009; 66:1518-33.
39. Burke B, Roux KJ. Nuclei take a position: Managing nuclear location. Dev Cell 2009; 17:587-97.
40. Zhang Q, Bethmann C, Worth NF, Davies JD, Wasner C, Feuer A, et al. Nesprin-1 and -2 are involved in the pathogenesis of Emery Dreifuss muscular dystrophy and are critical for nuclear envelope integrity. Hum Mol Genet 2007; 16:2816-33.
41. Zhang X, Xu R, Zhu B, Yang X, Ding X, Duan S, et al. Syne-1 and Syne-2 play crucial roles in myonuclear anchorage and motor neuron innervation. Development 2007; 134:901-8.
42. Lei K, Zhang X, Ding X, Guo X, Chen M, Zhu B, et al. SUN1 and SUN2 play critical but partially redundant roles in anchoring nuclei in skeletal muscle cells in mice. Proc Natl Acad Sci USA 2009; 106:10207-12.
43. Gros-Louis F, Dupre N, Dion P, Fox MA, Laurent S, Verreault S, et al. Mutations in SYNE1 lead to a newly discovered form of autosomal recessive cerebellar ataxia. Nat Genet 2007; 39:80-5.
44. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, Xu T, et al. 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.
45. 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.
46. 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.
47. Ji JY, Lee RT, Vergnes L, Fong LG, Stewart CL, Reue K, et al. Cell nuclei spin in the absence of lamin B1. J Biol Chem 2007; 282:20015-26.
48. Tsai JW, Bremner KH, Vallee RB. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 2007; 10:970-9.
49. Goodchild RE, Kim CE, Dauer WT. Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 2005; 48:923-32.
50. Tsai MY, Wang S, Heidinger JM, Shumaker DK, Adam SA, Goldman RD, et al. A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 2006; 311:1887-93.