B-type lamins in health and disease

Seminars in Cell and Developmental Biology

Volumn 29, Issue , 2014, Pages 158-163

  Hutchison, C J ^a  

^a DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Autosomal dominant leukodystrophy; Brain development; Cellular senescence; Lamin B1

Indexed keywords

DNA; LAMIN B; LAMIN B1; MESSENGER RNA; MYELIN BASIC PROTEIN; PROTEOLIPID PROTEIN; UNCLASSIFIED DRUG;

CELL AGING; CELL CYCLE ARREST; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CELL STRUCTURE; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DNA END JOINING REPAIR; DNA REPLICATION; DNA TRANSCRIPTION; DOWN REGULATION; GENE ACTIVATION; GENE SILENCING; GENETIC SUSCEPTIBILITY; HUMAN; LEUKODYSTROPHY; MITOSIS SPINDLE; NEURAL TUBE DEFECT; NONHUMAN; NUCLEAR LAMINA; NUCLEAR PORE COMPLEX; OXIDATIVE STRESS; PROTEIN FUNCTION; REVIEW; SPINDLE POLE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL MOTION; CYTOLOGY; GENE DUPLICATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOUSE; NERVE CELL; SPINDLE APPARATUS;

MUS;

ANIMALS; CELL AGING; CELL MOVEMENT; DNA REPLICATION; GENE DUPLICATION; HUMANS; LAMIN TYPE B; MICE; NEURAL TUBE DEFECTS; NEURODEGENERATIVE DISEASES; NEURONS; NUCLEAR LAMINA; SPINDLE APPARATUS; TRANSCRIPTION, GENETIC;

EID: 84901624357     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2013.12.012     Document Type: Review

References (74)

1. Dwyer N., Blobel G. A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei. J Cell Biol 1976, 70(3):581-591.
2. Aebi U., Cohn J., Buhle L., Gerace L. The nuclear lamina is a meshwork of intermediate-type filaments. Nature 1986, 32:560-564.
3. Fisher D.Z., Chaudhary N., Blobel G. cDNA sequencing of nuclear lamins A and C reveals primary and secondary structural homology to intermediate filament proteins. Proc Natl Acad Sci USA 1986, 83(17):6450-6454.
4. McKeon F.D., Kirschner M.W., Caput D. Homologies in both primary and secondary structure between nuclear envelope and intermediate filament proteins. Nature 1986, 319(6053):463-468.
5. Döring V., Stick R. Gene structure of nuclear lamin LIII of Xenopus laevis: a model for the evolution of IF proteins from a lamin-like ancestor. EMBO J 1990, 9(12):4073-4081.
6. Lin F., Worman H.J. Structural organization of the human gene encoding nuclear lamin A and nuclear lamin C. J Biol Chem 1993, 268(22):16321-16326.
7. Röber R.A., 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 1986, 105(2):365-378.
8. Goldberg M.W., Huttenlauch I., Hutchison C.J., Stick R. Filaments made from A- and B-type lamins differ in structure and organization. J Cell Sci 2008, 121(Pt 2):215-225.
9. Gerace L., Blobel G. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell 1980, 19(1):277-287.
10. Lin F., Worman H.J. Structural organization of the human gene (LMNB1) encoding nuclear lamin B1. Genomics 1995, 27(2):230-236.
11. Biamonti G., Giacca M., Perini G., Contreas G., Zentilin L., Weighardt F., et al. The gene for a novel human lamin maps at a highly transcribed locus of chromosome 19 which replicates at the onset of S-phase. Mol Cell Biol 1992, 12(8):3499-3506.
12. Furukawa K., Hotta Y. cDNA cloning of a germ cell specific lamin B3 from mouse spermatocytes and analysis of its function by ectopic expression in somatic cells. EMBO J 1993, 12(1):97-106.
13. Benavente R., Krohne G., Franke W.W. Cell type-specific expression of nuclear lamina proteins during development of Xenopus laevis. Cell 1985, 41(1):177-190.
14. Lehner C.F., Stick R., Eppenberger H.M., Nigg E.A. Differential expression of nuclear lamin proteins during chicken development. J Cell Biol 1987, 105(1):577-587.
15. Stuurman N., Heins S., Aebi U. Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 1998, 122(1-2):42-66.
16. Karabinos A., Schünemann J., Meyer M., Aebi U., Weber K. The single nuclear lamin of Caenorhabditis elegans forms in vitro stable intermediate filaments and paracrystals with a reduced axial periodicity. J Mol Biol 2003, 325(2):241-247.
17. Ben-Harush K., Wiesel N., Frenkiel-Krispin D., Moeller D., Soreq E., Aebi U., et al. The supramolecular organization of the C. elegans nuclear lamin filament. J Mol Biol 2009, 386(5):1392-1402.
18. Broers J.L., Ramaekers F.C., Bonne G., Yaou R.B., Hutchison C.J. Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 2006, 86(3):967-1008.
19. Meier J., Campbell K.H., Ford C.C., Stick R., Hutchison C.J. The role of lamin LIII in nuclear assembly and DNA replication, in cell-free extracts of Xenopus eggs. J Cell Sci 1991, 98(Pt 3):271-279.
20. Newport J.W., Wilson K.L., Dunphy W.G. A lamin-independent pathway for nuclear envelope assembly. J Cell Biol 1990, 111(6 Pt 1):2247-2259.
21. Jenkins H., Hölman T., Lyon C., Lane B., Stick R., Hutchison C. Nuclei that lack a lamina accumulate karyophilic proteins and assemble a nuclear matrix. J Cell Sci 1993, 106(Pt 1):275-285.
22. Spann T.P., Moir R.D., Goldman A.E., Stick R., Goldman R.D. Disruption of nuclear lamin organization alters the distribution of replication factors and inhibits DNA synthesis. J Cell Biol 1997, 136(6):1201-1212.
23. Moir R.D., Yoon M., Khuon S., Goldman R.D. Nuclear lamins A and B1: different pathways of assembly during nuclear envelope formation in living cells. J Cell Biol 2000, 149(6):1179-1192.
24. Ellis D.J., Jenkins H., Whitfield W.G., Hutchison C.J. GST-lamin fusion proteins act as dominant negative mutants in Xenopus egg extract and reveal the function of the lamina in DNA replication. J Cell Sci 1997, 110(Pt 20):2507-2518.
25. Izumi M., Vaughan O.A., Hutchison C.J., Gilbert D.M. Head and/or CaaX domain deletions of lamin proteins disrupt preformed lamin A and C but not lamin B structure in mammalian cells. Mol Biol Cell 2000, 11(12):4323-4337.
26. Spann T.P., Goldman A.E., Wang C., Huang S., Goldman R.D. Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J Cell Biol 2002, 156(4):603-608.
27. Smythe C., Jenkins H.E., Hutchison C.J. Incorporation of the nuclear pore basket protein nup153 into nuclear pore structures is dependent upon lamina assembly: evidence from cell-free extracts of Xenopus eggs. EMBO J 2000, 19(15):3918-3931.
28. Harborth J., Elbashir S.M., Bechert K., Tuschl T., Weber K. Identification of essential genes in cultured mammalian cells using small interfering RNAs. J Cell Sci 2001, 114(Pt 24):4557-4765.
29. Tsai M.Y., Wang S., Heidinger J.M., Shumaker D.K., Adam S.A., Goldman R.D., et al. A mitotic lamin B matrix induced by RanGTP required for spindle assembly. Science 2006, 311(5769):1887-1893.
30. Ma L., Tsai M.Y., Wang S., Lu B., Chen R., Iii J.R., et al. Requirement for Nudel and dynein for assembly of the lamin B spindle matrix. Nat Cell Biol 2009, 11(3):247-256.
31. Civelekoglu-Scholey G., Tao L., Brust-Mascher I., Wollman R., Scholey J.M. Prometaphase spindle maintenance by an antagonistic motor-dependent force balance made robust by a disassembling lamin-B envelope. J Cell Biol 2010, 188(1):49-68.
32. Goodman B., Channels W., Qiu M., Iglesias P., Yang G., Zheng Y. Lamin B counteracts the kinesin Eg5 to restrain spindle pole separation during spindle assembly. J Biol Chem 2010, 285(45):35238-35244.
33. Collado M., Serrano M. The power and the promise of oncogene-induced senescence markers. Nat Rev Cancer 2006, 6(6):472-476.
34. Shimi T., Butin-Israeli V., Adam S.A., Hamanaka R.B., Goldman A.E., Lucas C.A., et al. The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev 2011, 25(24):2579-2593.
35. Freund A., Laberge R.M., Demaria M., Campisi J. Lamin B1 loss is a senescence-associated biomarker. Mol Biol Cell 2012, 23(11):2066-2075.
36. Barascu A., Le Chalony C., Pennarun G., Genet D., Imam N., Lopez B., Bertrand P. Oxidative stress induces an ATM-independent senescence pathway through p38 MAPK-mediated lamin B1 accumulation. EMBO J. 2012, 31(5):1080-1094.
37. Dreesen O., Chojnowski A., Ong P.F., Zhao T.Y., Common J.E., Lunny D., et al. Lamin B1 fluctuations have differential effects on cellular proliferation and senescence. J Cell Biol 2013, 200(5):605-617.
38. Pekovic V., Gibbs-Seymour I., Markiewicz E., Alzoghaibi F., Benham A.M., Edwards R., et al. Conserved cysteine residues in the mammalian lamin A tail are essential for cellular responses to ROS generation. Aging Cell 2011, 10(6):1067-1079.
39. Hutchison C.J. B-type lamins and their elusive roles in metazoan cell proliferation and senescence. EMBO J 2012, 31(5):1058-1059.
40. Pickersgill H., Kalverda B., de Wit E., Talhout W., Fornerod M., van Steensel B. Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat Genet 2006, 38(9):1005-1014.
41. Guelen L., Pagie L., Brasset E., Meuleman W., Faza M.B., Talhout W., et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 2008, 453(7197):948-951.
42. Elcock L.S., Bridger J.M. Exploring the relationship between interphase gene positioning, transcriptional regulation and the nuclear matrix. Biochem Soc Trans 2010, 38(Pt 1):263-267.
43. Reddy K.L., Zullo J.M., Bertolino E., Singh H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature 2008, 452(7184):243-247.
44. Peric-Hupkes D., van Steensel B. Role of the nuclear lamina in genome organization and gene expression. Cold Spring Harb Symp Quant Biol 2010, 75:517-524.
45. Kim Y., Sharov A.A., McDole K., Cheng M., Hao H., Fan C.M., et al. Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 2011, 334(6063):1706-1710.
46. Sadaie M., Salama R., Carroll T., Tomimatsu K., Chandra T., Young A.R., et al. Redistribution of the lamin B1 genomic binding profile affects rearrangement of heterochromatic domains and SAHF formation during senescence. Genes Dev 2013, 27(16):1800-1808.
47. Shah P.P., Donahue G., Otte G.L., Capell B.C., Nelson D.M., Cao K., et al. Lamin B1 depletion in senescent cells triggers large-scale changes in gene expression and the chromatin landscape. Genes Dev 2013, 27(16):1787-1799.
48. Riemer D., Stuurman N., Berrios M., Hunter C., Fisher P.A., Weber K. Expression of Drosophila lamin C is developmentally regulated: analogies with vertebrate A-type lamins. J Cell Sci 1995, 108(Pt 10):3189-3198.
49. Osouda S., Nakamura Y., de Saint Phalle B., McConnell M., Horigome T., Sugiyama S., et al. Null mutants of Drosophila B-type lamin Dm(0) show aberrant tissue differentiation rather than obvious nuclear shape distortion or specific defects during cell proliferation. Dev Biol 2005, 284(1):219-232.
50. Liu J., Rolef Ben-Shahar T., Riemer D., Treinin M., Spann P., Weber K., et al. Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 2000, 11(11):3937-3947.
51. Haithcock E., Dayani Y., Neufeld E., Zahand A.J., Feinstein N., Mattout A., et al. Age-related changes of nuclear architecture in Caenorhabditis elegans. Proc Natl Acad Sci USA 2005, 102(46):16690-16695.
52. Vergnes L., Péterfy M., Bergo M.O., Young S.G., Reue K. Lamin B1 is required for mouse development and nuclear integrity. Proc Natl Acad Sci USA 2004, 101(28):10428-10433.
53. Coffinier C., Chang S.Y., Nobumori C., Tu Y., Farber E.A., Toth J.I., et al. Abnormal development of the cerebral cortex and cerebellum in the setting of lamin B2 deficiency. Proc Natl Acad Sci USA 2010, 107(11):5076-5081.
54. Jung H.J., Nobumori C., Goulbourne C.N., Tu Y., Lee J.M., Tatar A., et al. Farnesylation of lamin B1 is important for retention of nuclear chromatin during neuronal migration. Proc Natl Acad Sci USA 2013, 110(21):E1923-E1932.
55. Yang S.H., Chang S.Y., Yin L., Tu Y., Hu Y., Yoshinaga Y., et al. An absence of both lamin B1 and lamin B2 in keratinocytes has no effect on cell proliferation or the development of skin and hair. Hum Mol Genet 2011, 20(18):3537-3544.
56. Weisend C.M., Kundert J.A., Suvorova E.S., Prigge J.R., Schmidt E.E. Cre activity in fetal albCre mouse hepatocytes: Utility for developmental studies. Genesis 2009, 47(12):789-792. 2009.
57. Hegele R.A., Cao H., Liu D.M., Costain G.A., Charlton-Menys V., Rodger N.W., et al. Sequencing of the reannotated LMNB2 gene reveals novel mutations in patients with acquired partial lipodystrophy. Am J Hum Genet 2006, 79:383-389.
58. Gao J., Li Y., Fu X., Luo X. A Chinese patient with acquired partial lipodystrophy caused by a novel mutation with LMNB2 gene. J Pediatr Endocrinol Metab 2012, 25:375-377.
59. Padiath Q.S., Saigoh K., Schiffmann R., Asahara H., Yamada T., Koeppen A., et al. Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet 2006, 38(10):1114-1123.
60. Lin S.T., Ptácek L.J., Fu Y.H. Adult-onset autosomal dominant leukodystrophy: linking nuclear envelope to myelin. J Neurosci 2011, 31(4):1163-1166.
61. Potic A., Pavlovic A.M., Uziel G., Kozic D., Ostojic J., Rovelli A., et al. Adult-onset autosomal dominant leukodystrophy without early autonomic dysfunctions linked to lamin B1 duplication: a phenotypic variant. J Neurol 2013, 260(8):2124-2129.
62. Guaraldi P., Donadio V., Capellari S., Contin M., Casadio M.C., Montagna P., et al. Isolated noradrenergic failure in adult-onset autosomal dominant leukodystrophy. Auton Neurosci 2011, 159(1-2):123-126.
63. Sundblom J., Melberg A., Kalimo H., Smits A., Raininko R. MR imaging characteristics and neuropathology of the spinal cord in adult-onset autosomal dominant leukodystrophy with autonomic symptoms. AJNR Am J Neuroradiol 2009, 30(2):328-335.
64. Melberg A., Hallberg L., Kalimo H., Raininko R. MR characteristics and neuropathology in adult-onset autosomal dominant leukodystrophy with autonomic symptoms. AJNR Am J Neuroradiol 2006, 27(4):904-911.
65. Giorgio E., Rolyan H., Kropp L., Chakka A.B., Yatsenko S., Gregorio E.D., et al. Analysis of LMNB1 duplications in autosomal dominant leukodystrophy provides insights into duplication mechanisms and allele-specific expression. Hum Mutat 2013, 34(August (8)):1160-1171.
66. Lin S.T., Fu Y.H. miR-23 regulation of lamin B1 is crucial for oligodendrocyte development and myelination. Dis Model Mech 2009, 2(3-4):178-188.
67. De Castro S.C., Malhas A., Leung K.Y., Gustavsson P., Vaux D.J., Copp A.J., et al. Lamin B1 polymorphism influences morphology of the nuclear envelope, cell cycle progression, and risk of neural tube defects in mice. PLoS Genet 2012, 8(11):e1003059.
68. Robinson A., Partridge D., Malhas A., De Castro S.C., Gustavsson P., Thompson D.N., et al. Is LMNB1 a susceptibility gene for neural tube defects in humans?. Birth Defects Res A: Clin Mol Teratol 2013, 97(6):398-402.
69. Sun S., Xu M.Z., Day P.J., Luk J.M. Circulating lamin B1 (LMNB1) biomarker detects early stage liver cancer in patients. J Proteome Res 2010, 9:70-78.
70. Wong K.F., Luk J.M. Discovery of lamin B1 and vimentin as circulating biomarkers of early stage hepatocellular carcinoma. Methods Mol Biol 2012, 909:295-310.
71. Wazir U., Ahmed M.H., Bridger J.M., Harvey A., Jiang W.G., Sharma A.K., et al. The clinicopathological significance of lamin A/C, lamin B1 and lamin B receptor mRNA expression in human breast cancer. Cell Mol Biol Lett 2013, [epub ahead of print].
72. Li L., Kong X., Jia Z., Cui J., Gao J., Wang G., et al. Lamin B1 is a novel therapeutic target of betulinic acid in pancreatic cancer. Clin Cancer Res 2013, 19:4651-4661.
73. Liu L., Wang J., Lei S., Zhang W., Du X., Wang Z., et al. β-Asarone induces senescence in colorectal cancer cells by inducing lamin B1 expression. Phytomedicine 2013, 20:512-520.
74. Liu B., Wang J., Chan K.M., Tjia W.M., Deng W., Guan X., Huang J.D., Li K.M., Chau P.Y., Chen D.J., Pei D., Pendas A.M., Cadiñanos J., López-Otín C., Tse H.F., Hutchison C., Chen J., Cao Y., Cheah K.S., Tryggvason K., Zhou Z. Genomic instability in laminopathy-based premature aging. Nat Med. 2005, 11(7):780-785.