Lamins in development, tissue maintenance and stress

EMBO Reports

Volumn 13, Issue 12, 2012, Pages 1070-1078

  Zuela, Noam ^a   Bar, Daniel Z ^a   Gruenbaum, Yosef ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

development; lamin; nuclear envelope; nuclear lamina; stress

Indexed keywords

ACETYLCYSTEINE; ATM PROTEIN; BETA CATENIN; CAVEOLIN 3; EMERIN; HEAT SHOCK PROTEIN; LAMIN A; LAMIN B; LAMIN B1; LAMIN C; MYOGENIN; NOTCH RECEPTOR; REACTIVE OXYGEN METABOLITE; RNA POLYMERASE II; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

AGING; APOPTOSIS; ATAXIA TELANGIECTASIA; BONE DEVELOPMENT; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL FATE; CELL STRESS; CELL SURVIVAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SEGREGATION; CONGESTIVE CARDIOMYOPATHY; DEVELOPMENT; DEVELOPMENTAL DISORDER; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; EMERY DREIFUSS MUSCULAR DYSTROPHY; GENE MUTATION; GENE SILENCING; GENETIC ASSOCIATION; HEAT SHOCK; HOLT ORAM SYNDROME; HOMEOSTASIS; HUMAN; HYPERTHERMIA; LEUKODYSTROPHY; LIMB GIRDLE MUSCULAR DYSTROPHY; LYMPHOCYTE TRANSFORMATION; MECHANICAL STRESS; MESENCHYMAL STEM CELL; MITOSIS; MUSCULAR DYSTROPHY; NONHUMAN; ORGANOGENESIS; OSTEOLYSIS; OXIDATIVE STRESS; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROGERIA; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; TEMPERATURE STRESS; TISSUE DIFFERENTIATION; TRANSCRIPTION REGULATION;

CELL DIFFERENTIATION; CHROMATIN; DNA REPLICATION; HUMANS; LAMIN TYPE A; LAMIN TYPE B; NUCLEAR ENVELOPE; STRESS, PHYSIOLOGICAL; TRANSCRIPTION, GENETIC;

EID: 84870584178     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1038/embor.2012.167     Document Type: Review

References (96)

1. Stuurman N, Heins S, Aebi U (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122: 42-66 (Pubitemid 28411184)
2. Aebi U, Cohn J, Buhle L, Gerace L (1986) The nuclear lamina is a meshwork of intermediate-type filaments. Nature 323: 560-564 (Pubitemid 16025383)
3. Goldberg MW, Huttenlauch I, Hutchison CJ, Stick R (2008) Filaments made from A- and B-type lamins differ in structure and organization. J Cell Sci 121: 215-225 (Pubitemid 351228454)
4. Heitlinger E, Peter M, Haner M, Lustig A, Aebi U, Nigg EA (1991) Expression of chicken lamin B2 in Escherichia coli: characterization of its structure, assembly, and molecular interactions. J Cell Biol 113: 485-495 (Pubitemid 21926006)
5. Ben-Harush K, Wiesel N, Frenkiel-Krispin D, Moeller D, Soreq E, Aebi U, Herrmann H, Gruenbaum Y, Medalia O (2009) The supramolecular organization of the C. elegans nuclear lamin filament. J Mol Biol 386: 1392-1402
6. Broers JL, Machiels BM, Kuijpers HJ, Smedts F, van den Kieboom R, Raymond Y, Ramaekers FC (1997) A- and B-type lamins are differentially expressed in normal human tissues. Histochem Cell Biol 107: 505-517 (Pubitemid 27306980)
7. Rober RA, Gieseler RK, Peters JH, Weber K, Osborn M (1990) Induction of nuclear lamins A/C in macrophages in in vitro cultures of rat bone marrow precursor cells and human blood monocytes, and in macrophages elicited in vivo by thioglycollate stimulation. Exp Cell Res 190: 185-194
8. Stewart C, Burke B (1987) Teratocarcinoma stem cells and early mouse embryos contain only a single major lamin polypeptide closely resembling lamin B. Cell 51: 383-392
9. Weber K, Plessmann U, Traub P (1989) Maturation of nuclear lamin A involves a specific carboxy-terminal trimming, which removes the polyisoprenylation site from the precursor; implications for the structure of the nuclear lamina. FEBS Lett 257: 411-414 (Pubitemid 20032040)
10. Shimi T et al (2008) The A- and B-type nuclear lamin networks: microdomains involved in chromatin organization and transcription. Genes Dev 22: 3409-3421
11. Shimi T et al (2011) The role of nuclear lamin B1 in cell proliferation and senescence. Genes Dev 25: 2579-2593
12. Delbarre E, Tramier M, Coppey-Moisan M, Gaillard C, Courvalin JC, Buendia B (2006) The truncated prelamin A in Hutchinson-Gilford progeria syndrome alters segregation of A-type and B-type lamin homopolymers. Hum Mol Genet 15: 1113-1122
13. Kapinos LE, Schumacher J, Mücke N, Machaidze G, Burkhard P, Aebi U, Strelkov SV, Herrmann H (2010) Characterization of the head-to-tail overlap complexes formed by human lamin A, B1 and B2 'half-minilamin' dimers. J Mol Biol 396: 719-731
14. Schirmer EC, Guan T, Gerace L (2001) Involvement of the lamin rod domain in heterotypic lamin interactions important for nuclear organization. J Cell Biol 153: 479-490
15. Prokocimer M, Davidovich M, Nissim-Rafinia M, Wiesel-Motiuk N, Bar DZ, Barkan R, Meshorer E, Gruenbaum Y (2009) Nuclear lamins: key regulators of nuclear structure and activities. J Cell Mol Med 13: 1059-1085
16. Dittmer TA, Misteli T (2011) The lamin protein family. Genome Biol 12: 222
17. Harborth J, Elbashir SM, Bechert K, Tuschl T, Weber K (2001) Identification of essential genes in cultured mammalian cells using small interfering RNAs. J Cell Sci 114: 4557-4565 (Pubitemid 34086890)
18. Liu J, Rolef-Ben Shahar T, Riemer D, Spann P, Treinin M, Weber K, Fire A, Gruenbaum Y (2000) Essential roles for Caenorhabditis elegans lamin gene in nuclear organization, cell cycle progression, and spatial organization of nuclear pore complexes. Mol Biol Cell 11: 3937-3947
19. Margalit A, Liu J, Fridkin A, Wilson KL, Gruenbaum Y (2005) A lamin-dependent pathway that regulates nuclear organization, cell cycle progression and germ cell development. Novartis Found Symp 264: 231-240
20. Cohen M, Tzur YB, Neufeld E, Feinstein N, Delannoy MR, Wilson KL, Gruenbaum Y (2002) Transmission electron microscope studies of the nuclear envelope in Caenorhabditis elegans embryos. J Struct Biol 140: 232-240 (Pubitemid 36139864)
21. Padiath QS, Saigoh K, Schiffmann R, Asahara H, Yamada T, Koeppen A, Hogan K, Ptacek LJ, Fu YH (2006) Lamin B1 duplications cause autosomal dominant leukodystrophy. Nat Genet 38: 1114-1123 (Pubitemid 44470356)
22. Coffinier C et al (2011) Deficiencies in lamin B1 and lamin B2 cause neurodevelopmental defects and distinct nuclear shape abnormalities in neurons. Mol Biol Cell 22: 4683-4693
23. Kim Y, Sharov AA, McDole K, Cheng M, Hao H, Fan CM, Gaiano N, Ko MS, Zheng Y (2011) Mouse B-type lamins are required for proper organogenesis but not by embryonic stem cells. Science 334: 1706-1710
24. Yang SH, Chang SY, Yin L, Tu Y, Hu Y, Yoshinaga Y, de Jong PJ, Fong LG, Young SG (2011) 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 20: 3537-3544
25. Osouda S, Nakamura Y, de Saint Phalle B, McConnell M, Horigome T, Sugiyama S, Fisher PA, Furukawa K (2005) Null mutants of Drosophila B-type lamin Dm0 show aberrant tissue differentiation rather than obvious nuclear shape distortion or specific defects during cell proliferation. Dev Biol 284: 219-232 (Pubitemid 41096736)
26. Yoon BC, Jung H, Dwivedy A, O'Hare CM, Zivraj KH, Holt CE (2012) Local translation of extranuclear lamin B promotes axon maintenance. Cell 148: 752-764
27. Takamori Y, Tamura Y, Kataoka Y, Cui Y, Seo S, Kanazawa T, Kurokawa K, Yamada H (2007) Differential expression of nuclear lamin, the major component of nuclear lamina, during neurogenesis in two germinal regions of adult rat brain. Eur J Neurosci 25: 1653-1662 (Pubitemid 46550017)
28. Jung HJ et al (2012) Regulation of prelamin A but not lamin C by miR-9, a brain-specific microRNA. Proc Natl Acad Sci USA 109: E423-E431
29. Li W, Yeo LS, Vidal C, McCorquodale T, Herrmann M, Fatkin D, Duque G (2011) Decreased bone formation and osteopenia in lamin A/C-deficient mice. PLoS ONE 25: e19313
30. Akter R, Rivas D, Geneau G, Drissi H, Duque G (2009) Effect of lamin A/C knockdown on osteoblast differentiation and function. J Bone Miner Res 24: 283-293
31. Duque G, Troen BR (2008) Understanding the mechanisms of senile osteoporosis: new facts for a major geriatric syndrome. J Am Geriatr Soc 56: 935-941 (Pubitemid 351652419)
32. Bertrand AT, Chikhaoui K, Yaou RB, Bonne G (2011) Clinical and genetic heterogeneity in laminopathies. Biochem Soc Trans 39: 1687-1692
33. Naetar N et al (2008) Loss of nucleoplasmic LAP2alpha-lamin A complexes causes erythroid and epidermal progenitor hyperproliferation. Nat Cell Biol 10: 1341-1348
34. Morris GE (2001) The role of the nuclear envelope in Emery-Dreifuss muscular dystrophy. Trends Mol Med 7: 572-577 (Pubitemid 33127144)
35. Huber MD, Guan T, Gerace L (2009) Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation. Mol Cell Biol 29: 5718-5728
36. Zwerger M, Ho CY, Lammerding J (2011) Nuclear mechanics in disease. Annu Rev Biomed Eng 13: 397-428
37. Meister P, Towbin BD, Pike BL, Ponti A, Gasser SM (2010) The spatial dynamics of tissue-specific promoters during C. elegans development. Genes Dev 24: 766-782
38. Mattout A, Pike BL, Towbin BD, Bank EM, Gonzalez-Sandoval A, Stadler MB, Meister P, Gruenbaum Y, Gasser S (2011) An EDMD mutation in C. elegans lamin blocks muscle-specific gene relocation and compromises muscle Integrity. Curr Biol 21: 1603-1614
39. Bank EM, Ben-Harush K, Wiesel-Motiuk N, Barkan R, Feinstein N, Lotan O, Medalia O, Gruenbaum Y (2011) A laminopathic mutation disrupting lamin filament assembly causes disease-like phenotypes in Caenorhabditis elegans. Mol Biol Cell 22: 2716-2728
40. Bank EM, Ben-Harush K, Feinstein N, Medalia O, Gruenbaum Y (2011) Structural and physiological phenotypes of disease-linked lamin mutations in C. elegans. J Struct Biol 177: 106-112
41. Gotzmann J, Foisner R (2006) A-type lamin complexes and regenerative potential: a step towards understanding laminopathic diseases? Histochem Cell Biol 125: 33-41
42. Sullivan T, Escalente-Alcalde D, Bhatt H, Anver M, Naryan B, Nagashima K, Stewart CL, Burke B (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147: 913-920
43. Jahn D, Schramm S, Schnölzer M, Heilmann CJ, de Koster CG, Schütz W, Benavente R, Alsheimer M (2012) A truncated lamin A in the Lmna-/- mouse line: implications for the understanding of laminopathies. Nucleus 3: 463-474
44. Dorner D, Vlcek S, Foeger N, Gajewski A, Makolm C, Gotzmann J, Hutchison CJ, Foisner R (2006) Lamina-associated polypeptide 2alpha regulates cell cycle progression and differentiation via the retinoblastoma-E2F pathway. J Cell Biol 173: 83-93
45. Boban M, Braun J, Foisner R (2010) Lamins: 'structure goes cycling'. Biochem Soc Trans 38: 301-306
46. Gnocchi VF, Ellis JA, Zammit PS (2008) Does satellite cell dysfunction contribute to disease progression in Emery-Dreifuss muscular dystrophy? Biochem Soc Trans 36: 1344-1349
47. Capanni C et al (2008) Prelamin A is involved in early steps of muscle differentiation. Exp Cell Res 314: 3628-3637
48. Kandert S, Wehnert M, Müller CR, Buendia B, Dabauvalle MC (2009) Impaired nuclear functions lead to increased senescence and inefficient differentiation in human myoblasts with a dominant p.R545C mutation in the LMNA gene. Eur J Cell Biol 88: 593-608
49. Favreau C, Higuet D, Courvalin JC, Buendia B (2004) Expression of a mutant lamin A that causes Emery-Dreifuss muscular dystrophy inhibits in vitro differentiation of C2C12 myoblasts. Mol Biol Cell 24: 1481-1492 (Pubitemid 38167072)
50. Melcon G et al (2006) Loss of emerin at the nuclear envelope disrupts the Rb1/E2F and MyoD pathways during muscle regeneration. Hum Mol Genet 15: 637-651 (Pubitemid 43205427)
51. Tilgner K, Wojciechowicz K, Jahoda C, Hutchison C, Markiewicz E (2009) Dynamic complexes of A-type lamins and emerin influence adipogenic capacity of the cell via nucleocytoplasmic distribution of beta-catenin. J Cell Sci 122: 401-413
52. Goldman RD et al (2004) Accumulation of mutant lamin A causes progressive changes in nuclear architecture in Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci USA 101: 8963-8968 (Pubitemid 38781594)
53. Scaffidi P, Misteli T (2005) Reversal of the cellular phenotype in the premature aging disease Hutchinson-Gilford progeria syndrome. Nat Med 11: 440-445 (Pubitemid 40562336)
54. Cao K, Blair CD, Faddah DA, Kieckhaefer JE, Olive M, Erdos MR, Nabel EG, Collins FS (2011) Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest 121: 2833-2844
55. McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, Collins FS, Djabali K (2007) The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS ONE 2: e1269
56. Taimen P et al (2009) A progeria mutation reveals functions for lamin A in nuclear assembly, architecture, and chromosome organization. Proc Natl Acad Sci USA 106: 20788-20793
57. Bökenkamp R, Raz V, Venema A, DeRuiter MC, van Munsteren C, Olive M, Nabel EG, Gittenberger-de Groot AC (2011) Differential temporal and spatial progerin expression during closure of the ductus arteriosus in neonates. PLoS ONE 6: e23975
58. Broers JL, Ramaekers FC, Bonne G, Yaou RB, Hutchison CJ (2006) Nuclear lamins: laminopathies and their role in premature ageing. Physiol Rev 86: 967-1008 (Pubitemid 44042881)
59. Meshorer E, Gruenbaum Y (2009) NURD keeps chromatin young. Nat Cell Biol 11: 1176-1177
60. Moiseeva O, Bourdeau V, Vernier M, Dabauvalle MC, Ferbeyre G (2011) Retinoblastoma-independent regulation of cell proliferation and senescence by the p53-p21 axis in lamin A/C-depleted cells. Aging Cell 10: 789-797
61. Pegoraro G, Kubben N, Wickert U, Göhler H, Hoffmann K, TM (2009) Ageing-related chromatin defects through loss of the NURD complex. Nat Cell Biol 11: 1261-1267
62. Liu B et al (2005) Genomic instability in laminopathy-based premature aging. Nat Med 11: 780-785 (Pubitemid 41021211)
63. Osorio FG, Ugalde AP, Mariño G, Puente XS, Freije JM, López-Otín C (2011) Cell autonomous and systemic factors in progeria development. Biochem Soc Trans 39: 1710-1714
64. Musich PR, Zou Y (2009) Genomic instability and DNA damage responses in progeria arising from defective maturation of prelamin A. Aging (Albany NY) 1: 28-37
65. Gotzmann J, Foisner R (2005) A-type lamin complexes and regenerative potential: a step towards understanding laminopathic diseases? Histochem Cell Biol 125: 33-41 (Pubitemid 43049970)
66. Rosengardten Y, McKenna T, Grochová D, Eriksson M (2011) Stem cell depletion in Hutchinson-Gilford progeria syndrome. Aging Cell 10: 1011-1020
67. Espada J et al (2008) Nuclear envelope defects cause stem cell dysfunction in premature-aging mice. J Cell Biol 181: 27-35 (Pubitemid 351519761)
68. Hernandez L et al (2010) Functional coupling between the extracellular matrix and nuclear lamina by Wnt signaling in progeria. Dev Cell 19: 413-425
69. Hennekam RC (2006) Hutchinson-Gilford progeria syndrome: review of the phenotype. Am J Med Genet A 140: 2603-2624 (Pubitemid 44865091)
70. Liu GH et al (2011) Recapitulation of premature ageing with iPSCs from Hutchinson-Gilford progeria syndrome. Nature 472: 221-225
71. Zhang J et al (2011) A human iPSC model of Hutchinson-Gilford progeria reveals vascular smooth muscle and mesenchymal stem cell defects. Cell Stem Cell 8: 31-35
72. Boguslavsky RL, Stewart CL, Worman HJ (2006) Nuclear lamin A inhibits adipocyte differentiation: implications for Dunnigan-type familial partial lipodystrophy. Hum Mol Genet 15: 653-663 (Pubitemid 43205428)
73. Wu W, Muchir A, Shan J, Bonne G, HJW (2011) Mitogen-activated protein kinase inhibitors improve heart function and prevent fibrosis in cardiomyopathy caused by mutation in lamin A/C gene. Circulation 123: 53-61
74. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RS (2004) Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113: 370-378 (Pubitemid 38544181)
75. Cupesi M, Yoshioka J, Gannon J, Kudinova A, Stewart CL, Lammerding J (2010) Attenuated hypertrophic response to pressure overload in a lamin A/C haploinsufficiency mouse. J Mol Cell Cardiol 48: 1290-1297
76. Verstraeten VL, Ji JY, Cummings KS, Lee RT, Lammerding J (2008) Increased mechanosensitivity and nuclear stiffness in Hutchinson-Gilford progeria cells: effects of farnesyltransferase inhibitors. Aging Cell 7: 383-393 (Pubitemid 351663907)
77. Schlesinger MJ (1994) How the cell copes with stress and the function of heat shock proteins. Pediatr Res 36: 1-6 (Pubitemid 24185180)
78. Tonkiss J, Calderwood SK (2005) Regulation of heat shock gene transcription in neuronal cells. Int J Hyperthermia 21: 433-444 (Pubitemid 41102942)
79. Dynlacht JR, Story MD, Zhu WG, Danner J (1999) Lamin B is a prompt heat shock protein. J Cell Physiol 178: 28-34 (Pubitemid 28554919)
80. Haddad N, Paulin-Levasseur M (2008) Effects of heat shock on the distribution and expression levels of nuclear proteins in HeLa S3 cells. J Cell Biochem 105: 1485-1500
81. Malhas AN, Vaux DJ (2011) The nuclear envelope and its involvement in cellular stress responses. Biochem Soc Trans 39: 1795-1798
82. Adhikari AS, Sridhar Rao K, Rangaraj N, Parnaik VK, Mohan Rao C (2004) Heat stress-induced localization of small heat shock proteins in mouse myoblasts: intranuclear lamin A/C speckles as target for alphaB-crystallin and Hsp25. Exp Cell Res 299: 393-403 (Pubitemid 39179806)
83. Houck SA, Landsbury A, Clark JI, Quinlan RA (2011) Multiple sites in αB-crystallin modulate its interactions with desmin filaments assembled in vitro. PLoS ONE 6: e25859
84. Vicart P et al (1998) A missense mutation in the alphaB-crystallin chaperone gene causes a desmin-related myopathy. Nat Genet 20: 92-95 (Pubitemid 28410353)
85. Gonzalez-Suarez I et al (2009) Novel roles for A-type lamins in telomere biology and the DNA damage response pathway. EMBO J 28: 2414-2427
86. Lees-Miller SP (2006) Dysfunction of lamin A triggers a DNA damage response and cellular senescence. DNA Repair (Amst) 5: 286-289 (Pubitemid 43069529)
87. Liu B et al (2005) Genomic instability in laminopathy-based premature aging. Nat Med 11: 780-785 (Pubitemid 41021211)
88. Prokocimer M, Margalit A, Gruenbaum Y (2006) The nuclear lamina and its proposed roles in tumorigenesis: projection on the hematologic malignancies and future targeted therapy. J Struct Biol 155: 351-360 (Pubitemid 44376369)
89. Hutchison CJ (2011) The role of DNA damage in laminopathy progeroid syndromes. Biochem Soc Trans 39: 1715-1718
90. Liu B, Zhou Z (2008) Lamin A/C, laminopathies and premature ageing. Histol Histopathol 23: 747-763 (Pubitemid 351552360)
91. Benson EK, Lee SW, Aaronson SA (2010) Role of progerin-induced telomere dysfunction in HGPS premature cellular senescence. J Cell Sci 123: 2605-2612
92. Fabrini R et al (2010) Nuclear shield: a multi-enzyme task-force for nucleus protection. PLoS ONE 5: e14125
93. Malhas AN, Lee CF, Vaux DJ (2009) Lamin B1 controls oxidative stress responses via Oct-1. J Cell Biol 184: 45-55
94. Hutchison CJ (2012) B-type lamins and their elusive roles in metazoan cell proliferation and senescence. EMBO J 31: 1058-1059
95. Barascu A, Le Chalony C, Pennarun G, Genet D, Imam N, Lopez B, Bertrand P (2012) Oxidative stress induces an ATM-independent senescence pathway through p38 MAPK-mediated lamin B1 accumulation. EMBO J 31: 1080-1094
96. Pekovic V, Gibbs-Seymour I, Markiewicz E, Alzoghaibi F, Benham AM, Edwards R, Wenhert M, von Zglinicki T, Hutchison CJ (2011) Conserved cysteine residues in the mammalian lamin A tail are essential for cellular responses to ROS generation. Aging Cell 10: 1067-1079