Embryonic senescence and laminopathies in a progeroid zebrafish model

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Koshimizu, Eriko ^a,b   Imamura, Shintaro ^a,e   Qi, Jie ^a,d,f   Toure, Jamal ^a   Valdez Jr , Delgado M ^d   Carr, Christopher E ^c   Hanai, Jun ichi ^a   Kishi, Shuji ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e FISHERIES RESEARCH AGENCY   (Japan)

^f OCEAN UNIVERSITY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; LAMIN A; LAMIN C; PROGERIN; UNCLASSIFIED DRUG; ZEBRAFISH PROTEIN; ANTISENSE OLIGONUCLEOTIDE; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; MUTANT PROTEIN; NUCLEAR PROTEIN; PRELAMIN A; PROTEIN PRECURSOR;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY BUILD; CELL CYCLE ARREST; CELL CYCLE S PHASE; CELL LINEAGE; CELL NUCLEUS MEMBRANE; CHONDROPATHY; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; EMBRYO; GENE; GENE DELETION; GENE EXPRESSION; GENETIC DISORDER; LAMIN A GENE; LAMINOPATHY; LIFESPAN; LIPODYSTROPHY; MESENCHYME CELL; MUSCLE CELL; MUSCLE DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PREMATURE AGING; PROGERIA; PROTEIN DEFECT; PROTEIN FUNCTION; RNA SPLICING; SKIN DISEASE; ZEBRA FISH; AGING; AMINO ACID SEQUENCE; ANIMAL; ANIMAL EMBRYO; CARTILAGE; CHEMISTRY; CONGENITAL MALFORMATION; DISEASE MODEL; DRUG EFFECT; GENE SILENCING; GENETICS; HUMAN; LONGEVITY; METABOLISM; MOLECULAR GENETICS; MUSCLE; PATHOLOGY; TRANSGENE; TRANSGENIC ANIMAL;

DANIO RERIO; VERTEBRATA;

AGING; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CARTILAGE; DISEASE MODELS, ANIMAL; EMBRYO, NONMAMMALIAN; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HUMANS; LAMIN TYPE A; LIPODYSTROPHY; LONGEVITY; MOLECULAR SEQUENCE DATA; MUSCLES; MUTANT PROTEINS; NUCLEAR PROTEINS; OLIGONUCLEOTIDES, ANTISENSE; PROGERIA; PROTEIN PRECURSORS; TRANSGENES; ZEBRAFISH;

EID: 79953303050     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017688     Document Type: Article

References (90)

1. Raharjo WH, Enarson P, Sullivan T, Stewart CL, Burke B, (2001) Nuclear envelope defects associated with LMNA mutations cause dilated cardiomyopathy and Emery-Dreifuss muscular dystrophy. J Cell Sci 114: 4447-4457.
2. Gerace L, Burke B, (1988) Functional organization of the nuclear envelope. Annu Rev Cell Biol 4: 335-374.
3. Stuurman N, Heins S, Aebi U, (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122: 42-66.
4. Fawcett DW, (1966) On the occurrence of a fibrous lamina on the inner aspect of the nuclear envelope in certain cells of vertebrates. Am J Anat 119: 129-145.
5. Worman HJ, Ostlund C, Wang Y, (2010) Diseases of the nuclear envelope. Cold Spring Harb Perspect Biol 2: a000760.
6. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, et al. (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423: 293-298.
7. De Sandre-Giovannoli A, Bernard R, Cau P, Navarro C, Amiel J, et al. (2003) Lamin a truncation in Hutchinson-Gilford progeria. Science 300: 2055.
8. Capell BC, Erdos MR, Madigan JP, Fiordalisi JJ, Varga R, et al. (2005) Inhibiting farnesylation of progerin prevents the characteristic nuclear blebbing of Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 102: 12879-12884.
9. Glynn MW, Glover TW, (2005) Incomplete processing of mutant lamin A in Hutchinson-Gilford progeria leads to nuclear abnormalities, which are reversed by farnesyltransferase inhibition. Hum Mol Genet 14: 2959-2969.
10. Yang SH, Bergo MO, Toth JI, Qiao X, Hu Y, et al. (2005) Blocking protein farnesyltransferase improves nuclear blebbing in mouse fibroblasts with a targeted Hutchinson-Gilford progeria syndrome mutation. Proc Natl Acad Sci U S A 102: 10291-10296.
11. 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.
12. Sinensky M, Fantle K, Trujillo M, McLain T, Kupfer A, et al. (1994) The processing pathway of prelamin A. J Cell Sci 107 (Pt 1): 61-67.
13. Yang SH, Meta M, Qiao X, Frost D, Bauch J, et al. (2006) A farnesyltransferase inhibitor improves disease phenotypes in mice with a Hutchinson-Gilford progeria syndrome mutation. J Clin Invest 116: 2115-2121.
14. Scaffidi P, Misteli T, (2006) Lamin A-dependent nuclear defects in human aging. Science 312: 1059-1063.
15. van Engelen BG, Muchir A, Hutchison CJ, van der Kooi AJ, Bonne G, et al. (2005) The lethal phenotype of a homozygous nonsense mutation in the lamin A/C gene. Neurology 64: 374-376.
16. Navarro CL, De Sandre-Giovannoli A, Bernard R, Boccaccio I, Boyer A, et al. (2004) Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum Mol Genet 13: 2493-2503.
17. Moulson CL, Go G, Gardner JM, van der Wal AC, Smitt JH, et al. (2005) Homozygous and compound heterozygous mutations in ZMPSTE24 cause the laminopathy restrictive dermopathy. J Invest Dermatol 125: 913-919.
18. Scaffidi P, Misteli T, (2008) Lamin A-dependent misregulation of adult stem cells associated with accelerated ageing. Nat Cell Biol 10: 452-459.
19. Meshorer E, Gruenbaum Y, (2008) Gone with the Wnt/Notch: stem cells in laminopathies, progeria, and aging. J Cell Biol 181: 9-13.
20. Constantinescu D, Gray HL, Sammak PJ, Schatten GP, Csoka AB, (2006) Lamin A/C expression is a marker of mouse and human embryonic stem cell differentiation. Stem Cells 24: 177-185.
21. Halaschek-Wiener J, Brooks-Wilson A, (2007) Progeria of stem cells: stem cell exhaustion in Hutchinson-Gilford progeria syndrome. J Gerontol A Biol Sci Med Sci 62: 3-8.
22. Gotic I, Schmidt WM, Biadasiewicz K, Leschnik M, Spilka R, et al. (2010) Loss of LAP2 alpha delays satellite cell differentiation and affects postnatal fiber-type determination. Stem Cells 28: 480-488.
23. Espada J, Varela I, Flores I, Ugalde AP, Cadinanos J, et al. (2008) Nuclear envelope defects cause stem cell dysfunction in premature-aging mice. J Cell Biol 181: 27-35.
24. Naetar N, Korbei B, Kozlov S, Kerenyi MA, Dorner D, et al. (2008) Loss of nucleoplasmic LAP2alpha-lamin A complexes causes erythroid and epidermal progenitor hyperproliferation. Nat Cell Biol 10: 1341-1348.
25. Schulze SR, Curio-Penny B, Speese S, Dialynas G, Cryderman DE, et al. (2009) A comparative study of Drosophila and human A-type lamins. PLoS One 4: e7564.
26. Peter A, Stick R, (2008) Ectopic expression of prelamin A in early Xenopus embryos induces apoptosis. Eur J Cell Biol 87: 879-891.
27. Foster HA, Stokes P, Forsey K, Leese HJ, Bridger JM, (2007) Lamins A and C are present in the nuclei of early porcine embryos, with lamin A being distributed in large intranuclear foci. Chromosome Res 15: 163-174.
28. Rober RA, Weber K, Osborn M, (1989) Differential timing of nuclear lamin A/C expression in the various organs of the mouse embryo and the young animal: a developmental study. Development 105: 365-378.
29. Prather RS, Sims MM, Maul GG, First NL, Schatten G, (1989) Nuclear lamin antigens are developmentally regulated during porcine and bovine embryogenesis. Biol Reprod 41: 123-132.
30. Lehner CF, Stick R, Eppenberger HM, Nigg EA, (1987) Differential expression of nuclear lamin proteins during chicken development. J Cell Biol 105: 577-587.
31. Amati F, Biancolella M, D'Apice MR, Gambardella S, Mango R, et al. (2004) Gene expression profiling of fibroblasts from a human progeroid disease (mandibuloacral dysplasia, MAD #248370) through cDNA microarrays. Gene Expr 12: 39-47.
32. Bakay M, Wang Z, Melcon G, Schiltz L, Xuan J, et al. (2006) Nuclear envelope dystrophies show a transcriptional fingerprint suggesting disruption of Rb-MyoD pathways in muscle regeneration. Brain 129: 996-1013.
33. Ly DH, Lockhart DJ, Lerner RA, Schultz PG, (2000) Mitotic misregulation and human aging. Science 287: 2486-2492.
34. Csoka AB, English SB, Simkevich CP, Ginzinger DG, Butte AJ, et al. (2004) Genome-scale expression profiling of Hutchinson-Gilford progeria syndrome reveals widespread transcriptional misregulation leading to mesodermal/mesenchymal defects and accelerated atherosclerosis. Aging Cell 3: 235-243.
35. Young SG, Meta M, Yang SH, Fong LG, (2006) Prelamin A farnesylation and progeroid syndromes. J Biol Chem 281: 39741-39745.
36. Varela I, Pereira S, Ugalde AP, Navarro CL, Suarez MF, et al. (2008) Combined treatment with statins and aminobisphosphonates extends longevity in a mouse model of human premature aging. Nat Med 14: 767-772.
37. Yang SH, Andres DA, Spielmann HP, Young SG, Fong LG, (2008) Progerin elicits disease phenotypes of progeria in mice whether or not it is farnesylated. J Clin Invest 118: 3291-3300.
38. Davies BS, Barnes RH 2nd, Tu Y, Ren S, Andres DA, et al. (2010) An accumulation of non-farnesylated prelamin A causes cardiomyopathy but not progeria. Hum Mol Genet 19: 2682-2694.
39. Hukriede NA, Joly L, Tsang M, Miles J, Tellis P, et al. (1999) Radiation hybrid mapping of the zebrafish genome. Proc Natl Acad Sci U S A 96: 9745-9750.
40. Meng A, Jessen JR, Lin S, (1999) Transgenesis. Methods Cell Biol 60: 133-148.
41. Gerhard GS, Kauffman EJ, Wang X, Stewart R, Moore JL, et al. (2002) Life spans and senescent phenotypes in two strains of Zebrafish (Danio rerio). Exp Gerontol 37: 1055-1068.
42. Kishi S, Bayliss PE, Uchiyama J, Koshimizu E, Qi J, et al. (2008) The identification of zebrafish mutants showing alterations in senescence-associated biomarkers. PLoS Genet 4: e1000152.
43. Tsai SB, Tucci V, Uchiyama J, Fabian NJ, Lin MC, et al. (2007) Differential effects of genotoxic stress on both concurrent body growth and gradual senescence in the adult zebrafish. Aging Cell 6: 209-224.
44. Kishi S, Uchiyama J, Baughman AM, Goto T, Lin MC, et al. (2003) The zebrafish as a vertebrate model of functional aging and very gradual senescence. Exp Gerontol 38: 777-786.
45. Itahana K, Campisi J, Dimri GP, (2007) Methods to detect biomarkers of cellular senescence: the senescence-associated beta-galactosidase assay. Methods Mol Biol 371: 21-31.
46. Dimri GP, Lee X, Basile G, Acosta M, Scott G, et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 92: 9363-9367.
47. Sullivan T, Escalante-Alcalde D, Bhatt H, Anver M, Bhat N, et al. (1999) Loss of A-type lamin expression compromises nuclear envelope integrity leading to muscular dystrophy. J Cell Biol 147: 913-920.
48. Hernandez L, Roux KJ, Wong ES, Mounkes LC, Mutalif R, et al. (2010) Functional coupling between the extracellular matrix and nuclear lamina by Wnt signaling in progeria. Dev Cell 19: 413-425.
49. Corrigan DP, Kuszczak D, Rusinol AE, Thewke DP, Hrycyna CA, et al. (2005) Prelamin A endoproteolytic processing in vitro by recombinant Zmpste24. Biochem J 387: 129-138.
50. Mounkes LC, Kozlov S, Hernandez L, Sullivan T, Stewart CL, (2003) A progeroid syndrome in mice is caused by defects in A-type lamins. Nature 423: 298-301.
51. Domingo DL, Trujillo MI, Council SE, Merideth MA, Gordon LB, et al. (2009) Hutchinson-Gilford progeria syndrome: oral and craniofacial phenotypes. Oral Dis 15: 187-195.
52. Liu B, Wang J, Chan KM, Tjia WM, Deng W, et al. (2005) Genomic instability in laminopathy-based premature aging. Nat Med 11: 780-785.
53. Schlegel A, Stainier DY, (2006) Microsomal triglyceride transfer protein is required for yolk lipid utilization and absorption of dietary lipids in zebrafish larvae. Biochemistry 45: 15179-15187.
54. Schlombs K, Wagner T, Scheel J, (2003) Site-1 protease is required for cartilage development in zebrafish. Proc Natl Acad Sci U S A 100: 14024-14029.
55. Passeri MJ, Cinaroglu A, Gao C, Sadler KC, (2009) Hepatic steatosis in response to acute alcohol exposure in zebrafish requires sterol regulatory element binding protein activation. Hepatology 49: 443-452.
56. Young SG, Fong LG, Michaelis S, (2005) Prelamin A, Zmpste24, misshapen cell nuclei, and progeria-new evidence suggesting that protein farnesylation could be important for disease pathogenesis. J Lipid Res 46: 2531-2558.
57. Toth JI, Yang SH, Qiao X, Beigneux AP, Gelb MH, et al. (2005) Blocking protein farnesyltransferase improves nuclear shape in fibroblasts from humans with progeroid syndromes. Proc Natl Acad Sci U S A 102: 12873-12878.
58. Mallampalli MP, Huyer G, Bendale P, Gelb MH, Michaelis S, (2005) Inhibiting farnesylation reverses the nuclear morphology defect in a HeLa cell model for Hutchinson-Gilford progeria syndrome. Proc Natl Acad Sci U S A 102: 14416-14421.
59. Davies BS, Fong LG, Yang SH, Coffinier C, Young SG, (2009) The posttranslational processing of prelamin A and disease. Annu Rev Genomics Hum Genet 10: 153-174.
60. Kishi S, Slack BE, Uchiyama J, Zhdanova IV, (2009) Zebrafish as a genetic model in biological and behavioral gerontology: where development meets aging in vertebrates-a mini-review. Gerontology 55: 430-441.
61. Zhdanova IV, Yu L, Lopez-Patino M, Shang E, Kishi S, et al. (2008) Aging of the circadian system in zebrafish and the effects of melatonin on sleep and cognitive performance. Brain Res Bull 75: 433-441.
62. Yu L, Tucci V, Kishi S, Zhdanova IV, (2006) Cognitive aging in zebrafish. PLoS One 1: e14.
63. Kishi S, (2004) Functional aging and gradual senescence in zebrafish. Ann N Y Acad Sci 1019: 521-526.
64. McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, et al. (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.
65. Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, et al. (2010) Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation 121: 2200-2210.
66. Candelario J, Sudhakar S, Navarro S, Reddy S, Comai L, (2008) Perturbation of wild-type lamin A metabolism results in a progeroid phenotype. Aging Cell 7: 355-367.
67. Dialynas G, Speese S, Budnik V, Geyer PK, Wallrath LL, (2010) The role of Drosophila Lamin C in muscle function and gene expression. Development 137: 3067-3077.
68. Wilson KL, Foisner R, (2010) Lamin-binding Proteins. Cold Spring Harb Perspect Biol 2: a000554.
69. Johnson BR, Nitta RT, Frock RL, Mounkes L, Barbie DA, et al. (2004) A-type lamins regulate retinoblastoma protein function by promoting subnuclear localization and preventing proteasomal degradation. Proc Natl Acad Sci U S A 101: 9677-9682.
70. Mariappan I, Gurung R, Thanumalayan S, Parnaik VK, (2007) Identification of cyclin D3 as a new interaction partner of lamin A/C. Biochem Biophys Res Commun 355: 981-985.
71. Mariappan I, Parnaik VK, (2005) Sequestration of pRb by cyclin D3 causes intranuclear reorganization of lamin A/C during muscle cell differentiation. Mol Biol Cell 16: 1948-1960.
72. Nitta RT, Jameson SA, Kudlow BA, Conlan LA, Kennedy BK, (2006) Stabilization of the retinoblastoma protein by A-type nuclear lamins is required for INK4A-mediated cell cycle arrest. Mol Cell Biol 26: 5360-5372.
73. Andres V, Gonzalez JM, (2009) Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol 187: 945-957.
74. Jung YS, Qian Y, Chen X, (2010) Examination of the expanding pathways for the regulation of p21 expression and activity. Cell Signal 22: 1003-1012.
75. Shumaker DK, Dechat T, Kohlmaier A, Adam SA, Bozovsky MR, et al. (2006) Mutant nuclear lamin A leads to progressive alterations of epigenetic control in premature aging. Proc Natl Acad Sci U S A 103: 8703-8708.
76. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, et al. (2008) Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22: 832-853.
77. De Sandre-Giovannoli A, Levy N, (2006) Altered splicing in prelamin A-associated premature aging phenotypes. Prog Mol Subcell Biol 44: 199-232.
78. Rodriguez JI, Perez-Alonso P, Funes R, Perez-Rodriguez J, (1999) Lethal neonatal Hutchinson-Gilford progeria syndrome. Am J Med Genet 82: 242-248.
79. Kaufman CK, White RM, Zon L, (2009) Chemical genetic screening in the zebrafish embryo. Nat Protoc 4: 1422-1432.
80. Peterson RT, Shaw SY, Peterson TA, Milan DJ, Zhong TP, et al. (2004) Chemical suppression of a genetic mutation in a zebrafish model of aortic coarctation. Nat Biotechnol 22: 595-599.
81. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
82. Hofemeister H, Kuhn C, Franke WW, Weber K, Stick R, (2002) Conservation of the gene structure and membrane-targeting signals of germ cell-specific lamin LIII in amphibians and fish. Eur J Cell Biol 81: 51-60.
83. Bennett CM, Kanki JP, Rhodes J, Liu TX, Paw BH, et al. (2001) Myelopoiesis in the zebrafish, Danio rerio. Blood 98: 643-651.
84. Oxtoby E, Jowett T, (1993) Cloning of the zebrafish krox-20 gene (krx-20) and its expression during hindbrain development. Nucleic Acids Res 21: 1087-1095.
85. Liu TX, Howlett NG, Deng M, Langenau DM, Hsu K, et al. (2003) Knockdown of zebrafish Fancd2 causes developmental abnormalities via p53-dependent apoptosis. Dev Cell 5: 903-914.
86. Zeller J, Schneider V, Malayaman S, Higashijima S, Okamoto H, et al. (2002) Migration of zebrafish spinal motor nerves into the periphery requires multiple myotome-derived cues. Dev Biol 252: 241-256.
87. Neuhauss SC, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, et al. (1996) Mutations affecting craniofacial development in zebrafish. Development 123: 357-367.
88. Soroldoni D, Hogan BM, Oates AC, (2009) Simple and efficient transgenesis with meganuclease constructs in zebrafish. Methods Mol Biol 546: 117-130.
89. Grabher C, Joly JS, Wittbrodt J, (2004) Highly efficient zebrafish transgenesis mediated by the meganuclease I-SceI. Methods Cell Biol 77: 381-401.
90. Bland JM, Altman DG, (2004) The logrank test. BMJ 328: 1073.