Lamin A/C Haploinsufficiency Modulates the Differentiation Potential of Mouse Embryonic Stem Cells

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Sehgal, Poonam ^a   Chaturvedi, Pankaj ^a,b   Kumaran, R Ileng ^a,c   Kumar, Satish ^a   Parnaik, Veena K ^a  

^a CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA FETOPROTEIN; BETA TUBULIN; BIOLOGICAL MARKER; LAMIN A; LAMIN C; LAMININ; MESSENGER RNA; NESTIN; OCTAMER TRANSCRIPTION FACTOR 4; SHORT HAIRPIN RNA; STAGE SPECIFIC EMBRYO ANTIGEN 1; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; ENDODERM; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE TARGETING; HAPLOINSUFFICIENCY; HETEROZYGOTE; IN VITRO STUDY; LMNA GENE; MOLECULAR CLONING; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN;

ALPHA-FETOPROTEINS; ANIMALS; CELL DIFFERENTIATION; DOWN-REGULATION; EMBRYOID BODIES; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; ENDODERM; GENE EXPRESSION REGULATION; HAPLOINSUFFICIENCY; HETEROZYGOTE; LAMIN TYPE A; MICE; NEURONS;

EID: 84874344819     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057891     Document Type: Article

References (71)

1. 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.
2. Capell BC, Collins FS, (2006) Human laminopathies: nuclei gone genetically awry. Nat Rev Genet 7: 940-952.
3. Worman HJ, Bonne G, (2007) 'Laminopathies': a wide spectrum of human diseases. Exp Cell Res 313: 2121-2133.
4. 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.
5. Parnaik VK, (2008) Role of nuclear lamins in nuclear organization, cellular signaling, and inherited diseases. Int Rev Cell Mol Biol 266: 157-206.
6. Andrés V, González JM, (2009) Role of A-type lamins in signaling, transcription, and chromatin organization. J Cell Biol 187: 945-957.
7. Parnaik VK, Chaturvedi P, Muralikrishna B, (2011) Lamins, laminopathies and disease mechanisms: possible role for proteasomal degradation of key regulatory proteins. J Biosci 36: 471-479.
8. Sullivan T, Escalante-Acalde 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.
9. Nikolova V, Leimena C, McMahon AC, Tan JC, Chandar S, et al. (2004) Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. J Clin Invest 113: 357-369.
10. Stewart CL, Kozlov S, Fong LG, Young SG, (2007) Mouse models of the laminopathies. Exp Cell Res 313: 2144-2156.
11. Young SG, Jung HJ, Coffinier C, Fong LG, (2012) Understanding the roles of nuclear A- and B-type lamins in brain development. J Biol Chem 287: 16103-16110.
12. Wolf CM, Wang L, Alcalai R, Pizard A, Burgon PG, et al. (2008) Lamin A/C haploinsufficiency causes dilated cardiomyopathy and apoptosis-triggered cardiac conduction system disease. J Mol Cell Cardiol 44: 293-303.
13. Jahn D, Schramm S, Schnölzer M, Heilmann CJ, de Koster CG, et al. (2012) A truncated lamin A in the Lmna-/- mouse line: Implications for the understanding of laminopathies. Nucleus 3: 463-474.
14. Kumaran RI, Muralikrishna B, Parnaik VK, (2002) Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA polymerase II transcription. J Cell Biol 159: 783-793.
15. Spann TP, Goldman AE, Wang C, Huang S, Goldman RD, (2002) Alteration of nuclear lamin organization inhibits RNA polymerase II-dependent transcription. J Cell Biol 156: 603-608.
16. Solter D, (2006) From teratocarcinomas to embryonic stem cells and beyond: a history of embryonic stem cell research. Nat Rev Genet 7: 319-327.
17. Rossant J, (2007) Stem cells and lineage development in the mammalian blastocyst. Reprod Fertil Dev 19: 111-118.
18. Niwa H, (2010) Mouse ES cell culture system as a model of development. Dev Growth Differ 52: 275-283.
19. Schatten G, Maul GG, Schatten H, Chaly N, Simerly C, et al. (1985) Nuclear lamins and peripheral nuclear antigens during fertilization and embryogenesis in mice and sea urchins. Proc Natl Acad Sci USA 82: 4727-4731.
20. 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.
21. Röber 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.
22. 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.
23. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956.
24. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440.
25. Rogers MB, Hosler BA, Gudas LJ, (1991) Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 113: 815-824.
26. Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, et al. (1988) Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336: 688-690.
27. Beddington RS, Robertson EJ, (1989) An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105: 733-737.
28. Martin GR, Wiley LM, Damjanov I, (1977) The development of cystic embryoid bodies in vitro from clonal teratocarcinoma stem cells. Dev Biol 61: 230-244.
29. Doetschman TC, Eistetter H, Katz M, Schmidt W, Kemler R, (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87: 27-45.
30. Coucouvanis E, Martin GR, (1995) Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83: 279-287.
31. Dziadek M, Adamson E, (1978) Localization and synthesis of alphafoetoprotein in post-implantation mouse embryos. J Embryol Exp Morphol 43: 289-313.
32. Lazarevich NL, (2000) Molecular mechanisms of alpha-fetoprotein gene expression. Biochemistry (Mosc) 65: 117-133.
33. Soudais C, Bielinska M, Heikinheimo M, MacArthur CA, Narita N, et al. (1995) Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121: 3877-3888.
34. Coffinier C, Thépot D, Babinet C, Yaniv M, Barra J, (1999) Essential role for the homeoprotein vHNF1/HNF1beta in visceral endoderm differentiation. Development 126: 4785-4794.
35. Koutsourakis M, Langeveld A, Patient R, Beddington R, Grosveld F, (1999) The transcription factor GATA6 is essential for early extraembryonic development. Development 126: 723-732.
36. Dufort D, Schwartz L, Harpal K, Rossant J, (1998) The transcription factor HNF3beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125: 3015-3025.
37. Ang SL, Wierda A, Wong D, Stevens KA, Cascio S, et al. (1993) The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119: 1301-1315.
38. Thomas PQ, Brown A, Beddington RS, (1998) Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors. Development 125: 85-94.
39. Li H, Liu H, Corrales CE, Risner JR, Forrester J, et al. (2009) Differentiation of neurons from neural precursors generated in floating spheres from embryonic stem cells. BMC Neurosci 10: 122.
40. Bylund M, Andersson E, Novitch BG, Muhr J, (2003) Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6: 1162-1168.
41. Kan L, Israsena N, Zhang Z, Hu M, Zhao LR, et al. (2004) Sox1 acts through multiple independent pathways to promote neurogenesis. Dev Biol 269: 580-594.
42. Zhou Q, Wang S, Anderson DJ, (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25: 331-343.
43. Herrmann BG, Kispert A, (1994) The T genes in embryogenesis. Trends Genet 10: 280-286.
44. Kubo A, Shinozaki K, Shannon JM, Kouskoff V, Kennedy M, et al. (2004) Development of definitive endoderm from embryonic stem cells in culture. Development 131: 1651-1662.
45. Lassar AB, Skapek SX, Novitch B, (1994) Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr Opin Cell Biol 6: 788-794.
46. Rudnicki MA, Jaenisch R, (1995) The MyoD family of transcription factors and skeletal myogenesis. Bioessays 17: 203-209.
47. Crispino JD, Lodish MB, Thurberg BL, Litovsky SH, Collins T, et al. (2001) Proper coronary vascular development and heart morphogenesis depend on interaction of GATA-4 with FOG cofactors. Genes Dev 15: 839-844.
48. Winnier G, Blessing M, Labosky PA, Hogan BL, (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in mouse. Genes Dev 9: 2105-2116.
49. Charron F, Nemer M, (1999) GATA transcription factors and cardiac development. Semin Cell Dev Biol 10: 85-91.
50. Hall VJ, Cooney MA, Shanahan P, Tecirlioglu RT, Ruddock NT, et al. (2005) Nuclear lamin antigen and messenger RNA expression in bovine in vitro produced and nuclear transfer embryos. Mol Reprod Dev 72: 471-482.
51. 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.
52. Meshorer E, Misteli T, (2006) Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev Mol Cell Biol 7: 540-546.
53. Jung HJ, Coffinier C, Choe Y, Beigneux AP, Davies BS, 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.
54. Kennedy KA, Ostrakhovitch EA, Sandiford SD, Dayarathna T, Xie X, et al. (2010) Mammalian numb-interacting protein 1/dual oxidase maturation factor 1 directs neuronal fate in stem cells. J Biol Chem 285: 17974-17985.
55. 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 Cell Biol 24: 1481-1492.
56. Frock RL, Kudlow BA, Evans AM, Jameson SA, Hauschka SD, et al. (2006) Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation. Genes Dev 20: 486-500.
57. Parnaik VK, Manju K, (2006) Laminopathies: multiple disorders arising from defects in nuclear architecture. J Biosci 31: 405-421.
58. 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.
59. Markiewicz E, Ledran M, Hutchison CJ, (2005) Remodelling of the nuclear lamina and nucleoskeleton is required for skeletal muscle differentiation in vitro. J Cell Sci 118: 409-420.
60. Cupesi M, Yoshioka J, Gannon J, Kudinova A, Stewart CL, et al. (2010) Attenuated hypertrophic response to pressure overload in a lamin A/C haploinsufficiency mouse. J Mol Cell Cardiol 48: 1290-1297.
61. Duque G, Li W, Yeo LS, Vidal C, Fatkin D, (2011) Attenuated anabolic response to exercise in lamin A/C haploinsufficient mice. Bone 49: 412-418.
62. Tong J, Li W, Vidal C, Yeo LS, Fatkin D, et al. (2011) Lamin A/C deficiency is associated with fat infiltration of muscle and bone. Mech Ageing Dev 132: 552-559.
63. Bonne G, Di Barletta MR, Varnous S, Bécane HM, Hammouda EH, et al. (1999) Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat Genet 21: 285-288.
64. Muchir A, van Engelen BG, Lammens M, Mislow JM, McNally E, et al. (2003) Nuclear envelope alterations in fibroblasts from LGMD1B patients carrying nonsense Y259X heterozygous or homozygous mutation in lamin A/C gene. Exp Cell Res 291: 352-362.
65. Vlcek S, Foisner R, (2007) Lamins and lamin-associated proteins in aging and disease. Curr Opin Cell Biol 19: 298-304.
66. Pekovic V, Hutchison CJ, (2008) Adult stem cell maintenance and tissue regeneration in the ageing context: the role for A-type lamins as intrinsic modulators of ageing in adult stem cells and their niches. J Anat 213: 5-25.
67. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC, (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc Natl Acad Sci USA 90: 8424-8428.
68. Muralikrishna Bh, Chaturvedi P, Sinha K, Parnaik VK, (2012) Lamin misexpression mediates ATR kinase degradation by activation of three distinct ubiquitin ligase systems. Mol Cell Biochem 365: 323-332.
69. Metzger JM, Lin WI, Samuelson LC, (1996) Vital staining of cardiac myocytes during embryonic stem cell cardiogenesis in vitro. Circ Res 78: 547-552.
70. Kim WK, Lee CY, Kang MS, Kim MH, Ryu YH, et al. (2008) Effects of leptin on lipid metabolism and gene expression of differentiation-associated growth factors and transcription factors during differentiation and maturation of 3T3-L1 preadipocytes. Endocr J 55: 827-837.
71. Perrien DS, Achenbach SJ, Bledsoe SE, Walser B, Suva LJ, et al. (2006) Bone turnover across the menopause transition: correlations with inhibins and follicle-stimulating hormone. J Clin Endocrinol Metab 91: 1848-1854.