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PMID: 19720741 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Overlapping functions of nuclear envelope proteins NET25 (Lem2) and emerin in regulation of extracellular signal-regulated kinase signaling in myoblast differentiation.

Molecular and cellular biology ·Vol. 29 ·No. 21 ·2009-11-00 ·Pages 5718-28

Huber MD, Guan T, Gerace L

Abstract

Mutations in certain nuclear envelope (NE) proteins cause muscular dystrophies and other disorders, but the disease mechanisms remain unclear. The nuclear envelope transmembrane protein NET25 (Lem2) is a truncated paralog of MAN1, an NE component linked to bone disorders. NET25 and MAN1 share an approximately 40-residue LEM homology domain with emerin, the protein mutated in X-linked Emery-Dreifuss muscular dystrophy. However, roles for NET25 and MAN1 in myogenesis have not yet been described. Using RNA interference in C2C12 myoblasts, we show for the first time that both NET25 and MAN1 are required for myogenic differentiation. NET25 depletion causes hyperactivation of extracellular signal-regulated kinase 1/2 at the onset of differentiation, and pharmacological inhibition of this transient overactivation rescues myogenesis. In contrast, pharmacological inhibition of both mitogen-activated protein kinase and transforming growth factor beta signaling is required to rescue differentiation after MAN1 depletion. Ectopic expression of silencing-resistant NET25 rescues myogenesis after depletion of emerin but not after MAN1 silencing. Thus, NET25 and emerin have at least partially overlapping functions during myogenic differentiation, which are distinct from those of MAN1. Our work supports the hypothesis that deregulation of cell signaling contributes to NE-linked disorders and suggests that mutations in NET25 and MAN1 may cause muscle diseases.

MeSH Terms
Animals Cell Cycle/drug effects Cell Differentiation/drug effects Cells, Cultured DNA-Binding Proteins/metabolism Epidermal Growth Factor/pharmacology Extracellular Signal-Regulated MAP Kinases/metabolism Genetic Complementation Test Humans MAP Kinase Signaling System/drug effects Membrane Proteins/chemistry,deficiency,metabolism Mice Muscle Development/drug effects Myoblasts/cytology,drug effects,enzymology Nuclear Envelope/drug effects,metabolism Nuclear Proteins/chemistry,deficiency,metabolism
Chemicals
DNA-Binding Proteins LEMD2 protein, human Man1 protein, mouse Membrane Proteins Nuclear Proteins emerin lamina-associated polypeptide 2 Epidermal Growth Factor Extracellular Signal-Regulated MAP Kinases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Huber Michael D
Department of Cell Biology, IMM-10, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
Guan Tinglu
Gerace Larry
References (42)
42 references, click to expand
  1. What MAN1 does to the Smads. TGFbeta/BMP signaling and the nuclear envelope.
    FEBS J. 2007 Mar;274(6):1374-82 PMID: 17489095
  2. The nuclear envelope protein MAN1 regulates TGFbeta signaling and vasculogenesis in the embryonic yolk sac.
    Development. 2007 Apr;134(7):1385-95 PMID: 17329363
  3. Lamin A/C and emerin are critical for skeletal muscle satellite cell differentiation.
    Genes Dev. 2006 Feb 15;20(4):486-500 PMID: 16481476
  4. Man1, an inner nuclear membrane protein, regulates vascular remodeling by modulating transforming growth factor beta signaling.
    Development. 2006 Oct;133(19):3919-28 PMID: 16943282
  5. Efficient suppression of FGF-2-induced ERK activation by the cooperative interaction among mammalian Sprouty isoforms.
    J Cell Sci. 2005 Dec 15;118(Pt 24):5861-71 PMID: 16339969
  6. Cellular and molecular regulation of muscle regeneration.
    Physiol Rev. 2004 Jan;84(1):209-38 PMID: 14715915
  7. Insulin restores differentiation of Ras-transformed C2C12 myoblasts by inducing NF-kappaB through an AKT/P70S6K/p38-MAPK pathway.
    Oncogene. 2002 May 23;21(23):3739-53 PMID: 12032842
  8. LEM2 is a novel MAN1-related inner nuclear membrane protein associated with A-type lamins.
    J Cell Sci. 2005 Dec 15;118(Pt 24):5797-810 PMID: 16339967
  9. Docking domains and substrate-specificity determination for MAP kinases.
    Trends Biochem Sci. 2000 Sep;25(9):448-53 PMID: 10973059
  10. Mechanotransduction in cardiac myocytes.
    Ann N Y Acad Sci. 2004 May;1015:53-70 PMID: 15201149
  11. Asymmetric self-renewal and commitment of satellite stem cells in muscle.
    Cell. 2007 Jun 1;129(5):999-1010 PMID: 17540178
  12. Differentiation of C2C12 myoblasts expressing lamin A mutated at a site responsible for Emery-Dreifuss muscular dystrophy is improved by inhibition of the MEK-ERK pathway and stimulation of the PI3-kinase pathway.
    Exp Cell Res. 2008 Apr 1;314(6):1392-405 PMID: 18294630
  13. The carboxyl-terminal nucleoplasmic region of MAN1 exhibits a DNA binding winged helix domain.
    J Biol Chem. 2006 Jun 30;281(26):18208-15 PMID: 16648637
  14. Nuclear envelope transmembrane proteins (NETs) that are up-regulated during myogenesis.
    BMC Cell Biol. 2006 Oct 24;7:38 PMID: 17062158
  15. Reduced expression of A-type lamins and emerin activates extracellular signal-regulated kinase in cultured cells.
    Biochim Biophys Acta. 2009 Jan;1792(1):75-81 PMID: 19022376
  16. Integral membrane proteins of the nuclear envelope are dispersed throughout the endoplasmic reticulum during mitosis.
    J Cell Biol. 1997 Jun 16;137(6):1199-210 PMID: 9182656
  17. Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells.
    J Cell Biol. 2005 Aug 29;170(5):781-91 PMID: 16115958
  18. Integral membrane proteins of the nuclear envelope interact with lamins and chromosomes, and binding is modulated by mitotic phosphorylation.
    Cell. 1993 Jul 2;73(7):1267-79 PMID: 8324822
  19. Direct binding of nuclear membrane protein MAN1 to emerin in vitro and two modes of binding to barrier-to-autointegration factor.
    J Biol Chem. 2005 Apr 8;280(14):13863-70 PMID: 15681850
  20. Identification of a novel inhibitor of mitogen-activated protein kinase kinase.
    J Biol Chem. 1998 Jul 17;273(29):18623-32 PMID: 9660836
  21. MAN1, an integral protein of the inner nuclear membrane, binds Smad2 and Smad3 and antagonizes transforming growth factor-beta signaling.
    Hum Mol Genet. 2005 Feb 1;14(3):437-45 PMID: 15601644
  22. Lamin A/C deficiency causes defective nuclear mechanics and mechanotransduction.
    J Clin Invest. 2004 Feb;113(3):370-8 PMID: 14755334
  23. The integral inner nuclear membrane protein MAN1 physically interacts with the R-Smad proteins to repress signaling by the transforming growth factor-{beta} superfamily of cytokines.
    J Biol Chem. 2005 Apr 22;280(16):15992-6001 PMID: 15647271
  24. The duration, magnitude and compartmentalization of ERK MAP kinase activity: mechanisms for providing signaling specificity.
    J Cell Sci. 2005 Jul 15;118(Pt 14):2997-3002 PMID: 16014377
  25. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT.
    J Biol Chem. 2005 Dec 16;280(50):41342-51 PMID: 16251184
  26. Loss-of-function mutations in LEMD3 result in osteopoikilosis, Buschke-Ollendorff syndrome and melorheostosis.
    Nat Genet. 2004 Nov;36(11):1213-8 PMID: 15489854
  27. Inner nuclear membrane and regulation of Smad-mediated signaling.
    Biochim Biophys Acta. 2006 May-Jun;1761(5-6):626-31 PMID: 16574476
  28. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis.
    J Cell Biol. 1996 Feb;132(4):657-66 PMID: 8647896
  29. Long-term outcome and risk stratification in dilated cardiolaminopathies.
    J Am Coll Cardiol. 2008 Oct 7;52(15):1250-60 PMID: 18926329
  30. "Laminopathies": a wide spectrum of human diseases.
    Exp Cell Res. 2007 Jun 10;313(10):2121-33 PMID: 17467691
  31. Activation of MAPK in hearts of EMD null mice: similarities between mouse models of X-linked and autosomal dominant Emery Dreifuss muscular dystrophy.
    Hum Mol Genet. 2007 Aug 1;16(15):1884-95 PMID: 17567779
  32. Identification of a novel X-linked gene responsible for Emery-Dreifuss muscular dystrophy.
    Nat Genet. 1994 Dec;8(4):323-7 PMID: 7894480
  33. Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation.
    Cell. 1995 Jan 27;80(2):179-85 PMID: 7834738
  34. The inner nuclear membrane protein Lem2 is critical for normal nuclear envelope morphology.
    FEBS Lett. 2006 Nov 27;580(27):6435-41 PMID: 17097643
  35. Nuclear membrane proteins with potential disease links found by subtractive proteomics.
    Science. 2003 Sep 5;301(5638):1380-2 PMID: 12958361
  36. Expression of a mutant lamin A that causes Emery-Dreifuss muscular dystrophy inhibits in vitro differentiation of C2C12 myoblasts.
    Mol Cell Biol. 2004 Feb;24(4):1481-92 PMID: 14749366
  37. Scansite 2.0: Proteome-wide prediction of cell signaling interactions using short sequence motifs.
    Nucleic Acids Res. 2003 Jul 1;31(13):3635-41 PMID: 12824383
  38. Blurring the boundary: the nuclear envelope extends its reach.
    Science. 2007 Nov 30;318(5855):1408-12 PMID: 18048680
  39. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy.
    Nat Genet. 1999 Mar;21(3):285-8 PMID: 10080180
  40. Molecular interpretation of ERK signal duration by immediate early gene products.
    Nat Cell Biol. 2002 Aug;4(8):556-64 PMID: 12134156
  41. Identification of mutations in the gene encoding lamins A/C in autosomal dominant limb girdle muscular dystrophy with atrioventricular conduction disturbances (LGMD1B).
    Hum Mol Genet. 2000 May 22;9(9):1453-9 PMID: 10814726
  42. Sprouty-2 overexpression in C2C12 cells confers myogenic differentiation properties in the presence of FGF2.
    Mol Biol Cell. 2005 Sep;16(9):4454-61 PMID: 16000370
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
1098-5549
Published
2009-11-00
Epub
2009-00-31
Pages
5718-28
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC2772735
Subset
IM
Grants
NIGMS NIH HHS · R01 GM028521 · United States
NIGMS NIH HHS · R01 GM028521-26 · United States
NIGMS NIH HHS · R01 GM28521 · United States
NIGMS NIH HHS · R01 GM028521-27 · United States
NIGMS NIH HHS · F32 GM080045 · United States
NIGMS NIH HHS · R01 GM028521-25A1 · United States
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