Dominant Lethal Pathologies in Male Mice Engineered to Contain an X-Linked DUX4 Transgene

Cell Reports

Volumn 8, Issue 5, 2014, Pages 1484-1496

  Dandapat, Abhijit ^a   Bosnakovski, Darko ^a   Hartweck, Lynn M ^a   Arpke, Robert W ^a   Baltgalvis, Kristen A ^b   Vang, Derek ^b   Baik, June ^a   Darabi, Radbod ^a   Perlingeiro, Rita C R ^a   Hamra, F Kent ^c   Gupta, Kalpna ^b   Lowe, Dawn A ^b   Kyba, Michael ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; GENOMIC DNA; RNA; DUX4 PROTEIN, MOUSE; EUCHROMATIN; HOMEODOMAIN PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; DUX4 GENE; EPIGENETICS; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; FEMALE; GENE EXPRESSION; GENETIC ENGINEERING; IN VITRO STUDY; IN VIVO STUDY; LETHALITY; MALE; MOLECULAR PATHOLOGY; MOUSE; MOUSE MODEL; MUSCLE DISEASE; MUSCLE STEM CELL; NONHUMAN; PHENOTYPE; RETINAL TELANGIECTASIA; SATELLITE CELL; TRANSGENE; X CHROMOSOME; X CHROMOSOME LINKED DISORDER; ANIMAL; CELL CULTURE; DISEASE MODEL; DOMINANT GENE; EUCHROMATIN; GENETICS; METABOLISM; PATHOLOGY; RETINA; TRANSGENIC MOUSE; X CHROMOSOMAL INHERITANCE;

ANIMALIA; MUS;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; EUCHROMATIN; GENES, DOMINANT; GENES, X-LINKED; HOMEODOMAIN PROTEINS; MALE; MICE; MICE, TRANSGENIC; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; PHENOTYPE; RETINA; RNA, MESSENGER;

EID: 84922547186     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.056     Document Type: Article

References (59)

1. Agha-Mohammadi S., O'Malley M., Etemad A., Wang Z., Xiao X., Lotze M.T. Second-generation tetracycline-regulatable promoter: repositioned tet operator elements optimize transactivator synergy while shorter minimal promoter offers tight basal leakiness. J.Gene Med. 2004, 6:817-828.
2. Arpke R.W., Darabi R., Mader T.L., Zhang Y., Toyama A., Lonetree C.L., Nash N., Lowe D.A., Perlingeiro R.C., Kyba M. A new immuno-, dystrophin-deficient model, the NSG-mdx(4Cv) mouse, provides evidence for functional improvement following allogeneic satellite cell transplantation. Stem Cells 2013, 31:1611-1620.
3. Bakker E., Wijmenga C., Vossen R.H., Padberg G.W., Hewitt J., van der Wielen M., Rasmussen K., Frants R.R. The FSHD-linked locus D4F104S1 (p13E-11) on 4q35 has a homologue on 10qter. Muscle Nerve Suppl. 1995, 2:S39-S44.
4. Block G.J., Narayanan D., Amell A.M., Petek L.M., Davidson K.C., Bird T.D., Tawil R., Moon R.T., Miller D.G. Wnt/β-catenin signaling suppresses DUX4 expression and prevents apoptosis of FSHD muscle cells. Hum. Mol. Genet. 2013, 22:4661-4672.
5. Bosnakovski D., Xu Z., Gang E.J., Galindo C.L., Liu M., Simsek T., Garner H.R., Agha-Mohammadi S., Tassin A., Coppée F., et al. An isogenetic myoblast expression screen identifies DUX4-mediated FSHD-associated molecular pathologies. EMBO J. 2008, 27:2766-2779.
6. Bosnakovski D., Lamb S., Simsek T., Xu Z., Belayew A., Perlingeiro R., Kyba M. DUX4c, an FSHD candidate gene, interferes with myogenic regulators and abolishes myoblast differentiation. Exp. Neurol. 2008, 214:87-96.
7. Bosnakovski D., Xu Z., Li W., Thet S., Cleaver O., Perlingeiro R.C., Kyba M. Prospective isolation of skeletal muscle stem cells with a Pax7 reporter. Stem Cells 2008, 26:3194-3204.
8. Bronson S.K., Plaehn E.G., Kluckman K.D., Hagaman J.R., Maeda N., Smithies O. Single-copy transgenic mice with chosen-site integration. Proc. Natl. Acad. Sci. USA 1996, 93:9067-9072.
9. Brouwer O.F., Padberg G.W., Ruys C.J., Brand R., de Laat J.A., Grote J.J. Hearing loss in facioscapulohumeral muscular dystrophy. Neurology 1991, 41:1878-1881.
10. Celegato B., Capitanio D., Pescatori M., Romualdi C., Pacchioni B., Cagnin S., Viganò A., Colantoni L., Begum S., Ricci E., et al. Parallel protein and transcript profiles of FSHD patient muscles correlate to the D4Z4 arrangement and reveal a common impairment of slow to fast fibre differentiation and a general deregulation of MyoD-dependent genes. Proteomics 2006, 6:5303-5321.
11. Chan S.S., Shi X., Toyama A., Arpke R.W., Dandapat A., Iacovino M., Kang J., Le G., Hagen H.R., Garry D.J., Kyba M. Mesp1 patterns mesoderm into cardiac, hematopoietic, or skeletal myogenic progenitors in a context-dependent manner. Cell Stem Cell 2013, 12:587-601.
12. Chen T.H., Lai Y.H., Lee P.L., Hsu J.H., Goto K., Hayashi Y.K., Nishino I., Lin C.W., Shih H.H., Huang C.C., et al. Infantile facioscapulohumeral muscular dystrophy revisited: Expansion of clinical phenotypes in patients with a very short EcoRI fragment. Neuromuscul. Disord. 2013, 23:298-305.
13. Clapp J., Mitchell L.M., Bolland D.J., Fantes J., Corcoran A.E., Scotting P.J., Armour J.A., Hewitt J.E. Evolutionary conservation of a coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 2007, 81:264-279.
14. Cvetkovic B., Yang B., Williamson R.A., Sigmund C.D. Appropriate tissue- and cell-specific expression of a single copy human angiotensinogen transgene specifically targeted upstream of the HPRT locus by homologous recombination. J.Biol. Chem. 2000, 275:1073-1078.
15. de Greef J.C., Lemmers R.J., van Engelen B.G., Sacconi S., Venance S.L., Frants R.R., Tawil R., van der Maarel S.M. Common epigenetic changes of D4Z4 in contraction-dependent and contraction-independent FSHD. Hum. Mutat. 2009, 30:1449-1459.
16. Deidda G., Cacurri S., Piazzo N., Felicetti L. Direct detection of 4q35 rearrangements implicated in facioscapulohumeral muscular dystrophy (FSHD). J.Med. Genet. 1996, 33:361-365.
17. Dixit M., Ansseau E., Tassin A., Winokur S., Shi R., Qian H., Sauvage S., Mattéotti C., van Acker A.M., Leo O., et al. DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc. Natl. Acad. Sci. USA 2007, 104:18157-18162.
18. Fitzsimons R.B., Gurwin E.B., Bird A.C. Retinal vascular abnormalities in facioscapulohumeral muscular dystrophy. A general association with genetic and therapeutic implications. Brain 1987, 110:631-648.
19. Gabellini D., Green M.R., Tupler R. Inappropriate gene activation in FSHD: a repressor complex binds a chromosomal repeat deleted in dystrophic muscle. Cell 2002, 110:339-348.
20. Gabriëls J., Beckers M.C., Ding H., De Vriese A., Plaisance S., van der Maarel S.M., Padberg G.W., Frants R.R., Hewitt J.E., Collen D., Belayew A. Nucleotide sequence of the partially deleted D4Z4 locus in a patient with FSHD identifies a putative gene within each 3.3 kb element. Gene 1999, 236:25-32.
21. Geng L.N., Tyler A.E., Tapscott S.J. Immunodetection of human double homeobox 4. Hybridoma (Larchmt) 2011, 30:125-130.
22. Gieron M.A., Korthals J.K., Kousseff B.G. Facioscapulohumeral dystrophy with cochlear hearing loss and tortuosity of retinal vessels. Am. J. Med. Genet. 1985, 22:143-147.
23. Greising S.M., Call J.A., Lund T.C., Blazar B.R., Tolar J., Lowe D.A. Skeletal muscle contractile function and neuromuscular performance in Zmpste24 -/- mice, a murine model of human progeria. Age (Dordr.) 2012, 34:805-819.
24. Gupta K., Kshirsagar S., Chang L., Schwartz R., Law P.Y., Yee D., Hebbel R.P. Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res. 2002, 62:4491-4498.
25. Hao J., Yamamoto M., Richardson T.E., Chapman K.M., Denard B.S., Hammer R.E., Zhao G.Q., Hamra F.K. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008, 26:1587-1597.
26. Hartweck L.M., Anderson L.J., Lemmers R.J., Dandapat A., Toso E.A., Dalton J.C., Tawil R., Day J.W., van der Maarel S.M., Kyba M. A focal domain of extreme demethylation within D4Z4 in FSHD2. Neurology 2013, 80:392-399.
27. Hochedlinger K., Yamada Y., Beard C., Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 2005, 121:465-477.
28. Iacovino M., Bosnakovski D., Fey H., Rux D., Bajwa G., Mahen E., Mitanoska A., Xu Z., Kyba M. Inducible cassette exchange: a rapid and efficient system enabling conditional gene expression in embryonic stem and primary cells. Stem Cells 2011, 29:1580-1588.
29. Joe A.W., Yi L., Natarajan A., Le Grand F., So L., Wang J., Rudnicki M.A., Rossi F.M. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 2010, 12:153-163.
30. Jones T.I., Chen J.C., Rahimov F., Homma S., Arashiro P., Beermann M.L., King O.D., Miller J.B., Kunkel L.M., Emerson C.P., et al. Facioscapulohumeral muscular dystrophy family studies of DUX4 expression: evidence for disease modifiers and a quantitative model of pathogenesis. Hum. Mol. Genet. 2012, 21:4419-4430.
31. Kowaljow V., Marcowycz A., Ansseau E., Conde C.B., Sauvage S., Mattéotti C., Arias C., Corona E.D., Nuñez N.G., Leo O., et al. The DUX4 gene at the FSHD1A locus encodes a pro-apoptotic protein. Neuromuscul. Disord. 2007, 17:611-623.
32. Krom Y.D., Thijssen P.E., Young J.M., den Hamer B., Balog J., Yao Z., Maves L., Snider L., Knopp P., Zammit P.S., et al. Intrinsic epigenetic regulation of the D4Z4 macrosatellite repeat in a transgenic mouse model for FSHD. PLoS Genet. 2013, 9:e1003415.
33. Leidenroth A., Hewitt J.E. A family history of DUX4: phylogenetic analysis of DUXA, B, C and Duxbl reveals the ancestral DUX gene. BMC Evol. Biol. 2010, 10:364.
34. Lemmers R.J., Wohlgemuth M., Frants R.R., Padberg G.W., Morava E., van der Maarel S.M. Contractions of D4Z4 on 4qB subtelomeres do not cause facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 2004, 75:1124-1130.
35. Lemmers R.J., Wohlgemuth M., van der Gaag K.J., van der Vliet P.J., van Teijlingen C.M., de Knijff P., Padberg G.W., Frants R.R., van der Maarel S.M. Specific sequence variations within the 4q35 region are associated with facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 2007, 81:884-894.
36. Lemmers R.J., van der Vliet P.J., Klooster R., Sacconi S., Camaño P., Dauwerse J.G., Snider L., Straasheijm K.R., van Ommen G.J., Padberg G.W., et al. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 2010, 329:1650-1653.
37. Lemmers R.J., Tawil R., Petek L.M., Balog J., Block G.J., Santen G.W., Amell A.M., van der Vliet P.J., Almomani R., Straasheijm K.R., et al. Digenic inheritance of an SMCHD1 mutation and an FSHD-permissive D4Z4 allele causes facioscapulohumeral muscular dystrophy type 2. Nat. Genet. 2012, 44:1370-1374.
38. Lemos D.R., Paylor B., Chang C., Sampaio A., Underhill T.M., Rossi F.M. Functionally convergent white adipogenic progenitors of different lineages participate in a diffused system supporting tissue regeneration. Stem Cells 2012, 30:1152-1162.
39. Lin M.Y., Nonaka I. Facioscapulohumeral muscular dystrophy: muscle fiber type analysis with particular reference to small angular fibers. Brain Dev. 1991, 13:331-338.
40. Lutz K.L., Holte L., Kliethermes S.A., Stephan C., Mathews K.D. Clinical and genetic features of hearing loss in facioscapulohumeral muscular dystrophy. Neurology 2013, 81:1374-1377.
41. Olsen D.B., Ørngreen M.C., Vissing J. Aerobic training improves exercise performance in facioscapulohumeral muscular dystrophy. Neurology 2005, 64:1064-1066.
42. Osborne R.J., Welle S., Venance S.L., Thornton C.A., Tawil R. Expression profile of FSHD supports a link between retinal vasculopathy and muscular dystrophy. Neurology 2007, 68:569-577.
43. Padberg G.W., Brouwer O.F., de Keizer R.J., Dijkman G., Wijmenga C., Grote J.J., Frants R.R. On the significance of retinal vascular disease and hearing loss in facioscapulohumeral muscular dystrophy. Muscle Nerve Suppl. 1995, 2:S73-S80.
44. Portales-Casamar E., Swanson D.J., Liu L., de Leeuw C.N., Banks K.G., Ho Sui S.J., Fulton D.L., Ali J., Amirabbasi M., Arenillas D.J., et al. A regulatory toolbox of MiniPromoters to drive selective expression in the brain. Proc. Natl. Acad. Sci. USA 2010, 107:16589-16594.
45. Small R.G. Coats' disease and muscular dystrophy. Trans. Am. Acad. Ophthalmol. Otolaryngol. 1968, 72:225-231.
46. Snider L., Asawachaicharn A., Tyler A.E., Geng L.N., Petek L.M., Maves L., Miller D.G., Lemmers R.J., Winokur S.T., Tawil R., et al. RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum. Mol. Genet. 2009, 18:2414-2430.
47. Snider L., Geng L.N., Lemmers R.J., Kyba M., Ware C.B., Nelson A.M., Tawil R., Filippova G.N., van der Maarel S.M., Tapscott S.J., Miller D.G. Facioscapulohumeral dystrophy: incomplete suppression of a retrotransposed gene. PLoS Genet. 2010, 6:e1001181.
48. Tassin A., Laoudj-Chenivesse D., Vanderplanck C., Barro M., Charron S., Ansseau E., Chen Y.W., Mercier J., Coppée F., Belayew A. DUX4 expression in FSHD muscle cells: how could such a rare protein cause a myopathy?. J.Cell. Mol. Med. 2013, 17:76-89.
49. Touw K., Hoggatt A.M., Simon G., Herring B.P. Hprt-targeted transgenes provide new insights into smooth muscle-restricted promoter activity. Am. J. Physiol. Cell Physiol. 2007, 292:C1024-C1032.
50. Turki A., Hayot M., Carnac G., Pillard F., Passerieux E., Bommart S., Raynaud de Mauverger E., Hugon G., Pincemail J., Pietri S., et al. Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction. Free Radic. Biol. Med. 2012, 53:1068-1079.
51. Uezumi A., Fukada S., Yamamoto N., Takeda S., Tsuchida K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 2010, 12:143-152.
52. van Deutekom J.C., Wijmenga C., van Tienhoven E.A., Gruter A.M., Hewitt J.E., Padberg G.W., van Ommen G.J., Hofker M.H., Frants R.R. FSHD associated DNA rearrangements are due to deletions of integral copies of a 3.2 kb tandemly repeated unit. Hum. Mol. Genet. 1993, 2:2037-2042.
53. van Overveld P.G., Lemmers R.J., Sandkuijl L.A., Enthoven L., Winokur S.T., Bakels F., Padberg G.W., van Ommen G.J., Frants R.R., van der Maarel S.M. Hypomethylation of D4Z4 in 4q-linked and non-4q-linked facioscapulohumeral muscular dystrophy. Nat. Genet. 2003, 35:315-317.
54. Wallace L.M., Garwick S.E., Mei W., Belayew A., Coppee F., Ladner K.J., Guttridge D., Yang J., Harper S.Q. DUX4, a candidate gene for facioscapulohumeral muscular dystrophy, causes p53-dependent myopathy invivo. Ann. Neurol. 2011, 69:540-552.
55. Wijmenga C., Hewitt J.E., Sandkuijl L.A., Clark L.N., Wright T.J., Dauwerse H.G., Gruter A.M., Hofker M.H., Moerer P., Williamson R., et al. Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat. Genet. 1992, 2:26-30.
56. Winokur S.T., Chen Y.W., Masny P.S., Martin J.H., Ehmsen J.T., Tapscott S.J., van der Maarel S.M., Hayashi Y., Flanigan K.M. Expression profiling of FSHD muscle supports a defect in specific stages of myogenic differentiation. Hum. Mol. Genet. 2003, 12:2895-2907.
57. Winokur S.T., Barrett K., Martin J.H., Forrester J.R., Simon M., Tawil R., Chung S.A., Masny P.S., Figlewicz D.A. Facioscapulohumeral muscular dystrophy (FSHD) myoblasts demonstrate increased susceptibility to oxidative stress. Neuromuscul. Disord. 2003, 13:322-333.
58. Wu S.L., Tsai M.S., Wong S.H., Hsieh-Li H.M., Tsai T.S., Chang W.T., Huang S.L., Chiu C.C., Wang S.H. Characterization of genomic structures and expression profiles of three tandem repeats of a mouse double homeobox gene: Duxbl. Dev. Dyn. 2010, 239:927-940.
59. Zeng W., de Greef J.C., Chen Y.Y., Chien R., Kong X., Gregson H.C., Winokur S.T., Pyle A., Robertson K.D., Schmiesing J.A., et al. Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet. 2009, 5:e1000559.