DUX4 Activates Germline Genes, Retroelements, and Immune Mediators: Implications for Facioscapulohumeral Dystrophy

Developmental Cell

Volumn 22, Issue 1, 2012, Pages 38-51

  Geng, Linda N ^a   Yao, Zizhen ^a   Snider, Lauren ^a   Fong, Abraham P ^a   Cech, Jennifer N ^a   Young, Janet M ^a   vanderMaarel, Silvere M ^b   Ruzzo, Walter L ^c   Gentleman, Robert C ^d   Tawil, Rabi ^e   Tapscott, Stephen J ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF WASHINGTON   (United States)

^d GENENTECH INC   (United States)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCNA1 PROTEIN; CELL PROTEIN; DUX1 PROTEIN; DUXA PROTEIN; KHDC1 PROTEIN; MBD3L2 PROTEIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; PRAMEF1 PROTEIN; RFPL2 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DUX4; TRIM43 PROTEIN; UNCLASSIFIED DRUG; ZSCAN4 PROTEIN;

ARTICLE; CELL MATURATION; CONTROLLED STUDY; FACIOSCAPULOHUMERAL MUSCULAR DYSTROPHY; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INNATE IMMUNITY; MUSCLE DEVELOPMENT; MYOBLAST; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN MOTIF; SKELETAL MUSCLE; STEM CELL; TRANSCRIPTION INITIATION SITE; UPREGULATION;

APOPTOSIS; BETA-DEFENSINS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GERM CELLS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOENZYME TECHNIQUES; LUCIFERASES; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, FACIOSCAPULOHUMERAL; MYOBLASTS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RETROELEMENTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANSFECTION;

PRIMATES;

EID: 84855956147     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2011.11.013     Document Type: Article

References (59)

1. Belancio V.P., Roy-Engel A.M., Deininger P.L. All y'all need to know 'bout retroelements in cancer. Semin. Cancer Biol. 2010, 20:200-210.
2. Bonnefont J., Nikolaev S.I., Perrier A.L., Guo S., Cartier L., Sorce S., Laforge T., Aubry L., Khaitovich P., Peschanski M., et al. Evolutionary forces shape the human RFPL1,2,3 genes toward a role in neocortex development. Am. J. Hum. Genet. 2008, 83:208-218.
3. Booth H.A., Holland P.W. Annotation, nomenclature and evolution of four novel homeobox genes expressed in the human germ line. Gene 2007, 387:7-14.
4. Bosch N., Cáceres M., Cardone M.F., Carreras A., Ballana E., Rocchi M., Armengol L., Estivill X. Characterization and evolution of the novelgene family FAM90A in primates originated by multiple duplication and rearrangement events. Hum. Mol. Genet. 2007, 16:2572-2582.
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. Candille S.I., Kaelin C.B., Cattanach B.M., Yu B., Thompson D.A., Nix M.A., Kerns J.A., Schmutz S.M., Millhauser G.L., Barsh G.S. A-defensin mutation causes black coat color in domestic dogs. Science 2007, 318:1418-1423.
7. Cao Y., Yao Z., Sarkar D., Lawrence M., Sanchez G.J., Parker M.H., MacQuarrie K.L., Davison J., Morgan M.T., Ruzzo W.L., et al. Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev. Cell 2010, 18:662-674.
8. Chang T.C., Yang Y., Yasue H., Bharti A.K., Retzel E.F., Liu W.S. The expansion of the PRAME gene family in Eutheria. PLoS ONE 2011, 6:e16867.
9. Clapp J., Mitchell L.M., Bolland D.J., Fantes J., Corcoran A.E., Scotting P.J., Armour J.A., Hewitt J.E. Evolutionary conservation ofa coding function for D4Z4, the tandem DNA repeat mutated in facioscapulohumeral muscular dystrophy. Am. J. Hum. Genet. 2007, 81:264-279.
10. 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.
11. 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.
12. Du P., Kibbe W.A., Lin S.M. Lumi: a pipeline for processing Illumina microarray. Bioinformatics 2008, 24:1547-1548.
13. Falcon S., Gentleman R. Using GOstats to test gene lists for GO term association. Bioinformatics 2007, 23:257-258.
14. Feng Z., Dubyak G.R., Lederman M.M., Weinberg A. Cutting edge: human beta defensin 3-a novel antagonist of the HIV-1 coreceptor CXCR4. J.Immunol. 2006, 177:782-786.
15. Frisullo G., Frusciante R., Nociti V., Tasca G., Renna R., Iorio R., Patanella A.K., Iannaccone E., Marti A., Rossi M., et al. CD8(+) Tcells in facioscapulohumeral muscular dystrophy patients with inflammatory features at muscle MRI. J.Clin. Immunol. 2011, 31:155-166.
16. Funderburg N., Lederman M.M., Feng Z., Drage M.G., Jadlowsky J., Harding C.V., Weinberg A., Sieg S.F. Human-defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2. Proc. Natl. Acad. Sci. USA 2007, 104:18631-18635.
17. 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.
18. Gabellini D., D'Antona G., Moggio M., Prelle A., Zecca C., Adami R., Angeletti B., Ciscato P., Pellegrino M.A., Bottinelli R., et al. Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 2006, 439:973-977.
19. 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.
20. Geng L.N., Tyler A.E., Tapscott S.J. Immunodetection of human double homeobox 4. Hybridoma (Larchmt) 2011, 30:125-130.
21. Griffin C.A., Apponi L.H., Long K.K., Pavlath G.K. Chemokine expression and control of muscle cell migration during myogenesis. J.Cell Sci. 2010, 123:3052-3060.
22. Holland P.W., Booth H.A., Bruford E.A. Classification and nomenclature of all human homeobox genes. BMC Biol. 2007, 5:47.
23. Jiang C.L., Jin S.G., Lee D.H., Lan Z.J., Xu X., O'Connor T.R., Szabó P.E., Mann J.R., Cooney A.J., Pfeifer G.P. MBD3L1 and MBD3L2, two new proteins homologous to the methyl-CpG-binding proteins MBD2 and MBD3: characterization of MBD3L1 as a testis-specific transcriptional repressor. Genomics 2002, 80:621-629.
24. Jin G., Kawsar H.I., Hirsch S.A., Zeng C., Jia X., Feng Z., Ghosh S.K., Zheng Q.Y., Zhou A., McIntyre T.M., Weinberg A. An antimicrobial peptide regulates tumor-associated macrophage trafficking via the chemokine receptor CCR2, a model for tumorigenesis. PLoS ONE 2010, 5:e10993.
25. Jin S.G., Tsark W., Szabó P.E., Pfeifer G.P. Haploid male germ cell- and oocyte-specific Mbd3l1 and Mbd3l2 genes are dispensable for early development, fertility, and zygotic DNA demethylation in the mouse. Dev. Dyn. 2008, 237:3435-3443.
26. Kawamura-Saito M., Yamazaki Y., Kaneko K., Kawaguchi N., Kanda H., Mukai H., Gotoh T., Motoi T., Fukayama M., Aburatani H., et al. Fusion between CIC and DUX4 up-regulates PEA3 family genes in Ewing-like sarcomas with t(4;19)(q35;q13) translocation. Hum. Mol. Genet. 2006, 15:2125-2137.
27. Klooster R., Straasheijm K., Shah B., Sowden J., Frants R., Thornton C., Tawil R., van der Maarel S. Comprehensive expression analysis of FSHD candidate genes at the mRNA and protein level. Eur. J. Hum. Genet. 2009, 17:1615-1624.
28. 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.
29. Lai Y., Gallo R.L. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 2009, 30:131-141.
30. Laoudj-Chenivesse D., Carnac G., Bisbal C., Hugon G., Bouillot S., Desnuelle C., Vassetzky Y., Fernandez A. Increased levels of adenine nucleotide translocator 1 protein and response to oxidative stress are early events in facioscapulohumeral muscular dystrophy muscle. J.Mol. Med. 2005, 83:216-224.
31. 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.
32. Lokireddy S., McFarlane C., Ge X., Zhang H., Sze S.K., Sharma M., Kambadur R. Myostatin induces degradation of sarcomeric proteins through a Smad3 signaling mechanism during skeletal muscle wasting. Mol. Endocrinol. 2011, 25:1936-1949.
33. Lyle R., Wright T.J., Clark L.N., Hewitt J.E. The FSHD-associated repeat, D4Z4, is a member of a dispersed family of homeobox-containing repeats, subsets of which are clustered on the short arms of the acrocentric chromosomes. Genomics 1995, 28:389-397.
34. Melchionna R., Di Carlo A., De Mori R., Cappuzzello C., Barberi L., Musarò A., Cencioni C., Fujii N., Tamamura H., Crescenzi M., et al. Induction of myogenic differentiation by SDF-1 via CXCR4 and CXCR7 receptors. Muscle Nerve 2010, 41:828-835.
35. Midorikawa K., Ouhara K., Komatsuzawa H., Kawai T., Yamada S., Fujiwara T., Yamazaki K., Sayama K., Taubman M.A., Kurihara H., et al. Staphylococcus aureus susceptibility to innate antimicrobial peptides, beta-defensins and CAP18, expressed by human keratinocytes. Infect. Immun. 2003, 71:3730-3739.
36. Molnár M., Diószeghy P., Mechler F. Inflammatory changes in facioscapulohumeral muscular dystrophy. Eur. Arch. Psychiatry Clin. Neurosci. 1991, 241:105-108.
37. Palii C.G., Perez-Iratxeta C., Yao Z., Cao Y., Dai F., Davison J., Atkins H., Allan D., Dilworth F.J., Gentleman R., et al. Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. EMBO J. 2011, 30:494-509.
38. Pierre A., Gautier M., Callebaut I., Bontoux M., Jeanpierre E., Pontarotti P., Monget P. Atypical structure and phylogenomic evolution of the new eutherian oocyte- and embryo-expressed KHDC1/DPPA5/ECAT1/OOEP gene family. Genomics 2007, 90:583-594.
39. Reed P.W., Corse A.M., Porter N.C., Flanigan K.M., Bloch R.J. Abnormal expression of mu-crystallin in facioscapulohumeral muscular dystrophy. Exp. Neurol. 2007, 205:583-586.
40. Sass V., Schneider T., Wilmes M., Körner C., Tossi A., Novikova N., Shamova O., Sahl H.G. Human beta-defensin 3 inhibits cell wall biosynthesis in Staphylococci. Infect. Immun. 2010, 78:2793-2800.
41. Schulz W.A. L1 retrotransposons in human cancers. J.Biomed. Biotechnol. 2006, 2006:83672.
42. Semple F., Webb S., Li H.N., Patel H.B., Perretti M., Jackson I.J., Gray M., Davidson D.J., Dorin J.R. Human beta-defensin 3 has immunosuppressive activity invitro and invivo. Eur. J. Immunol. 2010, 40:1073-1078.
43. Semple F., Macpherson H., Webb S., Cox S.L., Mallin L.J., Tyrrell C., Grimes G.R., Semple C.A., Nix M.A., Millhauser G.L., et al. Human beta-defensin 3 affects the activity of pro-inflammatory pathways associated with MyD88 and TRIF. Eur. J. Immunol. 2011, 41:3291-3300.
44. Simpson A.J., Caballero O.L., Jungbluth A., Chen Y.T., Old L.J. Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 2005, 5:615-625.
45. Smit A.F. Identification of a new, abundant superfamily of mammalian LTR-transposons. Nucleic Acids Res. 1993, 21:1863-1872.
46. 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.
47. Stanghellini I., Falco G., Lee S.L., Monti M., Ko M.S. Trim43a, Trim43b, and Trim43c: Novel mouse genes expressed specifically in mouse preimplantation embryos. Gene Expr. Patterns 2009, 9:595-602.
48. Tupler R., Berardinelli A., Barbierato L., Frants R., Hewitt J.E., Lanzi G., Maraschio P., Tiepolo L. Monosomy of distal 4q does not cause facioscapulohumeral muscular dystrophy. J.Med. Genet. 1996, 33:366-370.
49. 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.
50. Vanderplanck C., Ansseau E., Charron S., Stricwant N., Tassin A., Laoudj-Chenivesse D., Wilton S.D., Coppée F., Belayew A. The FSHD atrophic myotube phenotype is caused by DUX4 expression. PLoS ONE 2011, 6:e26820.
51. 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.
52. Wettenhall J.M., Smyth G.K. limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics 2004, 20:3705-3706.
53. 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.
54. 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.
55. Wuebbles R.D., Long S.W., Hanel M.L., Jones P.L. Testing the effects of FSHD candidate gene expression in vertebrate muscle development. Int. J. Clin. Exp. Pathol. 2010, 3:386-400.
56. Yamaguchi Y., Nagase T., Tomita T., Nakamura K., Fukuhara S., Amano T., Yamamoto H., Ide Y., Suzuki M., Teramoto S., et al. Beta-defensin overexpression induces progressive muscle degeneration in mice. Am. J. Physiol. Cell Physiol. 2007, 292:C2141-C2149.
57. Yang D., Chertov O., Bykovskaia S.N., Chen Q., Buffo M.J., Shogan J., Anderson M., Schröder J.M., Wang J.M., Howard O.M., Oppenheim J.J. Beta-defensins: linking innate and adaptive immunity through dendritic and Tcell CCR6. Science 1999, 286:525-528.
58. Zalzman M., Falco G., Sharova L.V., Nishiyama A., Thomas M., Lee S.L., Stagg C.A., Hoang H.G., Yang H.T., Indig F.E., et al. Zscan4 regulates telomere elongation and genomic stability in ES cells. Nature 2010, 464:858-863.
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.