Epigenetic regulation of Tbx18 gene expression during endochondral bone formation

Cell and Tissue Research

Volumn 359, Issue 2, 2015, Pages 503-512

  Haraguchi, Ryuma ^a   Kitazawa, Riko ^a   Kitazawa, Sohei ^a  

^a EHIME UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

DNA methylation; Endochondral bone formation; Epigenetic; Gene expression analysis; Mouse; TBX18

Indexed keywords

TBX18 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; RUNX2 PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; TBX18 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CARTILAGE CELL; CELL DIFFERENTIATION; COL2A1 GENE; CPG ISLAND; DNA METHYLATION; EMBRYO; ENCHONDRAL OSSIFICATION; EPIGENETICS; EPIPHYSIS; GENE; GENE EXPRESSION; LIMB BUD; LIMB DEVELOPMENT; MARKER GENE; MESENCHYME CELL; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; PROMOTER REGION; RUNX2 GENE; SOX9 GENE; TBX18 GENE; TISSUE DISTRIBUTION; TRABECULAR BONE; ANIMAL; BIOLOGICAL MODEL; BONE DEVELOPMENT; CHONDROGENESIS; EMBRYO DEVELOPMENT; EMBRYOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; LIMB; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; TIME;

ANIMALS; BASE SEQUENCE; CHONDROGENESIS; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DNA METHYLATION; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; EXTREMITIES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OSTEOGENESIS; SOX9 TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEINS; TIME FACTORS;

EID: 84925534615     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-2028-0     Document Type: Article

References (49)

1. Airik R, Trowe MO, Foik A, Farin HF, Petry M, Schuster-Gossler K, Schweizer M, Scherer G, Kist R, Kispert A (2010) Hydroureternephrosis due to loss of Sox9-regulated smooth muscle cell differentiation of the ureteric mesenchyme. Hum Mol Genet 19:4918–4929
2. Akiyama H, Chaboissier MC, Martin JF, Schedl A, Crombrugghe B de (2002) The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6. Genes Dev 16:2813–2828
3. Akiyama H, Kim JE, Nakashima K, Balmes G, Iwai N, Deng JM, Zhang Z, Martin JF, Behringer RR, Nakamura T, Crombrugghe B de (2005) Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci U S A 102:14665–14670
4. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS (1997) SOX9 directly regulates the type-II collagen gene. Nat Genet 16:174–178
5. Bridgewater LC, Lefebvre V, Crombrugghe B de (1998) Chondrocyte-specific enhancer elements in the Col11a2 gene resemble the Col2a1 tissue-specific enhancer. J Biol Chem 273:14998–15006
6. Brummelkamp TR, Kortlever RM, Lingbeek M, Trettel F, MacDonald ME, van Lohuizen M, Bernards R (2002) TBX-3, the gene mutated in Ulnar-Mammary syndrome, is a negative regulator of p19ARF and inhibits senescence. J Biol Chem 277:6567–6572
7. Bussen M, Petry M, Schuster-Gossler K, Leitges M, Gossler A, Kispert A (2004) The T-box transcription factor Tbx18 maintains the separation of anterior and posterior somite compartments. Genes Dev 18:1209–1221
8. Cai CL, Martin JC, Sun Y, Cui L, Wang L, Ouyang K, Yang L, Bu L, Liang X, Zhang X, Stallcup WB, Denton CP, McCulloch A, Chen J, Evans SM (2008) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454:104–108
9. Cheung JO, Hillarby MC, Ayad S, Hoyland JA, Jones CJ, Denton J, Thomas JT, Wallis GA, Grant ME (2001) A novel cell culture model of chondrocyte differentiation during mammalian endochondral ossification. J Bone Miner Res 16:309–318
10. Christoffels VM, Grieskamp T, Norden J, Mommersteeg MT, Rudat C, Kispert A (2009) Tbx18 and the fate of epicardial progenitors. Nature 458:E8–E9
11. Clavel C, Grisanti L, Zemla R, Rezza A, Barros R, Sennett R, Mazloom AR, Chung CY, Cai X, Cai CL, Pevny L, Nicolis S, Máayan A, Rendl M (2012) Sox2 in the dermal papilla niche controls hair growth by fine-tuning BMP signaling in differentiating hair shaft progenitors. Dev Cell 23:981–994
12. Darwanto A, Kitazawa R, Mori K, Kondo T, Kitazawa S (2008) MeCP2 expression and promoter methylation of cyclin D1 gene are associated with cyclin D1 expression in developing rat epididymal duct. Acta Histochem Cytochem 41:135–142
13. Dias RR, Albuquerque JM, Pereira AC, Stolf NA, Krieger JE, Mady C, Oliveira SA (2007) Holt-Oram syndrome presenting as agenesis of the left pericardium. Int J Cardiol 114:98–100
14. Erlebacher A, Filvaroff EH, Gitelman SE, Derynck R (1995) Toward a molecular understanding of skeletal development. Cell 80:371–378
15. Farin HF, Bussen M, Schmidt MK, Singh MK, Schuster-Gossler K, Kispert A (2007) Transcriptional repression by the T-box proteins Tbx18 and Tbx15 depends on Groucho corepressors. J Biol Chem 282:25748–25759
16. Farin HF, Mansouri A, Petry M, Kispert A (2008) T-box protein Tbx18 interacts with the paired box protein Pax3 in the development of the paraxial mesoderm. J Biol Chem 283:25372–25380
17. Ghoshal K, Motiwala T, Claus R, Yan P, Kutay H, Datta J, Majumder S, Bai S, Majumder A, Huang T, Plass C, Jacob ST (2010) HOXB13, a target of DNMT3B, is methylated at an upstream CpG island, and functions as a tumor suppressor in primary colorectal tumors. PLoS One 5:e10338
18. Haraguchi R, Matsumaru D, Nakagata N, Miyagawa S, Suzuki K, Kitazawa S, Yamada G (2012) The hedgehog signal induced modulation of bone morphogenetic protein signaling: an essential signaling relay for urinary tract morphogenesis. PLoS One 7:e42245
19. Hojo H, Ohba S, Yano F, Saito T, Ikeda T, Nakajima K, Komiyama Y, Nakagata N, Suzuki K, Takato T, Kawaguchi H, Chung UI (2012) Gli1 protein participates in Hedgehog-mediated specification of osteoblast lineage during endochondral ossification. J Biol Chem 287:17860–17869
20. Johnson RL, Tabin CJ (1997) Molecular models for vertebrate limb development. Cell 90:979–990
21. Kapoor N, Galang G, Marban E, Cho HC (2011) Transcriptional suppression of connexin43 by TBX18 undermines cell-cell electrical coupling in postnatal cardiomyocytes. J Biol Chem 286:14073–14079
22. Karsenty G, Wagner EF (2002) Reaching a genetic and molecular understanding of skeletal development. Dev Cell 2:389–406
23. Kitazawa R, Kitazawa S (2007) Methylation status of a single CpG locus 3 bases upstream of TATA-box of receptor activator of nuclear factor-kappaB ligand (RANKL) gene promoter modulates cell- and tissue-specific RANKL expression and osteoclastogenesis. Mol Endocrinol 21:148–158
24. Kraus F, Haenig B, Kispert A (2001) Cloning and expression analysis of the mouse T-box gene Tbx18. Mech Dev 100:83–86
25. Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423:332–336
26. Lefebvre V, Huang W, Harley VR, Goodfellow PN, Crombrugghe B de (1997) SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol Cell Biol 17:2336–2346
27. Li E, Bestor TH, Jaenisch R (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69:915–926
28. Naiche LA, Harrelson Z, Kelly RG, Papaioannou VE (2005) T-box genes in vertebrate development. Annu Rev Genet 39:219–239
29. Nakagawa M, Kitazawa R, Kuwahara N, Yoshida K, Haraguchi R, Kitazawa S (2013) Efficient genetic analysis of microdissected samples by agarose-bead method: alterations of beta-catenin gene in fundic gland polyp and heterotopic gastric mucosa of duodenum. Acta Histochem Cytochem 46:19–24
30. Ng LJ, Wheatley S, Muscat GE, Conway-Campbell J, Bowles J, Wright E, Bell DM, Tam PP, Cheah KS, Koopman P (1997) SOX9 binds DNA, activates transcription, and coexpresses with type II collagen during chondrogenesis in the mouse. Dev Biol 183:108–121
31. Nilsson O, Mitchum RD Jr, Schrier L, Ferns SP, Barnes KM, Troendle JF, Baron J (2005) Growth plate senescence is associated with loss of DNA methylation. J Endocrinol 186:241–249
32. Nishino K, Hattori N, Tanaka S, Shiota K (2004) DNA methylation-mediated control of Sry gene expression in mouse gonadal development. J Biol Chem 279:22306–22313
33. Okano M, Bell DW, Haber DA, Li E (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257
34. Olsen BR, Reginato AM, Wang W (2000) Bone development. Annu Rev Cell Dev Biol 16:191–220
35. Schmahl W, Torok P, Kriegel H (1984) Embryotoxicity of 5-azacytidine in mice. Phase- and dose-specificity studies. Arch Toxicol 55:143–147
36. Soeda T, Deng JM, Crombrugghe B de, Behringer RR, Nakamura T, Akiyama H (2010) Sox9-expressing precursors are the cellular origin of the cruciate ligament of the knee joint and the limb tendons. Genesis 48:635–644
37. Song MR, Shirasaki R, Cai CL, Ruiz EC, Evans SM, Lee SK, Pfaff SL (2006) T-box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development 133:4945–4955
38. Sugimoto Y, Takimoto A, Akiyama H, Kist R, Scherer G, Nakamura T, Hiraki Y, Shukunami C (2013) Scx+/Sox9+ progenitors contribute to the establishment of the junction between cartilage and tendon/ligament. Development 140:2280–2288
39. Takeichi M, Nimura K, Mori M, Nakagami H, Kaneda Y (2013) The transcription factors Tbx18 and Wt1 control the epicardial epithelial-mesenchymal transition through bi-directional regulation of Slug in murine primary epicardial cells. PLoS One 8:e57829
40. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, Yanagisawa M, Fujita N, Nakao M, Taga T (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1:749–758
41. Trowe MO, Shah S, Petry M, Airik R, Schuster-Gossler K, Kist R, Kispert A (2010) Loss of Sox9 in the periotic mesenchyme affects mesenchymal expansion and differentiation, and epithelial morphogenesis during cochlea development in the mouse. Dev Biol 342:51–62
42. Vlahovic M, Bulic-Jakus F, Juric-Lekic G, Fucic A, Maric S, Serman D (1999) Changes in the placenta and in the rat embryo caused by the demethylating agent 5-azacytidine. Int J Dev Biol 43:843–846
43. Walsh CP, Bestor TH (1999) Cytosine methylation and mammalian development. Genes Dev 13:26–34
44. Wang Y, Tripathi P, Guo Q, Coussens M, Ma L, Chen F (2009) Cre/lox recombination in the lower urinary tract. Genesis 47:409–413
45. Xiao Z, Zhang S, Mahlios J, Zhou G, Magenheimer BS, Guo D, Dallas SL, Maser R, Calvet JP, Bonewald L, Quarles LD (2006) Cilia-like structures and polycystin-1 in osteoblasts/osteocytes and associated abnormalities in skeletogenesis and Runx2 expression. J Biol Chem 281:30884–30895
46. Yokonishi T, Sato T, Katagiri K, Komeya M, Kubota Y, Ogawa T (2013) In vitro reconstruction of mouse seminiferous tubules supporting germ cell differentiation. Biol Reprod (in press)
47. Zeng B, Ren XF, Cao F, Zhou XY, Zhang J (2011) Developmental patterns and characteristics of epicardial cell markers Tbx18 and Wt1 in murine embryonic heart. J Biomed Sci 18:67
48. Zhao Q, Eberspaecher H, Lefebvre V, Crombrugghe B de (1997) Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev Dyn 209:377–386
49. Zhou G, Zheng Q, Engin F, Munivez E, Chen Y, Sebald E, Krakow D, Lee B (2006) Dominance of SOX9 function over RUNX2 during skeletogenesis. Proc Natl Acad Sci U S A 103:19004–19009