Prdm5 Regulates Collagen Gene Transcription by Association with RNA Polymerase II in Developing Bone

English version České info

PRDM family members are transcriptional regulators involved in tissue specific differentiation. PRDM5 has been reported to predominantly repress transcription, but a characterization of its molecular functions in a relevant biological context is lacking. We demonstrate here that Prdm5 is highly expressed in developing bones; and, by genome-wide mapping of Prdm5 occupancy in pre-osteoblastic cells, we uncover a novel and unique role for Prdm5 in targeting all mouse collagen genes as well as several SLRP proteoglycan genes. In particular, we show that Prdm5 controls both Collagen I transcription and fibrillogenesis by binding inside the Col1a1 gene body and maintaining RNA polymerase II occupancy. In vivo, Prdm5 loss results in delayed ossification involving a pronounced impairment in the assembly of fibrillar collagens. Collectively, our results define a novel role for Prdm5 in sustaining the transcriptional program necessary to the proper assembly of osteoblastic extracellular matrix.

Vyšlo v časopise: Prdm5 Regulates Collagen Gene Transcription by Association with RNA Polymerase II in Developing Bone. PLoS Genet 8(5): e32767. doi:10.1371/journal.pgen.1002711
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002711

Souhrn

Zdroje

1. FogCKGalliGGLundAH 2011 PRDM proteins: Important players in differentiation and disease. Bioessays

2. TurnerCAJrMackDHDavisMM 1994 Blimp-1, a novel zinc finger-containing protein that can drive the maturation of B lymphocytes into immunoglobulin-secreting cells. Cell 77 297 306

3. SealePBjorkBYangWKajimuraSChinS 2008 PRDM16 controls a brown fat/skeletal muscle switch. Nature 454 961 967

4. DuanZPersonRELeeHHHuangSDonadieuJ 2007 Epigenetic regulation of protein-coding and microRNA genes by the Gfi1-interacting tumor suppressor PRDM5. Mol Cell Biol 27 6889 6902

5. DengQHuangS 2004 PRDM5 is silenced in human cancers and has growth suppressive activities. Oncogene 23 4903 4910

6. WatanabeYKimHSCastoroRJChungWEstecioMR 2009 Sensitive and specific detection of early gastric cancer with DNA methylation analysis of gastric washes. Gastroenterology 136 2149 2158

7. WatanabeYToyotaMKondoYSuzukiHImaiT 2007 PRDM5 identified as a target of epigenetic silencing in colorectal and gastric cancer. Clin Cancer Res 13 4786 4794

8. MeaniNPezzimentiFDeflorianGMioneMAlcalayM 2009 The tumor suppressor PRDM5 regulates Wnt signaling at early stages of zebrafish development. PLoS ONE 4 e4273 doi:10.1371/journal.pone.0004273

9. Burkitt WrightEMSpencerHLDalySBMansonFDZeefLA 2011 Mutations in PRDM5 in brittle cornea syndrome identify a pathway regulating extracellular matrix development and maintenance. Am J Hum Genet 88 767 777

10. TichoUIvryMMerinS 1980 Brittle cornea, blue sclera, and red hair syndrome (the brittle cornea syndrome). Br J Ophthalmol 64 175 177

11. SchenkRKHofstetterWFelixR 2003 Morphology and Chemical Composition of Connective Tissue: Bone Connective Tissue and Its Heritable Disorders John Wiley & Sons, Inc 67

12. OlsenBRReginatoAMWangW 2000 Bone development. Annu Rev Cell Dev Biol 16 191 220

13. VuorioEde CrombruggheB 1990 The family of collagen genes. Annu Rev Biochem 59 837 872

14. CantyEGKadlerKE 2005 Procollagen trafficking, processing and fibrillogenesis. J Cell Sci 118 1341 1353

15. KalamajskiSOldbergA 2010 The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol 29 248 253

16. DanielsonKGBaribaultHHolmesDFGrahamHKadlerKE 1997 Targeted disruption of decorin leads to abnormal collagen fibril morphology and skin fragility. J Cell Biol 136 729 743

17. de CrombruggheBVuorioTKarsentyGMaitySRutheshouserEC 1991 Transcriptional control mechanisms for the expression of type I collagen genes. Ann Rheum Dis 50 Suppl 4 872 876

18. KarsentyGParkRW 1995 Regulation of type I collagen genes expression. Int Rev Immunol 12 177 185

19. InagakiYTruterSRamirezF 1994 Transforming growth factor-beta stimulates alpha 2(I) collagen gene expression through a cis-acting element that contains an Sp1-binding site. J Biol Chem 269 14828 14834

20. GreenwelPTanakaSPenkovDZhangWOliveM 2000 Tumor necrosis factor alpha inhibits type I collagen synthesis through repressive CCAAT/enhancer-binding proteins. Mol Cell Biol 20 912 918

21. BozecABakiriLJimenezMSchinkeTAmlingM 2010 Fra-2/AP-1 controls bone formation by regulating osteoblast differentiation and collagen production. J Cell Biol 190 1093 1106

22. KomoriTYagiHNomuraSYamaguchiASasakiK 1997 Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89 755 764

23. KomoriT 2010 Regulation of bone development and extracellular matrix protein genes by RUNX2. Cell Tissue Res 339 189 195

24. KinameriEInoueTArugaJImayoshiIKageyamaR 2008 Prdm proto-oncogene transcription factor family expression and interaction with the Notch-Hes pathway in mouse neurogenesis. PLoS ONE 3 e3859 doi:10.1371/journal.pone.0003859

25. YamajiMSekiYKurimotoKYabutaYYuasaM 2008 Critical function of Prdm14 for the establishment of the germ cell lineage in mice. Nat Genet 40 1016 1022

26. ChiaNYChanYSFengBLuXOrlovYL 2010 A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature 468 316 320

27. BaudatFBuardJGreyCFledel-AlonAOberC 2010 PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327 836 840

28. FumasoniIMeaniNRambaldiDScafettaGAlcalayM 2007 Family expansion and gene rearrangements contributed to the functional specialization of PRDM genes in vertebrates. BMC Evol Biol 7 187

29. MaesCKobayashiTSeligMKTorrekensSRothSI 2011 Osteoblast precursors, but not mature osteoblasts, move into developing and fractured bones along with invading blood vessels. Dev Cell 19 329 344

30. RamirezFDi LibertoM 1990 Complex and diversified regulatory programs control the expression of vertebrate collagen genes. Faseb J 4 1616 1623

31. AntonivTTTanakaSSudanBDe ValSLiuK 2005 Identification of a repressor in the first intron of the human alpha2(I) collagen gene (COL1A2). J Biol Chem 280 35417 35423

32. TanakaSRamirezF 2007 The first intron of the human alpha2(I) collagen gene (COL1A2) contains a novel interferon-gamma responsive element. Matrix Biol 26 185 189

33. ReedR 2003 Coupling transcription, splicing and mRNA export. Curr Opin Cell Biol 15 326 331

34. KeeneDRSan AntonioJDMayneRMcQuillanDJSarrisG 2000 Decorin binds near the C terminus of type I collagen. J Biol Chem 275 21801 21804

35. CorsiAXuTChenXDBoydeALiangJ 2002 Phenotypic effects of biglycan deficiency are linked to collagen fibril abnormalities, are synergized by decorin deficiency, and mimic Ehlers-Danlos-like changes in bone and other connective tissues. J Bone Miner Res 17 1180 1189

36. Al-HussainHZeisbergerSMHuberPRGiuntaCSteinmannB 2004 Brittle cornea syndrome and its delineation from the kyphoscoliotic type of Ehlers-Danlos syndrome (EDS VI): report on 23 patients and review of the literature. Am J Med Genet A 124A 28 34

37. JunqueiraLCBignolasGBrentaniRR 1979 Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11 447 455

38. WuellingMKaiserFJBuelensLABraunholzDShivdasaniRA 2009 Trps1, a regulator of chondrocyte proliferation and differentiation, interacts with the activator form of Gli3. Dev Biol 328 40 53

39. Gailus-DurnerVFuchsHAdlerTAguilar PimentelABeckerL 2009 Systemic first-line phenotyping. Methods Mol Biol 530 463 509