Looping mediated interaction between the promoter and 3′ UTR regulates type II collagen expression in Chondrocytes

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Jash, Arijita ^a   Yun, Kangsun ^a,b   Sahoo, Anupama ^a,c   So, Jae Seon ^a,d   Im, Sin Hyeog ^a  

^a Gwangju Institute of Science and Technology (GIST)   (South Korea)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; COLLAGEN TYPE 2; LYMPHOID ENHANCER FACTOR 1;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BIOINFORMATICS; CARTILAGE CELL; CELL DEDIFFERENTIATION; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; COL2A1 GENE; DOWN REGULATION; GENE; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE LOCUS; GENE LOOPING; GENE SILENCING; GENETIC PARAMETERS; GENETIC TRANSCRIPTION; GENOME; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PROMOTER REGION; UPREGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; CELL DEDIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; CHROMATIN; COLLAGEN TYPE II; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; GENETIC LOCI; HUMANS; LYMPHOID ENHANCER-BINDING FACTOR 1; MICE; MICE, INBRED ICR; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84864023859     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040828     Document Type: Article

References (66)

1. Drissi H, Zuscik M, Rosier R, O'Keefe R, (2005) Transcriptional regulation of chondrocyte maturation: potential involvement of transcription factors in OA pathogenesis. Mol Aspects Med 26: 169-179.
2. Furumatsu T, Ozaki T, (2010) Epigenetic Regulation in Chondrogenesis. Acta medica Okayama 64: 155-161.
3. Ahmad NN, Ala-Kokko L, Knowlton RG, Jimenez SA, Weaver EJ, et al. (1991) Stop codon in the procollagen II gene (COL2A1) in a family with the Stickler syndrome (arthro-ophthalmopathy). Proc Natl Acad Sci U S A 88: 6624-6627.
4. Bogaert R, Wilkin D, Wilcox WR, Lachman R, Rimoin D, et al. (1994) Expression, in cartilage, of a 7-amino-acid deletion in type II collagen from two unrelated individuals with Kniest dysplasia. Am J Hum Genet 55: 1128-1136.
5. Tiller GE, Weis MA, Polumbo PA, Gruber HE, Rimoin DL, et al. (1995) An RNA-splicing mutation (G+5IVS20) in the type II collagen gene (COL2A1) in a family with spondyloepiphyseal dysplasia congenita. Am J Hum Genet 56: 388-395.
6. Vissing H, D'Alessio M, Lee B, Ramirez F, Godfrey M, et al. (1989) Glycine to serine substitution in the triple helical domain of pro-alpha 1 (II) collagen results in a lethal perinatal form of short-limbed dwarfism. J Biol Chem 264: 18265-18267.
7. Stokes DG, Liu G, Dharmavaram R, Hawkins D, Piera-Velazquez S, et al. (2001) Regulation of type-II collagen gene expression during human chondrocyte de-differentiation and recovery of chondrocyte-specific phenotype in culture involves Sry-type high-mobility-group box (SOX) transcription factors. Biochem J 360: 461-470.
8. de Crombrugghe B, Lefebvre V, Behringer RR, Bi W, Murakami S, et al. (2000) Transcriptional mechanisms of chondrocyte differentiation. Matrix Biology 19: 389-394.
9. Hollander AP, Pidoux I, Reiner A, Rorabeck C, Bourne R, et al. (1995) Damage to type II collagen in aging and osteoarthritis starts at the articular surface, originates around chondrocytes, and extends into the cartilage with progressive degeneration. J Clin Invest 96: 2859-2869.
10. von der Mark K, Gauss V, von der Mark H, Muller P, (1977) Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature 267: 531-532.
11. Ryan MC, Sieraski M, Sandell LJ, (1990) The human type II procollagen gene: identification of an additional protein-coding domain and location of potential regulatory sequences in the promoter and first intron. Genomics 8: 41-48.
12. Levy S, Hannenhalli S, Workman C, (2001) Enrichment of regulatory signals in conserved non-coding genomic sequence. Bioinformatics 17: 871-877.
13. Carey M, (1998) The Enhanceosome and Minireview Transcriptional Synergy. Cell 92: 5-8.
14. Fishburn J, Mohibullah N, Hahn S, (2005) Function of a eukaryotic transcription activator during the transcription cycle. Mol Cell 18: 369-378.
15. Woychik NA, Hampsey M, (2002) The RNA Polymerase II Machinery:: Structure Illuminates Function. Cell 108: 453-463.
16. Murrell A, Heeson S, Reik W, (2004) Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet 36: 889-893.
17. Lee CG KK, So JS, Kwon HK, Son JS, Song MK, Sahoo A, Yi HJ, Hwang KC, Matsuyama T, Yui K, Im SH, (2009) A distal cis-regulatory element, CNS-9, controls NFAT1 and IRF4-mediated IL-10 gene activation in T helper cells. Mol Immunol 46: 613-621.
18. Tsytsykova AV, Rajsbaum R, Falvo JV, Ligeiro F, Neely SR, et al. (2007) Activation-dependent intrachromosomal interactions formed by the TNF gene promoter and two distal enhancers. Proc Natl Acad Sci U S A 104: 16850-16855.
19. Jones EA, Flavell RA, (2005) Distal enhancer elements transcribe intergenic RNA in the IL-10 family gene cluster. J Immunol 175: 7437-7446.
20. Bell DM, Leung KKH, Wheatley SC, Ng LJ, Zhou S, et al. (1997) SOX9 directly regulates the type-ll collagen gene. Nat Genet 16: 174-178.
21. Ghayor C, Herrouin JF, Chadjichristos C, Ala-Kokko L, Takigawa M, et al. (2000) Regulation of human COL2A1 gene expression in chondrocytes. J Biol Chem 275: 27421-27438.
22. Krebsbach PH, Nakata K, Bernier SM, Hatano O, Miyashita T, et al. (1996) Identification of a minimum enhancer sequence for the type II collagen gene reveals several core sequence motifs in common with the link protein gene. J Biol Chem 271: 4298-4303.
23. Osaki M, Tan L, Choy BK, Yoshida Y, Cheah KSE, et al. (2003) The TATA-containing core promoter of the type II collagen gene (COL2A1) is the target of interferon-gamma-mediated inhibition in human chondrocytes: requirement for Stat1 alpha, Jak1 and Jak2. Biochem J 369: 103-115.
24. Mayor C, Brudno M, Schwartz JR, Poliakov A, Rubin EM, et al. (2000) VISTA: visualizing global DNA sequence alignments of arbitrary length. Bioinformatics 16: 1046-1047.
25. Savagner P, Krebsbach PH, Hatano O, Miyashita T, Liebman J, et al. (1995) Collagen II promoter and enhancer interact synergistically through Sp1 and distinct nuclear factors. DNA Cell Biol 14: 501-510.
26. Kahler RA, Westendorf JJ, (2003) Lymphoid enhancer factor-1 and b-catenin inhibit Runx2-dependent transcriptional activation of the osteocalcin promoter. J Biol Chem 278: 11937-11944.
27. Giese K, Cox J, Grosschedl R, (1992) The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 69: 185-195.
28. Kadauke S, Blobel GA, (2009) Chromatin loops in gene regulation. Biochim Biophys Acta 1789: 17-25.
29. O'Sullivan JM, Tan-Wong SM, Morillon A, Lee B, Coles J, et al. (2004) Gene loops juxtapose promoters and terminators in yeast. Nat Genet 36: 1014-1018.
30. Yun K, So JS, Jash A, Im SH, (2009) Lymphoid Enhancer Binding Factor 1 Regulates Transcription through Gene Looping. J Immunol 183: 5129-5137.
31. von der Mark K, Gauss V, von der Mark H, Müller P, (1977) Relationship between cell shape and type of collagen synthesised as chondrocytes lose their cartilage phenotype in culture. Nature 267: 531-532.
32. MacDonald BT, Tamai K, He X, (2009) Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 17: 9-26.
33. Waterman ML, Fischer WH, Jones KA, (1991) A thymus-specific member of the HMG protein family regulates the human T cell receptor C alpha enhancer. Genes Dev 5: 656-669.
34. Columbus J Examination of Expression and Function of TCF Genes in the Pancreatic Islets: University of Toronto.
35. Zhu M, Chen M, Zuscik M, Wu Q, Wang YJ, et al. (2008) Inhibition of-catenin signaling in articular chondrocytes results in articular cartilage destruction. Arthritis Rheum 58: 2053-2064.
36. Inada M, Yasui T, Nomura S, Miyake S, Deguchi K, et al. (1999) Maturational disturbance of chondrocytes in Cbfa1 deficient mice. Dev Dyn 214: 279-290.
37. Tamamura Y, Otani T, Kanatani N, Koyama E, Kitagaki J, et al. (2005) Developmental regulation of Wnt/beta-catenin signals is required for growth plate assembly, cartilage integrity, and endochondral ossification. J Biol Chem 280: 19185-19195.
38. Glass Ii DA, Bialek P, Ahn JD, Starbuck M, Patel MS, et al. (2005) Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 8: 751-764.
39. Maruyama Z, Yoshida CA, Furuichi T, Amizuka N, Ito M, et al. (2007) Runx2 determines bone maturity and turnover rate in postnatal bone development and is involved in bone loss in estrogen deficiency. Dev Dyn 236: 1876-1890.
40. Hartmann C, Tabin CJ, (2000) Dual roles of Wnt signaling during chondrogenesis in the chicken limb. Development 127: 3141-3159.
41. Yano F, Kugimiya F, Ohba S, Ikeda T, Chikuda H, et al. (2005) The canonical Wnt signaling pathway promotes chondrocyte differentiation in a Sox9-dependent manner. Biochem Biophys Res Commun 333: 1300-1308.
42. Yun K, Choi YD, Nam JH, Park Z, Im SH, (2007) NF-[kappa] B regulates Lef1 gene expression in chondrocytes. Biochem Biophys Res Commun 357: 589-595.
43. Yun K, Im SH, (2007) Lef1 regulates COX-2 transcription in chondrocytes. Biochem Biophys Res Commun 364: 270-275.
44. Yun K, Im SH, (2007) Transcriptional regulation of MMP13 by Lef1 in chondrocytes. Biochem Biophys Res Commun 364: 1009-1014.
45. Ning B, Wang P, Pei X, Kang Y, Song J, et al. (2012) Dual function of β-catenin in articular cartilage growth and degeneration at different stages of postnatal cartilage development. Int Orthop 655-654.
46. Chen M, Zhu M, Awad H, Li TF, Sheu TJ, et al. (2008) Inhibition of beta-catenin signaling causes defects in postnatal cartilage development. J Cell Sci 121: 1455-1465.
47. Huang Y, Zhang X, Du K, Yang F, Shi Y, et al. (2012) Inhibition of β-catenin signaling in chondrocytes induces delayed fracture healing in mice. J Orthop Res 30: 304-310.
48. Yang C, Li SW, Helminen HJ, Khillan JS, Bao Y, et al. (1997) Apoptosis of chondrocytes in transgenic mice lacking collagen II. Exp Cell Res 235: 370-373.
49. Kahler RA, Yingst S, Hoeppner LH, Jensen ED, Krawczak D, et al. (2008) Collagen 11a1 is indirectly activated by lymphocyte enhancer-binding factor 1 (Lef1) and negatively regulates osteoblast maturation. Matrix Biology 27: 330-338.
50. Arce L, Yokoyama NN, Waterman ML, (2006) Diversity of LEF/TCF action in development and disease. Oncogene 25: 7492-7504.
51. Lui VC, Kong RY, Nicholls J, Cheung AN, Cheah KS, (1995) The mRNAs for the three chains of human collagen type XI are widely distributed but not necessarily co-expressed: implications for homotrimeric, heterotrimeric and heterotypic collagen molecules. Biochem J 311: 511.
52. Yoshioka H, Iyama KI, Inoguchi K, Khaleduzzaman M, Ninomiya Y, et al. (1995) Developmental pattern of expression of the mouse alpha 1 (XI) collagen gene (Col11a1). Dev Dyn 204: 41-47.
53. Rodriguez RR, Seegmiller RE, Stark MR, Bridgewater LC, (2004) A type XI collagen mutation leads to increased degradation of type II collagen in articular cartilage. Osteoarthritis Cartilage 12: 314-320.
54. Carlsson P, Waterman ML, Jones KA, (1993) The hLEF/TCF-1 alpha HMG protein contains a context-dependent transcriptional activation domain that induces the TCR alpha enhancer in T cells. Genes Dev 7: 2418-2430.
55. Benya PD, Shaffer JD, (1982) Dedifferentiated chondrocytes reexpress the differentiated collagen phenotype when cultured in agarose gels. Cell 30: 215-224.
56. Huh YH, Ryu JH, Chun JS, (2007) Regulation of type II collagen expression by histone deacetylase in articular chondrocytes. J Biol Chem 282: 17123-17131.
57. Benya PD, Nimni ME, (1979) The stability of the collagen phenotype during stimulated collagen, glycosaminoglycan, and DNA synthesis by articular cartilage organ cultures. Arch Biochem Biophys 192: 327-335.
58. Yoon SW, Chun JS, Sung MH, Kim JY, Poo H, (2008) alpha-MSH inhibits TNF-alpha-induced matrix metalloproteinase-13 expression by modulating p38 kinase and nuclear factor kappaB signaling in human chondrosarcoma HTB-94 cells. Osteoarthritis Cartilage 16: 115-124.
59. Cormier SA, Mello MA, Kappen C, (2003) Normal proliferation and differentiation of Hoxc-8 transgenic chondrocytes in vitro. BMC Dev Biol 3: 4.
60. Gosset M, Berenbaum F, Thirion S, Jacques C, (2008) Primary culture and phenotyping of murine chondrocytes. Nat Protoc 3: 1253-1260.
61. Loots GG, Ovcharenko I, (2004) rVISTA 2.0: evolutionary analysis of transcription factor binding sites. Nucleic Acids Res 32: W217-W221.
62. Dermitzakis ET, Clark AG, (2002) Evolution of transcription factor binding sites in Mammalian gene regulatory regions: conservation and turnover. Mol Biol Evol 19: 1114-1121.
63. Rao S, Procko E, Shannon MF, (2001) Chromatin remodeling, measured by a novel real-time polymerase chain reaction assay, across the proximal promoter region of the IL-2 gene. J Immunol 167: 4494-4503.
64. Weinmann AS, Plevy SE, Smale ST, (1999) Rapid and selective remodeling of a positioned nucleosome during the induction of IL-12 p40 transcription. Immunity 11: 665-675.
65. Forrester WC, Epner E, Driscoll MC, Enver T, Brice M, et al. (1990) A deletion of the human beta-globin locus activation region causes a major alteration in chromatin structure and replication across the entire beta-globin locus. Genes Dev 4: 1637-1649.
66. Hagage H, Klous P, Braem C, Splinter E, Dekker J, et al. (2007) Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2: 1722-1733.