Transcriptional profiling of the human fibrillin/LTBP gene family, key regulators of mesenchymal cell functions

Molecular Genetics and Metabolism

Volumn 112, Issue 1, 2014, Pages 73-83

  Davis, Margaret R ^a   Andersson, Robin ^b   Severin, Jessica ^c   de Hoon, Michiel ^c   Bertin, Nicolas ^c   Baillie, J Kenneth ^a   Kawaji, Hideya ^c   Sandelin, Albin ^b   Forrest, Alistair R R ^c   Summers, Kim M ^a,d  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c RIKEN   (Japan)

^d UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Extracellular matrix; Fibrillin; Gene regulation; Latent transforming growth factor binding protein; Promoter; Transcription start sites

Indexed keywords

FIBRILLIN; FIBRILLIN 1; FIBRILLIN 2; FIBRILLIN 3; GTF2I PROTEIN; KRUPPEL LIKE FACTOR 4; LTBP1 PROTEIN; LTBP2 PROTEIN; LTBP3 PROTEIN; LTBP4 PROTEIN; MAZ PROTEIN; PROTEIN; SCLEROPROTEIN; SP1 PROTEIN; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN;

ADIPOSE TISSUE; ADOLESCENT; ADULT; ARTICLE; CELL FUNCTION; CHILD; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; EMBRYONIC STEM CELL; ENHANCER REGION; FEMALE; FETUS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN GENOME; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; MALE; MESENCHYMAL STEM CELL; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD; TATA BOX; TRANSCRIPTION INITIATION SITE; ANTIBODY SPECIFICITY; CELL LINE; EXTRACELLULAR MATRIX; GENETICS; MESENCHYMAL STROMA CELL; METABOLISM;

CELL LINE; ENHANCER ELEMENTS, GENETIC; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HUMANS; LATENT TGF-BETA BINDING PROTEINS; MESENCHYMAL STROMAL CELLS; MICROFILAMENT PROTEINS; MULTIGENE FAMILY; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC;

EID: 84899648191     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2013.12.006     Document Type: Article

References (52)

1. De Grassi A., Lanave C., Saccone C. Genome duplication and gene-family evolution: the case of three OXPHOS gene families. Gene 2008, 421:1-6.
2. Lowell C.A., Soriano P. Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev. 1996, 10:1845-1857.
3. Roden D.M. Taking the "idio" out of "idiosyncratic": predicting torsades de pointes. Pacing Clin. Electrophysiol. 1998, 21:1029-1034.
4. Bokil N.J., Baisden J.M., Radford D.J., Summers K.M. Molecular genetics of long QT syndrome. Mol. Genet. Metab. 2010, 101:1-8.
5. Guo W., Jung W.E., Marionneau C., Aimond F., Xu H., Yamada K.A., Schwarz T.L., Demolombe S., Nerbonne J.M. Targeted deletion of Kv4.2 eliminates I(to, f) and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circ. Res. 2005, 97:1342-1350.
6. Robertson I., Jensen S., Handford P. TB domain proteins: evolutionary insights into the multifaceted roles of fibrillins and LTBPs. Biochem. J. 2011, 433:263-276.
7. Davis M.R., Summers K.M. Structure and function of the mammalian fibrillin gene family: implications for human connective tissue diseases. Mol. Genet. Metab. 2012, 107:635-647.
8. Saharinen J., Taipale J., Keski-Oja J. Association of the small latent transforming growth factor-beta with an eight cysteine repeat of its binding protein LTBP-1. EMBO J. 1996, 15:245-253.
9. Corson G.M., Charbonneau N.L., Keene D.R., Sakai L.Y. Differential expression of fibrillin-3 adds to microfibril variety in human and avian, but not rodent, connective tissues. Genomics 2004, 83:461-472.
10. Summers K.M., Raza S., van Nimwegen E., Freeman T.C., Hume D.A. Co-expression of FBN1 with mesenchyme-specific genes in mouse cell lines: implications for phenotypic variability in Marfan syndrome. Eur. J. Hum. Genet. 2010, 18:1209-1215.
11. Fairclough R.J., Bareja A., Davies K.E. Progress in therapy for Duchenne muscular dystrophy. Exp. Physiol. 2011, 96:1101-1113.
12. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., Kodzius R., Shimokawa K., Bajic V.B., Brenner S.E., Batalov S., Forrest A.R., Zavolan M., Davis M.J., Wilming L.G., Aidinis V., Allen J.E., Ambesi-Impiombato A., Apweiler R., Aturaliya R.N., Bailey T.L., Bansal M., Baxter L., Beisel K.W., Bersano T., Bono H., Chalk A.M., Chiu K.P., Choudhary V., Christoffels A., Clutterbuck D.R., Crowe M.L., Dalla E., Dalrymple B.P., de Bono B., Della Gatta G., di Bernardo D., Down T., Engstrom P., Fagiolini M., Faulkner G., Fletcher C.F., Fukushima T., Furuno M., Futaki S., Gariboldi M., Georgii-Hemming P., Gingeras T.R., Gojobori T., Green R.E., Gustincich S., Harbers M., Hayashi Y., Hensch T.K., Hirokawa N., Hill D., Huminiecki L., Iacono M., Ikeo K., Iwama A., Ishikawa T., Jakt M., Kanapin A., Katoh M., Kawasawa Y., Kelso J., Kitamura H., Kitano H., Kollias G., Krishnan S.P., Kruger A., Kummerfeld S.K., Kurochkin I.V., Lareau L.F., Lazarevic D., Lipovich L., Liu J., Liuni S., Mcwilliam S., Madan Babu M., Madera M., Marchionni L., Matsuda H., Matsuzawa S., Miki H., Mignone F., Miyake S., Morris K., Mottagui-Tabar S., Mulder N., Nakano N., Nakauchi H., Ng P., Nilsson R., Nishiguchi S., Nishikawa S., Nori F., Ohara O., Okazaki Y., Orlando V., Pang K.C., Pavan W.J., Pavesi G., Pesole G., Petrovsky N., Piazza S., Reed J., Reid J.F., Ring B.Z., Ringwald M., Rost B., Ruan Y., Salzberg S.L., Sandelin A., Schneider C., Schonbach C., Sekiguchi K., Semple C.A., Seno S., Sessa L., Sheng Y., Shibata Y., Shimada H., Shimada K., Silva D., Sinclair B., Sperling S., Stupka E., Sugiura K., Sultana R., Takenaka Y., Taki K., Tammoja K., Tan S.L., Tang S., Taylor M.S., Tegner J., Teichmann S.A., Ueda H.R., van Nimwegen E., Verardo R., Wei C.L., Yagi K., Yamanishi H., Zabarovsky E., Zhu S., Zimmer A., Hide W., Bult C., Grimmond S.M., Teasdale R.D., Liu E.T., Brusic V., Quackenbush J., Wahlestedt C., Mattick J.S., Hume D.A., Kai C., Sasaki D., Tomaru Y., Fukuda S., Kanamori-Katayama M., Suzuki M., Aoki J., Arakawa T., Iida J., Imamura K., Itoh M., Kato T., Kawaji H., Kawagashira N., Kawashima T., Kojima M., Kondo S., Konno H., Nakano K., Ninomiya N., Nishio T., Okada M., Plessy C., Shibata K., Shiraki T., Suzuki S., Tagami M., Waki K., Watahiki A., Okamura-Oho Y., Suzuki H., Kawai J., Hayashizaki Y. The transcriptional landscape of the mammalian genome. Science 2005, 309:1559-1563.
13. Carninci P., Sandelin A., Lenhard B., Katayama S., Shimokawa K., Ponjavic J., Semple C.A., Taylor M.S., Engstrom P.G., Frith M.C., Forrest A.R., Alkema W.B., Tan S.L., Plessy C., Kodzius R., Ravasi T., Kasukawa T., Fukuda S., Kanamori-Katayama M., Kitazume Y., Kawaji H., Kai C., Nakamura M., Konno H., Nakano K., Mottagui-Tabar S., Arner P., Chesi A., Gustincich S., Persichetti F., Suzuki H., Grimmond S.M., Wells C.A., Orlando V., Wahlestedt C., Liu E.T., Harbers M., Kawai J., Bajic V.B., Hume D.A., Hayashizaki Y. Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 2006, 38:626-635.
14. Valen E., Pascarella G., Chalk A., Maeda N., Kojima M., Kawazu C., Murata M., Nishiyori H., Lazarevic D., Motti D., Marstrand T.T., Tang M.H., Zhao X., Krogh A., Winther O., Arakawa T., Kawai J., Wells C., Daub C., Harbers M., Hayashizaki Y., Gustincich S., Sandelin A., Carninci P. Genome-wide detection and analysis of hippocampus core promoters using DeepCAGE. Genome Res. 2009, 19:255-265.
15. Summers K.M., Bokil N.J., Baisden J.M., West M.J., Sweet M.J., Raggatt L.J., Hume D.A. Experimental and bioinformatic characterisation of the promoter region of the Marfan syndrome gene, FBN1. Genomics 2009, 94:233-240.
16. Forrest A.R.R., Kawaji H., Rehli M., Baillie J.K., de Hoon M.J.L., H.V., Lassmann T., K.I.V., Lizio M., Itoh M., Andersson R., Mungall C.J., Mehan T.F., et al. A promoter level mammalian expression atlas. Nature 2014, 10.1038/nature13182.
17. Fogh J., Fogh J.M., Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J. Natl. Cancer Inst. 1977, 59:221-226.
18. Rodan S.B., Imai Y., Thiede M.A., Wesolowski G., Thompson D., Bar-Shavit Z., Shull S., Mann K., Rodan G.A. Characterization of a human osteosarcoma cell line (Saos-2) with osteoblastic properties. Cancer Res. 1987, 47:4961-4966.
19. Billiau A., Edy V.G., Heremans H., Van Damme J., Desmyter J., Georgiades J.A., De Somer P. Human interferon: mass production in a newly established cell line, MG-63. Antimicrob. Agents Chemother. 1977, 12:11-15.
20. Heremans H., Billiau A., Cassiman J.J., Mulier J.C., de Somer P. In vitro cultivation of human tumor tissues. II. Morphological and virological characterization of three cell lines. Oncology 1978, 35:246-252.
21. Orimo H., Shimada T. Effects of phosphates on the expression of tissue-nonspecific alkaline phosphatase gene and phosphate-regulating genes in short-term cultures of human osteosarcoma cell lines. Mol. Cell. Biochem. 2006, 282:101-108.
22. Pautke C., Schieker M., Tischer T., Kolk A., Neth P., Mutschler W., Milz S. Characterization of osteosarcoma cell lines MG-63, Saos-2 and U-2 OS in comparison to human osteoblasts. Anticancer Res. 2004, 24:3743-3748.
23. Ledran M.H., Krassowska A., Armstrong L., Dimmick I., Renstrom J., Lang R., Yung S., Santibanez-Coref M., Dzierzak E., Stojkovic M., Oostendorp R.A., Forrester L., Lako M. Efficient hematopoietic differentiation of human embryonic stem cells on stromal cells derived from hematopoietic niches. Cell Stem Cell 2008, 3:85-98.
24. Fletcher J.M., Ferrier P.M., Gardner J.O., Harkness L., Dhanjal S., Serhal P., Harper J., Delhanty J., Brownstein D.G., Prasad Y.R., Lebkowski J., Mandalam R., Wilmut I., De Sousa P.A. Variations in humanized and defined culture conditions supporting derivation of new human embryonic stem cell lines. Cloning Stem Cells 2006, 8:319-334.
25. Barnett M.W., Old R.W., Jones E.A. Neural induction and patterning by fibroblast growth factor, notochord and somite tissue in Xenopus. Dev. Growth Differ. 1998, 40:47-57.
26. Kanamori-Katayama M., Itoh M., Kawaji H., Lassmann T., Katayama S., Kojima M., Bertin N., Kaiho A., Ninomiya N., Daub C.O., Carninci P., Forrest A.R., Hayashizaki Y. Unamplified cap analysis of gene expression on a single-molecule sequencer. Genome Res. 2011, 21:1150-1159.
27. Severin J., Lizio M., Harshbarger J., Kawaji H., Daub C.O., Hayashizaki Y., Bertin N., Forrest A.R.R. ZENBU: secured scientific collaborations, data integration and omics visualization. Nat. Biotechnol. 2014, 10.1038/nbt.2840.
28. Andersson R., Gebhardt C., Miguel-Escalada I., Hoof I., Zhao X., Schmidl C., Valen E., Li K., Schwarzfischer L., Glatz D., Raithel J., Chen Y., Lilje B., Rapin N., Bagger F.O., et al. An atlas of active enhancers across human cell types and tissues. Nature 2014, 10.1038/nature12787.
29. Freeman T.C., Goldovsky L., Brosch M., van Dongen S., Maziere P., Grocock R.J., Freilich S., Thornton J., Enright A.J. Construction, visualisation, and clustering of transcription networks from microarray expression data. PLoS Comput. Biol. 2007, 3:2032-2042.
30. Freeman T.C., Ivens A., Baillie J.K., Beraldi D., Barnett M.W., Dorward D., Downing A., Fairbairn L., Kapetanovic R., Raza S., Tomoiu A., Alberio R., Wu C., Su A.I., Summers K.M., Tuggle C.K., Archibald A.L., Hume D.A. A gene expression atlas of the domestic pig. BMC Biol. 2012, 10:90.
31. Meyer L.R., Zweig A.S., Hinrichs A.S., Karolchik D., Kuhn R.M., Wong M., Sloan C.A., Rosenbloom K.R., Roe G., Rhead B., Raney B.J., Pohl A., Malladi V.S., Li C.H., Lee B.T., Learned K., Kirkup V., Hsu F., Heitner S., Harte R.A., Haeussler M., Guruvadoo L., Goldman M., Giardine B.M., Fujita P.A., Dreszer T.R., Diekhans M., Cline M.S., Clawson H., Barber G.P., Haussler D., Kent W.J. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 2013, 41:D64-D69.
32. Notredame C., Higgins D.G., Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302:205-217.
33. Arnold P., Erb I., Pachkov M., Molina N., van Nimwegen E. MotEvo: integrated Bayesian probabilistic methods for inferring regulatory sites and motifs on multiple alignments of DNA sequences. Bioinformatics 2012, 28:487-494.
34. Suzuki H., Forrest A.R., van Nimwegen E., Daub C.O., Balwierz P.J., Irvine K.M., Lassmann T., Ravasi T., Hasegawa Y., de Hoon M.J., Katayama S., Schroder K., Carninci P., Tomaru Y., Kanamori-Katayama M., Kubosaki A., Akalin A., Ando Y., Arner E., Asada M., Asahara H., Bailey T., Bajic V.B., Bauer D., Beckhouse A.G., Bertin N., Bjorkegren J., Brombacher F., Bulger E., Chalk A.M., Chiba J., Cloonan N., Dawe A., Dostie J., Engstrom P.G., Essack M., Faulkner G.J., Fink J.L., Fredman D., Fujimori K., Furuno M., Gojobori T., Gough J., Grimmond S.M., Gustafsson M., Hashimoto M., Hashimoto T., Hatakeyama M., Heinzel S., Hide W., Hofmann O., Hornquist M., Huminiecki L., Ikeo K., Imamoto N., Inoue S., Inoue Y., Ishihara R., Iwayanagi T., Jacobsen A., Kaur M., Kawaji H., Kerr M.C., Kimura R., Kimura S., Kimura Y., Kitano H., Koga H., Kojima T., Kondo S., Konno T., Krogh A., Kruger A., Kumar A., Lenhard B., Lennartsson A., Lindow M., Lizio M., Macpherson C., Maeda N., Maher C.A., Maqungo M., Mar J., Matigian N.A., Matsuda H., Mattick J.S., Meier S., Miyamoto S., Miyamoto-Sato E., Nakabayashi K., Nakachi Y., Nakano M., Nygaard S., Okayama T., Okazaki Y., Okuda-Yabukami H., Orlando V., Otomo J., Pachkov M., Petrovsky N., Plessy C., Quackenbush J., Radovanovic A., Rehli M., Saito R., Sandelin A., Schmeier S., Schonbach C., Schwartz A.S., Semple C.A., Sera M., Severin J., Shirahige K., Simons C., St Laurent G., Suzuki M., Suzuki T., Sweet M.J., Taft R.J., Takeda S., Takenaka Y., Tan K., Taylor M.S., Teasdale R.D., Tegner J., Teichmann S., Valen E., Wahlestedt C., Waki K., Waterhouse A., Wells C.A., Winther O., Wu L., Yamaguchi K., Yanagawa H., Yasuda J., Zavolan M., Hume D.A., Arakawa T., Fukuda S., Imamura K., Kai C., Kaiho A., Kawashima T., Kawazu C., Kitazume Y., Kojima M., Miura H., Murakami K., Murata M., Ninomiya N., Nishiyori H., Noma S., Ogawa C., Sano T., Simon C., Tagami M., Takahashi Y., Kawai J., Hayashizaki Y. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat. Genet. 2009, 41:553-562.
35. Mabbott N.A., Kenneth Baillie J., Kobayashi A., Donaldson D.S., Ohmori H., Yoon S.O., Freedman A.S., Freeman T.C., Summers K.M. Expression of mesenchyme-specific gene signatures by follicular dendritic cells: insights from the meta-analysis of microarray data from multiple mouse cell populations. Immunology 2011, 133:482-498.
36. Consortium T.E.P. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011, 9:e1001046.
37. Guo G., Bauer S., Hecht J., Schulz M.H., Busche A., Robinson P.N. A short ultraconserved sequence drives transcription from an alternate FBN1 promoter. Int. J. Biochem. Cell Biol. 2008, 40:638-650.
38. Corson G.M., Chalberg S.C., Dietz H.C., Charbonneau N.L., Sakai L.Y. Fibrillin binds calcium and is coded by cDNAs that reveal a multidomain structure and alternatively spliced exons at the 5' end. Genomics 1993, 17:476-484.
39. Singh K.K., Shukla P.C., Schmidtke J. Conservation of 5'-upstream region of the FBN1 gene in primates. Eur. J. Hum. Genet. 2008, 16:869-872.
40. Sakai L.Y., Keene D.R., Engvall E. Fibrillin, a new 350-kD glycoprotein, is a component of extracellular microfibrils. J. Cell Biol. 1986, 103:2499-2509.
41. Zhang H., Apfelroth S.D., Hu W., Davis E.C., Sanguineti C., Bonadio J., Mecham R.P., Ramirez F. Structure and expression of fibrillin-2, a novel microfibrillar component preferentially located in elastic matrices. J. Cell Biol. 1994, 124:855-863.
42. Clark D.A., Coker R. Transforming growth factor-beta (TGF-beta). Int. J. Biochem. Cell Biol. 1998, 30:293-298.
43. Chang H., Brown C.W., Matzuk M.M. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr. Rev. 2002, 23:787-823.
44. Shi M., Zhu J., Wang R., Chen X., Mi L., Walz T., Springer T.A. Latent TGF-beta structure and activation. Nature 2011, 474:343-349.
45. Kitagawa T., Michalopoulos G., Pitot H.C. Unscheduled DNA synthesis in cells from N-2-fluorenylacetamide-induced hyperplastic nodules of rat liver maintained in a primary culture system. Cancer Res. 1975, 35:3682-3692.
46. Wang H., Yang L., Jamaluddin M.S., Boyd D.D. The Kruppel-like KLF4 transcription factor, a novel regulator of urokinase receptor expression, drives synthesis of this binding site in colonic crypt luminal surface epithelial cells. J. Biol. Chem. 2004, 279:22674-22683.
47. Moser M., Imhof A., Pscherer A., Bauer R., Amselgruber W., Sinowatz F., Hofstadter F., Schule R., Buettner R. Cloning and characterization of a second AP-2 transcription factor: AP-2 beta. Development 1995, 121:2779-2788.
48. Urbanek P., Wang Z.Q., Fetka I., Wagner E.F., Busslinger M. Complete block of early B cell differentiation and altered patterning of the posterior midbrain in mice lacking Pax5/BSAP. Cell 1994, 79:901-912.
49. Rolink A.G., Nutt S.L., Melchers F., Busslinger M. Long-term in vivo reconstitution of T-cell development by Pax5-deficient B-cell progenitors. Nature 1999, 401:603-606.
50. Vecellio M., Meraviglia V., Nanni S., Barbuti A., Scavone A., Difrancesco D., Farsetti A., Pompilio G., Colombo G.I., Capogrossi M.C., Gaetano C., Rossini A. In vitro epigenetic reprogramming of human cardiac mesenchymal stromal cells into functionally competent cardiovascular precursors. PLoS ONE 2012, 7:e51694.
51. Zhou P., He A., Pu W.T. Regulation of GATA4 transcriptional activity in cardiovascular development and disease. Curr. Top. Dev. Biol. 2012, 100:143-169.
52. Tapscott S.J., Weintraub H. MyoD and the regulation of myogenesis by helix-loop-helix proteins. J. Clin. Invest. 1991, 87:1133-1138.