DeepCAGE Transcriptomics Reveal an Important Role of the Transcription Factor MAFB in the Lymphatic Endothelium

Cell Reports

Volumn 13, Issue 7, 2015, Pages 1493-1504

  Dieterich, Lothar C ^a   Klein, Sarah ^a   Mathelier, Anthony ^b   Sliwa Primorac, Adriana ^a   Ma, Qiaoli ^a   Hong, Young Kwon ^c   Shin, Jay W ^d   Hamada, Michito ^e   Lizio, Marina ^d   Itoh, Masayoshi ^d   Kawaji, Hideya ^d   Lassmann, Timo ^d,f   Daub, Carsten O ^d   Arner, Erik ^d   Carninci, Piero ^d   Hayashizaki, Yoshihide ^d   Forrest, Alistair R R ^d   Wasserman, Wyeth W ^b   Detmar, Michael ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^d RIKEN   (Japan)

^e UNIVERSITY OF TSUKUBA   (Japan)

^f UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAFB; TRANSCRIPTION FACTOR PROX1; TRANSCRIPTION FACTOR SOX18; UNCLASSIFIED DRUG; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3; DIFFERENTIATION ANTIGEN; MAFB PROTEIN, MOUSE; PROTEIN BINDING; TRANSCRIPTOME;

ANIMAL CELL; ARTICLE; BLOOD VASCULAR ENDOTHELIAL CELL; CAP ANALYSIS OF GENE EXPRESSION; CELL DIFFERENTIATION; CELLS BY BODY ANATOMY; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; GENE; GENE EXPRESSION; GENE FUNCTION; GENETIC MARKER; HUMAN; HUMAN CELL; IN VIVO STUDY; LYMPH VESSEL; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MAFB GENE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA SEQUENCE; TRANSCRIPTOMICS; ANIMAL; BINDING SITE; C57BL MOUSE; CELL CULTURE; CYTOLOGY; GENE EXPRESSION PROFILING; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, DIFFERENTIATION; BASE SEQUENCE; BINDING SITES; CELL DIFFERENTIATION; CELLS, CULTURED; EMBRYONIC DEVELOPMENT; ENDOTHELIUM, LYMPHATIC; GENE EXPRESSION PROFILING; HUMANS; LYMPHANGIOGENESIS; LYMPHATIC VESSELS; MAFB TRANSCRIPTION FACTOR; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTIONAL ACTIVATION; TRANSCRIPTOME; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84947303632     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.10.002     Document Type: Article

References (58)

1. Abe M., Sato Y. cDNA microarray analysis of the gene expression profile of VEGF-activated human umbilical vein endothelial cells. Angiogenesis 2001, 4:289-298.
2. Amit I., Citri A., Shay T., Lu Y., Katz M., Zhang F., Tarcic G., Siwak D., Lahad J., Jacob-Hirsch J., et al. A module of negative feedback regulators defines growth factor signaling. Nat. Genet. 2007, 39:503-512.
3. Arner E., Daub C.O., Vitting-Seerup K., Andersson R., Lilje B., Drabløs F., Lennartsson A., Rönnerblad M., Hrydziuszko O., Vitezic M., et al. Gene regulation. Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science 2015, 347:1010-1014. FANTOM Consortium.
4. Aziz A., Vanhille L., Mohideen P., Kelly L.M., Otto C., Bakri Y., Mossadegh N., Sarrazin S., Sieweke M.H. Development of macrophages with altered actin organization in the absence of MafB. Mol. Cell. Biol. 2006, 26:6808-6818.
5. Badis G., Berger M.F., Philippakis A.A., Talukder S., Gehrke A.R., Jaeger S.A., Chan E.T., Metzler G., Vedenko A., Chen X., et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009, 324:1720-1723.
6. Blanchi B., Kelly L.M., Viemari J.C., Lafon I., Burnet H., Bévengut M., Tillmanns S., Daniel L., Graf T., Hilaire G., Sieweke M.H. MafB deficiency causes defective respiratory rhythmogenesis and fatal central apnea at birth. Nat. Neurosci. 2003, 6:1091-1100.
7. Cermenati S., Moleri S., Neyt C., Bresciani E., Carra S., Grassini D.R., Omini A., Goi M., Cotelli F., François M., et al. Sox18 genetically interacts with VegfC to regulate lymphangiogenesis in zebrafish. Arterioscler. Thromb. Vasc. Biol. 2013, 33:1238-1247.
8. A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011, 9:e1001046. ENCODE Project Consortium.
9. Eychène A., Rocques N., Pouponnot C. A new MAFia in cancer. Nat. Rev. Cancer 2008, 8:683-693.
10. Forrest A.R., Kawaji H., Rehli M., Baillie J.K., de Hoon M.J., Haberle V., Lassmann T., Kulakovskiy I.V., Lizio M., Itoh M., et al. A promoter-level mammalian expression atlas. Nature 2014, 507:462-470. FANTOM Consortium and the RIKEN PMI and CLST (DGT).
11. François M., Caprini A., Hosking B., Orsenigo F., Wilhelm D., Browne C., Paavonen K., Karnezis T., Shayan R., Downes M., et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008, 456:643-647.
12. François M., Short K., Secker G.A., Combes A., Schwarz Q., Davidson T.L., Smyth I., Hong Y.K., Harvey N.L., Koopman P. Segmental territories along the cardinal veins generate lymph sacs via a ballooning mechanism during embryonic lymphangiogenesis in mice. Dev. Biol. 2012, 364:89-98.
13. Friedman A.D. Transcriptional control of granulocyte and monocyte development. Oncogene 2007, 26:6816-6828.
14. Hägerling R., Pollmann C., Andreas M., Schmidt C., Nurmi H., Adams R.H., Alitalo K., Andresen V., Schulte-Merker S., Kiefer F. A novel multistep mechanism for initial lymphangiogenesis in mouse embryos based on ultramicroscopy. EMBO J. 2013, 32:629-644.
15. Halin C., Tobler N.E., Vigl B., Brown L.F., Detmar M. VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 2007, 110:3158-3167.
16. Hamada M., Nakamura M., Tran M.T., Moriguchi T., Hong C., Ohsumi T., Dinh T.T., Kusakabe M., Hattori M., Katsumata T., et al. MafB promotes atherosclerosis by inhibiting foam-cell apoptosis. Nat. Commun. 2014, 5:3147.
17. Hang Y., Stein R. MafA and MafB activity in pancreatic β cells. Trends Endocrinol. Metab. 2011, 22:364-373.
18. Harvey N.L., Srinivasan R.S., Dillard M.E., Johnson N.C., Witte M.H., Boyd K., Sleeman M.W., Oliver G. Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat. Genet. 2005, 37:1072-1081.
19. Hirakawa S., Hong Y.K., Harvey N., Schacht V., Matsuda K., Libermann T., Detmar M. Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am. J. Pathol. 2003, 162:575-586.
20. Johnson N.C., Dillard M.E., Baluk P., McDonald D.M., Harvey N.L., Frase S.L., Oliver G. Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev. 2008, 22:3282-3291.
21. Joukov V., Sorsa T., Kumar V., Jeltsch M., Claesson-Welsh L., Cao Y., Saksela O., Kalkkinen N., Alitalo K. Proteolytic processing regulates receptor specificity and activity of VEGF-C. EMBO J. 1997, 16:3898-3911.
22. Joukov V., Kumar V., Sorsa T., Arighi E., Weich H., Saksela O., Alitalo K. A recombinant mutant vascular endothelial growth factor-C that has lost vascular endothelial growth factor receptor-2 binding, activation, and vascular permeability activities. J. Biol. Chem. 1998, 273:6599-6602.
23. Kanamori-Katayama M., Itoh M., Kawaji H., Lassmann T., Katayama S., Kojima M., Bertin N., Kaiho A., Ninomiya N., Daub C.O., et al. Unamplified cap analysis of gene expression on a single-molecule sequencer. Genome Res. 2011, 21:1150-1159.
24. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., et al. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 2004, 5:74-80.
25. Koch S., Tugues S., Li X., Gualandi L., Claesson-Welsh L. Signal transduction by vascular endothelial growth factor receptors. Biochem. J. 2011, 437:169-183.
26. Koltowska K., Betterman K.L., Harvey N.L., Hogan B.M. Getting out and about: the emergence and morphogenesis of the vertebrate lymphatic vasculature. Development 2013, 140:1857-1870.
27. Koltowska K., Paterson S., Bower N.I., Baillie G.J., Lagendijk A.K., Astin J.W., Chen H., Francois M., Crosier P.S., Taft R.J., et al. mafba is a downstream transcriptional effector of Vegfc signaling essential for embryonic lymphangiogenesis in zebrafish. Genes Dev. 2015, 29:1618-1630.
28. Kukk E., Lymboussaki A., Taira S., Kaipainen A., Jeltsch M., Joukov V., Alitalo K. VEGF-C receptor binding and pattern of expression with VEGFR-3 suggests a role in lymphatic vascular development. Development 1996, 122:3829-3837.
29. Kwon A.T., Arenillas D.J., Worsley Hunt R., Wasserman W.W. oPOSSUM-3: advanced analysis of regulatory motif over-representation across genes or ChIP-Seq datasets. G3 (Bethesda) 2012, 2:987-1002.
30. Lin F.J., Chen X., Qin J., Hong Y.K., Tsai M.J., Tsai S.Y. Direct transcriptional regulation of neuropilin-2 by COUP-TFII modulates multiple steps in murine lymphatic vessel development. J. Clin. Invest. 2010, 120:1694-1707.
31. Lopez-Pajares V., Qu K., Zhang J., Webster D.E., Barajas B.C., Siprashvili Z., Zarnegar B.J., Boxer L.D., Rios E.J., Tao S., et al. A LncRNA-MAF:MAFB transcription factor network regulates epidermal differentiation. Dev. Cell 2015, 32:693-706.
32. Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15:550.
33. Martinez-Corral I., Ulvmar M.H., Stanczuk L., Tatin F., Kizhatil K., John S.W., Alitalo K., Ortega S., Makinen T. Nonvenous origin of dermal lymphatic vasculature. Circ. Res. 2015, 116:1649-1654.
34. Mathelier A., Zhao X., Zhang A.W., Parcy F., Worsley-Hunt R., Arenillas D.J., Buchman S., Chen C.Y., Chou A., Ienasescu H., et al. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 2014, 42:D142-D147.
35. Moriguchi T., Hamada M., Morito N., Terunuma T., Hasegawa K., Zhang C., Yokomizo T., Esaki R., Kuroda E., Yoh K., et al. MafB is essential for renal development and F4/80 expression in macrophages. Mol. Cell. Biol. 2006, 26:5715-5727.
36. Nagashima T., Shimodaira H., Ide K., Nakakuki T., Tani Y., Takahashi K., Yumoto N., Hatakeyama M. Quantitative transcriptional control of ErbB receptor signaling undergoes graded to biphasic response for cell differentiation. J. Biol. Chem. 2007, 282:4045-4056.
37. Nelson J.D., Denisenko O., Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 2006, 1:179-185.
38. Park D.Y., Lee J., Park I., Choi D., Lee S., Song S., Hwang Y., Hong K.Y., Nakaoka Y., Makinen T., et al. Lymphatic regulator PROX1 determines Schlemm's canal integrity and identity. J. Clin. Invest. 2014, 124:3960-3974.
39. Petrova T.V., Mäkinen T., Mäkelä T.P., Saarela J., Virtanen I., Ferrell R.E., Finegold D.N., Kerjaschki D., Ylä-Herttuala S., Alitalo K. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J. 2002, 21:4593-4599.
40. Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010, 26:139-140.
41. Rocques N., Abou Zeid N., Sii-Felice K., Lecoin L., Felder-Schmittbuhl M.P., Eychène A., Pouponnot C. GSK-3-mediated phosphorylation enhances Maf-transforming activity. Mol. Cell 2007, 28:584-597.
42. Rutkowski J.M., Ihm J.E., Lee S.T., Kilarski W.W., Greenwood V.I., Pasquier M.C., Quazzola A., Trono D., Hubbell J.A., Swartz M.A. VEGFR-3 neutralization inhibits ovarian lymphangiogenesis, follicle maturation, and murine pregnancy. Am. J. Pathol. 2013, 183:1596-1607.
43. Sabine A., Agalarov Y., Maby-El Hajjami H., Jaquet M., Hägerling R., Pollmann C., Bebber D., Pfenniger A., Miura N., Dormond O., et al. Mechanotransduction, PROX1, and FOXC2 cooperate to control connexin37 and calcineurin during lymphatic-valve formation. Dev. Cell 2012, 22:430-445.
44. Shin J.W., Huggenberger R., Detmar M. Transcriptional profiling of VEGF-A and VEGF-C target genes in lymphatic endothelium reveals endothelial-specific molecule-1 as a novel mediator of lymphangiogenesis. Blood 2008, 112:2318-2326.
45. Shiraki T., Kondo S., Katayama S., Waki K., Kasukawa T., Kawaji H., Kodzius R., Watahiki A., Nakamura M., Arakawa T., et al. Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc. Natl. Acad. Sci. USA 2003, 100:15776-15781.
46. Sieweke M.H., Tekotte H., Frampton J., Graf T. MafB is an interaction partner and repressor of Ets-1 that inhibits erythroid differentiation. Cell 1996, 85:49-60.
47. Srinivasan R.S., Oliver G. Prox1 dosage controls the number of lymphatic endothelial cell progenitors and the formation of the lymphovenous valves. Genes Dev. 2011, 25:2187-2197.
48. Srinivasan R.S., Geng X., Yang Y., Wang Y., Mukatira S., Studer M., Porto M.P., Lagutin O., Oliver G. The nuclear hormone receptor Coup-TFII is required for the initiation and early maintenance of Prox1 expression in lymphatic endothelial cells. Genes Dev. 2010, 24:696-707.
49. Srinivasan R.S., Escobedo N., Yang Y., Interiano A., Dillard M.E., Finkelstein D., Mukatira S., Gil H.J., Nurmi H., Alitalo K., Oliver G. The Prox1-Vegfr3 feedback loop maintains the identity and the number of lymphatic endothelial cell progenitors. Genes Dev. 2014, 28:2175-2187.
50. Tillmanns S., Otto C., Jaffray E., Du Roure C., Bakri Y., Vanhille L., Sarrazin S., Hay R.T., Sieweke M.H. SUMO modification regulates MafB-driven macrophage differentiation by enabling Myb-dependent transcriptional repression. Mol. Cell. Biol. 2007, 27:5554-5564.
51. Wang J., Zhuang J., Iyer S., Lin X., Whitfield T.W., Greven M.C., Pierce B.G., Dong X., Kundaje A., Cheng Y., et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 2012, 22:1798-1812.
52. Wang J., Zhuang J., Iyer S., Lin X.Y., Greven M.C., Kim B.H., Moore J., Pierce B.G., Dong X., Virgil D., et al. Factorbook.org: a Wiki-based database for transcription factor-binding data generated by the ENCODE consortium. Nucleic Acids Res. 2013, 41:D171-D176.
53. Wigle J.T., Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778.
54. Xu Y., Yuan L., Mak J., Pardanaud L., Caunt M., Kasman I., Larrivée B., Del Toro R., Suchting S., Medvinsky A., et al. Neuropilin-2 mediates VEGF-C-induced lymphatic sprouting together with VEGFR3. J. Cell Biol. 2010, 188:115-130.
55. Yang Y., Cvekl A. Large Maf Transcription Factors: Cousins of AP-1 Proteins and Important Regulators of Cellular Differentiation. Einstein J. Biol. Med. 2007, 23:2-11.
56. Yang Y., Oliver G. Development of the mammalian lymphatic vasculature. J. Clin. Invest. 2014, 124:888-897.
57. Yang Y., García-Verdugo J.M., Soriano-Navarro M., Srinivasan R.S., Scallan J.P., Singh M.K., Epstein J.A., Oliver G. Lymphatic endothelial progenitors bud from the cardinal vein and intersomitic vessels in mammalian embryos. Blood 2012, 120:2340-2348.
58. Yuan L., Moyon D., Pardanaud L., Bréant C., Karkkainen M.J., Alitalo K., Eichmann A. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 2002, 129:4797-4806.