Discovery of microvascular miRNAs using public gene expression data: MiR-145 is expressed in pericytes and is a regulator of Fli1

Genome Medicine

Volumn 1, Issue 11, 2009, Pages

  Larsson, Erik ^a,b   Fuchs, Peder Fredlund ^c   Heldin, Johan ^c   Barkefors, Irmeli ^c   Bondjers, Cecilia ^c   Genové, Guillem ^d   Arrondel, Christelle ^e,f   Gerwins, Pär ^c   Kurschat, Christine ^g   Schermer, Bernhard ^g   Benzing, Thomas ^g   Harvey, Scott J ^e   Kreuger, Johan ^c   Lindahl, Per ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

^d KAROLINSKA INSTITUTE   (Sweden)

^e HÔPITAL NECKER ENFANTS MALADES   (France)

^f UNIVERSITÉ PARIS DESCARTES   (France)

^g UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 145; MICRORNA 23A; MICRORNA 24; TRANSCRIPTION FACTOR FLI 1; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE TARGETING; IN SITU HYBRIDIZATION; MICROVASCULATURE; MOUSE; NONHUMAN; PERICYTE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE;

EID: 77953466413     PISSN: None     EISSN: 1756994X     Source Type: Journal    
DOI: 10.1186/gm108     Document Type: Article

References (51)

1. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN: MicroRNA genes are transcribed by RNA polymerase II. Embo J 2004, 23:4051-4060.
2. Bushati N, Cohen SM: microRNA functions. Annu Rev Cell Dev Biol 2007, 23:175-205.
3. Urbich C, Kuehbacher A, Dimmeler S: Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res 2008, 79:581-588.
4. Yang WJ, Yang DD, Na S, Sandusky GE, Zhang Q, Zhao G: Dicer is required for embryonic angiogenesis during mouse development. J Biol Chem 2005, 280:9330-9335.
5. Suarez Y, Fernandez-Hernando C, Yu J, Gerber SA, Harrison KD, Pober JS, Iruela-Arispe ML, Merkenschlager M, Sessa WC: Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci U S A 2008, 105:14082-14087.
6. Kuehbacher A, Urbich C, Zeiher AM, Dimmeler S: Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ Res 2007, 101:59-68.
7. Suarez Y, Fernandez-Hernando C, Pober JS, Sessa WC: Dicer dependent microRNAs regulate gene expression and functions in human endothelial cells. Circ Res 2007, 100:1164-1173.
8. Harris TA, Yamakuchi M, Ferlito M, Mendell JT, Lowenstein CJ: MicroRNA-126 regulates endothelial expression of vascular cell adhesion molecule 1. Proc Natl Acad Sci U S A 2008, 105:1516-1521.
9. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN: The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell 2008, 15:261-271.
10. Fish JE, Santoro MM, Morton SU, Yu S, Yeh RF, Wythe JD, Ivey KN, Bruneau BG, Stainier DY, Srivastava D: miR-126 regulates angiogenic signaling and vascular integrity. Dev Cell 2008, 15:272-284.
11. Kuhnert F, Mancuso MR, Hampton J, Stankunas K, Asano T, Chen CZ, Kuo CJ: Attribution of vascular phenotypes of the murine Egfl7 locus to the microRNA miR-126. Development 2008, 135:3989-3993.
12. Poliseno L, Tuccoli A, Mariani L, Evangelista M, Citti L, Woods K, Mercatanti A, Hammond S, Rainaldi G: MicroRNAs modulate the angiogenic properties of HUVECs. Blood 2006, 108:3068-3071.
13. Lee DY, Deng Z, Wang CH, Yang BB: MicroRNA-378 promotes cell survival, tumor growth, and angiogenesis by targeting SuFu and Fus-1 expression. Proc Natl Acad Sci U S A 2007, 104:20350-20355.
14. Dews M, Homayouni A, Yu D, Murphy D, Sevignani C, Wentzel E, Furth EE, Lee WM, Enders GH, Mendell JT, Thomas-Tikhonenko A: Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster. Nat Genet 2006, 38:1060-1065.
15. Wurdinger T, Tannous BA, Saydam O, Skog J, Grau S, Soutschek J, Weissleder R, Breakefield XO, Krichevsky AM: miR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell 2008, 14:382-393.
16. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foa R, Schliwka J, Fuchs U, Novosel A, Muller RU, Schermer B, Bissels U, Inman J, Phan Q, Chien M, Weir DB, Choksi R, De Vita G, Frezzetti D, Trompeter HI et al: A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 2007, 129:1401-1414.
17. Thomson JM, Parker J, Perou CM, Hammond SM: A custom microarray platform for analysis of microRNA gene expression. Nat Methods 2004, 1:47-53.
18. Beuvink I, Kolb FA, Budach W, Garnier A, Lange J, Natt F, Dengler U, Hall J, Filipowicz W, Weiler J: A novel microarray approach reveals new tissue-specific signatures of known and predicted mammalian microRNAs. Nucleic Acids Res 2007, 35:e52.
19. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ: miRBase: tools for microRNA genomics. Nucleic Acids Res 2008, 36:D154-158.
20. Hsiao LL, Dangond F, Yoshida T, Hong R, Jensen RV, Misra J, Dillon W, Lee KF, Clark KE, Haverty P, Weng Z, Mutter GL, Frosch MP, Macdonald ME, Milford EL, Crum CP, Bueno R, Pratt RE, Mahadevappa M, Warrington JA, Stephanopoulos G, Stephanopoulos G, Gullans SR: A compendium of gene expression in normal human tissues. Physiol Genomics 2001, 7:97-104.
21. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D: The human genome browser at UCSC. Genome Res 2002, 12:996-1006.
22. Bondjers C, He L, Takemoto M, Norlin J, Asker N, Hellstrom M, Lindahl P, Betsholtz C: Microarray analysis of blood microvessels from PDGF-B and PDGF-Rbeta mutant mice identifies novel markers for brain pericytes. FASEB J 2006, 20:1703-1705.
23. Lindblom P, Gerhardt H, Liebner S, Abramsson A, Enge M, Hellstrom M, Backstrom G, Fredriksson S, Landegren U, Nystrom HC, Bergstrom G, Dejana E, Ostman A, Lindahl P, Betsholtz C: Endothelial PDGF-B retention is required for proper investment of pericytes in the microvessel wall. Genes Dev 2003, 17:1835-1840.
24. Nagy A, Rossant J, Nagy R, Abramow-Newerly W, Roder JC: Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:8424-8428.
25. Jakobsson L, Kreuger J, Holmborn K, Lundin L, Eriksson I, Kjellen L, Claesson-Welsh L: Heparan sulfate in trans potentiates VEGFR-mediated angiogenesis. Developmental cell 2006, 10:625-634.
26. Harvey SJ, Jarad G, Cunningham J, Goldberg S, Schermer B, Harfe BD, McManus MT, Benzing T, Miner JH: Podocyte-specific deletion of dicer alters cytoskeletal dynamics and causes glomerular disease. J Am Soc Nephrol 2008, 19:2150-2158.
27. Barkefors I, Le Jan S, Jakobsson L, Hejll E, Carlson G, Johansson H, Jarvius J, Park JW, Li Jeon N, Kreuger J: Endothelial cell migration in stable gradients of vascular endothelial growth factor A and fibroblast growth factor 2: effects on chemotaxis and chemokinesis. J Biol Chem 2008, 283:13905-13912.
28. Schermer B, Ghenoiu C, Bartram M, Muller RU, Kotsis F, Hohne M, Kuhn W, Rapka M, Nitschke R, Zentgraf H, Fliegauf M, Omran H, Walz G, Benzing T: The von Hippel-Lindau tumor suppressor protein controls ciliogenesis by orienting microtubule growth. J Cell Biol 2006, 175:547-554
29. Wallgard E, Larsson E, He L, Hellstrom M, Armulik A, Nisancioglu MH, Genove G, Lindahl P, Betsholtz C: Identification of a Core Set of 58 Gene Transcripts With Broad and Specific Expression in the Microvasculature. Arterioscler Thromb Vasc Biol 2008.
30. Baskerville S, Bartel DP: Microarray profiling of microRNAs reveals frequent coexpression with neighboring miRNAs and host genes. Rna 2005, 11:241-247.
31. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS: Human MicroRNA targets. PLoS Biol 2004, 2:e363.
32. Krek A, Grun D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, Rajewsky N: Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500.
33. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB: Prediction of mammalian microRNA targets. Cell 2003, 115:787-798.
34. Asirvatham AJ, Gregorie CJ, Hu Z, Magner WJ, Tomasi TB: MicroRNA targets in immune genes and the Dicer/Argonaute and ARE machinery components. Mol Immunol 2008, 45:1995-2006.
35. Seppa H, Grotendorst G, Seppa S, Schiffmann E, Martin GR: Platelet-derived growth factor in chemotactic for fibroblasts. J Cell Biol 1982, 92:584-588.
36. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R: Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 1991, 253:1129-1132.
37. Lindahl P, Johansson BR, Leveen P, Betsholtz C: Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997, 277:242-245.
38. Kulshreshtha R, Davuluri RV, Calin GA, Ivan M: A microRNA component of the hypoxic response. Cell Death Differ 2008, 15:667-671.
39. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D: miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 2009, 460:705-710.
40. Xin M, Small EM, Sutherland LB, Qi X, McAnally J, Plato CF, Richardson JA, Bassel-Duby R, Olson EN: MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev 2009, 23:2166-2178.
41. Cheng Y, Liu X, Yang J, Lin Y, Xu DZ, Lu Q, Deitch EA, Huo Y, Delphin ES, Zhang C: MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation. Circ Res 2009, 105:158-166.
42. Zeng L, Carter AD, Childs SJ: miR-145 directs intestinal maturation in zebrafish. Proc Natl Acad Sci U S A 2009.
43. Spyropoulos DD, Pharr PN, Lavenburg KR, Jackers P, Papas TS, Ogawa M, Watson DK: Hemorrhage, impaired hematopoiesis, and lethality in mouse embryos carrying a targeted disruption of the Fli1 transcription factor. Mol Cell Biol 2000, 20:5643-5652.
44. Landry JR, Kinston S, Knezevic K, Donaldson IJ, Green AR, Gottgens B: Fli1, Elf1, and Ets1 regulate the proximal promoter of the LMO2 gene in endothelial cells. Blood 2005, 106:2680-2687.
45. Pimanda JE, Ottersbach K, Knezevic K, Kinston S, Chan WY, Wilson NK, Landry JR, Wood AD, Kolb-Kokocinski A, Green AR, Tannahill D, Lacaud G, Kouskoff V, Gottgens B: Gata2, Fli1, and Scl form a recursively wired gene-regulatory circuit during early hematopoietic development. Proc Natl Acad Sci U S A 2007, 104:17692-17697.
46. Liu F, Walmsley M, Rodaway A, Patient R: Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol 2008, 18:1234-1240.
47. Reddy K, Zhou Z, Schadler K, Jia SF, Kleinerman ES: Bone marrow subsets differentiate into endothelial cells and pericytes contributing to Ewing's tumor vessels. Mol Cancer Res 2008, 6:929-936.
48. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G: PDGFRbeta+ perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 2005, 7:870-879.
49. Rajantie I, Ilmonen M, Alminaite A, Ozerdem U, Alitalo K, Salven P: Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 2004, 104:2084-2086.
50. Kokovay E, Li L, Cunningham LA: Angiogenic recruitment of pericytes from bone marrow after stroke. J Cereb Blood Flow Metab 2006, 26:545-555.
51. Ozerdem U, Alitalo K, Salven P, Li A: Contribution of bone marrow-derived pericyte precursor cells to corneal vasculogenesis. Invest Ophthalmol Vis Sci 2005, 46:3502-3506.