MicroRNA-10 regulates the angiogenic behavior of zebrafish and human endothelial cells by promoting vascular endothelial growth factor signaling

Circulation Research

Volumn 111, Issue 11, 2012, Pages 1421-1433

  Hassel, David ^a,b,c,f   Cheng, Paul ^a,b,c   White, Mark P ^a,b,c   Ivey, Kathryn N ^a,b,c   Kroll, Jens ^d,e   Augustin, Hellmut G ^d,e   Katus, Hugo A ^f   Stainier, Didier Y R ^c,g   Srivastava, Deepak ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Roddenberry Center for Stem Cell Biology and Medicine at Gladstone   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Centre for Biomedicine and Medical Technology   (Germany)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

Author keywords

angiogenesis; developmental biology; fms related tyrosine kinase 1; microRNA; vascular endothelial growth factor

Indexed keywords

MICRORNA; MICRORNA 10; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA ANALYSIS; SIGNAL TRANSDUCTION; UMBILICAL VEIN ENDOTHELIAL CELL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BASE SEQUENCE; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; FEMALE; GENE KNOCKDOWN TECHNIQUES; GREEN FLUORESCENT PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; IMMUNOBLOTTING; LARVA; MALE; MICE; MICRORNAS; MICROSCOPY, CONFOCAL; NEOVASCULARIZATION, PHYSIOLOGIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, NUCLEIC ACID; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; ZEBRAFISH;

EID: 84870040707     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.279711     Document Type: Article

References (57)

1. Herbert SP, Stainier DY. Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol. 2011;12:551-564.
2. Shojaei F. Anti-angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett. 2012;320:130-137.
3. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439-442.
4. Carmeliet P, Ferreira V, Breier G, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 1996;380:435-439.
5. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-defcient mice. Nature. 1995;376:62-66.
6. Fong GH, Zhang L, Bryce DM, Peng J. Increased hemangioblast commitment, not vascular disorganization, is the primary defect in ft-1 knock-out mice. Development. 1999;126:3015-3025.
7. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothe-lium. Nature. 1995;376:66-70.
8. Roberts DM, Kearney JB, Johnson JH, Rosenberg MP, Kumar R, Bautch VL. The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am J Pathol. 2004;164:1531-1535.
9. Seetharam L, Gotoh N, Maru Y, Neufeld G, Yamaguchi S, Shibuya M. A unique signal transduction from FLT tyrosine kinase, a receptor for vascular endothelial growth factor VEGF. Oncogene. 1995;10:135-147.
10. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. Flt-1 lacking the tyrosine kinase domain is suffcient for normal development and angio-genesis in mice. Proc Natl Acad Sci USA. 1998;95:9349-9354.
11. Mäkinen T, Jussila L, Veikkola T, Karpanen T, Kettunen MI, Pulkkanen KJ, Kauppinen R, Jackson DG, Kubo H, Nishikawa S, Ylä-Herttuala S, Alitalo K. Inhibition of lymphangiogenesis with resulting lymphede-ma in transgenic mice expressing soluble VEGF receptor-3. Nat Med. 2001;7:199-205.
12. Karkkainen MJ, Ferrell RE, Lawrence EC, Kimak MA, Levinson KL, McTigue MA, Alitalo K, Finegold DN. Missense mutations interfere with VEGFR-3 signalling in primary lymphoedema. Nat Genet. 2000;25:153-159.
13. Hogan BM, Herpers R, Witte M, Heloterä H, Alitalo K, Duckers HJ, Schulte-Merker S. Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafsh intersegmental arteries. Development. 2009;136:4001-4009.
14. Covassin LD, Villefranc JA, Kacergis MC, Weinstein BM, Lawson ND. Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafsh. Proc Natl Acad Sci USA. 2006;103:6554-6559.
15. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438:932-936.
16. Fish JE, Srivastava D. MicroRNAs: opening a new vein in angiogenesis research. Sci Signal. 2009;2:pe1.
17. Zhao Y, Samal E, Srivastava D. Serum response factor regulates a mus-cle-specifc microRNA that targets Hand2 during cardiogenesis. Nature. 2005;436:214-220.
18. Sabatel C, Malvaux L, Bovy N, Deroanne C, Lambert V, Gonzalez ML, Colige A, Rakic JM, Noël A, Martial JA, Struman I. MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothe-lial cells. PLoS ONE. 2011;6:e16979.
19. 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.
20. 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.
21. Wang S, Aurora AB, Johnson BA, Qi X, McAnally J, Hill JA, Richardson JA, Bassel-Duby R, Olson EN. The endothelial-specifc mi-croRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261-271.
22. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682-688.
23. Fang Y, Shi C, Manduchi E, Civelek M, Davies PF. MicroRNA-10a regulation of proinfammatory phenotype in athero-susceptible endotheli-um in vivo and in vitro. Proc Natl Acad Sci USA. 2010;107:13450-13455.
24. Shen X, Fang J, Lv X, Pei Z, Wang Y, Jiang S, Ding K. Heparin impairs angiogenesis through inhibition of microRNA-10b. J Biol Chem. 2011;286:26616-26627.
25. Westerfeld M. The zebrafsh book. A guide for the laboratory use of zebrafsh (danio rerio). 3rd ed. Eugene, OR: University of Oregon Press; 1995:385.
26. Jin SW, Herzog W, Santoro MM, et al. A transgene-assisted genetic screen identifes essential regulators of vascular development in vertebrate embryos. Dev Biol. 2007;307:29-42.
27. Bussmann J, Bakkers J, Schulte-Merker S. Early endocardial morphogenesis requires Scl/Tal1. PLoS Genet. 2007;3:e140.
28. Tanzer A, Amemiya CT, Kim CB, Stadler PF. Evolution of microR-NAs located within Hox gene clusters. J Exp Zool B Mol Dev Evol. 2005;304:75-85.
29. Lim LP, Glasner ME, Yekta S, Burge CB, Bartel DP. Vertebrate microR-NA genes. Science. 2003;299:1540.
30. Kloosterman WP, Lagendijk AK, Ketting RF, Moulton JD, Plasterk RH. Targeted inhibition of miRNA maturation with morpho-linos reveals a role for miR-375 in pancreatic islet development. PLoS Biol. 2007;5:e203.
31. Woltering JM, Durston AJ. MiR-10 represses HoxB1a and HoxB3a in zebrafsh. PLoS ONE. 2008;3:e1396.
32. Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. Angiogenic network formation in the developing vertebrate trunk. Development. 2003;130:5281-5290.
33. Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A, Aqeilan R, Volinia S, Bhatt D, Alder H, Marcucci G, Calin GA, Liu CG, Bloomfeld CD, Andreeff M, Croce CM. MicroRNA fngerprints during human megakaryocytopoiesis. Proc Natl Acad Sci USA. 2006;103:5078-5083.
34. Shaw KM, Castranova DA, Pham VN, Kamei M, Kidd KR, Lo BD, Torres-Vasquez J, Ruby A, Weinstein BM. fused-somites-like mutants exhibit defects in trunk vessel patterning. Dev Dyn. 2006;235:1753-1760.
35. Schilling TF, Knight RD. Origins of anteroposterior patterning and Hox gene regulation during chordate evolution. Philos Trans R Soc Lond, B, Biol Sci. 2001;356:1599-1613.
36. van Eeden FJ, Granato M, Schach U, et al. Mutations affecting somite formation and patterning in the zebrafsh, Danio rerio. Development. 1996;123:153-164.
37. Laib AM, Bartol A, Alajati A, Korff T, Weber H, Augustin HG. Spheroid-based human endothelial cell microvessel formation in vivo. Nat Protoc. 2009;4:1202-1215.
38. Alajati A, Laib AM, Weber H, Boos AM, Bartol A, Ikenberg K, Korff T, Zentgraf H, Obodozie C, Graeser R, Christian S, Finkenzeller G, Stark GB, Héroult M, Augustin HG. Spheroid-based engineering of a human vasculature in mice. Nat Methods. 2008;5:439-445.
39. Kearney JB, Ambler CA, Monaco KA, Johnson N, Rapoport RG, Bautch VL. Vascular endothelial growth factor receptor Flt-1 negatively regulates developmental blood vessel formation by modulating endothelial cell division. Blood. 2002;99:2397-2407.
40. Lee SH, Schloss DJ, Jarvis L, Krasnow MA, Swain JL. Inhibition of angiogenesis by a mouse sprouty protein. J Biol Chem. 2001;276:4128-4133.
41. Roeckl W, Hecht D, Sztajer H, Waltenberger J, Yayon A, Weich HA. Differential binding characteristics and cellular inhibition by soluble VEGF receptors 1 and 2. Exp Cell Res. 1998;241:161-170.
42. Kappas NC, Zeng G, Chappell JC, Kearney JB, Hazarika S, Kallianos KG, Patterson C, Annex BH, Bautch VL. The VEGF receptor Flt-1 spatially modulates Flk-1 signaling and blood vessel branching. J Cell Biol. 2008;181:847-858.
43. Kearney JB, Kappas NC, Ellerstrom C, DiPaola FW, Bautch VL. The VEGF receptor ft-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood. 2004;103:4527-4535.
44. Chan J, Bayliss PE, Wood JM, Roberts TM. Dissection of angiogenic signaling in zebrafsh using a chemical genetic approach. Cancer Cell. 2002;1:257-267.
45. Zeng H, Zhao D, Mukhopadhyay D. Flt-1-mediated down-regulation of endothelial cell proliferation through pertussis toxin-sensitive G proteins, beta gamma subunits, small GTPase CDC42, and partly by Rac-1. J Biol Chem. 2002;277:4003-4009.
46. Rottbauer W, Just S, Wessels G, Trano N, Most P, Katus HA, Fishman MC. VEGF-PLCgamma1 pathway controls cardiac contractility in the embryonic heart. Genes Dev. 2005;19:1624-1634.
47. Torres-Vázquez J, Gitler AD, Fraser SD, Berk JD, Va n N Pham, Fishman MC, Childs S, Epstein JA, Weinstein BM. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev Cell. 2004;7:117-123.
48. Nicoli S, Knyphausen CP, Zhu LJ, Lakshmanan A, Lawson ND. miR-221 is required for endothelial tip cell behaviors during vascular development. Dev Cell. 2012;22:418-429.
49. Chappell JC, Taylor SM, Ferrara N, Bautch VL. Local guidance of emerging vessel sprouts requires soluble Flt-1. Dev Cell. 2009;17:377-386.
50. Krueger J, Liu D, Scholz K, Zimmer A, Shi Y, Klein C, Siekmann A, Schulte-Merker S, Cudmore M, Ahmed A, le Noble F. Flt1 acts as a negative regulator of tip cell formation and branching morphogenesis in the zebrafsh embryo. Development. 2011;138:2111-2120.
51. Myers C, Charboneau A, Cheung I, Hanks D, Boudreau N. Sustained expression of homeobox D10 inhibits angiogenesis. Am J Pathol. 2002;161:2099-2109.
52. Searle J, Mockel M, Gwosc S, et al. Heparin strongly induces soluble fms-like tyrosine kinase 1 release in vivo and in vitro-brief report. Arterioscler Thromb Vasc Biol. 2011;31:2972-2974.
53. Drewlo S, Levytska K, Sobel M, Baczyk D, Lye SJ, Kingdom JC. Heparin promotes soluble VEGF receptor expression in human pla-cental villi to impair endothelial VEGF signaling. J Thromb Haemost. 2011;9:2486-2497.
54. Zeng H, Dvorak HF, Mukhopadhyay D. Vascular permeability factor (VPF)/vascular endothelial growth factor (VEGF) peceptor-1 down-modulates VPF/VEGF receptor-2-mediated endothelial cell proliferation, but not migration, through phosphatidylinositol 3-kinase-dependent pathways. J Biol Chem. 2001;276:26969-26979.
55. Jongen-Lavrencic M, Sun SM, Dijkstra MK, Valk PJ, Löwenberg B. MicroRNA expression profling in relation to the genetic heterogeneity of acute myeloid leukemia. Blood. 2008;111:5078-5085.
56. Maynard SE, Min JY, Merchan J, Lim KH, Li J, Mondal S, Libermann TA, Morgan JP, Sellke FW, Stillman IE, Epstein FH, Sukhatme VP, Karumanchi SA. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003;111:649-658.
57. Hiratsuka S, Nakamura K, Iwai S, Murakami M, Itoh T, Kijima H, Shipley JM, Senior RM, Shibuya M. MMP9 induction by vascular endo-thelial growth factor receptor-1 is involved in lung-specifc metastasis. Cancer Cell. 2002;2:289-300.