The RNA binding protein Zfp36l1 is required for normal vascularisation and post-transcriptionally regulates VEGF expression

Developmental Dynamics

Volumn 235, Issue 11, 2006, Pages 3144-3155

  Bell, Sarah E ^a   Sanchez, Maria Jose ^b,g   Spasic Boskovic, Olivera ^c   Santalucia, Tomas ^d,h   Gambardella, Laure ^a   Burton, Graham J ^c   Murphy, John J ^e   Norton, John D ^f   Clark, Andrew R ^d   Turner, Martin ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF ESSEX   (United Kingdom)

^g UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^h INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

Extraembryonic and intraembryonic vasculature; VEGF; Zfp36l1

Indexed keywords

MESSENGER RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN A; ZFP36L1 PROTEIN; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CONGENITAL BLOOD VESSEL MALFORMATION; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; EMBRYONIC STRUCTURES; EXTRAEMBRYONIC VASCULATURE; FIBROBLAST; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE MUTATION; GENETIC TRANSCRIPTION; HYPOXIA; INTRAEMBRYONIC VASCULATURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLACENTA; POLYSOME; PRIORITY JOURNAL; RNA STABILITY; TRANSLATION REGULATION; VASCULARIZATION; ZFP36L1 GENE;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, MUTANT STRAINS; MUTATION; NEOVASCULARIZATION, PHYSIOLOGIC; NUCLEAR PROTEINS; POLYRIBOSOMES; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 33751018874     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.20949     Document Type: Article

References (54)

1. Adams RH, Porras A, Alonso G, Jones M, Vintersten K, Panelli S, Valladares A, Perez L, Klein R, Nebreda AR. 2000. Essential role of p38α MAP kinase in placental but not embryonic cardiovascular development. Mol Cell 6:109-116.
2. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, Cross JC. 2002. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 250:358-373.
3. Adelman DM, Gertsenstein M, Nagy A, Simon MC, Maltepe E. 2000. Placental cell fates are regulated in vivo by HIF-mediated hypoxia responses. Genes Dev 14:3191-3203.
4. Bakheet T, Frevel M, Williams BR, Greer W, Khabar KS. 2001. ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res 29:246-254.
5. Barak Y, Nelson MC, Ong ES, Jones YZ, Ruiz-Lozano P, Chien KR, Koder A, Evans RM. 1999. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell 4:585-595.
6. Barnard RC, Pascall JC, Brown KD, McKay IA, Williams NS, Bustin SA. 1993. Coding sequence of ERF-1, the human homologue of Tis11b/cMG1, members of the Tis11 family of early response genes. Nucleic Acids Res 21:3580.
7. Bustin SA, Nie XF, Barnard RC, Kumar V, Pascall JC, Brown KD, Leigh IM, Williams NS, McKay IA. 1994. Cloning and characterization of ERF-1, a human member of the Tis11 family of early-response genes. DNA Cell Biol 13:449-459.
8. Carballo E, Gilkeson GS, Blackshear PJ. 1997. Bone marrow transplantation reproduces the tristetraprolin-deficiency syndrome in recombination activating gene-2 (-/-) mice. Evidence that monocyte/macrophage progenitors may be responsible for TNFalpha overproduction. J Clin Invest 100:986-995.
9. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
10. Chung J, Bachelder RE, Lipscomb EA, Shaw LM, Mercurio AM. 2002. Integrin (alpha 6 beta 4) regulation of eIF-4E activity and VEGF translation: a survival mechanism for carcinoma cells. J Cell Biol 158:165-174.
11. Ciais D, Cherradi N, Bailly S, Grenier E, Berra E, Pouyssegur J, Lamarre J, Feige JJ. 2004. Destabilization of vascular endothelial growth factor mRNA by the zinc-finger protein TIS11b. Oncogene 23:8673-8680.
12. Damert A, Miquerol L, Gertsenstein M, Risau W, Nagy A. 2002. Insufficient VEGFA activity in yolk sac endoderm compromises haematopoietic and endothelial differentiation. Development 129:1881-1892.
13. Drake CJ, Little CD. 1995. Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc Natl Acad Sci USA 92:7657-7661.
14. DuBois RN, McLane MW, Ryder K, Lau LF, Nathans D. 1990. A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem 265:19185-19191.
15. Espel E. 2005. The role of the AU-rich elements of mRNAs in controlling translation. Semin Cell Dev Biol 16:59-67.
16. Ferrara N, Davis-Smyth T. 1997. The biology of vascular endothelial growth factor. Endocr Rev 18:4-25.
17. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
18. Fong GH, Rossant J, Gertsenstein M, Breitman ML. 1995. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70.
19. Godin I, Cumano A. 2002. The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol 2:593-604.
20. Gomperts M, Pascall JC, Brown KD. 1990. The nucleotide sequence of a cDNA encoding an EGF-inducible gene indicates the existence of a new family of mitogen-induced genes. Oncogene 5:1081-1083.
21. Hemberger M, Cross JC. 2001. Genes governing placental development. Trends Endocrinol Metab 12:162-168.
22. Heximer SP, Forsdyke DR. 1993. A human putative lymphocyte G0/G1 switch gene homologous to a rodent gene encoding a zinc-binding potential transcription factor. DNA Cell Biol 12:73-88.
23. Hiratsuka S, Minowa O, Kuno J, Noda T, Shibuya M. 1998. Flt-1 lacking the tyrosine kinase domain is sufficient for normal development and angiogenesis in mice. Proc Natl Acad Sci USA 95:9349-9354.
24. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL. 1998. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12:149-162.
25. Jat PS, Sharp PA. 1989. Cell lines established by a temperature-sensitive simian virus 40 large-T-antigen gene are growth restricted at the nonpermissive temperature. Mol Cell Biol 9:1672-1681.
26. Kearney JB, Kappas NC, Ellerstrom C, DiPaola FW, Bautch VL. 2004. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood 103:4527-4535.
27. Kevil CG, De Benedetti A, Payne DK, Coe LL, Laroux FS, Alexander JS. 1996. Translational regulation of vascular permeability factor by eukaryotic initiation factor 4E: implications for tumor angiogenesis. Int J Cancer 65:785-790.
28. Kozak KR, Abbott B, Hankinson O. 1997. ARNT-deficient mice and placental differentiation. Dev Biol 191:297-305.
29. Lai WS, Stumpo DJ, Blackshear PJ. 1990. Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J Biol Chem 265:16556-16563.
30. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ. 1999. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19:4311-4323.
31. Lai WS, Carballo E, Thorn JM, Kennington EA, Blackshear PJ. 2000. Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to AU-rich elements and destabilization of mRNA. J Biol Chem 275:17827-17837.
32. Lee YM, Jeong CH, Koo SY, Son MJ, Song HS, Bae SK, Raleigh JA, Chung HY, Yoo MA, Kim KW. 2001. Determination of hypoxic region by hypoxia marker in developing mouse embryos in vivo: a possible signal for vessel development. Dev Dyn 220:175-186.
33. Levy AP, Levy NS, Wegner S, Goldberg MA. 1995. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J Biol Chem 270:13333-13340.
34. Ma Q, Herschman HR. 1991. A corrected sequence for the predicted protein from the mitogen-inducible TIS11 primary response gene. Oncogene 6:1277-1278.
35. Maclean KN, See CG, McKay IA, Bustin SA. 1995. The human immediate early gene BRF1 maps to chromosome 14q22-q24. Genomics 30:89-90.
36. Maltepe E, Schmidt JV, Baunoch D, Bradfield CA, Simon MC. 1997. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature 386:403-407.
37. Mezquita P, Parghi SS, Brandvold KA, Ruddell A. 2005. Myc regulates VEGF production in B cells by stimulating initiation of VEGF mRNA translation. Oncogene 24:889-901.
38. Miquerol L, Langille BL, Nagy A. 2000. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 127:3941-3946.
39. Ning ZQ, Norton JD, Li J, Murphy JJ. 1996. Distinct mechanisms for rescue from apoptosis in Ramos human B cells by signaling through CD40 and interleukin-4 receptor: role for inhibition of an early response gene, Berg36. Eur J Immunol 26:2356-2563.
40. Ramos SB, Stumpo DJ, Kennington EA, Phillips RS, Bock CB, Ribeiro-Neto F, Blackshear PJ. 2004. The CCCH tandem zinc-finger protein Zfp3612 is crucial for female fertility and early embryonic development. Development 131:4883-4893.
41. Rigby WF, Roy K, Collins J, Rigby S, Connolly JE, Bloch DB, Brooks SA. 2005. Structure/function analysis of tristetraprolin (TTP): p38 stress-activated protein kinase and lipopolysaccharide stimulation do not alter TTP function. J Immunol 174:7883-7893.
42. Rossant J, Cross JC. 2001. Placental development: lessons from mouse mutants. Nat. Rev Genet 2:538-548.
43. Sanchez M, Gottgens B, Sinclair AM, Stanley M, Begley CG, Hunter S, Green AR. 1999. An SCL 3′ enhancer targets developing endothelium together with embryonic and adult haematopoietic progenitors. Development 126:3891-3904.
44. Sanchez MJ, Bockamp EO, Miller J, Gambardella L, Green AR. 2001. Selective rescue of early haematopoietic progenitors in Scl(-/-) mice by expressing Scl under the control of a stem cell enhancer. Development 128:4815-4827.
45. Schlaeger TM, Qin Y, Fujiwara Y, Magram J, Sato TN. 1995. Vascular endothelial cell lineage-specific promoter in transgenic mice. Development 121:1089-1098.
46. Sharpe J, Ahlgren U, Perry P, Hill B, Ross A, Hecksher-Sorensen J, Baldock R, Davidson D. 2002. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296:541-545.
47. Stoecklin G, Colombi M, Raineri I, Leuenberger S, Mallaun M, Schmidlin M, Gross B, Lu M, Kitamura T, Moroni C. 2002. Functional cloning of BRF1, a regulator of ARE-dependent mRNA turnover. EMBO J 21:4709-4718.
48. Stumpo DJ, Byrd NA, Phillips RS, Ghosh S, Maronpot RR, Castranio T, Meyers EN, Mishina Y, Blackshear PJ. 2004. Chorioallantoic fusion defects and embryonic lethality resulting from disruption of Zfp36L1, a gene encoding a CCCH tandem zinc finger protein of the Tristetraprolin family. Mol Cell Biol 24:6445-6455.
49. Taylor GA, Carballo E, Lee DM, Lai WS, Thompson MJ, Patel DD, Schenkman DI, Gilkeson GS, Broxmeyer HE, Haynes BF, Blackshear PJ. 1996. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4:445-454.
50. Tybulewicz VL, Crawford CE, Jackson PK, Bronson RT, Mulligan RC. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the ε-abl proto-oncogene. Cell 65:1153-1163.
51. Varnum BC, Lim RW, Sukbatme VP, Herschman HR. 1989. Nucleotide sequence of a cDNA encoding TIS11. a message induced in Swiss 3T3 cells by the tumor promoter tetradecanoyl phorbol acetate. Oncogene 4:119-120.
52. Varnum BC, Ma QF, Chi TH, Fletcher B, Herschman HR. 1991. The TIS11 primary response gene is a member of a gene family that encodes proteins with a highly conserved sequence containing an unusual Cys-His repeat. Mol Cell Biol 11:1754-1758.
53. Ylikorkala A, Rossi DJ, Korsisaari N, Luukko K, Alitalo K, Henkemeyer M, Makela TP. 2001. Vascular abnormalities and deregulation of VEGF in Lkb1-deficient mice. Science 293:1323-1326.
54. Zhang T, Kruys V, Huez G, Gueydan C. 2002. AU-rich element-mediated translational control: complexity and multiple activities of trans-activating factors. Biochem Soc Trans 30:952-958.