Toddler: An embryonic signal that promotes cell movement via apelin receptors

Science

Volumn 343, Issue 6172, 2014, Pages

  Pauli, Andrea ^a   Norris, Megan L ^a   Valen, Eivind ^a   Chew, Guo Liang ^a   Gagnon, James A ^a   Zimmerman, Steven ^a   Mitchell, Andrew ^b   Ma, Jiao ^b   Dubrulle, Julien ^a   Reyon, Deepak ^c,d   Tsai, Shengdar Q ^c,d   Joung, J Keith ^c,d,e   Saghatelian, Alan ^b   Schier, Alexander F ^a,b,e,f  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APELIN; APELIN RECEPTOR; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MESSENGER RNA; MUTANT PROTEIN; NUCLEASE; PEPTIDES AND PROTEINS; TODDLER PROTEIN; UNCLASSIFIED DRUG; APELIN RECEPTOR, ZEBRAFISH; CXCL12 PROTEIN, ZEBRAFISH; STROMAL CELL DERIVED FACTOR 1; TODDLER PEPTIDE, ZEBRAFISH; ZEBRAFISH PROTEIN;

CYTOLOGY; FISH; PEPTIDE; PROTEIN; SECRETION; SIGNALING;

ADULT; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; CELL MOTION; EMBRYO; EMBRYO DEVELOPMENT; ENDODERM; FRAMESHIFT MUTATION; GAIN OF FUNCTION MUTATION; GASTRULATION; GENE INTERACTION; HEART DEVELOPMENT; IN SITU HYBRIDIZATION; INTERNALIZATION; LOSS OF FUNCTION MUTATION; MARKER GENE; MASS SPECTROMETRY; MESODERM; NONHUMAN; NOTOCHORD; OPEN READING FRAME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN SYNTHESIS; RIBOSOME; SIGNAL TRANSDUCTION; SURVIVAL; ZEBRA FISH; ANIMAL; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT;

DANIO RERIO;

AMINO ACID SEQUENCE; ANIMALS; CELL MOVEMENT; CHEMOKINE CXCL12; FRAMESHIFT MUTATION; GASTRULATION; MOLECULAR SEQUENCE DATA; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84891749518     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1248636     Document Type: Article

References (56)

1. B. Alberts, A. Johnson, J. Lewis, M. Raff, K. Roberts, P. Walter, Molecular Biology of the Cell (Garland Science, New York, ed. 5, 2007).
2. C. P. Heisenberg, Y. Bellaïche, Forces in tissue morphogenesis and patterning. Cell 153, 948-962 (2013). doi: 10.1016/j.cell.2013.05.008; pmid: 23706734
3. L. Solnica-Krezel, D. S. Sepich, Gastrulation: Making and shaping germ layers. Annu. Rev. Cell Dev. Biol. 28, 687-717 (2012). doi: 10.1146/annurev- cellbio-092910-154043; pmid: 22804578
4. J. B. Wallingford, Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 28, 627-653 (2012). doi: 10.1146/annurev-cellbio-092910-154208; pmid: 22905955
5. S. Nowotschin, A. K. Hadjantonakis, Cellular dynamics in the early mouse embryo: From axis formation to gastrulation. Curr. Opin. Genet. Dev. 20, 420-427 (2010). doi: 10.1016/j.gde.2010.05.008; pmid: 20566281
6. N. T. Ingolia, L. F. Lareau, J. S. Weissman, Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147, 789-802 (2011). doi: 10.1016/j.cell.2011.10.002; pmid: 22056041
7. G. L. Chew et al., Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs. Development 140, 2828-2834 (2013). doi: 10.1242/dev.098343; pmid: 23698349
8. A. Pauli et al., Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res. 22, 577-591 (2012). doi: 10.1101/gr.133009.111; pmid: 22110045
9. I. Ulitsky, A. Shkumatava, C. H. Jan, H. Sive, D. P. Bartel, Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147, 1537-1550 (2011). doi: 10.1016/j.cell.2011.11.055; pmid: 22196729
10. A. S. Hassan, J. Hou, W. Wei, P. A. Hoodless, Expression of two novel transcripts in the mouse definitive endoderm. Gene Expr. Patterns 10, 127-134 (2010). doi: 10.1016/j.gep.2010.02.001; pmid: 20153842
11. M. Guttman et al., lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477, 295-300 (2011). doi: 10.1038/nature10398; pmid: 21874018
12. D. Reyon et al., FLASH assembly of TALENs for high-throughput genome editing. Nat. Biotechnol. 30, 460-465 (2012). doi: 10.1038/nbt.2170; pmid: 22484455
13. J. D. Sander et al., Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat. Biotechnol. 29, 697-698 (2011). doi: 10.1038/nbt.1934; pmid: 21822241
14. T. Mizoguchi, H. Verkade, J. K. Heath, A. Kuroiwa, Y. Kikuchi, Sdf1/Cxcr4 signaling controls the dorsal migration of endodermal cells during zebrafish gastrulation. Development 135, 2521-2529 (2008). doi: 10.1242/dev.020107; pmid: 18579679
15. G. Pézeron et al., Live analysis of endodermal layer formation identifies random walk as a novel gastrulation movement. Curr. Biol. 18, 276-281 (2008). doi: 10.1016/j.cub.2008.01.028; pmid: 18291651
16. M. Doitsidou et al., Guidance of primordial germ cell migration by the chemokine SDF-1. Cell 111, 647-659 (2002). doi: 10.1016/S0092-8674(02)01135-2; pmid: 12464177
17. M. Haskel-Ittah et al., Self-organized shuttling: Generating sharp dorsoventral polarity in the early Drosophila embryo. Cell 150, 1016-1028 (2012). doi: 10.1016/j.cell.2012.06.044; pmid: 22939625
18. G. Venkiteswaran et al., Generation and dynamics of an endogenous, self-generated signaling gradient across a migrating tissue. Cell 155, 674-687 (2013). doi: 10.1016/j.cell.2013.09.046; pmid: 24119842
19. E. Donà et al., Directional tissue migration through a self-generated chemokine gradient. Nature 503, 285-289 (2013). doi: 10.1038/nature12635; pmid: 24067609
20. E. M. Powell, W. M. Mars, P. Levitt, Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30, 79-89 (2001). doi: 10.1016/S0896-6273(01)00264-1; pmid: 11343646
21. P. Giacobini et al., Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J. Neurosci. 27, 431-445 (2007). doi: 10.1523/JNEUROSCI.4979-06.2007; pmid: 17215404
22. G. Kirfel, B. Borm, A. Rigort, V. Herzog, The secretory β-amyloid precursor protein is a motogen for human epidermal keratinocytes. Eur. J. Cell Biol. 81, 664-676 (2002). doi: 10.1078/0171-9335-00284; pmid: 12553667
23. S. Nair, T. F. Schilling, Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 322, 89-92 (2008). doi: 10.1126/science.1160038; pmid: 18719251
24. X. X. I. Zeng, T. P. Wilm, D. S. Sepich, L. Solnica-Krezel, Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev. Cell 12, 391-402 (2007). doi: 10.1016/j.devcel.2007.01.011; pmid: 17336905
25. I. C. Scott et al., The G protein-coupled receptor Agtrl1b regulates early development of myocardial progenitors. Dev. Cell 12, 403-413 (2007). doi: 10.1016/j.devcel.2007.01.012; pmid: 17336906
26. i/o protein-independent pathway. Biol. Open 1, 275-285 (2012). doi: 10.1242/bio.2012380; pmid: 23213418
27. X. Li et al., Gpr125 modulates Dishevelled distribution and planar cell polarity signaling. Development 140, 3028-3039 (2013). doi: 10.1242/dev.094839; pmid: 23821037
28. 12/13 regulate epiboly by inhibiting E-cadherin activity and modulating the actin cytoskeleton. J. Cell Biol. 184, 909-921 (2009). doi: 10.1083/jcb.200805148; pmid: 19307601
29. M. Costa, E. T. Wilson, E. Wieschaus, A putative cell signal encoded by the folded gastrulation gene coordinates cell shape changes during Drosophila gastrulation. Cell 76, 1075-1089 (1994). doi: 10.1016/0092-8674(94)90384-0; pmid: 8137424
30. S. Parks, E. Wieschaus, The Drosophila gastrulation gene concertina encodes a Gα-like protein. Cell 64, 447-458 (1991). doi: 10.1016/0092-8674(91)90652-F; pmid: 1899050
31. C. D'Aniello et al., G protein-coupled receptor APJ and its ligand apelin act downstream of Cripto to specify embryonic stem cells toward the cardiac lineage through extracellular signal-regulated kinase/p70S6 kinase signaling pathway. Circulation 105, 231-238 (2009). doi: 10.1161/CIRCRESAHA.109.201186; pmid: 19574549
32. I. N. Wang et al., Apelin enhances directed cardiac differentiation of mouse and human embryonic stem cells. PLOS One 7, e38328 (2012). doi: 10.1371/journal.pone.0038328; pmid: 22675543
33. D. Tempel et al., Apelin enhances cardiac neovascularization after myocardial infarction by recruiting Aplnr+ circulating cells. Circ. Res. 111, 585-598 (2012). doi: 10.1161/CIRCRESAHA.111.262097; pmid: 22753078
34. Y. Kang et al., Apelin-APJ signaling is a critical regulator of endothelial MEF2 activation in cardiovascular development. Circ. Res. 113, 22-31 (2013). doi: 10.1161/CIRCRESAHA.113.301324; pmid: 23603510
35. M. Inui, A. Fukui, Y. Ito, M. Asashima, Xapelin and Xmsr are required for cardiovascular development in Xenopus laevis. Dev. Biol. 298, 188-200 (2006). doi: 10.1016/j.ydbio.2006.06.028; pmid: 16876154
36. D. N. Charo et al., Endogenous regulation of cardiovascular function by apelin-APJ. Am. J. Physiol. Heart Circ. Physiol. 297, H1904-H1913 (2009). doi: 10.1152/ajpheart.00686.2009; pmid: 19767528
37. K. Tatemoto et al., Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun. 251, 471-476 (1998). doi: 10.1006/bbrc.1998.9489; pmid: 9792798
38. D. K. Lee et al., Characterization of apelin, the ligand for the APJ receptor. J. Neurochem. 74, 34-41 (2000). doi: 10.1046/j.1471-4159.2000.0740034. x; pmid: 10617103
39. B. Tucker et al., Zebrafish Angiotensin II Receptor-like 1a (agtrl1a) is expressed in migrating hypoblast, vasculature, and in multiple embryonic epithelia. Gene Expr. Patterns 7, 258-265 (2007). doi: 10.1016/j.modgep.2006.09. 006; pmid: 17085078
40. S. Nornes, B. Tucker, M. Lardelli, Zebrafish aplnra functions in epiboly. BMC Res. Notes 2, 231 (2009). doi: 10.1186/1756-0500-2-231; pmid: 19922670
41. M. C. Scimia et al., APJ acts as a dual receptor in cardiac hypertrophy. Nature 488, 394-398 (2012). doi: 10.1038/nature11263; pmid: 22810587
42. J. Ishida et al., Regulatory roles for APJ, a seven-transmembrane receptor related to angiotensin-type 1 receptor in blood pressure in vivo. J. Biol. Chem. 279, 26274-26279 (2004). doi: 10.1074/jbc.M404149200; pmid: 15087458
43. E. M. Roberts et al., Abnormal fluid homeostasis in apelin receptor knockout mice. J. Endocrinol. 202, 453-462 (2009). doi: 10.1677/JOE-09-0134; pmid: 19578099
44. H. Kidoya et al., Spatial and temporal role of the apelin/APJ system in the caliber size regulation of blood vessels during angiogenesis. EMBO J. 27, 522-534 (2008). doi: 10.1038/sj.emboj.7601982; pmid: 18200044
45. K. Kuba et al., Impaired heart contractility in Apelin gene-deficient mice associated with aging and pressure overload. Circ. Res. 101, e32-e42 (2007). doi: 10.1161/CIRCRESAHA.107.158659; pmid: 17673668
46. A. Y. Sheikh et al., In vivo genetic profiling and cellular localization of apelin reveals a hypoxia-sensitive, endothelial-centered pathway activated in ischemic heart failure. Am. J. Physiol. Heart Circ. Physiol. 294, H88-H98 (2008). doi: 10.1152/ajpheart.00935.2007; pmid: 17906101
47. N. A. Evans et al., Visualizing differences in ligand-induced β-arrestin-GFP interactions and trafficking between three recently characterized G protein-coupled receptors. J. Neurochem. 77, 476-485 (2001). doi: 10.1046/j.1471-4159.2001.00269.x; pmid: 11299310
48. D. K. Lee, S. S. G. Ferguson, S. R. George, B. F. O'Dowd, The fate of the internalized apelin receptor is determined by different isoforms of apelin mediating differential interaction with β-arrestin. Biochem. Biophys. Res. Commun. 395, 185-189 (2010). doi: 10.1016/j.bbrc.2010.03.151; pmid: 20353754
49. A. Reaux et al., Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J. Neurochem. 77, 1085-1096 (2001). doi: 10.1046/j.1471-4159.2001.00320.x; pmid: 11359874
50. N. Zhou et al., Cell-cell fusion and internalization of the CNS-based, HIV-1 co-receptor, APJ. Virology 307, 22-36 (2003). doi: 10.1016/S0042-6822(02) 00021-1; pmid: 12667811
51. S. C. Chng, L. Ho, J. Tian, B. Reversade, ELABELA: A hormone essential for heart development signals via the apelin receptor. Dev. Cell 27, 672-680 (2013). doi: 10.1016/j.devcel.2013.11.002; pmid: 24316148
52. A. F. Schier, W. S. Talbot, Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 39, 561-613 (2005). doi: 10.1146/annurev.genet.37. 110801.143752; pmid: 16285872
53. G. Barnes, A. G. Japp, D. E. Newby, Translational promise of the apelin-APJ system. Heart 96, 1011-1016 (2010). doi: 10.1136/hrt.2009.191122; pmid: 20584856
54. M. J. Kleinz, A. P. Davenport, Emerging roles of apelin in biology and medicine. Pharmacol. Ther. 107, 198-211 (2005). doi: 10.1016/j.pharmthera.2005. 04.001; pmid: 15907343
55. A. Kasai et al., Retardation of retinal vascular development in apelin-deficient mice. Arterioscler. Thromb. Vasc. Biol. 28, 1717-1722 (2008). doi: 10.1161/ATVBAHA.108.163402; pmid: 18599802
56. H. Kidoya, H. Naito, N. Takakura, Apelin induces enlarged and nonleaky blood vessels for functional recovery from ischemia. Blood 115, 3166-3174 (2010). doi: 10.1182/blood-2009-07-232306; pmid: 20185589