A phenotypic screen in zebrafish identifies a novel small-molecule inducer of ectopic tail formation suggestive of alterations in non-canonical Wnt/PCP signaling

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Gebruers, Evelien ^a   Cordero Maldonado, María Lorena ^a,b,d   Gray, Alexander I ^c   Clements, Carol ^c   Harvey, Alan L ^c   Edrada Ebel, Ruangelie ^c   De Witte, Peter A M ^a   Crawford, Alexander D ^a,d   Esguerra, Camila V ^a  

^a DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

^b UNIVERSIDAD DE CUENCA   (Ecuador)

^c UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^d UNIVERSITY OF LUXEMBOURG   (Luxembourg)

Author keywords

[No Author keywords available]

Indexed keywords

4 COUMARIC ACID METHYL ESTER; ANISOMYCIN; ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; ANTISENSE OLIGONUCLEOTIDE; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN INHIBITOR; DORSOMORPHIN; ESTER DERIVATIVE; JASMINUM GILGIANUM EXTRACT; LDN 193189; MORPHOLINO OLIGONUCLEOTIDE; PLANT EXTRACT; PROTEIN C JUN; PROTEIN INHIBITOR; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; (6-(4-(2-PIPERIDIN-1-YLETHOXY)PHENYL))-3-PYRIDIN-4-YLPYRAZOLO(1,5-A)PYRIMIDINE; 4-COUMARIC ACID METHYL ESTER; 6 [4 (1 PIPERAZINYL)PHENYL] 3 (4 QUINOLINYL)PYRAZOLO[1,5 A]PYRIMIDINE; COUMARIC ACID; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; ZEBRAFISH PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; BMP SIGNALING PATHWAY; CONGENITAL MALFORMATION; CONTROLLED STUDY; DRUG MECHANISM; DRUG STRUCTURE; ECTOPIC TAIL FORMATION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME INHIBITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; ISOLATION PROCEDURE; JASMINUM GILGIANUM; MALE; NATIVE SPECIES; NONHUMAN; OLEACEAE; PAPUA NEW GUINEA; PCP SIGNALING PATHWAY; PHARMACOLOGICAL BLOCKING; PHENOTYPE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; TAIL; WNT SIGNALING PATHWAY; ZEBRA FISH; ANIMAL; ANIMAL EMBRYO; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; EMBRYOLOGY; JASMINE; METABOLISM;

ANIMALS; BONE MORPHOGENETIC PROTEINS; COUMARIC ACIDS; DRUG EVALUATION, PRECLINICAL; EMBRYO, NONMAMMALIAN; JASMINUM; PYRAZOLES; PYRIMIDINES; TAIL; WNT SIGNALING PATHWAY; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84892608094     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083293     Document Type: Article

References (45)

1. Bohni N, Cordero-Maldonado ML, Maes J, Siverio-Mota D, Marcourt L et al. (2013) Integration of Microfractionation, qNMR and Zebrafish Screening for the In Vivo Bioassay-Guided Isolation and Quantitative Bioactivity Analysis of Natural Products. PLOS ONE 8: e64006. doi: 10.1371/journal.pone.0064006. PubMed: 23700445.
2. Challal S, Bohni N, Buenafe OE, Esguerra CV, de Witte PA et al. (2012) Zebrafish bioassay-guided microfractionation for the rapid in vivo identification of pharmacologically active natural products. Chimia (Aarau) 66: 229-232. doi:10.2533/chimia.2012.229. PubMed: 22613156.
3. Orellana-Paucar AM, Serruys A-SK, Afrikanova T, Maes J, De Borggraeve W et al. (2012) Anticonvulsant activity of bisabolene sesquiterpenoids of Curcuma longa in zebrafish and mouse seizure models. Epilepsy Behav 24: 14-22. doi:10.1016/j.yebeh.2012.02.020. PubMed: 22483646.
4. Langdon YG, Mullins MC (2011) Maternal and zygotic control of zebrafish dorsoventral axial patterning. Annu Rev Genet 45: 357-377. doi:10.1146/annurev- genet-110410-132517. PubMed: 21942367.
5. Mullins MC, Hammerschmidt M, Kane DA, Odenthal J, Brand M et al. (1996) Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123: 81-93. PubMed: 9007231.
6. Pyati UJ, Webb AE, Kimelman D (2005) Transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132: 2333-2343. doi:10.1242/dev.01806. PubMed: 15829520.
7. Yang Y, Thorpe C (2011) BMP and non-canonical Wnt signaling are required for inhibition of secondary tail formation in zebrafish. Development 138: 2601-2611. doi:10.1242/dev.058404. PubMed: 21610036.
8. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY et al. (2008) Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 4: 33-41. doi:10.1038/nchembio.2007.54. PubMed: 18026094.
9. Hong CC, Yu PB (2009) Applications of small molecule BMP inhibitors in physiology and disease. Cytokine Growth Factor Rev 20: 409-418. doi:10.1016/j.cytogfr.2009.10.021. PubMed: 19914855.
10. Kaufman CK, White RM, Zon L (2009) Chemical genetic screening in the zebrafish embryo. Nat Protoc 4: 1422-1432. doi:10.1038/nprot.2009.144. PubMed: 19745824.
11. Zon LI, Peterson RT (2005) In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 4: 35-44. doi:10.1038/nrd1606. PubMed: 15688071.
12. Jing L, Zon LI (2011) Zebrafish as a model for normal and malignant hematopoiesis. Dis Model. Journal of Mech 4: 433-438.
13. North TE, Goessling W, Walkley CR, Lengerke C, Kopani KR et al. (2007) Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447: 1007-1011. doi:10.1038/nature05883. PubMed: 17581586.
14. Bill BR, Petzold AM, Clark KJ, Schimmenti LA, Ekker SC (2009) A primer for morpholino use in zebrafish. Zebrafish 6: 69-77. doi: 10.1089/zeb.2008.0555. PubMed: 19374550.
15. Moore FE, Reyon D, Sander JD, Martinez SA, Blackburn JS et al. (2012) Improved somatic mutagenesis in zebrafish using transcription activator-like effector nucleases (TALENs). PLOS ONE 7: e37877. doi: 10.1371/journal.pone. 0037877. PubMed: 22655075.
16. Crawford AD, Esguerra CV, de Witte PA (2008) Fishing for drugs from nature: zebrafish as a technology platform for natural product discovery. Planta Med 74: 624-632. doi:10.1055/s-2008-1034374. PubMed: 18584811.
17. Crawford AD, Liekens S, Kamuhabwa AR, Maes J, Munck S et al. (2011) Zebrafish bioassay-guided natural product discovery: isolation of angiogenesis inhibitors from East African medicinal plants. PLOS ONE 6: e14694. doi:10.1371/journal.pone.0014694. PubMed: 21379387.
18. Sieber C, Kopf J, Hiepen C, Knaus P (2009) Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev 20: 343-355. doi: 10.1016/j.cytogfr.2009.10.007. PubMed: 19897402.
19. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480. doi:10.1016/j.cell.2006.10.018. PubMed: 17081971.
20. Moon RT, Kohn AD, De Ferrari GV, Kaykas A (2004) WNT and betacatenin signalling: diseases and therapies. Nat Rev Genet 5: 691-701. doi:10.1038/nrg1427. PubMed: 15372092.
21. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310. doi:10.1002/aja.1002030302. PubMed: 8589427.
22. Thisse C, Thisse B (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3: 59-69. doi:10.1038/nprot.2007.514. PubMed: 18193022.
23. Seo J, Asaoka Y, Nagai Y, Hirayama J, Yamasaki T et al. (2010) Negative regulation of wnt11 expression by Jnk signaling during zebrafish gastrulation. J Cell Biochem 110: 1022-1037. doi:10.1002/jcb.22616. PubMed: 20564202.
24. Faris M, Kokot N, Latinis K, Kasibhatla S, Green DR et al. (1998) The c-Jun N-Terminal Kinase Cascade Plays a Role in Stress-Induced Apoptosis in Jurkat Cells by Up-Regulating Fas Ligand. Expression - J Immunol160: 134-144.
25. Agathon A, Thisse C, Thisse B (2003) The molecular nature of the zebrafish tail organizer. Nature 424: 448-452. doi:10.1038/nature01822. PubMed: 12879074.
26. Row RH, Kimelman D (2009) Bmp inhibition is necessary for post-gastrulation patterning and morphogenesis of the zebrafish tailbud. Dev Biol 329: 55-63. PubMed: 19236859.
27. Kondo M (2007) Bone morphogenetic proteins in the early development of zebrafish. FEBS J 274: 2960-2967. doi:10.1111/j.1742-4658.2007.05838.x. PubMed: 17521339.
28. Boergermann JH, Kopf J, Yu PB, Knaus P (2010) Dorsomorphin and LDN-193189 inhibit BMP-mediated Smad, p38 and Akt signalling in C2C12 cells. Int J Biochem Cell Biol 42: 1802-1807. doi:10.1016/j.biocel.2010.07.018. PubMed: 20691279.
29. Von der Hardt S, Bakkers J, Inbal A, Carvalho L, Solnica-Krezel L et al. (2007) The Bmp gradient of the zebrafish gastrula guides migrating lateral cells by regulating cell-cell adhesion. Curr Biol 17: 475-487. doi: 10.1016/j.cub.2007.02.013. PubMed: 17331724.
30. Myers DC, Sepich DS, Solnica-Krezel L (2002) Convergence and extension in vertebrate gastrulae: cell movements according to or in search of identity? Trends Genet 18: 447-455. doi:10.1016/S0168-9525(02)02725-7. PubMed: 12175805.
31. Roszko I, Sawada A, Solnica-Krezel L (2009) Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin Cell Dev Biol 20: 986-997. doi: 10.1016/j.semcdb.2009.09.004. PubMed: 19761865.
32. Kim HY, Lee SM (2012) Ferulic acid attenuates ischemia/reperfusion- induced hepatocyte apoptosis via inhibition of JNK activation. Eur J Pharm Sci 45: 708-715. doi:10.1016/j.ejps.2012.01.010. PubMed: 22326704.
33. Kang NJ, Lee KW, Shin BJ, Jung SK, Hwang MK et al. (2009) Caffeic acid, a phenolic phytochemical in coffee, directly inhibits Fyn kinase activity and UVB-induced COX-2 expression. Carcinogenesis 30: 321-330. PubMed: 19073879.
34. James RG, Conrad WH, Moon RT (2008) Beta-catenin-independent Wnt pathways: singals, core proteins and effectors. Methods Mol Biol 468: 131-144. PubMed: 19099251.
35. Bennett BL, Sasaki DT, Murray BW, O'Leary EC, Sakata ST et al. (2001) SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc Natl Acad Sci U S A 98: 13681-13686. doi:10.1073/pnas.251194298. PubMed: 11717429.
36. Sharkey J, Khong T, Spencer A (2007) PKC412 demonstrates JNK-dependent activity against human multiple myeloma cells. Blood 109: 1712-1719. doi:10.1182/blood-2006-05-014092. PubMed: 17032922.
37. Asai N, Fukuda T, Wu Z, Enomoto A, Pachnis V et al. (2006) Targeted mutation of serine 697 in the Ret tyrosine kinase causes migration defect of enteric neural crest cells. Development 133: 4507-4516. doi: 10.1242/dev.02616. PubMed: 17050626.
38. Deng Z, Sui G, Rosa PM, Zhao W (2012) Radiation-induced c-Jun activation depends on MEK1-ERK1/2 signaling pathway in microglial cells. PLOS ONE 7: e36739. doi:10.1371/journal.pone.0036739. PubMed: 22606284.
39. Nys K, Maes H, Andrei G, Snoeck R, Garmyn M et al. (2012) Skin mild hypoxia enhances killing of UVB-damaged keratinocytes through reactive oxygen species-mediated apoptosis requiring Noxa and Bim. Free Radic Biol Med 52: 1111-1120. doi:10.1016/j.freeradbiomed.2011.12.017. PubMed: 22245094.
40. Bain J, McLauchlan H, Elliott M, Cohen P (2003) The specificities of protein kinase inhibitors: an update. Biochem J 371: 199-204. doi: 10.1042/BJ20021535. PubMed: 12534346.
41. Huang QS, Zhu YJ, Li HL, Zhuang JX, Zhang CL et al. (2009) Inhibitory effects of methyl trans-cinnamate on mushroom tyrosinase and its antimicrobial activities. J Agric Food Chem 57: 2565-2569. doi: 10.1021/jf8036227. PubMed: 19231901.
42. Song K, An SM, Kim M, Koh JS, Boo YC (2011) Comparison of the antimelanogenic effects of p-coumaric acid and its methyl ester and their skin permeabilities. J Dermatol Sci 63: 17-22. doi:10.1016/j.jdermsci.2011.03.012. PubMed: 21530181.
43. Kubo I, Nihei K, Tsujimoto K (2004) Methyl p-coumarate, a melanin formation inhibitor in B16 mouse melanoma cells. Bioorg Med Chem 12: 5349-5354. doi:10.1016/j.bmc.2004.07.052. PubMed: 15388162.
44. Lenhart KF, Lin S-Y, Titus TA, Postlethwait JH, Burdine RD (2011) Two additional midline barriers function with midline lefty1 expression to maintain asymmetric Nodal signaling during left-right axis specification in zebrafish. Development 138: 4405-4410. doi:10.1242/dev.071092. PubMed: 21937597.
45. Komisarczuk AZ, Topp S, Stigloher C, Kapsimali M, Bally-Cuif L et al. (2008) Enhancer detection and developmental expression of zebrafish sprouty1, a member of the fgf8 synexpression group. Dev Dyn 237: 2594-2603. doi:10.1002/dvdy.21689. PubMed: 18729221.