The retinoic acid metabolising gene, CYP26B1, patterns the cartilaginous cranial neural crest in zebrafish

International Journal of Developmental Biology

Volumn 51, Issue 5, 2007, Pages 351-360

  Reijntjes, Susan ^a   Rodaway, Adam ^a   Maden, Malcolm ^b  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cyp26B1; Jaw cartilage; Morpholino; Neural crest; RA; Retinoic acid; Zebrafish

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CYP26B1 ENZYME; CYTOCHROME P450; RETINOIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRANIAL NERVE; EMBRYO; ENZYME ACTIVITY; ENZYME METABOLISM; GENE EXPRESSION; IN SITU HYBRIDIZATION; JAW MALFORMATION; MOTONEURON; NEURAL CREST; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ZEBRA FISH;

ANIMALS; CARTILAGE; CYTOCHROME P-450 ENZYME SYSTEM; DNA, ANTISENSE; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MOTOR NEURONS; NEURAL CREST; P-AMINOAZOBENZENE; PHENOTYPE; RHOMBENCEPHALON; TRANSCRIPTION FACTORS; TRETINOIN; ZEBRAFISH;

DANIO RERIO;

EID: 34548247704     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.062258sr     Document Type: Article

References (51)

1. ABU-ABED S., DOLLE.P, METZGER D., BECKETT B., CHAMBON P. and PETKOVICH M. (2001). The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity and development of posterior structures. Genes Dev. 15: 226-240.
2. AKIMENKO M.A., EKKER M., WEGNER J., LIN W. and WESTERFIELD M. (1994). Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J. Neurosci. 14: 3475-3486.
3. ALEXANDRE D., CLARKE J.D.W., OXTOBY E., YAN Y-L., JOWETT T. and HOLDER N. (1996). Ectopic expression of Hoxa-1 in the zebrafish alters the fate of the mandibular arch neural crest and phenocopies a retinoic acid-induced phenotype. Development 122: 735-746.
4. BEGEMANN G., SCHILLING T.F, RAUCH G.J., GEISLER R. and INGHAM P.W. (2001). The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 128: 3081-3094.
5. BEGEMANN G., MARX M., MEBUS K., MEYER A. and BASTMEYER M. (2004). Beyond the neckless phenotype: influence of reduced retinoic acid signaling on motor neuron development in the zebrafish hindbrain. Dev. Biol. 271: 119-129.
6. BULFONE A., KIM H.J., PUELLES L., PORTEUS M.H., GRIPPO J.F. and RUBENSTEIN J.L. (1993). The mouse Dlx-2 (Tes-1) gene is expressed in spatially restricted domains of the forebrain, face and limbs in midgestation mouse embryos. Mech. Dev. 40: 129-140.
7. DE ROOS K., SONNEVELD E., COMPAAN B., TEN BERGE D., DURSTON A.J. and VAN DER SAAG P.T. (1999). Expression of retinoic acid 4-hydroxylase (CYP26) during mouse and Xenopus laevis embryogenesis. Mech. Dev. 82: 205-211.
8. DERSCH H. and ZILE M.H. (1993). Induction of normal cardiovascular development in the vitamin A-deprived quail embryo by natural retinoids. Dev. Biol. 160: 424-433.
9. DUPE V. and LUMSDEN A. (2001). Hindbrain patterning involves graded responses to retinoic acid signalling. Development 128: 2199-2208.
10. ELLIES D.L., LANGILLE R.M., MARTIN C.C., AKIMENKO M.A. and EKKER M. (1997). Specific craniofacial cartilage dysmorphogenesis coincides with a loss of dix gene expression in retinoic acid-treated zebrafish embryos. Mech. Dev. 61: 23-36.
11. EMOTO Y., WADA H., OKAMOTO H., KUDO A. and IMAI Y. (2005). Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev. Biol. 278: 415-427.
12. FREEMAN M.(2000). Feedback control of intercellular signalling in development. Nature 408:313-319.
13. FUJII H., SATO T., KANEKO S., GOTOH O., FUJII-KURIYAMA Y., OSAWA K., KATO S. and HAMADA H. (1997). Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. EMBO J 16: 4163-4173.
14. GAEMERS I.C., VAN PELT A.M.M., VAN DER SAAG P.T. and, DE ROOIJ D.G. (1996). All-trans-4-oxo-retinoic acid: a potent inducer of in vivo proliferation of growth-arrested A spermatogonia in the vitamin A-deficient mouse testis. Endocrinology 137: 479-486.
15. GRAHAM A. (2002). Jaw development: chinless wonders. Curr. Biol. 12: R810-R812.
16. GRANDEL H., LUN K., RAUCH G-J., RHINN M., PIOTROWSKI T., HOUART C., SORDINO P., KUCHLER A.M., SCHULTE-MERKER S., GEISLER R., HOLDER N., WILSON S.W. and BRAND, M. (2002). Retinoic acid signalling in the Zebrafish embryo is necessary during pre-segmentation stages to pattern the anterior-posterior axis of the CNS and to induce a pectoral fin bud. Development 129: 2851-2865.
17. GU X., XU F., WANG X., GAO X. and ZHAO Q. (2005). Molecular cloning and expression of a novel CYP26 gene (cyp26d1) during zebrafish early development. Gene Expr. Patt. 5: 733-739.
18. HERNANDEZ R.E., PUTZKE A.P., MYERS J.P., MARGARETHA L. and MOENS C.B. (2007). Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 134: 177-187.
19. HIGASHIJIMA S., HOTTA Y. and OKAMOTO H. (2000). Visualization of cranial motor neurons in live transgenic zebrafish expressing green fluorescent protein under the control of the islet-1 promoter/enhancer. J. Neurosci. 20: 206-218.
20. HILL J., CLARKE J.D., VARGESSON N., JOWETT T. and HOLDER N. (1995). Exogenous retinoic acid causes specific alterations in the development of the midbrain and hindbrain of the zebrafish embryo including positional respecification of the Mauthner neuron. Mech. Dev. 50: 3-16.
21. HOLLEMANN T., CHEN Y., GRUNZ H. and PIELER T. (1998). Regionalized metabolic activity establishes boundaries of retinoic acid signalling. EMBO J. 17: 7361-7372.
22. KASTNER P., CHAMBON P. and LEID M. 1(994). Role of Nuclear retinoic acid recepotors in the regulation of gene expression. In Vitamin A in Health and Disease. pp. 189-238. Marcel Dekker, New York.
23. KESSEL M. and GRUSS P. (1991 ). Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67: 89-104.
24. KLIEWER S.A., UMESONO K., EVANS R.M. and MANGELSDORF D. (1994). The retinoid X receptors: modulators of multiple hormonal signalling pathways. In Vitamin A in Health and Disease. pp. 239-256. Marcel Dekker, New York.
25. KOCHHAR D.M. (1973). Limb development in mouse embryos. Analysis of teratogenic effects of retinoic acid. Teratology 7: 289-298.
26. KOSTETSKII I., YUAN S-Y., KOSTETSKAIA E., LINASK K.K., BLANCHET S., SELEIRO E., MICHAILLE J-J,. BRICKELL P. and ZILE M. (1998). Initial retinoid requirement for early avian development coincides with retinoid receptor coexpression in the precardiac fields and induction of normal cardiovascular development. Dev. Dynam. 213: 188-198.
27. LINVILLE A., GUMUSANELI E., CHANDRARATNA R.A. and SCHILLING T.F. (2004). Independent roles for retinoic acid in segmentation and neuronal differentiation in the zebrafish hindbrain. Dev. Biol. 270: 186-199.
28. MACLEAN G., ABU-ABED S., DOLLE P., TAHAYATO A., CHAMBON P. and PETKOVICH M. (2001). Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1 and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 107: 195-201.
29. MADEN M. 2002. Retinoid signalling in the development of the central nervous system. Nature Neurosci. 3: 843-853.
30. MARSHALL H., NONCHEV S., SHAM M.H., MUCHAMORE I., LUMSDEN A. and KRUMLAUF R. (1992). Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360: 737-741.
31. MCCAFFERY P., WAGNER E., O'NEIL J.O., PETKOVICH M. and DRAGER U.C. (1999). Dorsal and ventral territories defined by retinoic acid synthesis, breakdown and nuclear receptor expression. Mech. Dev. 82: 1190130.
32. MERCADER N., LEONARDO E., PIEDRA M.E., MARTINEZ A.C., ROS M.A. and TORRES M. (2000). Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 127: 3861-3970.
33. MORRISS-KAY G. (1993). Retinoic acid and craniofacial development: molecules and morphogenesis. BioEssays 15: 9-15.
34. NIEDERREITHER K., ABU-ABEDS., SCHUBAUR B., PETKOVICH M., CHAMBON P. and DOLLE P. (2002). Genetic evidence that oxidative derivatives of retinoic acid are not involved in retinoid signalling during mouse development. Nature Genet. 31: 84-88.
35. NIKAWA T., SCHULZ W.A., VAN DEN BRINK C.E., HANUSCH M., VAN DER S.P., STAHL W. and SIES H. (1995). Efficacy of all-trans-beta-carotene, canthaxanthin and all-trans-, 9-cis- and 4-oxoretinoic acids in inducing differentiation of an F9 embryonal carcinoma RAR beta-lacZ reporter cell line. Arch. Biochem Biophys. 316: 665-672.
36. PIJNAPPEL W.W.M., HENDRICKS H.F.J., FOLKERS G.E., VAN DEN BRINK C.E., DEKKER E.J., EDELENBOSCH C., VAN DER SAAG P.T. and DURSTON A.J. (1993). The retinoid ligand 4-oxo-retinoic acid is a highly active modulator of positional specification. Nature 366: 340-344.
37. REIJNTJES S., GALE E. and MADEN M. (2003). Expression of the retinoic acid catabolising enzyme CYP26B1 in the chick embryo and its regulation by retinoic acid. Gene Expr. Patt. 3: 621-627.
38. REIJNTJES S., GALE E and MADEN M. (2004). Generating gradients of retinoic acid in the chick embryo: Cyp26C1 expression and a comparative analysis of the Cyp26 enzymes. Dev. Dynam. 230: 509-517.
39. REIJNTJES S., BLENTIC A., GALE E. and MADEN M. (2005). The control of morphogen signalling: Regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev. Biol. 285: 224-237.
40. REYNOLDS N.J., FISHER G.J., GRIFFITHS C.E., TAVAKKOL A., TALWAR H.S., ROWSE P.E., HAMILTON T.A. and VOORHEES J.J. (1993). Retinoic acid metabolites exhibit biological activity in human keratinocytes, mouse melanoma cells and hairless mouse skin in vivo. J. Pharmacol. Exp. Ther. 266: 1636-1642.
41. SAKAI Y., MENO C., FUJII H., NISHINO J., SHIRATORI H., SAIJOH Y., ROSSANT J. and HAMADA H. (2001). The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev. 15: 213-225.
42. SIRBU I.O., GRESH L., BARRA J. and DUESTER G. (2005). Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression. Development 132: 2611-2622.
43. SWINDELL E.C., THALLER C., SOCKANATHAN S., PETKOVICH M., JESSELL T.M. and EICHELE G. (1999). Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev. Biol. 216: 282-296.
44. TAHAYATO A., DOLLE P. and PETKOVICH M. (2003). Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Exp. Patt. 3: 449-454.
45. VANDERSEA M.W., FLEMING P., MCCARTHY R.A. and SMITH D.G. (1998). Fin duplications and deletions induced by disruption of retinoic acid signaling. Dev. Genes Evol. 208: 61-68.
46. WESTERFIELD M. (1995). The zebrafish Book. Guide for the Laboratory Use of Zebrafish (Danio rerio). Univ of Orgeon Press, Eugene.
47. WHITE J.A., BECKETT-JONES B., GUO Y.D., DILWORTH F.J., BONASORO J., JONES G. and PETKOVICH M. (1997). cDNA cloning of human retinoic acid-metabolizing enzyme (hP450RAI) identifies a novel family of cytochromes P450. J. Biol. Chem. 272: 18538-18541.
48. WHITE J.A., RAMSHAW H., TAIMI M., STANGLE W., ZHANG A, EVERINGHAM S., CREIGHTON S., TAM S.P., JONES G. and PETKOVICH M. (2000). Identification of the human cytochrome P450, P450RAI-2, which is predominantly expressed in the adult cerebellum and is responsible for all-trans-retinoic acid metabolism. Proc. Natl. Acad. Sci. USA 97: 6403-6408.
49. YASHIRO K., ZHAO X., UEHARA M., YAMASHITA K., NISHIJIMA M., NISHINO J., SAIJOH Y., SAKAI Y. and HAMADA H. (2004). Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Develop. Cell 6: 411-422.
50. ZHAO Q., DOBBS-MCAULIFFE B. and LINNEY E. (2005). Expression of cyp26b1 during zebrafish early development. Gene. Expr. Patt. 5: 363-369.
51. ZHANG M., KIM H-J., MARSHALL H., GENDRON-MAGUIRE M., LUCAS D.A., BARON A., GUDAS L.J., GRIDLEY.T, KRUMLAUF R and GRIPPO JF. (1994). Ectopic Hoxa-1 induces rhombomere transformation in mouse hindbrain. Development 120: 2431-2442.