Tổng hợp axit retinoic và vai trò trong sự phát triển phôi giai đoạn đầu
Tóm tắt
Axit retinoic (RA) là một morphogen có nguồn gốc từ retinol (vitamin A) và đóng vai trò quan trọng trong sự tăng trưởng tế bào, phân hóa và hình thành cơ quan. Quá trình tổng hợp RA từ retinol yêu cầu hai phản ứng enzym liên tiếp do các loại dehydrogenase khác nhau xúc tác. Retinol đầu tiên được oxy hóa thành retinal, sau đó được oxy hóa thành RA. RA tương tác với thụ thể axit retinoic (RAR) và thụ thể axit retinoic X (RXR), từ đó điều chỉnh biểu hiện gen mục tiêu. Trong bài đánh giá này, chúng tôi đã thảo luận về chuyển hóa của RA và các thành phần quan trọng của con đường tín hiệu của RA, đồng thời nhấn mạnh hiểu biết hiện tại về các chức năng của RA trong quá trình phát triển phôi giai đoạn đầu.
Từ khóa
Tài liệu tham khảo
Tang XH, Gudas LJ: Retinoids, retinoic acid receptors, and cancer. Annu Rev Pathol. 2011, 6: 345-364. 10.1146/annurev-pathol-011110-130303
Duriancik DM, Lackey DE, Hoag KA: Vitamin A as a regulator of antigen presenting cells. J Nutr. 140 (8): 1395-1399.
Gudas LJ, Wagner JA: Retinoids regulate stem cell differentiation. J Cell Physiol. 226 (2): 322-330.
Hogarth CA, Griswold MD: The key role of vitamin A in spermatogenesis. J Clin Invest. 120 (4): 956-962.
Mora JR, Iwata M, von Andrian UH: Vitamin effects on the immune system: vitamins A and D take centre stage. Nat Rev Immunol. 2008, 8 (9): 685-698. 10.1038/nri2378
Mukherjee S, Date A, Patravale V, Korting HC, Roeder A, Weindl G: Retinoids in the treatment of skin aging: an overview of clinical efficacy and safety. Clin Interv Aging. 2006, 1 (4): 327-348. 10.2147/ciia.2006.1.4.327
Pino-Lagos K, Benson MJ, Noelle RJ: Retinoic acid in the immune system. Ann N Y Acad Sci. 2008, 1143: 170-187. 10.1196/annals.1443.017
Davies WL, Hankins MW, Foster RG: Vertebrate ancient opsin and melanopsin: divergent irradiance detectors. Photochem Photobiol Sci. 2010, 9 (11): 1444-1457. 10.1039/c0pp00203h
Penzes P, Napoli JL: Holo-cellular retinol-binding protein: distinction of ligand-binding affinity from efficiency as substrate in retinal biosynthesis. Biochemistry. 1999, 38 (7): 2088-2093. 10.1021/bi982228t
Liu L, Gudas LJ: Disruption of the lecithin:retinol acyltransferase gene makes mice more susceptible to vitamin A deficiency. J Biol Chem. 2005, 280 (48): 40226-40234. 10.1074/jbc.M509643200
Deigner PS, Law WC, Canada FJ, Rando RR: Membranes as the energy source in the endergonic transformation of vitamin A to 11-cis-retinol. Science. 1989, 244 (4907): 968-971. 10.1126/science.2727688
Mata NL, Moghrabi WN, Lee JS, Bui TV, Radu RA, Horwitz J, Travis GH: Rpe65 is a retinyl ester binding protein that presents insoluble substrate to the isomerase in retinal pigment epithelial cells. J Biol Chem. 2004, 279 (1): 635-643.
Saari JC, Nawrot M, Kennedy BN, Garwin GG, Hurley JB, Huang J, Possin DE, Crabb JW: Visual cycle impairment in cellular retinaldehyde binding protein (CRALBP) knockout mice results in delayed dark adaptation. Neuron. 2001, 29 (3): 739-748. 10.1016/S0896-6273(01)00248-3
Driessen CA, Janssen BP, Winkens HJ, van Vugt AH, de Leeuw TL, Janssen JJ: Cloning and expression of a cDNA encoding bovine retinal pigment epithelial 11-cis retinol dehydrogenase. Invest Ophthalmol Vis Sci. 1995, 36 (10): 1988-1996.
Simon A, Hellman U, Wernstedt C, Eriksson U: The retinal pigment epithelial-specific 11-cis retinol dehydrogenase belongs to the family of short chain alcohol dehydrogenases. J Biol Chem. 1995, 270 (3): 1107-1112. 10.1074/jbc.270.3.1107
Duester G: Families of retinoid dehydrogenases regulating vitamin A function: production of visual pigment and retinoic acid. Eur J Biochem. 2000, 267 (14): 4315-4324. 10.1046/j.1432-1327.2000.01497.x
Agadir A, Nau H, Blaner WS: Retinoids: the biochemical and molecular basis of Vitamin A and retinoid action. 1999, Berlin; New York Springer.
Posch KC, Enright WJ, Napoli JL: Retinoic acid synthesis by cytosol from the alcohol dehydrogenase negative deermouse. Arch Biochem Biophys. 1989, 274 (1): 171-178. 10.1016/0003-9861(89)90428-1
Noy N: Retinoid-binding proteins: mediators of retinoid action. Biochem J. 2000, 348 (Pt 3): 481-495.
Boerman MH, Napoli JL: Characterization of a microsomal retinol dehydrogenase: a short-chain alcohol dehydrogenase with integral and peripheral membrane forms that interacts with holo-CRBP (type I). Biochemistry. 1995, 34 (21): 7027-7037. 10.1021/bi00021a014
Lapshina EA, Belyaeva OV, Chumakova OV, Kedishvili NY: Differential recognition of the free versus bound retinol by human microsomal retinol/sterol dehydrogenases: characterization of the holo-CRBP dehydrogenase activity of RoDH-4. Biochemistry. 2003, 42 (3): 776-784. 10.1021/bi026836r
Belyaeva OV, Stetsenko AV, Nelson P, Kedishvili NY: Properties of short-chain dehydrogenase/reductase RalR1: characterization of purified enzyme, its orientation in the microsomal membrane, and distribution in human tissues and cell lines. Biochemistry. 2003, 42 (50): 14838-14845. 10.1021/bi035288u
Pares X, Farres J, Kedishvili N, Duester G: Medium- and short-chain dehydrogenase/reductase gene and protein families: Medium-chain and short-chain dehydrogenases/reductases in retinoid metabolism. Cell Mol Life Sci. 2008, 65 (24): 3936-3949. 10.1007/s00018-008-8591-3
Cerignoli F, Guo X, Cardinali B, Rinaldi C, Casaletto J, Frati L, Screpanti I, Gudas LJ, Gulino A, Thiele CJ: retSDR1, a short-chain retinol dehydrogenase/reductase, is retinoic acid-inducible and frequently deleted in human neuroblastoma cell lines. Cancer Res. 2002, 62 (4): 1196-1204.
Lei Z, Chen W, Zhang M, Napoli JL: Reduction of all-trans-retinal in the mouse liver peroxisome fraction by the short-chain dehydrogenase/reductase RRD: induction by the PPAR alpha ligand clofibrate. Biochemistry. 2003, 42 (14): 4190-4196. 10.1021/bi026948i
Crosas B, Hyndman DJ, Gallego O, Martras S, Pares X, Flynn TG, Farres J: Human aldose reductase and human small intestine aldose reductase are efficient retinal reductases: consequences for retinoid metabolism. Biochem J. 2003, 373 (Pt 3): 973-979.
Kasus-Jacobi A, Ou J, Bashmakov YK, Shelton JM, Richardson JA, Goldstein JL, Brown MS: Characterization of mouse short-chain aldehyde reductase (SCALD), an enzyme regulated by sterol regulatory element-binding proteins. J Biol Chem. 2003, 278 (34): 32380-32389. 10.1074/jbc.M304969200
Duester G, Mic FA, Molotkov A: Cytosolic retinoid dehydrogenases govern ubiquitous metabolism of retinol to retinaldehyde followed by tissue-specific metabolism to retinoic acid. Chem Biol Interact. 2003, 143-144: 201-210.
Haselbeck RJ, Hoffmann I, Duester G: Distinct functions for Aldh1 and Raldh2 in the control of ligand production for embryonic retinoid signaling pathways. Dev Genet. 1999, 25 (4): 353-364. 10.1002/(SICI)1520-6408(1999)25:4<353::AID-DVG9>3.0.CO;2-G
Ang HL, Duester G: Retinoic acid biosynthetic enzyme ALDH1 localizes in a subset of retinoid-dependent tissues during xenopus development. Dev Dyn. 1999, 215 (3): 264-272. 10.1002/(SICI)1097-0177(199907)215:3<264::AID-AJA8>3.0.CO;2-I
Frota-Ruchon A, Marcinkiewicz M, Bhat PV: Localization of retinal dehydrogenase type 1 in the stomach and intestine. Cell Tissue Res. 2000, 302 (3): 397-400. 10.1007/s004410000281
Ang HL, Duester G: Stimulation of premature retinoic acid synthesis in Xenopus embryos following premature expression of aldehyde dehydrogenase ALDH1. Eur J Biochem. 1999, 260 (1): 227-234. 10.1046/j.1432-1327.1999.00139.x
Fan X, Molotkov A, Manabe S, Donmoyer CM, Deltour L, Foglio MH, Cuenca AE, Blaner WS, Lipton SA, Duester G: Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina. Mol Cell Biol. 2003, 23 (13): 4637-4648. 10.1128/MCB.23.13.4637-4648.2003
Blentic A, Gale E, Maden M: Retinoic acid signalling centres in the avian embryo identified by sites of expression of synthesising and catabolising enzymes. Dev Dyn. 2003, 227 (1): 114-127. 10.1002/dvdy.10292
Chen Y, Pollet N, Niehrs C, Pieler T: Increased XRALDH2 activity has a posteriorizing effect on the central nervous system of Xenopus embryos. Mech Dev. 2001, 101 (1-2): 91-103. 10.1016/S0925-4773(00)00558-X
Niederreither K, McCaffery P, Drager UC, Chambon P, Dolle P: Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech Dev. 1997, 62 (1): 67-78. 10.1016/S0925-4773(96)00653-3
Niederreither K, Subbarayan V, Dolle P, Chambon P: Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet. 1999, 21 (4): 444-448. 10.1038/7788
Niederreither K, Vermot J, Schuhbaur B, Chambon P, Dolle P: Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development. 2000, 127 (1): 75-85.
Grandel H, Lun K, Rauch GJ, Rhinn M, Piotrowski T, Houart C, Sordino P, Kuchler AM, Schulte-Merker S, Geisler R: 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. 2002, 129 (12): 2851-2865.
Kawakami Y, Raya A, Raya RM, Rodriguez-Esteban C, Belmonte JC: Retinoic acid signalling links left-right asymmetric patterning and bilaterally symmetric somitogenesis in the zebrafish embryo. Nature. 2005, 435 (7039): 165-171. 10.1038/nature03512
Begemann G, Marx M, Mebus K, Meyer A, Bastmeyer M: Beyond the neckless phenotype: influence of reduced retinoic acid signaling on motor neuron development in the zebrafish hindbrain. Dev Biol. 2004, 271 (1): 119-129. 10.1016/j.ydbio.2004.03.033
Dobbs-McAuliffe B, Zhao Q, Linney E: Feedback mechanisms regulate retinoic acid production and degradation in the zebrafish embryo. Mech Dev. 2004, 121 (4): 339-350. 10.1016/j.mod.2004.02.008
Strate I, Min TH, Iliev D, Pera EM: Retinol dehydrogenase 10 is a feedback regulator of retinoic acid signalling during axis formation and patterning of the central nervous system. Development. 2009, 136 (3): 461-472. 10.1242/dev.024901
Koenig SF, Brentle S, Hamdi K, Fichtner D, Wedlich D, Gradl D: En2, Pax2/5 and Tcf-4 transcription factors cooperate in patterning the Xenopus brain. Dev Biol. 340 (2): 318-328.
Lupo G, Liu Y, Qiu R, Chandraratna RA, Barsacchi G, He RQ, Harris WA: Dorsoventral patterning of the Xenopus eye: a collaboration of Retinoid, Hedgehog and FGF receptor signaling. Development. 2005, 132 (7): 1737-1748. 10.1242/dev.01726
Mic FA, Molotkov A, Fan X, Cuenca AE, Duester G: RALDH3, a retinaldehyde dehydrogenase that generates retinoic acid, is expressed in the ventral retina, otic vesicle and olfactory pit during mouse development. Mech Dev. 2000, 97 (1-2): 227-230. 10.1016/S0925-4773(00)00434-2
Pittlik S, Domingues S, Meyer A, Begemann G: Expression of zebrafish aldh1a3 (raldh3) and absence of aldh1a1 in teleosts. Gene Expr Patterns. 2008, 8 (3): 141-147. 10.1016/j.gep.2007.11.003
Suzuki R, Shintani T, Sakuta H, Kato A, Ohkawara T, Osumi N, Noda M: Identification of RALDH-3, a novel retinaldehyde dehydrogenase, expressed in the ventral region of the retina. Mech Dev. 2000, 98 (1-2): 37-50. 10.1016/S0925-4773(00)00450-0
Molotkova N, Molotkov A, Duester G: Role of retinoic acid during forebrain development begins late when Raldh3 generates retinoic acid in the ventral subventricular zone. Dev Biol. 2007, 303 (2): 601-610. 10.1016/j.ydbio.2006.11.035
Dupe V, Matt N, Garnier JM, Chambon P, Mark M, Ghyselinck NB: A newborn lethal defect due to inactivation of retinaldehyde dehydrogenase type 3 is prevented by maternal retinoic acid treatment. Proc Natl Acad Sci USA. 2003, 100 (24): 14036-14041. 10.1073/pnas.2336223100
Halilagic A, Ribes V, Ghyselinck NB, Zile MH, Dolle P, Studer M: Retinoids control anterior and dorsal properties in the developing forebrain. Dev Biol. 2007, 303 (1): 362-375. 10.1016/j.ydbio.2006.11.021
Chytil F, Ong DE: Cellular retinol- and retinoic acid-binding proteins in vitamin A action. Fed Proc. 1979, 38 (11): 2510-2514.
Napoli JL, Boerman MH, Chai X, Zhai Y, Fiorella PD: Enzymes and binding proteins affecting retinoic acid concentrations. J Steroid Biochem Mol Biol. 1995, 53 (1-6): 497-502. 10.1016/0960-0760(95)00096-I
Hoegberg P, Schmidt CK, Fletcher N, Nilsson CB, Trossvik C, Gerlienke Schuur A, Brouwer A, Nau H, Ghyselinck NB, Chambon P: Retinoid status and responsiveness to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking retinoid binding protein or retinoid receptor forms. Chem Biol Interact. 2005, 156 (1): 25-39. 10.1016/j.cbi.2005.06.006
Sessler RJ, Noy N: A ligand-activated nuclear localization signal in cellular retinoic acid binding protein-II. Mol Cell. 2005, 18 (3): 343-353. 10.1016/j.molcel.2005.03.026
Stachurska E, Loboda A, Niderla-Bielinska J, Szperl M, Juszynski M, Jozkowicz A, Dulak J, Ratajska A: Expression of cellular retinoic acid-binding protein I and II (CRABP I and II) in embryonic mouse hearts treated with retinoic acid. Acta Biochim Pol. 58 (1): 19-29.
Boylan JF, Gudas LJ: The level of CRABP-I expression influences the amounts and types of all-trans-retinoic acid metabolites in F9 teratocarcinoma stem cells. J Biol Chem. 1992, 267 (30): 21486-21491.
Gu X, Xu F, Wang X, Gao X, Zhao Q: Molecular cloning and expression of a novel CYP26 gene (cyp26d1) during zebrafish early development. Gene Expr Patterns. 2005, 5 (6): 733-739. 10.1016/j.modgep.2005.04.005
Sakai Y, Luo T, McCaffery P, Hamada H, Drager UC: CYP26A1 and CYP26C1 cooperate in degrading retinoic acid within the equatorial retina during later eye development. Dev Biol. 2004, 276 (1): 143-157. 10.1016/j.ydbio.2004.08.032
Takeuchi H, Yokota A, Ohoka Y, Iwata M: Cyp26b1 regulates retinoic acid-dependent signals in T cells and its expression is inhibited by transforming growth factor-beta. PLoS One. 6 (1): e16089.
Hernandez RE, Putzke AP, Myers JP, Margaretha L, Moens CB: Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development. 2007, 134 (1): 177-187. 10.1242/dev.02706
White JA, Beckett-Jones B, Guo YD, Dilworth FJ, Bonasoro J, Jones G, Petkovich M: cDNA cloning of human retinoic acid-metabolizing enzyme (hP450RAI) identifies a novel family of cytochromes P450. J Biol Chem. 1997, 272 (30): 18538-18541. 10.1074/jbc.272.30.18538
de Roos K, Sonneveld E, Compaan B, ten Berge D, Durston AJ, van der Saag PT: Expression of retinoic acid 4-hydroxylase (CYP26) during mouse and Xenopus laevis embryogenesis. Mech Dev. 1999, 82 (1-2): 205-211. 10.1016/S0925-4773(99)00016-7
Swindell EC, Thaller C, Sockanathan S, Petkovich M, Jessell TM, Eichele G: Complementary domains of retinoic acid production and degradation in the early chick embryo. Dev Biol. 1999, 216 (1): 282-296. 10.1006/dbio.1999.9487
Giguere V, Ong ES, Segui P, Evans RM: Identification of a receptor for the morphogen retinoic acid. Nature. 1987, 330 (6149): 624-629. 10.1038/330624a0
Petkovich M, Brand NJ, Krust A, Chambon P: A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature. 1987, 330 (6147): 444-450. 10.1038/330444a0
Brand N, Petkovich M, Krust A, Chambon P, de The H, Marchio A, Tiollais P, Dejean A: Identification of a second human retinoic acid receptor. Nature. 1988, 332 (6167): 850-853. 10.1038/332850a0
Ruberte E, Dolle P, Krust A, Zelent A, Morriss-Kay G, Chambon P: Specific spatial and temporal distribution of retinoic acid receptor gamma transcripts during mouse embryogenesis. Development. 1990, 108 (2): 213-222.
Li E, Sucov HM, Lee KF, Evans RM, Jaenisch R: Normal development and growth of mice carrying a targeted disruption of the alpha 1 retinoic acid receptor gene. Proc Natl Acad Sci USA. 1993, 90 (4): 1590-1594. 10.1073/pnas.90.4.1590
Ghyselinck NB, Dupe V, Dierich A, Messaddeq N, Garnier JM, Rochette-Egly C, Chambon P, Mark M: Role of the retinoic acid receptor beta (RARbeta) during mouse development. Int J Dev Biol. 1997, 41 (3): 425-447.
Subbarayan V, Kastner P, Mark M, Dierich A, Gorry P, Chambon P: Limited specificity and large overlap of the functions of the mouse RAR gamma 1 and RAR gamma 2 isoforms. Mech Dev. 1997, 66 (1-2): 131-142. 10.1016/S0925-4773(97)00098-1
Manshouri T, Yang Y, Lin H, Stass SA, Glassman AB, Keating MJ, Albitar M: Downregulation of RAR alpha in mice by antisense transgene leads to a compensatory increase in RAR beta and RAR gamma and development of lymphoma. Blood. 1997, 89 (7): 2507-2515.
Mark M, Ghyselinck NB, Wendling O, Dupe V, Mascrez B, Kastner P, Chambon P: A genetic dissection of the retinoid signalling pathway in the mouse. Proc Nutr Soc. 1999, 58 (3): 609-613. 10.1017/S0029665199000798
Chomienne C, Balitrand N, Ballerini P, Castaigne S, de The H, Degos L: All-trans retinoic acid modulates the retinoic acid receptor-alpha in promyelocytic cells. J Clin Invest. 1991, 88 (6): 2150-2154. 10.1172/JCI115547
Kamei Y, Kawada T, Kazuki R, Sugimoto E: Retinoic acid receptor gamma 2 gene expression is up-regulated by retinoic acid in 3T3-L1 preadipocytes. Biochem J. 1993, 293 (Pt 3): 807-812.
Sucov HM, Murakami KK, Evans RM: Characterization of an autoregulated response element in the mouse retinoic acid receptor type beta gene. Proc Natl Acad Sci USA. 1990, 87 (14): 5392-5396. 10.1073/pnas.87.14.5392
Chawla A, Repa JJ, Evans RM, Mangelsdorf DJ: Nuclear receptors and lipid physiology: opening the X-files. Science. 2001, 294 (5548): 1866-1870. 10.1126/science.294.5548.1866
Kastner P, Messaddeq N, Mark M, Wendling O, Grondona JM, Ward S, Ghyselinck N, Chambon P: Vitamin A deficiency and mutations of RXRalpha, RXRbeta and RARalpha lead to early differentiation of embryonic ventricular cardiomyocytes. Development. 1997, 124 (23): 4749-4758.
Kastner P, Mark M, Leid M, Gansmuller A, Chin W, Grondona JM, Decimo D, Krezel W, Dierich A, Chambon P: Abnormal spermatogenesis in RXR beta mutant mice. Genes Dev. 1996, 10 (1): 80-92. 10.1101/gad.10.1.80
Krezel W, Dupe V, Mark M, Dierich A, Kastner P, Chambon P: RXR gamma null mice are apparently normal and compound RXR alpha +/-/RXR beta -/-/RXR gamma -/- mutant mice are viable. Proc Natl Acad Sci USA. 1996, 93 (17): 9010-9014.
Mello T, Polvani S, Galli A: Peroxisome proliferator-activated receptor and retinoic x receptor in alcoholic liver disease. PPAR Res. 2009, 2009: 748174.
Rizzo G, Renga B, Antonelli E, Passeri D, Pellicciari R, Fiorucci S: The methyl transferase PRMT1 functions as co-activator of farnesoid X receptor (FXR)/9-cis retinoid X receptor and regulates transcription of FXR responsive genes. Mol Pharmacol. 2005, 68 (2): 551-558. 10.1124/mol.105.012104
Wingert RA, Davidson AJ: The zebrafish pronephros: a model to study nephron segmentation. Kidney Int. 2008, 73 (10): 1120-1127. 10.1038/ki.2008.37
Lagu B, Pio B, Lebedev R, Yang M, Pelton PD: RXR-LXR heterodimer modulators for the potential treatment of dyslipidemia. Bioorg Med Chem Lett. 2007, 17 (12): 3497-3503. 10.1016/j.bmcl.2007.01.047
Zhao C, Dahlman-Wright K: Liver X receptor in cholesterol metabolism. J Endocrinol. 204 (3): 233-240.
Desvergne B: RXR: from partnership to leadership in metabolic regulations. Vitam Horm. 2007, 75: 1-32.
Desvergne B, Wahli W: Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr Rev. 1999, 20 (5): 649-688. 10.1210/er.20.5.649
Desvergne B, Michalik L, Wahli W: Transcriptional regulation of metabolism. Physiol Rev. 2006, 86 (2): 465-514. 10.1152/physrev.00025.2005
Hollemann T, Chen Y, Grunz H, Pieler T: Regionalized metabolic activity establishes boundaries of retinoic acid signalling. EMBO J. 1998, 17 (24): 7361-7372. 10.1093/emboj/17.24.7361
Astrom A, Pettersson U, Voorhees JJ: Structure of the human cellular retinoic acid-binding protein II gene. Early transcriptional regulation by retinoic acid. J Biol Chem. 1992, 267 (35): 25251-25255.
Durand B, Saunders M, Leroy P, Leid M, Chambon P: All-trans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell. 1992, 71 (1): 73-85. 10.1016/0092-8674(92)90267-G
Zhu J, Heyworth CM, Glasow A, Huang QH, Petrie K, Lanotte M, Benoit G, Gallagher R, Waxman S, Enver T: Lineage restriction of the RARalpha gene expression in myeloid differentiation. Blood. 2001, 98 (8): 2563-2567. 10.1182/blood.V98.8.2563
Takeyama K, Kojima R, Ohashi R, Sato T, Mano H, Masushige S, Kato S: Retinoic acid differentially up-regulates the gene expression of retinoic acid receptor alpha and gamma isoforms in embryo and adult rats. Biochem Biophys Res Commun. 1996, 222 (2): 395-400. 10.1006/bbrc.1996.0755
Halme A, Cheng M, Hariharan IK: Retinoids regulate a developmental checkpoint for tissue regeneration in Drosophila. Curr Biol. 20 (5): 458-463.
Maden M: Retinoids in nonmammalian embryos. Methods Mol Biol. 2008, 461: 541-559. 10.1007/978-1-60327-483-8_37
Uehara M, Yashiro K, Takaoka K, Yamamoto M, Hamada H: Removal of maternal retinoic acid by embryonic CYP26 is required for correct Nodal expression during early embryonic patterning. Genes Dev. 2009, 23 (14): 1689-1698. 10.1101/gad.1776209
Kudoh T, Wilson SW, Dawid IB: Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development. 2002, 129 (18): 4335-4346.
White RJ, Schilling TF: How degrading: Cyp26s in hindbrain development. Dev Dyn. 2008, 237 (10): 2775-2790. 10.1002/dvdy.21695
Kessel M, Gruss P: Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell. 1991, 67 (1): 89-104. 10.1016/0092-8674(91)90574-I
Padmanabhan R: Retinoic acid-induced caudal regression syndrome in the mouse fetus. Reprod Toxicol. 1998, 12 (2): 139-151. 10.1016/S0890-6238(97)00153-6
Durston AJ, Timmermans JP, Hage WJ, Hendriks HF, de Vries NJ, Heideveld M, Nieuwkoop PD: Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature. 1989, 340 (6229): 140-144. 10.1038/340140a0
Sive HL, Draper BW, Harland RM, Weintraub H: Identification of a retinoic acid-sensitive period during primary axis formation in Xenopus laevis. Genes Dev. 1990, 4 (6): 932-942. 10.1101/gad.4.6.932
Ruiz i Altaba A, Jessell TM: Retinoic acid modifies the pattern of cell differentiation in the central nervous system of neurula stage Xenopus embryos. Development. 1991, 112 (4): 945-958.
Chazaud C, Chambon P, Dolle P: Retinoic acid is required in the mouse embryo for left-right asymmetry determination and heart morphogenesis. Development. 1999, 126 (12): 2589-2596.
Huang S, Ma J, Liu X, Zhang Y, Luo L: Retinoic acid signaling sequentially controls visceral and heart laterality in zebrafish. J Biol Chem. 286 (32): 28533-28543.
Vermot J, Gallego Llamas J, Fraulob V, Niederreither K, Chambon P, Dolle P: Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science. 2005, 308 (5721): 563-566. 10.1126/science.1108363
Vermot J, Pourquie O: Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos. Nature. 2005, 435 (7039): 215-220. 10.1038/nature03488
Anderson DJ: Lineages and transcription factors in the specification of vertebrate primary sensory neurons. Curr Opin Neurobiol. 1999, 9 (5): 517-524. 10.1016/S0959-4388(99)00015-X
Ribes V, Stutzmann F, Bianchetti L, Guillemot F, Dolle P, Le Roux I: Combinatorial signalling controls Neurogenin2 expression at the onset of spinal neurogenesis. Dev Biol. 2008, 321 (2): 470-481. 10.1016/j.ydbio.2008.06.003
Coyle DE, Li J, Baccei M: Regional differentiation of retinoic acid-induced human pluripotent embryonic carcinoma stem cell neurons. PLoS One. 2011, 6 (1): e16174. 10.1371/journal.pone.0016174
Shan ZY, Liu F, Lei L, Li QM, Jin LH, Wu YS, Li X, Shen JL: Generation of dorsal spinal cord GABAergic neurons from mouse embryonic stem cells. Cell Reprogram. 2011, 13 (1): 85-91.
Chen N, Napoli JL: All-trans-retinoic acid stimulates translation and induces spine formation in hippocampal neurons through a membrane-associated RARalpha. FASEB J. 2008, 22 (1): 236-245.
Krumlauf R: Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet. 1993, 9 (4): 106-112. 10.1016/0168-9525(93)90203-T
Studer M, Lumsden A, Ariza-McNaughton L, Bradley A, Krumlauf R: Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature. 1996, 384 (6610): 630-634. 10.1038/384630a0
Marshall H, Nonchev S, Sham MH, Muchamore I, Lumsden A, Krumlauf R: Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature. 1992, 360 (6406): 737-741. 10.1038/360737a0
Kessel M: Reversal of axonal pathways from rhombomere 3 correlates with extra Hox expression domains. Neuron. 1993, 10 (3): 379-393. 10.1016/0896-6273(93)90328-O
Hill J, Clarke JD, Vargesson N, Jowett T, Holder N: 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. 1995, 50 (1): 3-16. 10.1016/0925-4773(94)00321-D
Hernandez RE, Rikhof HA, Bachmann R, Moens CB: vhnf1 integrates global RA patterning and local FGF signals to direct posterior hindbrain development in zebrafish. Development. 2004, 131 (18): 4511-4520. 10.1242/dev.01297
Wiellette EL, Sive H: vhnf1 and Fgf signals synergize to specify rhombomere identity in the zebrafish hindbrain. Development. 2003, 130 (16): 3821-3829. 10.1242/dev.00572
Begemann G, Meyer A: Hindbrain patterning revisited: timing and effects of retinoic acid signalling. Bioessays. 2001, 23 (11): 981-986. 10.1002/bies.1142
Gavalas A: ArRAnging the hindbrain. Trends Neurosci. 2002, 25 (2): 61-64. 10.1016/S0166-2236(02)02067-2
Dupe V, Lumsden A: Hindbrain patterning involves graded responses to retinoic acid signalling. Development. 2001, 128 (12): 2199-2208.
Begemann G, Schilling TF, Rauch GJ, Geisler R, Ingham PW: The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development. 2001, 128 (16): 3081-3094.
Partanen J: FGF signalling pathways in development of the midbrain and anterior hindbrain. J Neurochem. 2007, 101 (5): 1185-1193. 10.1111/j.1471-4159.2007.04463.x
Emoto Y, Wada H, Okamoto H, Kudo A, Imai Y: Retinoic acid-metabolizing enzyme Cyp26a1 is essential for determining territories of hindbrain and spinal cord in zebrafish. Dev Biol. 2005, 278 (2): 415-427. 10.1016/j.ydbio.2004.11.023
Chen Y, Pan FC, Brandes N, Afelik S, Solter M, Pieler T: Retinoic acid signaling is essential for pancreas development and promotes endocrine at the expense of exocrine cell differentiation in Xenopus. Dev Biol. 2004, 271 (1): 144-160. 10.1016/j.ydbio.2004.03.030
Stafford D, Hornbruch A, Mueller PR, Prince VE: A conserved role for retinoid signaling in vertebrate pancreas development. Dev Genes Evol. 2004, 214 (9): 432-441.
Martin M, Gallego-Llamas J, Ribes V, Kedinger M, Niederreither K, Chambon P, Dolle P, Gradwohl G: Dorsal pancreas agenesis in retinoic acid-deficient Raldh2 mutant mice. Dev Biol. 2005, 284 (2): 399-411. 10.1016/j.ydbio.2005.05.035
Molotkov A, Molotkova N, Duester G: Retinoic acid generated by Raldh2 in mesoderm is required for mouse dorsal endodermal pancreas development. Dev Dyn. 2005, 232 (4): 950-957. 10.1002/dvdy.20256
Pan FC, Chen Y, Bayha E, Pieler T: Retinoic acid-mediated patterning of the pre-pancreatic endoderm in Xenopus operates via direct and indirect mechanisms. Mech Dev. 2007, 124 (7-8): 518-531. 10.1016/j.mod.2007.06.003
Bayha E, Jorgensen MC, Serup P, Grapin-Botton A: Retinoic acid signaling organizes endodermal organ specification along the entire antero-posterior axis. PLoS One. 2009, 4 (6): e5845. 10.1371/journal.pone.0005845
Stafford D, Prince VE: Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development. Curr Biol. 2002, 12 (14): 1215-1220. 10.1016/S0960-9822(02)00929-6
Stafford D, White RJ, Kinkel MD, Linville A, Schilling TF, Prince VE: Retinoids signal directly to zebrafish endoderm to specify insulin-expressing beta-cells. Development. 2006, 133 (5): 949-956. 10.1242/dev.02263
Dalgin G, Ward AB, Hao le T, Beattie CE, Nechiporuk A, Prince VE: Zebrafish mnx1 controls cell fate choice in the developing endocrine pancreas. Development. 138 (21): 4597-4608.
Kinkel MD, Prince VE: On the diabetic menu: zebrafish as a model for pancreas development and function. Bioessays. 2009, 31 (2): 139-152. 10.1002/bies.200800123
Kinkel MD, Eames SC, Alonzo MR, Prince VE: Cdx4 is required in the endoderm to localize the pancreas and limit beta-cell number. Development. 2008, 135 (5): 919-929. 10.1242/dev.010660
Ostrom M, Loffler KA, Edfalk S, Selander L, Dahl U, Ricordi C, Jeon J, Correa-Medina M, Diez J, Edlund H: Retinoic acid promotes the generation of pancreatic endocrine progenitor cells and their further differentiation into beta-cells. PLoS One. 2008, 3 (7): e2841. 10.1371/journal.pone.0002841
Tulachan SS, Doi R, Kawaguchi Y, Tsuji S, Nakajima S, Masui T, Koizumi M, Toyoda E, Mori T, Ito D: All-trans retinoic acid induces differentiation of ducts and endocrine cells by mesenchymal/epithelial interactions in embryonic pancreas. Diabetes. 2003, 52 (1): 76-84. 10.2337/diabetes.52.1.76
Shen CN, Marguerie A, Chien CY, Dickson C, Slack JM, Tosh D: All-trans retinoic acid suppresses exocrine differentiation and branching morphogenesis in the embryonic pancreas. Differentiation. 2007, 75 (1): 62-74.
Moriya N, Komazaki S, Takahashi S, Yokota C, Asashima M: In vitro pancreas formation from Xenopus ectoderm treated with activin and retinoic acid. Dev Growth Differ. 2000, 42 (6): 593-602. 10.1046/j.1440-169x.2000.00542.x
Asashima M, Michiue T, Kurisaki A: Elucidation of the role of activin in organogenesis using a multiple organ induction system with amphibian and mouse undifferentiated cells in vitro. Dev Growth Differ. 2008, 50 (Suppl 1): S35-45.
Heine UI, Roberts AB, Munoz EF, Roche NS, Sporn MB: Effects of retinoid deficiency on the development of the heart and vascular system of the quail embryo. Virchows Arch B Cell Pathol Incl Mol Pathol. 1985, 50 (2): 135-152.
Lin SC, Dolle P, Ryckebusch L, Noseda M, Zaffran S, Schneider MD, Niederreither K: Endogenous retinoic acid regulates cardiac progenitor differentiation. Proc Natl Acad Sci USA. 2010, 107 (20): 9234-9239. 10.1073/pnas.0910430107
Sirbu IO, Zhao X, Duester G: Retinoic acid controls heart anteroposterior patterning by down-regulating Isl1 through the Fgf8 pathway. Dev Dyn. 2008, 237 (6): 1627-1635. 10.1002/dvdy.21570
Stachurska E, Loboda A, Niderla-Bielinska J, Szperl M, Juszynski M, Jozkowicz A, Dulak J, Ratajska A: Expression of cellular retinoic acid-binding protein I and II (CRABP I and II) in embryonic mouse hearts treated with retinoic acid. Acta Biochim Pol. 2011, 58 (1): 19-29.
Keegan BR, Feldman JL, Begemann G, Ingham PW, Yelon D: Retinoic acid signaling restricts the cardiac progenitor pool. Science. 2005, 307 (5707): 247-249. 10.1126/science.1101573
Ryckebusch L, Wang Z, Bertrand N, Lin SC, Chi X, Schwartz R, Zaffran S, Niederreither K: Retinoic acid deficiency alters second heart field formation. Proc Natl Acad Sci USA. 2008, 105 (8): 2913-2918. 10.1073/pnas.0712344105
Mathew LK, Sengupta S, Franzosa JA, Perry J, La Du J, Andreasen EA, Tanguay RL: Comparative expression profiling reveals an essential role for raldh2 in epimorphic regeneration. J Biol Chem. 2009, 284 (48): 33642-33653. 10.1074/jbc.M109.011668
Kikuchi K, Holdway JE, Major RJ, Blum N, Dahn RD, Begemann G, Poss KD: Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration. Dev Cell. 20 (3): 397-404.
Serluca FC, Fishman MC: Pre-pattern in the pronephric kidney field of zebrafish. Development. 2001, 128 (12): 2233-2241.
Cartry J, Nichane M, Ribes V, Colas A, Riou JF, Pieler T, Dolle P, Bellefroid EJ, Umbhauer M: Retinoic acid signalling is required for specification of pronephric cell fate. Dev Biol. 2006, 299 (1): 35-51. 10.1016/j.ydbio.2006.06.047
Mendelsohn C, Lohnes D, Decimo D, Lufkin T, LeMeur M, Chambon P, Mark M: Function of the retinoic acid receptors (RARs) during development (II). Multiple abnormalities at various stages of organogenesis in RAR double mutants. Development. 1994, 120 (10): 2749-2771.
Carroll TJ, Vize PD: Synergism between Pax-8 and lim-1 in embryonic kidney development. Dev Biol. 1999, 214 (1): 46-59. 10.1006/dbio.1999.9414
Lee SJ, Kim S, Choi SC, Han JK: XPteg (Xenopus proximal tubules-expressed gene) is essential for pronephric mesoderm specification and tubulogenesis. Mech Dev. 2010, 127 (1-2): 49-61. 10.1016/j.mod.2009.11.001
Bollig F, Perner B, Besenbeck B, Kothe S, Ebert C, Taudien S, Englert C: A highly conserved retinoic acid responsive element controls wt1a expression in the zebrafish pronephros. Development. 2009, 136 (17): 2883-2892. 10.1242/dev.031773
Perner B, Englert C, Bollig F: The Wilms tumor genes wt1a and wt1b control different steps during formation of the zebrafish pronephros. Dev Biol. 2007, 309 (1): 87-96. 10.1016/j.ydbio.2007.06.022
Osafune K, Nishinakamura R, Komazaki S, Asashima M: In vitro induction of the pronephric duct in Xenopus explants. Dev Growth Differ. 2002, 44 (2): 161-167. 10.1046/j.1440-169x.2002.00631.x
Wingert RA, Selleck R, Yu J, Song HD, Chen Z, Song A, Zhou Y, Thisse B, Thisse C, McMahon AP: The cdx genes and retinoic acid control the positioning and segmentation of the zebrafish pronephros. PLoS Genet. 2007, 3 (10): 1922-1938.
Rosselot C, Spraggon L, Chia I, Batourina E, Riccio P, Lu B, Niederreither K, Dolle P, Duester G, Chambon P: Non-cell-autonomous retinoid signaling is crucial for renal development. Development. 137 (2): 283-292.
Desai TJ, Malpel S, Flentke GR, Smith SM, Cardoso WV: Retinoic acid selectively regulates Fgf10 expression and maintains cell identity in the prospective lung field of the developing foregut. Dev Biol. 2004, 273 (2): 402-415. 10.1016/j.ydbio.2004.04.039
Desai TJ, Chen F, Lu J, Qian J, Niederreither K, Dolle P, Chambon P, Cardoso WV: Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev Biol. 2006, 291 (1): 12-24. 10.1016/j.ydbio.2005.10.045
Chen F, Cao Y, Qian J, Shao F, Niederreither K, Cardoso WV: A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J Clin Invest. 120 (6): 2040-2048.
Malpel S, Mendelsohn C, Cardoso WV: Regulation of retinoic acid signaling during lung morphogenesis. Development. 2000, 127 (14): 3057-3067.
Shiotsugu J, Katsuyama Y, Arima K, Baxter A, Koide T, Song J, Chandraratna RA, Blumberg B: Multiple points of interaction between retinoic acid and FGF signaling during embryonic axis formation. Development. 2004, 131 (11): 2653-2667. 10.1242/dev.01129
Ho L, Mercola M, Gudas LJ: Xenopus laevis cellular retinoic acid-binding protein: temporal and spatial expression pattern during early embryogenesis. Mech Dev. 1994, 47 (1): 53-64. 10.1016/0925-4773(94)90095-7