Vitamin a in reproduction and development

Nutrients

Volumn 3, Issue 4, 2011, Pages 385-428

  Clagett Dame, Margaret ^a   Knutson, Danielle ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Embryonic; Retinoic acid; Vitamin A deficiency

Indexed keywords

CAROTENE; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOL;

BONE DEVELOPMENT; CELL DEATH; DEVELOPMENT; DIAPHRAGM; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EYE DEVELOPMENT; GAMETOGENESIS; GERM CELL; HEART DEVELOPMENT; HUMAN; KIDNEY DEVELOPMENT; LIMB DEVELOPMENT; LUNG DEVELOPMENT; MEIOSIS; NERVOUS SYSTEM DEVELOPMENT; NIDATION; NONHUMAN; ORGANOGENESIS; PANCREAS; PROTEIN FUNCTION; REPRODUCTION; RETINOL DEFICIENCY; REVIEW; SIGNAL TRANSDUCTION; SOMITE; SPERMATOGENESIS; SPINAL CORD; URINARY TRACT; VITAMIN METABOLISM; VITAMIN SUPPLEMENTATION;

MUS; RATTUS;

EID: 79953722853     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu3040385     Document Type: Review

References (297)

1. McCollum, E.V.; Davis, M. The necessity of certain lipins in the diet during growth. J. Biol. Chem. 1913, 15, 167-175.
2. Wolbach, S.B.; Howe, P.R. Tissue changes following deprivation of fat-soluble A vitamin. J. Exp. Med. 1925, 42, 753-777.
3. Evans, H.M. The effects of inadequate vitamin A on the sexual physiology of the female. J. Biol. Chem. 1928, 77, 651-654.
4. Carpenter, K.J.; Harper, A.E.; Olson, R.E. Experiments That Changed Nutritional Thinking. J. Nutr. 1997, 127, 1017S-1053S.
5. Moore, T. Vitamin A and carotene: The absence of the liver oil vitamin A from carotene. VI. The conversion of carotene to vitamin A in vivo. Biochem. J. 1930, 24, 692-702.
6. Karrer, P.; Morf, R.; Schoepp, K. Zur Kenntnis des Vitamins A in Gischtranen. Helv. Chim. Acta 1931, 14, 1431-1436.
7. Karrer, P. Carotenoids, flavins and vitamin A and B2: Nobel lecture, December 11, 1937. In Nobel Lectures, Chemistry (1922-1941); Elsevier: Amsterdam, The Netherlands, 1966; pp. 433-448.
8. Arens, J.F.; van Dorp, D.A. Synthesis of some compounds possessing vitamin A activity. Nature 1946, 157, 190-191.
9. Arens, J.F.; van Dorp, D.A. Activity of vitamin A-acid in the rat. Nature 1946, 158, 622.
10. van Dorp, D.A.; Arens, J.F. Biological activity of vitamin A acid. Nature 1946, 158, 60.
11. Dowling, J.E.; Wald, G. The biological function of vitamin A acid. Proc. Natl. Acad. Sci. USA 1960, 46, 587-608.
12. Moise, A.R.; Noy, N.; Palczewski, K.; Blaner, W.S. Delivery of retinoid-based therapies to target tissues. Biochemistry 2007, 46, 4449-4458.
13. 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, 3936-3949.
14. Duester, G. Families of retinoid dehydrogenases regulating vitamin A function: Production of visual pigment and retinoic acid. Eur. J. Biochem. 2000, 267, 4315-4324.
15. Sima, A.; Parisotto, M.; Mader, S.; Bhat, P.V. Kinetic characterization of recombinant mouse retinal dehydrogenase types 3 and 4 for retinal substrates. Biochim. Biophys. Acta 2009, 1790, 1660-1664.
16. Chambers, D.; Wilson, L.; Maden, M.; Lumsden, A. RALDH-independent generation of retinoic acid during vertebrate embryogenesis by CYP1B1. Development 2007, 134, 1369-1383.
17. White, J.A.; Beckett-Jones, B.; Guo, Y.D.; Dilworth, F.J.; 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, 18538-18541.
18. Fujii, H.; Sato, T.; Kaneko, S.; Gotoh, O.; Fujii-Kuriyama, Y.; Osawa, K.; Kato, S.; Hamada, H. Metabolic inactivation of retinoic acid by a novel P450 differentially expressed in developing mouse embryos. EMBO J. 1997, 16, 4163-4173.
19. Chithalen, J.V.; Luu, L.; Petkovich, M.; Jones, G. HPLC-MS/MS analysis of the products generated from all-trans-retinoic acid using recombinant human CYP26A. J. Lipid Res. 2002, 43, 1133-1142.
20. White, J.A.; Ramshaw, H.; Taimi, M.; Stangle, W.; Zhang, A.; Everingham, S.; Creighton, S.; Tam, S.P.; Jones, G.; Petkovich, M. 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 2000, 97, 6403-6408.
21. Tahayato, A.; Dolle, P.; Petkovich, M. Cyp26C1 encodes a novel retinoic acid-metabolizing enzyme expressed in the hindbrain, inner ear, first branchial arch and tooth buds during murine development. Gene Expr. Patterns 2003, 3, 449-454.
22. Taimi, M.; Helvig, C.; Wisniewski, J.; Ramshaw, H.; White, J.; Amad, M.; Korczak, B.; Petkovich, M. A Novel human cytochrome P450, CYP26C1, involved in metabolism of 9-cis and all-trans isomers of retinoic acid. J. Biol. Chem. 2004, 279, 77-85.
23. White, R.J.; Schilling, T.F. How degrading: Cyp26s in hindbrain development. Dev. Dyn. 2008, 237, 2775-2790.
24. D'Ambrosio, D.N.; Clugston, R.D.; Blaner, W.S. Vitamin A Metabolism: An Update. Nutrients 2011, 3, 63-103.
25. Soprano, D.R.; Blaner, W.S. Plasma Retinol-Binding Protein. In The Retinoids: Biology, Chemistry, and Medicine, 2nd ed.; Sporn, M.B., Roberts, A.B., Goodman, D.S., Eds.; Raven Press: New York, NY, USA, 1994; pp. 257-282.
26. Kawaguchi, R.; Yu, J.; Honda, J.; Hu, J.; Whitelegge, J.; Ping, P.; Wiita, P.; Bok, D.; Sun, H. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 2007, 315, 820-825.
27. Xueping, E.; Zhang, L.; Lu, J.; Tso, P.; Blaner, W.S.; Levin, M.S.; Li, E. Increased neonatal mortality in mice lacking cellular retinol-binding protein II. J. Biol. Chem. 2002, 277, 36617-36623.
28. Theodosiou, M.; Laudet, V.; Schubert, M. From carrot to clinic: an overview of the retinoic acid signaling pathway. Cell. Mol. Life Sci. 2010, 67, 1423-1445.
29. Chambon, P. A decade of molecular biology of retinoic acid receptors. FASEB J. 1996, 10, 940-954.
30. Rochette-Egly, C.; Germain, P. Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs). Nucl. Recept. Signal. 2009, 7, e005.
31. Repa, J.J.; Hanson, K.K.; Clagett-Dame, M. All-trans-retinol is a ligand for the retinoic acid receptors. Proc. Natl. Acad. Sci. USA 1993, 90, 7293-7297.
32. Mangelsdorf, D.; Umesono, K.; Evans, R.M. The Retinoid Receptors. In The Retinoids: Biology, Chemistry and Medicine, 2nd ed.; Sporn, M.B., Roberts, A.B., Goodman, D.S., Eds.; Raven Press: New York, NY, USA, 1994; pp. 319-350.
33. Knutson, D.C.; Clagett-Dame, M. at RA Regulation of NEDD9, a gene involved in neurite outgrowth and cell adhesion. Arch. Biochem. Biophys. 2008, 477, 163-174.
34. Glass, C.K.; Rosenfeld, M.G. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 2000, 14, 121-141.
35. Bastien, J.; Rochette-Egly, C. Nuclear retinoid receptors and the transcription of retinoid-target genes. Gene 2004, 328, 1-16.
36. Balmer, J.E.; Blomhoff, R. Gene expression regulation by retinoic acid. J. Lipid Res. 2002, 43, 1773-1808.
37. Blomhoff, R.; Blomhoff, H.K. Overview of retinoid metabolism and function. J. Neurobiol. 2006, 66, 606-630.
38. Mason, K.E. Differences in testis injury and repair after vitamin A-deficiency, vitamin E-deficiency, and inanition. Am. J. Anat. 1933, 52, 153-239.
39. Mitranond, V.; Sobhon, P.; Tosukhowong, P.; Chindaduangrat, W. Cytological changes in the testes of vitamin-A-deficient rats. I. Quantitation of germinal cells in the seminiferous tubules. Acta Anat. (Basel) 1979, 103, 159-168.
40. Huang, H.F.; Hembree, W.C. Spermatogenic response to vitamin A in vitamin A deficient rats. Biol. Reprod. 1979, 21, 891-904.
41. Unni, E.; Rao, M.R.; Ganguly, J. Histological & ultrastructural studies on the effect of vitamin A depletion & subsequent repletion with vitamin A on germ cells & Sertoli cells in rat testis. Indian J. Exp. Biol. 1983, 21, 180-192.
42. van Pelt, A.M.; de Rooij, D.G. Synchronization of the seminiferous epithelium after vitamin A replacement in vitamin A-deficient mice. Biol. Reprod. 1990, 43, 363-367.
43. Morales, C.; Griswold, M.D. Retinol-induced stage synchronization in seminiferous tubules of the rat. Endocrinology 1987, 121, 432-434.
44. van Pelt, A.M.; de Rooij, D.G. The origin of the synchronization of the seminiferous epithelium in vitamin A-deficient rats after vitamin A replacement. Biol. Reprod. 1990, 42, 677-682.
45. Hogarth, C.A.; Griswold, M.D. The key role of vitamin A in spermatogenesis. J. Clin. Invest. 2010, 120, 956-962.
46. Matson, C.K.; Murphy, M.W.; Griswold, M.D.; Yoshida, S.; Bardwell, V.J.; Zarkower, D. The mammalian doublesex homolog DMRT1 is a transcriptional gatekeeper that controls the mitosis versus meiosis decision in male germ cells. Dev. Cell 2010, 19, 612-624.
47. Snyder, E.M.; Small, C.; Griswold, M.D. Retinoic acid availability drives the asynchronous initiation of spermatogonial differentiation in the mouse. Biol. Reprod. 2010, 83, 783-790.
48. van Pelt, A.M.; de Rooij, D.G. Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high replicate doses support the full development of spermatogenic cells. Endocrinology 1991, 128, 697-704.
49. Vernet, N.; Dennefeld, C.; Rochette-Egly, C.; Oulad-Abdelghani, M.; Chambon, P.; Ghyselinck, N.B.; Mark, M. Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis. Endocrinology 2006, 147, 96-110.
50. Ghyselinck, N.B.; Vernet, N.; Dennefeld, C.; Giese, N.; Nau, H.; Chambon, P.; Viville, S.; Mark, M. Retinoids and spermatogenesis: lessons from mutant mice lacking the plasma retinol binding protein. Dev. Dyn. 2006, 235, 1608-1622.
51. Zhai, Y.; Sperkova, Z.; Napoli, J.L. Cellular expression of retinal dehydrogenase types 1 and 2: effects of vitamin A status on testis mRNA. J. Cell. Physiol. 2001, 186, 220-232.
52. Livera, G.; Rouiller-Fabre, V.; Pairault, C.; Levacher, C.; Habert, R. Regulation and perturbation of testicular functions by vitamin A. Reproduction 2002, 124, 173-180.
53. Lohnes, D.; Kastner, P.; Dierich, A.; Mark, M.; LeMeur, M.; Chambon, P. Function of retinoic acid receptor gamma in the mouse. Cell 1993, 73, 643-658.
54. Lufkin, T.; Lohnes, D.; Mark, M.; Dierich, A.; Gorry, P.; Gaub, M.P.; LeMeur, M.; Chambon, P. High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice. Proc. Natl. Acad. Sci. USA 1993, 90, 7225-7229.
55. Vernet, N.; Dennefeld, C.; Guillou, F.; Chambon, P.; Ghyselinck, N.B.; Mark, M. Prepubertal testis development relies on retinoic acid but not rexinoid receptors in Sertoli cells. EMBO J. 2006, 25, 5816-5825.
56. Doyle, T.J.; Braun, K.W.; McLean, D.J.; Wright, R.W.; Griswold, M.D.; Kim, K.H. Potential functions of retinoic acid receptor A in Sertoli cells and germ cells during spermatogenesis. Ann. N. Y. Acad. Sci. 2007, 1120, 114-130.
57. Chung, S.S.; Choi, C.; Wang, X.; Hallock, L.; Wolgemuth, D.J. Aberrant distribution of junctional complex components in retinoic acid receptor alpha-deficient mice. Microsc. Res. Tech. 2010, 73, 583-596.
58. Clagett-Dame, M.; DeLuca, H.F. The role of vitamin A in mammalian reproduction and embryonic development. Annu. Rev. Nutr. 2002, 22, 347-381.
59. Evans, H.M.; Bishop, K.S. On an invariable and characteristic disturbance of reproductive function in animals reared on a diet poor in fat soluble vitamine A. Anat. Rec. 1922, 23, 17-18.
60. Mason, K.E.; Ellison, E.T. Changes in the vaginal epithelium of the rat after vitamin A-deficiency. J. Nutr. 1935, 9, 735-755.
61. Warkany, J.; Schraffenberger, E. Congenital malformations induced in rats by maternal vitamin A deficiency. I. Defects of the eye. Arch. Ophthalmol. 1946, 35, 150-169.
62. Thompson, J.N.; Howell, J.M.; Pitt, G.A. Vitamin a and Reproduction in Rats. Proc. R. Soc. Lond. B Biol. Sci. 1964, 159, 510-535.
63. White, J.C.; Shankar, V.N.; Highland, M.; Epstein, M.L.; DeLuca, H.F.; Clagett-Dame, M. Defects in embryonic hindbrain development and fetal resorption resulting from vitamin A deficiency in the rat are prevented by feeding pharmacological levels of all-trans-retinoic acid. Proc. Natl. Acad. Sci. USA 1998, 95, 13459-13464.
64. White, J.C.; Highland, M.; Clagett-Dame, M. Abnormal development of the sinuatrial venous valve and posterior hindbrain may contribute to late fetal resorption of vitamin A-deficient rat embryos. Teratology 2000, 62, 374-384.
65. White, J.C.; Highland, M.; Kaiser, M.; Clagett-Dame, M. Vitamin A deficiency results in the dose-dependent acquisition of anterior character and shortening of the caudal hindbrain of the rat embryo. Dev. Biol. 2000, 220, 263-284.
66. Kaiser, M.E.; Merrill, R.A.; Stein, A.C.; Breburda, E.; Clagett-Dame, M. Vitamin A deficiency in the late gastrula stage rat embryo results in a one to two vertebral anteriorization that extends throughout the axial skeleton. Dev. Biol. 2003, 257, 14-29.
67. See, A.W.; Kaiser, M.E.; White, J.C.; Clagett-Dame, M. A nutritional model of late embryonic vitamin A deficiency produces defects in organogenesis at a high penetrance and reveals new roles for the vitamin in skeletal development. Dev. Biol. 2008, 316, 171-190.
68. Howell, J.M.; Thompson, J.N.; Pitt, G.A. Histology of the Lesions Produced in the Reproductive Tract of Animals Fed a Diet Deficient in Vitamin A Alcohol but Containing Vitamin A Acid. II. The Female Rat. J. Reprod. Fertil. 1964, 7, 251-258.
69. Noback, C.R.; Takahashi, Y.I. Micromorphology of the placenta of rats reared on marginal vitamin-A-deficient diet. Acta Anat. (Basel) 1978, 102, 195-202.
70. Koubova, J.; Menke, D.B.; Zhou, Q.; Capel, B.; Griswold, M.D.; Page, D.C. Retinoic acid regulates sex-specific timing of meiotic initiation in mice. Proc. Natl. Acad. Sci. USA 2006, 103, 2474-2479.
71. Bowles, J.; Knight, D.; Smith, C.; Wilhelm, D.; Richman, J.; Mamiya, S.; Yashiro, K.; Chawengsaksophak, K.; Wilson, M.J.; Rossant, J.; Hamada, H.; Koopman, P. Retinoid signaling determines germ cell fate in mice. Science 2006, 312, 596-600.
72. Bowles, J.; Koopman, P. Retinoic acid, meiosis and germ cell fate in mammals. Development 2007, 134, 3401-3411.
73. MacLean, G.; Li, H.; Metzger, D.; Chambon, P.; Petkovich, M. Apoptotic extinction of germ cells in testes of Cyp26b1 knockout mice. Endocrinology 2007, 148, 4560-4567.
74. Kumar, S.; Chatzi, C.; Brade, T.; Cunningham, T.J.; Zhao, X.; Duester, G. Sex-specific timing of meiotic initiation is regulated by Cyp26b1 independent of retinoic acid signalling. Nat. Commun. 2011, 2, 151.
75. Livera, G.; Rouiller-Fabre, V.; Valla, J.; Habert, R. Effects of retinoids on the meiosis in the fetal rat ovary in culture. Mol. Cell. Endocrinol. 2000, 165, 225-231.
76. Baltus, A.E.; Menke, D.B.; Hu, Y.C.; Goodheart, M.L.; Carpenter, A.E.; de Rooij, D.G.; Page, D.C. In germ cells of mouse embryonic ovaries, the decision to enter meiosis precedes premeiotic DNA replication. Nat. Genet. 2006, 38, 1430-1434.
77. Barrios, F.; Filipponi, D.; Pellegrini, M.; Paronetto, M.P.; Di Siena, S.; Geremia, R.; Rossi, P.; De Felici, M.; Jannini, E.A.; Dolci, S. Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J. Cell Sci. 2010, 123, 871-880.
78. Bowles, J.; Feng, C.W.; Spiller, C.; Davidson, T.L.; Jackson, A.; Koopman, P. FGF9 suppresses meiosis and promotes male germ cell fate in mice. Dev. Cell 2010, 19, 440-449.
79. Li, H.; Clagett-Dame, M. Vitamin A deficiency blocks the initiation of meiosis of germ cells in the developing rat ovary in vivo. Biol. Reprod. 2009, 81, 996-1001.
80. Zhao, X.; Sirbu, I.O.; Mic, F.A.; Molotkova, N.; Molotkov, A.; Kumar, S.; Duester, G. Retinoic acid promotes limb induction through effects on body axis extension but is unnecessary for limb patterning. Curr. Biol. 2009, 19, 1050-1057.
81. Bowles, J.; Feng, C.W.; Knight, D.; Smith, C.A.; Roeszler, K.N.; Bagheri-Fam, S.; Harley, V.R.; Sinclair, A.H.; Koopman, P. Male-specific expression of Aldh1a1 in mouse and chicken fetal testes: implications for retinoid balance in gonad development. Dev. Dyn. 2009, 238, 2073-2080.
82. Li, H.; MacLean, G.; Cameron, D.; Clagett-Dame, M.; Petkovich, M. Cyp26b1 expression in murine Sertoli cells is required to maintain male germ cells in an undifferentiated state during embryogenesis. PLoS ONE 2009, 4, e7501.
83. Li, H.; Palczewski, K.; Baehr, W.; Clagett-Dame, M. Vitamin A deficiency results in meiotic failure and accumulation of undifferentiated spermatogonia in prepubertal mouse testis. Biol. Reprod. 2011, 84, 336-341.
84. Zhou, Q.; Nie, R.; Li, Y.; Friel, P.; Mitchell, D.; Hess, R.A.; Small, C.; Griswold, M.D. Expression of stimulated by retinoic acid gene 8 (Stra8) in spermatogenic cells induced by retinoic acid: an in vivo study in vitamin A-sufficient postnatal murine testes. Biol. Reprod. 2008, 79, 35-42.
85. Bellve, A.R.; Millette, C.F.; Bhatnagar, Y.M.; O'Brien, D.A. Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J. Histochem. Cytochem. 1977, 25, 480-494.
86. Hale, F. Pigs born without eye balls. J. Hered. 1933, 24, 105-106.
87. Hale, F. The relation of vitamin A to anophthalmos in pigs. Am. J. Ophthalmol. 1935, 18, 1087-1093.
88. Warkany, J.; Schraffenberger, E. Congenital malformations of the eyes induced in rats by maternal vitamin A deficiency. Proc. Soc. Exp. Biol. Med. 1944, 57, 49-52.
89. Warkany, J.; Roth, C.B. Congenital malformations induced in rats by maternal vitamin A deficiency. II. Effect of varying the preparatory diet upon the yield of abnormal young. J. Nutr. 1948, 35, 1-11.
90. Warkany, J.; Roth, C.B.; Wilson, J.G. Multiple congenital malformations: a consideration of etiologic factors. Pediatrics 1948, 1, 462-471.
91. Wilson, J.G.; Warkany, J. Malformations in the genito-urinary tract induced by maternal vitamin A deficiency in the rat. Am. J. Anat. 1948, 83, 357-407.
92. Wilson, J.G.; Barch, S. Fetal death and maldevelopment resulting from maternal vitamin A deficiency in the rat. Proc. Soc. Exp. Biol. Med. 1949, 72, 687-693, illust.
93. Wilson, J.G.; Warkany, J. Aortic-arch and cardiac anomalies in the offspring of vitamin A deficient rats. Am. J. Anat. 1949, 85, 113-155.
94. Wilson, J.G.; Warkany, J. Cardiac and aortic arch anomalies in the offspring of vitamin A deficient rats correlated with similar human anomalies. Pediatrics 1950, 5, 708-725.
95. Wilson, J.G.; Roth, C.B.; Warkany, J. An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am. J. Anat. 1953, 92, 189-217.
96. Dickman, E.D.; Thaller, C.; Smith, S.M. Temporally-regulated retinoic acid depletion produces specific neural crest, ocular and nervous system defects. Development 1997, 124, 3111-3121.
97. Lohnes, D.; Mark, M.; Mendelsohn, C.; Dolle, P.; Dierich, A.; Gorry, P.; Gansmuller, A.; Chambon, P. Function of the retinoic acid receptors (RARs) during development (I). Craniofacial and skeletal abnormalities in RAR double mutants. Development 1994, 120, 2723-2748.
98. 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, 2749-2771.
99. Mark, M.; Ghyselinck, N.B.; Chambon, P. Function of retinoic acid receptors during embryonic development. Nucl. Recept. Signal. 2009, 7, e002.
100. Dolle, P. Developmental expression of retinoic acid receptors (RARs). Nucl. Recept. Signal. 2009, 7, e006.
101. Lohnes, D.; Mark, M.; Mendelsohn, C.; Dolle, P.; Decimo, D.; LeMeur, M.; Dierich, A.; Gorry, P.; Chambon, P. Developmental roles of the retinoic acid receptors. J. Steroid Biochem. Mol. Biol. 1995, 53, 475-486.
102. Mark, M.; Ghyselinck, N.B.; Chambon, P. Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 2006, 46, 451-480.
103. Warkany, J. Disturbance of embryonic development by maternal vitamin deficiencies. J. Cell. Physiol. 1954, 43, 207-236.
104. See, A.W.; Clagett-Dame, M. The temporal requirement for vitamin A in the developing eye: mechanism of action in optic fissure closure and new roles for the vitamin in regulating cell proliferation and adhesion in the embryonic retina. Dev. Biol. 2009, 325, 94-105.
105. 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, 9010-9014.
106. Mascrez, B.; Ghyselinck, N.B.; Chambon, P.; Mark, M. A transcriptionally silent RXRalpha supports early embryonic morphogenesis and heart development. Proc. Natl. Acad. Sci. USA 2009, 106, 4272-4277.
107. Mascrez, B.; Mark, M.; Dierich, A.; Ghyselinck, N.B.; Kastner, P.; Chambon, P. The RXRalpha ligand-dependent activation function 2 (AF-2) is important for mouse development. Development 1998, 125, 4691-4707.
108. Mic, F.A.; Molotkov, A.; Benbrook, D.M.; Duester, G. Retinoid activation of retinoic acid receptor but not retinoid X receptor is sufficient to rescue lethal defect in retinoic acid synthesis. Proc. Natl. Acad. Sci. USA 2003, 100, 7135-7140.
109. Morriss-Kay, G.M.; Ward, S.J. Retinoids and mammalian development. Int. Rev. Cytol. 1999, 188, 73-131.
110. Quadro, L.; Hamberger, L.; Gottesman, M.E.; Wang, F.; Colantuoni, V.; Blaner, W.S.; Mendelsohn, C.L. Pathways of vitamin A delivery to the embryo: insights from a new tunable model of embryonic vitamin A deficiency. Endocrinology 2005, 146, 4479-4490.
111. Soprano, D.R.; Soprano, K.J.; Goodman, D.S. Retinol-binding protein and transthyretin mRNA levels in visceral yolk sac and liver during fetal development in the rat. Proc. Natl. Acad. Sci. USA 1986, 83, 7330-7334.
112. Sapin, V.; Ward, S.J.; Bronner, S.; Chambon, P.; Dolle, P. Differential expression of transcripts encoding retinoid binding proteins and retinoic acid receptors during placentation of the mouse. Dev. Dyn. 1997, 208, 199-210.
113. Quadro, L.; Hamberger, L.; Gottesman, M.E.; Colantuoni, V.; Ramakrishnan, R.; Blaner, W.S. Transplacental delivery of retinoid: the role of retinol-binding protein and lipoprotein retinyl ester. Am. J. Physiol. Endocrinol. Metab 2004, 286, E844-E851.
114. Bavik, C.; Ward, S.J.; Chambon, P. Developmental abnormalities in cultured mouse embryos deprived of retinoic by inhibition of yolk-sac retinol binding protein synthesis. Proc. Natl. Acad. Sci. USA 1996, 93, 3110-3114.
115. Farese, R.V., Jr.; Cases, S.; Ruland, S.L.; Kayden, H.J.; Wong, J.S.; Young, S.G.; Hamilton, R.L. A novel function for apolipoprotein B: lipoprotein synthesis in the yolk sac is critical for maternal-fetal lipid transport in mice. J. Lipid Res. 1996, 37, 347-360.
116. Sapin, V.; Chaib, S.; Blanchon, L.; Alexandre-Gouabau, M.C.; Lemery, D.; Charbonne, F.; Gallot, D.; Jacquetin, B.; Dastugue, B.; Azais-Braesco, V. Esterification of vitamin A by the human placenta involves villous mesenchymal fibroblasts. Pediatr. Res. 2000, 48, 565-572.
117. Kochhar, D.M. Teratogenic activity of retinoic acid. Acta Pathol. Microbiol. Scand. 1967, 70, 398-404.
118. Conlon, R.A. Retinoic acid and pattern formation in vertebrates. Trends Genet. 1995, 11, 314-319.
119. Shenefelt, R.E. Morphogenesis of malformations in hamsters caused by retinoic acid: relation to dose and stage at treatment. Teratology 1972, 5, 103-118.
120. Collins, M.D.; Mao, G.E. Teratology of retinoids. Annu. Rev. Pharmacol. Toxicol. 1999, 39, 399-430.
121. Reijntjes, S.; Blentic, A.; Gale, E.; Maden, M. The control of morphogen signalling: regulation of the synthesis and catabolism of retinoic acid in the developing embryo. Dev. Biol. 2005, 285, 224-237.
122. Sandell, L.L.; Sanderson, B.W.; Moiseyev, G.; Johnson, T.; Mushegian, A.; Young, K.; Rey, J.P.; Ma, J.X.; Staehling-Hampton, K.; Trainor, P.A. RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development. Genes Dev. 2007, 21, 1113-1124.
123. Niederreither, K.; Subbarayan, V.; Dolle, P.; Chambon, P. Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat. Genet. 1999, 21, 444-448.
124. Reijntjes, S.; Zile, M.H.; Maden, M. The expression of Stra6 and Rdh10 in the avian embryo and their contribution to the generation of retinoid signatures. Int. J. Dev. Biol. 2010, 54, 1267-1275.
125. Strate, I.; Min, T.H.; Iliev, D.; Pera, E.M. Retinol dehydrogenase 10 is a feedback regulator of retinoic acid signalling during axis formation and patterning of the central nervous system. Development 2009, 136, 461-472.
126. Ang, H.L.; Deltour, L.; Hayamizu, T.F.; Zgombic-Knight, M.; Duester, G. Retinoic acid synthesis in mouse embryos during gastrulation and craniofacial development linked to class IV alcohol dehydrogenase gene expression. J. Biol. Chem. 1996, 271, 9526-9534.
127. Ang, H.L.; Deltour, L.; Zgombic-Knight, M.; Wagner, M.A.; Duester, G. Expression patterns of class I and class IV alcohol dehydrogenase genes in developing epithelia suggest a role for alcohol dehydrogenase in local retinoic acid synthesis. Alcohol. Clin. Exp. Res. 1996, 20, 1050-1064.
128. Molotkov, A.; Deltour, L.; Foglio, M.H.; Cuenca, A.E.; Duester, G. Distinct retinoid metabolic functions for alcohol dehydrogenase genes Adh1 and Adh4 in protection against vitamin A toxicity or deficiency revealed in double null mutant mice. J. Biol. Chem. 2002, 277, 13804-13811.
129. Molotkov, A.; Fan, X.; Deltour, L.; Foglio, M.H.; Martras, S.; Farres, J.; Pares, X.; Duester, G. Stimulation of retinoic acid production and growth by ubiquitously expressed alcohol dehydrogenase Adh3. Proc. Natl. Acad. Sci. USA 2002, 99, 5337-5342.
130. Mic, F.A.; Haselbeck, R.J.; Cuenca, A.E.; Duester, G. Novel retinoic acid generating activities in the neural tube and heart identified by conditional rescue of Raldh2 null mutant mice. Development 2002, 129, 2271-2282.
131. Dupe, V.; Matt, N.; Garnier, J.M.; Chambon, P.; Mark, M.; Ghyselinck, N.B. 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, 14036-14041.
132. Mic, F.A.; Molotkov, A.; Molotkova, N.; Duester, G. Raldh2 expression in optic vesicle generates a retinoic acid signal needed for invagination of retina during optic cup formation. Dev. Dyn. 2004, 231, 270-277.
133. Fan, X.; Molotkov, A.; Manabe, S.; Donmoyer, C.M.; Deltour, L.; Foglio, M.H.; Cuenca, A.E.; Blaner, W.S.; Lipton, S.A.; Duester, G. Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina. Mol. Cell. Biochem. 2003, 23, 4637-4648.
134. Matt, N.; Dupe, V.; Garnier, J.M.; Dennefeld, C.; Chambon, P.; Mark, M.; Ghyselinck, N.B. Retinoic acid-dependent eye morphogenesis is orchestrated by neural crest cells. Development 2005, 132, 4789-4800.
135. Molotkov, A.; Molotkova, N.; Duester, G. Retinoic acid guides eye morphogenetic movements via paracrine signaling but is unnecessary for retinal dorsoventral patterning. Development 2006, 133, 1901-1910.
136. Duester, G. Retinoic acid synthesis and signaling during early organogenesis. Cell 2008, 134, 921-931.
137. Buters, J.T.; Sakai, S.; Richter, T.; Pineau, T.; Alexander, D.L.; Savas, U.; Doehmer, J.; Ward, J.M.; Jefcoate, C.R.; Gonzalez, F.J. Cytochrome P450 CYP1B1 determines susceptibility to 7,12-dimethylbenz[a]anthracene-induced lymphomas. Proc. Natl. Acad. Sci. USA 1999, 96, 1977-1982.
138. Feng, L.; Hernandez, R.E.; Waxman, J.S.; Yelon, D.; Moens, C.B. Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanism. Dev. Biol. 2010, 338, 1-14.
139. Abu-Abed, S.; Dolle, P.; Metzger, D.; Beckett, B.; Chambon, P.; Petkovich, M. The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev. 2001, 15, 226-240.
140. Sakai, Y.; Meno, C.; Fujii, H.; Nishino, J.; Shiratori, H.; Saijoh, Y.; Rossant, J.; Hamada, H. 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. 2001, 15, 213-225.
141. Pennimpede, T.; Cameron, D.A.; Maclean, G.A.; Li, H.; Abu-Abed, S.; Petkovich, M. The role of CYP26 enzymes in defining appropriate retinoic acid exposure during embryogenesis. Birth Defects Res. A Clin. Mol. Teratol. 2010, 88, 883-894.
142. Yashiro, K.; Zhao, X.; Uehara, M.; Yamashita, K.; Nishijima, M.; Nishino, J.; Saijoh, Y.; Sakai, Y.; Hamada, H. Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev. Cell 2004, 6, 411-422.
143. MacLean, G.; Dolle, P.; Petkovich, M. Genetic disruption of CYP26B1 severely affects development of neural crest derived head structures, but does not compromise hindbrain patterning. Dev. Dyn. 2009, 238, 732-745.
144. Uehara, M.; Yashiro, K.; Mamiya, S.; Nishino, J.; Chambon, P.; Dolle, P.; Sakai, Y. CYP26A1 and CYP26C1 cooperatively regulate anterior-posterior patterning of the developing brain and the production of migratory cranial neural crest cells in the mouse. Dev. Biol. 2007, 302, 399-411.
145. 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, 1689-1698.
146. Ulven, S.M.; Gundersen, T.E.; Weedon, M.S.; Landaas, V.O.; Sakhi, A.K.; Fromm, S.H.; Geronimo, B.A.; Moskaug, J.O.; Blomhoff, R. Identification of endogenous retinoids, enzymes, binding proteins, and receptors during early postimplantation development in mouse: important role of retinal dehydrogenase type 2 in synthesis of all-trans-retinoic acid. Dev. Biol. 2000, 220, 379-391.
147. Rossant, J.; Zirngibl, R.; Cado, D.; Shago, M.; Giguere, V. Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 1991, 5, 1333-1344.
148. Niederreither, K.; McCaffery, P.; Drager, U.C.; 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, 67-78.
149. Ribes, V.; Le Roux, I.; Rhinn, M.; Schuhbaur, B.; Dolle, P. Early mouse caudal development relies on crosstalk between retinoic acid, Shh and Fgf signalling pathways. Development 2009, 136, 665-676.
150. Lai, L.; Bohnsack, B.L.; Niederreither, K.; Hirschi, K.K. Retinoic acid regulates endothelial cell proliferation during vasculogenesis. Development 2003, 130, 6465-6474.
151. Bohnsack, B.L.; Hirschi, K.K. Red light, green light: signals that control endothelial cell proliferation during embryonic vascular development. Cell Cycle 2004, 3, 1506-1511.
152. Bohnsack, B.L.; Lai, L.; Dolle, P.; Hirschi, K.K. Signaling hierarchy downstream of retinoic acid that independently regulates vascular remodeling and endothelial cell proliferation. Genes Dev. 2004, 18, 1345-1358.
153. Satre, M.A.; Kochhar, D.M. Elevations in the endogenous levels of the putative morphogen retinoic acid in embryonic mouse limb-buds associated with limb dysmorphogenesis. Dev. Biol. 1989, 133, 529-536.
154. Horton, C.; Maden, M. Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev. Dyn. 1995, 202, 312-323.
155. Scott, W.J., Jr.; Walter, R.; Tzimas, G.; Sass, J.O.; Nau, H.; Collins, M.D. Endogenous status of retinoids and their cytosolic binding proteins in limb buds of chick vs. mouse embryos. Dev. Biol. 1994, 165, 397-409.
156. Vermot, J.; Fraulob, V.; Dolle, P.; Niederreither, K. Expression of enzymes synthesizing (aldehyde dehydrogenase 1 and reinaldehyde dehydrogenase 2) and metabolizaing (Cyp26) retinoic acid in the mouse female reproductive system. Endocrinology 2000, 141, 3638-3645.
157. Clagett-Dame, M.; McNeill, E.M.; Muley, P.D. Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. J. Neurobiol. 2006, 66, 739-756.
158. Maden, M. Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 2007, 8, 755-765.
159. Glover, J.C.; Renaud, J.S.; Rijli, F.M. Retinoic acid and hindbrain patterning. J. Neurobiol. 2006, 66, 705-725.
160. Maden, M. Retinoids and spinal cord development. J. Neurobiol. 2006, 66, 726-738.
161. Gavalas, A.; Krumlauf, R. Retinoid signalling and hindbrain patterning. Curr. Opin. Genet. Dev. 2000, 10, 380-386.
162. Maden, M.; Gale, E.; Kostetskii, I.; Zile, M. Vitamin A-deficient quail embryos have half a hindbrain and other neural defects. Curr. Biol. 1996, 6, 417-426.
163. Niederreither, K.; Vermot, J.; Schuhbaur, B.; Chambon, P.; Dolle, P. Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 2000, 127, 75-85.
164. Begemann, G.; Schilling, T.F.; Rauch, G.J.; Geisler, R.; Ingham, P.W. The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 2001, 128, 3081-3094.
165. 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.; Brand, M. 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, 2851-2865.
166. Wendling, O.; Ghyselinck, N.B.; Chambon, P.; Mark, M. Roles of retinoic acid receptors in early embryonic morphogenesis and hindbrain patterning. Development 2001, 128, 2031-2038.
167. Dupe, V.; Ghyselinck, N.B.; Wendling, O.; Chambon, P.; Mark, M. Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 1999, 126, 5051-5059.
168. Linville, A.; Radtke, K.; Waxman, J.S.; Yelon, D.; Schilling, T.F. Combinatorial roles for zebrafish retinoic acid receptors in the hindbrain, limbs and pharyngeal arches. Dev. Biol. 2009, 325, 60-70.
169. Dupe, V.; Lumsden, A. Hindbrain patterning involves graded responses to retinoic acid signalling. Development 2001, 128, 2199-2208.
170. Sirbu, I.O.; Duester, G. Retinoic-acid signalling in node ectoderm and posterior neural plate directs left-right patterning of somitic mesoderm. Nat. Cell Biol. 2006, 8, 271-277.
171. MacLean, G.; Abu-Abed, S.; Dolle, P.; Tahayato, A.; Chambon, P.; Petkovich, M. Cloning of a novel retinoic-acid metabolizing cytochrome P450, Cyp26B1, and comparative expression analysis with Cyp26A1 during early murine development. Mech. Dev. 2001, 107, 195-201.
172. Sirbu, I.O.; Gresh, L.; Barra, J.; Duester, G. Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression. Development 2005, 132, 2611-2622.
173. Hernandez, R.E.; Putzke, A.P.; Myers, J.P.; Margaretha, L.; Moens, C.B. Cyp26 enzymes generate the retinoic acid response pattern necessary for hindbrain development. Development 2007, 134, 177-187.
174. Ribes, V.; Fraulob, V.; Petkovich, M.; Dolle, P. The oxidizing enzyme CYP26a1 tightly regulates the availability of retinoic acid in the gastrulating mouse embryo to ensure proper head development and vasculogenesis. Dev. Dyn. 2007, 236, 644-653.
175. Koide, T.; Downes, M.; Chandraratna, R.A.; Blumberg, B.; Umesono, K. Active repression of RAR signaling is required for head formation. Genes Dev. 2001, 15, 2111-2121.
176. Schneider, R.A.; Hu, D.; Rubenstein, J.L.; Maden, M.; Helms, J.A. Local retinoid signaling coordinates forebrain and facial morphogenesis by maintaining FGF8 and SHH. Development 2001, 128, 2755-2767.
177. Halilagic, A.; Zile, M.H.; Studer, M. A novel role for retinoids in patterning the avian forebrain during presomite stages. Development 2003, 130, 2039-2050.
178. Halilagic, A.; Ribes, V.; Ghyselinck, N.B.; Zile, M.H.; Dolle, P.; Studer, M. Retinoids control anterior and dorsal properties in the developing forebrain. Dev. Biol. 2007, 303, 362-375.
179. Marklund, M.; Sjodal, M.; Beehler, B.C.; Jessell, T.M.; Edlund, T.; Gunhaga, L. Retinoic acid signalling specifies intermediate character in the developing telencephalon. Development 2004, 131, 4323-4332.
180. 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, 601-610.
181. Luo, T.; Wagner, E.; Drager, U.C. Integrating retinoic acid signaling with brain function. Dev. Psychol. 2009, 45, 139-150.
182. Zhang, J.; Smith, D.; Yamamoto, M.; Ma, L.; McCaffery, P. The meninges is a source of retinoic acid for the late-developing hindbrain. J. Neurosci. 2003, 23, 7610-7620.
183. Yamamoto, M.; Fujinuma, M.; Hirano, S.; Hayakawa, Y.; Clagett-Dame, M.; Zhang, J.; McCaffery, P. Retinoic acid influences the development of the inferior olivary nucleus in the rodent. Dev. Biol. 2005, 280, 421-433.
184. Smith, D.; Wagner, E.; Koul, O.; McCaffery, P.; Drager, U.C. Retinoic acid synthesis for the developing telencephalon. Cereb. Cortex 2001, 11, 894-905.
185. Siegenthaler, J.A.; Ashique, A.M.; Zarbalis, K.; Patterson, K.P.; Hecht, J.H.; Kane, M.A.; Folias, A.E.; Choe, Y.; May, S.R.; Kume, T.; Napoli, J.L.; Peterson, A.S.; Pleasure, S.J. Retinoic acid from the meninges regulates cortical neuron generation. Cell 2009, 139, 597-609.
186. Wilson, V.; Olivera-Martinez, I.; Storey, K.G. Stem cells, signals and vertebrate body axis extension. Development 2009, 136, 1591-1604.
187. Molotkova, N.; Molotkov, A.; Sirbu, I.O.; Duester, G. Requirement of mesodermal retinoic acid generated by Raldh2 for posterior neural transformation. Mech. Dev. 2005, 122, 145-155.
188. Diez del Corral, R.; Olivera-Martinez, I.; Goriely, A.; Gale, E.; Maden, M.; Storey, K. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 2003, 40, 65-79.
189. Diez del Corral, R.; Storey, K.G. Opposing FGF and retinoid pathways: a signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 2004, 26, 857-869.
190. Pierani, A.; Brenner-Morton, S.; Chiang, C.; Jessell, T.M. A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 1999, 97, 903-915.
191. Novitch, B.G.; Wichterle, H.; Jessell, T.M.; Sockanathan, S. A requirement for retinoic acid-mediated transcriptional activation in ventral neural patterning and motor neuron specification. Neuron 2003, 40, 81-95.
192. Sockanathan, S.; Perlmann, T.; Jessell, T.M. Retinoid receptor signaling in postmitotic motor neurons regulates rostrocaudal positional identity and axonal projection pattern. Neuron 2003, 40, 97-111.
193. Vermot, J.; Schuhbaur, B.; Le Mouellic, H.; McCaffery, P.; Garnier, J.M.; Hentsch, D.; Brulet, P.; Niederreither, K.; Chambon, P.; Dolle, P.; Le Roux, I. Retinaldehyde dehydrogenase 2 and Hoxc8 are required in the murine brachial spinal cord for the specification of Lim1+ motoneurons and the correct distribution of Islet1+ motoneurons. Development 2005, 132, 1611-1621.
194. Misra, M.; Shah, V.; Carpenter, E.; McCaffery, P.; Lance-Jones, C. Restricted patterns of Hoxd10 and Hoxd11 set segmental differences in motoneuron subtype complement in the lumbosacral spinal cord. Dev. Biol. 2009, 330, 54-72.
195. Rodriguez-Tebar, A.; Rohrer, H. Retinoic acid induces NGF-dependent survival response and high-affinity NGF receptors in immature chick sympathetic neurons. Development 1991, 112, 813-820.
196. Plum, L.A.; Clagett-Dame, M. All-trans retinoic acid stimulates and maintains neurite outgrowth in nerve growth factor-supported developing chick embryonic sympathetic neurons. Dev. Biol. 1996, 205, 52-63.
197. Plum, L.A.; Parada, L.F.; Tsoulfas, P.; Clagett-Dame, M. Retinoic acid combined with neurotrophin-3 enhances the survival and neurite outgrowth of embryonic sympathetic neurons. Exp. Biol. Med. 2001, 226, 766-775.
198. Merrill, R.A.; Plum, L.A.; Kaiser, M.E.; Clagett-Dame, M. A mammalian homolog of unc-53 is regulated by all-trans retinoic acid in neuroblastoma cells and embryos. Proc. Natl. Acad. Sci. USA 2002, 99, 3422-3427.
199. Merrill, R.A.; Ahrens, J.M.; Kaiser, M.E.; Federhart, K.S.; Poon, V.Y.; Clagett-Dame, M. All-trans retinoic acid-responsive genes identified in the human SH-SY5Y neuroblastoma cell line and their regulated expression in the nervous system of early embryos. Biol. Chem. 2004, 385, 605-614.
200. Merrill, R.A.; See, A.W.; Wertheim, M.L.; Clagett-Dame, M. Crk-associated substrate (Cas) family member, NEDD9, is regulated in human neuroblastoma cells and in the embryonic hindbrain by all-trans retinoic acid. Dev. Dyn. 2004, 231, 564-575.
201. Muley, P.D.; McNeill, E.M.; Marzinke, M.A.; Knobel, K.M.; Barr, M.M.; Clagett-Dame, M. The atRA-responsive gene neuron navigator 2 functions in neurite outgrowth and axonal elongation. Dev. Neurobiol. 2008, 68, 1441-1453.
202. McNeill, E.M.; Roos, K.P.; Moechars, D.; Clagett-Dame, M. Nav2 is necessary for cranial nerve development and blood pressure regulation. Neural Dev. 2010, 5, 6.
203. Wagner, E.; McCaffery, P.; Drager, U.C. Retinoic acid in the formation of the dorsoventral retina and its central projections. Dev. Biol. 2000, 222, 460-470.
204. Drager, U.C.; Li, H.; Wagner, E.; McCaffery, P. Retinoic acid synthesis and breakdown in the developing mouse retina. Prog. Brain Res. 2001, 131, 579-587.
205. Mic, F.A.; Molotkov, A.; Fan, X.; Cuenca, A.E.; 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, 227-230.
206. Li, H.; Wagner, E.; McCaffery, P.; Smith, D.; Andreadis, A.; Drager, U.C. A retinoic acid synthesizing enzyme in ventral retina and telencephalon of the embryonic mouse. Mech. Dev. 2000, 95, 283-289.
207. McCaffery, P.; Tempst, P.; Lara, G.; Drager, U.C. Aldehyde dehydrogenase is a positional marker in the retina. Development 1991, 112, 693-702.
208. Mori, M.; Ghyselinck, N.B.; Chambon, P.; Mark, M. Systematic immunolocalization of retinoid receptors in developing and adult mouse eyes. Invest. Ophthalmol. Vis. Sci. 2001, 42, 1312-1318.
209. Ghyselinck, N.B.; Dupe, V.; Dierich, A.; Messaddeq, N.; Garnier, J.M.; Rochette-Egly, C.; Chambon, P.; Mark, M. Role of the retinoic acid receptor beta (RARbeta) during mouse development. Int. J. Dev. Biol. 1997, 41, 425-447.
210. Kastner, P.; Grondona, J.M.; Mark, M.; Gansmuller, A.; LeMeur, M.; Decimo, D.; Vonesch, J.L.; Dolle, P.; Chambon, P. Genetic analysis of RXR alpha developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 1994, 78, 987-1003.
211. Kastner, P.; Mark, M.; Ghyselinck, N.; Krezel, W.; Dupe, V.; Grondona, J.M.; Chambon, P. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 1997, 124, 313-326.
212. Matt, N.; Ghyselinck, N.B.; Pellerin, I.; Dupe, V. Impairing retinoic acid signalling in the neural crest cells is sufficient to alter entire eye morphogenesis. Dev. Biol. 2008, 320, 140-148.
213. Cammas, L.; Trensz, F.; Jellali, A.; Ghyselinck, N.B.; Roux, M.J.; Dolle, P. Retinoic acid receptor (RAR)-alpha is not critically required for mediating retinoic acid effects in the developing mouse retina. Invest. Ophthalmol. Vis. Sci. 2010, 51, 3281-3290.
214. Kumar, S.; Duester, G. Retinoic acid signaling in perioptic mesenchyme represses Wnt signaling via induction of Pitx2 and Dkk2. Dev. Biol. 2010, 340, 67-74.
215. Gage, P.J.; Suh, H.; Camper, S.A. Dosage requirement of Pitx2 for development of multiple organs. Development 1999, 126, 4643-4651.
216. Zacharias, A.L.; Gage, P.J. Canonical Wnt/beta-catenin signaling is required for maintenance but not activation of Pitx2 expression in neural crest during eye development. Dev. Dyn. 2010, 239, 3215-3225.
217. Aulehla, A.; Pourquie, O. Signaling gradients during paraxial mesoderm development. Cold Spring Harb. Perspect. Biol. 2010, 2, a000869.
218. Dubrulle, J.; McGrew, M.J.; Pourquie, O. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 2001, 106, 219-232.
219. Sawada, A.; Shinya, M.; Jiang, Y.J.; Kawakami, A.; Kuroiwa, A.; Takeda, H. Fgf/MAPK signalling is a crucial positional cue in somite boundary formation. Development 2001, 128, 4873-4880.
220. Tenin, G.; Wright, D.; Ferjentsik, Z.; Bone, R.; McGrew, M.J.; Maroto, M. The chick somitogenesis oscillator is arrested before all paraxial mesoderm is segmented into somites. BMC Dev. Biol. 2010, 10, 24.
221. Kieny, M.; Mauger, A.; Sengel, P. Early regionalization of somitic mesoderm as studied by the development of axial skeleton of the chick embryo. Dev. Biol. 1972, 28, 142-161.
222. Gruss, P.; Kessel, M. Axial specification in higher vertebrates. Curr. Opin. Genet. Dev. 1991, 1, 204-210.
223. Kessel, M. Respecification of vertebral identities by retinoic acid. Development 1992, 115, 487-501.
224. Kessel, M.; Gruss, P. Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 1991, 67, 89-104.
225. Marshall, H.; Nonchev, S.; Sham, M.H.; 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, 737-741.
226. Hall, B.K.; Horstadius, S. The Neural Crest; Oxford University Press: New York, NY, USA, 1988; pp. 1-303.
227. Dupe, V.; Pellerin, I. Retinoic acid receptors exhibit cell-autonomous functions in cranial neural crest cells. Dev. Dyn. 2009, 238, 2701-2711.
228. Dersch, H.; Zile, M.H. Induction of normal cardiovascular development in the vitamin A-deprived quail embryo by natural retinoids. Dev. Biol. 1993, 160, 424-433.
229. Zile, M.H. Vitamin A-Not for Your Eyes Only: Requirement for Heart Formation Begins Early in Embryogenesis. Nutrients 2010, 2, 532-550.
230. Niederreither, K.; Vermot, J.; Messaddeq, N.; Schuhbaur, B.; Chambon, P.; Dolle, P. Embryonic retinoic acid synthesis is essential for heart morphogenesis in the mouse. Development 2001, 128, 1019-1031.
231. Wagner, M.; Siddiqui, M.A. Signal transduction in early heart development (II): ventricular chamber specification, trabeculation, and heart valve formation. Exp. Biol. Med. (Maywood) 2007, 232, 866-880.
232. Hoover, L.L.; Burton, E.G.; Brooks, B.A.; Kubalak, S.W. The expanding role for retinoid signaling in heart development. Sci. World J. 2008, 8, 194-211.
233. Lin, S.C.; Dolle, P.; Ryckebusch, L.; Noseda, M.; Zaffran, S.; Schneider, M.D.; Niederreither, K. Endogenous retinoic acid regulates cardiac progenitor differentiation. Proc. Natl. Acad. Sci. USA 2010, 107, 9234-9239.
234. Rochais, F.; Mesbah, K.; Kelly, R.G. Signaling pathways controlling second heart field development. Circ. Res. 2009, 104, 933-942.
235. Lelievre-Pegorier, M.; Vilar, J.; Ferrier, M.L.; Moreau, E.; Freund, N.; Gilbert, T.; Merlet-Benichou, C. Mild vitamin A deficiency leads to inborn nephron deficit in the rat. Kidney Int. 1998, 54, 1455-1462.
236. Mendelsohn, C.; Batourina, E.; Fung, S.; Gilbert, T.; Dodd, J. Stromal cells mediate retinoid-dependent functions essential for renal development. Development 1999, 126, 1139-1148.
237. Batourina, E.; Gim, S.; Bello, N.; Shy, M.; Clagett-Dame, M.; Srinivas, S.; Costantini, F.; Mendelsohn, C. Vitamin A controls epithelial/mesenchymal interactions through Ret expression. Nat. Genet. 2001, 27, 74-78.
238. Niederreither, K.; Fraulob, V.; Garnier, J.M.; Chambon, P.; Dolle, P. Differential expression of retinoic acid-synthesizing (RALDH) enzymes during fetal development and organ differentiation in the mouse. Mech. Dev. 2002, 110, 165-171.
239. Schuchardt, A.; D'Agati, V.; Larsson-Blomberg, L.; Costantini, F.; Pachnis, V. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 1994, 367, 380-383.
240. Schuchardt, A.; D'Agati, V.; Pachnis, V.; Costantini, F. Renal agenesis and hypodysplasia in ret-k- mutant mice result from defects in ureteric bud development. Development 1996, 122, 1919-1929.
241. Batourina, E.; Choi, C.; Paragas, N.; Bello, N.; Hensle, T.; Costantini, F.D.; Schuchardt, A.; Bacallao, R.L.; Mendelsohn, C.L. Distal ureter morphogenesis depends on epithelial cell remodeling mediated by vitamin A and Ret. Nat. Genet. 2002, 32, 109-115.
242. Rosselot, C.; Spraggon, L.; Chia, I.; Batourina, E.; Riccio, P.; Lu, B.; Niederreither, K.; Dolle, P.; Duester, G.; Chambon, P.; Costantini, F.; Gilbert, T.; Molotkov, A.; Mendelsohn, C. Non-cell-autonomous retinoid signaling is crucial for renal development. Development 2010, 137, 283-292.
243. Hoy, W.E.; Hughson, M.D.; Bertram, J.F.; Douglas-Denton, R.; Amann, K. Nephron number, hypertension, renal disease, and renal failure. J. Am. Soc. Nephrol. 2005, 16, 2557-2564.
244. Brenner, B.M.; Mackenzie, H.S. Nephron mass as a risk factor for progression of renal disease. Kidney Int. Suppl. 1997, 63, S124-S127.
245. Poladia, D.P.; Kish, K.; Kutay, B.; Bauer, J.; Baum, M.; Bates, C.M. Link between reduced nephron number and hypertension: studies in a mutant mouse model. Pediatr. Res. 2006, 59, 489-493.
246. Keller, G.; Zimmer, G.; Mall, G.; Ritz, E.; Amann, K. Nephron number in patients with primary hypertension. New Engl. J. Med. 2003, 348, 101-108.
247. Makrakis, J.; Zimanyi, M.A.; Black, M.J. Retinoic acid enhances nephron endowment in rats exposed to maternal protein restriction. Pediatr. Nephrol. 2007, 22, 1861-1867.
248. Torfs, C.P.; Curry, C.J.; Bateson, T.F.; Honore, L.H. A population-based study of congenital diaphragmatic hernia. Teratology 1992, 46, 555-565.
249. Beurskens, L.W.; Tibboel, D.; Lindemans, J.; Duvekot, J.J.; Cohen-Overbeek, T.E.; Veenma, D.C.; de Klein, A.; Greer, J.J.; Steegers-Theunissen, R.P. Retinol status of newborn infants is associated with congenital diaphragmatic hernia. Pediatrics 2010, 126, 712-720.
250. Pasutto, F.; Sticht, H.; Hammersen, G.; Gillessen-Kaesbach, G.; Fitzpatrick, D.R.; Nurnberg, G.; Brasch, F.; Schirmer-Zimmermann, H.; Tolmie, J.L.; Chitayat, D.; et al. Mutations in STRA6 cause a broad spectrum of malformations including anophthalmia, congenital heart defects, diaphragmatic hernia, alveolar capillary dysplasia, lung hypoplasia, and mental retardation. Am. J. Hum. Genet. 2007, 80, 550-560.
251. Goumy, C.; Gouas, L.; Marceau, G.; Coste, K.; Veronese, L.; Gallot, D.; Sapin, V.; Vago, P.; Tchirkov, A. Retinoid pathway and congenital diaphragmatic hernia: hypothesis from the analysis of chromosomal abnormalities. Fetal Diagn. Ther. 2010, 28, 129-139.
252. Clugston, R.D.; Klattig, J.; Englert, C.; Clagett-Dame, M.; Martinovic, J.; Benachi, A.; Greer, J.J. Teratogen-induced, dietary and genetic models of congenital diaphragmatic hernia share a common mechanism of pathogenesis. Am. J. Pathol. 2006, 169, 1541-1549.
253. Mey, J.; Babiuk, R.P.; Clugston, R.; Zhang, W.; Greer, J.J. Retinal dehydrogenase-2 is inhibited by compounds that induce congenital diaphragmatic hernias in rodents. Am. J. Pathol. 2003, 162, 673-679.
254. Clugston, R.D.; Zhang, W.; Alvarez, S.; de Lera, A.R.; Greer, J.J. Understanding abnormal retinoid signaling as a causative mechanism in congenital diaphragmatic hernia. Am. J. Respir. Cell Mol. Biol. 2010, 42, 276-285.
255. Hind, M.; Corcoran, J.; Maden, M. Temporal/spatial expression of retinoid binding proteins and RAR isoforms in the postnatal lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 282, L468-L476.
256. Malpel, S.; Mendelsohn, C.; Cardoso, W.V. Regulation of retinoic acid signaling during lung morphogenesis. Development 2000, 127, 3057-3067.
257. Mollard, R.; Viville, S.; Ward, S.J.; Decimo, D.; Chambon, P.; Dolle, P. Tissue-specific expression of retinoic acid receptor isoform transcripts in the mouse embryo. Mech. Dev. 2000, 94, 223-232.
258. Wang, Z.; Dolle, P.; Cardoso, W.V.; Niederreither, K. Retinoic acid regulates morphogenesis and patterning of posterior foregut derivatives. Dev. Biol. 2006, 297, 433-445.
259. Desai, T.J.; Chen, F.; Lu, J.; Qian, J.; Niederreither, K.; Dolle, P.; Chambon, P.; Cardoso, W.V. Distinct roles for retinoic acid receptors alpha and beta in early lung morphogenesis. Dev. Biol. 2006, 291, 12-24.
260. Hind, M.; Gilthorpe, A.; Stinchcombe, S.; Maden, M. Retinoid induction of alveolar regeneration: from mice to man? Thorax 2009, 64, 451-457.
261. Mollard, R.; Ghyselinck, N.B.; Wendling, O.; Chambon, P.; Mark, M. Stage-dependent responses of the developing lung to retinoic acid signaling. Int. J. Dev. Biol. 2000, 44, 457-462.
262. Chen, F.; Cao, Y.; Qian, J.; Shao, F.; Niederreither, K.; Cardoso, W.V. A retinoic acid-dependent network in the foregut controls formation of the mouse lung primordium. J. Clin. Invest. 2010, 120, 2040-2048.
263. Wongtrakool, C.; Malpel, S.; Gorenstein, J.; Sedita, J.; Ramirez, M.I.; Underhill, T.M.; Cardoso, W.V. Down-regulation of retinoic acid receptor alpha signaling is required for sacculation and type I cell formation in the developing lung. J. Biol. Chem. 2003, 278, 46911-46918.
264. Massaro, D.; Massaro, G.D. Retinoids, alveolus formation, and alveolar deficiency: clinical implications. Am. J. Respir. Cell Mol. Biol. 2003, 28, 271-274.
265. Massaro, G.D.; Massaro, D. Retinoic acid treatment partially rescues failed septation in rats and in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 278, L955-L960.
266. Massaro, G.D.; Massaro, D. Postnatal treatment with retinoic acid increases the number of pulmonary alveoli in rats. Am. J. Physiol. 1996, 270, L305-L310.
267. Massaro, G.D.; Massaro, D.; Chambon, P. Retinoic acid receptor-alpha regulates pulmonary alveolus formation in mice after, but not during, perinatal period. Am. J. Physiol. Lung Cell. Mol. Physiol. 2003, 284, L431-L433.
268. Massaro, G.D.; Massaro, D.; Chan, W.Y.; Clerch, L.B.; Ghyselinck, N.; Chambon, P.; Chandraratna, R.A. Retinoic acid receptor-beta: an endogenous inhibitor of the perinatal formation of pulmonary alveoli. Physiol. Genomics 2000, 4, 51-57.
269. McGowan, S.; Jackson, S.K.; Jenkins-Moore, M.; Dai, H.H.; Chambon, P.; Snyder, J.M. Mice bearing deletions of retinoic acid receptors demonstrate reduced lung elastin and alveolar numbers. Am. J. Respir. Cell Mol. Biol. 2000, 23, 162-167.
270. Checkley, W.; West, K.P., Jr.; Wise, R.A.; Baldwin, M.R.; Wu, L.; LeClerq, S.C.; Christian, P.; Katz, J.; Tielsch, J.M.; Khatry, S.; Sommer, A. Maternal vitamin A supplementation and lung function in offspring. New Engl. J. Med. 2010, 362, 1784-1794.
271. 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, 399-411.
272. 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, 950-957.
273. Stafford, D.; Hornbruch, A.; Mueller, P.R.; Prince, V.E. A conserved role for retinoid signaling in vertebrate pancreas development. Dev. Genes Evol. 2004, 214, 432-441.
274. Stafford, D.; Prince, V.E. Retinoic acid signaling is required for a critical early step in zebrafish pancreatic development. Curr. Biol. 2002, 12, 1215-1220.
275. Chen, Y.; Pan, F.C.; 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, 144-160.
276. Alexa, K.; Choe, S.K.; Hirsch, N.; Etheridge, L.; Laver, E.; Sagerstrom, C.G. Maternal and zygotic aldh1a2 activity is required for pancreas development in zebrafish. PLoS ONE 2009, 4, e8261.
277. Pan, F.C.; 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, 518-531.
278. Tulachan, S.S.; Doi, R.; Kawaguchi, Y.; Tsuji, S.; Nakajima, S.; Masui, T.; Koizumi, M.; Toyoda, E.; Mori, T.; Ito, D.; Kami, K.; Fujimoto, K.; Imamura, M. All-trans retinoic acid induces differentiation of ducts and endocrine cells by mesenchymal/epithelial interactions in embryonic pancreas. Diabetes 2003, 52, 76-84.
279. Ahlgren, U.; Jonsson, J.; Edlund, H. The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice. Development 1996, 122, 1409-1416.
280. Jonsson, J.; Carlsson, L.; Edlund, T.; Edlund, H. Insulin-promoter-factor 1 is required for pancreas development in mice. Nature 1994, 371, 606-609.
281. Offield, M.F.; Jetton, T.L.; Labosky, P.A.; Ray, M.; Stein, R.W.; Magnuson, M.A.; Hogan, B.L.; Wright, C.V. PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development 1996, 122, 983-995.
282. Kinkel, M.D.; Sefton, E.M.; Kikuchi, Y.; Mizoguchi, T.; Ward, A.B.; Prince, V.E. Cyp26 enzymes function in endoderm to regulate pancreatic field size. Proc. Natl. Acad. Sci. USA 2009, 106, 7864-7869.
283. Gittes, G.K. Developmental biology of the pancreas: a comprehensive review. Dev. Biol. 2009, 326, 4-35.
284. Pearl, E.J.; Bilogan, C.K.; Mukhi, S.; Brown, D.D.; Horb, M.E. Xenopus pancreas development. Dev. Dyn. 2009, 238, 1271-1286.
285. Stratford, T.; Horton, C.; Maden, M. Retinoic acid is required for the initiation of outgrowth in the chick limb bud. Curr. Biol. 1996, 6, 1124-1133.
286. Stratford, T.; Logan, C.; Zile, M.; Maden, M. Abnormal anteroposterior and dorsoventral patterning of the limb bud in the absence of retinoids. Mech. Dev. 1999, 81, 115-125.
287. Niederreither, K.; Vermot, J.; Schuhbaur, B.; Chambon, P.; Dolle, P. Embryonic retinoic acid synthesis is required for forelimb growth and anteroposterior patterning in the mouse. Development 2002, 129, 3563-3574.
288. Mic, F.A.; Sirbu, I.O.; Duester, G. Retinoic acid synthesis controlled by Raldh2 is required early for limb bud initiation and then later as a proximodistal signal during apical ectodermal ridge formation. J. Biol. Chem. 2004, 279, 26698-26706.
289. Gibert, Y.; Gajewski, A.; Meyer, A.; Begemann, G. Induction and prepatterning of the zebrafish pectoral fin bud requires axial retinoic acid signaling. Development 2006, 133, 2649-2659.
290. Mercader, N.; Leonardo, E.; Piedra, M.E.; Martinez, A.C.; Ros, M.A.; Torres, M. Opposing RA and FGF signals control proximodistal vertebrate limb development through regulation of Meis genes. Development 2000, 127, 3961-3970.
291. Benazet, J.D.; Zeller, R. Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb. Perspect. Biol. 2009, 1, a001339.
292. Zeller, R.; Lopez-Rios, J.; Zuniga, A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 2009, 10, 845-858.
293. Lewandoski, M.; Mackem, S. Limb development: the rise and fall of retinoic acid. Curr. Biol. 2009, 19, R558-R561.
294. Dupe, V.; Ghyselinck, N.B.; Thomazy, V.; Nagy, L.; Davies, P.J.; Chambon, P.; Mark, M. Essential roles of retinoic acid signaling in interdigital apoptosis and control of BMP-7 expression in mouse autopods. Dev. Biol. 1999, 208, 30-43.
295. Zhao, X.; Brade, T.; Cunningham, T.J.; Duester, G. Retinoic acid controls expression of tissue remodeling genes Hmgn1 and Fgf18 at the digit-interdigit junction. Dev. Dyn. 2010, 239, 665-671.
296. Rodriguez-Leon, J.; Merino, R.; Macias, D.; Ganan, Y.; Santesteban, E.; Hurle, J.M. Retinoic acid regulates programmed cell death through BMP signalling. Nat. Cell Biol. 1999, 1, 125-126.
297. Hernandez-Martinez, R.; Castro-Obregon, S.; Covarrubias, L. Progressive interdigital cell death: regulation by the antagonistic interaction between fibroblast growth factor 8 and retinoic acid. Development 2009, 136, 3669-3678.