New insights and changing paradigms in the regulation of vitamin A metabolism in development

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 6, Issue 3, 2017, Pages

  Shannon, Stephen R ^a,b   Moise, Alexander R ^c   Trainor, Paul A ^a,b  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; FIBROBLAST GROWTH FACTOR 8; HORMONE SENSITIVE LIPASE; LECITHIN RETINOL ACYLTRANSFERASE; RETINAL; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR; RETINOL; RETINOL BINDING PROTEIN 4;

DEVELOPMENTAL BIOLOGY; DEVELOPMENTAL DISORDER; DHRS3 GENE; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HYPOPLASIA; LOSS OF FUNCTION MUTATION; NEGATIVE FEEDBACK; NONHUMAN; OXIDATION; PRIORITY JOURNAL; RDH10 GENE; RETINOL DEFICIENCY; REVIEW; STELLATE CELL; TERATOGENICITY; UPREGULATION; VITAMIN METABOLISM; ANIMAL; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; EMBRYONIC DEVELOPMENT; HOMEOSTASIS; HUMANS; SIGNAL TRANSDUCTION; VITAMIN A;

EID: 85013345304     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.264     Document Type: Review

References (188)

1. Duester G. Retinoic acid synthesis and signaling during early organogenesis. Cell 2008, 134:921–931.
2. Mark M, Ghyselinck NB, Chambon P. Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 2009, 7:e002.
3. Rhinn M, Dolle P. Retinoic acid signalling during development. Development 2012, 139:843–858.
4. Conaway HH, Henning P, Lerner UH. Vitamin a metabolism, action, and role in skeletal homeostasis. Endocr Rev 2013, 34:766–797.
5. Kawai T, Yanaka N, Richards JS, Shimada M. De novo-synthesized retinoic acid in ovarian antral follicles enhances FSH-mediated ovarian follicular cell differentiation and female fertility. Endocrinology 2016, 157:2160–2172.
6. Spinas E, Saggini A, Kritas SK, Cerulli G, Caraffa A, Antinolfi P, Pantalone A, Frydas A, Tei M, Speziali A, et al. Can vitamin a mediate immunity and inflammation? J Biol Regul Homeost Agents 2015, 29:1–6.
7. Petkovich M, Brand NJ, Krust A, Chambon P. A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature 1987, 330:444–450.
8. Giguere V, Ong ES, Segui P, Evans RM. Identification of a receptor for the morphogen retinoic acid. Nature 1987, 330:624–629.
9. Brand N, Petkovich M, Krust A, Chambon P, de Thé H, Marchio A, Tiollais P, Dejean A. Identification of a second human retinoic acid receptor. Nature 1988, 332:850–853.
10. Krust A, Kastner P, Petkovich M, Zelent A, Chambon P. A third human retinoic acid receptor, hRAR-gamma. Proc Natl Acad Sci USA 1989, 86:5310–5314.
11. Kliewer SA, Umesono K, Mangelsdorf DJ, Evans RM. Retinoid X receptor interacts with nuclear receptors in retinoic acid, thyroid hormone and vitamin D3 signalling. Nature 1992, 355:446–449.
12. Al Tanoury Z, Piskunov A, Rochette-Egly C. Vitamin A and retinoid signaling: genomic and non-genomic effects. J Lipid Res 2013, 54:1761–1775.
13. Studer M, Pöpperl H, Marshall H, Kuroiwa A, Krumlauf R. Role of a conserved retinoic acid response element in rhombomere restriction of Hoxb-1. Science 1994, 265:1728–1732.
14. Kumar S, Duester G. Retinoic acid controls body axis extension by directly repressing Fgf8 transcription. Development 2014, 141:2972–2977.
15. Kumar S, Cunningham TJ, Duester G. Nuclear receptor corepressors Ncor1 and Ncor2 (Smrt) are required for retinoic acid-dependent repression of Fgf8 during somitogenesis. Dev Biol 2016, 418:204–215.
16. Di Lascio S, Saba E, Belperio D, Raimondi A, Lucchetti H, Fornasari D, Benfante R. PHOX2A and PHOX2B are differentially regulated during retinoic acid-driven differentiation of SK-N-BE(2)C neuroblastoma cell line. Exp Cell Res 2016, 342:62–71.
17. Kastner P, Mark M, Ghyselinck N, Krezel W, Dupé V, Grondona JM, Chambon P. Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 1997, 124:313–326.
18. Niederreither K, Dolle P. Retinoic acid in development: towards an integrated view. Nat Rev Genet 2008, 9:541–553.
19. Iwata M, Hirakiyama A, Eshima Y, Kagechika H, Kato C, Song SY. Retinoic acid imprints gut-homing specificity on T cells. Immunity 2004, 21:527–538.
20. Mora JR, Iwata M, Eksteen B, Song SY, Junt T, Senman B, Otipoby KL, Yokota A, Takeuchi H, Ricciardi-Castagnoli P, et al. Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 2006, 314:1157–1160.
21. Blum N, Begemann G. Retinoic acid signaling controls the formation, proliferation and survival of the blastema during adult zebrafish fin regeneration. Development 2011, 139:107–116.
22. Gudas LJ. Retinoids induce stem cell differentiation via epigenetic changes. Semin Cell Dev Biol 2013, 24:701–705.
23. Shmarakov IO, Jiang H, Yang KJ, Goldberg IJ, Blaner WS. Hepatic retinoid stores are required for normal liver regeneration. J Lipid Res 2013, 54:893–908.
24. Kumar S, Sandell LL, Trainor PA, Koentgen F, Duester G. Alcohol and aldehyde dehydrogenases: retinoid metabolic effects in mouse knockout models. Biochim Biophys Acta 2012, 1821:198–205.
25. Kedishvili NY. Enzymology of retinoic acid biosynthesis and degradation. J Lipid Res 2013, 54:1744–1760.
26. Napoli JL. Physiological insights into all-trans-retinoic acid biosynthesis. Biochim Biophys Acta 2012, 1821:152–167.
27. Spiegler E, Kim YK, Wassef L, Shete V, Quadro L. Maternal-fetal transfer and metabolism of vitamin A and its precursor β-carotene in the developing tissues. Biochim Biophys Acta 2012, 1821:88–98.
28. Sandell LL, Sanderson BW, Moiseyev G, Johnson T, Mushegian A, Young K, Rey JP, Ma JX, Staehling-Hampton K, Trainor PA. RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development. Genes Dev 2007, 21:1113–1124.
29. Sandell LL, Lynn ML, Inman KE, McDowell W, Trainor PA. RDH10 oxidation of vitamin A is a critical control step in synthesis of retinoic acid during mouse embryogenesis. PLoS One 2012, 7:e30698.
30. Farjo KM, Moiseyev G, Nikolaeva O, Sandell LL, Trainor PA, Ma JX. RDH10 is the primary enzyme responsible for the first step of embryonic vitamin A metabolism and retinoic acid synthesis. Dev Biol 2011, 357:347–355.
31. Sosnik J, Zheng L, Rackauckas CV, Digman M, Gratton E, Nie Q, Schilling TF. Noise modulation in retinoic acid signaling sharpens segmental boundaries of gene expression in the embryonic zebrafish hindbrain. Elife 2016, 5:e14034.
32. Shimozono S, Iimura T, Kitaguchi T, Higashijima S, Miyawaki A. Visualization of an endogenous retinoic acid gradient across embryonic development. Nature 2013, 496:363–366.
33. White RJ, Nie Q, Lander AD, Schilling TF. Complex regulation of cyp26a1 creates a robust retinoic acid gradient in the zebrafish embryo. PLoS Biol 2007, 5:e304.
34. Rosselot C, Spraggon L, Chia I, Batourina E, Riccio P, Lu B, Niederreither K, Dolle P, Duester G, Chambon P, et al. Non-cell-autonomous retinoid signaling is crucial for renal development. Development 2010, 137:283–292.
35. Bonney S, Harrison-Uy S, Mishra S, MacPherson AM, Choe Y, Li D, Jaminet SC, Fruttiger M, Pleasure SJ, Siegenthaler JA. Diverse functions of retinoic acid in brain vascular development. J Neurosci 2016, 36:7786–7801.
36. Vernet N, Dennefeld C, Guillou F, Chambon P, Ghyselinck NB, Mark M. Prepubertal testis development relies on retinoic acid but not rexinoid receptors in Sertoli cells. EMBO J 2006, 25:5816–5825.
37. Ross AC. Retinoid production and catabolism: role of diet in regulating retinol esterification and retinoic acid oxidation. J Nutr 2003, 133:291S–296S.
38. Grune T, Lietz G, Palou A, Ross AC, Stahl W, Tang G, Thurnham D, Yin SA, Biesalski HK. β-carotene is an important vitamin A source for humans. J Nutr 2010, 140:2268S–2285S.
39. Weber D, Grune T. The contribution of β-carotene to vitamin A supply of humans. Mol Nutr Food Res 2011, 56:251–258.
40. Sommer A. Vitamin a deficiency and clinical disease: an historical overview. J Nutr 2008, 138:1835–1839.
41. von Lintig J. Provitamin A metabolism and functions in mammalian biology. Am J Clin Nutr 2012, 96:1234S–1244S.
42. Bloch CE. Further clinical investigations into the diseases arising in consequence of a deficiency in the fatsoluble a factor. Am J Dis Child 1924, 28:659–667.
43. Mason KE. Foetal death, prolonged gestation, and difficult parturition in the rat as a result of vitamin A-deficiency. Am J Anat 1935, 57:303–349.
44. 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.
45. Wilson JG, Roth CB, 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.
46. Cohlan SQ. Excessive intake of vitamin A as a cause of congenital anomalies in the rat. Science 1953, 117:535–536.
47. Cohlan SQ. Congenital anomalies in the rat produced by excessive intake of vitamin A during pregnancy. Pediatrics 1954, 13:556–567.
48. Kalter H, Warkany J. Experimental production of congenital malformations in strains of inbred mice by maternal treatment with hypervitaminosis A. Am J Pathol 1961, 38:1–21.
49. Conlon RA, Rossant J. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 1992, 116:357–368.
50. Jiang H, Gyda M III, Harnish DC, Chandraratna RA, Soprano KJ, Kochhar DM, Soprano DR. Teratogenesis by retinoic acid analogs positively correlates with elevation of retinoic acid receptor-β 2 mRNA levels in treated embryos. Teratology 1994, 50:38–43.
51. Melhus H, Michaëlsson K, Kindmark A, Bergström R, Holmberg L, Mallmin H, Wolk A, Ljunghall S. Excessive dietary intake of vitamin A is associated with reduced bone mineral density and increased risk for hip fracture. Ann Intern Med 1998, 129:770–778.
52. Feskanich D, Singh V, Willett WC, Colditz GA. Vitamin A intake and hip fractures among postmenopausal women. JAMA 2002, 287:47–54.
53. Michaelsson K, Lithell H, Vessby B, Melhus H. Serum retinol levels and the risk of fracture. N Engl J Med 2003, 348:287–294.
54. Larson RS, Tallman MS. Retinoic acid syndrome: manifestations, pathogenesis, and treatment. Best Pract Res Clin Haematol 2003, 16:453–461.
55. 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, 4:932–942.
56. Tickle C, Lee J, Eichele G. A quantitative analysis of the effect of all-trans-retinoic acid on the pattern of chick wing development. Dev Biol 1985, 109:82–95.
57. Frenz DA, Liu W, Cvekl A, Xie Q, Wassef L, Quadro L, Niederreither K, Maconochie M, Shanske A. Retinoid signaling in inner ear development: a "Goldilocks" phenomenon. Am J Med Genet A 2010, 152a:2947–2961.
58. Lee LM, Leung CY, Tang WW, Choi HL, Leung YC, McCaffery PJ, Wang CC, Woolf AS, Shum AS. A paradoxical teratogenic mechanism for retinoic acid. Proc Natl Acad Sci USA 2012, 109:13668–13673.
59. D'Aniello E, Rydeen AB, Anderson JL, Mandal A, Waxman JS. Depletion of retinoic acid receptors initiates a novel positive feedback mechanism that promotes teratogenic increases in retinoic acid. PLoS Genet 2013, 9:e1003689.
60. Kim YK, Wassef L, Chung S, Jiang H, Wyss A, Blaner WS, Quadro L. β-Carotene and its cleavage enzyme β-carotene-15,15'-oxygenase (CMOI) affect retinoid metabolism in developing tissues. FASEB J 2011, 25:1641–1652.
61. Ashique AM, May SR, Kane MA, Folias AE, Phamluong K, Choe Y, Napoli JL, Peterson AS. Morphological defects in a novel Rdh10 mutant that has reduced retinoic acid biosynthesis and signaling. Genesis 2012, 50:415–423.
62. Costabile BK, Kim Y-K, Iqbal J, Zuccaro MV, Wassef L, Narayanasamy S, Curley RW Jr, Harrison EH, Hussain MM, Quadro L. β-Apo-10'-carotenoids modulate placental microsomal triglyceride transfer protein expression and function to optimize transport of intact β-carotene to the embryo. J Biol Chem 2016, 291:18525–18535.
63. During A, Harrison EH. Mechanisms of provitamin A (carotenoid) and vitamin A (retinol) transport into and out of intestinal Caco-2 cells. J Lipid Res 2007, 48:2283–2294.
64. Wyss A, Wirtz GM, Woggon WD, Brugger R, Wyss M, Friedlein A, Bachmann H, Hunziker W. Cloning and expression of β,β-carotene 15,15'-dioxygenase. Biochem Biophys Res Commun 2000, 271:334–336.
65. von Lintig J, Vogt K. Filling the gap in vitamin A research molecular identification of an enzyme cleaving β-carotene to retinal. J Biol Chem 2000, 275:11915–11920.
66. Hessel S, Eichinger A, Isken A, Amengual J, Hunzelmann S, Hoeller U, Elste V, Hunziker W, Goralczyk R, Oberhauser V, et al. CMO1 deficiency abolishes vitamin A production from β-carotene and alters lipid metabolism in mice. J Biol Chem 2007, 282:33553–33561.
67. Mora O, Kuri-Melo L, González-Gallardo A, Meléndez E, Morales A, Shimada A, Varela-Echavarría A. A potential role for β-carotene in avian embryonic development. Int J Vitam Nutr Res 2004, 74:116–122.
68. Lindqvist A, He YG, Andersson S. Cell type-specific expression of β-carotene 9',10'-monooxygenase in human tissues. J Histochem Cytochem 2005, 53:1403–1412.
69. Shmarakov I, Fleshman MK, D'Ambrosio DN, Piantedosi R, Riedl KM, Schwartz SJ, Curley RW Jr, von Lintig J, Rubin LP, Harrison EH, et al. Hepatic stellate cells are an important cellular site for β-carotene conversion to retinoid. Arch Biochem Biophys 2010, 504:3–10.
70. Choi MY, Romer AI, Hu M, Lepourcelet M, Mechoor A, Yesilaltay A, Krieger M, Gray PA, Shivdasani RA. A dynamic expression survey identifies transcription factors relevant in mouse digestive tract development. Development 2006, 133:4119–4129.
71. Seino Y, Miki T, Kiyonari H, Abe T, Fujimoto W, Kimura K, Takeuchi A, Takahashi Y, Oiso Y, Iwanaga T, et al. ISX participates in the maintenance of vitamin A metabolism by regulation of β-carotene 15,15'-monooxygenase (Bcmo1) expression. J Biol Chem 2008, 283:4905–4911.
72. Bondurand N, Kuhlbrodt K, Pingault V, Enderich J, Sajus M, Tommerup N, Warburg M, Hennekam RC, Read AP, Wegner M, et al. A molecular analysis of the yemenite deaf-blind hypopigmentation syndrome: SOX10 dysfunction causes different neurocristopathies. Hum Mol Genet 1999, 8:1785–1789.
73. Lobo GP, Amengual J, Baus D, Shivdasani RA, Taylor D, von Lintig J. Genetics and diet regulate vitamin A production via the homeobox transcription factor ISX. J Biol Chem 2013, 288:9017–9027.
74. Harrison EH. Mechanisms involved in the intestinal absorption of dietary vitamin A and provitamin A carotenoids. Biochim Biophys Acta 2012, 1821:70–77.
75. Reboul E. Absorption of vitamin A and carotenoids by the enterocyte: focus on transport proteins. Nutrients 2013, 5:3563–3581.
76. Wongsiriroj N, Piantedosi R, Palczewski K, Goldberg IJ, Johnston TP, Li E, Blaner WS. The molecular basis of retinoid absorption: a genetic dissection. J Biol Chem 2008, 283:13510–13519.
77. Ong DE, Kakkad B, MacDonald PN. Acyl-CoA-independent esterification of retinol bound to cellular retinol-binding protein (type II) by microsomes from rat small intestine. J Biol Chem 1987, 262:2729–2736.
78. E X, Zhang L, Lu J, Tso P, Blaner WS, Levin MS, Li E. Increased neonatal mortality in mice lacking cellular retinol-binding protein II. J Biol Chem 2002, 277:36617–36623.
79. Kane MA, Bright FV, Napoli JL. Binding affinities of CRBPI and CRBPII for 9-cis-retinoids. Biochim Biophys Acta 2011, 1810:514–518.
80. Quadro L, Blaner WS, Salchow DJ, Vogel S, Piantedosi R, Gouras P, Freeman S, Cosma MP, Colantuoni V, Gottesman ME. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J 1999, 18:4633–4644.
81. Quadro L, Hamberger L, Gottesman ME, Wang F, Colantuoni V, Blaner WS, Mendelsohn CL. Pathways of vitamin A delivery to the embryo: insights from a new tunable model of embryonic vitamin A deficiency. Endocrinology 2005, 146:4479–4490.
82. Wassef L, Quadro L. Uptake of dietary retinoids at the maternal-fetal barrier: in vivo evidence for the role of lipoprotein lipase and alternative pathways. J Biol Chem 2011, 286:32198–32207.
83. Dueker SR, Lin Y, Buchholz BA, Schneider PD, Lamé MW, Segall HJ, Vogel JS, Clifford AJ. Long-term kinetic study of β-carotene, using accelerator mass spectrometry in an adult volunteer. J Lipid Res 2000, 41:1790–1800.
84. Shirakami Y, Lee SA, Clugston RD, Blaner WS. Hepatic metabolism of retinoids and disease associations. Biochim Biophys Acta 2012, 1821:124–136.
85. Schreiber R et al. Retinyl ester hydrolases and their roles in vitamin A homeostasis. Biochim Biophys Acta 2012, 1821:113–123.
86. Blaner WS, Obunike JC, Kurlandsky SB, al-Haideri M, Piantedosi R, Deckelbaum RJ, Goldberg IJ. Lipoprotein lipase hydrolysis of retinyl ester: possible implications for retinoid uptake by cells. J Biol Chem 1994, 269:16559–16565.
87. Soprano DR, Soprano KJ, Goodman DS. 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.
88. Bavik C, Ward SJ, 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.
89. Shen J, Shi D, Suzuki T, Xia Z, Zhang H, Araki K, Wakana S, Takeda N, Yamamura K, Jin S, et al. Severe ocular phenotypes in Rbp4-deficient mice in the C57BL/6 genetic background. Lab Invest 2016, 96:680–691.
90. Ghyselinck NB, 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.
91. Bouillet P, Sapin V, Chazaud C, Messaddeq N, Décimo D, Dollé P, Chambon P. Developmental expression pattern of Stra6, a retinoic acid-responsive gene encoding a new type of membrane protein. Mech Dev 1997, 63:173–186.
92. Sapin V, Bouillet P, Oulad-Abdelghani M, Dastugue B, Chambon P, Dollé P. Differential expression of retinoic acid-inducible (Stra) genes during mouse placentation. Mech Dev 2000, 92:295–299.
93. Amengual J, Zhang N, Kemerer M, Maeda T, Palczewski K, Von Lintig J. STRA6 is critical for cellular vitamin A uptake and homeostasis. Hum Mol Genet 2014, 23:5402–5417.
94. Skazik C, Amann PM, Heise R, Marquardt Y, Czaja K, Kim A, Rühl R, Kurschat P, Merk HF, Bickers DR, et al. Downregulation of STRA6 expression in epidermal keratinocytes leads to hyperproliferation-associated differentiation in both in vitro and in vivo skin models. J Invest Dermatol 2014, 134:1579–1588.
95. Ruiz A, Mark M, Jacobs H, Klopfenstein M, Hu J, Lloyd M, Habib S, Tosha C, Radu RA, Ghyselinck NB, et al. Retinoid content, visual responses, and ocular morphology are compromised in the retinas of mice lacking the retinol-binding protein receptor, STRA6. Invest Ophthalmol Vis Sci 2012, 53:3027–3039.
96. Berry DC, Jacobs H, Marwarha G, Gely-Pernot A, O'Byrne SM, DeSantis D, Klopfenstein M, Feret B, Dennefeld C, Blaner WS, et al. The STRA6 receptor is essential for retinol-binding protein-induced insulin resistance but not for maintaining vitamin A homeostasis in tissues other than the eye. J Biol Chem 2013, 288:24528–24539.
97. Terra R, Wang X, Hu Y, Charpentier T, Lamarre A, Zhong M, Sun H, Mao J, Qi S, Luo H, et al. To investigate the necessity of STRA6 upregulation in T cells during T cell immune responses. PLoS One 2013, 8:e82808.
98. Redondo C, Vouropoulou M, Evans J, Findlay JB. Identification of the retinol-binding protein (RBP) interaction site and functional state of RBPs for the membrane receptor. FASEB J 2008, 22:1043–1054.
99. Kawaguchi R, Zhong M, Kassai M, Ter-Stepanian M, Sun H. STRA6-catalyzed vitamin A influx, efflux, and exchange. J Membr Biol 2012, 245:731–745.
100. Chen Y, Clarke OB, Kim J, Stowe S, Kim YK, Assur Z, Cavalier M, Godoy-Ruiz R, von Alpen DC, Manzini C, et al. Structure of the STRA6 receptor for retinol uptake. Science 2016, 353:pii:aad8266.
101. Isken A, Golczak M, Oberhauser V, Hunzelmann S, Driever W, Imanishi Y, Palczewski K, von Lintig J. RBP4 disrupts vitamin A uptake homeostasis in a STRA6-deficient animal model for Matthew-Wood syndrome. Cell Metab 2008, 7:258–268.
102. Muenzner M, Tuvia N, Deutschmann C, Witte N, Tolkachov A, Valai A, Henze A, Sander LE, Raila J, Schupp M. Retinol-binding protein 4 and its membrane receptor STRA6 control adipogenesis by regulating cellular retinoid homeostasis and retinoic acid receptor alpha activity. Mol Cell Biol 2013, 33:4068–4082.
103. Alapatt P, Guo F, Komanetsky SM, Wang S, Cai J, Sargsyan A, Rodríguez Díaz E, Bacon BT, Aryal P, Graham TE. Liver retinol transporter and receptor for serum retinol-binding protein (RBP4). J Biol Chem 2013, 288:1250–1265.
104. Quadro L, Hamberger L, Gottesman ME, Colantuoni V, Ramakrishnan R, Blaner WS. Transplacental delivery of retinoid: the role of retinol-binding protein and lipoprotein retinyl ester. Am J Physiol Endocrinol Metab 2004, 286:E844–E851.
105. Rask L, Peterson PA. In vitro uptake of vitamin A from the retinol-binding plasma protein to mucosal epithelial cells from the monkey's small intestine. J Biol Chem 1976, 251:6360–6366.
106. Sivaprasadarao A, Findlay JB. The mechanism of uptake of retinol by plasma-membrane vesicles. Biochem J 1988, 255:571–579.
107. Smeland S, Bjerknes T, Malaba L, Eskild W, Norum KR, Blomhoff R. Tissue distribution of the receptor for plasma retinol-binding protein. Biochem J 1995, 305 (pt 2):419–424.
108. 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.
109. Georgiades P, Ferguson-Smith AC, Burton GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta 2002, 23:3–19.
110. Furukawa S, Hayashi S, Usuda K, Abe M, Hagio S, Ogawa I. Toxicological pathology in the rat placenta. J Toxicol Pathol 2011, 24:95–111.
111. Dancis J, Levitz M, Katz J, Wilson D, Blaner WS, Piantedosi R, Goodman DS. Transfer and metabolism of retinol by the perfused human placenta. Pediatr Res 1992, 32:195–199.
112. Sapin V, Chaïb S, Blanchon L, Alexandre-Gouabau MC, Lémery 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.
113. Amengual J, Golczak M, Palczewski K, von Lintig J. Lecithin:retinol acyltransferase is critical for cellular uptake of vitamin A from serum retinol-binding protein. J Biol Chem 2012, 287:24216–24227.
114. Friedman SL. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008, 88:125–172.
115. Yost RW, Harrison EH, Ross AC. Esterification by rat liver microsomes of retinol bound to cellular retinol-binding protein. J Biol Chem 1988, 263:18693–18701.
116. Ghyselinck NB, Båvik C, Sapin V, Mark M, Bonnier D, Hindelang C, Dierich A, Nilsson CB, Håkansson H, Sauvant P, et al. Cellular retinol-binding protein I is essential for vitamin A homeostasis. EMBO J 1999, 18:4903–4914.
117. Saari JC, Nawrot M, Garwin GG, Kennedy MJ, Hurley JB, Ghyselinck NB, Chambon P. Analysis of the visual cycle in cellular retinol-binding protein type I (CRBPI) knockout mice. Invest Ophthalmol Vis Sci 2002, 43:1730–1735.
118. Wei S, Lai K, Patel S, Piantedosi R, Shen H, Colantuoni V, Kraemer FB, Blaner WS. Retinyl ester hydrolysis and retinol efflux from BFC-1β adipocytes. J Biol Chem 1997, 272:14159–14165.
119. Strom K, Gundersen TE, Hansson O, Lucas S, Fernandez C, Blomhoff R, Holm C. Hormone-sensitive lipase (HSL) is also a retinyl ester hydrolase: evidence from mice lacking HSL. FASEB J 2009, 23:2307–2316.
120. Pirazzi C, Valenti L, Motta BM, Pingitore P, Hedfalk K, Mancina RM, Burza MA, Indiveri C, Ferro Y, Montalcini T, et al. PNPLA3 has retinyl-palmitate lipase activity in human hepatic stellate cells. Hum Mol Genet 2014, 23:4077–4085.
121. Taneja R, Bouillet P, Boylan JF, Gaub MP, Roy B, Gudas LJ, Chambon P. Reexpression of retinoic acid receptor (RAR) gamma or overexpression of RAR alpha or RAR beta in RAR gamma-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc Natl Acad Sci USA 1995, 92:7854–7858.
122. Bouillet P, Oulad-Abdelghani M, Vicaire S, Garnier JM, Schuhbaur B, Dollé P, Chambon P. Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel mouse gene, Stra1 (mouse LERK-2/Eplg2). Dev Biol 1995, 170:420–433.
123. Kashyap V, Laursen KB, Brenet F, Viale AJ, Scandura JM, Gudas LJ. RARγ is essential for retinoic acid induced chromatin remodeling and transcriptional activation in embryonic stem cells. J Cell Sci 2013, 126:999–1008.
124. Mangelsdorf DJ, Umesono K, Kliewer SA, Borgmeyer U, Ong ES, Evans RM. A direct repeat in the cellular retinol-binding protein type II gene confers differential regulation by RXR and RAR. Cell 1991, 66:555–561.
125. Smith WC, Nakshatri H, Leroy P, Rees J, Chambon P. A retinoic acid response element is present in the mouse cellular retinol binding protein I (mCRBPI) promoter. EMBO J 1991, 10:2223–2230.
126. Rajan N, Blaner WS, Soprano DR, Suhara A, Goodman DS. Cellular retinol-binding protein messenger RNA levels in normal and retinoid-deficient rats. J Lipid Res 1990, 31:821–829.
127. Wu L, Ross AC. Acidic retinoids synergize with vitamin A to enhance retinol uptake and STRA6, LRAT, and CYP26B1 expression in neonatal lung. J Lipid Res 2009, 51:378–387.
128. Zolfaghari R, Ross AC. An essential set of basic DNA response elements is required for receptor-dependent transcription of the lecithin:retinol acyltransferase (Lrat) gene. Arch Biochem Biophys 2009, 489:1–9.
129. Dixon JL, Kim YK, Brinker A, Quadro L. Loss of β-carotene 15,15'-oxygenase in developing mouse tissues alters esterification of retinol, cholesterol and diacylglycerols. Biochim Biophys Acta 2014, 1841:34–43.
130. Ang HL, Deltour L, Zgombic-Knight M, Wagner MA, 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.
131. Molotkov A, Deltour L, Foglio MH, Cuenca AE, 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.
132. Molotkov A, Fan X, Deltour L, Foglio MH, Martras S, Farrés J, Parés 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.
133. Deltour L, Foglio MH, Duester G. Metabolic deficiencies in alcohol dehydrogenase Adh1, Adh3, and Adh4 null mutant mice: overlapping roles of Adh1 and Adh4 in ethanol clearance and metabolism of retinol to retinoic acid. J Biol Chem 1999, 274:16796–16801.
134. 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.
135. Billings SE, Pierzchalski K, Butler Tjaden NE, Pang XY, Trainor PA, Kane MA, Moise AR. The retinaldehyde reductase DHRS3 is essential for preventing the formation of excess retinoic acid during embryonic development. FASEB J 2013, 27:4877–4889.
136. Cunningham TJ, Chatzi C, Sandell LL, Trainor PA, Duester G. Rdh10 mutants deficient in limb field retinoic acid signaling exhibit normal limb patterning but display interdigital webbing. Dev Dyn 2011, 240:1142–1150.
137. Cunningham TJ, Zhao X, Sandell LL, Evans SM, Trainor PA, Duester G. Antagonism between retinoic acid and fibroblast growth factor signaling during limb development. Cell Rep 2013, 3:1503–1511.
138. Farjo KM, Moiseyev G, Takahashi Y, Crouch RK, Ma JX. The 11-cis-retinol dehydrogenase activity of RDH10 and its interaction with visual cycle proteins. Invest Ophthalmol Vis Sci 2009, 50:5089–5097.
139. Adams MK, Belyaeva OV, Wu L, Kedishvili NY. The retinaldehyde reductase activity of DHRS3 is reciprocally activated by Retinol Dehydrogenase 10 to control retinoid homeostasis. J Biol Chem 2014, 289:14868–14880.
140. Cunningham TJ, Duester G. Mechanisms of retinoic acid signalling and its roles in organ and limb development. Nat Rev Mol Cell Biol 2015, 16:110–123.
141. Kam RK, Shi W, Chan SO, Chen Y, Xu G, Lau CB, Fung KP, Chan WY, Zhao H. Dhrs3 protein attenuates retinoic acid signaling and is required for early embryonic patterning. J Biol Chem 2013, 288:31477–31487.
142. Rhinn M, Schuhbaur B, Niederreither K, Dolle P. Involvement of retinol dehydrogenase 10 in embryonic patterning and rescue of its loss of function by maternal retinaldehyde treatment. Proc Natl Acad Sci USA 2011, 108:16687–16692.
143. Chatzi C, Cunningham TJ, Duester G. Investigation of retinoic acid function during embryonic brain development using retinaldehyde-rescued Rdh10 knockout mice. Dev Dyn 2013, 242:1056–1065.
144. D'Aniello E, Ravisankar P, Waxman JS. Rdh10a provides a conserved critical step in the synthesis of retinoic acid during zebrafish embryogenesis. PLoS One 2015, 10:e0138588.
145. Sahu B, Sun W, Perusek L, Parmar V, Le Y-Z, Griswold MD, Palczewski K, Maeda A. Conditional ablation of retinol dehydrogenase 10 in the retinal pigmented epithelium causes delayed dark adaption in mice. J Biol Chem 2015, 290:27239–27247.
146. Wright DM, Buenger DE, Abashev TM, Lindeman RP, Ding J, Sandell LL. Retinoic acid regulates embryonic development of mammalian submandibular salivary glands. Dev Biol 2015, 407:57–67.
147. Tong MH, Yang QE, Davis JC, Griswold MD. Retinol dehydrogenase 10 is indispensible for spermatogenesis in juvenile males. Proc Natl Acad Sci USA 2013, 110:543–548.
148. Feng L, Hernandez RE, Waxman JS, Yelon D, Moens CB. Dhrs3a regulates retinoic acid biosynthesis through a feedback inhibition mechanism. Dev Biol 2010, 338:1–14.
149. 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, 136:461–472.
150. Zhang M, Hu P, Krois CR, Kane MA, Napoli JL. Altered vitamin A homeostasis and increased size and adiposity in the rdh1-null mouse. FASEB J 2007, 21:2886–2896.
151. Wang C, Kane MA, Napoli JL. Multiple retinol and retinal dehydrogenases catalyze all-trans-retinoic acid biosynthesis in astrocytes. J Biol Chem 2011, 286:6542–6553.
152. Deltour L, Foglio MH, Duester G. Impaired retinol utilization in Adh4 alcohol dehydrogenase mutant mice. Dev Genet 1999, 25:1–10.
153. Molotkov A, Fan X, Duester G. Excessive vitamin A toxicity in mice genetically deficient in either alcohol dehydrogenase Adh1 or Adh3. Eur J Biochem 2002, 269:2607–2612.
154. Molotkov A, Ghyselinck NB, Chambon P, Duester G. Opposing actions of cellular retinol-binding protein and alcohol dehydrogenase control the balance between retinol storage and retinoic acid synthesis. Biochem J 2004, 383:295–302.
155. Kiser PD, Golczak M, Palczewski K. Chemistry of the retinoid (visual) cycle. Chem Rev 2014, 114:194–232.
156. Travis GH, Golczak M, Moise AR, Palczewski K. Diseases caused by defects in the visual cycle: retinoids as potential therapeutic agents. Annu Rev Pharmacol Toxicol 2007, 47:469–512.
157. Lundova T, Zemanová L, Malčeková B, Skarka A, Štambergová H, Havránková J, Šafr M, Wsól V. Molecular and biochemical characterisation of human short-chain dehydrogenase/reductase member 3 (DHRS3). Chem Biol Interact 2015, 234:178–187.
158. Kam RK, Chen Y, Chan SO, Chan WY, Dawid IB, Zhao H. Developmental expression of Xenopus short-chain dehydrogenase/reductase 3. Int J Dev Biol 2010, 54:1355–1360.
159. Gallego O, Ruiz FX, Ardèvol A, Domínguez M, Alvarez R, de Lera AR, Rovira C, Farrés J, Fita I, Parés X. Structural basis for the high all-trans-retinaldehyde reductase activity of the tumor marker AKR1B10. Proc Natl Acad Sci USA 2007, 104:20764–20769.
160. Ruiz FX, Gallego O, Ardèvol A, Moro A, Domínguez M, Alvarez S, Alvarez R, de Lera AR, Rovira C, Fita I, et al. Aldo-keto reductases from the AKR1B subfamily: retinoid specificity and control of cellular retinoic acid levels. Chem Biol Interact 2009, 178:171–177.
161. Ruiz FX, Porté S, Gallego O, Moro A, Ardèvol A, Del Río-Espínola A, Rovira C, Farrés J, Parés X. Retinaldehyde is a substrate for human aldo-keto reductases of the 1C subfamily. Biochem J 2011, 440:335–344.
162. Porté S, Xavier Ruiz F, Giménez J, Molist I, Alvarez S, Domínguez M, Alvarez R, de Lera AR, Parés X, Farrés J. Aldo-keto reductases in retinoid metabolism: search for substrate specificity and inhibitor selectivity. Chem Biol Interact 2012, 202:186–194.
163. Bhat PV, Labrecque J, Boutin JM, Lacroix A, Yoshida A. Cloning of a cDNA encoding rat aldehyde dehydrogenase with high activity for retinal oxidation. Gene 1995, 166:303–306.
164. Wang X, Penzes P, Napoli JL. Cloning of a cDNA encoding an aldehyde dehydrogenase and its expression in Escherichia coli: recognition of retinal as substrate. J Biol Chem 1996, 271:16288–16293.
165. Zhao D, McCaffery P, Ivins KJ, Neve RL, Hogan P, Chin WW, Dräger UC. Molecular identification of a major retinoic-acid-synthesizing enzyme, a retinaldehyde-specific dehydrogenase. Eur J Biochem 1996, 240:15–22.
166. Penzes P, Wang X, Sperkova Z, Napoli JL. Cloning of a rat cDNA encoding retinal dehydrogenase isozyme type I and its expression in E. coli. Gene 1997, 191:167–172.
167. McCaffery P, Tempst P, Lara G, Drager UC. Aldehyde dehydrogenase is a positional marker in the retina. Development 1991, 112:693–702.
168. Hochgreb T, Linhares VL, Menezes DC, Sampaio AC, Yan CY, Cardoso WV, Rosenthal N, Xavier-Neto J. A caudorostral wave of RALDH2 conveys anteroposterior information to the cardiac field. Development 2003, 130:5363–5374.
169. Wagner E, McCaffery P, Drager UC. Retinoic acid in the formation of the dorsoventral retina and its central projections. Dev Biol 2000, 222:460–470.
170. Chen F, Marquez H, Kim YK, Qian J, Shao F, Fine A, Cruikshank WW, Quadro L, Cardoso WV. Prenatal retinoid deficiency leads to airway hyperresponsiveness in adult mice. J Clin Invest 2014, 124:801–811.
171. Romand R, Albuisson E, Niederreither K, Fraulob V, Chambon P, Dollé P. Specific expression of the retinoic acid-synthesizing enzyme RALDH2 during mouse inner ear development. Mech Dev 2001, 106:185–189.
172. Grun F, Hirose Y, Kawauchi S, Ogura T, Umesono K. Aldehyde dehydrogenase 6, a cytosolic retinaldehyde dehydrogenase prominently expressed in sensory neuroepithelia during development. J Biol Chem 2000, 275:41210–41218.
173. 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, 97:227–230.
174. 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, 100:14036–14041.
175. Yahyavi M, Abouzeid H, Gawdat G, de Preux AS, Xiao T, Bardakjian T, Schneider A, Choi A, Jorgenson E, Baier H, et al. ALDH1A3 loss of function causes bilateral anophthalmia/microphthalmia and hypoplasia of the optic nerve and optic chiasm. Hum Mol Genet 2013, 22:3250–3258.
176. 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, 23:4637–4648.
177. Ziouzenkova O, Orasanu G, Sharlach M, Akiyama TE, Berger JP, Viereck J, Hamilton JA, Tang G, Dolnikowski GG, Vogel S, et al. Retinaldehyde represses adipogenesis and diet-induced obesity. Nat Med 2007, 13:695–702.
178. Kiefer FW, Orasanu G, Nallamshetty S, Brown JD, Wang H, Luger P, Qi NR, Burant CF, Duester G, Plutzky J. Retinaldehyde dehydrogenase 1 coordinates hepatic gluconeogenesis and lipid metabolism. Endocrinology 2012, 153:3089–3099.
179. Kiefer FW, Vernochet C, O'Brien P, Spoerl S, Brown JD, Nallamshetty S, Zeyda M, Stulnig TM, Cohen DE, Kahn CR, et al. Retinaldehyde dehydrogenase 1 regulates a thermogenic program in white adipose tissue. Nat Med 2012, 18:918–925.
180. Nallamshetty S, Wang H, Rhee EJ, Kiefer FW, Brown JD, Lotinun S, Le P, Baron R, Rosen CJ, Plutzky J. Deficiency of retinaldehyde dehydrogenase 1 induces BMP2 and increases bone mass in vivo. PLoS One 2013, 8:e71307.
181. Yasmeen R, Reichert B, Deiuliis J, Yang F, Lynch A, Meyers J, Sharlach M, Shin S, Volz KS, Green KB, et al. Autocrine function of aldehyde dehydrogenase 1 as a determinant of diet- and sex-specific differences in visceral adiposity. Diabetes 2013, 62:124–136.
182. Zhang QY, Dunbar D, Kaminsky L. Human cytochrome P-450 metabolism of retinals to retinoic acids. Drug Metab Dispos 2000, 28:292–297.
183. Chambers D, Wilson L, Maden M, Lumsden A. RALDH-independent generation of retinoic acid during vertebrate embryogenesis by CYP1B1. Development 2007, 134:1369–1383.
184. Elizondo G, Corchero J, Sterneck E, Gonzalez FJ. Feedback inhibition of the retinaldehyde dehydrogenase gene ALDH1 by retinoic acid through retinoic acid receptor α and CCAAT/enhancer-binding protein β. J Biol Chem 2000, 275:39747–39753.
185. Elizondo G, Medina-Diaz IM, Cruz R, Gonzalez FJ, Vega L. Retinoic acid modulates retinaldehyde dehydrogenase 1 gene expression through the induction of GADD153-C/EBPβ interaction. Biochem Pharmacol 2009, 77:248–257.
186. 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, 62:67–78.
187. Cerignoli F, Guo X, Cardinali B, Rinaldi C, Casaletto J, Frati L, Screpanti I, Gudas LJ, Gulino A, Thiele CJ, et al. retSDR1, a short-chain retinol dehydrogenase/reductase, is retinoic acid-inducible and frequently deleted in human neuroblastoma cell lines. Cancer Res 2002, 62:1196–1204.
188. Zolfaghari R, Chen Q, Ross AC. DHRS3, a retinal reductase, is differentially regulated by retinoic acid and lipopolysaccharide-induced inflammation in THP-1 cells and rat liver. Am J Physiol Gastrointest Liver Physiol 2012, 303:G578–G588.