The Journal of Nutritional Biochemistry
Volume 21, Issue 8 , Pages 710-716 , August 2010

Suppression of retinoic acid receptors may contribute to embryonic skeleton hypoplasia in maternal rats with chronic vitamin A deficiency

  • Na Li

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Shanshan Sun

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Di Wang

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Ping Yao

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Xuefeng Yang

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Hong Yan

      Affiliations

    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Yukai Du

      Affiliations

    • Department of Youngster and Woman’s Healthcare, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Chengjiang Ying

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • ,
  • Liegang Liu

      Affiliations

    • Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • MOE Key Lab of Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430030, P.R. China
    • Corresponding Author InformationCorresponding author. Department of Nutrition and Food Hygiene, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, P.R. China. Tel.: +86 27 83692711; fax: +86 27 83693307.

Received 18 November 2008 ,Revised 18 March 2009 ,Accepted 27 April 2009.

References 

  1. Zile MH. Function of vitamin A in vertebrate embryonic development. J Nutr. 2001;131(3):705–708
  2. Zile MH. Vitamin A and embryonic development: an overview. J Nutr. 1998;128(2 Suppl):455S–458S
  3. Kalter H, Warkany J. Experimental production of congenital malformations in mammals by metabolic procedure. Physiol Rev. 1959;39(1):69–115
  4. Warkany J. Manifestations of prenatal nutritional deficiency. Vitam Horm. 1945;3:73–103
  5. Warkany J, Roth C, Wilson JG. Multiple congenital malformations: a consideration of etiologic factors. Pediatrics. 1948;1:462–471
  6. White JC, Shankar VN, Highland M, Epstein ML, DeLuca HF, 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 U S A. 1998;95(23):13459–13464
  7. White JC, 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(2):263–284
  8. White JC, 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(6):374–384
  9. Clagett-Dame M, DeLuca HF. The role of vitamin A in mammalian reproduction and embryonic development. Annu Rev Nutr. 2002;22:347–381
  10. Giguère V. Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocr Rev. 1994;15(1):61–79
  11. Dollé P, Ruberte E, Leroy P, Morriss-Kay G, Chambon P. Retinoic acid receptors and cellular retinoid binding proteins. I. A systematic study of their differential pattern of transcription during mouse organogenesis. Development. 1990;110(4):1133–1151
  12. Ruberte E, Dolle P, Chambon P, Morriss-Kay G. Retinoic acid receptors and cellular retinoid binding proteins. II. Their differential pattern of transcription during early morphogenesis in mouse embryos. Development. 1991;111(1):45–60
  13. Ruberte E, Friederich V, Chambon P, Morriss-Kay G. Retinoic acid receptors and cellular retinoid binding proteins. III. Their differential transcript distribution during mouse nervous system development. Development. 1993;118(1):267–282
  14. McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell. 1992;68(2):283–302
  15. Krumlauf R. Hox genes in vertebrate development. Cell. 1994;78(2):191–201
  16. Marshall H, Morrison A, Studer M, Pöpperl H, Krumlauf R. Retinoids and Hox genes. FASEB J. 1996;10(9):969–978
  17. Ross SA, McCaffery PJ, Drager UC, De Luca LM. Retinoids in embryonal development. Physiol Rev. 2000;80(3):1021–1054
  18. Langston AW, Gudas LJ. Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6. Mech Dev. 1992;38(3):217–227
  19. Pöpperl H, Featherstone MS. Identification of a retinoic acid response element upstream of the murine Hox-4.2 gene. Mol Cell Biol. 1993;13(1):257–265
  20. Marshall H, Studer M, Pöpperl H, Aparicio S, Kuroiwa A, Brenner S, et al. A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature. 1994;370(6490):567–571
  21. Doerksen LF, Bhattacharya A, Kannan P, Pratt D, Tainsky MA. Functional interaction between a RARE and an AP-2 binding site in the regulation of the human HOX A4 gene promoter. Nucleic Acids Res. 1996;24(14):2849–2856
  22. Morrison A, Moroni MC, Ariza-McNaughton L, Krumlauf R, Mavilio F. In vitro and transgenic analysis of a human HOXD4 retinoid-responsive enhancer. Development. 1996;122(6):1895–1907
  23. Langston AW, Thompson JR, Gudas LJ. Retinoic acid-responsive enhancers located 3′ of the Hox A and Hox B homeobox gene clusters. J Biol Chem. 1997;272(4):2167–2175
  24. Huang D, Chen SW, Gudas LJ. Analysis of two distinct retinoic acid response elements in the homeobox gene Hoxb1 in transgenic mice. Dev Dyn. 2002;223(3):353–370
  25. Kelleher SL, Lönnerdal B. Long-term marginal intakes of zinc and retinol affect retinol homeostasis without compromising circulating levels during lactation in rats. J Nutr. 2001;131(12):3237–3242
  26. Gardner EM, Ross AC. Dietary vitamin A restriction produces marginal vitamin A status in young rats. J Nutr. 1993;123(8):1435–1443
  27. Menegola E, Broccia ML, Giavini E. Atlas of rat fetal skeleton double stained for bone and cartilage. Teratology. 2001;64(3):125–133
  28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 2001;25(4):402–408
  29. Kelleher SL, Lönnerdal B. Low vitamin a intake affects milk iron level and iron transporters in rat mammary gland and liver. J Nutr. 2005;135(1):27–32
  30. Cohlan SQ. Excessive intake of vitamin A during pregnancy as a cause of congenital anomalies in the rat. AMA Am J Dis Child. 1953;86(3):348–349
  31. Cui J, Michaille JJ, Jiang W, Zile MH. Retinoid receptors and vitamin A deficiency: differential patterns of transcription during early avian development and the rapid induction of RARs by retinoic acid. Dev Biol. 2003;260(2):496–511
  32. Gendron-Maguire M, Mallo M, Zhang M, Gridley T. Hoxa-2 mutant mice exhibit homeotic transformation of skeletal elements derived from cranial neural crest. Cell. 1993;75(7):1317–1331
  33. Rijli FM, Mark M, Lakkaraju S, Dierich A, Dollé P, Chambon P. A homeotic transformation is generated in the rostral branchial region of the head by disruption of Hoxa-2, which acts as a selector gene. Cell. 1993;75(7):1333–1349
  34. Patel CV, Gorski DH, LePage DF, Lincecum J, Walsh K. Molecular cloning of a homeobox transcription factor from adult aortic smooth muscle. J Biol Chem. 1992;267(36):26085–26090
  35. Tan DP, Ferrante J, Nazarali A, Shao X, Kozak CA, Guo V, et al. Murine Hox-1.11 homeobox gene structure and expression. Proc Natl Acad Sci U S A. 1992;89(14):6280–6284
  36. Jeannotte L, Lemieux M, Charron J, Poirier F, Robertson EJ. Specification of axial identity in the mouse: role of the Hoxa-5 (Hox1.3) gene. Genes Dev. 1993 Nov;7(11):2085–2096
  37. Fromental-Ramain C, Warot X, Lakkaraju S, Favier B, Haack H, Birling C, et al. Specific and redundant functions of the paralogous Hoxa-9 and Hoxd-9 genes in forelimb and axial skeleton patterning. Development. 1996;122(2):461–472
  38. Kondo T, Duboule D. Breaking colinearity in the mouse HoxD complex. Cell. 1999;97(3):407–417
  39. Kondo T, Dollé P, Zákány J, Duboule D. Function of posterior HoxD genes in the morphogenesis of the anal sphincter. Development. 1996;122(9):2651–2659
  40. Kondo T, Zákány J, Innis JW, Duboule D. Of fingers, toes and penises. Nature. 1997;390(6655):29
  41. Aubin J, Lemieux M, Tremblay M, Behringer RR, Jeannotte L. Transcriptional interferences at the Hoxa4/Hoxa5 locus: importance of correct Hoxa5 expression for the proper specification of the axial skeleton. Dev Dyn. 1998;212(1):141–156
  42. Kaiser ME, Merrill RA, Stein AC, 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(1):14–29
  43. See AW, Kaiser ME, White JC, 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(2):171–190
  44. Miller M, Humphrey J, Johnson E, Marinda E, Brookmeyer R, Katz J. Why do children become vitamiccn A deficient?. J Nutr. 2002;132(9 Suppl):2867S–2880S
  45. Underwood BA. Maternal vitamin A status and its importance in infancy and early childhood. Am J Clin Nutr. 1994;59(2 Suppl):517S–522S[discussion 522S–524S]

PII: S0955-2863(09)00098-9

doi: 10.1016/j.jnutbio.2009.04.011

The Journal of Nutritional Biochemistry
Volume 21, Issue 8 , Pages 710-716 , August 2010

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