Iron deficiency and marginal vitamin A deficiency affect growth, hematological indices and the regulation of iron metabolism genes in rats

Journal of Nutrition

Volumn 132, Issue 12, 2002, Pages 3607-3615

  Strube, Yi Ning J ^a   Beard, John L ^a   Ross, A Catharine ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Ferritin; Iron deficiency; Marginal vitamin A deficiency; Rats; Transferrin

Indexed keywords

CERULOPLASMIN; FERRITIN; HEMOPEXIN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN LIGHT CHAIN; IRON; MESSENGER RNA; RETINOL; RETINOL BINDING PROTEIN; TRANSFERRIN; TRANSFERRIN RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY GROWTH; CONTROLLED STUDY; FEEDING; HEMATOCRIT; HEMOGLOBIN DETERMINATION; IRON BLOOD LEVEL; IRON DEFICIENCY; IRON METABOLISM; IRON RESTRICTION; LIVER LEVEL; MALE; NONHUMAN; PROTEIN BLOOD LEVEL; RAT; RETINOL DEFICIENCY; VITAMIN BLOOD LEVEL; VITAMIN SUPPLEMENTATION; WEIGHT GAIN;

ANIMALIA; EUKARYOTA;

EID: 0036898096     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/132.12.3607     Document Type: Article

References (71)

1. DeMaeyer, E. & Adiels-Tegman, M. (1985) The prevalence of anaemia in the world. World Health Stat. Q. 38: 302-316.
2. Stephenson, L. S., Latham, M. C. & Ottesen, E. A. (2000) Global malnutrition. Parasitology 121: S5-S22.
3. West, K. P., Jr., LeClerq, S. C., Shrestha, S. R., Wu, L.S.F., Pradhan, E. K., Khatry, S. K., Katz, J., Adhikari, R. & Sommer, A. (1997) Effects of vitamin A on growth of vitamin A-deficient children: Field studies in Nepal. J. Nutr. 127: 1957-1965.
4. Findlay, G. M. & MacKenzie, R. D. (1922) The bone marrow in deficiency diseases. J. Pathol. 25: 402-403.
5. Koessler, K., Maurer, S. & Loughlin, R. (1926) The relation of anemia, primary and secondary, to vitamin A deficiency. J. Am. Med. Assoc. 87: 476-482.
6. Blackfan, K. D. & Wolbach, S. B. (1933) Vitamin A deficiency in infants, a clinical and pathological study. J. Pediatr. 3: 679-706.
7. Mejia, L. A., Hodges, R. E., Arroyave, G., Viteri, M. D. & Torun, B. (1977) Vitamin A deficiency and anemia in Central American children. Am. J. Clin. Nutr. 30: 1175-1184.
8. Mejia, L. A. & Chew, F. (1988) Hematological effect of supplementing anemic children with vitamin A alone and in combination with iron. Am. J. Clin. Nutr. 48: 595-600.
9. Bloem, M. W., Wedel, M., van Agtmaal, E. J., Speek, A. J., Saowakontha, S. & Schreurs, W.H.P. (1990) Vitamin A intervention: Short-term effects of a single, oral, massive dose on iron metabolism. Am. J. Clin. Nutr. 51: 76-79.
10. van Stuijvenberg, M. E., Kruger, M., Badenhorst, C. J., Mansvelt, E. P. & Laubscher, J.A. (1997) Response to an iron fortification programme in relation to vitamin A status in 6-12-year-old school children. Int. J. Food Sci. Nutr. 48: 41-49.
11. Bloem, M. W., Wedel, M., Egger, J. J., Speek, A. J., Schrijver, J., Saowakontha, S. & Schreurs, W.H.P. (1989) Iron metabolism and vitamin A deficiency in children in Northeast Thailand. Am. J. Clin. Nutr. 50: 332-338.
12. Suharno, D., West, C. E., Muhilal, Logman, M.H.G., deWaart, F. G., Karyadi, D. & Hautvast, J.G.A.J. (1992) Cross-sectional study on the iron and vitamin A status of pregnant women in West Java, Indonesia. Am. J. Clin. Nutr. 56: 988-993.
13. Bloem, M. W., Wedel, M., Egger, R. J., Speek, A. J., Chuslip, K., Saowakontha, S. & Schreurs, W.H.P. (1989) A prevalence study of vitamin A deficiency and xerophthalmia in northeastern Thailand. Am. J. Epidemiol. 129: 1095-1103.
14. Hodges, R. E., Rucker, R. B. & Gardner, R. H. (1979) Vitamin A deficiency and abnormal metabolism of iron. Ann. N.Y. Acad. Sci. 58-61.
15. Panth, M., Shatrugna, V., Yasodhara, P. & Sivakumar, B. (1990) Effect of vitamin A supplementation on haemoglobin and vitamin A levels during pregnancy. Br. J. Nutr. 64: 351-358.
16. Semba, R. D., Muhilal & West, K. P., Jr. (1992) Impact of vitamin A supplementation on hematological indicators of iron metabolism and protein status in children. Nutr. Res. 12: 469-478.
17. Kolsteren, P., Rahman, S. R., Hilderbrand, K. & Diniz, A. (1999) Treatment for iron deficiency anaemia with a combined supplementation of iron, vitamin A and zinc in women of Dinajpur, Bangladesh. Eur. J. Clin. Nutr. 53: 102-106.
18. Muhilal, Permeisih, D., Idjradinata, Y. R., Muherdiyantiningsih & Karyadi, D. (1988) Vitamin A-fortified monosodium glutamate and health growth, and survival of children: A control field trial. Am. J. Clin. Nutr. 48: 1271-1276.
19. Mejia, L. A. & Arroyave, G. (1982) The effect of vitamin A fortification of sugar on iron metabolism in preschool children in Guatemala. Am. J. Clin. Nutr. 36: 87-93.
20. Angeles-Agdeppa, I., Schultink, W., Sastroamidjojo, S., Gross, R. & Karyadi, D. (1997) Weekly micronutrient supplementation to build iron stores in female Indonesian adolescents. Am. J. Clin. Nutr. 66: 177-183.
21. Mejia, L. A., Hodges, R. E. & Rucker, R. B. (1979) Role of vitamin A in the absorption, retention and distribution of iron in the rat. J. Nutr. 109: 129-137.
22. Beynen, A. C., Sijatsma, K. W., van den Berg, G. J., Lammens, A. G. & West, C. E. (1991) Iron metabolism in vitamin A deficiency. In: Trace Elements in Man and Animals - 7 (Momcilovic, B., ed.), pp. 21-5-21-6. IMI, Zagreb, Yugoslavia.
23. Roodenburg, A. J., West, C. E., Yu, S. & Beynen, A. C. (1994) Comparison between time-dependent changes in iron metabolism of rats as induced by marginal deficiency of either vitamin A or iron. Br. J. Nutr. 71: 687-699.
24. Roodenburg, A.J.C., West, C. E., Beguin, Y., Van Dijk, J. E., Van Eijk, H. G., Marx, J. J. M. & Beynen, A. C. (2000) Indicators of erythrocyte formation and degradation in rats with either vitamin A or iron deficiency. J. Nutr. Biochem. 11: 223-230.
25. Roodenburg, A.J.C., West, C. E., Hovenier, R. & Beynen, A. C. (1996) Supplemental vitamin A enhances the recovery from iron deficiency in rats with chronic vitamin A deficiency. Br. J. Nutr. 75: 623-636.
26. Green, M. H., Uhl, L. & Balmer Green, J. (1985) A multicompartmental model of vitamin A kinetics in rats with marginal liver vitamin A stores. J. Lipid Res. 26: 806-818.
27. Underwood, B. A. (1998) From research to global reality: The micronutrient story. J. Nutr. 128: 145-151.
28. Borel, M. J., Smith, S. H., Brigham, D. E. & Beard, J. L. (1991) The impact of varying degrees of iron nutriture on several functional consequences of iron deficiency in rats. J. Nutr. 121: 729-736.
29. Beard, J. L., Zhan, C. S. & Brigham, D. E. (1995) Growth in iron-deficient rats. Proc. Soc. Exp. Biol. Med. 209: 65-72.
30. Roodenburg, A.J.C., West, C. E. & Beynen, A. C. (1996) Vitamin A status affects the efficacy of iron repletion in rats with mild iron deficiency. J. Nutr. Biochem. 7: 99-105.
31. Bowman, T. A., Goonewardene, I. M., Pasatiempo, A.M.G., Ross, A. C. & Taylor, C. E. (1990) Vitamin A deficiency decreases natural killer cell activity and interferon production in rats. J. Nutr. 120: 1264-1273.
32. Pasatiempo, A.M.G., Taylor, C. E. & Ross, A. C. (1991) Vitamin A status and the immune response to pneumococcal polysaccharide: Effects of age and early stages of retinol deficiency in the rat. J. Nutr. 121: 556-562.
33. Davila, M. E., Norris, L., Cleary, M. P. & Ross, A. C. (1985) Vitamin A during lactation: Relationship of maternal diet to milk vitamin A content and to the vitamin A status of lactating rats and their pups. J. Nutr. 115: 1033-1041.
34. Reeves, P. G., Nielsen, F. H. & Fahey, G. C., Jr. (1993) AIN-93 purified diets for laboratory rodents: Final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123: 1939-1951.
35. Torrance, J. D. & Bothwell, T. H. (1980) Tissue iron stores. In: Methods in Hematology (Cook, J. D. ed.). Churchill Livingston, New York, NY.
36. Ross, A. C. (1986) Separation and quantitation of retinyl esters and retinol by high-performance liquid chromatography. Methods Enzymol. 123: 68-74.
37. Zolfaghari, R. & Ross, A. C. (1994) Effect of vitamin A deficiency and retinoic acid repletion on intestinal and hepatic apolipoprotein A-I mRNA levels of adult rats. J. Lipid Res. 35: 1985-1992.
38. Rosales, F. J., Ritter, S. J., Zolfaghari, R., Smith, J. E. & Ross, A. C. (1996) Effects of acute inflammation on plasma retinol, retinol-binding protein, and its mRNA in the liver and kidneys of vitamin A-sufficient rats. J. Lipid Res. 37: 962-971.
39. Han, J., Day, J. R., Thomson, K., Connor, J. R. & Beard, J. L. (2000) Iron deficiency alters H- and L-ferritin expression in rat brain. Cell. Mol. Biol. (Noisy-le-grand) 46: 517-528.
40. Han, J., Day, J. R., Connor, J. R. & Beard, J. L. (2002) Iron deficiency in rats alters brain transferrin and transferrin receptor message and protein distributions. J. Nutr. 132: 2769-2774.
41. Simovich, M. J., Conrad, M. E., Umbreit, J. N., Moore, E. G., Hainsworth, L. N. & Smith, H. K. (2002) Cellular location of proteins related to iron absorption and transport. Am. J. Hematol. 69: 164-170.
42. Crompton, D. W. & Nesheim, M. C. (2002) Nutritional impact of intestinal helminthiasis during the human life cycle. Annu. Rev. Nutr. 22: 35-59.
43. Rahmathullah, L., Underwood, B. A., Thulasiraj, R. D. & Milton, R. C. (1991) Diarrhea, respiratory infections, and growth are not affected by a weekly low-dose vitamin A supplement: A masked, controlled field trial in children in southern India. Am. J. Clin. Nutr. 54: 568-577.
44. Ramakrishnan, U., Latham, M. C. & Abel, R. (1995) Vitamin A supplementation does not improve growth of preschool children: A randomized, doubleblind field trial in south India. J. Nutr. 125: 202-211.
45. Fawzi, W. W., Herrera, M. G., Willett, W. C., Nestel, P., El Amin, A. & Mohamed, K. A. (1997) Dietary vitamin A intake in relation to child growth. Epidemiology 8: 402-407.
46. Tanumihardjo, S. A., Cheng, J. C., Permaesih, D., Muherdiyantiningsih, Rustan, E., Muhilal, Karyadi, D. & Olson, J. A. (1996) Refinement of the modified-dose-response test as a method for assessing vitamin A status in a field setting: Experience with Indonesian children. Am. J. Clin. Nutr. 64: 966-971.
47. Benevenga, N. J., Calvert, C., Eckhert, C. D., Fahey, G. C., Greger, J. L., Keen, C. L., Knapka, J. J., Magalhaes, H., Oftedal, O. T., Reeves, P. G., Shaw, H. A., Smith, J. E. & Steele, R. D. (1995) Nutrient Requirements of the Laboratory Rat. Nutrient Requirements of Laboratory Animals, 4th Ed. National Academy Press, Washington, DC.
48. Rosales, F. J., Jang, J. T., Pinero, D. J., Erikson, K. M., Beard, J. L. & Ross, A.C. (1999) Iron deficiency in young rats alters the distribution of vitamin A between plasma and liver and between hepatic retinol and retinyl esters. J. Nutr. 129: 1223-1228.
49. Mejia, L. A., Hodges, R. E. & Rucker, R. B. (1979) Clinical signs of anemia in vitamin A-deficient rats. Am. J. Clin. Nutr. 32: 1439-1444.
50. Eisenstein, R. S. & Blemings, K. P. (1998) Iron regulatory proteins, iron responsive elements and iron homeostasis. J. Nutr. 128: 2295-2298.
51. Ponka, P., Beaumont, C. & Richardson, D. R. (1998) Function and regulation of transferrin and ferritin. Semin. Hematol. 35: 35-54.
52. Hugly, S. & Griswold, M. (1987) Regulation of levels of specific Sertoli cell mRNAs by vitamin A. Dev. Biol. 121: 316-324.
53. Skinner, M. K. & Griswold, M. D. (1982) Secretion of testicular transferrin by cultured Sertoli cells is regulated by hormones and retinoids. Biol. Reprod. 27: 211-221.
54. Idzerda, R. L., Huebers, H., Finch, C. A. & McKnight, G. S. (1986) Rat transferrin gene expression: Tissue-specific regulation by iron deficiency. Proc. Natl. Acad. Sci. U.S.A. 83: 3723-3727.
55. Ponka, P. (1997) Tissue-specific regulation of iron metabolism and heme synthesis: Distinct control mechanisms in erythroid cells. Blood 89: 1-25.
56. Levi, S., Yewdall, S. J., Harrison, P. M., Santambrogio, P., Cozzi, A., Rovida, E., Albertini, A. & Arosio, P. (1992) Evidence that H- and L-chains have co-operative roles in the iron-uptake mechanism of human ferritin. Biochem. J. 288:591-596.
57. Kwak, E. L., Larochelle, D. A., Beaumont, C., Torti, S. V. & Torti, F. M. (1995) Role for NF-κB in the regulation of ferritin H by tumor necrosis factor-α. J. Biol. Chem. 270: 15285-15293.
58. Tsuji, Y., Moran, E., Torti, S. V. & Torti, F. M. (1999) Transcriptional regulation of the mouse ferritin H gene. Involvement of p300/CBP adaptor proteins in FER-1 enhancer activity. J. Biol. Chem. 274: 7501-7507.
59. Tsuji, Y., Torti, S. V. & Torti, F. M. (1998) Activation of the ferritin H enhancer, FER-1, by the cooperative action of members of the AP1 and Sp1 transcription factor families. J. Biol. Chem. 273: 2984-2992.
60. Wu, K. J., Polack, A. & Dalla-Favera, R. (1999) Coordinated regulation of iron-controlling genes, H-ferritin and IRP2, by c-MYC. Science (Washington, DC) 283: 676-679.
61. White, K. & Munro, H. N. (1988) Induction of ferritin subunit synthesis by iron is regulated at both the transcriptional and translational levels. J. Biol. Chem. 263: 8938-8942.
62. Miyajima, H., Nishimura, Y., Mizoguchi, K., Sakamoto, M., Shimizu, T. & Honda, N. (1987) Familial apoceruloplasmin deficiency associated with blepharospasm and retinal degeneration. Neurology 37: 761-767.
63. Mukhopadhyay, C. K., Mazumder, B. & Fox, P. L. (2000) Role of hypoxia-inducible factor-1 in transcriptional activation of ceruloplasmin by iron deficiency. J. Biol. Chem. 275: 21048-21054.
64. Mukhopadhyay, C. K., Attieh, Z. K. & Fox, P. L. (1998) Role of ceruloplasmin in cellular iron uptake. Science (Washington, DC) 279: 714-717.
65. Attieh, Z. K., Mukhopadhyay, C. K., Seshadri, V., Tripoulas, N. A. & Fox, P. L. (1999) Ceruloplasmin ferroxidase activity stimulates cellular iron uptake by a trivalent cation-specific transport mechanism. J. Biol. Chem. 274: 1116-1123.
66. Barber, E. F. & Cousins, R. J. (1987) Induction of ceruloplasmin synthesis by retinoic acid in rats: Influence of dietary copper and vitamin A status. J. Nutr. 117: 1615-1622.
67. Eskew, J. D., Vanacore, R. M., Sung, L., Morales, P. J. & Smith, A. (1999) Cellular protection mechanisms against extracellular heme, heme-hemopexin, but not free heme, activates the N-terminal c-jun kinase. J. Biol. Chem. 274: 638-648.
68. Gardner, E. M. & Ross, A. C. (1993) Dietary vitamin A restriction produces marginal vitamin A status in young rats. J. Nutr. 123: 1435-1443.
69. Jang, J. T., Green, J. B., Beard, J. L. & Green, M. H. (2000) Kinetic analysis shows that iron deficiency decreases liver vitamin A mobilization in rats. J. Nutr. 130: 1291-1296.
70. Rajan, N., Blaner, W. S., Soprano, D. R., Suhara, A. & Goodman, D. S. (1990) Cellular retinol-binding protein messenger RNA levels in normal and retinoid-deficient rats. J. Lipid Res. 31: 821-829.
71. Ye, Z. & Connor, J. R. (2000) Identification of iron responsive genes by screening cDNA libraries from suppression subtractive hybridization with antisense probes from three iron conditions. Nucleic Acids Res. 28: 1802-1807.