High dietary intake of retinol leads to bone marrow hypoxia and diaphyseal endosteal mineralization in rats

Bone

Volumn 48, Issue 3, 2011, Pages 496-506

  Lind, Thomas ^a   Lind, P Monica ^a   Jacobson, Annica ^a   Hu, Lijuan ^a   Sundqvist, Anders ^a,f   Risteli, Juha ^b   Yebra Rodriguez, Africa ^c   Rodriguez Navarro, Alejandro ^d   Andersson, Göran ^e   Melhus, Håkan ^a  

^a UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^b OULU UNIVERSITY HOSPITAL   (Finland)

^c UNIVERSITY OF JAÉN   (Spain)

^d UNIVERSITY OF GRANADA   (Spain)

^e KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^f UPPSALA UNIVERSITY   (Sweden)

Author keywords

Bone mineralization; Nutrition; Osteoporosis; Retinol; Rodent

Indexed keywords

ESRUM RETINOL TRANSPORT PROTEIN; PLASMA PROTEIN; RETINOL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE DENSITY; BONE MARROW HYPOXIA; BONE MINERALIZATION; BONE TURNOVER; CAPILLARY BLOOD; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DIAPHYSIS; DIETARY INTAKE; DOSE RESPONSE; ENDOTHELIUM CELL; HISTOPATHOLOGY; HUMAN; HYPOXEMIA; INFRARED SPECTROSCOPY; MALE; NONHUMAN; OSTEOCLAST; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINOL INTOXICATION;

ANIMALS; ANOXIA; BIOLOGICAL MARKERS; BONE MARROW; BONE REMODELING; CALCIFICATION, PHYSIOLOGIC; CELL LINE; DIAPHYSES; DIET; ENDOTHELIAL CELLS; FEEDING BEHAVIOR; IMMUNOHISTOCHEMISTRY; MALE; MICE; OSTEOCLASTS; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; STAINING AND LABELING; TOMOGRAPHY, X-RAY COMPUTED; VITAMIN A;

EID: 79751532689     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2010.10.169     Document Type: Article

References (57)

1. Binkley N., Krueger D. Hypervitaminosis A and bone. Nutr Rev 2000, 58:138-144.
2. Blomhoff R., Blomhoff H.K. Overview of retinoid metabolism and function. J Neurobiol 2006, 66:606-630.
3. Hua S., Kittler R., White K.P. Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Cell 2009, 137:1259-1271.
4. WHO Global prevalence of vitamin A deficiency in populations at risk 1995-2005 2009, World Health Organization, Geneva.
5. Melhus H., Michaëlsson K., Kindmark A., Bergström R., Holmberg L., Mallmin H., et al. 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.
6. Michaëlsson K., Lithell H., Vessby B., Melhus H. Serum retinol levels and the risk of fracture. N Engl J Med 2003, 348:287-294.
7. Ribaya-Mercado J.D., Blumberg J.B. Vitamin A: is it a risk factor for osteoporosis and bone fracture?. Nutr Rev 2007, 65:425-438.
8. Moore T., Wang Y.L. Hypervitaminosis A. Biochem J 1945, 39:222-228.
9. Wolbach S.B. Vitamin-A deficiency and excess in relation to skeletal growth. J Bone Joint Surg 1947, 29:171-192.
10. Clark I., Smith M.R. Effects of hypervitaminosis A and D on skeletal metabolism. J Biol Chem 1964, 239:1266-1271.
11. Melhus H. Vitamin A and fracture risk. Nutritional aspects of bone health, The Royal Society of Chemistry 2003, 368-402. Cambridge RSC publishing. S.A. New, J.-P. Bonjour (Eds.).
12. Kneissel M., Studer A., Cortesi R., Susa M. Retinoid-induced bone thinning is caused by subperiosteal osteoclast activity in adult rodents. Bone 2005, 36:202-214.
13. Johansson S., Lind P.M., Hakansson H., Oxlund H., Orberg J., Melhus H. Subclinical hypervitaminosis A causes fragile bones in rats. Bone 2002, 31:685-689.
14. Lind P.M., Johansson S., Rönn M., Melhus H. Subclinical hypervitaminosis A in rat: measurements of bone mineral density (BMD) do not reveal adverse skeletal changes. Chem Biol Interact 2006, 159:73-80.
15. Boskey A.L., Gadaleta S., Gundberg C., Doty S.B., Ducy P., Karsenty G. Fourier transform infrared microspectroscopic analysis of bones of osteocalcin-deficient mice provides insight into the function of osteocalcin. Bone 1998, 23:187-196.
16. Lind P.M., Larsson S., Johansson S., Melhus H., Wikström M., Lindhe O., et al. Bone tissue composition, dimensions and strength in female rats given an increased dietary level of vitamin A or exposed to 3, 3′, 4, 4′, 5-pentachlorobiphenyl (PCB126) alone or in combination with vitamin C. Toxicology 2000, 151:11-23.
17. Risteli J., Elomaa I., Niemi S., Novamo A., Risteli L. Radioimmunoassay for the pyridinoline cross-linked carboxy-terminal telopeptide of type I collagen: a new serum marker of bone collagen degradation. Clin Chem 1993, 39:635-640.
18. Hollberg K., Hultenby K., Hayman A., Cox T., Andersson G. Osteoclasts from mice deficient in tartrate-resistant acid phosphatase have altered ruffled borders and disturbed intracellular vesicular transport. Exp Cell Res 2002, 279:227-238.
19. Hollberg K., Marsell R., Norgård M., Larsson T., Jonsson K.B., Andersson G. Osteoclast polarization is not required for degradation of bone matrix in rachitic FGF23 transgenic mice. Bone 2008, 42:1111-1121.
20. Melhus H., Båvik C.O., Rask L., Peterson P.A., Eriksson U. Epitope mapping of a monoclonal antibody that blocks the binding of retinol-binding protein to its receptor. Biochem Biophys Res Commun 1995, 210:105-112.
21. Kang S., Bennett C.N., Gerin I., Rapp L.A., Hankenson K.D., Macdougald O.A. Wnt signaling stimulates osteoblastogenesis of mesenchymal precursors by suppressing CCAAT/enhancer-binding protein alpha and peroxisome proliferator-activated receptor gamma. J Biol Chem 2007, 282:14515-14524.
22. Rodriguez-Navarro A.B., Romanek C.S., Alvarez-Lloret P., Gaines K.F. Effect of in ovo exposure to PCBs and Hg on Clapper Rail bone mineral chemistry from a contaminated salt marsh in coastal Georgia. Environ Sci Technol 2006, 40:4936-4942.
23. Hough S., Avioli L.V., Muir H., Gelderblom D., Jenkins G., Kurasi H., et al. Effects of hypervitaminosis A on the bone and mineral metabolism of the rat. Endocrinology 1988, 122:2933-2939.
24. Horstman L.L., Jy W., Jimenez J.J., Ahn Y.S. Endothelial microparticles as markers of endothelial dysfunction. Front Biosci 2004, 9:1118-1135.
25. Hirose S., Li M., Kojima T., de Freitas P.H., Ubaidus S., Oda K., et al. A histological assessment on the distribution of the osteocytic lacunar canalicular system using silver staining. J Bone Miner Metab 2007, 25:374-382.
26. Trechsel U., Stutzer A., Fleisch H. Hypercalcemia induced with an arotinoid in thyroparathyroidectomized rats. New model to study bone resorption in vivo. J Clin Invest 1987, 80:1679-1686.
27. Rissanen J.P., Suominen M.I., Peng Z., Halleen J.M. Secreted tartrate-resistant acid phosphatase 5b is a marker of osteoclast number in human osteoclast cultures and the rat ovariectomy model. Calcif Tissue Int 2008, 82:108-115.
28. Rissanen J.P., Suominen M.I., Peng Z., Morko J., Rasi S., Risteli J., et al. Short-term changes in serum PINP predict long-term changes in trabecular bone in the rat ovariectomy model. Calcif Tissue Int 2008, 82:155-161.
29. Singer C.F., Hudelist G., Schreiber M., Kubista E. Pharmacological modulation of IGF serum concentrations as a therapeutic approach to control the growth of malignant breast tumors. Drugs Today (Barc) 2003, 39:115-125.
30. Yakar S., Rosen C.J., Bouxsein M.L., Sun H., Mejia W., Kawashima Y., et al. Serum complexes of insulin-like growth factor-1 modulate skeletal integrity and carbohydrate metabolism. Faseb J 2009, 23:709-719.
31. Bielohuby M., Matsuura M., Herbach N., Kienzle E., Slawik M., Hoeflich A., et al. Short term exposure to low-carbohydrate/high fat diets induces low bone mineral density and reduces bone formation in rats. J Bone Miner Res 2010, 25:275-284.
32. Nerurkar M.K., Sahasrabudhe M.B. Metabolism of calcium, phosphorus and nitrogen in hypervitaminosis A in young rats. Biochem J 1956, 63:344-349.
33. Conaway H.H., Persson E., Halén M., Granholm S., Svensson O., Pettersson U., et al. Retinoids inhibit differentiation of hematopoietic osteoclast progenitors. Faseb J 2009, 23:3526-3538.
34. Mizoguchi T., Muto A., Udagawa N., Arai A., Yamashita T., Hosoya A., et al. Identification of cell cycle-arrested quiescent osteoclast precursors in vivo. J Cell Biol 2009, 184:541-554.
35. Kindmark A., Melhus H., Ljunghall S., Ljunggren O. Inhibitory effects of 9-cis and all-trans retinoic acid on 1,25 (OH)2 vitamin D3-induced bone resorption. Calcif Tissue Int 1995, 57:242-244.
36. Fell H.B., Mellanby E. The effect of hypervitaminosis A on embryonic limb bones cultivated in vitro. J Physiol 1952, 116:320-349.
37. Larson R.S., Tallman M.S. Retinoic acid syndrome: manifestations, pathogenesis, and treatment. Best Pract Res Clin Haematol 2003, 16:453-461.
38. Perrotta S., Nobili B., Rossi F., Criscuolo M., Iolascon A., Di Pinto D., et al. Infant hypervitaminosis A causes severe anemia and thrombocytopenia: evidence of a retinol-dependent bone marrow cell growth inhibition. Blood 2002, 99:2017-2022.
39. Hatake K., Uwai M., Ohtsuki T., Tomizuka H., Izumi T., Yoshida M., et al. Rare but important adverse effects of all-trans retinoic acid in acute promyelocytic leukemia and their management. Int J Hematol 1997, 66:13-19.
40. Kini A.R., Peterson L.A., Tallman M.S., Lingen M.W. Angiogenesis in acute promyelocytic leukemia: induction by vascular endothelial growth factor and inhibition by all-trans retinoic acid. Blood 2001, 97:3919-3924.
41. Tallman M.S., Andersen J.W., Schiffer C.A., Appelbaum F.R., Feusner J.H., Ogden A., et al. Clinical description of 44 patients with acute promyelocytic leukemia who developed the retinoic acid syndrome. Blood 2000, 95:90-95.
42. Ingber D., Folkman J. Inhibition of angiogenesis through modulation of collagen metabolism. Lab Invest 1988, 59:44-51.
43. Yang M.H., Wu M.Z., Chiou S.H., Chen P.M., Chang S.Y., Liu C.J., et al. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 2008, 10:295-305.
44. Suzuki Y., Komi Y., Ashino H., Yamashita J., Inoue J., Yoshiki A., et al. Retinoic acid controls blood vessel formation by modulating endothelial and mural cell interaction via suppression of Tie2 signaling in vascular progenitor cells. Blood 2004, 104:166-169.
45. Lendahl U., Lee K.L., Yang H., Poellinger L. Generating specificity and diversity in the transcriptional response to hypoxia. Nat Rev Genet 2009, 10:821-832.
46. Wang Y., Wan C., Deng L., Liu X., Cao X., Gilbert S.R., et al. The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 2007, 117:1616-1626.
47. Catto M. Ischaemia of bone. J Clin Pathol Suppl R Coll Pathol 1977, 11:78-93.
48. Bloomfield S.A., Hogan H.A., Delp M.D. Decreases in bone blood flow and bone material properties in aging Fischer-344 rats. Clin Orthop Relat Res 2002, 396:248-257.
49. Lehner C.E., Adams W.M., Dubielzig R.R., Palta M., Lanphier E.H. Dysbaric osteonecrosis in divers and caisson workers. An animal model. Clin Orthop Relat Res 1997, 344:320-332.
50. Kalantari F., Miao D., Emadali A., Tzimas G.N., Goltzman D., Vali H., et al. Cellular and molecular mechanisms of abnormal calcification following ischemia-reperfusion injury in human liver transplantation. Mod Pathol 2007, 20:357-366.
51. Brodt M.D., Pelz G.B., Taniguchi J., Silva M.J. Accuracy of peripheral quantitative computed tomography (pQCT) for assessing area and density of mouse cortical bone. Calcif Tissue Int 2003, 73:411-418.
52. Knowles H.J., Athanasou N.A. Acute hypoxia and osteoclast activity: a balance between enhanced resorption and increased apoptosis. J Pathol 2009, 218:256-264.
53. White J.A., Beckett-Jones B., Guo Y.D., Dilworth F.J., Bonasoro J., Jones G., et al. cDNA cloning of human retinoic acid-metabolizing enzyme (hP450RAI) identifies a novel family of cytochromes P450. J Biol Chem 1997, 272:18538-18541.
54. Taneja R., Bouillet P., Boylan J.F., Gaub M.P., Roy B., Gudas L.J., et al. 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.
55. Lee S.H., Lee Y.J., Han H.J. Effect of arachidonic acid on hypoxia-induced IL-6 production in mouse ES cells: involvement of MAPKs, NF-kappaB, and HIF-1alpha. J Cell Physiol 2010, 222:574-585.
56. Mallia A.K., Smith J.E., Goodman D.W. Metabolism of retinol-binding protein and vitamin A during hypervitaminosis A in the rat. J Lipid Res 1975, 16:180-188.
57. Smith F.R., Goodman D.S. Vitamin A transport in human vitamin A toxicity. N Engl J Med 1976, 294:805-808.