Abstract
The effects of dietary vitamin E (VIT E) and lipids on tissue lipid peroxidation and fatty acid composition, epiphyseal growth plate cartilage development, and trabecular bone formation were evaluated in chicks. A 2×2 factorial design was followed using two levels (30 and 90 IU/kg of diet) of dl-α-tocopheryl acetate and two different dietary lipids. The basal semipurified diet contained one of the following lipid treatments: anhydrous butter oil (40 g/kg)+ soybean oil (60 g/kg), [BSO], or soybean oil (100 g/kg), [SBO]. After 14 days of feeding, the level of α-tocopherol in plasma was higher and thiobarbituric acid reactive substances (TBARS) were less in plasma and liver of chicks supplemented with 90 IU of VIT E compared with those given 30 IU of VIT E. Body weights and tibiotarsal bone lengths were not affected by the dietary treatments Saturated fatty acids (14:0, 15:0, 16:0, 17:0, and 18:0) were increased in tibiotarsal bone of chicks fed the BSO diet. In contrast, total polyunsaturated fatty acids and the ratio of unsaturated fatty acids/saturated fatty acids were higher in plasma of chicks fed SBO compared with the values from chicks fed BSO. The thickness of the entire growth plate cartilage and the lower hypertrophic chondrocyte zone was significantly greater in chicks fed 90 IU/kg of VIT E. Kinetic parameters on bone histomorphometry indicated that mineral apposition rate was higher in chicks fed 90 IU/kg of VIT E. The interaction effect between the VIT E and BSO treatments led to the highest trabecular bone formation rate among the groups. These data suggest that VIT E protects against cellular lipid peroxidation in cartilage to sustain normal bone growth and modeling.
Similar content being viewed by others
References
Hunziker EB, Schenk RK, Crus-Orive LM (1987) Quantification of chondrocyte performance in growth-plate cartilage during longitudinal bone growth. J Bone Joint Surg 69:162–173
Kwan APL, Dickson IR, Freemont AJ, Grant ME (1989) Comparative studies of type X collagen expression in normal and rachitic chicken epiphyseal cartilage. J Cell Biol 109:1849–1856
Poole AR, Pidoux I (1989) Immunoelectron microscopy of type X collagen in endochondral ossification. J Cell Biol 109:2547–2554
Oshima O, Leboy PS, McDonald SA, Tuan RS, Shapiro IM (1989) Developmental expression of genes in chick growth cartilage detected by in situ hybridization. Calcif Tissue Int 45:182–192
Nilsson A, Isgaard J, Lindahl A, Dahlstrom A, Skottner A, Isaksson O (1986) Regulation by growth hormone of number of chondrocytes containing IGF-I in rat growth plate. Science 233:571–574
Logan A, Hill DJ, Gonzalez AM (1991) Expression and release of basic fibroblast growth factor by epiphyseal growth plate chondrocytes. Ann NY Acad Sci 638:459–462
Thorp BH, Anderson I, Jakowlew SB (1992) Transforming growth factors-β1, -β2 and -β3 in cartilage and bone during endochondral ossification in the chick. Development 114:907–911
Rosselot G, Vasilatos-Younken R, Leach RM (1994) Effect of growth hormone, insulin-like growth factor I, basic fibroblast growth factor, and transforming growth factor β on cell proliferation and proteoglycan synthesis by avian postembryonic growth plate chondrocytes. J Bone Miner Res 9:431–439
Leboy PS, Vaias L, Uschmann B, Golub E, Adams SL, Pacifici M (1989) Ascorbic acid induces alkaline phosphatase, type X collagen, and calcium deposition in chick chondrocytes. J Biol Chem 264:17281–17286
Pacifici M, Golden EB, Iwamoto M, Adams SL (1991) Retinoic acid treatment induces type X collagen gene expression in cultured chick chondrocytes. Exp Cell Res 195:38–46
Alini M, Carey D, Hirata S, Grynpas MD, Pidoux I, Poole AR (1994) Cellular and matrix changes before and at the time of calcification in the growth plate studied in vitro: arrest of type X collagen synthesis and net loss of collagen when calcification is initiated. J Bone Miner Res 9:1077–1087
Watkins BA (1991) Importance of essential fatty acids and their derivatives in poultry. J Nutr 121:1475–1485
Wuthier RE (1988) Mechanism of matrix vesicle-mediated mineralization of cartilage. ISI Atlas Sci Biochem 1:231–241
Raisz LG (1993) Bone cell biology: new approaches and unanswered questions. J Bone Miner Res 8:S457-S465
Jee WSS, Akamine T, Ke HZ, Li XJ, Tang LY, Zeng QQ (1992) Prostaglandin E2 prevents disuse-induced cortical bone loss. Bone 13:153–159
Mori S, Jee WSS, Li XJ (1992) Production of new trabecular bone in osteogenic, ovariectomized rats by prostaglandin E2. Calcif Tissue Int 50:80–87
Marks SC Jr., Miller SC (1993) Prostaglandins and the skeleton: the legacy and challenges of two decades of research. Endocrine J 1:337–344
Xu H, Watkins BA, Adkisson HD (1994) Dietary lipids modify the fatty acid composition of cartilage, isolated chondrocytes and matrix vesicles. Lipids 29:619–625
Watkins BA, Shen CL, McMurtry JP, Xu H, Bain SD (1995) Dietary lipids alter histomorphometry and concentrations of fatty acids and insulin-like growth factor-I in tibiotarsal bone. J Nutr (in press)
Garrett IR, Boyce BF, Oreffo ROC, Bonewald L, Poser J, Mundy GR (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639
Matsumoto H, Silverton SF, Debolt K, Shapiro IM (1991) Superoxide dismutase and catalase activities in the growth cartilage: relationship between oxidoreductase activity and chondrocyte maturation. J Bone Miner Res 6:569–574
Ames BN, Shigenage MK, Hagen TM (1993) Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 90:7915–7922
Halliwell B (1994) Free radicals and antioxidants: a personal view. Nutr Rev 52:253–265
Burton GW, Traber MG (1990) Vitamin E: antioxidant activity, biokinetics, and bioavailability. Ann Rev Nutr 10:357–382
Schwartz ER (1979) Effect of vitamins C and E on sulfated proteoglycan metabolism and sulfatase and phosphatase activities in organ cultures of human cartilage. Calcif Tissue Int 28:201–208
Ebina Y, Okada S, Hamazaki S, Toda Y, Midorikawa O (1991) Impairment of bone formation with aluminum and ferric nitrilotriacetate complexes. Calcif Tissue Int 48:28–36
National Research Council (1994) Nutrient requirements of poultry, 9th ed. National Academy Press, Washington, DC
Prabha PS, Das UN, Koratkar R, Sagar PS, Ramesh G (1990) Free radical generation, lipid peroxidation and essential fatty acids in uncontrolled essential hypertension. Prostaglandins Leukot Essent Fatty Acids 41:27–33
Lee HS, Scallany AS (1987) Measurement of free and bound malondialdehyde in vitamin E-deficient and-supplemented rat liver tissues. Lipids 22:104–107
MacCrehan WA (1990) Determination of retinol, α-tocopherol, and β-carotene in serum by liquid chromatography. Methods Enzymol 189:172–182
Baron R, Vignery A, Neff L, Silvergate A, Santa Maria A (1983) Processing of undecalcified bone specimens for bone histomorphometry. In: Recker RR (ed) Bone histomorphometry: techniques and interpretation. Boca Raton, FL, pp 13–35
Ruhl-Fehlert CI, Ludi E (1987) A new methyl methacrylate embedding method for rapid histochemical demonstration of phosphatases in undecalcified bone tissues. J Histotechnol 10:103–106
Schenk RK, Olah AJ, Herrmann W (1984) Preparation of calcified tissues for light microscopy. In: Dickson GR (ed) Methods of calcified tissue preparation. Elsevier, NY, pp 1–56
Seifert MF (1994) Lack of evidence for rickets in the osteopetrotic rat mutation, toothless. J Bone Miner Res 9:1813–1821
Howlett CR (1979) The fine structure of the proximal growth plate of avian tibia. J Anat 128:377–399
Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ (1987) Bone histomorphometry: standardization of nomenclature, symbols and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2:595–610
SAS Institute Inc (1989) SAS/STAT User's guide: version 6, 4th ed, Cary, NC
Snedecor GW, Cochran, WG (1967) Statistical methods. Iowa State University Press, Ames, pp 343–363
Neter J, Wasserman W (1974) Applied linear statistical models. Richard D. Irwin, Inc., Homewood, IL
Parker RS (1989) Dietary and biochemical aspects of vitamin E. Adv Food Nutr Res 33:157–232
Hu ML, Frankel EN, Leibovitz BE, Tappel AL (1989) Effect of dietary lipids and vitamin E on in vitro lipid peroxidation in rat liver and kidney homogenates. J Nutr 119:1574–1582
Barclay LRC, Bailey AMH, Kong D (1985) The antioxidant activity of α-tocopherol-bovine albumin complex in micellar and liposome autoxidations. J Biol Chem 260:15809–15814
Niki E, Yamamoto Y, Takahashi M, Komuro E, Miyama Y (1989) Inhibition of oxidation of biomembrane by tocopherol. Ann NY Acad Sci 570:23–31
Frei BB, Ames BN (1993) Relative importance of vitamin E in antiperoxidative defenses in human blood plasma and lowdensity lipoprotein (LDL). In: Packer L, Fuchs J (eds) Vitamin E in health and disease. Marcel Dekker, Inc. New York, pp 131–139
Watkins BA, Bain SD, Newbrey JW (1989) Eicosanoic fatty acid reduction in the tibiotarsus of biotin-deficient chicks. Calcif Tissue Int 45:41–46
Watkins BA, Whitehead CC, Duff SRI (1991) Hydrogenated oils reduce tissue concentrations of n-6 polyunsaturates and may contribute to dyschondroplasia in broilers. Br Poultry Sci 32:1109–1119
Gallop PM, Paz MA, Fluckiger R, Henson E (1993) Is the antioxidant, anti-inflammatory putative new vitamin, PQQ, involved with nitric oxide in bone metabolism? Connect Tissue Res 29:153–161
Cohen ME, Meyer DM (1993) Effect of dietary vitamin E supplementation and rotational stress on alveolar bone loss in rice rats. Arch Oral Biol 38:601–606
Maenpaa PH, Pirhonen A, Pirskanen A, Pekkanen J, Alfthan G, Kivela SL, Nissinen A (1989) Biochemical indicators related to antioxidant status and bone metabolic activity in Finnish elderly men. Int J Vitam Nutr Res 59:14–19
Galotto M, Campanile G, Robino G, Cancedda FD, Bianco P, Cancedda R (1994) Hypertrophic chondrocytes undergo further differentiation to osteoblast-like cells and participate in the initial bone formation in developing chick embryo. J Bone Miner Res 9:1239–1249
Adkisson HD, Risener FS Jr, Zarrinkar PP, Walla MD, Christie WW, Wuthier RE (1991) Unique fatty acid composition of normal cartilage: discovery of high levels of n-9 eicosatrienoic acid and low levels of n-6 polyunsaturated fatty acids. FASEB J 5:344–353
Author information
Authors and Affiliations
Additional information
Approved as Journal Paper Number 14556 of the Purdue Agricultural Experiment Station
Rights and permissions
About this article
Cite this article
Xu, H., Watkins, B.A. & Seifert, M.F. Vitamin E stimulates trabecular bone formation and alters epiphyseal cartilage morphometry. Calcif Tissue Int 57, 293–300 (1995). https://doi.org/10.1007/BF00298885
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00298885