Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-15T05:19:10.214Z Has data issue: false hasContentIssue false
  • English
  • Français

High-phosphorus diet stimulates receptor activator of nuclear factor-κB ligand mRNA expression by increasing parathyroid hormone secretion in rats

Published online by Cambridge University Press:  08 March 2007

Shin-ichi Katsumata ,
Ritsuko Masuyama ,
Mariko Uehara  and
Kazuharu Suzuki
Shin-ichi Katsumata
Affiliation:
Department of Nutritional Science, Faculty of Applied Bioscience, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan
Ritsuko Masuyama
Affiliation:
Department of Nutritional Science, Faculty of Applied Bioscience, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan
Mariko Uehara
Affiliation:
Department of Nutritional Science, Faculty of Applied Bioscience, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan
Kazuharu Suzuki*
Affiliation:
Department of Nutritional Science, Faculty of Applied Bioscience, Tokyo University of Agriculture, 1-1-1 Sakuragaoka, Setagaya-ku, Tokyo 156-8502, Japan
*
*Corresponding author: Dr Kazuharu Suzuki, fax +81 3 5477 2658, email [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

The purpose of the present study was to clarify the manner by which the supplementation of high-P diet induces bone loss. Eighteen 4-week-old male Wistar-strain rats were assigned randomly to three groups and fed diets containing three P levels (0·3, 0·9, and 1·5%) for 21d. A lower serum Ca concentration was observed in the rats fed on the 1·5% P diet than in the other two groups. Serum P and parathyroid hormone concentrations and urinary excretion of C-terminal telopeptide of type I collagen were elevated with increasing dietary P levels. Serum osteocalcin concentration was increased in the rats fed on the 1·5% P diet than in the other two groups. Bone formation rate of the lumbar vertebra was significantly increased in the two high-P groups than in the 0·3% P group. Osteoclast number was significantly increased with increasing dietary P levels. Bone mineral content and bone mineral density of the femur and lumbar vertebra and ultimate compression load of the lumbar vertebra were decreased with increasing dietary P levels. Additionally, ultimate bending load of the femur was decreased in the rats fed on the 1·5% P diet than in the other two groups. Receptor activator of NF-κB ligand (RANKL) mRNA expression in the femur was significantly higher with increasing dietary P levels. These results suggest that secondary hyperparathyroidism due to a high-P diet leads to bone loss via an increase in bone turnover. Furthermore, an increase in osteoclast number was caused by increased RANKL mRNA expression.

Keywords

High-phosphorus dietParathyroid hormoneReceptor activator of nuclear factor-κB ligand mRNA expressionBone loss
Type
Research Article
Information
British Journal of Nutrition , Volume 94 , Issue 5 , November 2005 , pp. 666 - 674
Copyright
Copyright © The Nutrition Society 2005

References

Almaden, Y, Canalejo, A, Hernandez, A, Ballesteros, E, Garcia, NS, Torres, A & Rodriguez, M (1996) Direct effect of phosphorus on PTH secretion from whole rat parathyroid glands in vitro. J Bone Miner Res 11, 970–976.CrossRefGoogle ScholarPubMed
Bauer, KD & Griminger, P (1983) Long-term effects of activity and of calcium and phosphorus intake on bones and kidneys of female rats. J Nutr 113, 2011–2021.CrossRefGoogle ScholarPubMed
Bell, RR, Draper, HH, Tzeng, DY, Shin, HK & Schmidt, GR (1977) Physiological responses of human adults to foods containing phosphate additives. J Nutr 107, 42–50.CrossRefGoogle ScholarPubMed
Bonde, M, Qvist, P, Fledelius, C, Riis, BJ & Christiansen, C (1994) Immunoassay for quantifying type I collagen degradation products in urine evaluated. Clin Chem 40, 2022–2025.CrossRefGoogle Scholar
Bonde, M, Qvist, P, Fledelius, C, Riis, BJ & Christiansen, C (1995) Applications of an enzyme immunoassay for a new marker of bone resorption (CrossLaps): follow-up on hormone replacement therapy and osteoporosis risk assessment. J Clin Endocrinol Metab 80, 864–868.Google ScholarPubMed
Brown, JP, Delmas, PD, Malaval, L, Chapuy, MC, Delmas, PD, Edouard, C & Meunier, PJ (1984) Serum bone gla protein: a specific marker for bone formation in post-menopausal osteoporosis. Lancet i, 1091–1093.CrossRefGoogle Scholar
Calvo, MS, Kumar, R & Heath, H III (1988) Elevated secretion and action of serum parathyroid hormone in young adults consuming high phosphorus, low calcium diets assembled from common foods. J Clin Endocrinol Metab 66, 823–829.CrossRefGoogle ScholarPubMed
Caputi, M, Melo, CA & Baralle, FE (1995) Regulation of fibronectin expression in rat regenerating liver. Nucleic Acids Res 23, 238–243.CrossRefGoogle ScholarPubMed
Draper, HH, Sie, TL & Bergan, JG (1972) Osteoporosis in aging rats induced by high phosphorus diets. J Nutr 102, 1133–1142.CrossRefGoogle ScholarPubMed
Gimblet, EG, Marney, AF & Bonsnes, RW (1967) Determination of calcium and magnesium in serum, urine, diets and stool by atomic absorption spectrophotometry. Clin Chem 13, 204–214.CrossRefGoogle ScholarPubMed
Gomori, G (1942) A modification of the colorimetric phosphorus determination for use with the photoelectric colorimeter. J Lab Clin Med 27, 955–960.Google Scholar
Grey, A, Mitnick, M, Masiukiewicz, U, Sun, B, Rudikoff, S, Jilka, RL, Manolagas, SC & Insobna, K (1999) A role for interleukin-6 in parathyroid hormone-induced bone resorption in vivo. Endocrinology 140, 4683–4690.CrossRefGoogle ScholarPubMed
Hsu, H, Lacey, DL, Dunstan, CR et al. (1999) Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc Natl Acad Sci USA 96, 3540–3545.CrossRefGoogle ScholarPubMed
Katsumata, S, Masuyama, R, Koshihara, M, Matsuzaki, H, Uehara, M & Suzuki, K (2004) High phosphorus diet changes phosphorus metabolism regardless of PTH action in rats. Biosci Biotechnol Biochem 68, 243–246.CrossRefGoogle ScholarPubMed
Katsumata, S, Masuyama, R, Uehara, M & Suzuki, K (2004) Decreased mRNA expression of the PTH/PTHrP receptor and type II sodium-dependent phosphate transporter in the kidney of rats fed a high phosphorus diet accompanied with a decrease in serum calcium concentration. Biosci Biotechnol Biochem 68, 2484–2489.CrossRefGoogle ScholarPubMed
Kroll, MH (2000) Parathyroid hormone temporal effects on bone formation and resorption. Bull Math Biol 62, 163–188.CrossRefGoogle ScholarPubMed
Lacy, DL, Timms, E, Tan, H et al. (1998) Osteoprotegerin (OPG) ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93, 165–176.CrossRefGoogle Scholar
Lee, S & Lorenzo, JA (1999) Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology 140, 3552–3561.CrossRefGoogle ScholarPubMed
Ma, YL, Cain, RL, Halladay, DL, Yang, X, Zeng, Q, Miles, RR, Chandrasekhar, S, Martin, TJ & Onyia, JE (2001) Catabolic effects of continuous human PTH (1–38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology 142, 4047–4054.CrossRefGoogle ScholarPubMed
Martin, TJ & Ng, KW (1994) Mechanisms by which cells of the osteoblast lineage control osteoclast formation and activity. J Cell Biochem 56, 357–366.CrossRefGoogle ScholarPubMed
Masuyama, R, Kajita, Y, Odachi, J, Uehara, M, Shigematsu, T, Suzuki, K & Goto, S (2000a) Chronic phosphorus supplementation decreases the expression of renal PTH/PTHrP receptor mRNA in rats. Am J Nephrol 20, 491–495.CrossRefGoogle ScholarPubMed
Masuyama, R, Nakaya, Y, Katsumata, S, Kajita, Y, Uehara, M, Tanaka, S, Sakai, A, Kato, S, Nakamura, T & Suzuki, K (2003) Dietary calcium and phosphorus ratio regulates bone mineralisation and turnover in vitamin D receptor knockout mice by affecting intestinal calcium and phosphorus absorption. J Bone Miner Res 18, 1217–1226.CrossRefGoogle ScholarPubMed
Masuyama, R, Uehara, M & Suzuki, K (2000b) High P diet induces acute secretion of parathyroid hormone without alteration of serum calcium levels in rats. Biosci Biotechnol Biochem 64, 2316–2319.CrossRefGoogle Scholar
Masuyama, R, Uehara, M, Suzuki, K & Goto, S (1995) The action of magnesium in reducing renal calcification in rats receiving high phosphorus supplemented diet. Nutr Res 15, 1673–1682.CrossRefGoogle Scholar
Myers, DE, Collier, FM, Minkin, C, Wang, H, Holloway, WR, Malakellis, M & Nicholson, GC (1999) Expression of functional RANK on mature rat and human osteoclasts. FEBS Lett 463, 295–300.CrossRefGoogle ScholarPubMed
Ravn, P, Rix, M, Andreassen, H, Clemmesen, B, Bidstrup, M & Gunnes, M (1997) High bone turnover is associated with low bone mass and spinal fracture in postmenopausal women. Calcif Tissue Int 60, 255–260.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH & Fahey, GC (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.CrossRefGoogle Scholar
Reiss, E, Canterbury, JM, Bercovitz, MA & Kaplan, EL (1970) The role of phosphate in the secretion of parathyroid hormone in man. J Clin Invest 49, 2146–2149.CrossRefGoogle ScholarPubMed
Sakai, A, Nishida, S, Okimoto, N, Okazaki, Y, Hirano, T, Norimura, T, Suda, T & Nakamura, T (1998) Bone marrow cell development and trabecular bone dynamics after ovariectomy in ddy mice. Bone 23, 443–451.CrossRefGoogle ScholarPubMed
Seto, H, Aoki, K, Kasugai, S & Ohya, K (1999) Trabecular bone turnover, bone marrow cell development, and gene expression of bone matrix proteins after low calcium feeding in rats. Bone 25, 687–695.CrossRefGoogle ScholarPubMed
Takahashi, N, Yamana, H, Yoshiki, S, Roodman, GD, Mundy, GR, Jones, SJ, Boyde, A & Suda, T (1988) Osteoclast-like cell formation and its regulation by osteotropic hormones in mouse bone marrow cultures. Endocrinology 122, 1373–1382.CrossRefGoogle ScholarPubMed
Takeda, E, Sakamoto, K, Yokota, K, Shinohara, M, Taketani, Y, Morita, K, Yamamoto, H, Miyamoto, K & Shibayama, M (2002) Phosphorus supply per capita from food in Japan between 1960 and 1995. J Nutr Sci Vitaminol 48, 102–108.CrossRefGoogle ScholarPubMed
Tanaka, S, Tsurukami, H, Sakai, A, Okimoto, N, Ikeda, S, Otomo, H & Nakamura, T (2003) Effects of 1,25(OH) 2 D 3 on turnover, mineralization, and strength of bone in growing rats with liver cirrhosis induced by administration of carbon tetrachloride. Bone 32, 275–283.CrossRefGoogle ScholarPubMed
Tsukii, K, Shima, N, Mochizuki, S et al. (1998) Osteoclast differentiation factor mediates an essential signal for bone resorption induced by 1α,25-dihydroxyvitamin D 3, prostaglandin E 2, or parathyroid hormone in the microenvironment of bone. Biochem Biophys Res Commun 246, 337–341.CrossRefGoogle ScholarPubMed
Urena, P, Kong, XF, Abou-Samra, AB, Juppner, H, Kronenberg, HM, Potts, JT Jr & Segre, GV (1993) Parathyroid hormone (PTH)/PTH-related peptide receptor messenger ribonucleic acids are widely distributed in rat tissues. Endocrinology 133, 617–623.CrossRefGoogle ScholarPubMed
Weir, EC, Lowik, CWGM, Paliwal, I & Insogna, KL (1996) Colony stimulating factor-1 plays a role in osteoclast formation and function in bone resorption induced by parathyroid hormone and parathyroid hormone-related protein. J Bone Miner Res 11, 1474–1481.CrossRefGoogle Scholar
Yasuda, H, Shima, N, Nakagawa, N et al. (1998a) Identity of osteoclastgenesis inhibitory factor (OCIF) and osteoprotegerin (OPG): a mechanism by which OPG/OCIF inhibits osteoclastgenesis in vitro. Endocrinology 39, 1329–1337.CrossRefGoogle Scholar
Yasuda, H, Shima, N, Nakagawa, N et al. (1998b) Osteoclast differentiation factor is a ligand for osteoprotegerine/osteoclastgenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA 95, 3597–3602.CrossRefGoogle Scholar