Effects of Soy and Isoflavones on Bone Metabolism in Growing Female Rats

성장기 암컷 쥐에서 콩 단백질과 Isoflavones가 골 대사에 미치는 영향

  • 최미자 (계명대학교 식품영양학과) ;
  • 조현주 (계명대학교 식품영양학과)
  • Published : 2003.07.01

Abstract

The purpose of this study was to determine which differences in the source of protein (soy vs casein) and isoflavones in soy protein are responsible for the differential effects of bone marks and hormones in growing female rats. Forty-two 21-day-old Sprague-Dawley female rats were randomly assigned to one of three groups, consuming casein (control group), soy protein isolate (57 mg isoflavones/100 g diet), or soy protein concentrate (about 1.2 mg isoflavones/100 g diet). All rats were fed on experimental diet and deionized water ad libitum for 9 weeks. Bone formation was measured by serum osteocalcin and alkaline phosphatase (ALP) concentrations. And bone resorption rate was measured by deoxypyridinoline (DPD) crosslinks immunoassay and corrected for creatinine. Serum osteocalcin, growth hormone, estrogen and calcitonin were analyzed using radioimmunoassay kits. Diet did not affect weight gain and mean food intake. Food efficiency ratio was lower in the soy protein groups. The soy isolate group had a higher ALP and osteocalcin concentration and lower crosslinks value than the casein group. Therefore, the soy isolate groups had a higher bone formation/resorption ratio than the casein group. And, the soy group had significantly higher growth hormone than the casein group. The findings of this study suggest that soy protein and isoflavones are beneficial for bone formation in growing female rats. Therefore, exposure to these soy protein and isoflavones early in life may have benefits for osteoporosis prevention.

References

  1. Kim WY. Osteoporosis and dietary factors. Korean J Nutrition 27: 636-645, 1994
  2. Wasnich RD. Bone mass measurements in diagnosis and assessment of therapy. Am J Med 91 (suppl5): 54s-58s, 1991 https://doi.org/10.1016/0002-9343(91)90249-W
  3. Adlercreutz H, Mazur W. Phytoestrogen and western disease. Ann Med 29: 95-120, 1997
  4. Cooper C, Campion G, Melton LJ. Hip fractures in the elderly; a world-wide projection. Osteoporosis Int 2: 285-289, 1992 https://doi.org/10.1007/BF01623184
  5. Scheiber MD, Rebar RW. Isoflavones and postmenopausal bone health. Menopause 6: 233-241, 1999 https://doi.org/10.1097/00042192-199906030-00010
  6. Miksick RJ. Estrogenic flavonoids: structural requirements for biological activity. PSEBM 208: 44-50, 1995
  7. Song TT, Hendrich S, Murphy PA. Estrogenic activity of glycitein, a Soy Isoflavone. J Agric Food Chem 47: 1607-1610, 1999 https://doi.org/10.1021/jf981054j
  8. Dwyer JT, Goldin BR, Saul N, Gualtieri L, Barakat S, Adlercreutz H. Tofu and soy drinks contain phytoestrogens. J Am Diet Assoc 94: 739-743, 1994 https://doi.org/10.1016/0002-8223(94)91939-9
  9. Martin RM, Horwitz KB, Ryan DS, McGuire WL. Phytoestrogen interaction with estrogen receptors in human breast cancer cells. Endocrinology 198: 1860-1867, 1978
  10. Shutt DA, Cox RI. Steroid and phytoestrogen binding to sheep uterine receptors in vitro. J Endocrino 52: 299-310, 1972 https://doi.org/10.1677/joe.0.0520299
  11. Choi MJ. Effects of soy protein on bone mineral content and bone mineral density in growing male rats. Kor J Nutr 35(4): 409-413, 2002
  12. Choi MJ. Cho HJ. Effects of soy protein and isoflavones on bone mineral density in growing female rats. Korean J Nutrition 36(5) : 452-458, 2003
  13. Hannon R, Blumsohn A, Dehaimi AW, Eastell R. The use of biochemical markers of bone turnover to monitor the skeletal response to hormone replacement therapy. Bone 10 (suppl2) : 549s-555s, 1995
  14. Andreassen TT, Jorgensen PH, Flyvbjerg A, Orskov H, Oxlund H. Growth hormone stimulates bone formation and strength of cortical bone in aged rats. J Bone Miner Res 10: 1057-1067, 1995 https://doi.org/10.1002/jbmr.5650100710
  15. Draper CR, Edel MJ, Dick IM, Randall AG, Martin GB, Raince RL. Phytoestrogens reduce bone loss and bone resorption in ophorectomized rats. J Nutr 127: 1795-1799, 1997
  16. Alekel DL, Germain AS, Peterson CT, Hanson KB, Stewart JW, Toda T. Isoflavone-rich soy protein isolate attenuates bone loss in the lumbar spine of perimenopausal women. Am J Clin Nutr 72: 844-852, 2000
  17. Reeves PG, Nielsen FH, Fahey GC. AIN-93 purified diets for laboratory rodents. J Nutr 123: 1939-1951, 1993
  18. Xing S, Cekan SZ, Dicafalusy U. Validation of radioimunoassay for estadiol-17 isotope dilution-mass spectrometry and a test of radiochemical purity. Clin Chem Acta 135: 189-201, 1983 https://doi.org/10.1016/0009-8981(83)90135-3
  19. Guarnero P, Grimaux M, Seguin P, Delmas P. Characterization of immunoreactive forms of human osteocalcin generated in vivo and in vitro. J Bone Min Res 9: 692-698, 1994
  20. Nanda N, Joshi H, Subbarao SK, Sharma VP. Two-site immuno-radiometricassay (IRMA): detection, efficiency, and procedural modifications. J Am Mosq Control Assoc 10: 225-227, 1994
  21. Mahan LK, Escott-Stump S. Krauses's food, nutrition & diet therapy. 9th ed. W.B. Saunders Company, Philadelphia, pp346, 1996
  22. Garmero P, Delmas PD. New developments in biochemical markers of osteoporosis. Calcif Tissue Intl 59(7): 2-9, 1996 https://doi.org/10.1007/s002239900168
  23. Johnell O, Oden A, De Laet C, Garnero P, Delmas PD, Kanis JA. Biochemical indices of bone turnover and the assessment of fracture probability. Osteoporos Int 13: 523-526, 2002 https://doi.org/10.1007/s001980200068
  24. Delmas PD, Stenner D, Wahner HW, Mann KG, Riggs BL. Increase in serum bone gamma-carboxyglutamic acid protein with aging in women. Implications for the mechanism of age-related bone loss. J Clin Invest 71: 1316-1321, 1983 https://doi.org/10.1172/JCI110882
  25. Eyre DR. Biochemical markers of bone turnover. Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism. 3rd ed. in: 3Favus MJ. Raven Press, New York, pp114-118, 1996
  26. Lian JB, Gundberg CM. Osteocalcin biochemical considerations and clinical applications. Clin Ortho Rei Res 226: 267-291, 1998
  27. Murakami H, Nakamura T, Tsurukami H, Abe M, Barbier A, Suzuke K. Effects of tiludronate on bone mass, structure, and turnover, at the epiphyseal, primary, and secondary spongiosa in the proximal tibia growing rats after sciatic neurectomy. J Bone Miner Res 9: 1355-1364, 1994 https://doi.org/10.1002/jbmr.5650090906
  28. Mathur SR. Effect of protein source and excercise on skeletal health of growing female rats. Dissertation of Ph.D in Texas Woman's University, 1998
  29. Hauschka PV, Lian JB, Dole DEC, Gundberg CM. Osteocalcin and matrix gla protein: vitamin K-dependent proteins in bone. Physiol Rev 69: 990-1047, 1989
  30. Delmas PD. Biological markers of bone turnover for the clinical investigation of osteoporosis. Osteoporosis Int (suppl): s81-s86, 1993 https://doi.org/10.1007/BF01621873
  31. Chae JH. The effect of isoflavones on bone mineral density and bone mineral content in growing male rats. Master's thesis, Keimyung University, 2002
  32. Calvo MS, Bell RR, Forbes RM. Effect of protein-induced calciuria on calcium metabolism and bone status in adult rats. J Nutr 112: 1401-1409, 1982
  33. Bonaccorsi G, Albertazzi P, Constantino D. Soy phytoestrogen and bone. N Am Menopause Soc Meet 44 (abstract) : 44, 1997
  34. Mei J, Yeung SS, Kung AW. High dietary phytoestrogen intake is associated with higher bone mineral density in postmenopausal but not premenopausal women. J Clin Endocrinol Metab 86 (11) : 5217-5221, 2001 https://doi.org/10.1210/jc.86.11.5217
  35. Picherit C, Bennetau-Pelissero C, Chanternne B, Lebecque P, Cavicco MJ, Barlet JP, Coxam V. Soybean isoflavones dose-dependently reduce bone turnover but do not reverse established osteopenia in adult ovariectomized rats. J Nutr 131: 723-728, 2001
  36. Uesugi T, Toda T, Tsuji K, Ishida H. Comparative study on reduction of bone loss and lipid metabolism abnormality in ovariectomized rats by soy isoflavones, daidzin, genistin, and glycitin. Biol Pharm Bull 24(4) : 368-372, 2001 https://doi.org/10.1248/bpb.24.368
  37. Jung SH. The effect of dietary protein source and sulfur amino acid content on bone metabolism in male rats. Master's thesis, Keimyung University, 1995
  38. Komm BS, Terpening CM, Benz DJ, Graeme KA, Gallegos A, Korc M, Greene GL, O'Malley BW, Haussler MR. Estrogen binding, receptor mRNA, and biologic response in osteoblast-like osteosarcoma cells. Science 241: 81-84, 1998 https://doi.org/10.1126/science.3164526
  39. Min HK. Osteoporosis. J Korean Soc Internal Medicine 34: 442-445, 1976
  40. Kalu DN, Masoro EJ, Yu Bp, Hardin RR, Hollis BW. Modulation of age related hyperparathyroidism and senile bone loss in fischer rats by soy protein and food restriction. Endocrinology 122: 1847-1854, 1998 https://doi.org/10.1210/endo-122-5-1847
  41. Gruber HF, Ivey JL, Baylink DJ. Long Term Calcitonin Therapy in postmenopausal osteoporosis. Metabolism 33: 295-303, 1984 https://doi.org/10.1016/0026-0495(84)90187-2
  42. Lee DH, Lee HS, Kim MH, Yoon ME, Sung CJ. Effect of isoflavones supplementation on bone mineral density and sex hormones in postmenopausal women. Korean J Nutrition 35: 863-869. 2002
  43. Lowenstein J, Wiencke J, Lee MM, Miike R, Kirk M. Stimulatory influence of soy protein isolate on breast sedretion in pre- and postmenopausal women. Cancer Epodemiol Biomarkers Prev 5: 785-794, 1996
  44. Arjmandi BH, Alekel L, Hollis BW. Dietary soybean protein prevents bone loss in an ovariectomized osteoporosis. J Nutr 126: 161-167, 1996
  45. Fanti O, Faugere MC, Gang Z, Schmidt J, Cohen D, Malluche HH. Systematic administration of genistein partially prevents bone loss in ovariectomized rats in a nonestrogen-like mechanism. Am J Clin Nutr 68 (suppl): 1517s(abs), 1998
  46. Kim MS. Beneficial effect of soy isoflavone on bone loss and hyperlipidemia in ovariectomized rats. Dissertation of Ph.D, Seoul National University, 1999
  47. Lely AJ. Growth Hormone and aging. GH & IGF Res 9: 117-119, 1999 https://doi.org/10.1016/S1096-6374(99)80023-9
  48. Dean HJ, Kellett JG, Bala RM. The effect of growth hormone treatment on somatomedin levels in growth hormone deficient children. J clin Endocrinol Metab 55: 1167-1173, 1982 https://doi.org/10.1210/jcem-55-6-1167
  49. Monson JP, Arake WM, Carroll PV, Weaver JU, Rodriguez-Arnao J, Savage MO. Influence of growth hormone on accretion of bone mass. Horm Res 58 (Suppl) 1: 52s-56s, 2002
  50. Attie KM. The importance of growth hormone replacement therapy for bone mass in young adults with growth hormone deficiency. J Pediatr Endocrinol Metab 13(suppl): 1011-1021, 2000
  51. Ki OH, Kim DY, Yong HI, Woo JT, Kim SW, Yang IM, Kim JW. Changes of bone turnover markers after treatment with growth retardation. J Korea Soc Endocrinol 9: 344-349, 1994
  52. Nass R, Pezzoli SS, Chapman IM, Patrie J, Hintz RL, Hartman ML, Thorner MO. IGF-I does not affect the net increase in GH release in response to arginine. Am J Physiol Endocrinol Metab 283(4): E702-710, 2002
  53. Pfeuffer M, Wuttke, Baryh CA. Influence of different dietary proteins on plasma growth hormone in rats. Z Ernahrungggswiss 27(4): 229-35, 1988 https://doi.org/10.1007/BF02019511
  54. Kim KL, Kim WY. The effect of soy protein and casein on serum lipid, amino acid. Korean J Nutr 17: 309-310, 1983
  55. Khalil DA, Lucas EA, Juma S, Smith BJ, Payton ME, Arjmandi BH. Soy protein supplementation increases serum insulin-like growth factor-I in young and old men but does not affect markers of bone metabolism. J Nutr 132(9): 2605-2608, 2002