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Published in: BMC Complementary Medicine and Therapies 1/2017

Open Access 01-12-2017 | Research article

Effects of Salvia miltiorrhiza extract with supplemental liquefied calcium on osteoporosis in calcium-deficient ovariectomized mice

Authors: Bongkyun Park, Hae Seong Song, Jeong Eun Kwon, Se Min Cho, Seon-A Jang, Mi Yeon Kim, Se Chan Kang

Published in: BMC Complementary Medicine and Therapies | Issue 1/2017

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Abstract

Background

Extracts from Salvia miltiorrhiza Bunge have been used in traditional Asian medicine to treat coronary heart disease, chronic renal failure, atherosclerosis, myocardial infraction, angina pectoris, myocardial ischemia, dysmenorrheal, neurasthenic insomnia, liver fibrosis and cirrhosis. The aim of the study was to investigate the anti-RANK signal effect of the combination of S.miltiorrhiza Bunge (SME) and liquefied calcium (LCa) supplement with ovariectomized (OVX-SML) mice, a osteoporosis animal model. Results were compared to 17β-estradiol (E2) treatment.

Methods

A total of 70 female ICR strain mice (7 weeks) were randomly divided into 10 groups with 7 mice in each group as follows: (1) sham-operated control mice (sham) received daily oral phosphate-buffered-saline (PBS) of equal volumes through oral administration. (2) OVX mice received a daily oral administration of PBS (OVX). (3) OVX mice treated daily with 50 mg/kg b.w./ day of SME (4) with 100 mg/kg b.w./day of SME or (5) with 200 mg/kg b.w./day of SME via oral administration. (6) OVX mice treated daily with 50 mg/kg b.w./day of SML (7) with 100 mg/kg b.w./day of SML or (8) with 200 mg/kg b.w./day of SML via oral administration. (9) OVX mice treated daily with 10 ml/kg b.w./day of LCa (10) OVX mice received i.p. injections of 17β-estradiol (E2) (0.1 mg/kg b.w./day) three times per week for 12 weeks.

Results

micro-CT analysis revealed that oral administration of SML inhibited tibial bone loss, sustained trabecular bone state, and ameliorated bone biochemical markers. In addition, SML administration compared to SEM and LCa reduced serum levels of RANKL, osteocalcin and BALP through increased serum levels of OPG and E2 in OVX mice. SML also had more beneficial effects on protection of estrogen-dependent bone loss through blocking expression of TRAF6 and NFTAc1 and produces cathepsin K and calcitonin receptor to develop osteoclast differentiation.

Conclusion

These data suggest that S. miltiorrhiza Bunge combined with liquefied calcium supplement has an inhibitory activity in OVX mice. This result implies the possibility of a pharmacological intervention specifically directed toward a disease such as osteoporosis where decreased bone strength increases the risk of a broken bone.
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Literature
1.
go back to reference Farrokhi S, Tashman S, Gil AB, Klatt BA, Fitzgerald GK. Are the kinematics of the knee joint altered during the loading response phase of gait in individuals with concurrent knee osteoarthritis and complaints of joint instability? A dynamic stereo X-ray study. Clin Biomech. 2012;27(4):384–9.CrossRef Farrokhi S, Tashman S, Gil AB, Klatt BA, Fitzgerald GK. Are the kinematics of the knee joint altered during the loading response phase of gait in individuals with concurrent knee osteoarthritis and complaints of joint instability? A dynamic stereo X-ray study. Clin Biomech. 2012;27(4):384–9.CrossRef
3.
go back to reference Roman-Blas JA, Castañeda S, Largo R, Herrero-Beaumont G. Osteoarthritis associated with estrogen deficiency. Arthritis research & therapy. 2009;11(5):1.CrossRef Roman-Blas JA, Castañeda S, Largo R, Herrero-Beaumont G. Osteoarthritis associated with estrogen deficiency. Arthritis research & therapy. 2009;11(5):1.CrossRef
4.
go back to reference Fraser L-A, Vogt KN, Adachi JD, Thabane L. Fracture risk associated with continuation versus discontinuation of bisphosphonates after 5 years of therapy in patients with primary osteoporosis: a systematic review and meta-analysis. Ther Clin Risk Manag. 2011;7:157–66.CrossRefPubMedPubMedCentral Fraser L-A, Vogt KN, Adachi JD, Thabane L. Fracture risk associated with continuation versus discontinuation of bisphosphonates after 5 years of therapy in patients with primary osteoporosis: a systematic review and meta-analysis. Ther Clin Risk Manag. 2011;7:157–66.CrossRefPubMedPubMedCentral
5.
go back to reference Koo HJ, Sohn E-H, Kim Y-J, Jang S-A, Namkoong S, Kang SC. Effect of the combinatory mixture of Rubus Coreanus Miquel and Astragalus Membranaceus Bunge extracts on ovariectomy-induced osteoporosis in mice and anti-RANK signaling effect. J Ethnopharmacol. 2014;151(2):951–9.CrossRef Koo HJ, Sohn E-H, Kim Y-J, Jang S-A, Namkoong S, Kang SC. Effect of the combinatory mixture of Rubus Coreanus Miquel and Astragalus Membranaceus Bunge extracts on ovariectomy-induced osteoporosis in mice and anti-RANK signaling effect. J Ethnopharmacol. 2014;151(2):951–9.CrossRef
6.
go back to reference Abuohashish HM, Ahmed MM, Al-Rejaie SS, Eltahir KE. The antidepressant bupropion exerts alleviating properties in an ovariectomized osteoporotic rat model. Acta Pharmacol Sin. 2015;36(2):209.CrossRefPubMed Abuohashish HM, Ahmed MM, Al-Rejaie SS, Eltahir KE. The antidepressant bupropion exerts alleviating properties in an ovariectomized osteoporotic rat model. Acta Pharmacol Sin. 2015;36(2):209.CrossRefPubMed
7.
go back to reference Thompson D, Simmons H, Pirie C, Ke H. FDA Guidelines and animal models for osteoporosis. Bone. 1995;17(4):S125–33.CrossRef Thompson D, Simmons H, Pirie C, Ke H. FDA Guidelines and animal models for osteoporosis. Bone. 1995;17(4):S125–33.CrossRef
8.
go back to reference Abukhadir S S, Mohamed N, Mohamed N. Pathogenesis of alcohol-induced osteoporosis and its treatment: a review. Curr Drug Targets. 2013;14(13):1601–10.CrossRefPubMed Abukhadir S S, Mohamed N, Mohamed N. Pathogenesis of alcohol-induced osteoporosis and its treatment: a review. Curr Drug Targets. 2013;14(13):1601–10.CrossRefPubMed
9.
go back to reference You L, Sheng Z-Y, Tang C, Chen L, Pan L, Chen J-Y. High cholesterol diet increases osteoporosis risk via inhibiting bone formation in rats. Acta Pharmacol Sin. 2011;32(12):1498.CrossRefPubMedPubMedCentral You L, Sheng Z-Y, Tang C, Chen L, Pan L, Chen J-Y. High cholesterol diet increases osteoporosis risk via inhibiting bone formation in rats. Acta Pharmacol Sin. 2011;32(12):1498.CrossRefPubMedPubMedCentral
10.
go back to reference Seto H, Aoki K, Kasugai S, Ohya K. Trabecular bone turnover, bone marrow cell development, and gene expression of bone matrix proteins after low calcium feeding in rats. Bone. 1999;25(6):687–95.CrossRefPubMed Seto H, Aoki K, Kasugai S, Ohya K. Trabecular bone turnover, bone marrow cell development, and gene expression of bone matrix proteins after low calcium feeding in rats. Bone. 1999;25(6):687–95.CrossRefPubMed
11.
go back to reference Abuohashish HM, Al-Rejaie SS, Al-Hosaini KA, Parmar MY, Ahmed MM. Alleviating effects of morin against experimentally-induced diabetic osteopenia. Diabetology & metabolic syndrome. 2013;5(1):5.CrossRef Abuohashish HM, Al-Rejaie SS, Al-Hosaini KA, Parmar MY, Ahmed MM. Alleviating effects of morin against experimentally-induced diabetic osteopenia. Diabetology & metabolic syndrome. 2013;5(1):5.CrossRef
12.
go back to reference Li B, Wang Y, Liu Y, Ma J, Li Y. Altered gene expression involved in insulin signaling pathway in type II diabetic osteoporosis rats model. Endocrine. 2013;43(1):136–46.CrossRefPubMed Li B, Wang Y, Liu Y, Ma J, Li Y. Altered gene expression involved in insulin signaling pathway in type II diabetic osteoporosis rats model. Endocrine. 2013;43(1):136–46.CrossRefPubMed
13.
go back to reference Kelly P: Is osteoporosis a genetically determined disease? Br J Obstet Gynaecol 1996, 103:20–26; discussion 26-27. Kelly P: Is osteoporosis a genetically determined disease? Br J Obstet Gynaecol 1996, 103:20–26; discussion 26-27.
14.
go back to reference Pacifici R. Editorial: cytokines, estrogen, and postmenopausal osteoporosis—the second decade. Endocrinology. 1998;139(6):2659–61.CrossRefPubMed Pacifici R. Editorial: cytokines, estrogen, and postmenopausal osteoporosis—the second decade. Endocrinology. 1998;139(6):2659–61.CrossRefPubMed
15.
go back to reference Kearns AE, Khosla S, Kostenuik PJ. Receptor activator of nuclear factor κB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr Rev. 2008;29(2):155–92.CrossRefPubMed Kearns AE, Khosla S, Kostenuik PJ. Receptor activator of nuclear factor κB ligand and osteoprotegerin regulation of bone remodeling in health and disease. Endocr Rev. 2008;29(2):155–92.CrossRefPubMed
16.
go back to reference Flynn A. The role of dietary calcium in bone health. Proceedings of the Nutrition Society. 2003;62(04):851–8.CrossRefPubMed Flynn A. The role of dietary calcium in bone health. Proceedings of the Nutrition Society. 2003;62(04):851–8.CrossRefPubMed
17.
go back to reference Kang S-C, Kim HJ, Kim M-H. Effects of Astragalus Membranaceus with supplemental calcium on bone mineral density and bone metabolism in calcium-deficient ovariectomized rats. Biol Trace Elem Res. 2013;151(1):68–74.CrossRefPubMed Kang S-C, Kim HJ, Kim M-H. Effects of Astragalus Membranaceus with supplemental calcium on bone mineral density and bone metabolism in calcium-deficient ovariectomized rats. Biol Trace Elem Res. 2013;151(1):68–74.CrossRefPubMed
18.
go back to reference Marsden J. The menopause, hormone replacement therapy and breast cancer. J Steroid Biochem Mol Biol. 2002;83(1):123–32.CrossRefPubMed Marsden J. The menopause, hormone replacement therapy and breast cancer. J Steroid Biochem Mol Biol. 2002;83(1):123–32.CrossRefPubMed
19.
go back to reference Reid IR. Pharmacotherapy of osteoporosis in postmenopausal women: focus on safety. Expert Opin Drug Saf. 2002;1(1):93–107.CrossRefPubMed Reid IR. Pharmacotherapy of osteoporosis in postmenopausal women: focus on safety. Expert Opin Drug Saf. 2002;1(1):93–107.CrossRefPubMed
20.
go back to reference Yeh I-T. Postmenopausal hormone replacement therapy: endometrial and breast effects. Adv Anat Pathol. 2007;14(1):17–24.CrossRefPubMed Yeh I-T. Postmenopausal hormone replacement therapy: endometrial and breast effects. Adv Anat Pathol. 2007;14(1):17–24.CrossRefPubMed
21.
go back to reference Miksicek RJ. Interaction of naturally occurring nonsteroidal estrogens with expressed recombinant human estrogen receptor. J Steroid Biochem Mol Biol. 1994;49(2):153–60.CrossRefPubMed Miksicek RJ. Interaction of naturally occurring nonsteroidal estrogens with expressed recombinant human estrogen receptor. J Steroid Biochem Mol Biol. 1994;49(2):153–60.CrossRefPubMed
22.
go back to reference Breitman PL, Fonseca D, Cheung AM, Ward WE. Isoflavones with supplemental calcium provide greater protection against the loss of bone mass and strength after ovariectomy compared to isoflavones alone. Bone. 2003;33(4):597–605.CrossRefPubMedPubMedCentral Breitman PL, Fonseca D, Cheung AM, Ward WE. Isoflavones with supplemental calcium provide greater protection against the loss of bone mass and strength after ovariectomy compared to isoflavones alone. Bone. 2003;33(4):597–605.CrossRefPubMedPubMedCentral
23.
go back to reference Huangb MW, Zhuc Y-C, Linzd W, Duanb W, Zhua Y-Z. Effects of salvia miltiorrhiza after acute myocardial infarction in rats. Novel Compounds from Natural Products in the New Millennium: Potential and Challenges. 2004;183 Huangb MW, Zhuc Y-C, Linzd W, Duanb W, Zhua Y-Z. Effects of salvia miltiorrhiza after acute myocardial infarction in rats. Novel Compounds from Natural Products in the New Millennium: Potential and Challenges. 2004;183
24.
go back to reference Kim SY, Moon TC, Chang HW, Son KH, Kang SS, Kim HP. Effects of tanshinone I isolated from salvia miltiorrhiza bunge on arachidonic acid metabolism and in vivo inflammatory responses. Phytother Res. 2002;16(7):616–20.CrossRefPubMed Kim SY, Moon TC, Chang HW, Son KH, Kang SS, Kim HP. Effects of tanshinone I isolated from salvia miltiorrhiza bunge on arachidonic acid metabolism and in vivo inflammatory responses. Phytother Res. 2002;16(7):616–20.CrossRefPubMed
25.
go back to reference Y-J W, Hong C-Y, Lin S-J, Wu P, Shiao M-S. Increase of vitamin E content in LDL and reduction of atherosclerosis in cholesterol-fed rabbits by a water-soluble antioxidant-rich fraction of salvia miltiorrhiza. Arterioscler Thromb Vasc Biol. 1998;18(3):481–6.CrossRef Y-J W, Hong C-Y, Lin S-J, Wu P, Shiao M-S. Increase of vitamin E content in LDL and reduction of atherosclerosis in cholesterol-fed rabbits by a water-soluble antioxidant-rich fraction of salvia miltiorrhiza. Arterioscler Thromb Vasc Biol. 1998;18(3):481–6.CrossRef
26.
go back to reference Guo Y, Li Y, Xue L, Severino RP, Gao S, Niu J, Qin L-P, Zhang D, Brömme D. Salvia miltiorrhiza: an ancient Chinese herbal medicine as a source for anti-osteoporotic drugs. J Ethnopharmacol. 2014;155(3):1401–16.CrossRefPubMed Guo Y, Li Y, Xue L, Severino RP, Gao S, Niu J, Qin L-P, Zhang D, Brömme D. Salvia miltiorrhiza: an ancient Chinese herbal medicine as a source for anti-osteoporotic drugs. J Ethnopharmacol. 2014;155(3):1401–16.CrossRefPubMed
27.
go back to reference Liu H, Wang X, Wang D, Zou Z, Liang Z. Effect of drought stress on growth and accumulation of active constituents in salvia miltiorrhiza Bunge. Ind Crop Prod. 2011;33(1):84–8.CrossRef Liu H, Wang X, Wang D, Zou Z, Liang Z. Effect of drought stress on growth and accumulation of active constituents in salvia miltiorrhiza Bunge. Ind Crop Prod. 2011;33(1):84–8.CrossRef
28.
go back to reference Kim H-H, Kim JH, Kwak HB, Huang H, Han S-H, Ha H, Lee SW, Woo E-R, Lee ZH. Inhibition of osteoclast differentiation and bone resorption by tanshinone IIA isolated from salvia miltiorrhiza Bunge. Biochem Pharmacol. 2004;67(9):1647–56.CrossRefPubMed Kim H-H, Kim JH, Kwak HB, Huang H, Han S-H, Ha H, Lee SW, Woo E-R, Lee ZH. Inhibition of osteoclast differentiation and bone resorption by tanshinone IIA isolated from salvia miltiorrhiza Bunge. Biochem Pharmacol. 2004;67(9):1647–56.CrossRefPubMed
29.
go back to reference Cao E-H, Liu X-Q, Wang J-J, N-F X. Effect of natural antioxidant tanshinone II-A on DNA damage by lipid peroxidation in liver cells. Free Radic Biol Med. 1996;20(6):801–6.CrossRefPubMed Cao E-H, Liu X-Q, Wang J-J, N-F X. Effect of natural antioxidant tanshinone II-A on DNA damage by lipid peroxidation in liver cells. Free Radic Biol Med. 1996;20(6):801–6.CrossRefPubMed
30.
go back to reference Chen Y-H, G-H D, Zhang J-T. Salvianolic acid B protects brain against injuries caused by ischemia-reperfusion in rats. Acta Pharmacol Sin. 2000;21(5):463–6.PubMed Chen Y-H, G-H D, Zhang J-T. Salvianolic acid B protects brain against injuries caused by ischemia-reperfusion in rats. Acta Pharmacol Sin. 2000;21(5):463–6.PubMed
31.
go back to reference G-H D, Qiu Y, Zhang J-T. Salvianolic acid B protects the memory functions against transient cerebral ischemia in mice. J Asian Nat Prod Res. 2000;2(2):145–52.CrossRef G-H D, Qiu Y, Zhang J-T. Salvianolic acid B protects the memory functions against transient cerebral ischemia in mice. J Asian Nat Prod Res. 2000;2(2):145–52.CrossRef
32.
go back to reference Jang S-Y, Jeong Y-J, Kwon T-K, Seo J-H. Effects of water-soluble calcium supplements made from eggshells and oyster shells on the calcium metabolism of growing rats. Journal of Food Science and Nutrition. 2010;15(1):78–82. Jang S-Y, Jeong Y-J, Kwon T-K, Seo J-H. Effects of water-soluble calcium supplements made from eggshells and oyster shells on the calcium metabolism of growing rats. Journal of Food Science and Nutrition. 2010;15(1):78–82.
33.
go back to reference Heaney RP, Dowell MS, Bierman J, Hale CA, Bendich A. Absorbability and cost effectiveness in calcium supplementation. J Am Coll Nutr. 2001;20(3):239–46.CrossRefPubMed Heaney RP, Dowell MS, Bierman J, Hale CA, Bendich A. Absorbability and cost effectiveness in calcium supplementation. J Am Coll Nutr. 2001;20(3):239–46.CrossRefPubMed
34.
go back to reference Hanzlik RP, Fowler SC, Fisher DH. Relative bioavailability of calcium from calcium formate, calcium citrate, and calcium carbonate. J Pharmacol Exp Ther. 2005;313(3):1217–22.CrossRefPubMed Hanzlik RP, Fowler SC, Fisher DH. Relative bioavailability of calcium from calcium formate, calcium citrate, and calcium carbonate. J Pharmacol Exp Ther. 2005;313(3):1217–22.CrossRefPubMed
35.
go back to reference Jang S-Y, Jeong Y-J, Kwon T-K, Seo J-H, Park E-M. The effect of water-soluble calcium supplements on calcium metabolism and bone metabolism of growing rats. Preventive Nutrition and Food Science. 2007;12(4):217–21.CrossRef Jang S-Y, Jeong Y-J, Kwon T-K, Seo J-H, Park E-M. The effect of water-soluble calcium supplements on calcium metabolism and bone metabolism of growing rats. Preventive Nutrition and Food Science. 2007;12(4):217–21.CrossRef
36.
go back to reference Jeong Y, Kim J, Kim G. Effects of liquefied calcium supplement on bone mineral density in middle-aged women. Journal of the Korean Society of Food Science and Nutrition. 2004; Jeong Y, Kim J, Kim G. Effects of liquefied calcium supplement on bone mineral density in middle-aged women. Journal of the Korean Society of Food Science and Nutrition. 2004;
37.
go back to reference Jang S-Y, Baek C-H, Jeong K-H, Park N-Y, Jeong Y-J. Effect of vinegar on the solubility of calcium. Korean Journal of Food Preservation. 2005;12(2):112–6. Jang S-Y, Baek C-H, Jeong K-H, Park N-Y, Jeong Y-J. Effect of vinegar on the solubility of calcium. Korean Journal of Food Preservation. 2005;12(2):112–6.
38.
go back to reference Judex S, Luu Y, Ozcivici E, Adler B, Lublinsky S, Rubin C. Quantification of adiposity in small rodents using micro-CT. Methods. 2010;50(1):14–9.CrossRefPubMed Judex S, Luu Y, Ozcivici E, Adler B, Lublinsky S, Rubin C. Quantification of adiposity in small rodents using micro-CT. Methods. 2010;50(1):14–9.CrossRefPubMed
39.
go back to reference Yeh O, Keaveny T. Biomechanical effects of intraspecimen variations in trabecular architecture: a three-dimensional finite element study. Bone. 1999;25(2):223–8.CrossRefPubMed Yeh O, Keaveny T. Biomechanical effects of intraspecimen variations in trabecular architecture: a three-dimensional finite element study. Bone. 1999;25(2):223–8.CrossRefPubMed
40.
go back to reference Roudsari JM, Mahjoub S. Quantification and comparison of bone-specific alkaline phosphatase with two methods in normal and paget’s specimens. Caspian journal of internal medicine. 2012;3(3):478. Roudsari JM, Mahjoub S. Quantification and comparison of bone-specific alkaline phosphatase with two methods in normal and paget’s specimens. Caspian journal of internal medicine. 2012;3(3):478.
41.
go back to reference Leung P, Pickarski M, Zhuo Y, Masarachia P, Duong L. The effects of the cathepsin K inhibitor odanacatib on osteoclastic bone resorption and vesicular trafficking. Bone. 2011;49(4):623–35.CrossRefPubMed Leung P, Pickarski M, Zhuo Y, Masarachia P, Duong L. The effects of the cathepsin K inhibitor odanacatib on osteoclastic bone resorption and vesicular trafficking. Bone. 2011;49(4):623–35.CrossRefPubMed
42.
go back to reference Dacquin R, Davey RA, Laplace C, Levasseur R, Morris HA, Goldring SR, Gebre-Medhin S, Galson DL, Zajac JD, Karsenty G. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J Cell Biol. 2004;164(4):509–14.CrossRefPubMedPubMedCentral Dacquin R, Davey RA, Laplace C, Levasseur R, Morris HA, Goldring SR, Gebre-Medhin S, Galson DL, Zajac JD, Karsenty G. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J Cell Biol. 2004;164(4):509–14.CrossRefPubMedPubMedCentral
43.
go back to reference Chen X, Guo J, Bao J, Lu J, Wang Y. The anticancer properties of salvia miltiorrhiza Bunge (Danshen): a systematic review. Med Res Rev. 2014;34(4):768–94.CrossRefPubMed Chen X, Guo J, Bao J, Lu J, Wang Y. The anticancer properties of salvia miltiorrhiza Bunge (Danshen): a systematic review. Med Res Rev. 2014;34(4):768–94.CrossRefPubMed
44.
go back to reference Wu W, Zhu Y, Zhang L, Yang R, Zhou Y. Extraction, preliminary structural characterization, and antioxidant activities of polysaccharides from salvia miltiorrhiza Bunge. Carbohydr Polym. 2012;87(2):1348–53.CrossRef Wu W, Zhu Y, Zhang L, Yang R, Zhou Y. Extraction, preliminary structural characterization, and antioxidant activities of polysaccharides from salvia miltiorrhiza Bunge. Carbohydr Polym. 2012;87(2):1348–53.CrossRef
45.
go back to reference Li M, Zhang L, Cai RL, Gao Y, Qi Y. Lipid-soluble extracts from salvia miltiorrhiza inhibit production of LPS-induced inflammatory mediators via NF-κB modulation in RAW 264.7 cells and perform Antiinflammatory effects in vivo. Phytother Res. 2012;26(8):1195–204.CrossRefPubMed Li M, Zhang L, Cai RL, Gao Y, Qi Y. Lipid-soluble extracts from salvia miltiorrhiza inhibit production of LPS-induced inflammatory mediators via NF-κB modulation in RAW 264.7 cells and perform Antiinflammatory effects in vivo. Phytother Res. 2012;26(8):1195–204.CrossRefPubMed
46.
go back to reference Cui Y, Bhandary B, Marahatta A, Lee G-H, Li B, Kim D-S, Chae S-W, Kim H-R, Chae H-J: Characterization of salvia Miltiorrhiza ethanol extract as an anti-osteoporotic agent. BMC Complement Altern Med 2011, 11(1):1. Cui Y, Bhandary B, Marahatta A, Lee G-H, Li B, Kim D-S, Chae S-W, Kim H-R, Chae H-J: Characterization of salvia Miltiorrhiza ethanol extract as an anti-osteoporotic agent. BMC Complement Altern Med 2011, 11(1):1.
47.
go back to reference Fan G, Zhu Y, Guo H, Wang X, Wang H, Gao X. Direct vasorelaxation by a novel phytoestrogen tanshinone IIA is mediated by nongenomic action of estrogen receptor through endothelial nitric oxide synthase activation and calcium mobilization. J Cardiovasc Pharmacol. 2011;57(3):340–7.CrossRefPubMed Fan G, Zhu Y, Guo H, Wang X, Wang H, Gao X. Direct vasorelaxation by a novel phytoestrogen tanshinone IIA is mediated by nongenomic action of estrogen receptor through endothelial nitric oxide synthase activation and calcium mobilization. J Cardiovasc Pharmacol. 2011;57(3):340–7.CrossRefPubMed
48.
go back to reference Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson J-A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology. 1997;138(3):863–70.CrossRefPubMed Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson J-A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology. 1997;138(3):863–70.CrossRefPubMed
49.
go back to reference Onoe Y, Miyaura C, Ohta H, Nozawa S, Suda T. Expression of estrogen receptor β in rat bone. Endocrinology. 1997;138(10):4509–12.CrossRefPubMed Onoe Y, Miyaura C, Ohta H, Nozawa S, Suda T. Expression of estrogen receptor β in rat bone. Endocrinology. 1997;138(10):4509–12.CrossRefPubMed
50.
go back to reference Couse JF, Lindzey J, Grandien K, AK GJ, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology. 1997;138(11):4613–21.CrossRefPubMed Couse JF, Lindzey J, Grandien K, AK GJ, Korach KS. Tissue distribution and quantitative analysis of estrogen receptor-α (ERα) and estrogen receptor-β (ERβ) messenger ribonucleic acid in the wild-type and ERα-knockout mouse. Endocrinology. 1997;138(11):4613–21.CrossRefPubMed
51.
go back to reference Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson J-Å. Mechanisms of estrogen action. Physiol Rev. 2001;81(4):1535–65.PubMed Nilsson S, Mäkelä S, Treuter E, Tujague M, Thomsen J, Andersson G, Enmark E, Pettersson K, Warner M, Gustafsson J-Å. Mechanisms of estrogen action. Physiol Rev. 2001;81(4):1535–65.PubMed
52.
go back to reference Winuthayanon W, Piyachaturawat P, Suksamrarn A, Burns KA, Arao Y, Hewitt SC, Pedersen LC, Korach KS. The natural estrogenic compound diarylheptanoid (D3): in vitro mechanisms of action and in vivo uterine responses via estrogen receptor [alpha]. Environmental Health Perspectives (Online). 2013;121(4):433. Winuthayanon W, Piyachaturawat P, Suksamrarn A, Burns KA, Arao Y, Hewitt SC, Pedersen LC, Korach KS. The natural estrogenic compound diarylheptanoid (D3): in vitro mechanisms of action and in vivo uterine responses via estrogen receptor [alpha]. Environmental Health Perspectives (Online). 2013;121(4):433.
53.
go back to reference Andreoli T, Bennett J, Carpenter C, Plum F. Compendio de Medicina Interna Cecil. In: EEUU: Me Graw-Hill Interamericana. 1997; Andreoli T, Bennett J, Carpenter C, Plum F. Compendio de Medicina Interna Cecil. In: EEUU: Me Graw-Hill Interamericana. 1997;
54.
go back to reference Erlandsson M, Jonsson C, Lindberg MK, Ohlsson C, Carlsten H. Raloxifene-and estradiol-mediated effects on uterus, bone and B lymphocytes in mice. J Endocrinol. 2002;175(2):319–27.CrossRefPubMed Erlandsson M, Jonsson C, Lindberg MK, Ohlsson C, Carlsten H. Raloxifene-and estradiol-mediated effects on uterus, bone and B lymphocytes in mice. J Endocrinol. 2002;175(2):319–27.CrossRefPubMed
55.
go back to reference Puel C, Mathey J, Agalias A, Kati-coulibaly S, Mardon J, Obled C, Davicco M-J, Lebecque P, Horcajada M-N, Skaltsounis AL. Dose–response study of effect of oleuropein, an olive oil polyphenol, in an ovariectomy/inflammation experimental model of bone loss in the rat. Clin Nutr. 2006;25(5):859–68.CrossRefPubMed Puel C, Mathey J, Agalias A, Kati-coulibaly S, Mardon J, Obled C, Davicco M-J, Lebecque P, Horcajada M-N, Skaltsounis AL. Dose–response study of effect of oleuropein, an olive oil polyphenol, in an ovariectomy/inflammation experimental model of bone loss in the rat. Clin Nutr. 2006;25(5):859–68.CrossRefPubMed
56.
go back to reference Yellayi S, Naaz A, Szewczykowski MA, Sato T, Woods JA, Chang J, Segre M, Allred CD, Helferich WG, Cooke PS. The phytoestrogen genistein induces thymic and immune changes: a human health concern? Proc Natl Acad Sci. 2002;99(11):7616–21.CrossRefPubMedPubMedCentral Yellayi S, Naaz A, Szewczykowski MA, Sato T, Woods JA, Chang J, Segre M, Allred CD, Helferich WG, Cooke PS. The phytoestrogen genistein induces thymic and immune changes: a human health concern? Proc Natl Acad Sci. 2002;99(11):7616–21.CrossRefPubMedPubMedCentral
57.
go back to reference Aubin JE, Bonnelye E. Osteoprotegerin and its ligand: a new paradigm for regulation of osteoclastogenesis and bone resorption. Osteoporos Int. 2000;11(11):905–13.CrossRefPubMed Aubin JE, Bonnelye E. Osteoprotegerin and its ligand: a new paradigm for regulation of osteoclastogenesis and bone resorption. Osteoporos Int. 2000;11(11):905–13.CrossRefPubMed
58.
go back to reference Xie H, Xie P-L, X-P W, Chen S-M, Zhou H-D, Yuan L-Q, Sheng Z-F, Tang S-Y, Luo X-H, Liao E-Y. Omentin-1 attenuates arterial calcification and bone loss in osteoprotegerin-deficient mice by inhibition of RANKL expression. Cardiovasc Res. 2011;92(2):296–306.CrossRefPubMed Xie H, Xie P-L, X-P W, Chen S-M, Zhou H-D, Yuan L-Q, Sheng Z-F, Tang S-Y, Luo X-H, Liao E-Y. Omentin-1 attenuates arterial calcification and bone loss in osteoprotegerin-deficient mice by inhibition of RANKL expression. Cardiovasc Res. 2011;92(2):296–306.CrossRefPubMed
59.
go back to reference Lacey DL, Boyle WJ, Simonet WS, Kostenuik PJ, Dougall WC, Sullivan JK, San Martin J, Dansey R. Bench to bedside: elucidation of the OPG–RANK–RANKL pathway and the development of denosumab. Nat Rev Drug Discov. 2012;11(5):401–19.CrossRefPubMed Lacey DL, Boyle WJ, Simonet WS, Kostenuik PJ, Dougall WC, Sullivan JK, San Martin J, Dansey R. Bench to bedside: elucidation of the OPG–RANK–RANKL pathway and the development of denosumab. Nat Rev Drug Discov. 2012;11(5):401–19.CrossRefPubMed
60.
go back to reference Lacey D, Timms E, Tan H-L, Kelley M, Dunstan C, Burgess T, Elliott R, Colombero A, Elliott G, Scully S. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93(2):165–76.CrossRefPubMed Lacey D, Timms E, Tan H-L, Kelley M, Dunstan C, Burgess T, Elliott R, Colombero A, Elliott G, Scully S. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93(2):165–76.CrossRefPubMed
61.
go back to reference Mizuno A, Kanno T, Hoshi M, Shibata O, Yano K, Fujise N, Kinosaki M, Yamaguchi K, Tsuda E, Murakami A. Transgenic mice overexpressing soluble osteoclast differentiation factor (sODF) exhibit severe osteoporosis. J Bone Miner Metab. 2002;20(6):337–44.CrossRefPubMed Mizuno A, Kanno T, Hoshi M, Shibata O, Yano K, Fujise N, Kinosaki M, Yamaguchi K, Tsuda E, Murakami A. Transgenic mice overexpressing soluble osteoclast differentiation factor (sODF) exhibit severe osteoporosis. J Bone Miner Metab. 2002;20(6):337–44.CrossRefPubMed
62.
go back to reference Ominsky MS, Li X, Asuncion FJ, Barrero M, Warmington KS, Dwyer D, Stolina M, Geng Z, Grisanti M, Tan HL. RANKL inhibition with osteoprotegerin increases bone strength by improving cortical and trabecular bone architecture in ovariectomized rats. J Bone Miner Res. 2008;23(5):672–82.CrossRefPubMed Ominsky MS, Li X, Asuncion FJ, Barrero M, Warmington KS, Dwyer D, Stolina M, Geng Z, Grisanti M, Tan HL. RANKL inhibition with osteoprotegerin increases bone strength by improving cortical and trabecular bone architecture in ovariectomized rats. J Bone Miner Res. 2008;23(5):672–82.CrossRefPubMed
64.
go back to reference Nishizawa Y, Nakamura T, Ohta H, Kushida K, Gorai I, Shiraki M, Fukunaga M, Hosoi T, Miki T, Chaki O. Guidelines for the use of biochemical markers of bone turnover in osteoporosis (2004). J Bone Miner Metab. 2005;23(2):97–104.CrossRefPubMed Nishizawa Y, Nakamura T, Ohta H, Kushida K, Gorai I, Shiraki M, Fukunaga M, Hosoi T, Miki T, Chaki O. Guidelines for the use of biochemical markers of bone turnover in osteoporosis (2004). J Bone Miner Metab. 2005;23(2):97–104.CrossRefPubMed
65.
go back to reference Lomaga MA, Yeh W-C, Sarosi I, Duncan GS, Furlonger C, Ho A, Morony S, Capparelli C, Van G, Kaufman S. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 1999;13(8):1015–24.CrossRefPubMedPubMedCentral Lomaga MA, Yeh W-C, Sarosi I, Duncan GS, Furlonger C, Ho A, Morony S, Capparelli C, Van G, Kaufman S. TRAF6 deficiency results in osteopetrosis and defective interleukin-1, CD40, and LPS signaling. Genes Dev. 1999;13(8):1015–24.CrossRefPubMedPubMedCentral
66.
go back to reference Zhao Q, Shao J, Chen W, Li Y-P. Osteoclast differentiation and gene regulation. Front Biosci. 2007;12(1):2519–29.CrossRefPubMed Zhao Q, Shao J, Chen W, Li Y-P. Osteoclast differentiation and gene regulation. Front Biosci. 2007;12(1):2519–29.CrossRefPubMed
67.
go back to reference Zhao Q, Wang X, Liu Y, He A, Jia R. NFATc1: functions in osteoclasts. Int J Biochem Cell Biol. 2010;42(5):576–9.CrossRefPubMed Zhao Q, Wang X, Liu Y, He A, Jia R. NFATc1: functions in osteoclasts. Int J Biochem Cell Biol. 2010;42(5):576–9.CrossRefPubMed
68.
go back to reference Cagnetta V, Patella V. The role of the immune system in the physiopathology of osteoporosis. Clinical cases in mineral and bone Metabolism. 2012;9(2):85–8.PubMedPubMedCentral Cagnetta V, Patella V. The role of the immune system in the physiopathology of osteoporosis. Clinical cases in mineral and bone Metabolism. 2012;9(2):85–8.PubMedPubMedCentral
69.
go back to reference Roato I, Brunetti G, Gorassini E, Grano M, Colucci S, Bonello L, Buffoni L, Manfredi R, Ruffini E, Ottaviani D. IL-7 up-regulates TNF-α-dependent osteoclastogenesis in patients affected by solid tumor. PLoS One. 2006;1(1):e124.CrossRefPubMedPubMedCentral Roato I, Brunetti G, Gorassini E, Grano M, Colucci S, Bonello L, Buffoni L, Manfredi R, Ruffini E, Ottaviani D. IL-7 up-regulates TNF-α-dependent osteoclastogenesis in patients affected by solid tumor. PLoS One. 2006;1(1):e124.CrossRefPubMedPubMedCentral
70.
go back to reference Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL, Riggs BL. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest. 2003;111(8):1221–30.CrossRefPubMedPubMedCentral Eghbali-Fatourechi G, Khosla S, Sanyal A, Boyle WJ, Lacey DL, Riggs BL. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest. 2003;111(8):1221–30.CrossRefPubMedPubMedCentral
71.
go back to reference Basu S, Michaëlsson K, Olofsson H, Johansson S, Melhus H. Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun. 2001;288(1):275–9.CrossRefPubMed Basu S, Michaëlsson K, Olofsson H, Johansson S, Melhus H. Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun. 2001;288(1):275–9.CrossRefPubMed
Metadata
Title
Effects of Salvia miltiorrhiza extract with supplemental liquefied calcium on osteoporosis in calcium-deficient ovariectomized mice
Authors
Bongkyun Park
Hae Seong Song
Jeong Eun Kwon
Se Min Cho
Seon-A Jang
Mi Yeon Kim
Se Chan Kang
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2017
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-017-2047-y

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