Comparative study of the effects of osteoprotegerin and testosterone on bone quality in male orchidectomised rats

References

• Boyce BF, Xing L. Biology of RANK, RANKL, and osteoprotegerin. Arthritis Res Ther. 2007;9 Suppl 1:S1.
   PubMed Web of Science ®Google Scholar
• Lacey DL, Timms E, Tan HL. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93:165–176.
   PubMed Web of Science ®Google Scholar
• Yasuda H, Shima N, Nakagawa N. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA. 1998;95:3597–3602.
   PubMed Web of Science ®Google Scholar
• Anderson DM, Maraskovsky E, Billingsley WL, et al. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997;390:175–179.
   PubMed Web of Science ®Google Scholar
• Wong BR, Rho J, Arron J, et al. TRANCE is a novel ligand of the tumor necrosis factor receptor family that activates c-Jun N-terminal kinase in T cells. J Biol Chem. 1997;272:25190–25194.
   PubMed Web of Science ®Google Scholar
• Quinn JM, Elliott J, Gillespie MT, et al. A combination of osteoclast differentiation factor and macrophage-colony stimulating factor is sufficient for both human and mouse osteoclast formation in vitro. Endocrinology. 1998;139:4424–4427.
   PubMed Web of Science ®Google Scholar
• Arboleya L, Castañeda S. Osteoclastos: mucho más que células remodeladoras del hueso. Rev Osteoporos Metab Miner. 2014;6:109–121.
   Google Scholar
• Hofbauer LC, Dunstan CR, Spelsberg TC, et al. Osteoprotegerin production by human osteoblast lineage cells is stimulated by vitamin D, bone morphogenetic protein-2, and cytokines. Biochem Biophys Res Commun. 1998;250:776–781.
   PubMed Web of Science ®Google Scholar
• Hamdy NA. Osteoprotegerin as a potential therapy for osteoporosis. Curr Rheumatol Rep. 2006;8:50–54.
   PubMedGoogle Scholar
• Schwarz ED, Ritchlin CT. Clinical development of anti-RANKL teraphy. Arthritis Res Ther. 2007;9:(Suppl. 1):S7.
   PubMed Web of Science ®Google Scholar
• Greenspan SI, Coates P, Sereika SM, et al. Bone loss after initiation of androgen deprivation theraphy in patients with prostate cancer. J Clin Endocrinol Metab. 2005;90:6410–6417.
   PubMed Web of Science ®Google Scholar
• Shahinian VB, Kuo YF, Freeman JI, et al. Risk of fracture after androgen deprivation for prostate cancer. N Engl J Med. 2005;352:154–164.
   PubMed Web of Science ®Google Scholar
• Snyder PJ, Kopperdahl DL, Stephens-Shields AJ, et al. Effect of testosterone treatment on volumetric bone density and strength in older men with low testosterone: a controlled clinical trial. JAMA Intern Med. 2017;177:471–479.
   PubMed Web of Science ®Google Scholar
• Turner RT, Hannon KS, Demers LM, et al. Differential effects of gonadal function on bone histomorphometry in male and female rats. J Bone Miner Res. 1989;4:557–563.
   PubMed Web of Science ®Google Scholar
• Turner RT, Wakley GK, Hannon KS. Differential effects of androgens on cortical bone histomorphometry in gonadectomized male and female rats. J Orthop Res. 1990;8:612–617.
   PubMed Web of Science ®Google Scholar
• Erben RG, Eberle J, Stahr K, et al. Androgen deficiency induced high turnover osteopenia in aged male rats: a sequential histomorphometric study. J Bone Miner Res. 2000;15:1085–1098.
   PubMed Web of Science ®Google Scholar
• Li X, Ominsky MS, Stolina M, et al. Increased RANK ligand in bone marrow of orchiectomized rats and prevention of their bone loss by the RANK ligand inhibitor osteoprotegerin. Bone. 2009;45:669–676.
   PubMed Web of Science ®Google Scholar
• Borchers RE, Gibson LJ, Burchardt H, et al. Effects of selected thermal variables on the mechanical properties of trabecular bone. Biomaterials. 1995;16:545–551.
   PubMed Web of Science ®Google Scholar
• Gala Paniagua J, Díaz-Curiel M, De la Piedra Gordo C, et al. Bone mass assessment in rats by dual energy X-ray absorptiometry. Br J Radiol. 1998;71:754–758.
   PubMed Web of Science ®Google Scholar
• Feldkamp LA, Davis LC, Kress JW. Practical cone-beam algorithm. J Opt Soc Am A. 1984;1:612–619.
   Google Scholar
• Hildebrand T, Ruegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc. 1997;185:67–75.
   Web of Science ®Google Scholar
• Ulrich D, Van Rietbergen B, Laib A, et al. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone. 1999;25:55–60.
   PubMed Web of Science ®Google Scholar
• Hildebrand T, Rüegsegger P. Quantification of bone microarchitecture with the structure model index. Comput Methods Biomech Biomed Eng. 1997;1:15–23.
   PubMedGoogle Scholar
• Hahn M, Vogel M, Pompesius-Kempa M, et al. Trabecular bone pattern factor – a new parameter for simple quantification of bone microarchitecture. Bone. 1992;13:327–330.
   PubMed Web of Science ®Google Scholar
• Harrigan TP, Mann RW. Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor. J Mater Sci. 1984;19:761–767.
   Web of Science ®Google Scholar
• Vanderschueren D, Vandenput I, Boonen S, et al. An aged rat model of partial androgen deficiency: prevention of both loss of bone and lean body mass by low dose androgen replacement. Endocrinology. 2000;141:1642–1647.
   PubMed Web of Science ®Google Scholar
• Kawano H, Sato T, Yamada T, et al. Suppressive function of androgen receptor in bone resorption. Proc Natl Acad Sci USA. 2003;100:9416–9421.
   PubMed Web of Science ®Google Scholar
• Franklin M, Bu SY, Lerner MR, et al. Dried plum prevents bone loss in a male osteoporosis model via IGF-I and the RANK pathway. Bone. 2006;39:1331–1342.
   PubMed Web of Science ®Google Scholar
• Tyagi V, Scordo M, Yoon RS, et al. Revisiting the role of testosterone: are we missing something? Rev Urol. 2017;19:16–24.
   PubMedGoogle Scholar
• Tuck SP, Francis RM. Testosterone, bone and osteoporosis. Front Horm Res. 2009;37:123–132.
   PubMed Web of Science ®Google Scholar
• Hunter I, Hay CW, Esswein B, et al. Tissue control of androgen action: the ups and downs of androgen receptor expression. Mol Cell Endocrinol. 2018;465:27–35.
   PubMed Web of Science ®Google Scholar
• Taxel P, Kaneko H, Lee SK, et al. Estradiol rapidly inhibits osteoclastogenesis and RANKL expression in bone marrow cultures in postmenopausal women: a pilot study. Osteoporos Int. 2008;19:193–199.
   PubMed Web of Science ®Google Scholar
• Eghbali-Fatourechi G, Khosla S, Sanyal A, et al. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women. J Clin Invest. 2003;111:1221–1230.
   PubMed Web of Science ®Google Scholar
• Wong SK, Mohamad NV, Jayusman PA, et al. The use of selective estrogen receptor modulators on bone health in men. Aging Male. 2018 DOI:10.1080/13685538.2018.1448058.
   Web of Science ®Google Scholar
• World Health Organization. Guidelines for preclinical evaluation and clinical trials in osteoporosis. Geneva: WHO; 1998.
   Google Scholar
• De la Piedra C, Quiroga I, Montero M, et al. Daily or monthly ibandronate prevents or restores deteriorations of bone mass, architecture, biochemical properties and markers of bone turnover in androgen-deficient aged rats. Aging Male. 2011;14:220–230.
   PubMed Web of Science ®Google Scholar
• Ominsky MS, Kostenuik PJ, Cranmer P, et al. The RANKL inhibitor OPG-Fc increases cortical and trabecular bone mass in young gond-intact cynomolgus monkeys. Osteoporos Int. 2007;18:1073–1082.
   PubMed Web of Science ®Google Scholar
• Sipos W, Zysset P, Kostenuik P, et al. OPG-Fc treatment in growing pigs leads to rapid reductions in bone resorption markers, serum calcium, and bone formation markers. Horm Metab Res. 2011;43:944–949.
   PubMed Web of Science ®Google Scholar
• Almeida M, Laurent MR, Dubois V, et al. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol Rev. 2017;97:135–187.
   PubMed Web of Science ®Google Scholar
• Shigehara K, Konaka H, Koh E, et al. Effects of testosterone replacement therapy on hypogonadal men with osteopenia or osteoporosis: a subanalysis of a prospective randomized controlled study in Japan (EARTH study). Aging Male. 2017;20:139–145.
   PubMed Web of Science ®Google Scholar
• Basurto L, Zarate A, Gomez R, et al. Effect of testosterone therapy on lumbar spine and hip mineral density in elderly men. Aging Male. 2008;11:140–145.
   PubMed Web of Science ®Google Scholar
• Bouloux PM, Legros JJ, Elbers JM, et al. Effects of oral testosterone undecanoate therapy on bone mineral density and body composition in 322 aging men with symptomatic testosterone deficiency: a 1-year, randomized, placebo-controlled, dose-ranging study. Aging Male. 2013;16:38–47.
   PubMed Web of Science ®Google Scholar
• Rittmaster R, Hahn RG, Ray P, et al. Effect of dutasteride on intraprostatic androgen levels in men with benign prostatic hyperplasia or prostate cancer. Urology. 2008;72:808–812.
   PubMed Web of Science ®Google Scholar
• Shigehara K, Koh E, Sakamoto J, et al. Effects of dutasteride on lower urinary tract symptoms and general health in men with benign prostatic hypertroplasia and hypogonadism: a prospective study. Aging Male. 2014;17:51–56.
   PubMed Web of Science ®Google Scholar
• Wada N, Hashizume K, Matsumoto S, et al. Dutasteride improves bone mineral density in male patients with lower urinary tract symptoms and prostatic enlargement: a preliminary study. Aging Male. 2016;19:12–14.
   PubMed Web of Science ®Google Scholar
• Rabijewski M, Papierska L, Piątkiewicz P. An association between bone mineral density and anabolic hormones in middle-aged and elderly men with prediabetes. Aging Male. 2017;20:205–213.
   PubMed Web of Science ®Google Scholar
• Yamashita T, Okada S, Higashio K, et al. Double mutations in klotho and osteoprotegerin gene loci rescued osteopetrotic phenotype. Endocrinology. 2002;143:4711–4717.
   PubMed Web of Science ®Google Scholar
• Ominsky MS, Stolina M, Li X, et al. One year of transgenic overexpression of osteoprotegerin in rats suppressed bone resorption and increased vertebral bone volume, density, and strength. J Bone Miner Res. 2009;24:1234–1246.
   PubMed Web of Science ®Google Scholar
• Yarrow JF, Conover CF, Purandare AV, et al. Supraphysiological testosterone enanthate administration prevents bone loss and augments bone strength in gonadectomised male and female rats. Am J Physiol Endocrinol Metab. 2008;295:E1213–E1222.
   PubMed Web of Science ®Google Scholar
• Filipovic B, Sosic JB, Ajdzanovic V, et al. The effects of sex steroids on thyroid C cells and trabecular bone structure in the rat model of male osteoporosis. J Anat. 2013;222:313–320.
   PubMed Web of Science ®Google Scholar
• Xiong Q, Zhang LC, Zhang LH, et al. Effects of recombinant human osteoprotegerin and recombinant RANK protein on the differentiation of osteoclast precursors. Zhongguo Gu Shang. 2013;26:324–327.
   PubMedGoogle Scholar
• Schneider DA, Smith SM, Campbell C, et al. Locally limited inhibition of bone resorption and orthodontic relapse by recombinant osteoprotegerin protein. Orthod Craniofac Res. 2015;18(Suppl 1):187–195.
   PubMedGoogle Scholar
• Fernández González FJ, Cañigral A, López-Caballo JL, et al. Recombinant osteoprotegerin effects during orthodontic movement in a rat model. Eortho. 2016;38:379–385.
   Google Scholar
• Roux S, Orcel P. Bone loss factors that regulate osteoclast differentiation: an update. Arthritis Res. 2000;2:451–456.
   PubMedGoogle Scholar
• Risto O, Hammar E, Hammar K, et al. Elderly men with a history of distal radius fracture have significantly lower calcaneal bone density and free androgen index than age-matched controls. Aging Male. 2012;15:59–62.
   PubMed Web of Science ®Google Scholar
• Francis RM. The effects of testosterone on osteoporosis in men. Clin Endocrinol (Oxf). 1999;50:411–414.
   PubMed Web of Science ®Google Scholar
• Aversa A, Bruzziches R, Francomano D, et al. Effects of long-acting testosterone undecanoate on bone mineral density in middle-aged men with late-onset hypogonadism and metabolic syndrome: results from a 36 months controlled study. Aging Male. 2012;15:96–102.
   PubMed Web of Science ®Google Scholar