Estrogen receptor α- (ERα), but not ERβ-signaling, is crucially involved in mechanostimulation of bone fracture healing by whole-body vibration

Bone - Tập 110 - Trang 11-20 - 2018
Melanie Haffner-Luntzer1, Anna Kovtun1, Ina Lackner1, Yvonne Mödinger1, Steffen Hacker1, Astrid Liedert1, Jan Tuckermann2, Anita Ignatius1
1Institute of Orthopedic Research and Biomechanics, University Medical Center Ulm, Helmholtzstraße 14, 89081 Ulm, Germany
2Institute of Comparative Molecular Endocrinology, Ulm University, Helmholtzstraße 8, 89081 Ulm, Germany

Tài liệu tham khảo

Claes, 1995, Effect of dynamization on gap healing of diaphyseal fractures under external fixation, Clin. Biomech. (Bristol, Avon), 10, 227, 10.1016/0268-0033(95)99799-8 Haffner-Luntzer, 2015, Mechanobiology and bone metabolism: clinical relevance for fracture treatment, Unfallchirurg, 118, 1000, 10.1007/s00113-015-0102-z Claes, 2017, Mechanobiology of fracture healing part 1: principles, Unfallchirurg, 120, 14, 10.1007/s00113-016-0280-3 Xie, 2006, Low-level mechanical vibrations can influence bone resorption and bone formation in the growing skeleton, Bone, 39, 1059, 10.1016/j.bone.2006.05.012 Tezval, 2011, Improvement of femoral bone quality after low-magnitude, high-frequency mechanical stimulation in the ovariectomized rat as an osteopenia model, Calcif. Tissue Int., 88, 33, 10.1007/s00223-010-9423-7 Wenger, 2010, Effect of whole-body vibration on bone properties in aging mice, Bone, 47, 746, 10.1016/j.bone.2010.07.014 Dubosc-Marchenay, 1992, Role of blast cell immunophenotyping for the diagnosis and prognosis of acute myeloid leukemia, Hematol. Oncol., 10, 235, 10.1002/hon.2900100502 Rubin, 2004, Prevention of postmenopausal bone loss by a low-magnitude, high-frequency mechanical stimuli: a clinical trial assessing compliance, efficacy, and safety, J. Bone Miner. Res., 19, 343, 10.1359/JBMR.0301251 Ward, 2004, Low magnitude mechanical loading is osteogenic in children with disabling conditions, J. Bone Miner. Res., 19, 360, 10.1359/JBMR.040129 Lynch, 2011, Low-magnitude whole-body vibration does not enhance the anabolic skeletal effects of intermittent PTH in adult mice, J. Orthop. Res., 29, 465, 10.1002/jor.21280 Brouwers, 2010, Effects of vibration treatment on tibial bone of ovariectomized rats analyzed by in vivo micro-CT, J. Orthop. Res., 28, 62 Leung, 2014, Effects of 18-month low-magnitude high-frequency vibration on fall rate and fracture risks in 710 community elderly—a cluster-randomized controlled trial, Osteoporos. Int., 25, 1785, 10.1007/s00198-014-2693-6 Stuermer, 2010, Musculoskeletal response to whole-body vibration during fracture healing in intact and ovariectomized rats, Calcif. Tissue Int., 87, 168, 10.1007/s00223-010-9381-0 Komrakova, 2013, Identification of a vibration regime favorable for bone healing and muscle in estrogen-deficient rats, Calcif. Tissue Int., 92, 509, 10.1007/s00223-013-9706-x Chung, 2014, Low-magnitude high-frequency vibration enhances gene expression related to callus formation, mineralization and remodeling during osteoporotic fracture healing in rats, J. Orthop. Res., 32, 1572, 10.1002/jor.22715 Wehrle, 2015, The impact of low-magnitude high-frequency vibration on fracture healing is profoundly influenced by the oestrogen status in mice, Dis. Model. Mech., 8, 93, 10.1242/dmm.018622 Wang, 2017, The effect of whole body vibration on fracture healing - a systematic review, Eur. Cell. Mater., 34, 108, 10.22203/eCM.v034a08 Wehrle, 2014, Distinct frequency dependent effects of whole-body vibration on non-fractured bone and fracture healing in mice, J. Orthop. Res., 32, 1006, 10.1002/jor.22629 Shi, 2010, Low-magnitude high-frequency vibration treatment augments fracture healing in ovariectomy-induced osteoporotic bone, Bone, 46, 1299, 10.1016/j.bone.2009.11.028 Saxon, 2005, Estrogen receptor beta: the antimechanostat?, Bone, 36, 185, 10.1016/j.bone.2004.08.003 Saxon, 2007, The skeletal responsiveness to mechanical loading is enhanced in mice with a null mutation in estrogen receptor-beta, Am. J. Physiol. Endocrinol. Metab., 293, E484, 10.1152/ajpendo.00189.2007 Chow, 2016, Mechanical stimulation enhanced estrogen receptor expression and callus formation in diaphyseal long bone fracture healing in ovariectomy-induced osteoporotic rats, Osteoporos. Int., 27, 2989, 10.1007/s00198-016-3619-2 Borjesson, 2013, The role of estrogen receptor alpha in the regulation of bone and growth plate cartilage, Cell. Mol. Life Sci., 70, 4023, 10.1007/s00018-013-1317-1 Seitz, 2012, Pharmacological estrogen administration causes a FSH-independent osteo-anabolic effect requiring ER alpha in osteoblasts, PLoS One, 7, 10.1371/journal.pone.0050301 Illing, 2012, Estradiol increases hematopoietic stem and progenitor cells independent of its actions on bone, Haematologica, 97, 1131, 10.3324/haematol.2011.052456 Jessop, 2004, Osteoblast-like cells from estrogen receptor alpha knockout mice have deficient responses to mechanical strain, J. Bone Miner. Res., 19, 938, 10.1359/jbmr.2004.19.6.938 Windahl, 2013, Estrogen receptor-alpha is required for the osteogenic response to mechanical loading in a ligand-independent manner involving its activation function 1 but not 2, J. Bone Miner. Res., 28, 291, 10.1002/jbmr.1754 Lee, 2003, Endocrinology: bone adaptation requires oestrogen receptor-alpha, Nature, 424, 389, 10.1038/424389a Lindberg, 2003, Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a “ying yang” relationship between ERalpha and ERbeta in mice, Mol. Endocrinol., 17, 203, 10.1210/me.2002-0206 Khalid, 2016, Estrogen receptors alpha and beta in bone, Bone, 87, 130, 10.1016/j.bone.2016.03.016 Kushner, 2000, Estrogen receptor pathways to AP-1, J. Steroid Biochem. Mol. Biol., 74, 311, 10.1016/S0960-0760(00)00108-4 Cherlet, 2007, Estrogen receptors inhibit Smad3 transcriptional activity through Ap-1 transcription factors, Mol. Cell. Biochem., 306, 33, 10.1007/s11010-007-9551-1 Stellato, 2016, The “busy life” of unliganded estrogen receptors, Proteomics, 16, 288, 10.1002/pmic.201500261 Billon-Gales, 2011, Activation function 2 (AF2) of estrogen receptor-alpha is required for the atheroprotective action of estradiol but not to accelerate endothelial healing, Proc. Natl. Acad. Sci. U. S. A., 108, 13311, 10.1073/pnas.1105632108 Haffner-Luntzer, 2017, The inflammatory phase of fracture healing is influenced by oestrogen status in mice, Eur. J. Med. Res., 22, 23, 10.1186/s40001-017-0264-y Morgan, 2009, Micro-computed tomography assessment of fracture healing: relationships among callus structure, composition, and mechanical function, Bone, 44, 335, 10.1016/j.bone.2008.10.039 Haffner-Luntzer, 2014, Midkine-deficiency delays chondrogenesis during the early phase of fracture healing in mice, PLoS One, 9, 10.1371/journal.pone.0116282 Andersson, 2017, Insufficient antibody validation challenges oestrogen receptor beta research, Nat. Commun., 8, 15840, 10.1038/ncomms15840 Mamounis, 2014, Estrogen response element-independent signaling partially restores post-ovariectomy body weight gain but is not sufficient for 17beta-estradiol's control of energy homeostasis, Steroids, 81, 88, 10.1016/j.steroids.2013.10.018 He, 2012, Deletion of estrogen receptor beta accelerates early stage of bone healing in a mouse osteotomy model, Osteoporos. Int., 23, 377, 10.1007/s00198-011-1812-x Ke, 2002, The role of estrogen receptor-beta, in the early age-related bone gain and later age-related bone loss in female mice, J. Musculoskelet. Neuronal Interact., 2, 479 Lindberg, 2001, Estrogen receptor specificity in the regulation of the skeleton in female mice, J. Endocrinol., 171, 229, 10.1677/joe.0.1710229 Beil, 2010, Effects of estrogen on fracture healing in mice, J. Trauma, 69, 1259, 10.1097/TA.0b013e3181c4544d Yang, 2013, Estradiol inhibits osteoblast apoptosis via promotion of autophagy through the ER-ERK-mTOR pathway, Apoptosis, 18, 1363, 10.1007/s10495-013-0867-x Shang, 2014, Differentially expressed genes and signalling pathways are involved in mouse osteoblast-like MC3T3-E1 cells exposed to 17-beta estradiol, Int. J. Oral Sci., 6, 142, 10.1038/ijos.2014.2 Sims, 2003, A functional androgen receptor is not sufficient to allow estradiol to protect bone after gonadectomy in estradiol receptor-deficient mice, J. Clin. Invest., 111, 1319, 10.1172/JCI200317246 Cheung, 2012, Stimulated angiogenesis for fracture healing augmented by low-magnitude, high-frequency vibration in a rat model-evaluation of pulsed-wave Doppler, 3-D power Doppler ultrasonography and micro-CT microangiography, Ultrasound Med. Biol., 38, 2120, 10.1016/j.ultrasmedbio.2012.07.025 Haisenleder, 2011, Estimation of estradiol in mouse serum samples: evaluation of commercial estradiol immunoassays, Endocrinology, 152, 4443, 10.1210/en.2011-1501 Arnal, 2013, Lessons from the dissection of the activation functions (AF-1 and AF-2) of the estrogen receptor alpha in vivo, Steroids, 78, 576, 10.1016/j.steroids.2012.11.011 Al-Sherbini, 2014, Estrogen deficiency reduces the expression of estrogen receptor-beta in Wistar rats' periodontal tissues, Saudi Med. J., 35, 242 Zaman, 2006, Osteocytes use estrogen receptor alpha to respond to strain but their ERalpha content is regulated by estrogen, J. Bone Miner. Res., 21, 1297, 10.1359/jbmr.060504 Castillo, 2014, Estrogen receptor-beta regulates mechanical signaling in primary osteoblasts, Am. J. Phys. Endocrinol. Metab., 306 Ren, 2013, 17beta estradiol regulation of connexin 43-based gap junction and mechanosensitivity through classical estrogen receptor pathway in osteocyte-like MLO-Y4 cells, Bone, 53, 587, 10.1016/j.bone.2012.12.004 Zhang, 2012, Estrogen and its receptor enhance mechanobiological effects in compressed bone mesenchymal stem cells, Cells Tissues Organs, 195, 400, 10.1159/000328003 Lima, 2004, Interactions between estrogen and mechanical strain effects on U2OS human osteosarcoma cells are not influenced by estrogen receptor type, Bone, 35, 1127, 10.1016/j.bone.2004.07.005 Damien, 1998, The estrogen receptor's involvement in osteoblasts' adaptive response to mechanical strain, J. Bone Miner. Res., 13, 1275, 10.1359/jbmr.1998.13.8.1275 Liedert, 2010, Estrogen receptor and Wnt signaling interact to regulate early gene expression in response to mechanical strain in osteoblastic cells, Biochem. Biophys. Res. Commun., 394, 755, 10.1016/j.bbrc.2010.03.065 Zhao, 2016, The distinct effects of estrogen and hydrostatic pressure on mesenchymal stem cells differentiation: involvement of estrogen receptor signaling, Ann. Biomed. Eng., 44, 2971, 10.1007/s10439-016-1631-5 Aguirre, 2007, A novel ligand-independent function of the estrogen receptor is essential for osteocyte and osteoblast mechanotransduction, J. Biol. Chem., 282, 25501, 10.1074/jbc.M702231200 Armstrong, 2007, Wnt/beta-catenin signaling is a component of osteoblastic bone cell early responses to load-bearing and requires estrogen receptor alpha, J. Biol. Chem., 282, 20715, 10.1074/jbc.M703224200 Zaman, 2010, Loading-related regulation of gene expression in bone in the contexts of estrogen deficiency, lack of estrogen receptor alpha and disuse, Bone, 46, 628, 10.1016/j.bone.2009.10.021 Centrella, 2012, Estrogen receptor dependent gene expression by osteoblasts - direct, indirect, circumspect, and speculative effects, Steroids, 77, 174, 10.1016/j.steroids.2011.10.016