دورية أكاديمية

Spatial control of perilacunar canalicular remodeling during lactation.

التفاصيل البيبلوغرافية
العنوان: Spatial control of perilacunar canalicular remodeling during lactation.
المؤلفون: Sieverts M; Department of Mechanical Engineering, University of Utah, Salt Lake City, UT, 84112, USA., Yee C; Department of Orthopedic Surgery, University of California, San Francisco, CA, 94131, USA., Nemani M; Department of Orthopedic Surgery, University of California, San Francisco, CA, 94131, USA., Parkinson DY; Advanced Light Source, Lawrence Berkeley Laboratory, Berkeley, CA, 94720, USA., Alliston T; Department of Orthopedic Surgery, University of California, San Francisco, CA, 94131, USA., Acevedo C; Department of Mechanical Engineering, University of Utah, Salt Lake City, UT, 84112, USA. claire.acevedo@gmail.com.; Department of Biomedical Engineering, University of Utah, Salt Lake City, UT, 84112, USA. claire.acevedo@gmail.com.; Department of Mechanical and Aerospace Engineering, University of California San Diego, San Diego, CA, 92161, USA. claire.acevedo@gmail.com.
المصدر: Scientific reports [Sci Rep] 2024 Jun 25; Vol. 14 (1), pp. 14655. Date of Electronic Publication: 2024 Jun 25.
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Nature Publishing Group Country of Publication: England NLM ID: 101563288 Publication Model: Electronic Cited Medium: Internet ISSN: 2045-2322 (Electronic) Linking ISSN: 20452322 NLM ISO Abbreviation: Sci Rep Subsets: MEDLINE
أسماء مطبوعة: Original Publication: London : Nature Publishing Group, copyright 2011-
مواضيع طبية MeSH: Lactation*/physiology , Osteocytes*/metabolism , Osteocytes*/physiology , Bone Remodeling*/physiology , X-Ray Microtomography*, Animals ; Female ; Mice ; Matrix Metalloproteinase 13/metabolism
مستخلص: Osteocytes locally remodel their surrounding tissue through perilacunar canalicular remodeling (PLR). During lactation, osteocytes remove minerals to satisfy the metabolic demand, resulting in increased lacunar volume, quantifiable with synchrotron X-ray radiation micro-tomography (SRµCT). Although the effects of lactation on PLR are well-studied, it remains unclear whether PLR occurs uniformly throughout the bone and what mechanisms prevent PLR from undermining bone quality. We used SRµCT imaging to conduct an in-depth spatial analysis of the impact of lactation and osteocyte-intrinsic MMP13 deletion on PLR in murine bone. We found larger lacunae undergoing PLR are located near canals in the mid-cortex or endosteum. We show lactation-induced hypomineralization occurs 14 µm away from lacunar edges, past a hypermineralized barrier. Our findings reveal that osteocyte-intrinsic MMP13 is crucial for lactation-induced PLR near lacunae in the mid-cortex but not for whole-bone resorption. This research highlights the spatial control of PLR on mineral distribution during lactation.
(© 2024. The Author(s).)
References: Hyatt, H. W., Zhang, Y., Hood, W. R. & Kavazis, A. N. Lactation has persistent effects on a mother’s metabolism and mitochondrial function. Sci. Rep. 7, 17118 (2017). (PMID: 29215072571942410.1038/s41598-017-17418-7)
Wysolmerski, J. J. Osteocytes remove and replace perilacunar mineral during reproductive cycles. Bone 54, 230–236 (2013). (PMID: 23352996362406910.1016/j.bone.2013.01.025)
Kovacs, C. S. Control of mineral and skeletal homeostasis during pregnancy and lactation. In Genetics of Bone Biology and Skeletal Disease, 349–373 (Elsevier, 2018).
Qing, H. et al. Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J. Bone Miner. Res. 27, 1018–1029 (2012). (PMID: 2230801810.1002/jbmr.1567)
Liu, X. S., Wang, L., de Bakker, C. M. & Lai, X. Mechanical regulation of the maternal skeleton during reproduction and lactation. Curr. Osteoporos. Rep. 17, 375–386 (2019). (PMID: 31755029737349710.1007/s11914-019-00555-5)
Bonewald, L. F. The amazing osteocyte. J. Bone Miner. Res. 26, 229–238 (2011). (PMID: 2125423010.1002/jbmr.320)
Mazur, C. M. et al. Osteocyte dysfunction promotes osteoarthritis through MMP13-dependent suppression of subchondral bone homeostasis. Bone Res. 7, 1–17 (2019). (PMID: 10.1038/s41413-019-0070-y)
Yee, C. S., Schurman, C. A., White, C. R. & Alliston, T. Investigating osteocytic perilacunar/canalicular remodeling. Curr. Osteoporos. Rep. 17, 157–168 (2019). (PMID: 31227998720239710.1007/s11914-019-00514-0)
Winter, E. M. et al. Pregnancy and lactation, a challenge for the skeleton. Endocr. Connect. 9, R143–R157 (2020). (PMID: 32438342735473010.1530/EC-20-0055)
Boyce, B., Yao, Z. & Xing, L. Osteoclasts have multiple roles in bone in addition to bone resorption. Crit. Rev. Eukaryot. Gene Expr. 19, 171–180 (2009). (PMID: 19883363285646510.1615/CritRevEukarGeneExpr.v19.i3.10)
Ryan, B. A. et al. The puzzle of lactational bone physiology: Osteocytes masquerade as osteoclasts and osteoblasts. J. Clin. Investig. 129, 3041–3044 (2019). (PMID: 31232705666881510.1172/JCI130640)
Kaya, S. et al. Lactation-induced changes in the volume of osteocyte lacunar-canalicular space alter mechanical properties in cortical bone tissue. J. Bone Miner. Res. 32, 688–697 (2017). (PMID: 2785958610.1002/jbmr.3044)
Vahidi, G., Rux, C., Sherk, V. & Heveran, C. Lacunar-canalicular bone remodeling: Impacts on bone quality and tools for assessment. Bone 143, 115663 (2021). (PMID: 3298719810.1016/j.bone.2020.115663)
Miller, S. C. & Bowman, B. M. Rapid improvements in cortical bone dynamics and structure after lactation in established breeder rats. Ana. Rec. Part A Discov. Mol. Cell. Evol. Biol. 276, 143–149 (2004). (PMID: 10.1002/ar.a.10138)
Vajda, E. G., Bowman, B. M. & Miller, S. C. Cancellous and cortical bone mechanical properties and tissue dynamics during pregnancy, lactation, and postlactation in the rat. Biol. Reprod. 65, 689–695 (2001). (PMID: 1151432910.1095/biolreprod65.3.689)
Tang, S. Y., Herber, R.-P., Ho, S. P. & Alliston, T. Matrix metalloproteinase-13 is required for osteocytic perilacunar remodeling and maintains bone fracture resistance. J. Bone Miner. Res. 27, 1936–1950 (2012). (PMID: 2254993110.1002/jbmr.1646)
Jähn, K. et al. Osteocytes acidify their microenvironment in response to PTHrP in vitro and in lactating mice in vivo. J. Bone Miner. Res. 32, 1761–1772 (2017). (PMID: 2847075710.1002/jbmr.3167)
Tsourdi, E., Jähn, K., Rauner, M., Busse, B. & Bonewald, L. F. Physiological and pathological osteocytic osteolysis. J. Musculoskelet. Neuronal Interact. 18, 292 (2018). (PMID: 301792066146198)
Buenzli, P. R. & Sims, N. A. Quantifying the osteocyte network in the human skeleton. Bone 75, 144–150 (2015). (PMID: 2570805410.1016/j.bone.2015.02.016)
Obata, Y. et al. Quantitative and qualitative bone imaging: A review of synchrotron radiation microtomography analysis in bone research. J. Mech. Behav. Biomed. Mater. 110, 103887 (2020). (PMID: 3295719410.1016/j.jmbbm.2020.103887)
Dong, P. et al. 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-ct images. Bone 60, 172–185 (2014). (PMID: 2433418910.1016/j.bone.2013.12.008)
Paganin, D., Mayo, S. C., Gureyev, T. E., Miller, P. R. & Wilkins, S. W. Simultaneous phase and amplitude extraction from a single defocused image of a homogeneous object. J. Microsc. 206, 33–40 (2002). (PMID: 1200056110.1046/j.1365-2818.2002.01010.x)
Faragó, T. et al. syris: A flexible and efficient framework for X-ray imaging experiments simulation. J. Synchrotron Radiat. 24, 1283–1295 (2017). (PMID: 2909107210.1107/S1600577517012255)
Gürsoy, D., De Carlo, F., Xiao, X. & Jacobsen, C. TomoPy: A framework for the analysis of synchrotron tomographic data. J. Synchrotron Radiat. 21, 1188–1193 (2014). (PMID: 25178011418164310.1107/S1600577514013939)
Núñez, J. et al. Regional diversity in the murine cortical vascular network is revealed by synchrotron X-ray tomography and is amplified with age. Eur. Cells Mater. 35, 281–299 (2018). (PMID: 10.22203/eCM.v035a20)
Trend, J. et al. Regional assessment of male murine bone exposes spatial heterogeneity in osteocyte lacunar volume associated with intracortical canals and regulation by VEGF. bioRxiv 2023–02 (2023).
Nango, N. et al. Osteocyte-directed bone demineralization along canaliculi. Bone 84, 279–288 (2016). (PMID: 2670923610.1016/j.bone.2015.12.006)
Hesse, B. et al. Canalicular network morphology is the major determinant of the spatial distribution of mass density in human bone tissue: Evidence by means of synchrotron radiation phase-contrast nano-CT. J. Bone Miner. Res. 30, 346–356 (2015). (PMID: 2513072010.1002/jbmr.2324)
Kerschnitzki, M. et al. Architecture of the osteocyte network correlates with bone material quality. J. Bone Miner. Res. 28, 1837–1845 (2013). (PMID: 2349489610.1002/jbmr.1927)
Zhang, S. et al. Nanostructure and mechanical properties of the osteocyte lacunar-canalicular network-associated bone matrix revealed by quantitative nanomechanical mapping. Nano Res. 8, 3250–3260 (2015). (PMID: 10.1007/s12274-015-0825-8)
Stickens, D. et al. Altered endochondral bone development in matrix metalloproteinase 13-deficient mice. Development 131, 5883–5895 (2004). (PMID: 1553948510.1242/dev.01461)
Lu, Y. et al. DMP1-targeted Cre expression in odontoblasts and osteocytes. J. Dent. Res. 86, 320–325 (2007). (PMID: 1738402510.1177/154405910708600404)
Snorrason, F. & Kärrholm, J. Early loosening of revision hip arthroplasty: A Roentgen stereophotogrammetric analysis. J. Arthroplasty 5, 217–229 (1990). (PMID: 223081810.1016/S0883-5403(08)80076-9)
Mamillapalli, R. et al. Mammary-specific ablation of the calcium-sensing receptor during lactation alters maternal calcium metabolism, milk calcium transport, and neonatal calcium accrual. Endocrinology 154, 3031–3042 (2013). (PMID: 23782944374948510.1210/en.2012-2195)
Cole, J. H. & van der Meulen, M. C. Whole bone mechanics and bone quality. Clin. Orthop. Relat. Res. 469, 2139–2149 (2011). (PMID: 21274760312694710.1007/s11999-011-1784-3)
Kovacs, C. S. Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol. Rev. 96, 449–547 (2016). (PMID: 2688767610.1152/physrev.00027.2015)
VanHouten, J. N. & Wysolmerski, J. J. Low estrogen and high parathyroid hormone-related peptide levels contribute to accelerated bone resorption and bone loss in lactating mice. Endocrinology 144, 5521–5529 (2003). (PMID: 1450056810.1210/en.2003-0892)
Kilkenny, C., Browne, W., Cuthill, I., Emerson, M. & Altman, D. Improving bioscience research reporting: The ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412 (2010). (PMID: 20613859289395110.1371/journal.pbio.1000412)
Dole, N. S. et al. Osteocyte-intrinsic TGF-β signaling regulates bone quality through perilacunar/canalicular remodeling. Cell Rep. 21, 2585–2596 (2017). (PMID: 29186693601461510.1016/j.celrep.2017.10.115)
Fowler, T. W. et al. Glucocorticoid suppression of osteocyte perilacunar remodeling is associated with subchondral bone degeneration in osteonecrosis. Sci. Rep. 7, 1–13 (2017). (PMID: 10.1038/srep44618)
Dole, N. S., Yee, C. S., Mazur, C. M., Acevedo, C. & Alliston, T. TGFβ regulation of perilacunar/canalicular remodeling is sexually dimorphic. J. Bone Miner. Res. 35, 1549–1561 (2020). (PMID: 3228296110.1002/jbmr.4023)
Forien, J.-B. & Mohan, K. A. PhaseCT. https://github.com/jbforien/phaseCT (2021).
Henke, B. L., Gullikson, E. M. & Davis, J. C. X-ray interactions: Photoabsorption, scattering, transmission, and reflection at e = 50–30,000 ev, z = 1–92. At. Data Nucl. Data Tables 54, 181–342 (1993). (PMID: 10.1006/adnd.1993.1013)
Bouxsein, M. L. et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 25, 1468–1486 (2010). (PMID: 2053330910.1002/jbmr.141)
Aarts, E., Verhage, M., Veenvliet, J. V., Dolan, C. V. & Van Der Sluis, S. A solution to dependency: Using multilevel analysis to accommodate nested data. Nat. Neurosci. 17, 491–496 (2014). (PMID: 2467106510.1038/nn.3648)
Wright, S. P. Adjusted p-values for simultaneous inference. Biometrics 48, 1005–1013 (1992).
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B (Methodol.) 57, 289–300 (1995). (PMID: 10.1111/j.2517-6161.1995.tb02031.x)
معلومات مُعتمدة: 5T42OH008414-16 United States OH NIOSH CDC HHS; R01DE019284 United States NH NIH HHS; AR066262 United States NH NIH HHS; DE-AC02-05CH11231 U.S. Department of Energy
المشرفين على المادة: EC 3.4.24.- (Matrix Metalloproteinase 13)
تواريخ الأحداث: Date Created: 20240625 Date Completed: 20240625 Latest Revision: 20240625
رمز التحديث: 20240626
DOI: 10.1038/s41598-024-63645-0
PMID: 38918485
قاعدة البيانات: MEDLINE
الوصف
تدمد:2045-2322
DOI:10.1038/s41598-024-63645-0