Microgravity Promotes Osteoclast Activity in Medaka Fish Reared at the International Space Station

Overview

Journal Sci Rep

Specialty Science

Date 2015 Sep 22

PMID 26387549

Citations 31

Authors

Masahiro Chatani

Akiko Mantoku

Kazuhiro Takeyama

Dawud Abduweli

Yasutaka Sugamori

Kazuhiro Aoki

Keiichi Ohya

Hiromi Suzuki

Satoko Uchida

Toru Sakimura

Yasushi Kono

Fumiaki Tanigaki

Masaki Shirakawa

Yoshiro Takano

Akira Kudo

Affiliations

Soon will be listed here.

Abstract

The bone mineral density (BMD) of astronauts decreases specifically in the weight-bearing sites during spaceflight. It seems that osteoclasts would be affected by a change in gravity; however, the molecular mechanism involved remains unclear. Here, we show that the mineral density of the pharyngeal bone and teeth region of TRAP-GFP/Osterix-DsRed double transgenic medaka fish was decreased and that osteoclasts were activated when the fish were reared for 56 days at the international space station. In addition, electron microscopy observation revealed a low degree of roundness of mitochondria in osteoclasts. In the whole transcriptome analysis, fkbp5 and ddit4 genes were strongly up-regulated in the flight group. The fish were filmed for abnormal behavior; and, interestingly, the medaka tended to become motionless in the late stage of exposure. These results reveal impaired physiological function with a change in mechanical force under microgravity, which impairment was accompanied by osteoclast activation.

Citing Articles

Vibration Rather than Microgravity Affects Bone Metabolism in Adult Zebrafish Scale Model.

Carnovali M, Zava S, Banfi G, Rizzo A, Mariotti M Cells. 2024; 13(6.

PMID: 38534353 PMC: 10969198. DOI: 10.3390/cells13060509.

Why Animal Experiments Are Still Indispensable in Bone Research: A Statement by the European Calcified Tissue Society.

Stein M, Elefteriou F, Busse B, Fiedler I, Kwon R, Farrell E J Bone Miner Res. 2023; 38(8):1045-1061.

PMID: 37314012 PMC: 10962000. DOI: 10.1002/jbmr.4868.

D-Mannose prevents bone loss under weightlessness.

Gu R, Liu H, Hu M, Zhu Y, Liu X, Wang F J Transl Med. 2023; 21(1):8.

PMID: 36617569 PMC: 9827691. DOI: 10.1186/s12967-022-03870-1.

Substrate stiffness regulates the differentiation profile and functions of osteoclasts via cytoskeletal arrangement.

Wang Q, Xie J, Zhou C, Lai W Cell Prolif. 2021; 55(1):e13172.

PMID: 34953003 PMC: 8780927. DOI: 10.1111/cpr.13172.

Simulated Galactic Cosmic Rays Modify Mitochondrial Metabolism in Osteoclasts, Increase Osteoclastogenesis and Cause Trabecular Bone Loss in Mice.

Kim H, Richardson K, Krager K, Ling W, Simmons P, Allen A Int J Mol Sci. 2021; 22(21).

PMID: 34769141 PMC: 8583929. DOI: 10.3390/ijms222111711.

References

Purdue P, Crotti T, Shen Z, Swantek J, Li J, Hill J . Comprehensive profiling analysis of actively resorbing osteoclasts identifies critical signaling pathways regulated by bone substrate. Sci Rep. 2014; 4:7595. PMC: 4274512. DOI: 10.1038/srep07595. View

Uchida S, Masukawa M, Kamigaichi S . NASDA aquatic animal experiment facilities for Space Shuttle and ISS. Adv Space Res. 2003; 30(4):797-802. DOI: 10.1016/s0273-1177(02)00398-8. View

Sakimura T, Suzuki T, Matsubara S, Uchida S, Kato M, Tanemura R . NASDA aquatic animal experiment facilities for Space Shuttle. Biol Sci Space. 2001; 13(4):314-20. DOI: 10.2187/bss.13.314. View

Porazinski S, Wang H, Asaoka Y, Behrndt M, Miyamoto T, Morita H . YAP is essential for tissue tension to ensure vertebrate 3D body shape. Nature. 2015; 521(7551):217-221. PMC: 4720436. DOI: 10.1038/nature14215. View

Jee W, Wronski T, MOREY E, Kimmel D . Effects of spaceflight on trabecular bone in rats. Am J Physiol. 1983; 244(3):R310-4. DOI: 10.1152/ajpregu.1983.244.3.R310. View

Kimura M, Nagai T, Matsushita R, Hashimoto A, Miyashita T, Hirohata S . Role of FK506 binding protein 5 (FKBP5) in osteoclast differentiation. Mod Rheumatol. 2012; 23(6):1133-9. DOI: 10.1007/s10165-012-0809-4. View

Chatani M, Takano Y, Kudo A . Osteoclasts in bone modeling, as revealed by in vivo imaging, are essential for organogenesis in fish. Dev Biol. 2011; 360(1):96-109. DOI: 10.1016/j.ydbio.2011.09.013. View

Nemoto Y, Higuchi K, Baba O, Kudo A, Takano Y . Multinucleate osteoclasts in medaka as evidence of active bone remodeling. Bone. 2006; 40(2):399-408. DOI: 10.1016/j.bone.2006.08.019. View

Knowles H, Cleton-Jansen A, Korsching E, Athanasou N . Hypoxia-inducible factor regulates osteoclast-mediated bone resorption: role of angiopoietin-like 4. FASEB J. 2010; 24(12):4648-59. PMC: 2992372. DOI: 10.1096/fj.10-162230. View

10.

Ishii M, Saeki Y . Osteoclast cell fusion: mechanisms and molecules. Mod Rheumatol. 2008; 18(3):220-7. DOI: 10.1007/s10165-008-0051-2. View

11.

KRUTSAY M . [METHODS FOR DEMONSTRATION OF SOME CALCIUM COMPOUNDS IN HISTOLOGICAL SECTIONS]. Acta Histochem. 1963; 15:189-91. View

12.

Lang T, LeBlanc A, Evans H, Lu Y, Genant H, Yu A . Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res. 2004; 19(6):1006-12. DOI: 10.1359/JBMR.040307. View

13.

Shyy J, Chien S . Role of integrins in endothelial mechanosensing of shear stress. Circ Res. 2002; 91(9):769-75. DOI: 10.1161/01.res.0000038487.19924.18. View

14.

Tavella S, Ruggiu A, Giuliani A, Brun F, Canciani B, Manescu A . Bone turnover in wild type and pleiotrophin-transgenic mice housed for three months in the International Space Station (ISS). PLoS One. 2012; 7(3):e33179. PMC: 3305296. DOI: 10.1371/journal.pone.0033179. View

15.

Nabavi N, Khandani A, Camirand A, Harrison R . Effects of microgravity on osteoclast bone resorption and osteoblast cytoskeletal organization and adhesion. Bone. 2011; 49(5):965-74. DOI: 10.1016/j.bone.2011.07.036. View

16.

Alles N, Soysa N, Hayashi J, Khan M, Shimoda A, Shimokawa H . Suppression of NF-kappaB increases bone formation and ameliorates osteopenia in ovariectomized mice. Endocrinology. 2010; 151(10):4626-34. DOI: 10.1210/en.2010-0399. View

17.

Feng Q, Zou X, Lu L, Li Y, Liu Y, Zhou J . The stress-response gene redd1 regulates dorsoventral patterning by antagonizing Wnt/β-catenin activity in zebrafish. PLoS One. 2013; 7(12):e52674. PMC: 3530439. DOI: 10.1371/journal.pone.0052674. View

18.

Du J, McEwen B, Manji H . Glucocorticoid receptors modulate mitochondrial function: A novel mechanism for neuroprotection. Commun Integr Biol. 2009; 2(4):350-2. PMC: 2734045. DOI: 10.4161/cib.2.4.8554. View

19.

Lee S, Kim H, Song I, Youm J, Dizon L, Jeong S . Glucocorticoids and their receptors: insights into specific roles in mitochondria. Prog Biophys Mol Biol. 2013; 112(1-2):44-54. DOI: 10.1016/j.pbiomolbio.2013.04.001. View

20.

Renn J, Winkler C . Osterix-mCherry transgenic medaka for in vivo imaging of bone formation. Dev Dyn. 2008; 238(1):241-8. DOI: 10.1002/dvdy.21836. View