Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-08T19:27:56.976Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of autophagy during osteoclastogenesis under microgravity conditions

Published online by Cambridge University Press:  10 July 2018

Ioanna Markolefa  and
George I. Lambrou Open the ORCID record for George I. Lambrou [Opens in a new window]
Ioanna Markolefa
Affiliation:
Graduate Program ‘Metabolic Bones Diseases’, National and Kapodistrian University of Athens, Medical School, Mikras Asias 75, Goudi 11527, Athens, Greece
George I. Lambrou*
Affiliation:
Graduate Program ‘Metabolic Bones Diseases’, National and Kapodistrian University of Athens, Medical School, Mikras Asias 75, Goudi 11527, Athens, Greece First Department of Pediatrics, University of Athens, Choremeio Research Laboratory, National and Kapodistrian University of Athens, Athens, Greece.
*
Author for correspondence: George I. Lambrou, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Space represents a rather hostile environment for the human body, with the bone loss being one of the most important consequences. Autophagy is a complex cellular process contributing to several cellular processes including recycling, nutrition, apoptosis and response to stressful environments. Recent reports have indicated that autophagy is a process that increases under microgravity conditions. In particular, this was shown to be true in skeletal cells such as the osteoclasts. Suppression of autophagy results in downregulation of osteoclastogenesis, making autophagy a quite tempting therapeutic target for preventing bone loss during space flights. The present work attempts to review the literature on the topic of autophagy role in osteoclastogenesis under microgravity conditions.

Keywords

Autophagymicrogravityosteoclastogenesis
Type
Review Article
Information
International Journal of Astrobiology , Volume 18 , Issue 4 , August 2019 , pp. 384 - 390
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arfat, Y, Xiao, WZ, Iftikhar, S, Zhao, F, Li, DJ, Sun, YL, Zhang, G, Shang, P and Qian, AR (2014) Physiological effects of microgravity on bone cells. Calcified Tissue International 94, 569–579.Google Scholar
Bonewald, LF and Johnson, ML (2008) Osteocytes, mechanosensing and Wnt signaling. Bone 42, 606–615.Google Scholar
Boone, BA, Zeh, HJ III, and Bahary, N (2018) Autophagy inhibition in pancreatic adenocarcinoma. Clinical Colorectal Cancer 17, 25–31.Google Scholar
Buravkova, LB, Romanov, YA, Konstantinova, NA, Buravkov, SV, Gershovich, YG and Grivennikov, IA (2008) Cultured stem cells are sensitive to gravity changes. Acta Astronautica 63, 603–608.Google Scholar
Carmeliet, G, Nys, G and Bouillon, R (1997) Microgravity reduces the differentiation of human osteoblastic MG-63 cells. Journal of Bone and Mineral Research 12, 786–794.Google Scholar
Carmona-Gutierrez, D, Hughes, AL, Madeo, F and Ruckenstuhl, C (2016) The crucial impact of lysosomes in aging and longevity. Ageing Research Reviews 32, 2–12.Google Scholar
Chung, YH, Yoon, SY, Choi, B, Sohn, DH, Yoon, KH, Kim, WJ, Kim, DH and Chang, EJ (2012) Microtubule-associated protein light chain 3 regulates Cdc42-dependent actin ring formation in osteoclast. International Journal of Biochemistry & Cell Biology 44, 989–997.Google Scholar
Chung, YH, Jang, Y, Choi, B, Song, DH, Lee, EJ, Kim, SM, Song, Y, Kang, SW, Yoon, SY and Chang, EJ (2014) Beclin-1 is required for RANKL-induced osteoclast differentiation. Journal of Cellular Physiology 229, 1963–1971.Google Scholar
DeSelm, CJ, Miller, BC, Zou, W, Beatty, WL, Van Meel, E, Takahata, Y, Klumperman, J, Tooze, SA, Teitelbaum, SL and Virgin, HW (2011) Autophagy proteins regulate the secretory component of osteoclastic bone resorption. Developmental Cell 21, 966–974.Google Scholar
Des Marais, DJ, Nuth, JA III, Allamandola, LJ, Boss, AP, Farmer, JD, Hoehler, TM, Jakosky, BM, Meadows, VS, Pohorille, A, Runnegar, B and Spormann, AM (2008) The NASA astrobiology roadmap. Astrobiology 8, 715–730.Google Scholar
Di, SM, Qian, AR, Qu, LN, Zhang, W, Wang, Z, Ding, C, Li, YH, Ren, HG and Shang, P (2011) Graviresponses of osteocytes under altered gravity. Advances in Space Research 48, 1161–1166.Google Scholar
Ferranti, F, Caruso, M, Cammarota, M, Masiello, MG, Corano Scheri, K, Fabrizi, C, Fumagalli, L, Schiraldi, C, Cucina, A, Catizone, A and Ricci, G (2014) Cytoskeleton modifications and autophagy induction in TCam-2 seminoma cells exposed to simulated microgravity. Biomed Research International 2014, 904396.Google Scholar
Feve, B (2005) Adipogenesis: cellular and molecular aspects. Best Practice & Research. Clinical Endocrinology & Metabolism 19, 483–499.Google Scholar
Globus, RK and Morey-Holton, E (2016) Hindlimb unloading: rodent analog for microgravity. Journal of Applied Physiology (1985) 120, 1196–1206.Google Scholar
Guo, JY and White, E (2016) Autophagy, metabolism, and cancer. Cold Spring Harbor Symposia on Quantitative Biology 81, 73–78.Google Scholar
Hammond, TG and Hammond, JM (2001) Optimized suspension culture: the rotating-wall vessel. American Journal of Physiology. Renal Physiology 281, F12–F25.Google Scholar
Hargens, AR and Vico, L (2016) Long-duration bed rest as an analog to microgravity. Journal of Applied Physiology (1985) 120, 891–903.Google Scholar
Herranz, R, Anken, R, Boonstra, J, Braun, M, Christianen, PC, De Geest, M, Hauslage, J, Hilbig, R, Hill, RJ, Lebert, M, Medina, FJ, Vagt, N, Ullrich, O, Van Loon, JJ and Hemmersbach, R (2013) Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology 13, 1–17.Google Scholar
Hou, J, Han, ZP, Jing, YY, Yang, X, Zhang, SS, Sun, K, Hao, C, Meng, Y, Yu, FH, Liu, XQ, Shi, YF, Wu, MC, Zhang, L and Wei, LX (2013) Autophagy prevents irradiation injury and maintains stemness through decreasing ROS generation in mesenchymal stem cells. Cell Death & Disease 4, e844.Google Scholar
Hu, Z, Wang, H, Wang, Y, Zhou, H, Shi, F, Zhao, J, Zhang, S and Cao, X (2017) Genomewide analysis and prediction of functional long noncoding RNAs in osteoblast differentiation under simulated microgravity. Molecular Medicine Reports 16, 8180–8188.Google Scholar
Hughes-Fulford, M (2002) Physiological effects of microgravity on osteoblast morphology and cell biology. Advances in Space Biology and Medicine 8, 129–157.Google Scholar
Hughes-Fulford, M (2003) Function of the cytoskeleton in gravisensing during spaceflight. Advances in Space Research 32, 1585–1593.Google Scholar
Indo, HP, Tomiyoshi, T, Suenaga, S, Tomita, K, Suzuki, H, Masuda, D, Terada, M, Ishioka, N, Gusev, O, Cornette, R, Okuda, T, Mukai, C and Majima, HJ (2015) MnSOD downregulation induced by extremely low 0.1 mGy single and fractionated X-rays and microgravity treatment in human neuroblastoma cell line, NB-1. Journal of Clinical Biochemistry and Nutrition 57, 98–104.Google Scholar
Jia, J, Yao, W, Guan, M, Dai, W, Shahnazari, M, Kar, R, Bonewald, L, Jiang, JX and Lane, NE (2011) Glucocorticoid dose determines osteocyte cell fate. FASEB Journal 25, 3366–3376.Google Scholar
Kennedy, OD, Herman, BC, Laudier, DM, Majeska, RJ, Sun, HB and Schaffler, MB (2012) Activation of resorption in fatigue-loaded bone involves both apoptosis and active pro-osteoclastogenic signaling by distinct osteocyte populations. Bone 50, 1115–1122.Google Scholar
Kroemer, G, Marino, G and Levine, B (2010) Autophagy and the integrated stress response. Molecular Cell 40, 280–293.Google Scholar
Lambrou, GI, Papadimitriou, L, Chrousos, GP and Vlahopoulos, SA (2012) Glucocorticoid and proteasome inhibitor impact on the leukemic lymphoblast: multiple, diverse signals converging on a few key downstream regulators. Molecular and Cellular Endocrinology 351, 142–151.Google Scholar
Lee, NK, Choi, YG, Baik, JY, Han, SY, Jeong, DW, Bae, YS, Kim, N and Lee, SY (2005) A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 106, 852–859.Google Scholar
Lin, C, Jiang, X, Dai, Z, Guo, X, Weng, T, Wang, J, Li, Y, Feng, G, Gao, X and He, L (2009) Sclerostin mediates bone response to mechanical unloading through antagonizing Wnt/beta-catenin signaling. Journal of Bone and Mineral Research 24, 1651–1661.Google Scholar
Liu, F, Fang, F, Yuan, H, Yang, D, Chen, Y, Williams, L, Goldstein, SA, Krebsbach, PH and Guan, JL (2013) Suppression of autophagy by FIP200 deletion leads to osteopenia in mice through the inhibition of osteoblast terminal differentiation. Journal of Bone and Mineral Research 28, 2414–2430.Google Scholar
Liu, FL, Mo, EP, Yang, L, Du, J, Wang, HS, Zhang, H, Kurihara, H, Xu, J and Cai, SH (2016 a) Autophagy is involved in TGF-beta1-induced protective mechanisms and formation of cancer-associated fibroblasts phenotype in tumor microenvironment. Oncotarget 7, 4122–4141.Google Scholar
Liu, S, Zhu, L, Zhang, J, Yu, J, Cheng, X and Peng, B (2016 b) Anti-osteoclastogenic activity of isoliquiritigenin via inhibition of NF-kappaB-dependent autophagic pathway. Biochemical Pharmacology 106, 82–93.Google Scholar
Mizushima, N (2007) Autophagy: process and function. Genes & Development 21, 2861–2873.Google Scholar
Mizushima, N, Levine, B, Cuervo, AM and Klionsky, DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069–1075.Google Scholar
Nabavi, N, Khandani, A, Camirand, A and Harrison, RE (2011) Effects of microgravity on osteoclast bone resorption and osteoblast cytoskeletal organization and adhesion. Bone 49, 965–974.Google Scholar
Nollet, M, Santucci-Darmanin, S, Breuil, V, Al-Sahlanee, R, Cros, C, Topi, M, Momier, D, Samson, M, Pagnotta, S, Cailleteau, L, Battaglia, S, Farlay, D, Dacquin, R, Barois, N, Jurdic, P, Boivin, G, Heymann, D, Lafont, F, Lu, SS, Dempster, DW, Carle, GF and Pierrefite-Carle, V (2014) Autophagy in osteoblasts is involved in mineralization and bone homeostasis. Autophagy 10, 1965–1977.Google Scholar
Nuschke, A, Rodrigues, M, Stolz, DB, Chu, CT, Griffith, L and Wells, A (2014) Human mesenchymal stem cells/multipotent stromal cells consume accumulated autophagosomes early in differentiation. Stem Cell Research & Therapy 5, 140.Google Scholar
Pierrefite-Carle, V, Santucci-Darmanin, S, Breuil, V, Camuzard, O and Carle, GF (2015) Autophagy in bone: self-eating to stay in balance. Ageing Research Reviews 24, 206–217.Google Scholar
Riley, DA, Ellis, S, Slocum, GR, Satyanarayana, T, Bain, JL and Sedlak, FR (1987) Hypogravity-induced atrophy of rat soleus and extensor digitorum longus muscles. Muscle & Nerve 10, 560–568.Google Scholar
Rokhlenko, KD and Mul'diiarov, P (1981) [Myocardial ultrastructure of rats exposed aboard biosatellite ‘Cosmos-936’]. Kosmicheskaia Biologiia I Aviakosmicheskaia Meditsina 15, 77–82.Google Scholar
Roos, WP, Thomas, AD and Kaina, B (2016) DNA damage and the balance between survival and death in cancer biology. Nature Reviews Cancer 16, 20–33.Google Scholar
Ryu, HW, Choi, SH, Namkoong, S, Jang, IS, Seo, DH, Choi, I, Kim, HS and Park, J (2014) Simulated microgravity contributes to autophagy induction by regulating AMP-activated protein kinase. DNA and Cell Biology 33, 128–135.Google Scholar
Sambandam, Y, Blanchard, JJ, Daughtridge, G, Kolb, RJ, Shanmugarajan, S, Pandruvada, SN, Bateman, TA and Reddy, SV (2010) Microarray profile of gene expression during osteoclast differentiation in modelled microgravity. Journal of Cellular Biochemistry 111, 1179–1187.Google Scholar
Sambandam, Y, Townsend, MT, Pierce, JJ, Lipman, CM, Haque, A, Bateman, TA and Reddy, SV (2014) Microgravity control of autophagy modulates osteoclastogenesis. Bone 61, 125–131.Google Scholar
Sambandam, Y, Baird, KL, Stroebel, M, Kowal, E, Balasubramanian, S and Reddy, SV (2016) Microgravity induction of TRAIL expression in preosteoclast cells enhances osteoclast differentiation. Scientific Reports 6, 25143.Google Scholar
Sandona, D, Desaphy, JF, Camerino, GM, Bianchini, E, Ciciliot, S, Danieli-Betto, D, Dobrowolny, G, Furlan, S, Germinario, E, Goto, K, Gutsmann, M, Kawano, F, Nakai, N, Ohira, T, Ohno, Y, Picard, A, Salanova, M, Schiffl, G, Blottner, D, Musaro, A, Ohira, Y, Betto, R, Conte, D and Schiaffino, S (2012) Adaptation of mouse skeletal muscle to long-term microgravity in the MDS mission. PLoS ONE 7, e33232.Google Scholar
Song, C, Song, C and Tong, F (2014) Autophagy induction is a survival response against oxidative stress in bone marrow-derived mesenchymal stromal cells. Cytotherapy 16, 1361–1370.Google Scholar
Sun, Y, Jiang, Y, Huang, J, Chen, H, Liao, Y and Yang, Z (2017) CISD2 enhances the chemosensitivity of gastric cancer through the enhancement of 5-FU-induced apoptosis and the inhibition of autophagy by AKT/mTOR pathway. Cancer Medicine 6, 2331–2346.Google Scholar
Tamma, R, Colaianni, G, Camerino, C, Di Benedetto, A, Greco, G, Strippoli, M, Vergari, R, Grano, A, Mancini, L, Mori, G, Colucci, S, Grano, M and Zallone, A (2009) Microgravity during spaceflight directly affects in vitro osteoclastogenesis and bone resorption. FASEB Journal 23, 2549–2554.Google Scholar
Vico, L, Collet, P, Guignandon, A, Lafage-Proust, MH, Thomas, T, Rehaillia, M and Alexandre, C (2000) Effects of long-term microgravity exposure on cancellous and cortical weight-bearing bones of cosmonauts. Lancet 355, 1607–1611.Google Scholar
Wang, K, Niu, J, Kim, H and Kolattukudy, PE (2011) Osteoclast precursor differentiation by MCPIP via oxidative stress, endoplasmic reticulum stress, and autophagy. Journal of Molecular Cell Biology 3, 360–368.Google Scholar
Wang, YC, Lu, DY, Shi, F, Zhang, S, Yang, CB, Wang, B, Cao, XS, Du, TY, Gao, Y, Zhao, JD and Sun, XQ (2013) Clinorotation enhances autophagy in vascular endothelial cells. Biochemistry and Cell Biology 91, 309–314.Google Scholar
Wang, Z, Deng, Z, Gan, J, Zhou, G, Shi, T, Wang, Z, Huang, Z, Qian, H, Bao, N, Guo, T, Chen, J, Zhang, J, Liu, F, Dong, L and Zhao, J (2017) Tial6v4 particles promote osteoclast formation via autophagy-mediated downregulation of interferon-beta in osteocytes. Acta Biomaterialia 48, 489–498.Google Scholar
Xiu, Y, Xu, H, Zhao, C, Li, J, Morita, Y, Yao, Z, Xing, L and Boyce, BF (2014) Chloroquine reduces osteoclastogenesis in murine osteoporosis by preventing TRAF3 degradation. Journal of Clinical Investigation 124, 297–310.Google Scholar
Xu, J, Wise, JTF, Wang, L, Schumann, K, Zhang, Z and Shi, X (2017) Dual roles of oxidative stress in metal carcinogenesis. Journal of Environmental Pathology Toxicology and Oncology 36, 345–376.Google Scholar
Yang, Y, Zheng, X, Li, B, Jiang, S and Jiang, L (2014) Increased activity of osteocyte autophagy in ovariectomized rats and its correlation with oxidative stress status and bone loss. Biochemical and Biophysical Research Communications 451, 86–92.Google Scholar
Yoo, YM, Han, TY and Kim, HS (2016) Melatonin suppresses autophagy induced by clinostat in preosteoblast MC3T3-E1 cells. International Journal of Molecular Sciences 17, 526.Google Scholar
Yuge, L, Sasaki, A, Kawahara, Y, Wu, SL, Matsumoto, M, Manabe, T, Kajiume, T, Takeda, M, Magaki, T, Takahashi, T, Kurisu, K and Matsumoto, M (2011) Simulated microgravity maintains the undifferentiated state and enhances the neural repair potential of bone marrow stromal cells. Stem Cells and Development 20, 893–900.Google Scholar
Zahm, AM, Bohensky, J, Adams, CS, Shapiro, IM and Srinivas, V (2011) Bone cell autophagy is regulated by environmental factors. Cells Tissues Organs 194, 274–278.Google Scholar
Zayzafoon, M, Gathings, WE and Mcdonald, JM (2004) Modeled microgravity inhibits osteogenic differentiation of human mesenchymal stem cells and increases adipogenesis. Endocrinology 145, 2421–2432.Google Scholar
Zeng, Q, Liu, J, Cao, P, Li, J, Liu, X, Fan, X, Liu, L, Cheng, Y, Xiong, W, Li, J, Bo, H, Zhu, Y, Yang, F, Hu, J, Zhou, M, Zhou, Y, Zou, Q, Zhou, J and Cao, K (2018) Inhibition of REDD1 sensitizes bladder urothelial carcinoma to paclitaxel by inhibiting autophagy. Clinical Cancer Research 24, 445–459.Google Scholar
Zhang, X, Chen, W, Fan, J, Wang, S, Xian, Z, Luan, J, Li, Y, Wang, Y, Nan, Y, Luo, M, Li, S, Tian, W and Ju, D (2018) Disrupting CD47-SIRPalpha axis alone or combined with autophagy depletion for the therapy of glioblastoma. Carcinogenesis 39, 689–699.Google Scholar
Zhao, Y, Qu, T, Wang, P, Li, X, Qiang, J, Xia, Z, Duan, H, Huang, J and Zhu, L (2016) Unravelling the relationship between macroautophagy and mitochondrial ROS in cancer therapy. Apoptosis 21, 517–531.Google Scholar
Zhong, GH, Ling, SK and Li, YX (2016) [Mechanism of cardiac atrophy under weightlessness/simulated weightlessness]. Sheng Li Xue Bao 68, 194–200.Google Scholar