392
Views
22
CrossRef citations to date
0
Altmetric
Review

Current knowledge about the impact of microgravity on the proteome

, , ORCID Icon, ORCID Icon, , , , & show all
Pages 5-16 | Received 30 Aug 2018, Accepted 16 Nov 2018, Published online: 29 Nov 2018

References

  • Cogoli A, Tschopp A, Fuchs-Bislin P. Cell sensitivity to gravity. Science. 1984;225(4658):228–230.
  • Cogoli A, Tschopp A. Lymphocyte reactivity during spaceflight. Immunol Today. 1985;6(1):1–4.
  • Battista N, Meloni MA, Bari M, et al. 5-Lipoxygenase-dependent apoptosis of human lymphocytes in the International Space Station: data from the ROALD experiment. FASEB J. 2012;26(5):1791–1798.
  • Gasperi V, Rapino C, Battista N, et al. A functional interplay between 5-lipoxygenase and mu-calpain affects survival and cytokine profile of human Jurkat T lymphocyte exposed to simulated microgravity. Biomed Res Int. 2014;2014:782390.
  • Chang TT, Spurlock SM, Candelario TL, et al. Spaceflight impairs antigen-specific tolerance induction in vivo and increases inflammatory cytokines. FASEB J. 2015;29(10):4122–4132.
  • Boonyaratanakornkit JB, Cogoli A, Li CF, et al. Key gravity-sensitive signaling pathways drive T cell activation. FASEB J. 2005;19(14):2020–2022.
  • Monici M, Fusi F, Paglierani M, et al. Modeled gravitational unloading triggers differentiation and apoptosis in preosteoclastic cells. J Cell Biochem. 2006;98(1):65–80.
  • Svejgaard B, Wehland M, Ma X, et al. Common effects on cancer cells exerted by a random positioning machine and a 2D clinostat. PLoS One. 2015;10(8):e0135157.
  • Grimm D, Pietsch J, Wehland M, et al. The impact of microgravity-based proteomics research. Expert Rev Proteomics. 2014;11(4):465–476.
  • Braun M, Limbach C. Rhizoids and protonemata of characean algae: model cells for research on polarized growth and plant gravity sensing. Protoplasma. 2006;229(2–4):133–142.
  • Strauch SM, Richter P, Schuster M, et al. The beating pattern of the flagellum of Euglena gracilis under altered gravity during parabolic flights. J Plant Physiol. 2010;167(1):41–46.
  • Corydon TJ, Kopp S, Wehland M, et al. Alterations of the cytoskeleton in human cells in space proved by life-cell imaging. Sci Rep. 2016;6:20043.
  • Thiel CS, Hauschild S, Huge A, et al. Dynamic gene expression response to altered gravity in human T cells. Sci Rep. 2017;7(1):5204.
  • Wehland M, Aleshcheva G, Schulz H, et al. Differential gene expression of human chondrocytes cultured under short-term altered gravity conditions during parabolic flight maneuvers. Cell Commun Signal. 2015;13:18.
  • Nasir A, Strauch SM, Becker I, et al. The influence of microgravity on Euglena gracilis as studied on Shenzhou 8. Plant Biol (Stuttg). 2014;16(Suppl 1):113–119.
  • Tauber S, Lauber BA, Paulsen K, et al. Cytoskeletal stability and metabolic alterations in primary human macrophages in long-term microgravity. PLoS One. 2017;12(4):e0175599.
  • Baio J, Martinez AF, Silva I, et al. Cardiovascular progenitor cells cultured aboard the International Space Station exhibit altered developmental and functional properties. NPJ Microgravity. 2018;4:13.
  • Li N, Wang C, Sun S, et al. Microgravity-induced alterations of inflammation-related mechanotransduction in endothelial cells on board SJ-10 satellite. Front Physiol. 2018;9:1025.
  • Borst AG, van Loon JJWA. Technology and developments for the random positioning machine, RPM. Microgravity Sci Technol. 2008;21(4):287.
  • Wuest SL, Richard S, Kopp S, et al. Simulated microgravity: critical review on the use of random positioning machines for mammalian cell culture. Biomed Res Int. 2015;2015:971474.
  • Herranz R, Anken R, Boonstra J, et al. Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology. 2013;13(1):1–17.
  • Grimm D, Egli M, Krüger M, et al. Tissue engineering under microgravity conditions - use of stem cells and specialized cells. Stem Cells Dev. 2018;27(12):787–804.
  • Wuest SL, Stern P, Casartelli E, et al. Fluid dynamics appearing during simulated microgravity using random positioning machines. PLoS One. 2017;12(1):e0170826.
  • Strauch SM, Hemmersbach R, Seibt D, et al. Behavior of gravisensitive cells on 2D and 3D clinostats. J Gravitat Physiol. 2005;12:259–260.
  • Hemmersbach R, Strauch SM, Seibt D, et al. Comparative studies on gravisensitive protists on ground (2D and 3D clinostats) and in microgravity. Microgravity Sci Technol. 2006;18(3):257–259.
  • Pietsch J, Gass S, Nebuloni S, et al. Three-dimensional growth of human endothelial cells in an automated cell culture experiment container during the SpaceX CRS-8 ISS space mission - The SPHEROIDS project. Biomaterials. 2017;124:126–156.
  • Pietsch J, Ma X, Wehland M, et al. Spheroid formation of human thyroid cancer cells in an automated culturing system during the Shenzhou-8 Space mission. Biomaterials. 2013;34(31):7694–7705.
  • Häder D-P, Braun M, Hemmersbach R. Gravity sensing, graviorientation and microgravity. In: Ruyters G, Braun M, Editors. Gravitational biology I: gravity sensing and graviorientation in microorganisms and plants. SpringerBriefs in Space Life Sciences Cham: Springer International Publishing; 2018. p. 1–11.
  • Machemer H, Braucker R. Gravireception and graviresponses in ciliates. Acta Protozool. 1992;31(4):185–214.
  • Plattner H. Signalling in ciliates: long- and short-range signals and molecular determinants for cellular dynamics. Biol Rev Camb Philos Soc. 2017;92(1):60–107.
  • Bedini C, Lanfranchi A, Nobili R. The ultrastructure of the müller body in remanellA (Ciliata Holothrica Loxodidae). Monitore Zoologico Italiano. 1973;7(1–2):87–95.
  • Hemmersbach R, Voormanns R, Briegleb W, et al. Influence of accelerations on the spatial orientation of Loxodes and Paramecium. J Biotechnol. 1996;47(2–3):271–278.
  • Hemmersbach R, Donath R. Gravitaxis of Loxodes and Paramecium. Eur J Protistol. 1995;31:433.
  • Ten Hagen B, Kümmel F, Wittkowski R, et al. Gravitaxis of asymmetric self-propelled colloidal particles. Nat Commun. 2014;5:4829.
  • Roberts AM. Mechanisms of gravitaxis in Chlamydomonas. Biol Bull. 2006;210(2):78–80.
  • Roberts AM, Deacon FM. Gravitaxis in motile micro-organisms: the role of fore–aft body asymmetry. J Fluid Mech. 2002;452:405–423.
  • Ebenezer TE, Carrington M, Lebert M, et al. Euglena gracilis genome and transcriptome: organelles, nuclear genome assembly strategies and initial features. Adv Exp Med Biol. 2017;979:125–140.
  • Ebenezer T The genome of Euglena gracilis: Annotation, function and expression University of Cambridge. 2018.
  • Häder D-P, Richter P, Lebert M. Signal transduction in gravisensing of flagellates. Signal Transduction. 2006;6(6):422–431.
  • Häder D-P, Richter PR, Schuster M, et al. Molecular analysis of the graviperception signal transduction in the flagellate Euglena gracilis: involvement of a transient receptor potential-like channel and a calmodulin. Adv Space Res. 2009;43(8):1179–1184.
  • Daiker V, Häder DP, Richter PR, et al. The involvement of a protein kinase in phototaxis and gravitaxis of Euglena gracilis. Planta. 2011;233(5):1055–1062.
  • Daiker V, Lebert M, Richter P, et al. Molecular characterization of a calmodulin involved in the signal transduction chain of gravitaxis in Euglena gracilis. Planta. 2010;231(5):1229–1236.
  • Nasir A, Le Bail A, Daiker V, et al. Identification of a flagellar protein implicated in the gravitaxis in the flagellate Euglena gracilis. Sci Rep. 2018;8(1):7605.
  • Nasir A Analysis of signal transduction chains of gravity and light sensing in Euglena gracilis: Friedrich-Alexander-University Erlangen-Nuremberg. 2016.
  • Rakusova H, Fendrych M, Friml J. Intracellular trafficking and PIN-mediated cell polarity during tropic responses in plants. Curr Opin Plant Biol. 2015;23:116–123.
  • Band LR, Wells DM, Fozard JA, et al. Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell. 2014;26(3):862–875.
  • Kitakura S, Vanneste S, Robert S, et al. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell. 2011;23(5):1920–1931.
  • Grimm D, Wise P, Lebert M, et al. How and why does the proteome respond to microgravity? Expert Rev Proteomics. 2011;8(1):13–27.
  • Kordyum EL, Chapman DK. Plants and microgravity: patterns of microgravity effects at the cellular and molecular levels. Cytol Genet. 2017;51(2):108–116.
  • Kordyum EL. Plant cell gravisensitivity and adaptation to microgravity. Plant Biol (Stuttg). 2014;16(Suppl 1):79–90.
  • Zhang Y, Wang L, Xie J, et al. Differential protein expression profiling of Arabidopsis thaliana callus under microgravity on board the Chinese SZ-8 spacecraft. Planta. 2015;241(2):475–488.
  • Zhang Y, Zheng HQ. Changes in plastid and mitochondria protein expression in Arabidopsis thaliana callus on board Chinese Spacecraft SZ-8 [journal article]. Microgravity Sci Technol. 2015;27(6):387–401.
  • Manzano AI, van Loon JJ, Christianen PC, et al. Gravitational and magnetic field variations synergize to cause subtle variations in the global transcriptional state of Arabidopsis in vitro callus cultures. BMC Genomics. 2012;13:105.
  • Herranz R, Manzano AI, van Loon JJ, et al. Proteomic signature of Arabidopsis cell cultures exposed to magnetically induced hyper- and microgravity environments. Astrobiology. 2013;13(3):217–224.
  • Mazars C, Briere C, Grat S, et al. Microgravity induces changes in microsome-associated proteins of Arabidopsis seedlings grown on board the international space station. PLoS One. 2014;9(3):e91814.
  • Mazars C, Briere C, Grat S, et al. Microsome-associated proteome modifications of Arabidopsis seedlings grown on board the International Space Station reveal the possible effect on plants of space stresses other than microgravity. Plant Signal Behav. 2014;9(9):e29637.
  • Ferl RJ, Koh J, Denison F, et al. Spaceflight induces specific alterations in the proteomes of Arabidopsis. Astrobiology. 2015;15(1):32–56.
  • Chen B, Wang Y. Proteomic and physiological studies provide insight into photosynthetic response of rice (Oryza sativa L.) seedlings to microgravity. Photochem Photobiol. 2016;92(4):561–570.
  • Jiao S, Hilaire E, Paulsen AQ, et al. Brassica rapa plants adapted to microgravity with reduced photosystem I and its photochemical activity. Physiol Plant. 2004;122(2):281–290.
  • Chen B, Zhang A, Lu Q, et al. Characterization of photosystem I in rice (Oryza sativa L.) seedlings upon exposure to random positioning machine. Photosynth Res. 2013;116(1):93–105.
  • Schüler O, Krause L, Görög M, et al. ARADISH - Development of a standardized plant growth chamber for experiments in gravitational biology using ground based facilities. Microgravity Sci Technol. 2016;28(3):297–305.
  • Hashiguchi Y, Tasaka M, Morita MT. Mechanism of higher plant gravity sensing. Am J Bot. 2013;100(1):91–100.
  • Vandenbrink JP, Kiss JZ. Space, the final frontier: a critical review of recent experiments performed in microgravity. Plant Sci. 2016;243:115–119.
  • Pietsch J, Kussian R, Sickmann A, et al. Application of free-flow IEF to identify protein candidates changing under microgravity conditions. Proteomics. 2010;10(5):904–913.
  • Aleshcheva G, Sahana J, Ma X, et al. Changes in morphology, gene expression and protein content in chondrocytes cultured on a random positioning machine. PLoS One. 2013;8(11):e79057.
  • Aleshcheva G, Wehland M, Sahana J, et al. Moderate alterations of the cytoskeleton in human chondrocytes after short-term microgravity produced by parabolic flight maneuvers could be prevented by up-regulation of BMP-2 and SOX-9. FASEB J. 2015;29(6):2303–2314.
  • Grimm D, Bauer J, Kossmehl P, et al. Simulated microgravity alters differentiation and increases apoptosis in human follicular thyroid carcinoma cells. FASEB J. 2002;16(6):604–606.
  • Kopp S, Slumstrup L, Corydon TJ, et al. Identifications of novel mechanisms in breast cancer cells involving duct-like multicellular spheroid formation after exposure to the random positioning machine. Sci Rep. 2016;6:26887.
  • Kopp S, Warnke E, Wehland M, et al. Mechanisms of three-dimensional growth of thyroid cells during long-term simulated microgravity. Sci Rep. 2015;5:16691.
  • Pietsch J, Sickmann A, Weber G, et al. A proteomic approach to analysing spheroid formation of two human thyroid cell lines cultured on a random positioning machine. Proteomics. 2011;11(10):2095–2104.
  • Warnke E, Pietsch J, Wehland M, et al. Spheroid formation of human thyroid cancer cells under simulated microgravity: a possible role of CTGF and CAV1. Cell Commun Signal. 2014;12:32.
  • Ulbrich C, Pietsch J, Grosse J, et al. Differential gene regulation under altered gravity conditions in follicular thyroid cancer cells: relationship between the extracellular matrix and the cytoskeleton. Cell Physiol Biochem. 2011;28(2):185–198.
  • Bauer J, Kopp S, Schlagberger EM, et al. Proteome analysis of human follicular thyroid cancer cells exposed to the random positioning machine. Int J Mol Sci. 2017;18(3).
  • Sahana J, Nassef MZ, Wehland M, et al. Decreased E-Cadherin in MCF7 human breast cancer cells forming multicellular spheroids exposed to simulated microgravity. Proteomics. 2018;18(13):e1800015.
  • White RJ, Averner M. Humans in space. Nature. 2001;409:1115.
  • Ma X, Pietsch J, Wehland M, et al. Differential gene expression profile and altered cytokine secretion of thyroid cancer cells in space. FASEB J. 2014;28(2):813–835.
  • Grimm D, Wehland M, Pietsch J, et al. Growing tissues in real and simulated microgravity: new methods for tissue engineering. Tissue Eng Part B Rev. 2014;20(6):555–566.
  • Grenon SM, Jeanne M, Aguado-Zuniga J, et al. Effects of gravitational mechanical unloading in endothelial cells: association between caveolins, inflammation and adhesion molecules [Article]. Sci Rep. 2013;3:1494.
  • Maier JA, Cialdai F, Monici M, et al. The impact of microgravity and hypergravity on endothelial cells. Biomed Res Int. 2015;2015:434803.
  • Edgell CJ, McDonald CC, Graham JB. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci U S A. 1983;80(12):3734–3737.
  • Ma X, Sickmann A, Pietsch J, et al. Proteomic differences between microvascular endothelial cells and the EA.hy926 cell line forming three-dimensional structures. Proteomics. 2014;14(6):689–698.
  • Dittrich A, Grimm D, Sahana J, et al. Key proteins involved in spheroid formation and angiogenesis in endothelial cells after long-term exposure to simulated microgravity. Cell Physiol Biochem. 2018;45(2):429–445.
  • Li C-F, Sun J-X, Gao Y, et al. Clinorotation-induced autophagy via HDM2-p53-mTOR pathway enhances cell migration in vascular endothelial cells. Cell Death Dis. 2018;9(2):147.
  • Griffoni C, Di Molfetta S, Fantozzi L, et al. Modification of proteins secreted by endothelial cells during modeled low gravity exposure. J Cell Biochem. 2011;112(1):265–272.
  • Janmaleki M, Pachenari M, Seyedpour SM, et al. Impact of simulated microgravity on cytoskeleton and viscoelastic properties of endothelial cell. Sci Rep. 2016;6:32418.
  • Feger BJ, Thompson JW, Dubois LG, et al. Microgravity induces proteomics changes involved in endoplasmic reticulum stress and mitochondrial protection [Article]. Sci Rep. 2016;6:34091.
  • Baio J, Martinez AF, Bailey L, et al. Spaceflight activates protein kinase C alpha signaling and modifies the developmental stage of human neonatal cardiovascular progenitor cells. Stem Cells Dev. 2018;27(12):805–818.
  • Fuentes TI, Appleby N, Raya M, et al. Simulated microgravity exerts an age-dependent effect on the differentiation of cardiovascular progenitors isolated from the human heart. PLoS One. 2015;10(7):e0132378.
  • Hunziker EB. Articular cartilage repair: are the intrinsic biological constraints undermining this process insuperable? Osteoarthritis Cartilage. 1999;7(1):15–28.
  • Jha R, Wu Q, Singh M, et al. Simulated microgravity and 3d culture enhance induction, viability, proliferation and differentiation of cardiac progenitors from human pluripotent stem cells [Article]. Sci Rep. 2016;6:30956.
  • Berry CA. Effects of weightlessness in man. Life Sci Space Res. 1973;11:187–199.
  • Lang T, LeBlanc A, Evans H, et al. Cortical and trabecular bone mineral loss from the spine and hip in long-duration spaceflight. J Bone Miner Res. 2004;19(6):1006–1012.
  • Huey DJ, Hu JC, Athanasiou KA. Unlike bone, cartilage regeneration remains elusive. Science. 2012;338(6109):917–921.
  • Stamenković V, Keller G, Nesic D, et al. Neocartilage formation in 1 g, simulated, and microgravity environments: implications for tissue engineering. Tissue Eng Part A. 2010;16(5):1729–1736.
  • Ulbrich C, Westphal K, Pietsch J, et al. Characterization of human chondrocytes exposed to simulated microgravity. Cell Physiol Biochem. 2010;25(4–5):551–560.
  • Wuest SL, Caliò M, Wernas T, et al. Influence of mechanical unloading on articular chondrocyte dedifferentiation. Int J Mol Sci. 2018;19(5).
  • Yin H, Wang Y, Sun X, et al. Functional tissue-engineered microtissue derived from cartilage extracellular matrix for articular cartilage regeneration. Acta Biomater. 2018;77:127–141.
  • Albi E, Krüger M, Hemmersbach R, et al. Impact of gravity on thyroid cells. Int J Mol Sci. 2017;18(5):972.
  • Obermaier C, Jankowski V, Schmutzler C, et al. Free-flow isoelectric focusing of proteins remaining in cell fragments following sonication of thyroid carcinoma cells. Electrophoresis. 2005;26(11):2109–2116.
  • Pietsch J, Sickmann A, Weber G, et al. Metabolic enzyme diversity in different human thyroid cell lines and their sensitivity to gravitational forces. Proteomics. 2012;12(15–16):2539–2546.
  • Pietsch J, Riwaldt S, Bauer J, et al. Interaction of proteins identified in human thyroid cells. Int J Mol Sci. 2013;14(1):1164–1178.
  • Wildgruber R, Weber G, Wise P, et al. Free-flow electrophoresis in proteome sample preparation. Proteomics. 2014;14(4–5):629–636.
  • Riwaldt S, Pietsch J, Sickmann A, et al. Identification of proteins involved in inhibition of spheroid formation under microgravity. Proteomics. 2015;15(17):2945–2952.
  • Riwaldt S, Bauer J, Pietsch J, et al. The importance of caveolin-1 as key-regulator of three-dimensional growth in thyroid cancer cells cultured under real and simulated microgravity conditions. Int J Mol Sci. 2015;16(12):28296–28310.
  • Chua HL, Bhat-Nakshatri P, Clare SE, et al. NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene. 2007;26(5):711–724.
  • Kopp S, Sahana J, Islam T, et al. The role of NFκB in spheroid formation of human breast cancer cells cultured on the random positioning machine. Sci Rep. 2018;8(1):921.
  • Masiello MG, Cucina A, Proietti S, et al. Phenotypic switch induced by simulated microgravity on MDA-MB-231 breast cancer cells. Biomed Res Int. 2014;2014:12.
  • Tascher G, Brioche T, Maes P, et al. Proteome-wide adaptations of mouse skeletal muscles during a full month in space. J Proteome Res. 2017;16(7):2623–2638.
  • Shen H, Lim C, Schwartz AG, et al. Effects of spaceflight on the muscles of the murine shoulder. FASEB J. 2017;31(12):5466–5477.
  • Radugina EA, Almeida EAC, Blaber E, et al. Exposure to microgravity for 30 days onboard Bion M1 caused muscle atrophy and impaired regeneration in murine femoral quadriceps. Life Sci Space Res (Amst). 2018;16:18–25.
  • Hosoyama T, Ichida S, Kanno M, et al. Microgravity influences maintenance of the human muscle stem/progenitor cell pool. Biochem Biophys Res Commun. 2017;493(2):998–1003.
  • Bauer J, Wehland M, Infanger M, et al. Semantic analysis of posttranslational modification of proteins accumulated in thyroid cancer cells exposed to simulated microgravity. Int J Mol Sci. 2018;19(8).
  • Bauer J, Grimm D, Gombocz E. Semantic analysis of thyroid cancer cell proteins obtained from rare research opportunities. J Biomed Inform. 2017;76:138–153.
  • Warner C. Expands plans for moon exploration: more missions, more science. [cited 2018 Nov 10] Available from: https://www.nasa.gov/feature/nasa-expands-plans-for-moon-exploration-more-missions-more-science
  • Grimm D, Grosse J, Wehland M, et al. The impact of microgravity on bone in humans. Bone. 2016;87:44–56.
  • Hauslage J, Strauch SM, Eßmann O, et al. Eu:CROPIS– “Euglena gracilis: combined regenerative organic-food production in space” - a space experiment testing biological life support systems under lunar and Martian gravity [journal article]. Microgravity Sci Technol. 2018.
  • Costessi A. Bone proteomics. ISS Science for Everyone. [cited 2018 Nov 10] Available from: https://www.nasa.gov/mission_pages/station/research/experiments/565.html
  • Kobayashi H. Medical proteome analysis of osteoporosis and bone mass-related proteins using the Kibo Japanese experiment module of international space station (Medical proteomics). ISS Science for Everyone. [cited 2018 Nov 10] Available from: https://www.nasa.gov/mission_pages/station/research/experiments/2630.html

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.