Scaffold-free Tissue Formation Under Real and Simulated Microgravity Conditions

Basic and Clinical Pharmacology and Toxicology

Volumn 119, Issue , 2016, Pages 26-33

  Aleshcheva, Ganna ^a   Bauer, Johann ^b   Hemmersbach, Ruth ^c   Slumstrup, Lasse ^d   Wehland, Markus ^a   Infanger, Manfred ^a   Grimm, Daniela ^a,d  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^c GERMAN AEROSPACE CENTER DLR   (Germany)

^d AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADHERENT CELL; CANCER CELL; CELL AGGREGATION; CELL CULTURE; CELL DENSITY; CELLULAR DISTRIBUTION; CHONDROGENESIS; CULTURE MEDIUM; CULTURE VESSEL; ENDOTHELIUM CELL; GENE EXPRESSION; GENOMICS; HISTOGENESIS; HUMAN; MICROGRAVITY; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SCAFFOLD FREE TISSUE FORMATION; SIMULATION; TISSUE ENGINEERING; TISSUE REGENERATION; TUMOR SPHEROID; ADVERSE EFFECTS; AEROSPACE MEDICINE; ANIMAL; CARTILAGE; CELL CULTURE TECHNIQUE; CELL LINE; CYTOLOGY; DEVICES; MEDICAL RESEARCH; PHYSIOLOGY; PROCEDURES; REGENERATION; REGENERATIVE MEDICINE; TRENDS; VASCULAR ENDOTHELIUM; WEIGHTLESSNESS;

AEROSPACE MEDICINE; ANIMALS; BIOMEDICAL RESEARCH; CARTILAGE; CELL CULTURE TECHNIQUES; CELL LINE; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; HUMANS; REGENERATION; REGENERATIVE MEDICINE; TISSUE ENGINEERING; WEIGHTLESSNESS; WEIGHTLESSNESS SIMULATION;

EID: 84959301676     PISSN: 17427835     EISSN: 17427843     Source Type: Journal    
DOI: 10.1111/bcpt.12561     Document Type: Review

References (54)

1. Ulbrich C, Westphal K, Pietsch J, Winkler HD, Leder A, Bauer J et al. Characterization of human chondrocytes exposed to simulated microgravity. Cell Physiol Biochem 2010;25:551–60.
2. Grosse J, Wehland M, Pietsch J, Schulz H, Saar K, Hubner N et al. Gravity-sensitive signaling drives 3-dimensional formation of multicellular thyroid cancer spheroids. FASEB J 2012;26:5124–40.
3. Unsworth BR, Lelkes PI. Growing tissues in microgravity. Nat Med 1998;4:901–7.
4. Chang TT, Hughes-Fulford M. Monolayer and spheroid culture of human liver hepatocellular carcinoma cell line cells demonstrate distinct global gene expression patterns and functional phenotypes. Tissue Eng Part A 2009;15:559–67.
5. Ingram M, Techy GB, Saroufeem R, Yazan O, Narayan KS, Goodwin TJ et al. Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor. In Vitro Cell Dev Biol Anim 1997;33:459–66.
6. Grimm D, Bauer J, Kossmehl P, Shakibaei M, Schoberger J, Pickenhahn H et al. Simulated microgravity alters differentiation and increases apoptosis in human follicular thyroid carcinoma cells. FASEB J 2002;16:604–6.
7. Warnke E, Pietsch J, Wehland M, Bauer J, Infanger M, Gorog 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.
8. Svejgaard B, Wehland M, Ma X, Kopp S, Sahana J, Warnke E et al. Common effects on cancer cells exerted by a random positioning machine and a 2D clinostat. PLoS One 2015;10:e0135157.
9. Pietsch J, Ma X, Wehland M, Aleshcheva G, Schwarzwalder A, Segerer J et al. Spheroid formation of human thyroid cancer cells in an automated culturing system during the Shenzhou-8 Space mission. Biomaterials 2013;34:7694–705.
10. Herranz R, Anken R, Boonstra J, Braun M, Christianen PC, de Geest M et al. Ground-based facilities for simulation of microgravity: organism-specific recommendations for their use, and recommended terminology. Astrobiology 2013;13:1–17.
11. Grimm D, Wehland M, Pietsch J, Aleshcheva G, Wise P, van Loon J et al. Growing tissues in real and simulated microgravity: new methods for tissue engineering. Tissue Eng Part B Rev 2014;20:555–66.
12. Grimm D, Infanger M, Westphal K, Ulbrich C, Pietsch J, Kossmehl P et al. A delayed type of three-dimensional growth of human endothelial cells under simulated weightlessness. Tissue Eng Part A 2009;15:2267–75.
13. Mitteregger R, Vogt G, Rossmanith E, Falkenhagen D. Rotary cell culture system (RCCS): a new method for cultivating hepatocytes on microcarriers. Int J Artif Organs 1999;22:816–22.
14. Hammond TG, Hammond JM. Optimized suspension culture: the rotating-wall vessel. Am J Physiol Renal Physiol 2001;281:F12–25.
15. Aird WC. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med 2012;2:a006429.
16. Chiu B, Wan JZ, Abley D, Akabutu J. Induction of vascular endothelial phenotype and cellular proliferation from human cord blood stem cells cultured in simulated microgravity. Acta Astronaut 2005;56:918–22.
17. Zhang X, Nan Y, Wang H, Chen J, Wang N, Xie J et al. Model microgravity enhances endothelium differentiation of mesenchymal stem cells. Naturwissenschaften 2013;100:125–33.
18. Carlsson SI, Bertilaccio MT, Ascari I, Bradamante S, Maier JA. Modulation of human endothelial cell behaviour in simulated microgravity. J Gravit Physiol 2002;9:P273–4.
19. Morbidelli L, Monici M, Marziliano N, Cogoli A, Fusi F, Waltenberger J et al. Simulated hypogravity impairs the angiogenic response of endothelium by up-regulating apoptotic signals. Biochem Biophys Res Commun 2005;334:491–9.
20. Infanger M, Kossmehl P, Shakibaei M, Cogoli A, Witzing A, Faramarzi S et al. Vascular endothelial growth factor inhibits programmed cell death of endothelial cells induced by clinorotation. J Gravit Physiol 2004;11:P199–200.
21. Infanger M, Kossmehl P, Shakibaei M, Baatout S, Witzing A, Grosse J et al. Induction of three-dimensional assembly and increase in apoptosis of human endothelial cells by simulated microgravity: impact of vascular endothelial growth factor. Apoptosis 2006;11:749–64.
22. Grimm D, Bauer J, Ulbrich C, Westphal K, Wehland M, Infanger M et al. Different responsiveness of endothelial cells to vascular endothelial growth factor and basic fibroblast growth factor added to culture media under gravity and simulated microgravity. Tissue Eng Part A 2010;16:1559–73.
23. Ma X, Wehland M, Schulz H, Saar K, Hubner N, Infanger M et al. Genomic approach to identify factors that drive the formation of three-dimensional structures by EA.hy926 endothelial cells. PLoS ONE 2013;8:e64402.
24. Ma X, Sickmann A, Pietsch J, Wildgruber R, Weber G, Infanger M et al. Proteomic differences between microvascular endothelial cells and the EA.hy926 cell line forming three-dimensional structures. Proteomics 2014;14:689–98.
25. Tamura T, Sakai Y, Nakazawa K. Two-dimensional microarray of HepG2 spheroids using collagen/polyethylene glycol micropatterned chip. J Mater Sci Mater Med 2008;19:2071–7.
26. Spheroids in cancer research: methods and perspectives. Acker H, Carlsson J, Durand R, Sutherland RM (eds). Berlin, NY, Springer-Verlag, 1984.
27. Durand RE, Sutherland RM. Dependence of the radiation response of an in vitro tumor model on cell cycle effects. Cancer Res 1973;33:213–9.
28. Nederman T, Carlsson J, Malmqvist M. Penetration of substances into tumor tissue–a methodological study on cellular spheroids. In Vitro 1981;17:290–8.
29. Freyer JP, Sutherland RM. Regulation of growth saturation and development of necrosis in EMT6/Ro multicellular spheroids by the glucose and oxygen supply. Cancer Res 1986;46:3504–12.
30. Grimm D, Bauer J, Schoenberger J. Blockade of neoangiogenesis, a new and promising technique to control the growth of malignant tumors and their metastases. Curr Vasc Pharmacol 2009;7:347–57.
31. Hirschhaeuser F, Menne H, Dittfeld C, West J, Mueller-Klieser W, Kunz-Schughart LA. Multicellular tumor spheroids: an underestimated tool is catching up again. J Biotechnol 2010;148:3–15.
32. Ma X, Pietsch J, Wehland M, Schulz H, Saar K, Hubner N et al. Differential gene expression profile and altered cytokine secretion of thyroid cancer cells in space. FASEB J 2014;28:813–35.
33. Riwaldt S, Pietsch J, Sickmann A, Bauer J, Braun M, Segerer J et al. Identification of proteins involved in inhibition of spheroid formation under microgravity. Proteomics 2015;15:2945–52.
34. Bauer J, Wehland M, Pietsch J, Sickmann A, Weber G, Grimm D. Annotated gene and proteome data support recognition of interconnections between the results of different experiments in space research. Microgravity Sci Technol 2016; in press, published online 02 September 2015; doi:10.1007/s12217-015-9451-z.
35. Vidyasekar P, Shyamsunder P, Arun R, Santhakumar R, Kapadia NK, Kumar R et al. Genome wide expression profiling of cancer cell lines cultured in microgravity reveals significant dysregulation of cell cycle and microRNA gene networks. PLoS One 2015;10:e0135958.
36. Ingram M, Techy GB, Ward BR, Imam SA, Atkinson R, Ho H et al. Tissue engineered tumor models. Biotech Histochem 2010;85:213–29.
37. Kaur P, Ward B, Saha B, Young L, Groshen S, Techy G et al. Human breast cancer histoid: an in vitro 3-dimensional co-culture model that mimics breast cancer tissue. J Histochem Cytochem 2011;59:1087–100.
38. Martin A, Zhou A, Gordon RE, Henderson SC, Schwartz AE, Schwartz AE et al. Thyroid organoid formation in simulated microgravity: influence of keratinocyte growth factor. Thyroid 2000;10:481–7.
39. Wenger R, Hans MG, Welter JF, Solchaga LA, Sheu YR, Malemud CJ. Hydrostatic pressure increases apoptosis in cartilage-constructs produced from human osteoarthritic chondrocytes. Front Biosci 2006;11:1690–5.
40. Marlovits S, Tichy B, Truppe M, Gruber D, Vecsei V. Chondrogenesis of aged human articular cartilage in a scaffold-free bioreactor. Tissue Eng 2003;9:1215–26.
41. Giannoni P, Pagano A, Maggi E, Arbico R, Randazzo N, Grandizio M et al. Autologous chondrocyte implantation (ACI) for aged patients: development of the proper cell expansion conditions for possible therapeutic applications. Osteoarthritis Cartilage 2005;13:589–600.
42. Foldager CB, Nielsen AB, Munir S, Ulrich-Vinther M, Soballe K, Bunger C et al. Combined 3D and hypoxic culture improves cartilage-specific gene expression in human chondrocytes. Acta Orthop 2011;82:234–40.
43. Barbero A, Grogan S, Schafer D, Heberer M, Mainil-Varlet P, Martin I. Age related changes in human articular chondrocyte yield, proliferation and post-expansion chondrogenic capacity. Osteoarthritis Cartilage 2004;12:476–84.
44. Kim IL, Mauck RL, Burdick JA. Hydrogel design for cartilage tissue engineering: a case study with hyaluronic acid. Biomaterials 2011;32:8771–82.
45. Aleshcheva G, Sahana J, Ma X, Hauslage J, Hemmersbach R, Egli M et al. Changes in morphology, gene expression and protein content in chondrocytes cultured on a random positioning machine. PLoS One 2013;8:e79057.
46. Pietsch J, Bauer J, Egli M, Infanger M, Wise P, Ulbrich C et al. The effects of weightlessness on the human organism and mammalian cells. Curr Mol Med 2011;11:350–64.
47. Grosse J, Wehland M, Pietsch J, Ma X, Ulbrich C, Schulz H et al. Short-term weightlessness produced by parabolic flight maneuvers altered gene expression patterns in human endothelial cells. FASEB J 2012;26:639–55.
48. Ma X, Wehland M, Aleshcheva G, Hauslage J, Wasser K, Hemmersbach R et al. Interleukin-6 expression under gravitational stress due to vibration and hypergravity in follicular thyroid cancer cells. PLoS ONE 2013;8:e68140.
49. Wehland M, Aleshcheva G, Schulz H, Saar K, Hubner N, Hemmersbach R 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.
50. Aleshcheva G, Wehland M, Sahana J, Bauer J, Corydon TJ, Hemmersbach R 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;29:2303–14.
51. Obermaier C, Jankowski V, Schmutzler C, Bauer J, Wildgruber R, Infanger M et al. Free-flow isoelectric focusing of proteins remaining in cell fragments following sonication of thyroid carcinoma cells. Electrophoresis 2005;26:2109–16.
52. Eiermann P, Kopp S, Hauslage J, Hemmersbach R, Gerzer R, Ivanova K. Adaptation of a 2-D clinostat for simulated microgravity experiments with adherent cells. Microgravity Sci Technol 2013;25:153–9.
53. Van Loon JWA. Some history and use of the random positioning machine, RPM, in gravity related research. Adv Space Res 2007;39:1161–5.
54. Klaus DM. Clinostats and bioreactors. Gravit Space Biol Bull 2001;14:55–64.