Identifications of novel mechanisms in breast cancer cells involving duct-like multicellular spheroid formation after exposure to the Random Positioning Machine

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Kopp, Sascha ^a   Slumstrup, Lasse ^b   Corydon, Thomas J ^b   Sahana, Jayashree ^b   Aleshcheva, Ganna ^a   Islam, Tawhidul ^b   Magnusson, Nils E ^b   Wehland, Markus ^a   Bauer, Johann ^c   Infanger, Manfred ^a   Grimm, Daniela ^a,b  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

^c MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSKELETON PROTEIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA, HUMAN; FLT1 PROTEIN, HUMAN; IL8 PROTEIN, HUMAN; INTERLEUKIN 8; MRFAP1 PROTEIN, HUMAN; NUCLEAR PROTEIN; SIGNAL PEPTIDE; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VEGFA PROTEIN, HUMAN;

CELL MEMBRANE; DEVICES; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MCF-7 CELL LINE; METABOLISM; MULTICELLULAR SPHEROID; PHENOTYPE; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; ULTRASTRUCTURE; WEIGHTLESSNESS;

CELL MEMBRANE; CYTOSKELETAL PROTEINS; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-8; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MCF-7 CELLS; NUCLEAR PROTEINS; PHENOTYPE; PROTEIN INTERACTION MAPPING; SIGNAL TRANSDUCTION; SPHEROIDS, CELLULAR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; WEIGHTLESSNESS SIMULATION;

EID: 84971326359     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep26887     Document Type: Article

References (97)

1. Ferlay, J., et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136, E359-386, doi: 10.1002/ijc.29210 (2015).
2. Kristensen, T. B., et al. Anti-vascular endothelial growth factor therapy in breast cancer. Int. J. Mol. Sci. 15, 23024-23041, doi: 10.3390/ijms151223024 (2014).
3. Grimm, D., Wehland, M., Pietsch, J., Infanger, M., & Bauer, J. Drugs interfering with apoptosis in breast cancer. Curr. Pharm. Des. 17, 272-283, doi: 10.2174/138161211795049723 (2011).
4. Wehland, M., Bauer, J., Infanger, M., & Grimm, D. Target-based anti-Angiogenic therapy in breast cancer. Curr. Pharm. Des. 18, 4244-4257, doi: 10.2174/138161212802430468 (2012).
5. Pietsch, J., et al. A proteomic approach to analysing spheroid formation of two human thyroid cell lines cultured on a random positioning machine. Proteomics 11, 2095-2104, doi: 10.1002/pmic.201000817 (2011).
6. Grosse, J., et al. Gravity-sensitive signaling drives 3-dimensional formation of multicellular thyroid cancer spheroids. FASEB J. 26, 5124-5140, doi: 10.1096/fj.12-215749 (2012).
7. Kopp, S., et al. Mechanisms of three-dimensional growth of thyroid cells during long-Term simulated microgravity. Sci. Rep. 5, 16691, doi: 10.1038/srep16691 (2015).
8. Aleshcheva, G., et al. Scaffold-free tissue formation under real and simulated microgravity conditions. Basic Clin. Pharmacol. Toxicol., doi: 10.1111/bcpt.12561 (2016).
9. Pietsch, J., et al. Spheroid formation of human thyroid cancer cells in an automated culturing system during the Shenzhou-8 Space mission. Biomaterials 34, 7694-7705, doi: 10.1016/j.biomaterials.2013.06.054 (2013).
10. Warnke, E., et al. Spheroid formation of human thyroid cancer cells under simulated microgravity: a possible role of CTGF and CAV1. Cell Commun. Signal. 12, 32, doi: 10.1186/1478-811X-12-32 (2014).
11. Kunz-Schughart, L. A. Multicellular tumor spheroids: intermediates between monolayer culture and in vivo tumor. Cell Biol. Int. 23, 157-161, doi: 10.1006/cbir.1999.0384 (1999).
12. Hirschhaeuser, F., et al. Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol. 148, 3-15, doi: 10.1016/j.jbiotec.2010.01.012 (2010).
13. Grimm, D., et al. Growing tissues in real and simulated microgravity: new methods for tissue engineering. Tissue Eng. Pt. B Rev. 20, 555-566, doi: 10.1089/ten.TEB.2013.0704 (2014).
14. Vassy, J., et al. The effect of weightlessness on cytoskeleton architecture and proliferation of human breast cancer cell line MCF-7. FASEB J. 15, 1104-1106, doi: 10.1096/fj.00-0527fje (2001).
15. Qian, A., et al. Simulated weightlessness alters biological characteristics of human breast cancer cell line MCF-7. Acta Astronaut. 63, 947-958, doi: http://dx.doi.org/10.1016/j.actaastro.2008.01.024 (2008).
16. Li, J., et al. Modeled microgravity causes changes in the cytoskeleton and focal adhesions, and decreases in migration in malignant human MCF-7 cells. Protoplasma 238, 23-33, doi: 10.1007/s00709-009-0068-1 (2009).
17. Zheng, H.-X., et al. Expression of estrogen receptor α in human breast cancer cells regulates mitochondrial oxidative stress under simulated microgravity. Adv. Space Res. 49, 1432-1440, doi: 10.1016/j.asr.2012.02.020 (2012).
18. Masiello, M. G., et al. Phenotypic switch induced by simulated microgravity on MDA-MB-231 breast cancer cells. Biomed Res. Int. 2014, 652434, doi: 10.1155/2014/652434 (2014).
19. Wuest, S. L., Richard, S., Kopp, S., Grimm, D., & Egli, M. Simulated microgravity: critical review on the use of random positioning machines for mammalian cell culture. Biomed Res. Int. 2015, 971474, doi: 10.1155/2015/971474 (2015).
20. Pietsch, J., et al. Metabolic enzyme diversity in different human thyroid cell lines and their sensitivity to gravitational forces. Proteomics 12, 2539-2546, doi: 10.1002/pmic.201200070 (2012).
21. Soule, H. D., Vazguez, J., Long, A., Albert, S., & Brennan, M. A human cell line from a pleural effusion derived from a breast carcinoma. J. Natl. Cancer Inst. 51, 1409-1416, doi: 10.1093/jnci/51.5.1409 (1973).
22. Pietsch, J., et al. The effects of weightlessness on the human organism and mammalian cells. Curr. Mol. Med. 11, 350-364, doi: 10.2174/156652411795976600 (2011).
23. Suzuki, A., & Ohno, S. The PAR-APKC system: lessons in polarity. J. Cell Sci. 119, 979-987, doi: 10.1242/jcs.02898 (2006).
24. Ma, X., et al. Genomic approach to identify factors that drive the formation of three-dimensional structures by EA.hy926 endothelial cells. PLoS One 8, e64402, doi: 10.1371/journal.pone.0064402 (2013).
25. Calo, E., & Khutoryanskiy, V. V. Biomedical applications of hydrogels: A review of patents and commercial products. Eur. Polym. J. 65, 252-267, doi: 10.1016/j.eurpolymj.2014.11.024 (2015).
26. Ma, X., et al. Differential gene expression profile and altered cytokine secretion of thyroid cancer cells in space. FASEB J. 28, 813-835, doi: 10.1096/fj.13-243287 (2014).
27. Bizzarri, M., Monici, M., & van Loon, J. J. How microgravity affects the biology of living systems. Biomed Res. Int. 2015, 863075, doi: 10.1155/2015/863075 (2015).
28. Becker, J. L., & Souza, G. R. Using space-based investigations to inform cancer research on Earth. Nat. Rev. Cancer 13, 315-327, doi: 10.1038/nrc3507 (2013).
29. Grimm, D., et al. A delayed type of three-dimensional growth of human endothelial cells under simulated weightlessness. Tissue Eng. Pt. A 15, 2267-2275, doi: 10.1089/ten.tea.2008.0576 (2009).
30. Testa, F., et al. Fractal analysis of shape changes in murine osteoblasts cultured under simulated microgravity. Rend Lincei-Sci Fis. 25, S39-S47, doi: 10.1007/s12210-014-0291-3 (2014).
31. Mesland, D. A. Possible actions of gravity on the cellular machinery. Adv. Space Res. 12, 15-25, doi: 10.1016/0273-1177(92)90259-Z (1992).
32. Mesland, D. A. Mechanisms of gravity effects on cells: are there gravity-sensitive windows?. Adv. Space Biol. Med. 2, 211-228, doi: 10.1016/S1569-2574(08)60022-2 (1992).
33. Grimm, D., Wise, P., Lebert, M., Richter, P., & Baatout, S. How and why does the proteome respond to microgravity?. Expert Rev. Proteomics 8, 13-27, doi: 10.1586/epr.10.105 (2011).
34. Lewis, M. L., et al. Spaceflight alters microtubules and increases apoptosis in human lymphocytes (Jurkat). FASEB J. 12, 1007-1018, doi: 0892-6638/98/0012-1007 (1998).
35. Hughes-Fulford, M., & Lewis, M. L. Effects of microgravity on osteoblast growth activation. Exp. Cell Res. 224, 103-109, doi: 10.1006/excr.1996.0116 (1996).
36. Morbidelli, L., et al. Simulated hypogravity impairs the angiogenic response of endothelium by up-regulating apoptotic signals. Biochem. Biophys. Res. Commun. 334, 491-499, doi: 10.1016/j.bbrc.2005.06.124 (2005).
37. Cogoli, A., Tschopp, A., & Fuchs-Bislin, P. Cell sensitivity to gravity. Science 225, 228-230, doi: 10.1126/science.6729481 (1984).
38. Uva, B. M., et al. Clinorotation-induced weightlessness influences the cytoskeleton of glial cells in culture. Brain Res. 934, 132-139, doi: 10.1016/S0006-8993(02)02415-0 (2002).
39. Grimm, D., et al. Simulated microgravity alters differentiation and increases apoptosis in human follicular thyroid carcinoma cells. FASEB J. 16, 604-606, doi: 10.1096/fj.01-0673fje (2002).
40. Ulbrich, C., 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. 28, 185-198, doi: 10.1159/000331730 (2011).
41. Grosse, J., et al. Short-Term weightlessness produced by parabolic flight maneuvers altered gene expression patterns in human endothelial cells. FASEB J. 26, 639-655, doi: 10.1096/fj.11-194886 (2012).
42. Gruener, R., Roberts, R., & Reitstetter, R. Reduced receptor aggregation and altered cytoskeleton in cultured myocytes after spaceflight. Biol. Sci. Space 8, 79-93, doi: http://doi.org/10.2187/bss.8.79 (1994).
43. Lewis, M. L., et al. cDNA microarray reveals altered cytoskeletal gene expression in space-flown leukemic T lymphocytes (Jurkat). FASEB J. 15, 1783-1785, doi: 10.1096/fj.00-0820fje (2001).
44. Vorselen, D., Roos, W. H., MacKintosh, F. C., Wuite, G. J., & van Loon, J. J. The role of the cytoskeleton in sensing changes in gravity by nonspecialized cells. FASEB J. 28, 536-547, doi: 10.1096/fj.13-236356 (2014).
45. Boonstra, J. Growth factor-induced signal transduction in adherent mammalian cells is sensitive to gravity. FASEB J. 13 Suppl, S35-42, doi: 0892-6638/99/0013-0S35 (1999).
46. Bizzarri, M., Cucina, A., Palombo, A., & Masiello, M. G. Gravity sensing by cells: mechanisms and theoretical grounds. Rend. Lincei-Sci. Fis. 25, S29-S38, doi: 10.1007/s12210-013-0281-x (2014).
47. Svejgaard, B., et al. Common Effects on Cancer Cells Exerted by a Random Positioning Machine and a 2D Clinostat. PLoS One 10, e0135157, doi: 10.1371/journal.pone.0135157 (2015).
48. Grosse, J., et al. Mechanisms of apoptosis in irradiated and sunitinib-Treated follicular thyroid cancer cells. Apoptosis 19, 480-490, doi: 10.1007/s10495-013-0937-0 (2014).
49. Kondepudi, D. K., & Storm, P. B. Gravity detection through bifurcation. Adv. Space Res. 12, 7-14, doi: 10.1016/0273-1177(92)90258-Y (1992).
50. Grimm, D., 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. Pt. A 16, 1559-1573, doi: 10.1089/ten.TEA.2009.0524 (2010).
51. Ma, X., et al. Proteomic differences between microvascular endothelial cells and the EA.hy926 cell line forming three-dimensional structures. Proteomics 14, 689-698, doi: 10.1002/pmic.201300453 (2014).
52. Plachot, C., et al. Factors necessary to produce basoapical polarity in human glandular epithelium formed in conventional and highthroughput three-dimensional culture: example of the breast epithelium. BMC Biol. 7, 77, doi: 10.1186/1741-7007-7-77 (2009).
53. Debnath, J., et al. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 111, 29-40, doi: http://dx.doi.org/10.1016/S0092-8674(02)01001-2 (2002).
54. Debnath, J., & Brugge, J. S. Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5, 675-688, doi: 10.1038/nrc1695 (2005).
55. Vassy, J., et al. Weightlessness acts on human breast cancer cell line MCF-7. Adv. Space Res. 32, 1595-1603, doi: 10.1016/S0273-1177(03)90400-5 (2003).
56. Ulbrich, C., et al. Characterization of human chondrocytes exposed to simulated microgravity. Cell. Physiol. Biochem. 25, 551-560, doi: 10.1159/000303059 (2010).
57. Beck, M., et al. Simulated microgravity decreases apoptosis in fetal fibroblasts. Int. J. Mol. Med. 30, 309-313, doi: 10.3892/ijmm.2012.1001 (2012).
58. Aleshcheva, G., et al. Tissue engineering of cartilage on ground-based facilities. Microgravity Sci. Technol. In press, doi: 10.1007/s12217-015-9479-0 (2016).
59. Russo, J., Hu, Y. F., Silva, I. D., & Russo, I. H. Cancer risk related to mammary gland structure and development. Microsc. Res. Tech. 52, 204-223, doi: 10.1002/1097-0029(20010115)52:2 3.0.CO;2-F (2001).
60. Pisanu, M. E., et al. Lung cancer stem cell lose their stemness default state after exposure to microgravity. Biomed Res. Int. 2014, 470253, doi: 10.1155/2014/470253 (2014).
61. Kenny, P. A., & Bissell, M. J. Tumor reversion: correction of malignant behavior by microenvironmental cues. Int. J. Cancer 107, 688-695, doi: 10.1002/ijc.11491 (2003).
62. Vidi, P. A., Bissell, M. J., & Lelievre, S. A. Three-dimensional culture of human breast epithelial cells: the how and the why. Methods Mol. Biol. 945, 193-219, doi: 10.1007/978-1-62703-125-7-13 (2013).
63. Nakamura, T., et al. E-cadherin-dependent intercellular adhesion enhances chemoresistance. Int. J. Mol. Med. 12, 693-700, doi: 10.3892/ijmm.12.5.693 (2003).
64. Brouty-Boye, D., Mainguene, C., Magnien, V., Israel, L., & Beaupain, R. Fibroblast-mediated differentiation in human breast carcinoma cells (MCF-7) grown as nodules in vitro. Int. J. Cancer 56, 731-735, doi: 10.1002/ijc.2910560520 (1994).
65. Kocaturk, B., et al. Alternatively spliced tissue factor synergizes with the estrogen receptor pathway in promoting breast cancer progression. J. Thromb. Haemost. 13, 1683-1693, doi: 10.1111/jth.13049 (2015).
66. Mohammed, H., et al. Progesterone receptor modulates ERalpha action in breast cancer. Nature 523, 313-317, doi: 10.1038/nature14583 (2015).
67. Infanger, M., et al. Simulated weightlessness changes the cytoskeleton and extracellular matrix proteins in papillary thyroid carcinoma cells. Cell Tissue Res. 324, 267-277, doi: 10.1007/s00441-005-0142-8 (2006).
68. Tseng, L., Tang, M., Wang, Z., & Mazella, J. Progesterone receptor (hPR) upregulates the fibronectin promoter activity in human decidual fibroblasts. DNA Cell Biol. 22, 633-640, doi: 10.1089/104454903770238102 (2003).
69. Chen, S., et al. Regulation of vascular endothelial growth factor expression by extra domain B segment of fibronectin in endothelial cells. Invest. Ophthalmol. Vis. Sci. 53, 8333-8343, doi: 10.1167/iovs.12-9766 (2012).
70. Sandig, H., et al. Fibronectin is a TH1-specific molecule in human subjects. J. Allergy Clin. Immunol. 124, 528-535, 535 e521-525, doi: 10.1016/j.jaci.2009.04.036 (2009).
71. Higashimoto, I., Chihara, J., Kawabata, M., Nakajima, S., & Osame, M. Adhesion to fibronectin regulates expression of intercellular adhesion molecule-1 on eosinophilic cells. Int. Arch. Allergy Immunol. 120 Suppl 1, 34-37, doi: 53591 (1999).
72. Orecchia, A., et al. Endothelial cell adhesion to soluble vascular endothelial growth factor receptor-1 triggers a cell dynamic and angiogenic phenotype. FASEB J. 28, 692-704, doi: 10.1096/fj.12-225771 (2014).
73. Mainiero, F., et al. RAC1/P38 MAPK signaling pathway controls beta1 integrin-induced interleukin-8 production in human natural killer cells. Immunity 12, 7-16, doi: 10.1016/S1074-7613(00)80154-5 (2000).
74. Nam, J. M., Onodera, Y., Bissell, M. J., & Park, C. C. Breast cancer cells in three-dimensional culture display an enhanced radioresponse after coordinate targeting of integrin alpha5beta1 and fibronectin. Cancer Res. 70, 5238-5248, doi: 10.1158/0008-5472.CAN-09-2319 (2010).
75. Howe, E. N., Cochrane, D. R., & Richer, J. K. Targets of miR-200c mediate suppression of cell motility and anoikis resistance. Breast Cancer Res. 13, R45, doi: 10.1186/bcr2867 (2011).
76. Fehon, R. G., McClatchey, A. I., & Bretscher, A. Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287, doi: 10.1038/nrm2866 (2010).
77. Tsukita, S., & Yonemura, S. Cortical actin organization: lessons from ERM (ezrin/radixin/moesin) proteins. J. Biol. Chem. 274, 34507-34510, doi: 10.1074/jbc.274.49.34507 (1999).
78. Thompson, P. W., Randi, A. M., & Ridley, A. J. Intercellular adhesion molecule (ICAM)-1, but not ICAM-2, activates RhoA and stimulates c-fos and rhoA transcription in endothelial cells. J. Immunol. 169, 1007-1013, doi: 10.4049/jimmunol.169.2.1007 (2002).
79. Simpson, K. J., et al. Identification of genes that regulate epithelial cell migration using an siRNA screening approach. Nat. Cell Biol. 10, 1027-1038, doi: 10.1038/ncb1762 (2008).
80. Vantangoli, M. M., Madnick, S. J., Huse, S. M., Weston, P., & Boekelheide, K. MCF-7 Human Breast Cancer Cells Form Differentiated Microtissues in Scaffold-Free Hydrogels. PLoS One 10, e0135426, doi: 10.1371/journal.pone.0135426 (2015).
81. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687, doi: 10.1016/S0092-8674(02)00971-6 (2002).
82. Halon, A., Donizy, P., Surowiak, P., & Matkowski, R. ERM/Rho protein expression in ductal breast cancer: a 15 year follow-up. Cell. Oncol. (Dordr.) 36, 181-190, doi: 10.1007/s13402-013-0125-9 (2013).
83. Yeh, Y. C., Lin, H. H., & Tang, M. J. A tale of two collagen receptors, integrin beta1 and discoidin domain receptor 1, in epithelial cell differentiation. Am. J. Physiol. Cell Physiol. 303, C1207-1217, doi: 10.1152/ajpcell.00253.2012 (2012).
84. Lu, P., Weaver, V. M., & Werb, Z. The extracellular matrix: a dynamic niche in cancer progression. J. Cell Biol. 196, 395-406, doi: 10.1083/jcb.201102147 (2012).
85. Dvorak, H. F., Weaver, V. M., Tlsty, T. D., & Bergers, G. Tumor microenvironment and progression. J. Surg. Oncol. 103, 468-474, doi: 10.1002/jso.21709 (2011).
86. Infanger, M., et al. Modeled gravitational unloading induced downregulation of endothelin-1 in human endothelial cells. J. Cell. Biochem. 101, 1439-1455, doi: 10.1002/jcb.21261 (2007).
87. Ferrara, N., Gerber, H. P., & LeCouter, J. The biology of VEGF and its receptors. Nat. Med. 9, 669-676, doi: 10.1038/nm0603-669 (2003).
88. 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. 7, 347-357, doi: http://dx.doi.org/10.2174/157016109788340640 (2009).
89. Kowanetz, M., & Ferrara, N. Vascular endothelial growth factor signaling pathways: therapeutic perspective. Clin. Cancer Res. 12, 5018-5022, doi: 10.1158/1078-0432.CCR-06-1520 (2006).
90. Freund, A., et al. IL-8 expression and its possible relationship with estrogen-receptor-negative status of breast cancer cells. Oncogene 22, 256-265, doi: 10.1038/sj.onc.1206113 (2003).
91. Sankpal, N. V., Fleming, T. P., & Gillanders, W. E. EpCAM modulates NF-kappaB signaling and interleukin-8 expression in breast cancer. Mol. Cancer Res. 11, 418-426, doi: 10.1158/1541-7786.MCR-12-0518 (2013).
92. Corydon, T. J., et al. Alterations of the cytoskeleton in human cells in space proved by life-cell imaging. Sci. Rep. 6, 20043, doi: 10.1038/srep20043 (2016).
93. Aleshcheva, G., et al. Changes in morphology, gene expression and protein content in chondrocytes cultured on a random positioning machine. PLoS One 8, e79057, doi: 10.1371/journal.pone.0079057 (2013).
94. Rothermund, L., et al. Early onset of chondroitin sulfate and osteopontin expression in angiotensin II-dependent left ventricular hypertrophy. Am. J. Hypertens. 15, 644-652, doi: 10.1016/S0895-7061(02)02956-4 (2002).
95. Zhang, Y., et al. Lipocalin 2 expression and secretion is highly regulated by metabolic stress, cytokines, and nutrients in adipocytes. PLoS One 9, e96997, doi: 10.1371/journal.pone.0096997 (2014).
96. Thomas, S., & Bonchev, D. A survey of current software for network analysis in molecular biology. Human genomics 4, 353-360, doi: 10.1186/1479-7364-4-5-353 (2010).
97. Pietsch, J., et al. Interaction of proteins identified in human thyroid cells. Int. J. Mol. Sci. 14, 1164-1178, doi: 10.3390/ijms14011164 (2013).