Fluid flow modulation of murine embryonic stem cell pluripotency gene expression in the absence of LIF

Cellular and Molecular Bioengineering

Volumn 6, Issue 3, 2013, Pages 335-345

  Lara, Giovanna G ^a   Hazenbiller, Olesja ^a   Gareau, Tia ^a   Shepherd, Robert D ^a   Kallos, Michael S ^a   Rancourt, Derrick E ^a   Rinker, Kristina D ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Fluid shear stress; Mechanobiology; Parallel plate flow chambers; Suspension bioreactors.; Viscosity

Indexed keywords

CELL PROTEIN; LEUKEMIA INHIBITORY FACTOR; MESSENGER RNA; OCTAMER TRANSCRIPTION FACTOR 4; REX1 PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CONTACT; CELL DENSITY; CELL DIFFERENTIATION; CELL LEVEL; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FLOW RATE; FLUID FLOW MODULATION; GENE; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENETIC MARKER; MODULATION; MOLECULAR DYNAMICS; MOLECULAR WEIGHT; MOUSE; NANOG GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLURIPOTENT STEM CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REX1 GENE; RNA SEQUENCE; SEQUENCE ANALYSIS; SHEAR STRESS;

MURINAE;

EID: 84892794858     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-013-0287-6     Document Type: Article

References (39)

1. Adamo, L., O. Naveiras, P. L. Wenzel, S. McKinney-Freeman, P. J. Mack, J. Gracia-Sancho, A. Suchy-Dicey, M. Yoshimoto, M. W. Lensch, M. C. Yoder, G. García-Cardeña, and G. Q. Daley. Biomechanical forces promote embryonic haematopoiesis. Nature 459:1131-1135, 2009.
2. Ahsan, T., and R. M. Nerem. Fluid shear stress promotes an endothelial-like phenotype during the early differentiation of embryonic stem cells. Tissue Eng. Part A 16: 3547-3553, 2010.
3. Borghi, N., M. Sorokina, O. G. Shcherbakova, W. I. Weis, B. L. Pruitt, W. J. Nelson, and A. R. Dunn. E-cadherin is under constitutive actomyosin-generated tension that is increased at cell-cell contacts upon externally applied stretch. Proc. Natl Acad. Sci. U.S.A. 109:12568-12573, 2012.
4. Carpenedo, R. L., C. Y. Sargent, and T. C. McDevitt. Rotary suspension culture enhances the efficiency, yield, and homogeneity of embryoid body differentiation. Stem Cells 25:2224-2234, 2007.
5. Chang, T. C., Y. C. Chen, M. H. Yang, C. H. Chen, E. W. Hsing, B. S. Ko, J. Y. Liou, and K. K. Wu. Rho kinases regulate the renewal and neural differentiation of embryonic stem cells in a cell plating density-dependent manner. PLoS ONE 5:e9187, 2010.
6. Chowdhury, F., Y. Li, Y.-C. Poh, T. Yokohama-Tamaki, N. Wang, and T. S. Tanaka. Soft substrates promote homogeneous self-renewal of embryonic stem cells via downregulating cell-matrix tractions. PLoS ONE 5(12): e15655, 2010.
7. Cormier, J. T., N. I. zur Nieden, D. E. Rancourt, and M. S. Kallos. Expansion of undifferentiated murine embryonic stem cells as aggregates in suspension culture bioreactors. Tissue Eng. 12:3233-3245, 2006.
8. Fok, E. Y. L., and P. W. Zandstra. Shear-controlled singlestep mouse embryonic stem cell expansion and EB-based differentiation. Stem Cell 23:1333-1342, 2005.
9. Fridley, K. M., M. A. Kinney, and T. C. McDevitt. Hydrodynamic modulation of pluripotent stem cells. Stem Cell Res. Ther. 3:45, 2012.
10. Fridley, K. M., I. Fernandez, M. T. Li, R. B. Kettlewell, and K. Roy. Unique differentiation profile of mouse embryonic stem cells in rotary and stirred tank bioreactors. Tissue Eng. Part A 16:3285-3298, 2010.
11. Gareau, T., G. Lara, R. D. Shepherd, J. Taiani, R. Krawetz, D. Rancourt, K. D. Rinker, M. S. Kallos. Shear stress influences pluripotency of murine embryonic stem cells in stirred suspension bioreactors. J. Tissue Eng. Regen. Med., 2012. doi:10.1002/term.1518.
12. Gilbertson, J., A. Sen, L. A. Behie, and M. S. Kallos. Scaled-up production of mammalian neural stem and progenitor cells in computer-controlled suspension bioreactors. Biotechnol. Bioeng. 94:783-792, 2006.
13. Kavlock, K. D., and A. S. Goldstein. Effect of pulse frequency on the osteogenic differentiation of mesenchymal stem cells in a pulsatile perfusion bioreactor. J. Biomech. Eng. 133:091005, 2011.
14. Liu, H., J. Lin, and K. Roy. Effect of 3D scaffold and dynamic culture condition on the global gene expression profile of mouse embryonic stem cells. Biomaterials 27:5978-5989, 2006.
15. Loh, Y. H., Q. Wu, J. L. Chew, V. B. Vega, W. Zhang, X. Chen, G. Bourque, J. George, B. Leong, J. Liu, et al. The Oct4 and Nanog transcription network regulates plu-ripotency in mouse embryonic stem cells. Nat. Genet. 38:431-440, 2006.
16. Masui, S., Y. Nakatake, Y. Toyooka, D. Shimosato, R. Yagi, K. Takahashi, H. Okochi, A. Okuda, R. Matoba, A. A. Sharov, M. S. Ko, and H. Niwa. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat. Cell Biol. 9:625-635, 2007.
17. Masui, S., S. Ohtsuka, R. Yagi, K. Takahashi, M. S. Ko, and H. Niwa. Rex1/Zfp42 is dispensable for pluripotency in mouse ES cells. BMC Dev. Biol. 8:45, 2008.
18. Maul, T. M., D. W. Chew, A. Nieponice, and D. A. Vorp. Mechanical stimuli differentially control stem cell behavior: morphology, proliferation, and differentiation. Biomech. Model Mechanobiol. 6:939-953, 2011.
19. McBride, S. H., and M. L. Knothe Tate. Modulation of stem cell shape and fate A: the role of density and seeding protocol on nucleus shape and gene expression. Tissue Eng. Part A. 14:1561-1572, 2008.
20. Moledina, F., G. Clarke, A. Oskooei, K. Onishi, A. Günther, and P. W. Zandstra. Predictive microfluidic control of regulatory ligand trajectories in individual pluripotent cells. Proc. Natl. Acad. Sci. U.S.A. 9:3264-3269, 2012.
21. Niwa, H., J. Miyazaki, and A. G. Smith. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24:372-376, 2000.
22. Palmqvist, L., C. H. Glover, L. Hsu, M. Lu, B. Bossen, J. M. Piret, R. K. Humphries, and C. D. Helgason. Correlation of murine embryonic stem cell gene expression profiles with functional measures of pluripotency. Stem Cells 23:663-680, 2005.
23. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45, 2001.
24. Sargent, C. Y., G. Y. Berguig, M. A. Kinney, L. A. Hiatt, R. L. Carpenedo, R. E. Berson, and T. C. McDevitt. Hydrodynamic modulation of embryonic stem cell differentiation by rotary orbital suspension culture. Biotechnol. Bioeng. 105:611-626, 2010.
25. Shafa, M., R. Krawetz, Y. Zhang, J. B. Rattner, A. Godollei, H. J. Duff, and D. E. Rancourt. Impact of stirred suspension bioreactor culture on the differentiation of murine embryonic stem cells into cardiomyocytes. BMC Cell Biol. 12:53, 2011.
26. Sharp, L. A., Y. W. Lee, and A. S. Goldstein. Effect of lowfrequency pulsatile flow on expression of osteoblastic genes by bone marrow stromal cells. Ann. Biomed. Eng. 37: 445-453, 2009.
27. Shepherd, R. D., S. M. Kos, and K. D. Rinker. Long-term pulsatile shear stress leads to increased phosphorylation of multiple MAPK species in cultured human aortic endothelial cells. Biorheology 46:529-538, 2009.
28. Sun, Y., L. G. Villa-Diaz, R. H. W. Lam, W. Chen, P. H. Krebsback, and J. Fu. Mechanics regulates fate decisions of human embryonic stem cells. PLoS ONE 7(5):e37178. doi:10.1371/journal.pone.0037178.
29. Taiani, J., R. J. Krawetz, N. zur Nieden, Y. E. Wu, M. S. Kallos, J. R. Matyas, and D. E. Rancourt. Reduced differentiation efficiency of murine embryonic stem cells in stirred suspension bioreactors. Stem Cells Dev. 19:989-998, 2010.
30. Toh, Y.-C., and J. Voldman. Fluid shear stress primes mouse embryonic stem cells for differentiation in a selfrenewing environment via heparin sulfate proteoglycans transduction. FASEB J. 25:1208-1217, 2011.
31. Uda, Y., Y.-C. Poh, F. Chowdhury, D. C. Wu, T. S. Tanaka, M. Sato, and N. Wang. Force via integrins but not E-cadherin decreases Oct3/4 expression in embryonic stem cells. Biochem. Biophys. Res. Commun. 415:396-400, 2011.
32. Venkat, R. V., and J. J. Chalmers. Characterization of agitation environments in 250 ml spinner vessel, 3 L, and 20 L reactor vessels used for animal cell microcarrier culture. Cytotechnology 22:95-102, 1996.
33. Viegas, K. D., M. Mehdi, S. Dol, R. D. Shepherd, R. Martinuzzi, and K. D. Rinker. Methicillin Resistant Staphylococcus aureus attachment to endothelium is wall shear stress dependent. BioMed. Eng. OnLine 10:20, 2011.
34. Williams, R. L., D. J. Hilton, S. Pease, T. A. Willson, C. L. Stewart, D. P. Gearing, E. F. Wagner, D. Metcalf, N. A. Nicola, and N. M. Gough. Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells. Nature 336:684-687, 1988.
35. Wolfe, R. P., and T. Ahsan. Shear stress during early embryonic stem cell differentiation promotes hematopoietic and endothelial phenotypes. Biotechnol. Bioeng. 110:1231-1242, 2013.
36. Wolfe, R. P., J. Leleux, R. M. Nerem, and T. Ahsan. Effects of shear stress on germ lineage specification of embryonic stem cells. Integr. Biol. 4:1263-1273, 2012.
37. Yamamoto, K., T. Sokabe, T. Watabe, K. Miyazono, J. K. Yamashita, S. Obi, N. Ohura, A. Matsushita, A. Kamiya, and J. Ando. Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am. J. Physiol. Heart Circ. Physiol. 288:1915-1924, 2005.
38. Yee, A., K. A. Bosworth, D. E. Conway, S. G. Eskin, and L. V. McIntire. Gene expression of endothelial cells under pulsatile non-reversing vs. steady shear stress; comparison of nitric oxide production. Ann. Biomed. Eng. 36:571-579, 2008.
39. zur Nieden, N. I., J. T. Cormier, D. E. Rancourt, and M. S. Kallos. Embryonic stem cells remain highly pluripotent following long term expansion as aggregates in suspension bioreactors. J. Biotechnol. 129:421-432, 2007.