Porous Membranes Promote Endothelial Differentiation of Adipose-Derived Stem Cells and Perivascular Interactions
Tóm tắt
Efforts to create physiologically relevant microenvironments for cell differentiation have led to the creation of three-dimensional (3D) support matrices with varying physical and chemical properties. In an effort to simplify the complexity of these matrices, while maintaining their unique permeable nature, we investigated the culture and differentiation of adipose-derived stem cells (ADSCs) on porous membranes. Membranes offer many of the benefits of a 3D matrix, but simplify cell seeding, imaging, analysis and post-differentiation recovery. After inducing the differentiation of ADSCs into endothelial cells (ECs), the cells cultured on porous substrates produce more branch points and greater tube length in angiogenesis assays compared to the cells cultured on non-porous controls. While we confirm that ADSCs can be induced with vascular endothelial growth factor to express endothelial adhesion molecule CD31 (PECAM-1), only when co-cultured across a membrane with human umbilical vein endothelial cells (HUVECs), do a subset of ADSCs show appropriate CD31 distribution along cell boundaries. Others have recently described that mesenchymal stem cells derive from perivascular cells including pericytes, which are known to wrap circumferentially around microvessels. We used ultrathin porous membranes to permit limited physical interactions between polarized HUVECs and ADSCs. In this arrangement, we found that the majority of ADSCs aligned perpendicular to the polarized HUVECs even though contact between the cell types was limited by pores less than 500 nm in diameter. Together, this ADSC pericyte behavior in combination with the ability to differentiate into ECs shows the potential versatility of ADSCs in the engineering of vascular networks.
Từ khóa
Tài liệu tham khảo
Agrawal, A. A., et al. Porous nanocrystalline silicon membranes as highly permeable and molecularly thin substrates for cell culture. Biomaterials 31:5408–5417, 2010.
Armulik, A., A. Abramsson, and C. Betsholtz. Endothelial/pericyte interactions. Circ. Res. 97:512–523, 2005.
Armulik, A., G. Genové, and C. Betsholtz. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21:193–215, 2011.
Bae, H., et al. Building vascular networks. Sci. Transl. Med. 4:160ps23, 2012.
Battinelli, E. M., B. A. Markens, R. A. Kulenthirarajan, K. R. Machlus, R. Flaumenhaft, and J. E. Italiano. Anticoagulation inhibits tumor cell-mediated release of platelet angiogenic proteins and diminishes platelet angiogenic response. Blood 123:101–112, 2014.
Benoit, D. S. W., M. P. Schwartz, A. R. Durney, and K. S. Anseth. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat. Mater. 7:816–823, 2008.
Blocki, A., et al. Not all MSCs can act as pericytes: functional in vitro assays to distinguish pericytes from other mesenchymal stem cells in angiogenesis. Stem Cells Dev. 22:2347–2355, 2013.
Bunnell, B. A., M. Flatt, C. Gagliardi, B. Patel, and C. Ripoll. Adipose-derived stem cells: isolation, expansion and differentiation. Methods 45:115–120, 2008.
Cheng, A. Y., and A. J. García. Engineering the matrix microenvironment for cell delivery and engraftment for tissue repair. Curr. Opin. Biotechnol. 24:864–871, 2013.
Cheng, G., et al. Engineered blood vessel networks connect to host vasculature via wrapping-and-tapping anastomosis. Blood 118:4740–4749, 2011.
Chua, K. H., F. Raduan, W. K. Z. Wan Safwani, N. F. M. Manzor, B. Pingguan-Murphy, and S. Sathapan. Effects of serum reduction and VEGF supplementation on angiogenic potential of human adipose stromal cells in vitro. Cell Prolif. 46:300–311, 2013.
Crisan, M., M. Corselli, W. C. W. Chen, and B. Péault. Perivascular cells for regenerative medicine. J. Cell Mol. Med. 16:2851–2860, 2012; (edited by N. I. Moldovan).
Crisan, M., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313, 2008.
Discher, D. E., D. J. Mooney, and P. W. Zandstra. Growth factors, matrices, and forces combine and control stem cells. Science 324:1673–1677, 2009.
Dominici, M., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317, 2006.
Dubois, S. G., et al. Isolation of human adipose-derived stem cells from biopsies and liposuction specimens. Methods Mol. Biol. 449:69–79, 2008.
Escobedo-Lucea, C., et al. A xenogeneic-free protocol for isolation and expansion of human adipose stem cells for clinical uses. PLoS ONE 8:e67870, 2013.
Fischer, L. J., et al. Endothelial differentiation of adipose-derived stem cells: effects of endothelial cell growth supplement and shear force. J. Surg. Res. 152:157–166, 2009.
Flaherty, J. T., J. E. Pierce, V. J. Ferrans, D. J. Patel, W. K. Tucker, and D. L. Fry. Endothelial nuclear patterns in the canine arterial tree with particular reference to hemodynamic events. Circ. Res. 30:23–33, 1972.
Gaustad, K. G., A. C. Boquest, B. E. Anderson, A. M. Gerdes, and P. Collas. Differentiation of human adipose tissue stem cells using extracts of rat cardiomyocytes. Biochem. Biophys. Res. Commun. 314:420–427, 2004.
Geevarghese, A., and I. M. Herman. Pericyte-endothelial crosstalk: implications and opportunities for advanced cellular therapies. Transl. Res. 163:296–306, 2014.
Gimble, J. M., B. A. Bunnell, E. S. Chiu, and F. Guilak. Concise review: adipose-derived stromal vascular fraction cells and stem cells: let’s not get lost in translation. Stem Cells 29:749–754, 2011.
Gimble, J. M., A. J. Katz, and B. A. Bunnell. Adipose-derived stem cells for regenerative medicine. Circ. Res. 100:1249–1260, 2007.
Khademhosseini, A., R. Langer, J. Borenstein, and J. P. Vacanti. Microscale technologies for tissue engineering and biology. Proc. Natl. Acad. Sci. USA 103:2480–2487, 2006.
Langille, B. L., and S. L. Adamson. Relationship between blood flow direction and endothelial cell orientation at arterial branch sites in rabbits and mice. Circ. Res. 48:481–488, 1981.
Lee, J. S., et al. A long-term follow-up study of intravenous autologous mesenchymal stem cell transplantation in patients with ischemic stroke. Stem Cells 28:1099–1106, 2010.
Malda, J., T. J. Klein, and Z. Upton. The roles of hypoxia in the in vitro engineering of tissues. Tissue Eng. 13:2153–2162, 2007.
Meijering, E., M. Jacob, J.-C. F. Sarria, P. Steiner, H. Hirling, and M. Unser. Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58:167–176, 2004.
Merfeld-Clauss, S., N. Gollahalli, K. L. March, and D. O. Traktuev. Adipose tissue progenitor cells directly interact with endothelial cells to induce vascular network formation. Tissue Eng. Part A 16:2953–2966, 2010.
Miller, J. S., et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat. Mater. 11:768–774, 2012.
Peng, L., et al. Autologous bone marrow mesenchymal stem cell transplantation in liver failure patients caused by hepatitis B: short-term and long-term outcomes. Hepatology 54:820–828, 2011.
Reinhart-King, C. A. How matrix properties control the self-assembly and maintenance of tissues. Ann. Biomed. Eng. 39:1849–1856, 2011.
Sorrell, J. M., M. A. Baber, and A. I. Caplan. Influence of adult mesenchymal stem cells on in vitro vascular formation. Tissue Eng. Part A 15:1751–1761, 2009.
Striemer, C. C., T. R. Gaborski, J. L. McGrath, and P. M. Fauchet. Charge- and size-based separation of macromolecules using ultrathin silicon membranes. Nature 445:749–753, 2007.
Traktuev, D. O., et al. A population of multipotent CD34-positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ. Res. 102:77–85, 2008.
Versaevel, M., T. Grevesse, and S. Gabriele. Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nat. Commun. 2:1–11, 2012.
Williams, A. R., and J. M. Hare. Mesenchymal stem cells: biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ. Res. 109:923–940, 2011.
Yang, C., W. Wang, and Z. Li. Optimization of corona-triggered PDMS–PDMS bonding method. Proceedings of the IEEE International Conference on NEMS, pp. 319–322, 2009.
Yuan, L., N. Sakamoto, G. Song, and M. Sato. High-level shear stress stimulates endothelial differentiation and VEGF secretion by human mesenchymal stem cells. Cell. Mol. Bioeng. 6:220–229, 2013.
Yuen, P. K., and V. N. Goral. Low-cost rapid prototyping of flexible microfluidic devices using a desktop digital craft cutter. Lab Chip 10:384–387, 2010.
Zeng, G., et al. Orientation of endothelial cell division is regulated by VEGF signaling during blood vessel formation. Blood 109:1345–1352, 2007.
Zouani, O. F., Y. Lei, and M.-C. Durrieu. Pericytes, stem-cell-like cells, but not mesenchymal stem cells are recruited to support microvascular tube stabilization. Small 9:3070–3075, 2013.