Endothelial cells derived from embryonic stem cells respond to cues from topographical surface patterns

Journal of Biological Engineering

Kara E McCloskey²  Valerie J Leppert²  Drew E Glaser¹  Jesus Isaac Luna¹  Kevin Mercurio¹  Rachel Hatano³ 

[1] Graduate Program in Biological Engineering and Small-scale Technologies, University of California, Merced, CA, USA;School of Engineering, University of California, P.O. Box 2039, Merced, CA 95344, USA;School of Natural Sciences, University of California, Merced, CA, USA

关键词: Differentiation;    Embryonic stem cells;    Topography;    Contact guidance;    Alignment;    Endothelial cells;   

Others  :  805401
DOI  :  10.1186/1754-1611-7-18

 received in 2012-09-28, accepted in 2013-05-22,  发布年份 2013

【 摘 要 】

The generation of micro- and nano-topography similar to those found in the extra cellular matrix of three-dimensional tissues is one technique used to recapitulate the cell-tissue physiology found in the native tissues. Despite the fact that ample studies have been conducted on the physiological significance of endothelial cells alignment parallel to shear stress, as this is the normal physiologic arrangement for healthy arterial EC, very few studies have examined the use of topographical signals to initiate endothelial cell alignment. Here, we have examined the ability for our mouse embryonic stem cell-derived endothelial cells (ESC-EC) to align on various microchip topographical systems. Briefly, we generated metal molds with ‘wrinkled’ topography using 1) 15 nm and 2) 30 nm of gold coating on the pre-strained polystryene (PS) sheets. After thermal-induced shrinkage of the PS sheets, polydimethylsiloxane (PDMS) microchips were then generated from the wrinkled molds. Using similar Shrink™-based technology, 3) larger selectively crazed acetone-etched lines in the PS sheets, and 4) fully crazed acetone-treated PS sheets of stochastic topographical morphology were also generated. The 15 nm and 30 nm gold coating generated ‘wrinkles’ of uniaxial anisotropic channels at nano-scaled widths while the crazing generated micron-sized channels. The ESC-EC were able to respond and align on the 320 nm, 510 nm, and the acetone-etched 10.5 μm channels, but not on the fully ‘crazed’ topographies. Moreover, the ESC-EC aligned most robustly on the wrinkles, and preferentially to ridge edges on the 10.5 μm-sized channels. The ability to robustly align EC on topographical surfaces enables a variety of controlled physiological studies of EC-EC and EC-ECM contact guidance, as well as having potential applications for the rapid endothelialization of stents and vascular grafts.

【 授权许可】

   
2013 Hatano et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Dalby MJ, Yarwood SJ, Riehle MO, Johnstone HJ, Affrossman S, Curtis AS: Increasing fibroblast response to materials using nanotopography: morphological and genetic measurements of cell response to 13-nm-high polymer demixed islands. Exp Cell Res 2002, 276(1):1-9.
• [2]Recknor JB, Recknor JC, Sakaguchi DS, Mallapragada SK: Oriented astroglial cell growth on micropatterned polystyrene substrates. Biomaterials 2004, 25(14):2753-2767.
• [3]Sorensen A, Alekseeva T, Katechia K, Robertson M, Riehle MO, Barnett SC: Long-term neurite orientation on astrocyte monolayers aligned by microtopography. Biomaterials 2007, 28(36):5498-5508.
• [4]Webb A, Clark P, Skepper J, Compston A, Wood A: Guidance of oligodendrocytes and their progenitors by substratum topography. J Cell Sci 1995, 108(Pt 8):2747-2760.
• [5]Shimizu K, Fujita H, Nagamori E: Alignment of skeletal muscle myoblasts and myotubes using linear micropatterned surfaces ground with abrasives. Biotechnol Bioeng 2009, 103(3):631-638.
• [6]Au HT, Cheng I, Chowdhury MF, Radisic M: Interactive effects of surface topography and pulsatile electrical field stimulation on orientation and elongation of fibroblasts and cardiomyocytes. Biomaterials 2007, 28(29):4277-4293.
• [7]Badie N, Bursac N: Novel micropatterned cardiac cell cultures with realistic ventricular microstructure. Biophys J 2009, 96(9):3873-3885.
• [8]Biehl JK, Yamanaka S, Desai TA, Boheler KR, Russell B: Proliferation of mouse embryonic stem cell progeny and the spontaneous contractile activity of cardiomyocytes are affected by microtopography. Dev Dyn 2009, 238(8):1964-1973.
• [9]Deutsch J, Motlagh D, Russell B, Desai TA: Fabrication of microtextured membranes for cardiac myocyte attachment and orientation. J Biomed Mater Res 2000, 53(3):267-275.
• [10]Geisse NA, Sheehy SP, Parker KK: Control of myocyte remodeling in vitro with engineered substrates. In Vitro Cell Dev Biol Anim 2009, 45(7):343-350.
• [11]Heidi Au HT, Cui B, Chu ZE, Veres T, Radisic M: Cell culture chips for simultaneous application of topographical and electrical cues enhance phenotype of cardiomyocytes. Lab on a chip 2009, 9(4):564-575.
• [12]Luna JI, Ciriza J, Garcia-Ojeda ME, Kong M, Herren A, Lieu DK, Li R, Fowlkes CC, Khine M, McCloskey KE: Multi-scale biomimetic topography for the alignment of neonatal and embryonic stem cell-derived heart cells. Tissue Eng Part C Methods 2011, 17(5):579-588.
• [13]Motlagh D, Hartman TJ, Desai TA, Russell B: Microfabricated grooves recapitulate neonatal myocyte connexin43 and N-cadherin expression and localization. J Biomed Mater Res 2003, 67(1):148-157.
• [14]Thomas SP, Bircher-Lehmann L, Thomas SA, Zhuang J, Saffitz JE, Kleber AG: Synthetic strands of neonatal mouse cardiac myocytes: structural and electrophysiological properties. Circ Res 2000, 87(6):467-473.
• [15]Yeong WY, Yu H, Lim KP, Ng KL, Boey YC, Subbu VS, Tan LP: Multiscale topological guidance for cell alignment via direct laser writing on biodegradable polymer. Tissue Eng Part C Methods 2010, 16(5):1011-1021.
• [16]Zong X, Bien H, Chung CY, Yin L, Fang D, Hsiao BS, Chu B, Entcheva E: Electrospun fine-textured scaffolds for heart tissue constructs. Biomaterials 2005, 26(26):5330-5338.
• [17]Rajnicek AM, Foubister LE, McCaig CD: Alignment of corneal and lens epithelial cells by co-operative effects of substratum topography and DC electric fields. Biomaterials 2008, 29(13):2082-2095.
• [18]Teixeira AI, McKie GA, Foley JD, Bertics PJ, Nealey PF, Murphy CJ: The effect of environmental factors on the response of human corneal epithelial cells to nanoscale substrate topography. Biomaterials 2006, 27(21):3945-3954.
• [19]Stolberg S, McCloskey KE: Can shear stress direct stem cell fate? Biotechnol Prog 2009, 25(1):10-19.
• [20]Liliensiek SJ, Wood JA, Yong J, Auerbach R, Nealey PF, Murphy CJ: Modulation of human vascular endothelial cell behaviors by nanotopographic cues. Biomaterials 2010, 31(20):5418-5426.
• [21]Wood JA, Shah NM, McKee CT, Hughbanks ML, Liliensiek SJ, Russell P, Murphy CJ: The role of substratum compliance of hydrogels on vascular endothelial cell behavior. Biomaterials 2011, 32(22):5056-5064.
• [22]Gasiorowski JZ, Liliensiek SJ, Russell P, Stephan DA, Nealey PF, Murphy CJ: Alterations in gene expression of human vascular endothelial cells associated with nanotopographic cues. Biomaterials 2010, 31(34):8882-8888.
• [23]Candiello J, Balasubramani M, Schreiber EM, Cole GJ, Mayer U, Halfter W, Lin H: Biomechanical properties of native basement membranes. FEBS J 2007, 274(11):2897-2908.
• [24]Liliensiek SJ, Nealey P, Murphy CJ: Characterization of endothelial basement membrane nanotopography in rhesus macaque as a guide for vessel tissue engineering. Tissue eng Part A 2009, 15(9):2643-2651.
• [25]McKee CT, Wood JA, Ly I, Russell P, Murphy CJ: The influence of a biologically relevant substratum topography on human aortic and umbilical vein endothelial cells. Biophys J 2012, 102(5):1224-1233.
• [26]Wood MA: Colloidal lithography and current fabrication techniques producing in-plane nanotopography for biological applications. J R Soc Interface 2007, 4(12):1-17.
• [27]Fu C, Grimes A, Long M, Ferri C, Rich BD, Ghosh S, Ghosh S, Lee LP, Gopinathan A, Khine M: Tunable nanowrinkles on shape memory polymer sheets. Adv Mater 2009, 21:4472-4476.
• [28]Yamashita JK: Differentiation of arterial, venous, and lymphatic endothelial cells from vascular progenitors. Trends Cardiovasc Med 2007, 17(2):59-63.
• [29]You LR, Lin FJ, Lee CT, DeMayo FJ, Tsai MJ, Tsai SY: Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 2005, 435(7038):98-104.
• [30]Glaser DE, Gower RM, Lauer NE, Tam K, Blancas AA, Shih AJ, Simon SI, McCloskey KE: Functional characterization of embryonic stem cell-derived endothelial cells. J Vasc Res 2011, 48(5):415-428.
• [31]McCloskey KE, Lyons I, Rao RR, Stice SL, Nerem RM: Purified and proliferating endothelial cells derived and expanded in vitro from embryonic stem cells. Endothelium 2003, 10(6):329-336.
• [32]McCloskey KE, Smith DA, Jo H, Nerem RM: Embryonic stem cell-derived endothelial cells may lack complete functional maturation in vitro. J Vasc Res 2006, 43(5):411-421.
• [33]McCloskey KE, Stice SL, Nerem RM: In vitro derivation and expansion of endothelial cells from embryonic stem cells. Methods Mol Biol 2006, 330:287-301.
• [34]Wang HU, Chen ZF, Anderson DJ: Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998, 93(5):741-753.
• [35]Yurugi-Kobayashi T, Itoh H, Schroeder T, Nakano A, Narazaki G, Kita F, Yanagi K, Hiraoka-Kanie M, Inoue E, Ara T, et al.: Adrenomedullin/cyclic AMP pathway induces notch activation and differentiation of arterial endothelial cells from vascular progenitors. Arterioscler Thromb Vasc Biol 2006, 26(9):1977-1984.
• [36]Shi Z, Neoh KG, Kang ET, Poh CK, Wang W: Enhanced endothelial differentiation of adipose-derived stem cells by substrate nanotopography. J Tissue Eng Regen Med 2012. PMID: 22628362
• [37]Le Saux G, Magenau A, Bocking T, Gaus K, Gooding JJ: The relative importance of topography and RGD ligand density for endothelial cell adhesion. PLoS One 2011, 6(7):e21869.
• [38]Uttayarat P, Toworfe GK, Dietrich F, Lelkes PI, Composto RJ: Topographic guidance of endothelial cells on silicone surfaces with micro- to nanogrooves: orientation of actin filaments and focal adhesions. J Biomed Mater Res 2005, 75(3):668-680.
• [39]Mani G, Feldman MD, Patel D, Agrawal CM: Coronary stents: a materials perspective. Biomaterials 2007, 28(9):1689-1710.
• [40]Kausch HH, Gensler R, Grein C, Plummer CJG, Scaramuzzino P: Crazing in semicrystalline thermoplastics. J Macromol Sci Phys 1999, B38(5–6):803-815.
• [41]Blancas AA, Lauer NE, McCloskey KE: Endothelial differentiation of embryonic stem cells. Curr Protoc Stem Cell Biol 2008. Chapter 1: Unit 1F 5
• [42]Rao GN, Shaw EL, Arthur EJ, Aquavella JV: Endothelial cell morphology and corneal deturgescence. Ann Ophthalmol 1979, 11(6):885-899.