Nanotopographical control for maintaining undifferentiated human embryonic stem cell colonies in feeder free conditions

Biomaterials

Volumn 35, Issue 3, 2014, Pages 916-928

  Bae, Daekyeong ^a   Moon, Sung Hwan ^b   Park, Bo Gi ^c   Park, Soon Jung ^b   Jung, Taekhee ^b   Kim, Jung Suk ^c   Lee, Kyu Back ^c   Chung, Hyung Min ^a,b,d  

^a CHA Stem Cell Institute   (South Korea)

^b Konkuk University School of Medicine   (South Korea)

^c Korea University   (South Korea)

^d CHA University   (South Korea)

Author keywords

Epithelial mesenchymal transition; Focal adhesions; Gradient nanopattern; Human embryonic stem cells; Nanotopography; Stem cell niche

Indexed keywords

EPITHELIAL-MESENCHYMAL TRANSITION; FOCAL ADHESIONS; HUMAN EMBRYONIC STEM CELLS; NANO PATTERN; NANOTOPOGRAPHIES; STEM-CELL NICHES;

CELL ADHESION; CELL GROWTH; GENE EXPRESSION; NANOSTRUCTURES; STEM CELLS; SUBSTRATES;

FEEDING;

FIBRONECTIN; NERVE CELL ADHESION MOLECULE; UVOMORULIN; VIMENTIN;

ACTIN FILAMENT; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL SURVIVAL; COLONY FORMATION; COMPARATIVE STUDY; CONTROL; CONTROLLED STUDY; CYTOSKELETON; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; FEEDER CELL; FOCAL ADHESION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; STEM CELL CULTURE; TOPOGRAPHY;

EPITHELIAL-MESENCHYMAL TRANSITION; FOCAL ADHESIONS; GRADIENT NANOPATTERN; HUMAN EMBRYONIC STEM CELLS; NANOTOPOGRAPHY; STEM CELL NICHE;

BIOCOMPATIBLE MATERIALS; CADHERINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE; CELLS, CULTURED; EMBRYONIC STEM CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FOCAL ADHESIONS; HUMANS; SURFACE PROPERTIES;

EID: 84887622883     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.10.031     Document Type: Article

References (65)

1. Keung A.J., Kumar S., Schaffer D.V. Presentation counts: microenvironmental regulation of stem cells by biophysical and material cues. Annu Rev Cell Dev Biol 2010, 26:533-556.
2. Lyssiotis C.A., Lairson L.L., Boitano A.E., Wurdak H., Zhu S., Schultz P.G. Chemical control of stem cell fate and developmental potential. Angew Chem Int Ed Engl 2011, 50:200-242.
3. Moore K.A., Lemischka I.R. Stem cells and their niches. Science 2006, 311:1880-1885.
4. Discher D.E., Mooney D.J., Zandstra P.W. Growth factors, matrices, and forces combine and control stem cells. Science 2009, 324:1673-1677.
5. Titushkin I.A., Shin J., Cho M. Anew perspective for stem-cell mechanobiology: biomechanical control of stem-cell behavior and fate. Crit Rev Biomed Eng 2010, 38:393-433.
6. Sun Y., Chen C.S., Fu J. Forcing stem cells to behave: a biophysical perspective of the cellular microenvironment. Annu Rev Biophys 2012, 41:519-542.
7. Guilak F., Cohen D.M., Estes B.T., Gimble J.M., Liedtke W., Chen C.S. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 2009, 5:17-26.
8. Lutolf M.P., Gilbert P.M., Blau H.M. Designing materials to direct stem-cell fate. Nature 2009, 462:433-441.
9. Pakzad M., Totonchi M., Taei A., Seifinejad A., Hassani S.N., Baharvand H. Presence of a ROCK inhibitor in extracellular matrix supports more undifferentiated growth of feeder-free human embryonic and induced pluripotent stem cells upon passaging. Stem Cell Rev 2010, 6:96-107.
10. Abrams G.A., Schaus S.S., Goodman S.L., Nealey P.F., Murphy C.J. Nanoscale topography of the corneal epithelial basement membrane and Descemet's membrane of the human. Cornea 2000, 19:57-64.
11. Timpl R. Macromolecular organization of basement membranes. Curr Opin Cell Biol 1996, 8:618-624.
12. Yim E.K., Pang S.W., Leong K.W. Synthetic nanostructures inducing differentiation of human mesenchymal stem cells into neuronal lineage. Exp Cell Res 2007, 313:1820-1829.
13. Yim E.K., Darling E.M., Kulangara K., Guilak F., Leong K.W. Nanotopography-induced changes in focal adhesions, cytoskeletal organization, and mechanical properties of human mesenchymal stem cells. Biomaterials 2010, 31:1299-1306.
14. Dalby M.J., Gadegaard N., Tare R., Andar A., Riehle M.O., Herzyk P., et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 2007, 6:997-1003.
15. McMurray R.J., Gadegaard N., Tsimbouri P.M., Burgess K.V., McNamara L.E., Tare R., et al. Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat Mater 2011, 10:637-644.
16. Park K.S., Cha K.J., Han I.B., Shin D.A., Cho D.W., Lee S.H., et al. Mass-producible nano-featured polystyrene surfaces for regulating the differentiation of human adipose-derived stem cells. Macromol Biosci 2012, 12:1480-1489.
17. Thomson J.A., Itskovitz-Eldor J., Shapiro S.S., Waknitz M.A., Swiergiel J.J., Marshall V.S., et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282:1145-1147.
18. Chen W., Villa-Diaz L.G., Sun Y., Weng S., Kim J.K., Lam R.H., et al. Nanotopography influences adhesion, spreading, and self-renewal of human embryonic stem cells. ACS Nano 2012, 6:4094-4103.
19. Kong Y.P., Tu C.H., Donovan P.J., Yee A.F. Expression of Oct4 in human embryonic stem cells is dependent on nanotopographical configuration. Acta Biomater 2013, 9:6369-6380.
20. Atala A. Human embryonic stem cells: early hints on safety and efficacy. Lancet 2012, 379:689-690.
21. Gerecht S., Bettinger C.J., Zhang Z., Borenstein J.T., Vunjak-Novakovic G., Langer R. The effect of actin disrupting agents on contact guidance of human embryonic stem cells. Biomaterials 2007, 28:4068-4077.
22. Lee M.R., Kwon K.W., Jung H., Kim H.N., Suh K.Y., Kim K., et al. Direct differentiation of human embryonic stem cells into selective neurons on nanoscale ridge/groove pattern arrays. Biomaterials 2010, 31:4360-4366.
23. Chan L.Y., Birch W.R., Yim E.K., Choo A.B. Temporal application of topography to increase the rate of neural differentiation from human pluripotent stem cells. Biomaterials 2013, 34:382-392.
24. Kingham E., White K., Gadegaard N., Dalby M.J., Oreffo R.O. Nanotopographical cues augment mesenchymal differentiation of human embryonic stem cells. Small 2013, 9:2140-2151.
25. Ankam S., Suryana M., Chan L.Y., Moe A.A., Teo B.K., Law J.B., et al. Substrate topography and size determine the fate of human embryonic stem cells to neuronal or glial lineage. Acta Biomater 2013, 9:4535-4545.
26. Zaraska L., Sulka G.D., Jaskula M. The effect of n-alcohols on porous anodic alumina formed by self-organized two-step anodizing of aluminum in phosphoric acid. Surf Coat Tech 2010, 204:1729-1737.
27. Zhao X., Meng G., Xu Q., Han F., Huang Q. Color fine-tuning of CNTsatAAO composite thin films via isotropically etching porous AAO before CNT growth and color modification by water infusion. Adv Mater 2010, 22:2637-2641.
28. Choi D.H., Lee P.S., Hwang W., Lee K.H., Park H.C. Measurement of the pore sizes for anodic aluminum oxide (AAO). Curr Appl Phys 2006, 6:e125-e129.
29. Xu C., Inokuma M.S., Denham J., Golds K., Kundu P., Gold J.D., et al. Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 2001, 19:971-974.
30. Xu Y., Zhu X., Hahm H.S., Wei W., Hao E., Hayek A., et al. Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci U S A 2010, 107:8129-8134.
31. Li D., Zhou J., Wang L., Shin M.E., Su P., Lei X., et al. Integrated biochemical and mechanical signals regulate multifaceted human embryonic stem cell functions. JCell Biol 2010, 191:631-644.
32. Oda H., Takeichi M. Evolution: structural and functional diversity of cadherin at the adherens junction. JCell Biol 2011, 193:1137-1146.
33. Yonemura S., Itoh M., Nagafuchi A., Tsukita S. Cell-to-cell adherens junction formation and actin filament organization: similarities and differences between non-polarized fibroblasts and polarized epithelial cells. JCell Sci 1995, 108(Pt 1):127-142.
34. Kim J.M., Moon S.H., Park S.J., Lee H.Y., Hong K.S., Seo J., et al. Pertussis toxin enhances colony organization of enzymatic-dissociated single human embryonic stem cells. Stem Cells Dev 2013, 22:307-319.
35. DeMali K.A., Burridge K. Coupling membrane protrusion and cell adhesion. JCell Sci 2003, 116:2389-2397.
36. Petit V., Thiery J.P. Focal adhesions: structure and dynamics. Biol Cell 2000, 92:477-494.
37. Ezzell R.M., Goldmann W.H., Wang N., Parashurama N., Ingber D.E. Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp Cell Res 1997, 231:14-26.
38. Ciobanasu C., Faivre B., Le Clainche C. Actin dynamics associated with focal adhesions. Int J Cell Biol 2012, 2012:941292.
39. Wakatsuki T., Wysolmerski R.B., Elson E.L. Mechanics cell spreading: role of myosin II. JCell Sci 2003, 116:1617-1625.
40. Zimerman B., Volberg T., Geiger B. Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil Cytoskelet 2004, 58:143-159.
41. Lee J.W., Lee K.B., Jeon H.S., Park H.K. Effects of surface nano-topography on human osteoblast filopodia. Anal Sci 2011, 27:369.
42. Edlund S., Landstrom M., Heldin C.H., Aspenstrom P. Transforming growth factor-beta-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol Biol Cell 2002, 13:902-914.
43. Duband J.L., Thiery J.P. Appearance and distribution of fibronectin during chick embryo gastrulation and neurulation. Dev Biol 1982, 94:337-350.
44. Hay E.D. An overview of epithelio-mesenchymal transformation. Acta Anat (Basel) 1995, 154:8-20.
45. Zeisberg M., Shah A.A., Kalluri R. Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney. JBiol Chem 2005, 280:8094-8100.
46. Wei J., Xu G., Wu M., Zhang Y., Li Q., Liu P., et al. Overexpression of vimentin contributes to prostate cancer invasion and metastasis via scr regulation. Anticancer Res 2008, 28:327-334.
47. Ullmann U., In't Veld P., Gilles C., Sermon K., De Rycke M., Van de Velde H., et al. Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions. Mol Hum Reprod 2007, 13:21-32.
48. Kim K.K., Kugler M.C., Wolters P.J., Robillard L., Galvez M.G., Brumwell A.N., et al. Alveolar epithelial cell mesenchymal transition develops invivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc Natl Acad Sci U S A 2006, 103:13180-13185.
49. Bhowmick N.A., Chiassi M., Bakin A., Aakre M., Lundquist C.A., Engel M.E., et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a Rho-A dependent mechanism. Mol Biol Cell 2001, 12:27-36.
50. Moustakas A., Heldin C.H. Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 2007, 98:1512-1520.
51. Watanabe K., Ueno M., Kamiya D., Nishiyama A., Matsumura M., Wataya T., et al. AROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat Biotechnol 2007, 25:681-686.
52. Ji L., LaPointe V.L., Evans N.D., Stevens M.M. Changes in embryonic stem cell colony morphology and early differentiation markers driven by colloidal crystal topographical cues. Eur Cell Mater 2012, 23:135-146.
53. Nagaoka M., Koshimizu U., Yuasa S., Hattori F., Chen H., Tanaka T., et al. E-cadherin-coated plates maintain pluripotent ES cells without colony formation. PLoS One 2006, 1:e15.
54. Li L., Wang B.H., Wang S., Moalim-Nour L., Mohib K., Lohnes D., et al. Individual cell movement, asymmetric colony expansion, rho-associated kinase, and E-cadherin impact the clonogenicity of human embryonic stem cells. Biophys J 2010, 98:2442-2451.
55. Ohgushi M., Matsumura M., Eiraku M., Murakami K., Aramaki T., Nishiyama A., et al. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell. 2010, 7:225-239.
56. Harb N., Archer T.K., Sato N. The Rho-Rock-Myosin signaling axis determines cell-cell integrity of self-renewing pluripotent stem cells. PLoS One 2008, 3:e3001.
57. 2 nanotube diameter directs cell fate. Nano Lett 2007, 7:1686-1691.
58. Adams C.L., Nelson W.J. Cytomechanics of cadherin-mediated cell-cell adhesion. Curr Opin Cell Biol 1998, 10:572-577.
59. Yilmaz M., Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev 2009, 28:15-33.
60. Kaibuchi K., Kuroda S., Amano M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu Rev Biochem 1999, 68:459-486.
61. Schmitz A.A., Govek E.E., Bottner B., Van Aelst L. Rho GTPases: signaling, migration, and invasion. Exp Cell Res 2000, 261:1-12.
62. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
63. Riento K., Ridley A.J. Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 2003, 4:446-456.
64. Giancotti F.G., Ruoslahti E. Integrin signaling. Science 1999, 285:1028-1032.
65. Dedhar S. Cell-substrate interactions and signaling through ILK. Curr Opin Cell Biol 2000, 12:250-256.