Advertisement

Microenvironmental Control of Stem Cell Fate

  • Andrew J. PutnamEmail author
Chapter

Abstract

The field of regenerative medicine has witnessed impressive advances over the past 25–30 years, moving us ever closer to the goal of translating engineered tissue constructs into human patients. However, despite an exponentially expanding literature documenting advances in biomaterials and stem cell biology, generating tissues that function equivalently to the native tissues they are intended to replace remains an enormous challenge. Translating stem cell-based therapies from the bench to the bedside requires a better understanding of the mechanisms by which stem cell fate decisions are controlled. Extrinsic factors in the cellular microenvironment, particularly the extracellular matrix (ECM), include chemical, mechanical, and topographic cues, which in turn alter cell adhesion, cell shape, and cell migration, and activate signal transduction pathways to influence gene expression, proliferation, and differentiation. This chapter focuses on the links between the ECM microenvironment and the control of cell fate. The concept of the stem cell niche is also highlighted, along with evidence that the proximity of stem cells to the microvasculature may be instructive. Finally, the impact of these findings for the design and clinical utility of biomaterials for cardiac regenerative medicine is discussed.

Keywords

Stem Cell Niche Cell Fate Decision Migration Speed Cellular Microenvironment Urethane Acrylate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Ahn EH, Kim Y, Kshitiz et al (2014) Spatial control of adult stem cell fate using nanotopographic cues. Biomaterials 35:2401–2410Google Scholar
  2. Anderson DG, Levenberg S, Langer R (2004) Nanoliter-scale synthesis of arrayed biomaterials and application to human embryonic stem cells. Nat Biotechnol 22:863–866Google Scholar
  3. Andreu-Agullo C, Morante-Redolat JM, Delgado AC, Farinas I (2009) Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci 12:1514–1523Google Scholar
  4. Assmus B, Schachinger V, Teupe C et al (2002) Transplantation of progenitor cells and regeneration enhancement in acute myocardial infarction (TOPCARE-AMI). Circulation 106:3009–3017Google Scholar
  5. Beckermann BM, Kallifatidis G, Groth A et al (2008) VEGF expression by mesenchymal stem cells contributes to angiogenesis in pancreatic carcinoma. Br J Cancer 99:622–631Google Scholar
  6. Bernard A, Delamarche E, Schmid H et al (1998) Printing patterns of proteins. Langmuir 14:2225–2229Google Scholar
  7. Biela SA, Su Y, Spatz JP, Kemkemer R (2009) Different sensitivity of human endothelial cells, smooth muscle cells and fibroblasts to topography in the nano-micro range. Acta Biomater 5:2460–2466Google Scholar
  8. Blocki A, Wang Y, Koch M et al (2013) Not all MSCs can act as pericytes: functional in vitro assays to distinguish pericytes from other mesenchymal stem cells in angiogenesis. Stem Cells Dev 22:2347–2355Google Scholar
  9. Brammer KS, Oh S, Gallagher JO, Jin S (2008) Enhanced cellular mobility guided by TiO2 nanotube surfaces. Nano Lett 8:786–793Google Scholar
  10. Brockes JR, Kumar A (2002) Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat Rev Mol Cell Biol 3:566–574Google Scholar
  11. Butler JM, Kobayashi H, Rafii S (2010a) Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer 10:138–146Google Scholar
  12. Butler JM, Nolan DJ, Vertes EL et al (2010b) Endothelial cells are essential for the self-renewal and repopulation of Notch-dependent hematopoietic stem cells. Cell Stem Cell 6:251–264Google Scholar
  13. Calvi LM, Adams GB, Weibrecht KW et al (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425:841–846Google Scholar
  14. Caplan AI (2008) All MSCs are pericytes? Cell Stem Cell 3:229–230Google Scholar
  15. Carreira BP, Morte MI, Inacio A et al (2010) Nitric oxide stimulates the proliferation of neural stem cells bypassing the epidermal growth factor receptor. Stem Cells 28:1219–1230Google Scholar
  16. Carrion B, Kong YP, Kaigler D, Putnam AJ (2013) Bone marrow-derived mesenchymal stem cells enhance angiogenesis via their alpha6beta1 integrin receptor. Exp Cell Res 319:2964–2976Google Scholar
  17. Charest JL, Eliason MT, Garcia AJ, King WP (2006) Combined microscale mechanical topography and chemical patterns on polymer cell culture substrates. Biomaterials 27:2487–2494Google Scholar
  18. Chen W, Villa-Diaz LG, Sun Y et al (2012) Nanotopography influences adhesion, spreading, and self-renewal of human embryonic stem cells. ACS Nano 6:4094–4103Google Scholar
  19. Chien KR (2004) Stem cells: lost in translation. Nature 428:607–608Google Scholar
  20. Choi J, Costa ML, Mermelstein CS et al (1990) MyoD converts primary dermal fibroblasts, chondroblasts, smooth-muscle, and retinal pigmented epithelial-cells into striated mononucleated myoblasts and mutinucleated myotubes. Proc Natl Acad Sci U S A 87:7988–7992Google Scholar
  21. Choi SJ, Kim HN, Bae WG, Suh KY (2011) Modulus- and surface energy-tunable ultraviolet-curable polyurethane acrylate: properties and applications. J Mater Chem 21:14325–14335Google Scholar
  22. Choi SJ, Yoo PJ, Baek SJ, Kim TW, Lee HH (2004) An ultraviolet-curable mold for sub-100-nm lithography. J Am Chem Soc 126:7744–7745Google Scholar
  23. Chong JJ, Yang X, Don CW et al (2014) Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510:273–277Google Scholar
  24. Crisan M, Yap S, Casteilla L et al (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3:301–313Google Scholar
  25. Curtis ASG, Casey B, Gallagher JO et al (2001) Substratum nanotopography and the adhesion of biological cells. Are symmetry or regularity of nanotopography important? Biophys Chem 94:275–283Google Scholar
  26. Da Silva Meirelles L, Fontes AM, Covas DT, Caplan AI (2009) Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 20:419–427Google Scholar
  27. Dalby MJ, Gadegaard N, Tare R et al (2007) The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 6:997–1003Google Scholar
  28. Dalby MJ, Mccloy D, Robertson M et al (2006a) Osteoprogenitor response to semi-ordered and random nanotopographies. Biomaterials 27:2980–2987Google Scholar
  29. Dalby MJ, Mccloy D, Robertson M, Wilkinson CD, Oreffo RO (2006b) Osteoprogenitor response to defined topographies with nanoscale depths. Biomaterials 27:1306–1315Google Scholar
  30. Dalby MJ, Riehle MO, Johnstone H, Affrossman S, Curtis AS (2002a) In vitro reaction of endothelial cells to polymer demixed nanotopography. Biomaterials 23:2945–2954Google Scholar
  31. Dalby MJ, Riehle MO, Johnstone HJ, Affrossman S, Curtis AS (2002b) Polymer-demixed nanotopography: control of fibroblast spreading and proliferation. Tissue Eng 8:1099–1108Google Scholar
  32. Dalby MJ, Yarwood SJ, Riehle MO et al (2002c) Increasing fibroblast response to materials using nanotopography: morphological and genetic measurements of cell response to 13-nm-high polymer demixed islands. Exp Cell Res 276:1–9Google Scholar
  33. Dewitt ND, Trounson A (2012) Direct conversion in the heart: a simple twist of fate. EMBO J 31:2244–2246Google Scholar
  34. Diehl KA, Foley JD, Nealey PF, Murphy CJ (2005) Nanoscale topography modulates corneal epithelial cell migration. J Biomed Mater Res A 75:603–611Google Scholar
  35. Ding L, Saunders TL, Enikolopov G, Morrison SJ (2012) Endothelial and perivascular cells maintain haematopoietic stem cells. Nature 481:457–462Google Scholar
  36. Dingal PC, Discher DE (2014) Combining insoluble and soluble factors to steer stem cell fate. Nat Mater 13:532–537Google Scholar
  37. Discher DE, Mooney DJ, Zandstra PW (2009) Growth factors, matrices, and forces combine and control stem cells. Science 324:1673–1677Google Scholar
  38. Doorn J, Moll G, Le Blanc K, Van Blitterswijk C, De Boer J (2011) Therapeutic applications of mesenchymal stromal cells: paracrine effects and potential improvements. Tissue Eng Part B Rev 18:101–115Google Scholar
  39. Doyle AD, Wang FW, Matsumoto K, Yamada KM (2009) One-dimensional topography underlies three-dimensional fibrillar cell migration. J Cell Biol 184:481–490Google Scholar
  40. Efe JA, Hilcove S, Kim J et al (2011) Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol 13:215–222Google Scholar
  41. Engler AJ, Carag-Krieger C, Johnson CP et al (2008) Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J Cell Sci 121:3794–3802Google Scholar
  42. Engler AJ, Griffin MA, Sen S et al (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166:877–887Google Scholar
  43. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677–689Google Scholar
  44. Ferreira LS, Gerecht S, Fuller J et al (2007) Bioactive hydrogel scaffolds for controllable vascular differentiation of human embryonic stem cells. Biomaterials 28:2706–2717Google Scholar
  45. Ghajar CM, Chen X, Harris JW et al (2008) The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J 94:1930–1941Google Scholar
  46. Goldman SA, Chen Z (2011) Perivascular instruction of cell genesis and fate in the adult brain. Nat Neurosci 14:1382–1389Google Scholar
  47. Gurdon JB, Uehlinger V (1966) “Fertile” intestine nuclei. Nature 210:1240–1241Google Scholar
  48. Hadland BK, Huppert SS, Kanungo J et al (2004) A requirement for Notch1 distinguishes 2 phases of definitive hematopoiesis during development. Blood 104:3097–3105Google Scholar
  49. Huang XD, Bao LR, Cheng X et al (2002) Reversal imprinting by transferring polymer from mold to substrate. J Vac Sci Technol B 20:2872–2876Google Scholar
  50. Huebsch N, Arany PR, Mao AS et al (2010) Harnessing traction-mediated manipulation of the cell/matrix interface to control stem-cell fate. Nat Mater 9:518–526Google Scholar
  51. Hwang NS, Varghese S, Elisseeff J (2008) Controlled differentiation of stem cells. Adv Drug Deliv Rev 60:199–214Google Scholar
  52. Ieda M, Fu JD, Delgado-Olguin P et al (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142:375–386Google Scholar
  53. Jacot JG, Mcculloch AD, Omens JH (2008) Substrate stiffness affects the functional maturation of neonatal rat ventricular myocytes. Biophys J 95:3479–3487Google Scholar
  54. Jain R, Von Recum AF (2003) Effect of titanium surface texture on the cell-biomaterial interface. J Investig Surg 16:263–273Google Scholar
  55. Janson IA, Kong YP, Putnam AJ (2014) Nanotopographic substrates of poly(Methyl Methacrylate) do not strongly influence the osteogenic phenotype of mesenchymal stem cells in vitro. PLoS One 9:e90719Google Scholar
  56. Jopling C, Sleep E, Raya M et al (2010) Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464:606–U168Google Scholar
  57. Kaigler D, Krebsbach PH, West ER et al (2005) Endothelial cell modulation of bone marrow stromal cell osteogenic potential. FASEB J 19:665Google Scholar
  58. Kajstura J, Rota M, Whang B et al (2005) Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ Res 96:127–137Google Scholar
  59. Karuri NW, Liliensiek S, Teixeira AI et al (2004) Biological length scale topography enhances cell-substratum adhesion of human corneal epithelial cells. J Cell Sci 117:3153–3164Google Scholar
  60. Khatiwala CB, Peyton SR, Metzke M, Putnam AJ (2007) The regulation of osteogenesis by ECM rigidity in MC3T3-E1 cells requires MAPK activation. J Cell Physiol 211:661–672Google Scholar
  61. Khatiwala CB, Peyton SR, Putnam AJ (2006) Intrinsic mechanical properties of the extracellular matrix affect the behavior of pre-osteoblastic MC3T3-E1 cells. Am J Physiol Cell Physiol 290:C1640–C1650Google Scholar
  62. Khetan S, Guvendiren M, Legant WR et al (2013) Degradation-mediated cellular traction directs stem cell fate in covalently crosslinked three-dimensional hydrogels. Nat Mater 12:458–465Google Scholar
  63. Kiel MJ, Morrison SJ (2008) Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 8:290–301Google Scholar
  64. Kikuchi K, Holdway JE, Werdich AA et al (2010) Primary contribution to zebrafish heart regeneration by gata4(+) cardiomyocytes. Nature 464:601–U162Google Scholar
  65. Kim DH, Han K, Gupta K et al (2009) Mechanosensitivity of fibroblast cell shape and movement to anisotropic substratum topography gradients. Biomaterials 30:5433–5444Google Scholar
  66. Kim DH, Lipke EA, Kim P et al (2010) Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs. Proc Natl Acad Sci U S A 107:565–570Google Scholar
  67. Kim DH, Provenzano PP, Smith CL, Levchenko A (2012) Matrix nanotopography as a regulator of cell function. J Cell Biol 197:351–360Google Scholar
  68. Kim J, Kim HN, Lim KT et al (2013) Synergistic effects of nanotopography and co-culture with endothelial cells on osteogenesis of mesenchymal stem cells. Biomaterials 34:7257–7268MathSciNetGoogle Scholar
  69. Kocher AA, Schuster MD, Szabolcs MJ et al (2001) Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7:430–436Google Scholar
  70. Kokovay E, Li L, Cunningham LA (2005) Angiogenic recruitment of pericytes from bone marrow after stroke. J Cereb Blood Flow Metab 26:545–555Google Scholar
  71. Kolf CM, Cho E, Tuan RS (2007) Mesenchymal stromal cells. Biology of adult mesenchymal stem cells: regulation of niche, self-renewal and differentiation. Arthritis Res Ther 9:204Google Scholar
  72. Kong YP, Carrion B, Singh RK, Putnam AJ (2013a) Matrix identity and tractional forces influence indirect cardiac reprogramming. Sci Rep 3:3474Google Scholar
  73. Kong YP, Tu CH, Donovan PJ, Yee AF (2013b) Expression of Oct4 in human embryonic stem cells is dependent on nanotopographical configuration. Acta Biomater 9:6369–6380Google Scholar
  74. Laflamme MA, Chen KY, Naumova AV et al (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25:1015–1024Google Scholar
  75. Laflamme MA, Murry CE (2011) Heart regeneration. Nature 473:326–335Google Scholar
  76. Lamers E, Walboomers XF, Domanski M et al (2010) The influence of nanoscale grooved substrates on osteoblast behavior and extracellular matrix deposition. Biomaterials 31:3307–3316Google Scholar
  77. Lapointe VL, Fernandes AT, Bell NC, Stellacci F, Stevens MM (2013) Nanoscale topography and chemistry affect embryonic stem cell self-renewal and early differentiation. Adv Healthc Mater 2:1644–1650Google Scholar
  78. Lepilina A, Coon AN, Kikuchi K et al (2006) A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration. Cell 127:607–619Google Scholar
  79. Leventhal C, Rafii S, Rafii D, Shahar A, Goldman SA (1999) Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 13:450–464Google Scholar
  80. Limbourg FP, Drexler H (2005) Bone marrow stem cells for myocardial infarction: effector or mediator? Circ Res 96:6–8Google Scholar
  81. Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79:144–152Google Scholar
  82. Lu D, Luo C, Zhang C, Li Z, Long M (2014) Differential regulation of morphology and stemness of mouse embryonic stem cells by substrate stiffness and topography. Biomaterials 35:3945–3955Google Scholar
  83. Lutolf MP, Gilbert PM, Blau HM (2009) Designing materials to direct stem-cell fate. Nature 462:433–441Google Scholar
  84. Mathieu C, Sii-Felice K, Fouchet P et al (2008) Endothelial cell-derived bone morphogenetic proteins control proliferation of neural stem/progenitor cells. Mol Cell Neurosci 38:569–577Google Scholar
  85. Mcbeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483–495Google Scholar
  86. Mcmurray RJ, Gadegaard N, Tsimbouri PM et al (2011) Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat Mater 10:637–644Google Scholar
  87. Mello AP, Volkov Y, Kelleher D, Prendergast PJ (2003) Comparative locomotory behavior of T lymphocytes versus T lymphoma cells on flat and grooved surfaces. Ann Biomed Eng 31:1106–1113Google Scholar
  88. Mrksich M, Chen CS, Xia YN et al (1996) Controlling cell attachment on contoured surfaces with self-assembled monolayers of alkanethiolates on gold. Proc Natl Acad Sci U S A 93:10775–10778Google Scholar
  89. Murry CE, Kay MA, Bartosek T, Hauschka SD, Schwartz SM (1996) Muscle differentiation during repair of myocardial necrosis in rats via gene transfer with MyoD. J Clin Invest 98:2209–2217Google Scholar
  90. Nagaya N, Fujii T, Iwase T et al (2004) Intravenous administration of mesenchymal stem cells improves cardiac function in rats with acute myocardial infarction through angiogenesis and myogenesis. Am J Physiol Heart Circ Physiol 287:H2670–H2676Google Scholar
  91. Nagaya N, Kangawa K, Itoh T et al (2005) Transplantation of mesenchymal stem cells improves cardiac function in a rat model of dilated cardiomyopathy. Circulation 112:1128–1135Google Scholar
  92. Oh S, Brammer KS, Li YS et al (2009) Stem cell fate dictated solely by altered nanotube dimension. Proc Natl Acad Sci U S A 106:2130–2135Google Scholar
  93. Ott HC, Matthiesen TS, Goh SK et al (2008) Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med 14:213–221Google Scholar
  94. Packer MA, Stasiv Y, Benraiss A et al (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci U S A 100:9566–9571Google Scholar
  95. Pelham RJ, Wang YL (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc Natl Acad Sci U S A 94:13661–13665Google Scholar
  96. Peyton SR, Putnam AJ (2005) Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol 204:198–209Google Scholar
  97. Peyton SR, Raub CB, Keschrumrus VP, Putnam AJ (2006) The use of poly(ethylene glycol) hydrogels to investigate the impact of ECM chemistry and mechanics on smooth muscle cells. Biomaterials 27:4881–4893Google Scholar
  98. Pompe T, Glorius S, Bischoff T et al (2009) Dissecting the impact of matrix anchorage and elasticity in cell adhesion. Biophys J 97:2154–2163Google Scholar
  99. Porrello ER, Mahmoud AI, Simpson E et al (2011) Transient regenerative potential of the neonatal mouse heart. Science 331:1078–1080Google Scholar
  100. Poss KD, Wilson LG, Keating MT (2002) Heart regeneration in zebrafish. Science 298:2188–2190Google Scholar
  101. Poulos MG, Guo P, Kofler NM et al (2013) Endothelial Jagged-1 is necessary for homeostatic and regenerative hematopoiesis. Cell Rep 4:1022–1034Google Scholar
  102. Qian L, Huang Y, Spencer CI et al (2012) In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 485:593–598Google Scholar
  103. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C et al (2006) Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9:331–339Google Scholar
  104. Ranucci CS, Moghe PV (2001) Substrate microtopography can enhance cell adhesive and migratory responsiveness to matrix ligand density. J Biomed Mater Res 54:149–161Google Scholar
  105. Ross AM, Jiang ZX, Bastmeyer M, Lahann J (2012) Physical aspects of cell culture substrates: topography, roughness, and elasticity. Small 8:336–355Google Scholar
  106. Saha K, Keung AJ, Irwin EF et al (2008) Substrate modulus directs neural stem cell behavior. Biophys J 95:4426–4438Google Scholar
  107. Schofield R (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4:7–25Google Scholar
  108. Shen Q, Goderie SK, Jin L et al (2004) Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340Google Scholar
  109. Shen Q, Wang Y, Kokovay E et al (2008) Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 3:289–300Google Scholar
  110. Silva GV, Litovsky S, Assad JA et al (2005) Mesenchymal stem cells differentiate into an endothelial phenotype, enhance vascular density, and improve heart function in a canine chronic ischemia model. Circulation 111:150–156Google Scholar
  111. Song K, Nam YJ, Luo X et al (2012) Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 485:599–604Google Scholar
  112. Stevens KR, Kreutziger KL, Dupras SK et al (2009) Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 106:16568–16573Google Scholar
  113. Suh KY, Park MC, Kim P (2009) Capillary force lithography: a versatile tool for structured biomaterials interface towards cell and tissue engineering. Adv Funct Mater 19:2699–2712Google Scholar
  114. Takahashi K, Tanabe K, Ohnuki M et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872Google Scholar
  115. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676Google Scholar
  116. Tan J, Saltzman WM (2002) Topographical control of human neutrophil motility on micropatterned materials with various surface chemistry. Biomaterials 23:3215–3225Google Scholar
  117. Tanaka EM (2003) Cell differentiation and cell fate during urodele tail and limb regeneration. Curr Opin Genet Dev 13:497–501Google Scholar
  118. Tavazoie M, Van Der Veken L, Silva-Vargas V et al (2008) A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279–288Google Scholar
  119. Teixeira AI, Abrams GA, Bertics PJ, Murphy CJ, Nealey PF (2003) Epithelial contact guidance on well-defined micro- and nanostructured substrates. J Cell Sci 116:1881–1892Google Scholar
  120. Teixeira AI, Nealey PF, Murphy CJ (2004) Responses of human keratocytes to micro- and nanostructured substrates. J Biomed Mater Res A 71:369–376Google Scholar
  121. Trappmann B, Gautrot JE, Connelly JT et al (2012) Extracellular-matrix tethering regulates stem-cell fate. Nat Mater 11:642–649Google Scholar
  122. Unadkat HV, Hulsman M, Cornelissen K et al (2011) An algorithm-based topographical biomaterials library to instruct cell fate. Proc Natl Acad Sci U S A 108:16565–16570Google Scholar
  123. Vazin T, Schaffer DV (2009) Engineering strategies to emulate the stem cell niche. Trends Biotechnol 28:117Google Scholar
  124. Vazin T, Schaffer DV (2010) Engineering strategies to emulate the stem cell niche. Trends Biotechnol 28:117–124Google Scholar
  125. Vierbuchen T, Ostermeier A, Pang ZP et al (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463:1035–1041Google Scholar
  126. Vunjak-Novakovic G, Tandon N, Godier A et al (2010) Challenges in cardiac tissue engineering. Tissue Eng B Rev 16:169–187Google Scholar
  127. Watari S, Hayashi K, Wood JA et al (2012) Modulation of osteogenic differentiation in hMSCs cells by submicron topographically-patterned ridges and grooves. Biomaterials 33:128–136Google Scholar
  128. Webster TJ, Ergun C, Doremus RH, Siegel RW, Bizios R (2000) Enhanced functions of osteoblasts on nanophase ceramics. Biomaterials 21:1803–1810Google Scholar
  129. Winkler IG, Barbier V, Nowlan B et al (2012) Vascular niche E-selectin regulates hematopoietic stem cell dormancy, self renewal and chemoresistance. Nat Med 18:1651–1657Google Scholar
  130. Wong JY, Velasco A, Rajagopalan P, Pham Q (2003) Directed movement of vascular smooth muscle cells on gradient-compliant hydrogels. Langmuir 19:1908–1913Google Scholar
  131. Xie HF, Ye M, Feng R, Graf T (2004) Stepwise reprogramming of B cells into macrophages. Cell 117:663–676Google Scholar
  132. Xu H, Yi BA, Chien KR (2011) Shortcuts to making cardiomyocytes. Nat Cell Biol 13:191–193Google Scholar
  133. Yamada KM, Cukierman E (2007) Modeling tissue morphogenesis and cancer in 3D. Cell 130:601–610Google Scholar
  134. Yim EK, Reano RM, Pang SW et al (2005) Nanopattern-induced changes in morphology and motility of smooth muscle cells. Biomaterials 26:5405–5413Google Scholar
  135. You MH, Kwak MK, Kim DH et al (2010) Synergistically enhanced osteogenic differentiation of human mesenchymal stem cells by culture on nanostructured surfaces with induction media. Biomacromolecules 11:1856–1862Google Scholar
  136. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA (2008) In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455:627–U30Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringUniversity of MichiganAnn ArborUSA

Personalised recommendations