568
Views
19
CrossRef citations to date
0
Altmetric
Review Article

In vitro spatially organizing the differentiation in individual multicellular stem cell aggregates

, , , , , , & show all
Pages 20-31 | Received 15 Aug 2013, Accepted 21 Feb 2014, Published online: 15 Jul 2014

References

  • Abilez O, Benharash P, Mehrotra M, et al. (2006). A novel culture system shows that stem cells can be grown in 3D and under physiologic pulsatile conditions for tissue engineering of vascular grafts. J Surg Res, 132, 170–8
  • Arnold SJ, Robertson EJ. (2009). Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nature Rev Mol Cell Biol, 10, 91–103
  • Azagarsamy MA, Anseth KS. (2013). Bioorthogonal click chemistry: an indispensable tool to create multifaceted cell culture scaffolds. ACS Macro Lett, 2, 5–9
  • Azarin SM, Palecek SP. (2010). Development of scalable culture systems for human embryonic stem cells. Biochem Eng J, 48, 378
  • Baker K, Holtzman NG, Burdine RD. (2008). Direct and indirect roles for Nodal signaling in two axis conversions during asymmetric morphogenesis of the zebrafish heart. Proc Natl Acad Sci USA, 105, 13924–9
  • Barkefors I, Thorslund S, Nikolajeff F, Kreuger J. (2009). A fluidic device to study directional angiogenesis in complex tissue and organ culture models. Lab Chip, 9, 529–35
  • Bauwens CL, Peerani R, Niebruegge S, et al. (2008). Control of human embryonic stem cell colony and aggregate size heterogeneity influences differentiation trajectories. Stem Cells, 26, 2300–10
  • Beddington RS, Robertson EJ. (1998). Anterior patterning in mouse. Trends Genet, 14, 277–84
  • Bielinska M, Narita N, Wilson DB. (1999). Distinct roles for visceral endoderm during embryonic mouse development. Int J Dev Biol, 43, 183–205
  • Boland T, Xu T, Damon B, Cui X. (2006). Application of inkjet printing to tissue engineering. Biotechnol J, 1, 910–7
  • Boo JS, Yamada Y, Okazaki Y, et al. (2002). Tissue-engineered bone using mesenchymal stem cells and a biodegradable scaffold. J Craniofacial Surg, 13, 231–9
  • Bratt-Leal AM, Carpenedo RL, Mcdevitt TC. (2009). Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation. Biotechnol Prog, 25, 43–51
  • Burridge PW, Anderson D, Priddle H, et al. (2007). Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells, 25, 929–38
  • Carpenedo RL, Bratt-Leal AM, Marklein RA, et al. (2009). Homogeneous and organized differentiation within embryoid bodies induced by microsphere-mediated delivery of small molecules. Biomaterials, 30, 2507–15
  • Carpenedo RL, Sargent CY, Mcdevitt TC. (2007). Rotary suspension culture enhances the efficiency, yield, and homogeneity of embryoid body differentiation. Stem Cells, 25, 2224–34
  • Ceyhan E, Xu F, Gurkan UA, et al. (2012). Prediction and control of number of cells in microdroplets by stochastic modeling. Lab on a Chip, 12, 4884–93
  • Chen D, Zhao M, Mundy GR. (2004). Bone morphogenetic proteins. Growth Factors, 22, 233–41
  • Choi D, Lee HJ, Jee S, et al. (2005). In vitro differentiation of mouse embryonic stem cells: enrichment of endodermal cells in the embryoid body. Stem Cells, 23, 817–27
  • Choi YS, Noh SE, Lim SM, Kim DI. (2010a). Optimization of ex vivo hematopoietic stem cell expansion in intermittent dynamic cultures. Biotechnol Lett, 32, 1969–75
  • Choi YY, Chung BG, Lee DH, et al. (2010b). Controlled-size embryoid body formation in concave microwell arrays. Biomaterials, 31, 4296–303
  • Clark AT, Bodnar MS, Fox M, et al. (2004). Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum Mol Genet, 13, 727–39
  • Cormier JT, Zur Nieden NI, Rancourt DE, Kallos MS. (2006). Expansion of undifferentiated murine embryonic stem cells as aggregates in suspension culture bioreactors. Tissue Eng, 12, 3233–45
  • Dang SM, Kyba M, Perlingeiro R, et al. (2002). Efficiency of embryoid body formation and hematopoietic development from embryonic stem cells in different culture systems. Biotechnol Bioeng, 78, 442–53
  • De Bank PA, Hou Q, Warner RM, et al. (2007). Accelerated formation of multicellular 3-D structures by cell-to-cell cross-linking. Biotechnol Bioeng, 97, 1617–25
  • De Bank PA, Kellam B, Kendall DA, Shakesheff KM. (2003). Surface engineering of living myoblasts via selective periodate oxidation. Biotechnol Bioeng, 81, 800–8
  • Deforest CA, Anseth KS. (2011). Cytocompatible click-based hydrogels with dynamically tunable properties through orthogonal photoconjugation and photocleavage reactions. Nat Chem, 3, 925–31
  • Demirci U, Montesano G. (2007). Single cell epitaxy by acoustic picolitre droplets. Lab Chip, 7, 1139–45
  • Du Y, Lo E, Ali S, Khademhosseini A. (2008). Directed assembly of cell-laden microgels for fabrication of 3D tissue constructs. Proc Natl Acad Sci USA, 105, 9522–7
  • Faulkner-Jones A, Greenhough S, King JA, et al. (2013). Development of a valve-based cell printer for the formation of human embryonic stem cell spheroid aggregates. Biofabrication, 5, 015013
  • Fernandes-Platzgummer A, Diogo MM, Baptista RP, et al. (2011). Scale-up of mouse embryonic stem cell expansion in stirred bioreactors. Biotechnol Prog, 27, 1421–32
  • Fung WT, Beyzavi A, Abgrall P, et al. (2009). Microfluidic platform for controlling the differentiation of embryoid bodies. Lab Chip, 9, 2591–5
  • Gaebel R, Ma N, Liu J, et al. (2011). Patterning human stem cells and endothelial cells with laser printing for cardiac regeneration. Biomaterials, 32, 9218–30
  • Gerecht S, Burdick JA, Ferreira LS, et al. (2007). Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci USA, 104, 11298–303
  • Gomes ME, Sikavitsas VI, Behravesh E, et al. (2003). Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. J Biomed Mater Res A, 67, 87–95
  • Gothard D, Roberts SJ, Shakesheff KM, Buttery LD. (2009). Controlled embryoid body formation via surface modification and avidin-biotin cross-linking. Cytotechnology, 61, 135–44
  • Grayson WL, Bhumiratana S, Grace Chao PH, et al. (2010). Spatial regulation of human mesenchymal stem cell differentiation in engineered osteochondral constructs: effects of pre-differentiation, soluble factors and medium perfusion. Osteoarthritis Cartilage, 18, 714–23
  • Guillotin B, Souquet A, Catros S, et al. (2010). Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials, 31, 7250–6
  • Han YL, Yang Y, Liu S, et al. (2013). Directed self-assembly of microscale hydrogels by electrostatic interaction. Biofabrication, 5, 035004
  • Han YL, Hu J, Genin GM, et al. (2014). BioPen: direct writing of functional materials at the point of care. Scientific Reports, 4, 4872 doi:10.1038/srep04872
  • Huang C-C, Liao C-K, Yang M-J, et al. (2010). A strategy for fabrication of a three-dimensional tissue construct containing uniformly distributed embryoid body-derived cells as a cardiac patch. Biomaterials, 31, 6218–27
  • Huang G, Wang S, He X, et al. (2013). Helical spring template fabrication of cell-laden microfluidic hydrogels for tissue engineering. Biotechnol Bioeng, 110, 980–9
  • Huang G, Zhang X, Xiao Z, et al. (2012). Cell-encapsulating microfluidic hydrogels with enhanced mechanical stability. Soft Matter, 8, 10687–94
  • Huang GY, Zhou LH, Zhang QC, et al. (2011). Microfluidic hydrogels for tissue engineering. Biofabrication, 3, 012001
  • Hwang YS, Chung BG, Ortmann D, et al. (2009). Microwell-mediated control of embryoid body size regulates embryonic stem cell fate via differential expression of WNT5a and WNT11. Proc Natl Acad Sci USA, 106, 16978–83
  • Ishaug SL, Crane GM, Miller MJ, et al. (1997). Bone formation by three-dimensional stromal osteoblast culture in biodegradable polymer scaffolds. J Biomed Mater Res, 36, 17–28
  • Itskovitz-Eldor J, Schuldiner M, Karsenti D, et al. (2000). Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol Med, 6, 88–95
  • Izraeli S, Lowe LA, Bertness VL, et al. (1999). The SIL gene is required for mouse embryonic axial development and left-right specification. Nature, 399, 691–4
  • Jeong GS, Song JH, Kang AR, et al. (2013). Surface tension-mediated, concave-microwell arrays for large-scale, simultaneous production of homogeneously sized embryoid bodies. Adv Healthcare Mater, 2, 119–25
  • Kallos MS, Behie LA, Vescovi AL. (1999). Extended serial passaging of mammalian neural stem cells in suspension bioreactors. Biotechnol Bioeng, 65, 589–99
  • Kallos MS, Sen A, Behie LA. (2003). Large-scale expansion of mammalian neural stem cells: a review. Med Biol Eng Comput, 41, 271–82
  • Karlsson KR, Cowley S, Martinez FO, et al. (2008). Homogeneous monocytes and macrophages from human embryonic stem cells following coculture-free differentiation in M-CSF and IL-3. Exp Hematol, 36, 1167–75
  • Karp JM, Yeh J, Eng G, et al. (2007). Controlling size, shape and homogeneity of embryoid bodies using poly(ethylene glycol) microwells. Lab Chip, 7, 786–94
  • Kehoe DE, Jing D, Lock LT, Tzanakakis ES. (2010). Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. Tissue Eng Part A, 16, 405–21
  • Khademhosseini A, Ferreira L, Blumling J III, et al. (2006). Co-culture of human embryonic stem cells with murine embryonic fibroblasts on microwell-patterned substrates. Biomaterials, 27, 5968–77
  • Kim C, Lee IH, Lee K, et al. (2007). Multi-well chip for forming a uniform embryoid body in a tiny droplet with mouse embryonic stem cells. Biosci Biotechnol Biochem, 71, 2985–91
  • Kloxin AM, Kasko AM, Salinas CN, Anseth KS. (2009). Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science, 324, 59–63
  • Koch L, Kuhn S, Sorg H, et al. (2010). Laser printing of skin cells and human stem cells. Tissue Eng Part C Methods, 16, 847–54
  • Koike M, Sakaki S, Amano Y, Kurosawa H. (2007). Characterization of embryoid bodies of mouse embryonic stem cells formed under various culture conditions and estimation of differentiation status of such bodies. J Biosci Bioeng, 104, 294–9
  • Krawetz R, Taiani JT, Liu S, et al. (2010). Large-scale expansion of pluripotent human embryonic stem cells in stirred-suspension bioreactors. Tissue Eng Part C Methods, 16, 573–82
  • Kurosawa H, Imamura T, Koike M, et al. (2003). A simple method for forming embryoid body from mouse embryonic stem cells. J Biosci Bioeng, 96, 409–11
  • Kurosawa H. (2007). Methods for inducing embryoid body formation: in vitro differentiation system of embryonic stem cells. J Biosci Bioeng, 103, 389–98
  • Lee LH, Peerani R, Ungrin M, et al. (2009). Micropatterning of human embryonic stem cells dissects the mesoderm and endoderm lineages. Stem Cell Res, 2, 155–62
  • Lee PJ, Hung PJ, Lee LP. (2007). An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture. Biotechnol Bioeng, 97, 1340–6
  • Lee WG, Ortmann D, Hancock MJ, et al. (2010). A hollow sphere soft lithography approach for long-term hanging drop methods. Tissue Eng Part C Methods, 16, 249–59
  • Lenhart KF, Holtzman NG, Williams JR, Burdine RD. (2013). Integration of nodal and BMP signals in the heart requires FoxH1 to create left-right differences in cell migration rates that direct cardiac asymmetry. PLoS Genet, 9, e1003109
  • Lenhart KF, Lin SY, Titus TA, et al. (2011). Two additional midline barriers function with midline lefty1 expression to maintain asymmetric Nodal signaling during left-right axis specification in zebrafish. Development, 138, 4405–10
  • Lewis SL, Tam PP. (2006). Definitive endoderm of the mouse embryo: formation, cell fates, and morphogenetic function. Dev Dyn, 235, 2315–29
  • Lutolf MP, Lauer-Fields JL, Schmoekel HG, et al. (2003). Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc Natl Acad Sci USA, 100, 5413–8
  • Martin I, Obradovic B, Freed LE, Vunjak-Novakovic G. (1999). Method for quantitative analysis of glycosaminoglycan distribution in cultured natural and engineered cartilage. Ann Biomed Eng, 27, 656–62
  • Maurer J, Nelson B, Cecena G, et al. (2008). Contrasting expression of keratins in mouse and human embryonic stem cells. PLoS One, 3, e3451
  • Moeller HC, Mian MK, Shrivastava S, et al. (2008). A microwell array system for stem cell culture. Biomaterials, 29, 752–63
  • Mohr JC, De Pablo JJ, Palecek SP. (2006). 3-D microwell culture of human embryonic stem cells. Biomaterials, 27, 6032–42
  • Mohr JC, Zhang J, Azarin SM, et al. (2010). The microwell control of embryoid body size in order to regulate cardiac differentiation of human embryonic stem cells. Biomaterials, 31, 1885–93
  • Moon S, Hasan SK, Song YS, et al. (2010). Layer by layer three-dimensional tissue epitaxy by cell-laden hydrogel droplets. Tissue Eng Part C Methods, 16, 157–66
  • Nelson CM, Jean RP, Tan JL, et al. (2005). Emergent patterns of growth controlled by multicellular form and mechanics. Proc Natl Acad Sci USA, 102, 11594–9
  • Ng ES, Davis RP, Azzola L, et al. (2005). Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation. Blood, 106, 1601–3
  • Niebruegge S, Nehring A, Baer H, et al. (2008). Cardiomyocyte production in mass suspension culture: embryonic stem cells as a source for great amounts of functional cardiomyocytes. Tissue Eng A, 14, 1591–602
  • Novik EI, Maguire TJ, Orlova K, et al. (2006). Embryoid body-mediated differentiation of mouse embryonic stem cells along a hepatocyte lineage: insights from gene expression profiles. Tissue Eng, 12, 1515–25
  • Ong SM, Zhang C, Toh YC, et al. (2008). A gel-free 3D microfluidic cell culture system. Biomaterials, 29, 3237–44
  • Pampaloni F, Reynaud EG, Stelzer EH. (2007). The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol, 8, 839–45
  • Park J, Cho CH, Parashurama N, et al. (2007). Microfabrication-based modulation of embryonic stem cell differentiation. Lab Chip, 7, 1018–28
  • Peerani R, Rao BM, Bauwens C, et al. (2007). Niche-mediated control of human embryonic stem cell self-renewal and differentiation. EMBO J, 26, 4744–55
  • Pekkanen-Mattila M, Pelto-Huikko M, Kujala V, et al. (2010). Spatial and temporal expression pattern of germ layer markers during human embryonic stem cell differentiation in embryoid bodies. Histochem Cell Biol, 133, 595–606
  • Peter IS, Davidson EH. (2009). Genomic control of patterning. Int J Dev Biol, 53, 707–16
  • Pfister S, Steiner KA, Tam PP. (2007). Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene Expr Patterns, 7, 558–73
  • Qi H, Du Y, Wang L, et al. (2010). Patterned differentiation of individual embryoid bodies in spatially organized 3D hybrid microgels. Adv Mater, 22, 5276–81
  • Rauch F, Lauzier D, Croteau S, et al. (2000). Temporal and spatial expression of bone morphogenetic protein-2, -4, and -7 during distraction osteogenesis in rabbits. Bone, 27, 453–9
  • Reubinoff BE, Pera MF, Fong CY, et al. (2000). Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat Biotechnol, 18, 399–404
  • Rohani L, Karbalaie K, Vahdati A, et al. (2008). Embryonic stem cell sphere: a controlled method for production of mouse embryonic stem cell aggregates for differentiation. Int J Artif Organs, 31, 258–65
  • Sasaki D, Shimizu T, Masuda S, et al. (2009). Mass preparation of size-controlled mouse embryonic stem cell aggregates and induction of cardiac differentiation by cell patterning method. Biomaterials, 30, 4384–9
  • Schier AF, Talbot WS. (2005). Molecular genetics of axis formation in zebrafish. Ann Rev Genet, 39, 561–613
  • Schroeder M, Niebruegge S, Werner A, et al. (2005). Differentiation and lineage selection of mouse embryonic stem cells in a stirred bench scale bioreactor with automated process control. Biotechnol Bioeng, 92, 920–33
  • Segev H, Kenyagin-Karsenti D, Fishman B, et al. (2005). Molecular analysis of cardiomyocytes derived from human embryonic stem cells. Dev Growth Differ, 47, 295–306
  • Seiler AE, Spielmann H. (2011). The validated embryonic stem cell test to predict embryotoxicity in vitro. Nat Protoc, 6, 961–78
  • Shin Y, Han S, Jeon JS, et al. (2012). Microfluidic assay for simultaneous culture of multiple cell types on surfaces or within hydrogels. Nat Protoc, 7, 1247–59
  • Singla DK, Jayaraman S, Zhang J, Kamp TJ. (2007). Cardiomyocyte derivation from human embryonic stem cells. In: Master JR, Palsson BO, Thomson JA, eds. Human cell culture, 6. Embryonic stem cells. New York: Springer-Verlag
  • Tam PP, Beddington RS. (1992). Establishment and organization of germ layers in the gastrulating mouse embryo. Ciba Foundation Symp, 165, 27–41; discussion 42–9
  • Tam PP, Behringer RR. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech Dev, 68, 3–25
  • Tam PP, Loebel DA. (2007). Gene function in mouse embryogenesis: get set for gastrulation. Nat Rev Genet, 8, 368–81
  • Toh YC, Zhang C, Zhang J, et al. (2007). A novel 3D mammalian cell perfusion-culture system in microfluidic channels. Lab Chip, 7, 302–9
  • Torisawa YS, Chueh BH, Huh D, et al. (2007). Efficient formation of uniform-sized embryoid bodies using a compartmentalized microchannel device. Lab Chip, 7, 770–6
  • Trkov S, Eng G, Di Liddo R, et al. (2010). Micropatterned three-dimensional hydrogel system to study human endothelial-mesenchymal stem cell interactions. J Tissue Eng Regen Med, 4, 205–15
  • Ungrin MD, Joshi C, Nica A, et al. (2008). Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates. PLoS One, 3, e1565
  • Valamehr B, Jonas SJ, Polleux J, et al. (2008). Hydrophobic surfaces for enhanced differentiation of embryonic stem cell-derived embryoid bodies. Proc Natl Acad Sci USA, 105, 14459–64
  • Van Der Sanden B, Dhobb M, Berger F, Wion D. (2010). Optimizing stem cell culture. J Cell Biochem, 111, 801–7
  • Van Noort D, Ong SM, Zhang C, et al. (2009). Stem cells in microfluidics. Biotechnol Prog, 25, 52–60
  • Veerkamp J, Rudolph F, Cseresnyes Z, et al. (2013). Unilateral dampening of Bmp activity by nodal generates cardiac left-right asymmetry. Dev Cell, 24, 660–7
  • Villar G, Graham AD, Bayley H. (2013). A tissue-like printed material. Science, 340, 48–52
  • Wells JM, Melton DA. (1999). Vertebrate endoderm development. Ann Rev Cell Dev Biol, 15, 393–410
  • White DE, Kinney MA, Mcdevitt TC, Kemp ML. (2013). Spatial pattern dynamics of 3D stem cell loss of pluripotency via rules-based computational modeling. PLoS Comput Biol, 9, e1002952
  • Whitesides GM. (2006). The origins and the future of microfluidics. Nature, 442, 368–73
  • Xu F, Finley TD, Turkaydin M, et al. (2011a). The assembly of cell-encapsulating microscale hydrogels using acoustic waves. Biomaterials, 32, 7847–55
  • Xu F, Moon S, Emre A, et al. (2010). A droplet-based building block approach for bladder smooth muscle cell (SMC) proliferation. Biofabrication, 2, 014105
  • Xu F, Sridharan B, Durmus NG, et al. (2011b). Living bacterial sacrificial porogens to engineer decellularized porous scaffolds. PLoS One, 6, e19344
  • Xu F, Sridharan B, Wang SQ, et al. (2011c). Embryonic stem cell bioprinting for uniform and controlled size embryoid body formation. Biomicrofluidics, 5, 22207
  • Xu F, Wu C-AM, Rengarajan V, Finley TD, et al. (2011d). Three-dimensional magnetic assembly of microscale hydrogels. Adv Mater, 23, 4254–60
  • Xu F, Wu J, Wang S, et al. (2011e). Microengineering methods for cell-based microarrays and high-throughput drug-screening applications. Biofabrication, 3, 034101
  • Yang MJ, Chen CH, Lin PJ, et al. (2007). Novel method of forming human embryoid bodies in a polystyrene dish surface-coated with a temperature-responsive methylcellulose hydrogel. Biomacromolecules, 8, 2746–52
  • Yirme G, Amit M, Laevsky I, et al. (2008). Establishing a dynamic process for the formation, propagation, and differentiation of human embryoid bodies. Stem cells and development, 17, 1227–41
  • Youn BS, Sen A, Behie LA, et al. (2006). Scale-up of breast cancer stem cell aggregate cultures to suspension bioreactors. Biotechnol Prog, 22, 801–10
  • Zambon AC, Barker CS. (2010). Microarray analysis of embryonic stem cells and differentiated embryoid bodies. Methods Mol Biol, 632, 45–61
  • Zhang R, Mjoseng HK, Hoeve MA, et al. (2013). A thermoresponsive and chemically defined hydrogel for long-term culture of human embryonic stem cells. Nat Commun, 4, 1335
  • Zhang W, Wang S, Lin M, et al. (2012). Advances in experimental approaches for investigating cell aggregate mechanics. Acta Mech Solida Sin, 25, 473–82
  • Zhang ZY, Teoh SH, Teo EY, et al. (2010). A comparison of bioreactors for culture of fetal mesenchymal stem cells for bone tissue engineering. Biomaterials, 31, 8684–95
  • Zhao F, Ma T. (2005). Perfusion bioreactor system for human mesenchymal stem cell tissue engineering: dynamic cell seeding and construct development. Biotechnol Bioeng, 91, 482–93
  • Zhao Z, Liu Y, Yan H. (2011). Organizing DNA origami tiles into larger structures using preformed scaffold frames. Nano Lett, 11, 2997–3002

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.