Bioprocess Development for the Expansion of Embryonic Stem Cells

Megan M. Hunt1,3, Roz Alfred1,3, Derrick E. Rancourt2, Ian D. Gates3 and Michael S. Kallos1,3 1Pharmaceutical Production Research Facility (PPRF), Schulich School of Engineering, University of Calgary, Alberta 2Department of Biochemistry and Molecular Biology, Faculty of Medicine, University of Calgary, Alberta 3Department of Chemical and Petroleum Engineering, Schulich School of Engineering, University of Calgary, Alberta, Canada

[1]  Michael S Kallos,et al.  Embryonic stem cells remain highly pluripotent following long term expansion as aggregates in suspension bioreactors. , 2007, Journal of biotechnology.

[2]  A. Trounson,et al.  Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro , 2000, Nature Biotechnology.

[3]  Tiago G. Fernandes,et al.  Kinetic and metabolic analysis of mouse embryonic stem cell expansion under serum-free conditions , 2009, Biotechnology Letters.

[4]  J. Crook,et al.  Attachment and growth of human embryonic stem cells on microcarriers. , 2008, Journal of biotechnology.

[5]  Tiago G Fernandes,et al.  Mouse embryonic stem cell expansion in a microcarrier-based stirred culture system. , 2007, Journal of biotechnology.

[6]  Donghui Jing,et al.  Cardiac Cell Generation from Encapsulated Embryonic Stem Cells in Static and Scalable Culture Systems , 2010, Cell transplantation.

[7]  D. Kehoe,et al.  Scalable stirred-suspension bioreactor culture of human pluripotent stem cells. , 2010, Tissue engineering. Part A.

[8]  William Stafford Noble,et al.  Support vector machine , 2013 .

[9]  G. Martin,et al.  Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Thomson,et al.  Derivation of human embryonic stem cells in defined conditions , 2006, Nature Biotechnology.

[11]  G. Lajoie,et al.  An Enhanced Mass Spectrometry Approach Reveals Human Embryonic Stem Cell Growth Factors in Culture*S , 2009, Molecular & Cellular Proteomics.

[12]  Hossein Baharvand,et al.  Long-term maintenance of undifferentiated human embryonic and induced pluripotent stem cells in suspension. , 2011, Stem cells and development.

[13]  Oliver Brüstle,et al.  Automated maintenance of embryonic stem cell cultures , 2007, Biotechnology and bioengineering.

[14]  D. Kirouac,et al.  The systematic production of cells for cell therapies. , 2008, Cell stem cell.

[15]  M. S. Kallos,et al.  Large-scale expansion of pluripotent human embryonic stem cells in stirred-suspension bioreactors. , 2010, Tissue engineering. Part C, Methods.

[16]  Daniel I. C. Wang,et al.  Effects of paddle impeller geometry on power input and mass transfer in small‐scale animal cell culture vessels , 1989, Biotechnology and bioengineering.

[17]  D. Golde.  The stem cell. , 1991, Scientific American.

[18]  D K Robinson,et al.  Industrial choices for protein production by large-scale cell culture. , 2001, Current opinion in biotechnology.

[19]  J. Thomson,et al.  Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells , 2005, Nature Methods.

[20]  E. Kumacheva,et al.  Micropatterning of human embryonic stem cells dissects the mesoderm and endoderm lineages. , 2009, Stem cell research.

[21]  D. Kehoe,et al.  Propagation of embryonic stem cells in stirred suspension without serum , 2008, Biotechnology progress.

[22]  Joel Voldman,et al.  Fluid shear stress primes mouse embryonic stem cells for differentiation in a self‐renewing environment via heparan sulfate proteoglycans transduction , 2011, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[23]  Michael S Kallos,et al.  Expansion of mammalian neural stem cells in bioreactors: effect of power input and medium viscosity. , 2002, Brain research. Developmental brain research.

[24]  P. Daoutidis,et al.  Numerical solution of multi-variable cell population balance models. II. Spectral methods , 2001 .

[25]  W. Miller,et al.  Bioreactor development for stem cell expansion and controlled differentiation. , 2007, Current opinion in chemical biology.

[26]  Greg Lemon,et al.  Mathematical modelling of human mesenchymal stem cell proliferation and differentiation inside artificial porous scaffolds. , 2007, Journal of theoretical biology.

[27]  S. Reuveny,et al.  Investigations into the metabolism of two-dimensional colony and suspended microcarrier cultures of human embryonic stem cells in serum-free media. , 2010, Stem cells and development.

[28]  J. Audet.  Adventures in time and space: Nonlinearity and complexity of cytokine effects on stem cell fate decisions. , 2010, Biotechnology and bioengineering.

[29]  M. S. Kallos,et al.  Reduced differentiation efficiency of murine embryonic stem cells in stirred suspension bioreactors. , 2010, Stem cells and development.

[30]  G. Garcı́a-Cardeña,et al.  Directed stem cell differentiation by fluid mechanical forces. , 2011, Antioxidants & redox signaling.

[31]  F. García-Ochoa,et al.  Bioreactor scale-up and oxygen transfer rate in microbial processes: an overview. , 2009, Biotechnology advances.

[32]  S. Rehen,et al.  Successful scale-up of human embryonic stem cell production in a stirred microcarrier culture system. , 2009, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[33]  P. Itsykson,et al.  Derivation, propagation and controlled differentiation of human embryonic stem cells in suspension , 2010, Nature Biotechnology.

[34]  M. S. Kallos,et al.  Efficient suspension bioreactor expansion of murine embryonic stem cells on microcarriers in serum‐free medium , 2011, Biotechnology progress.

[35]  Shangtian Yang,et al.  A two-stage perfusion fibrous bed bioreactor system for mass production of embryonic stem cells. , 2008, Expert opinion on biological therapy.

[36]  K. Woodhouse,et al.  Control of Human Embryonic Stem Cell Colony and Aggregate Size Heterogeneity Influences Differentiation Trajectories , 2008, Stem cells.

[37]  Tsutomu Kitoh,et al.  Finite‐Difference Methods , 2002 .

[38]  M. S. Kallos,et al.  Inoculation and growth conditions for high-cell-density expansion of mammalian neural stem cells in suspension bioreactors. , 1999, Biotechnology and bioengineering.

[39]  Peter W. Zandstra,et al.  Expansion of Hematopoietic Progenitor Cell Populations in Stirred Suspension Bioreactors of Normal Human Bone Marrow Cells , 1994, Bio/Technology.

[40]  D. Largaespada,et al.  Mouse models of human disease. Part II: recent progress and future directions. , 1997, Genes & development.

[41]  Michael S Kallos,et al.  Serum‐free scaled up expansion and differentiation of murine embryonic stem cells to osteoblasts in suspension bioreactors , 2010, Biotechnology and bioengineering.

[42]  R. Cherry,et al.  Transient shear stresses on a suspension cell in turbulence , 1990, Biotechnology and bioengineering.

[43]  M. S. Kallos,et al.  Production of Islet‐Like Structures from Neonatal Porcine Pancreatic Tissue in Suspension Bioreactors , 2006, Biotechnology progress.

[44]  M. S. Kallos,et al.  Large-scale expansion of mammalian neural stem cells: a review , 2003, Medical and Biological Engineering and Computing.

[45]  T. Putti,et al.  Teratoma formation by human embryonic stem cells: evaluation of essential parameters for future safety studies. , 2009, Stem cell research.

[46]  J. Thomson,et al.  Pluripotent stem cell lines. , 2008, Genes & development.

[47]  Diane Gershon,et al.  Complex political, ethical and legal issues surround research on human embryonic stem cells. , 2003, Nature.

[48]  Yi Zhang,et al.  Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification , 2010, Nature.

[49]  Karin Schütze,et al.  Laser-assisted selection and passaging of human pluripotent stem cell colonies. , 2009, Journal of biotechnology.

[50]  J. Thomson,et al.  Basic Fibroblast Growth Factor Support of Human Embryonic Stem Cell Self‐Renewal , 2006, Stem cells.

[51]  Robert Zweigerdt,et al.  Up-scaling single cell-inoculated suspension culture of human embryonic stem cells. , 2010, Stem cell research.

[52]  N. Copeland,et al.  Mouse models of human disease. Part I: techniques and resources for genetic analysis in mice. , 1997, Genes & development.

[53]  Chris Mason,et al.  The impact of manual processing on the expansion and directed differentiation of embryonic stem cells , 2008, Biotechnology and bioengineering.

[54]  Johannes Tramper,et al.  Basic Bioreactor Design , 1991 .

[55]  M. S. Kallos,et al.  Bioreactor expansion of human neural precursor cells in serum‐free media retains neurogenic potential , 2009, Biotechnology and bioengineering.

[56]  J. Itskovitz‐Eldor,et al.  Suspension Culture of Undifferentiated Human Embryonic and Induced Pluripotent Stem Cells , 2010, Stem Cell Reviews and Reports.

[57]  C. Galbán,et al.  Analysis of cell growth kinetics and substrate diffusion in a polymer scaffold. , 1999, Biotechnology and bioengineering.

[58]  L. Lock,et al.  Expansion and differentiation of human embryonic stem cells to endoderm progeny in a microcarrier stirred-suspension culture. , 2009, Tissue engineering. Part A.

[59]  Peter W Zandstra,et al.  Shear‐Controlled Single‐Step Mouse Embryonic Stem Cell Expansion and Embryoid Body–Based Differentiation , 2005, Stem cells.

[60]  Joaquim M S Cabral,et al.  Expansion of mouse embryonic stem cells on microcarriers , 2007, Biotechnology and bioengineering.

[61]  J. Chaudhuri,et al.  Three-dimensional culture systems for the expansion of pluripotent embryonic stem cells , 2010, Biotechnology and bioengineering.

[62]  F. Schmidt.  Optimization and scale up of industrial fermentation processes , 2005, Applied Microbiology and Biotechnology.

[63]  J. Clemente,et al.  Improving expansion of pluripotent human embryonic stem cells in perfused bioreactors through oxygen control. , 2010, Journal of biotechnology.

[64]  M. Kaufman,et al.  Establishment in culture of pluripotential cells from mouse embryos , 1981, Nature.

[65]  Thomas Scheper,et al.  Long term expansion of undifferentiated human iPS and ES cells in suspension culture using a defined medium. , 2010, Stem cell research.

[66]  Colin N. Dewey,et al.  Initial sequencing and comparative analysis of the mouse genome. , 2002 .

[67]  S. Reuveny,et al.  Agitation can induce differentiation of human pluripotent stem cells in microcarrier cultures. , 2011, Tissue engineering. Part C, Methods.

[68]  Peter W Zandstra,et al.  Niche‐mediated control of human embryonic stem cell self‐renewal and differentiation , 2007, The EMBO journal.

[69]  Wendy A. Prudhomme,et al.  Cell population dynamics model for deconvolution of murine embryonic stem cell self‐renewal and differentiation responses to cytokines and extracellular matrix , 2004, Biotechnology and bioengineering.

[70]  E. Papoutsakis,et al.  Fluid-mechanical damage of animal cells in bioreactors. , 1991, Trends in biotechnology.

[71]  J. R. Sharpe,et al.  Microcarriers and their potential in tissue regeneration. , 2011, Tissue engineering. Part B, Reviews.

[72]  S. Reuveny,et al.  Long-term microcarrier suspension cultures of human embryonic stem cells. , 2009, Stem cell research.

[73]  Michael C. Borys,et al.  Formation of bridges and large cellular clumps in CHO-cell microcarrier cultures: Effects of agitation dimethyl sulfoxide and calf serum , 2006, Cytotechnology.

[74]  Shangtian Yang,et al.  A two-stage perfusion fibrous bed bioreactor system for mass production of embryonic stem cells , 2008, Expert opinion on biological therapy.

[75]  Maintenance of pluripotency in mouse embryonic stem cells cultivated in stirred microcarrier cultures , 2009, Biotechnology progress.

[76]  Michael S Kallos,et al.  Scaled‐up production of mammalian neural precursor cell aggregates in computer‐controlled suspension bioreactors , 2006, Biotechnology and bioengineering.

[77]  S. Ratnam,et al.  Isolation and culture of inner cell mass cells from human blastocysts. , 1994, Human reproduction.

[78]  Steve Oh,et al.  High density cultures of embryonic stem cells. , 2005, Biotechnology and bioengineering.

[79]  G. I. Obrams,et al.  Clinical and Translational Science Awards , 2009 .

[80]  John A. Williams,et al.  Keys to bioreactor selections , 2002 .

[81]  S. Palecek,et al.  Scalable culture and cryopreservation of human embryonic stem cells on microcarriers , 2009, Biotechnology progress.

[82]  Bülent Yener,et al.  Multiway modeling and analysis in stem cell systems biology , 2008, BMC Systems Biology.

[83]  Eugenia Kumacheva,et al.  Generation of human embryonic stem cell‐derived mesoderm and cardiac cells using size‐specified aggregates in an oxygen‐controlled bioreactor , 2009, Biotechnology and bioengineering.

[84]  S. Nishikawa,et al.  A ROCK inhibitor permits survival of dissociated human embryonic stem cells , 2007, Nature Biotechnology.

[85]  C A Chung,et al.  Analysis of cell growth and diffusion in a scaffold for cartilage tissue engineering , 2006, Biotechnology and bioengineering.

[86]  J. Crook,et al.  Efficient expansion of clinical-grade human fibroblasts on microcarriers: cells suitable for ex vivo expansion of clinical-grade hESCs. , 2008, Journal of biotechnology.

[87]  R. Nerem,et al.  Fluid shear stress promotes an endothelial-like phenotype during the early differentiation of embryonic stem cells. , 2010, Tissue engineering. Part A.

[88]  David J. Williams,et al.  Automated, scalable culture of human embryonic stem cells in feeder‐free conditions , 2009, Biotechnology and bioengineering.

[89]  Caroline M. Jakuba,et al.  Single-cell transcript analysis of human embryonic stem cells. , 2009, Integrative biology : quantitative biosciences from nano to macro.

[90]  Herbert Schulz,et al.  Neural Differentiation of Embryonic Stem Cells In Vitro: A Road Map to Neurogenesis in the Embryo , 2009, PloS one.

[91]  Andre Terzic,et al.  Stem Cell Platforms for Regenerative Medicine , 2009, Clinical and translational science.

[92]  J. Thomson,et al.  Isolation of a primate embryonic stem cell line. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Karim Mukhida,et al.  Expansion of Human Neural Precursor Cells in Large‐Scale Bioreactors for the Treatment of Neurodegenerative Disorders , 2008, Biotechnology progress.

[94]  Michael S Kallos,et al.  Expansion of undifferentiated murine embryonic stem cells as aggregates in suspension culture bioreactors. , 2006, Tissue engineering.

[95]  J. Thomson,et al.  Embryonic stem cell lines derived from human blastocysts. , 1998, Science.

[96]  Steve Oh,et al.  Identification of proteins from feeder conditioned medium that support human embryonic stem cells. , 2007, Journal of biotechnology.