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Article ; Online: Differentiation of hepatocytes from pluripotent stem cells.

Mallanna, Sunil K / Duncan, Stephen A

Current protocols in stem cell biology

2013 Volume 26, Page(s) 1G.4.1–1G.4.13

Abstract: Differentiation of human embryonic stem (ES) and induced pluripotent stem (iPS) cells into hepatocyte-like cells provides a platform to study the molecular basis of human hepatocyte differentiation, to develop cell culture models of liver disease, and to ...

Abstract	Differentiation of human embryonic stem (ES) and induced pluripotent stem (iPS) cells into hepatocyte-like cells provides a platform to study the molecular basis of human hepatocyte differentiation, to develop cell culture models of liver disease, and to potentially provide hepatocytes for treatment of end-stage liver disease. Additionally, hepatocyte-like cells generated from human pluripotent stem cells could serve as platforms for drug discovery, determination of pharmaceutical-induced hepatotoxicity, and evaluation of idiosyncratic drug-drug interactions. Here, we describe a step-wise protocol previously developed in our laboratory that facilitates the highly efficient and reproducible differentiation of human pluripotent stem cells into hepatocyte-like cells. Our protocol uses defined culture conditions and closely recapitulates key developmental events that are found to occur during hepatogenesis.
MeSH term(s)	Biomarkers/metabolism ; Cadherins/metabolism ; Cell Differentiation/drug effects ; Collagen/pharmacology ; Drug Combinations ; Hepatocytes/cytology ; Hepatocytes/drug effects ; Hepatocytes/metabolism ; Humans ; Laminin/pharmacology ; Pluripotent Stem Cells/cytology ; Pluripotent Stem Cells/drug effects ; Pluripotent Stem Cells/metabolism ; Proteoglycans/pharmacology
Chemical Substances	Biomarkers ; Cadherins ; Drug Combinations ; Laminin ; Proteoglycans ; matrigel (119978-18-6) ; Collagen (9007-34-5)
Language	English
Publishing date	2013-09-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1938-8969
ISSN (online)	1938-8969
DOI	10.1002/9780470151808.sc01g04s26
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Article ; Online: N-glycoprotein surfaceome of human induced pluripotent stem cell derived hepatic endoderm.

Mallanna, Sunil K / Waas, Matthew / Duncan, Stephen A / Gundry, Rebekah L

Proteomics

2017 Volume 17, Issue 5

Abstract: Using cell surface capture technology, the cell surface N-glycoproteome of human-induced pluripotent stem cell derived hepatic endoderm cells was assessed. Altogether, 395 cell surface N-glycoproteins were identified, represented by 1273 N-glycopeptides. ...

Abstract	Using cell surface capture technology, the cell surface N-glycoproteome of human-induced pluripotent stem cell derived hepatic endoderm cells was assessed. Altogether, 395 cell surface N-glycoproteins were identified, represented by 1273 N-glycopeptides. This study identified N-glycoproteins that are not predicted to be localized to the cell surface and provides experimental data that assist in resolving ambiguous or incorrectly annotated transmembrane topology annotations. In a proof-of-concept analysis, combining these data with other cell surface proteome datasets is useful for identifying potentially cell type and lineage restricted markers and drug targets to advance the use of stem cell technologies for mechanistic developmental studies, disease modeling, drug discovery, and regenerative medicine.
MeSH term(s)	Endoderm/cytology ; Humans ; Induced Pluripotent Stem Cells/metabolism ; Liver/embryology ; Membrane Glycoproteins/analysis ; Membrane Glycoproteins/metabolism ; Proteomics/methods
Chemical Substances	Membrane Glycoproteins
Language	English
Publishing date	2017-02-01
Publishing country	Germany
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2032093-0
ISSN	1615-9861 ; 1615-9853
ISSN (online)	1615-9861
ISSN	1615-9853
DOI	10.1002/pmic.201600397
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Article ; Online: Systems biology provides new insights into the molecular mechanisms that control the fate of embryonic stem cells.

Mallanna, Sunil K / Rizzino, Angie

Journal of cellular physiology

2011 Volume 227, Issue 1, Page(s) 27–34

Abstract: During the last 5 years there has been enormous progress in developing a deeper understanding of the molecular mechanisms that control the self-renewal and pluripotency of embryonic stem cells (ESC). Early progress resulted from studying individual ... ...

Abstract	During the last 5 years there has been enormous progress in developing a deeper understanding of the molecular mechanisms that control the self-renewal and pluripotency of embryonic stem cells (ESC). Early progress resulted from studying individual transcription factors and signaling pathways. Unexpectedly, these studies demonstrated that small changes in the levels of master regulators, such as Oct4 and Sox2, promote the differentiation of ESC. More recently, impressive progress has been made using technologies that provide a global view of the signaling pathways and the gene regulatory networks that control the fate of ESC. This review provides an overview of the progress made using several different high-throughput technologies and focuses on proteomic studies, which provide the first glimpse of the protein-protein interaction networks used by ESC. The latter studies indicate that transcription factors required for the self-renewal of ESC are part of a large, highly integrated protein-protein interaction landscape, which helps explain why the levels of master regulators need to be regulated precisely in ESC.
MeSH term(s)	Animals ; Cell Differentiation/physiology ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/physiology ; Gene Expression Regulation ; High-Throughput Screening Assays ; Humans ; Proteomics ; Systems Biology/methods
Language	English
Publishing date	2011-05-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	3116-1
ISSN	1097-4652 ; 0021-9541
ISSN (online)	1097-4652
ISSN	0021-9541
DOI	10.1002/jcp.22721
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Article ; Online: Chemically Defined Neural Conversion of Human Pluripotent Stem Cells.

Chen, Yu / Tristan, Carlos A / Mallanna, Sunil K / Ormanoglu, Pinar / Titus, Steven / Simeonov, Anton / Singeç, Ilyas

Methods in molecular biology (Clifton, N.J.)

2019 Volume 1919, Page(s) 59–72

Abstract: Human pluripotent stem cells (hPSCs) are characterized by their ability to self-renew and differentiate into any cell type of the human body. To fully utilize the potential of hPSCs for translational research and clinical applications, it is critical to ... ...

Abstract	Human pluripotent stem cells (hPSCs) are characterized by their ability to self-renew and differentiate into any cell type of the human body. To fully utilize the potential of hPSCs for translational research and clinical applications, it is critical to develop rigorous cell differentiation protocols under feeder-free conditions that are efficient, reproducible, and scalable for high-throughput projects. Focusing on neural conversion of hPSCs, here we describe robust small molecule-based procedures that generate neural stem cells (NSCs) in less than a week under chemically defined conditions. These protocols can be used to dissect the mechanisms of neural lineage entry and to further develop systematic protocols that produce the cellular diversity of the central nervous system at industrial scale.
MeSH term(s)	Animals ; Biomarkers ; Cell Culture Techniques ; Cell Differentiation/drug effects ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/drug effects ; Embryonic Stem Cells/metabolism ; Humans ; Immunohistochemistry ; Immunophenotyping ; Induced Pluripotent Stem Cells/cytology ; Induced Pluripotent Stem Cells/drug effects ; Induced Pluripotent Stem Cells/metabolism ; Mice ; Neural Stem Cells/cytology ; Neural Stem Cells/drug effects ; Neural Stem Cells/metabolism ; Pluripotent Stem Cells/cytology ; Pluripotent Stem Cells/drug effects ; Pluripotent Stem Cells/metabolism
Chemical Substances	Biomarkers
Language	English
Publishing date	2019-01-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-4939-9007-8_5
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Article ; Online: Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells.

Mallanna, Sunil K / Rizzino, Angie

Developmental biology

2010 Volume 344, Issue 1, Page(s) 16–25

Abstract: MicroRNAs (miRNAs) have emerged as critical regulators of gene expression. These small, non-coding RNAs are believed to regulate more than a third of all protein coding genes, and they have been implicated in the control of virtually all biological ... ...

Abstract	MicroRNAs (miRNAs) have emerged as critical regulators of gene expression. These small, non-coding RNAs are believed to regulate more than a third of all protein coding genes, and they have been implicated in the control of virtually all biological processes, including the biology of stem cells. The essential roles of miRNAs in the control of pluripotent stem cells were clearly established by the finding that embryonic stem (ES) cells lacking proteins required for miRNA biogenesis exhibit defects in proliferation and differentiation. Subsequently, the function of numerous miRNAs has been shown to control the fate of ES cells and to directly influence critical gene regulatory networks controlled by pluripotency factors Sox2, Oct4, and Nanog. Moreover, a growing list of tissue-specific miRNAs, which are silenced or not processed fully in ES cells, has been found to promote differentiation upon their expression and proper processing. The importance of miRNAs for ES cells is further indicated by the exciting discovery that specific miRNA mimics or miRNA inhibitors promote the reprogramming of somatic cells into induced pluripotent stem (iPS) cells. Although some progress has been made during the past two years in our understanding of the contribution of specific miRNAs during reprogramming, further progress is needed since it is highly likely that miRNAs play even wider roles in the generation of iPS cells than currently appreciated. This review examines recent developments related to the roles of miRNAs in the biology of pluripotent stem cells. In addition, we posit that more than a dozen additional miRNAs are excellent candidates for influencing the generation of iPS cells as well as for providing new insights into the process of reprogramming.
MeSH term(s)	Animals ; Body Patterning ; Cell Lineage ; Embryonic Stem Cells/cytology ; Gene Expression Regulation, Developmental ; Humans ; Mice ; MicroRNAs/genetics ; MicroRNAs/metabolism ; Models, Biological ; Pluripotent Stem Cells/cytology ; Promoter Regions, Genetic ; Proto-Oncogene Proteins c-myc/metabolism ; RNA, Untranslated/genetics ; Tumor Suppressor Protein p53/metabolism
Chemical Substances	MicroRNAs ; Proto-Oncogene Proteins c-myc ; RNA, Untranslated ; Tumor Suppressor Protein p53 ; mirnlet7 microRNA, human
Language	English
Publishing date	2010-05-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2010.05.014
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Article ; Online: Mapping the Cell-Surface N-Glycoproteome of Human Hepatocytes Reveals Markers for Selecting a Homogeneous Population of iPSC-Derived Hepatocytes.

Mallanna, Sunil K / Cayo, Max A / Twaroski, Kirk / Gundry, Rebekah L / Duncan, Stephen A

Stem cell reports

2016 Volume 7, Issue 3, Page(s) 543–556

Abstract: When comparing hepatic phenotypes between iPSC-derived hepatocyte-like cells from different liver disease patients, cell heterogeneity can confound interpretation. We proposed that homogeneous cell populations could be generated by fluorescence-activated ...

Abstract	When comparing hepatic phenotypes between iPSC-derived hepatocyte-like cells from different liver disease patients, cell heterogeneity can confound interpretation. We proposed that homogeneous cell populations could be generated by fluorescence-activated cell sorting (FACS). Using cell-surface capture proteomics, we identified a total of 300 glycoproteins on hepatocytes. Analyses of the expression profiles during the differentiation of iPSCs revealed that SLC10A1, CLRN3, and AADAC were highly enriched during the final stages of hepatocyte differentiation. FACS purification of hepatocyte-like cells expressing SLC10A1, CLRN3, or AADAC demonstrated enrichment of cells with hepatocyte characteristics. Moreover, transcriptome analyses revealed that cells expressing the liver gene regulatory network were enriched while cells expressing a pluripotent stem cell network were depleted. In conclusion, we report an extensive catalog of cell-surface N-linked glycoproteins expressed in primary hepatocytes and identify cell-surface proteins that facilitate the purification of homogeneous populations of iPSC-derived hepatocyte-like cells.
Language	English
Publishing date	2016-09-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2016.07.016
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Article ; Online: Robotic high-throughput biomanufacturing and functional differentiation of human pluripotent stem cells.

Tristan, Carlos A / Ormanoglu, Pinar / Slamecka, Jaroslav / Malley, Claire / Chu, Pei-Hsuan / Jovanovic, Vukasin M / Gedik, Yeliz / Jethmalani, Yogita / Bonney, Charles / Barnaeva, Elena / Braisted, John / Mallanna, Sunil K / Dorjsuren, Dorjbal / Iannotti, Michael J / Voss, Ty C / Michael, Sam / Simeonov, Anton / Singeç, Ilyas

Stem cell reports

2021 Volume 16, Issue 12, Page(s) 3076–3092

Abstract: Efficient translation of human induced pluripotent stem cells (hiPSCs) requires scalable cell manufacturing strategies for optimal self-renewal and functional differentiation. Traditional manual cell culture is variable and labor intensive, posing ... ...

Abstract	Efficient translation of human induced pluripotent stem cells (hiPSCs) requires scalable cell manufacturing strategies for optimal self-renewal and functional differentiation. Traditional manual cell culture is variable and labor intensive, posing challenges for high-throughput applications. Here, we established a robotic platform and automated all essential steps of hiPSC culture and differentiation under chemically defined conditions. This approach allowed rapid and standardized manufacturing of billions of hiPSCs that can be produced in parallel from up to 90 different patient- and disease-specific cell lines. Moreover, we established automated multi-lineage differentiation and generated functional neurons, cardiomyocytes, and hepatocytes. To validate our approach, we compared robotic and manual cell culture operations and performed comprehensive molecular and cellular characterizations (e.g., single-cell transcriptomics, mass cytometry, metabolism, electrophysiology) to benchmark industrial-scale cell culture operations toward building an integrated platform for efficient cell manufacturing for disease modeling, drug screening, and cell therapy.
MeSH term(s)	Automation ; Cell Culture Techniques/methods ; Cell Differentiation ; Cell Lineage ; Cells, Cultured ; Embryoid Bodies/cytology ; Hepatocytes/cytology ; Hepatocytes/virology ; Human Embryonic Stem Cells/cytology ; Humans ; Induced Pluripotent Stem Cells/cytology ; Myocytes, Cardiac/cytology ; Myocytes, Cardiac/virology ; Neurons/cytology ; RNA-Seq ; Reference Standards ; Robotics ; Single-Cell Analysis ; Zika Virus Infection/pathology
Language	English
Publishing date	2021-12-02
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, N.I.H., Intramural
ZDB-ID	2720528-9
ISSN	2213-6711 ; 2213-6711
ISSN (online)	2213-6711
ISSN	2213-6711
DOI	10.1016/j.stemcr.2021.11.004
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Article ; Online: FGF2 mediates hepatic progenitor cell formation during human pluripotent stem cell differentiation by inducing the WNT antagonist NKD1.

Twaroski, Kirk / Mallanna, Sunil K / Jing, Ran / DiFurio, Francesca / Urick, Amanda / Duncan, Stephen A

Genes & development

2015 Volume 29, Issue 23, Page(s) 2463–2474

Abstract: Fibroblast growth factors (FGFs) are required to specify hepatic fate within the definitive endoderm through activation of the FGF receptors (FGFRs). While the signaling pathways involved in hepatic specification are well understood, the mechanisms ... ...

Abstract	Fibroblast growth factors (FGFs) are required to specify hepatic fate within the definitive endoderm through activation of the FGF receptors (FGFRs). While the signaling pathways involved in hepatic specification are well understood, the mechanisms through which FGFs induce hepatic character within the endoderm are ill defined. Here we report the identification of genes whose expression is directly regulated by FGFR activity during the transition from endoderm to hepatic progenitor cell. The FGFR immediate early genes that were identified include those encoding transcription factors, growth factors, and signaling molecules. One of these immediate early genes encodes naked cuticle homolog 1 (NKD1), which is a repressor of canonical WNT (wingless-type MMTV integration site) signaling. We show that loss of NKD1 suppresses the formation of hepatic progenitor cells from human induced pluripotent stem cells and that this phenotype can be rescued by using a pharmacological antagonist of canonical WNT signaling. We conclude that FGF specifies hepatic fate at least in large part by inducing expression of NKD1 to transiently suppress the canonical WNT pathway.
MeSH term(s)	Carrier Proteins/genetics ; Carrier Proteins/metabolism ; Cell Differentiation/genetics ; Endoderm/cytology ; Fibroblast Growth Factor 2/metabolism ; Gene Expression Regulation, Developmental/genetics ; Humans ; Induced Pluripotent Stem Cells/cytology ; Liver/cytology ; Liver/embryology ; Wnt Signaling Pathway/physiology
Chemical Substances	Carrier Proteins ; NKD1 protein, human ; Fibroblast Growth Factor 2 (103107-01-3)
Language	English
Publishing date	2015-12-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	806684-x
ISSN	1549-5477 ; 0890-9369
ISSN (online)	1549-5477
ISSN	0890-9369
DOI	10.1101/gad.268961.115
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Article ; Online: Design of a Vitronectin-Based Recombinant Protein as a Defined Substrate for Differentiation of Human Pluripotent Stem Cells into Hepatocyte-Like Cells.

Nagaoka, Masato / Kobayashi, Motohiro / Kawai, Chie / Mallanna, Sunil K / Duncan, Stephen A

PloS one

2015 Volume 10, Issue 8, Page(s) e0136350

Abstract: Maintenance and differentiation of human pluripotent stem cells (hPSCs) usually requires culture on a substrate for cell adhesion. A commonly used substratum is Matrigel purified from Engelbreth-Holm-Swarm sarcoma cells, and consists of a complex mixture ...

Abstract	Maintenance and differentiation of human pluripotent stem cells (hPSCs) usually requires culture on a substrate for cell adhesion. A commonly used substratum is Matrigel purified from Engelbreth-Holm-Swarm sarcoma cells, and consists of a complex mixture of extracellular matrix proteins, proteoglycans, and growth factors. Several studies have successfully induced differentiation of hepatocyte-like cells from hPSCs. However, most of these studies have used Matrigel as a cell adhesion substrate, which is not a defined culture condition. In an attempt to generate a substratum that supports undifferentiated properties and differentiation into hepatic lineage cells, we designed novel substrates consisting of vitronectin fragments fused to the IgG Fc domain. hPSCs adhered to these substrates via interactions between integrins and the RGD (Arg-Gly-Asp) motif, and the cells maintained their undifferentiated phenotypes. Using a previously established differentiation protocol, hPSCs were efficiently differentiated into mesendodermal and hepatic lineage cells on a vitronectin fragment-containing substrate. We found that full-length vitronectin did not support stable cell adhesion during the specification stage. Furthermore, the vitronectin fragment with the minimal RGD-containing domain was sufficient for differentiation of human induced pluripotent stem cells into hepatic lineage cells under completely defined conditions that facilitate the clinical application of cells differentiated from hPSCs.
MeSH term(s)	Animals ; Blotting, Western ; Cell Adhesion ; Cell Culture Techniques ; Cell Differentiation ; Cells, Cultured ; Collagen ; Drug Combinations ; Embryonic Stem Cells/cytology ; Embryonic Stem Cells/metabolism ; Flow Cytometry ; Hepatocytes/cytology ; Hepatocytes/metabolism ; Humans ; Laminin ; Mice ; Mice, SCID ; Pluripotent Stem Cells/cytology ; Pluripotent Stem Cells/metabolism ; Proteoglycans ; RNA, Messenger/genetics ; Real-Time Polymerase Chain Reaction ; Recombinant Proteins/genetics ; Recombinant Proteins/metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Teratoma/genetics ; Teratoma/metabolism ; Teratoma/pathology ; Vitronectin/genetics ; Vitronectin/metabolism
Chemical Substances	Drug Combinations ; Laminin ; Proteoglycans ; RNA, Messenger ; Recombinant Proteins ; Vitronectin ; matrigel (119978-18-6) ; Collagen (9007-34-5)
Language	English
Publishing date	2015-08-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0136350
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Article ; Online: Mapping the Cell-Surface N-Glycoproteome of Human Hepatocytes Reveals Markers for Selecting a Homogeneous Population of iPSC-Derived Hepatocytes

Sunil K. Mallanna / Max A. Cayo / Kirk Twaroski / Rebekah L. Gundry / Stephen A. Duncan

Stem Cell Reports, Vol 7, Iss 3, Pp 543-

2016 Volume 556

Abstract	When comparing hepatic phenotypes between iPSC-derived hepatocyte-like cells from different liver disease patients, cell heterogeneity can confound interpretation. We proposed that homogeneous cell populations could be generated by fluorescence-activated cell sorting (FACS). Using cell-surface capture proteomics, we identified a total of 300 glycoproteins on hepatocytes. Analyses of the expression profiles during the differentiation of iPSCs revealed that SLC10A1, CLRN3, and AADAC were highly enriched during the final stages of hepatocyte differentiation. FACS purification of hepatocyte-like cells expressing SLC10A1, CLRN3, or AADAC demonstrated enrichment of cells with hepatocyte characteristics. Moreover, transcriptome analyses revealed that cells expressing the liver gene regulatory network were enriched while cells expressing a pluripotent stem cell network were depleted. In conclusion, we report an extensive catalog of cell-surface N-linked glycoproteins expressed in primary hepatocytes and identify cell-surface proteins that facilitate the purification of homogeneous populations of iPSC-derived hepatocyte-like cells.
Keywords	Medicine (General) ; R5-920 ; Biology (General) ; QH301-705.5
Subject code	610
Language	English
Publishing date	2016-09-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
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