A High-Efficiency System for the Generation and Study of Human Induced Pluripotent Stem Cells
Open accessAbstract
Direct reprogramming of human fibroblasts to a pluripotent state has been achieved through ectopic expression of the transcription factors OCT4, SOX2, and either cMYC and KLF4 or NANOG and LIN28. Little is known, however, about the mechanisms by which reprogramming occurs, which is in part limited by the low efficiency of conversion. To this end, we sought to create a doxycycline-inducible lentiviral system to convert primary human fibroblasts and keratinocytes into human induced pluripotent stem cells (hiPSCs). hiPSCs generated with this system were molecularly and functionally similar to human embryonic stem cells (hESCs), demonstrated by gene expression profiles, DNA methylation status, and differentiation potential. While expression of the viral transgenes was required for several weeks in fibroblasts, we found that 10 days was sufficient for the reprogramming of keratinocytes. Using our inducible system, we developed a strategy to induce hiPSC formation at high frequency. Upon addition of doxycycline to hiPSC-derived differentiated cells, we obtained "secondary" hiPSCs at a frequency at least 100-fold greater than the initial conversion. The ability to reprogram cells at high efficiency provides a unique platform to dissect the underlying molecular and biochemical processes that accompany nuclear reprogramming.
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Several studies have suggested an unanticipated level of cellular plasticity within epidermal keratinocytes, resulting in cell-fate flexibility during wound repair.
“Several studies have suggested an unanticipated level of cellular plasticity within epidermal keratinocytes, resulting in cell‐fate flexibility during wound repair.[ 8 , 9 , 10 , 11 , 12 ]”
From Sweat Gland Organoids Originating from Reprogrammed Epidermal Keratinocytes Functionally Recapitulated Damaged Skin (2021) · cites this paper as [11]
The Discussion reports that neonatal foreskin keratinocytes were experimentally reprogrammed to a pluripotent state, supporting cellular fate flexibility under induced conditions. It does not address keratinocyte fate changes during wound repair, so it cannot support that setting-specific part of the claim. Our copy provides section labels but no page numbers. (LLM, conf=0.88)
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Cites
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Epigenetic memory in induced pluripotent stem cells
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“Keratinocytes reprogram more readily than fibroblasts 9 , and iPSC from stomach or liver cells harbor fewer integrated proviruses than fibroblasts, suggesting they require lower levels of the reprogramming factors to achieve pluripotency 10 .”
BackgroundInduced pluripotent stem cells generated without viral integration
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“Reprogramming of mouse and human somatic cells to a pluripotent state has been achieved by viral transduction of four transcription factors, OCT4, KLF4, SOX2, and c-MYC (Aasen et al., 2008; Dimos et al., 2008; Hockemeyer et al., 2008; Lowry et al., 2008; Maherali et al., 2008; Nakagawa et al., 2008; Okita et al., 2007…”
BackgroundPluripotent stem cells induced from mouse somatic cells by small-molecule compounds.
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Self-citationThe promise of induced pluripotent stem cells in research and therapy
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Immortalization eliminates a roadblock during cellular reprogramming into iPS cells
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“Using microarray expression data sets of human fibroblasts and ES cells (Lowry et al., 2008; Maherali et al., 2008), we found that silent genes were extensively targeted by the O, S, K, and M factors at 48 hr, which is in contrast to that seen in ES cells (Chen et al., 2008; Sridharan et al.,…”
Induced pluripotency: history, mechanisms, and applicationsPreprint
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“These systems entail differentiating ‘‘primary’’ iPSC clones, generated with doxycyline-inducible lentiviral vectors or transposons, into genetically homogeneous somatic cells using either in vitro differentiation (for human cells) (Hockemeyer et al. 2008; Maherali et al. 2008) or blastocyst injection (for mice) (Wern…”
BackgroundInfluentialSelf-citationAberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells
Stadtfeld, M., Apostolou, E., Akutsu, H., Fukuda, A., Follett, P., Natesan, S., Kono, T., Shioda, T., & Hochedlinger, K. (2010) · Nature · doi:10.1038/nature09017 · Cited by 801 · see citing works
“It remains to be tested, however, (1) if other consistent expression changes exist in iPSCs that are not detectable in the undifferentiated state or with current profiling technology; (2) whether iPSC-specific non-recurrent genetic and epigenetic aberrations are present in only some clones; and (3) if iPSCs derived fr…”
Self-citationReprogramming of Human Primary Somatic Cells by OCT4 and Chemical Compounds
Zhu, S.-Y., Li, W., Zhou, H.-Y., Wei, W.-G., Ambasudhan, R., Lin, T.-X., Kim, J., Zhang, K., & Ding, S. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.11.015 · Cited by 676 · see citing works
“Keratinocytes also endogenously express KLF4 and cMYC, and can be reprogrammed efficiently using the conventional four TFs or three TFs (without cMYC) (Aasen et al., 2008; Maherali et al., 2008).”
BackgroundZheng, X., Boyer, L., Jin, M., Mertens, J., Kim, Y., Ma, L., Ma, L., Hamm, M., Gage, F. H., & Hunter, T. (2016) · eLife · doi:10.7554/elife.13374 · Cited by 671 · see citing works
“The inducible c-MYC (T58A, a mutation stabilizing c-MYC) lentivirus expression vectors, FUdeltaGW-rtTA (#19780) and FU-tet-o-hc-MYC (#19775) were developed by Maherali et al. (2008) and obtained from Addg- ene.”
MethodSenescence impairs successful reprogramming to pluripotent stem cells
Banito, A., Rashid, S. T., Acosta, J. C., Li, S., Pereira, C. F., Geti, I., Pinho, S., Silva, J. C., Azuara, V., Walsh, M., et al. (2009) · Genes & Development · doi:10.1101/gad.1811609 · Cited by 642 · see citing works
“(Maherali et al., 2008).”
BackgroundEpigenetic reprogramming and induced pluripotency
Hochedlinger, K., & Plath, K. (2009) · Development · doi:10.1242/dev.020867 · Cited by 606 · see citing works
“When mouse or human fibroblasts derived from such iPS cells were treated with doxycycline, between 3-5% of the cells gave rise to iPS cells (Hockemeyer et al., 2008; Maherali et al., 2008; Wernig et al., 2008a) (Table 1).”
BackgroundMethodInfluentialSelf-citationIncomplete DNA methylation underlies a transcriptional memory of the somatic cell in human iPS cells
Ohi, Y., Qin, H., Hong, C., Blouin, L., Polo, J., Guo, T.-X., Qi, Z.-X., Downey, S. L., Manos, P. D., Rossi, D. J., et al. (2011) · Nature Cell Biology · doi:10.1038/ncb2239 · Cited by 604 · see citing works
“RESULTS Generation of human iPS cells from somatic cells representative of all three embryonic germ layers We used a doxycycline-inducible lentivirus transgene syste”
Self-citationWang, S., Bates, J., Li, X., Schanz, S., Chandler-Militello, D., Levine, C., Maherali, N., Studer, L., Hochedlinger, K., Windrem, M., et al. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2012.12.002 · Cited by 586 · see citing works
“We used four different iPSC lines from three different sources for this study; these included WA09/H9 hESCs (Thomson et al., 1998); keratinocyte-derived K04 hiPSCs (Maherali et al., 2008); and fibroblast-derived C14 and C27 hiPSCs (Chambers et al., 2009).”
MethodSelf-citationLong-term self-renewal of human pluripotent stem cells on human recombinant laminin-511
Rodin, S., Domogatskaya, A., Ström, S., Hansson, E., Chien, K., Inzunza, J., Hovatta, O., & Tryggvason, K. (2010) · Nature Biotechnology · doi:10.1038/nbt.1620 · Cited by 569 · see citing works
Elite and stochastic models for induced pluripotent stem cell generation
Yamanaka, S. (2009) · Nature · doi:10.1038/nature08180 · Cited by 551 · see citing works
Live cell imaging distinguishes bona fide human iPS cells from partially reprogrammed cells
Chan, E., Ratanasirintrawoot, S., Park, I.-H., Manos, P. D., Loh, Y., Huo, H.-G., Miller, J. D., Hartung, O., Rho, J., Ince, T., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1580 · Cited by 529 · see citing works
“We first studied reprogramming of human ES cell–derived fibroblasts, which, like mouse embryonic fibroblasts (MEFs), can be reprogrammed at a relatively high efficienc”
BackgroundGeneration of induced pluripotent stem cells from human cord blood.
Haase, A., Olmer, R., Schwanke, K., Wunderlich, S., Merkert, S., Hess, C., Zweigerdt, R., Gruh, I., Meyer, J., Wagner, S., et al. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.08.021 · Cited by 520 · see citing works
“This efficiency is similar to that previously found after the lentiviral transduction of fibroblasts and keratinocytes (Maherali et al., 2008).”
ResultDeng, J., Shoemaker, R., Xie, B., Gore, A., Leproust, E., Antosiewicz-Bourget, J. E., Egli, D., Maherali, N., Park, I.-H., Yu, J.-Y., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1530 · Cited by 520 · see citing works
“reprogrammed with a different set of factors (Oct4, Sox2, Klf4 and Myc); BJ/BJ-iPS11/BJ-iPS12 (ref”
Self-citationGuidelines and techniques for the generation of induced pluripotent stem cells.
Maherali, N., & Hochedlinger, K. (2008) · Cell Stem Cell · doi:10.1016/j.stem.2008.11.008 · Cited by 508 · see citing works
“…cells (Aoi et al., 2008; Stadtfeld et al., 2008c), pancreatic b cells (Stadtfeld et al., 2008a), lymphocytes (Hanna et al., 2008), and neural progenitor cells (Eminli et al., 2008; Kim et al., 2008), as well as human keratinocytes (Aasen et al., 2008; Maherali et al., 2008), have been reprogrammed.”
BackgroundInfluentialSelf-citationRole of TAZ as Mediator of Wnt Signaling
Azzolin, L., Zanconato, F., Bresolin, S., Forcato, M., Basso, G., Bicciato, S., Cordenonsi, M., & Piccolo, S. (2012) · Cell · doi:10.1016/j.cell.2012.11.027 · Cited by 490 · see citing works
UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells
Zhang, J., Khvorostov, I., Hong, J. S., Oktay, Y., Vergnes, L., Nuebel, E., Wahjudi, P., Setoguchi, K., Wang, G.-Y., Do, A., et al. (2011) · EMBO Journal · doi:10.15252/embj.201694054 · Cited by 489
“Two studies compared gene expression be- tween hPSCs and fibroblasts (Lowry et al, 2008; Maherali et al, 2008) and a third study evaluated gene expression with hESC differentiation to embryoid bodies (EBs) and cardio- myocytes (Cao et al, 2008).”
ResultGuenther, M. G., Frampton, G. M., Soldner, F., Hockemeyer, D., Mitalipova, M., Jaenisch, R., & Young, R. A. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.06.015 · Cited by 456 · see citing works
“Human ESC and iPSC Expression Data Clusters More by Laboratory than by ESC/iPSC Identity Gene expression data sets for human ESCs, iPSCs, and fibroblast cells from four laboratories (Guenther et al., present study; Maherali et al., 2008; Chin et al., 2009; Yu et al., 2009) were quantile normalized as one group.”
MethodResultDifferentiation stage determines reprogramming potential of hematopoietic cells into iPS cells
Eminli, S., Foudi, A., Stadtfeld, M., Maherali, N., Ahfeldt, T., Mostoslavsky, G., Hock, H., & Hochedlinger, K. (2009) · Nature Genetics · doi:10.1038/ng.428 · Cited by 421 · see citing works
“Exposure of these cells to doxycycline then results in the re-expression of the factors and the generation of 'secondary' iPS cell”
BackgroundSelf-citationTechnical Challenges in Using Human Induced Pluripotent Stem Cells to Model Disease
Saha, K., & Jaenisch, R. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.11.009 · Cited by 411 · see citing works
“In amyotrophic lateral sclerosis (ALS) for example, cocultures of wild-type, hESC-derived motor neurons with mutant ALS astrocytes induced motor neuron death (Di Giorgio et al., 2008; Marchetto et al., 2008).”
BackgroundInduced pluripotent stem cells: current progress and potential for regenerative medicine.
Amabile, G., & Meissner, A. (2009) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.12.003 · Cited by 408 · see citing works
Current Challenges of iPSC-Based Disease Modeling and Therapeutic Implications
Doss, M., & Sachinidis, A. (2019) · Cells · doi:10.3390/cells8050403 · Cited by 395 · see citing works
Singh, V. K., Kalsan, M., Kumar, N., Saini, A., & Chandra, R. (2015) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2015.00002 · Cited by 421 · see citing works
Generation of iPSCs from mouse fibroblasts with a single gene, Oct4, and small molecules
Li, Y., Zhang, Q., Yin, X., Yang, W., Du, Y.-Y., Hou, P.-P., Ge, J., Liu, C., Zhang, W.-Q., Zhang, X., et al. (2011) · Cell Research · doi:10.1038/cr.2010.142 · Cited by 381 · see citing works
Tgfβ Signal Inhibition Cooperates in the Induction of iPSCs and Replaces Sox2 and cMyc
Maherali, N., & Hochedlinger, K. (2009) · Current Biology · doi:10.1016/j.cub.2009.08.025 · Cited by 348 · see citing works
Self-citationUtikal, J., Maherali, N., Kulalert, W., & Hochedlinger, K. (2009) · Journal of Cell Science · doi:10.1242/jcs.054783 · Cited by 348 · see citing works
“Oct4 and Nanog promoter sequences were as previously described for mouse (Eminli et al., 2008) and human (Maherali et al., 2008).”
BackgroundResultInfluentialSelf-citationBioengineering human myocardium on native extracellular matrix
Guyette, J. P., Charest, J. M., Mills, R. W., Jank, B. J., Moser, P. T., Gilpin, S. E., Gershlak, J. R., Okamoto, T., Gonzalez, G., Milan, D. J., et al. (2016) · Circulation Research · doi:10.1161/circresaha.115.306874 · Cited by 343 · see citing works
“Primary antibody dilutions were made with blocking buffer, as follows: 1:50 anti-laminin G1 (cat#: sc-13144; Santa Cruz Biotechnology, Dallas, TX), 1:50 anti-elastin (cat#: sc-58756; Santa Cruz Biotechnology), 1:50 anti-fibronectin (cat#: sc-59826; Santa Cruz Biotechnology), 1:100 anti-collagen I (cat#: ab6308; Abcam,…”
Blin, G., Nury, D., Stefanovic, S., Néri, T., Guillevic, O., Brinon, B., Bellamy, V., Rücker-Martin, C., Barbry, P., Bel, A., et al. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40120 · Cited by 342 · see citing works
“The HUESC lines (HUES-24 and HUES-9 pOct4/GFP from Harvard Stem cell Center) and one human iPS cell line generated using human dermal fibroblasts infected by lentivirus harbouring the cDNAs encoding Oct4, Sox2, Lin 28, Klf4 and nanog (58), were used throughout this study without any difference in results.”
MethodSelf-citationProgress toward the clinical application of patient-specific pluripotent stem cells
Kiskinis, E., & Eggan, K. (2010) · Journal of Clinical Investigation · doi:10.1172/jci40553 · Cited by 339 · see citing works
Ruiz, S., Panopoulos, A. D., Herrerías, A., Bissig, K., Lutz, M. K., Berggren, W. T., Verma, I., & Belmonte, J. C. I. (2010) · Current Biology · doi:10.1016/j.cub.2010.11.049 · Cited by 328 · see citing works
“It has been shown that reactivation of endogenous pluripotent gene expression is a necessary and early event for successful reprogramming [14].”
BackgroundGonzãlez, F., Monasterio, M. B., Tiscornia, G., Pulido, N. M., Vassena, R., Batlle-Morera, L., Rodriguez-Piza, I., & Belmonte, J. C. (2009) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0901471106 · Cited by 324 · see citing works
“Reprogramming requires the delivery of all of the factors to the cell and their adequate expression for a period of !8–12 days for fibroblasts and keratinocytes (13, 19, 20).”
Induction of Pluripotency in Mouse Somatic Cells with Lineage Specifiers
Shu, J., Wu, C., Wu, Y., Li, Z., Shao, S., Zhao, W., Tang, X., Yang, H., Shen, L.-J., Zuo, X.-H., et al. (2013) · Cell · doi:10.1016/j.cell.2013.05.001 · Cited by 315 · see citing works
“Accordingly, the reprogramming factors that induce pluripotency have been identified primarily from embryonic stem cell (ESC)-enriched factors, pluripotency-associated factors, or maternal factors such as Oct4, Sox2, Klf4, c-Myc, Nanog, PRDM14, Sall4, Esrrb, Utf1, Tet2, and Glis1 (Aoi et al., 2008; Buganim et al., 201…”
BackgroundMethodInfluentialInduced Pluripotent Stem Cells and Their Use in Human Models of Disease and Development
Karagiannis, P., Takahashi, K., Saito, M. K., Yoshida, Y., Okita, K., Watanabe, A., Inoue, H., Yamashita, J. K., Todani, M., Nakagawa, M., et al. (2018) · Physiological Reviews · doi:10.1152/physrev.00039.2017 · Cited by 367 · see citing works
Progress in understanding reprogramming to the induced pluripotent state
Plath, K., & Lowry, W. (2011) · Nature reviews genetics · doi:10.1038/nrg2955 · Cited by 306 · see citing works
SWI/SNF as mechanoregulated inhibitor of YAP/TAZ
Chang, L., Azzolin, L., di Biagio, D., Zanconato, F., Battilana, G., Xiccato, R. L., Aragona, M., Giulitti, S., Panciera, T., Gandin, A., et al. (2018) · Nature · doi:10.1038/s41586-018-0658-1 · Cited by 291 · see citing works
Papapetrou, E. P., Tomishima, M. J., Chambers, S. M., Mica, Y., Reed, E., Menon, J., Tabar, V., Mo, Q., Studer, L., & Sadelain, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904825106 · Cited by 286 · see citing works
“This finding is consistent with the notion that successfully reprogrammed cells become independent of ectopic expression of the RFs and rely on endogenous factor expression (5, 20, 21, 27).”
MethodResultFanning, S., Haque, A., Imberdis, T., Baru, V., Barrasa, M. I., Nuber, S., Termine, D., Ramalingam, N., Ho, G. P. H., Noble, T., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2018.11.028 · Cited by 285 · see citing works
Cell-free and cell-based approaches for bone regeneration
Bueno, E., & Glowacki, J. (2009) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2009.228 · Cited by 285 · see citing works
YAP/TAZ link cell mechanics to Notch signalling to control epidermal stem cell fate
Totaro, A., Castellan, M., Battilana, G., Zanconato, F., Azzolin, L., Giulitti, S., Cordenonsi, M., & Piccolo, S. (2017) · Nature Communications · doi:10.1038/ncomms15206 · Cited by 294 · see citing works
THE CELL CYCLE AND MYC INTERSECT WITH MECHANISMS FOR PLURIPOTENCY AND REPROGRAMMING
Singh, A. M., & Dalton, S. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2009.07.003 · Cited by 276 · see citing works
A comparison of genetically matched cell lines reveals the equivalence of human iPSCs and ESCs
Choi, J., Lee, S., Clement, K., Mallard, W., Tagliazucchi, G., Lim, H., Choi, I.-Y., Ferrari, F., Tsankov, A. M., Pop, R., et al. (2015) · Nature Biotechnology · doi:10.1038/nbt.3388 · Cited by 268 · see citing works
Self-citationMouse liver repopulation with hepatocytes generated from human fibroblasts
Zhu, S.-Y., Rezvani, M., Harbell, J., Mattis, A. N., Wolfe, A., Benet, L., Willenbring, H., & Ding, S. (2014) · Nature · doi:10.1038/nature13020 · Cited by 266 · see citing works
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Ji, Z., & Tian, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008419 · Cited by 264 · see citing works
“, and 4 data sets of human iPS cells derived from neonatal foreskin fibroblasts and fetal lung fibroblasts”
BackgroundLin, M., Pedrosa, E., Shah, A., Hrabovsky, A., Maqbool, S., Zheng, D.-Y., & Lachman, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023356 · Cited by 262 · see citing works
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“Dermal fibroblasts cultured from skin punch biopsy were reprogrammed to iPSCs using lentiviruses expressing human Oct4, Sox2, Klf4, c-Myc and Nano”
MethodA reprogrammable mouse strain from gene targeted embryonic stem cells
Stadtfeld, M., Maherali, N., Borkent, M., & Hochedlinger, K. (2009) · Nature Methods · doi:10.1038/nmeth.1409 · Cited by 254 · see citing works
Self-citationProgramming human pluripotent stem cells into white and brown adipocytes
Ahfeldt, T., Schinzel, R., Lee, Y.-K., Hendrickson, D. G., Kaplan, A., Lum, D. H., Camahort, R., Xia, F., Shay, J., Rhee, E., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2411 · Cited by 250 · see citing works
Self-citationA XEN-like State Bridges Somatic Cells to Pluripotency during Chemical Reprogramming.
Zhao, Y., Zhao, T., Guan, J.-Y., Zhang, X., Fu, Y., Ye, J., Zhu, J., Meng, G., Ge, J., Yang, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.11.017 · Cited by 249 · see citing works
Generation of mouse-induced pluripotent stem cells with plasmid vectors
Okita, K., Hong, H., Takahashi, K., & Yamanaka, S. (2010) · Nature Protocols · doi:10.1038/nprot.2009.231 · Cited by 242 · see citing works
“For example, the induction efficiency of iPS cells from human fibroblasts is very low and requires longer expression periods of reprogramming factors than mouse fibroblast”
BackgroundBuecker, C., Chen, H.-H., Polo, J., Daheron, L., Bu, L., Barakat, T. S., Okwieka, P., Porter, A., Gribnau, J., Hochedlinger, K., et al. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.05.003 · Cited by 236 · see citing works
“Doxycycline-inducible lentiviral vectors were added either as individual vectors (Maherali et al., 2008) or the polycystronic human STEMCCA virus (Sommer et al., 2009) and inducible NANOG as indicated in the text.”
BackgroundMethodResultInfluentialSelf-citationLab-Specific Gene Expression Signatures in Pluripotent Stem Cells
Newman, A. M., & Cooper, J. B. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.06.016 · Cited by 217 · see citing works
“(2007) and Park et al. (2008) data sets are clearly distinguished from the other data sets by genes composing cluster 4.”
BackgroundPanciera, T., Azzolin, L., Fujimura, A., di Biagio, D., Frasson, C., Bresolin, S., Soligo, S. M., Basso, G., Bicciato, S., Rosato, A., et al. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.08.009 · Cited by 228 · see citing works
“For Cre-excisable expression of rtTA, we used LV-CMV-rtTA-LoxP (Figures S4L-N), obtained by substituting the Cre cDNA in LV-CMV-Cre-LoxP with the cDNA of rtTA from FUdeltaGW-rtTA (Addgene #19780(Maherali et al., 2008)).”
MethodDental Pulp Cells for Induced Pluripotent Stem Cell Banking
Tamaoki, N., Takahashi, K., Tanaka, T., Ichisaka, T., Aoki, H., Takeda-Kawaguchi, T., Iida, K., Kunisada, T., Shibata, T., Yamanaka, S., et al. (2010) · Journal of dentistry research · doi:10.1177/0022034510366846 · Cited by 215 · see citing works
“Previous reports suggested that the endogenous expression of reprogramming factors affects the reprogramming efficiency and the requirement for these factors (Aasen et al., 2008; Eminli et al., 2008; Kim et al., 2008; Maherali et al., 2008).”
BackgroundA single-gene transgenic mouse strain for reprogramming adult somatic cells
Carey, B. W., Markoulaki, S., Beard, C., Hanna, J., & Jaenisch, R. (2009) · Nature Methods · doi:10.1038/nmeth.1410 · Cited by 215 · see citing works
Expansion and patterning of cardiovascular progenitors derived from human pluripotent stem cells
Birket, M., Ribeiro, M. C., Verkerk, A., Ward, D., Leitoguinho, A. R. C., den Hartogh, S. D., Orlova, V., Devalla, H., Schwach, V., Bellin, M., et al. (2015) · Nature Biotechnology · doi:10.1038/nbt.3271 · Cited by 205 · see citing works
Historical origins of transdifferentiation and reprogramming
Graf, T. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2011.11.012 · Cited by 194 · see citing works
Pluripotency can be rapidly and efficiently induced in human amniotic fluid-derived cells.
Li, C.-L., Zhou, J.-M., Shi, G., Ma, Y., Yang, Y., Gu, J.-J., Yu, H.-Y., Jin, S.-B., Wei, Z., Chen, F., et al. (2009) · Human Molecular Genetics · doi:10.1093/hmg/ddp386 · Cited by 186 · see citing works
“human fibroblasts to pluripotency requires several weeks (24), although Aasen et al.”
BackgroundClone- and Gene-Specific Aberrations of Parental Imprinting in Human Induced Pluripotent Stem Cells
Pick, M., Stelzer, Y., Bar‐Nur, O., Mayshar, Y., Eden, A., & Benvenisty, N. (2009) · Stem Cells · doi:10.1002/stem.205 · Cited by 183 · see citing works
Omole, A. E., & Fakoya, A. O. J. (2018) · PeerJ · doi:10.7717/peerj.4370 · Cited by 207 · see citing works
“, 2009) and keratinocytes (Maherali et al., 2008), demonstrating the universality of cellular reprogramming.”
BackgroundSox2 Is an Androgen Receptor-Repressed Gene That Promotes Castration-Resistant Prostate Cancer
Kregel, S., Kiriluk, K. J., Rosen, A. M., Cai, Y., Reyes, E. E., Otto, K. B., Tom, W. R., Paner, G., Szmulewitz, R., & Griend, D. V. V. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053701 · Cited by 177 · see citing works
Golipour, A., David, L., Liu, Y., Jayakumaran, G., Hirsch, C. L., Trcka, D., & Wrana, J. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.11.008 · Cited by 175 · see citing works
“These primary iPSCs are then differentiated either in vivo, via the generation of chimeric mice, or in vitro, via the differentiation of primary iPSCs (Maherali et al., 2008; Woltjen et al., 2009).”
BackgroundA Zebrafish Embryo Culture System Defines Factors that Promote Vertebrate Myogenesis across Species
Xu, C., Tabebordbar, M., Iovino, S., Ciarlo, C., Liu, J.-X., Castiglioni, A., Price, E. N., Liu, M., Barton, E. R., Kahn, C. R., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.023 · Cited by 168 · see citing works
“BJ-iPSCs (Maherali et al., 2008) were obtained from Chad Cowan (Harvard Stem Cell Institute).”
Molecular analyses of human induced pluripotent stem cells and embryonic stem cells
Chin, M. H., Pellegrini, M., Plath, K., & Lowry, W. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.06.019 · Cited by 163 · see citing works
“It has since been shown that lentivirus is suitable for delivering the reprogramming factors (Brambrink et al., 2008; Maherali et al., 2008; Stadtfeld et al., 2008), and newer methods use polycistronic vectors to deliver all four reprogramming factors in one virus and were shown to be very effective at generating hiPS…”
BackgroundMethodAnguera, M. C., Sadreyev, R. I., Zhang, Z.-Q., Szántó, A., Payer, B., Sheridan, S., Kwok, S.-M., Haggarty, S., Sur, M., Alvarez, J., et al. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2012.03.008 · Cited by 160 · see citing works
“These ‘‘human induced pluripotent stem cells’’ (hiPSCs) share similar gene expression profiles, morphologies, and differentiation potential with hESCs (Wernig et al., 2007; Maherali et al., 2008), and mouse-derived iPSCs can be passaged through the germline (Okita et al.”
InfluentialMetabolic control of primed human pluripotent stem cell fate and function by the miR-200c–SIRT2 axis
Cha, Y., Han, M.-J., Cha, H.-J., Zoldan, J., Burkart, A. M., Jung, J., Jang, Y.-W., Kim, C.-H., Jeong, H.-C., Kim, B.-G., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3517 · Cited by 157 · see citing works
Induced Pluripotent Stem Cells from Individuals with Recessive Dystrophic Epidermolysis Bullosa
Tolar, J., Xia, L., Riddle, M. J., Lees, C. J., Eide, C. R., McElmurry, R. T., Titeux, M., Osborn, M. J., Lund, T. C., Hovnanian, A., et al. (2011) · Journal of Investigative Dermatology · doi:10.1038/jid.2010.346 · Cited by 155 · see citing works
“These reprogramming factors are believed to activate a network of transcriptional factors, which in turn induce epigenetic changes (Freberg et al., 2007; Aasen et al., 2008; Okita et al., 2008; Maherali et al., 2008a; Park et al., 2008a).”
BackgroundInfluentialAddis, R., Hsu, F., Wright, R., Dichter, M., Coulter, D., & Gearhart, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028719 · Cited by 155 · see citing works
“Astrocytes were transduced with FUdeltaGW-rtTA (the reverse tetracycline transactivator,”
MethodYücel, G., Zhao, Z.-H., El-Battrawy, I., Lan, H., Lang, S., Li, X., Buljubasic, F., Zimmermann, W., Cyganek, L., Utikal, J., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-03147-4 · Cited by 154 · see citing works
Self-citationChristoforou, N., Chellappan, M. K., Adler, A. F., Kirkton, R., Wu, T.-Y., Addis, R., Bursac, N., & Leong, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063577 · Cited by 153 · see citing works
Gillis, A., Stoop, H. A., Biermann, K., van Gurp, R. V., Swartzman, E., Cribbes, S., Ferlinz, A., Shannon, M., Oosterhuis, J., & Looijenga, L. (2011) · International Journal of Andrology · doi:10.1111/j.1365-2605.2011.01148.x · Cited by 149 · see citing works
A blueprint for engineering cell fate: current technologies to reprogram cell identity
Morris, S. A., & Daley, G. Q. (2013) · Cell Research · doi:10.1038/cr.2013.1 · Cited by 129 · see citing works
The quantitative proteomes of human-induced pluripotent stem cells and embryonic stem cells
Muñoz, J., Low, T., Kok, Y., Chin, A., Frese, C., Ding, V., Choo, A., & Heck, A. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.84 · Cited by 137 · see citing works
“The comparisons showed some genes in common with the differential transcripts published by Yu et al (2007): 12/58 (e.g., CDH2, TFRC, RRM2 ACAT1, CAPG, SDR39U1) and by Maherali et al (2008): 10/58 (e.g., DCXR, RCN3, CDH2, SLC38A2, ACOX1, HSPA2).”
Kuzmenkin, A., Liang, H.-M., Xu, G., Pfannkuche, K., Eichhorn, H., Fatima, A., Luo, H.-Y., Šarić, T., Wernig, M., Jaenisch, R., et al. (2009) · The FASEB Journal · doi:10.1096/fj.08-128546 · Cited by 136 · see citing works
VLDLR and ApoER2 are receptors for multiple alphaviruses
Clark, L., Clark, S., Lin, C., Liu, J., Coscia, A., Nabel, K., Yang, P., Neel, D. V., Lee, H., Brusic, V., et al. (2021) · Nature · doi:10.1038/s41586-021-04326-0 · Cited by 129 · see citing works
Engineering of human pluripotent stem cells by AAV-mediated gene targeting.
Khan, I., Hirata, R., Wang, P.-R., Li, Y., Kho, J., Nelson, A. M., Huo, Y., Zavaljevski, M., Ware, C., & Russell, D. (2010) · Molecular Therapy · doi:10.1038/mt.2010.55 · Cited by 126 · see citing works
David, L., & Polo, J. (2014) · Stem Cell Research · doi:10.1016/j.scr.2014.03.007 · Cited by 125 · see citing works
“To overcome this, secondary systems were implemented, and the resultant transgenic fibroblast could be reprogrammed through inducible expression of Oct4, Klf4, Myc and Sox2 (OKMS) (Carey et al., 2010; Maherali et al., 2008; Nagy, 2013; Stadtfeld et al., 2010; Woltjen et al., 2009).”
MethodDevelopment of Patient-Specific Neurons in Schizophrenia Using Induced Pluripotent Stem Cells
Pedrosa, E., Sandler, V. M., Shah, A., Carroll, R. C., Chang, C.-J., Rockowitz, S., Guo, X., Zheng, D., & Lachman, H. M. (2011) · Journal of Neurogenetics · doi:10.3109/01677063.2011.597908 · Cited by 129 · see citing works
“…and Rett syndrome, and most recently, SZ (Brennand et al., 2011; Chiang et al., 2011; Dimos et al., 2008; Ku et al., 2010; G. Lee et al., 2009; Maherali et al., 2008; Marchetto et al., 2010a, 2010b; Nizzardo et al., 2010; Swistowski et al., 2010; Takahashi et al., 2007; Wernig et al., 2008).”
BackgroundHoganson, D. M., O'Doherty, E., Owens, G. E., Harilal, D., Goldman, S., Bowley, C. M., Neville, C. M., Kronengold, R., & Vacanti, J. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.05.019 · Cited by 123 · see citing works
Stefanovic, S., Abboud, N., Désilets, S., Nury, D., Cowan, C., & Pucéat, M. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200901040 · Cited by 118
“Two HUES cell lines and one HUiPS cell line 11(Maherali et al., 2008) , using human dermal fibroblasts infected by lentivirus harbouring the cDNAs encoding Oct4, Sox2, Lin 28, Klf4 and Nanog, were used throughout this study without any difference in results.”
MethodSelf-citationKLF4-dependent epigenetic remodeling modulates podocyte phenotypes and attenuates proteinuria.
Hayashi, K., Sasamura, H., Nakamura, M., Azegami, T., Oguchi, H., Sakamaki, Y., & Itoh, H. (2014) · Journal of Clinical Investigation · doi:10.1172/jci69557 · Cited by 117 · see citing works
Functional Myogenic Engraftment from Mouse iPS Cells
Darabi, R., Pan, W., Bosnakovski, D., Baik, J., Kyba, M., & Perlingeiro, R. C. R. (2011) · Stem Cell Reviews and Reports · doi:10.1007/s12015-011-9258-2 · Cited by 116 · see citing works
“efficiency [56, 57] as well as the safety [58, 59] of this approach.”
BackgroundInduced pluripotent stem cells and senescence: learning the biology to improve the technology
Banito, A., & Gil, J. (2010) · EMBO Reports · doi:10.1038/embor.2010.47 · Cited by 117 · see citing works
“In the latter strategy, fibroblast-like cells (or other somatic cell types) are obtained after in vitro differentiation of iPSCs that harbour doxycycline-inducible Yamanaka factors or, in the case of mouse cells, by the generation of chimeric mice”
BackgroundiPSC-Derived Hepatocytes as a Platform for Disease Modeling and Drug Discovery
Corbett, J., & Duncan, S. (2019) · Frontiers in Medicine · doi:10.3389/fmed.2019.00265 · Cited by 116 · see citing works
PIEZO2 is required for mechanotransduction in human stem cell–derived touch receptors
Schrenk-Siemens, K., Wende, H., Prato, V., Song, K., Rostock, C., Loewer, A., Utikal, J., Lewin, G., Lechner, S. G., & Siemens, J. (2014) · Nature Neuroscience · doi:10.1038/nn.3894 · Cited by 113 · see citing works
Self-citationTechnological Overview of iPS Induction from Human Adult Somatic Cells
Bayart, É., & Cohen‐Haguenauer, O. (2013) · Current Gene Therapy · doi:10.2174/1566523211313020002 · Cited by 112 · see citing works
“Another way to prevent re-expression of oncogene related factors is to control expression via a Tet-inducible system, which allows transgene repression in iPS like colony and further selection of fully reprogrammed cells [16, 33-37].”
iPSC Preparation and Epigenetic Memory: Does the Tissue Origin Matter?
Scesa, G., Adami, R., & Bottai, D. (2021) · Cells · doi:10.3390/cells10061470 · Cited by 110 · see citing works
“Recently, iPSCs have been produced by choosing less invasive cells to obtain, such as keratinocytes isolated from hair follicles [74].”
BackgroundInduced Pluripotent Stem Cells: Reprogramming Platforms and Applications in Cell Replacement Therapy
Abbar, A. A., Ngai, S. C., Nograles, N., Alhaji, S. Y., & Abdullah, S. (2020) · BioResearch open access · doi:10.1089/biores.2019.0046 · Cited by 136 · see citing works
“Nevertheless, efforts have been made to improve the safety of this strategy.(58,59) One of the advancements made in FIG.”
BackgroundTsix RNA and the germline factor, PRDM14, link X-reactivation and stem cell reprogramming
Payer, B., Rosenberg, M. H., Yamaji, M., Yabuta, Y., Koyanagi-Aoi, M., Hayashi, K., Yamanaka, S., Saitou, M., & Lee, J. (2013) · Molecules and Cells · doi:10.1016/j.molcel.2013.10.023 · Cited by 110 · see citing works
“For lentiviral reprogramming, fibroblasts were coinfected with polycistronic, Dox-inducible, four-factor STEMCCA (stem cell cassette; Sommer et al., 2009) and rtTA lentivirus (Maherali et al., 2008).”
Fluri, D. A., Tonge, P. D., Song, H., Baptista, R. P., Shakiba, N., Shukla, S., Clarke, G., Nagy, A., & Zandstra, P. W. (2012) · Nature Methods · doi:10.1038/nmeth.1939 · Cited by 106 · see citing works
- Authors
- Maherali, N., Ahfeldt, T., Rigamonti, A., Utikal, J., Cowan, C., & Hochedlinger, K.
- Affiliations
- Harvard University (US)
- Corresponding author
- Cowan, Chad
- Hochedlinger, Konrad
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 3
- Issue
- 3
- Pages
- 340-345
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC3987901
- OpenAlex
- W2086046223
- Cited by
- 563
- References
- 20
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 16 · 2023: 14 · 2022: 11 · 2021: 21 · 2020: 17 · 2019: 16 · 2018: 36 · 2017: 20 · 2016: 28 · 2015: 44 · 2014: 40 · 2013: 49 · 2012: 56
- FWCI
- 24.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1816 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell stem cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (1dp2od003266-01)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- human induced pluripotent stem cells, direct reprogramming, fibroblast reprogramming, Oct4, SOX2, c-Myc, KLF4, Nanog, Lin28, reprogramming efficiency, nuclear reprogramming, DNA methylation, differentiation potential
- MeSH terms
- Kruppel-Like Factor 4, Cytological Techniques, Fibroblasts, Genetic Techniques, Genetic Vectors, Humans, Lentivirus, Pluripotent Stem Cells, Cell Dedifferentiation, Cellular Reprogramming
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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