eISSN: 1509-572x
ISSN: 1641-4640
Folia Neuropathologica
Current issue Archive Manuscripts accepted About the journal Special Issues Editorial board Reviewers Abstracting and indexing Subscription Contact Instructions for authors Ethical standards and procedures
Editorial System
Submit your Manuscript
SCImago Journal & Country Rank
1/2024
vol. 62
 
Share:
Share:
Original paper

Safety of GMP-compliant iPSC lines generated by Sendai virus transduction is dependent upon clone identity and sex of the donor

Zuzanna Kuczynska
1
,
Pawan Kumar Neglur
1
,
Erkan Metin
1
,
Michal Liput
1
,
Marzena Zychowicz
1
,
Valery Zayat
1
,
Natalia E. Krześniak
2
,
Leonora Buzanska
1
,
Marta Kot
1

1.
Department of Stem Cell Bioengineering, Mossakowski Medical Research Institute, Polish Academy of Sciences, Warsaw, Poland
2.
Department of Plastic and Reconstructive Surgery, Centre of Postgraduate Medical Education, Prof. W. Orlowski Memorial Hospital, Warsaw, Poland
Folia Neuropathol 2024; 62 (1): 32-46
Online publish date: 2024/03/29
Article file
- Safety of GMP.PDF  [6.17 MB]
Get citation
 
PlumX metrics:
 
1. Baker D, Hirst AJ, Gokhale PJ, Juarez MA, Williams S, Wheeler M, Bean K, Allison TF, Moore HD, Andrews PW, Barbaric I. Detecting genetic mosaicism in cultures of human pluripotent stem cells. Stem Cell Reports 2016; 7: 998-1012.
2. Ban H, Nishishita N, Fusaki N, Tabata T, Saeki K, Shikamura M, Takada N, Inoue M, Hasegawa M, Kawamata S, Nishikawa S. Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc Natl Acad Sci U S A 2011; 108: 14234-14239.
3. Ben-David U, Arad G, Weissbein U, Mandefro B, Maimon A, Golan-Lev T, Narwani K, Clark AT, Andrews PW, Benvenisty N, Carlos Biancotti J. Aneuploidy induces profound changes in gene expression, proliferation and tumorigenicity of human pluripotent stem cells. Nat Commun 2014; 5: 4825.
4. Bercovich B, Stancovski I, Mayer A, Blumenfeld N, Laszlo A, Schwartz AL, Ciechanover A. Ubiquitin-dependent degradation of certain protein substrates in vitro requires the molecular chaperone Hsc70. J Biol Chem 1997; 272: 9002-9010.
5. Brenes AJ, Yoshikawa H, Bensaddek D, Mirauta B, Seaton D, Hukelmann JL, Jiang H, Stegle O, Lamond AI. Erosion of human X chromosome inactivation causes major remodeling of the iPSC proteome. Cell Rep 2021; 35: 109032.
6. Casimir GJA, Mulier S, Hanssens L, Zylberberg K, Duchateau J. Gender differences in inflammatory markers in children. Shock 2010; 33: 258-262.
7. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003; 113: 643-655.
8. Chin MH, Mason MJ, Xie W, Volinia S, Singer M, Peterson C, Ambartsumyan G, Aimiuwu O, Richter L, Zhang J, Khvorostov I, Ott V, Grunstein M, Lavon N, Benvenisty N, Croce CM, Clark AT, Baxter T, Pyle AD, Teitell MA, Pelegrini M, Plath K, Lowry WE. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 2009; 5: 111-123.
9. Cramer MN, Gagnon D, Laitano O, Crandall CG. Human temperature regulation under heat stress in health, disease, and injury. Physiol Rev 2022; 102: 1907-1989.
10. Darr H, Mayshar Y, Benvenisty N. Overexpression of NANOG in human ES cells enables feeder-free growth while inducing primitive ectoderm features. Development 2006; 133: 1193-1201.
11. Doss MX, Sachinidis A. Current challenges of iPSC-based disease modeling and therapeutic implications. Cells 2019; 8: 403.
12. Dubose CO, Daum JR, Sansam CL, Gorbsky GJ. Dynamic features of chromosomal instability during culture of induced pluripotent stem cells. Genes (Basel) 2022; 13: 1157.
13. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M. Efficient induction of transgene-free human pluripotent stem cells using a vector based on Sendai virus, an RNA virus that does not integrate into the host genome. Proc Jpn Acad Ser B Phys Biol Sci 2009; 85: 348-362.
14. Kajiwara M, Aoi T, Okita K, Takahashi R, Inoue H, Takayama N, Endo H, Eto K, Toguchida J, Uemoto S, Yamanaka S. Donordependent variations in hepatic differentiation from humaninduced pluripotent stem cells. Proc Natl Acad Sci U S A 2012; 109: 12538-12543.
15. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Ulrich Hartl F. Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 2013; 82: 323-355.
16. Kim JH, Kang KW, Lee BH, Park Y, Kim BS. Generation of induced pluripotent stem cell line KUMi002-A with normal karyotype from a patient with Philadelphia chromosome-positive chronic myeloid leukemia. Stem Cell Res 2021; 55: 102465.
17. Kim JH, Kang KW, Lee BH, Park Y, Kim BS. Generation of human induced iPSC KUMi003-A from acute promyelocytic leukemia (APL) M3. Stem Cell Res 2022; 63: 102861.
18. Kim D, Kim CH, Moon J Il, Chung YG, Chang MY, Han BS, Ko S, Yang E, Cha KY, Lanza R, Kim KS. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009; 4: 472-476.
19. Kim JY, Nam Y, Rim YA, Ju JH. Review of the current trends in clinical trials involving induced pluripotent stem cells. Stem Cell Rev Reports 2022; 18: 142-154.
20. Kopp JL, Ormsbee BD, Desler M, Rizzino A. Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells. Stem Cells 2008; 26: 903-911.
21. Koyanagi-Aoi M, Ohnuki M, Takahashi K, Okita K, Noma H, Sawamura Y, Teramoto I, Narita M, Sato Y, Ichisaka T, Amano N, Watanabe A, Morizane A, Yamada Y, Sato T, Takahashi J, Yamanaka S. Differentiation-defective phenotypes revealed by large-scale analyses of human pluripotent stem cells. Proc Natl Acad Sci U S A 2013; 110: 20569-20574.
22. Laurent LC, Ulitsky I, Slavin I, Tran H, Schork A, Morey R, Lynch C, Harness JV, Lee S, Barrero MJ, Ku S, Martynova M, Semechkin R, Galat V, Gottesfeld J, Izpisua Belmonte JC, Murry C, Keirstead HS, Park HS, Schmidt U, Laslett AL, Muller FJ, Nievergelt CM, Shamir R, Loring JF. Dynamic changes in the copy number of pluripotency and cell proliferation genes in human ESCs and iPSCs during reprogramming and time in culture. Cell Stem Cell 2011; 8: 106-118.
23. Li HO, Zhu YF, Asakawa M, Kuma H, Hirata T, Ueda Y, Lee YS, Fukumura M, Iida A, Kato A, Nagai Y, Hasegawa M. A Cytoplasmic RNA vector derived from nontransmissible Sendai virus with efficient gene transfer and expression. J Virol 2000; 74: 6564-6569.
24. Liang G, Zhang Y. Genetic and epigenetic variations in iPSCs: potential causes and implications for application. Cell Stem Cell 2013; 13: 149-159.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods 2001; 25: 402-408.
26. Lowry WE, Richter L, Yachechko R, Pyle AD, Tchieu J, Sridharan R,Clark AT, Plath K. Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci U S A 2008; 105: 2883-2888.
27. Lovell R, Madden L, Carroll S, McNaughton L. The time-profile of the PBMC HSP70 response to in vitro heat shock appears temperature-dependent. Amino Acids 2007; 33: 137-144.
28. Lyu X, Rowley MJ, Corces VG. Architectural proteins and pluripotency factors cooperate to orchestrate the transcriptional response of hESCs to temperature stress. Mol Cell 2018; 71: 940-955.e7.
29. MacArthur CC, Fontes A, Ravinder N, Kuninger D, Kaur J, Bailey M, Taliana A, Vemuri MC, Lieu PT. Generation of humaninduced pluripotent stem cells by a nonintegrating RNA Sendai virus vector in feeder-free or xeno-free conditions. Stem Cells Int 2012; 2012: 564612.
30. Marchetto MCN, Yeo GW, Kainohana O, Marsala M, Gage FH, Muotri AR. Transcriptional signature and memory retention of human-induced pluripotent stem cells. PLoS One 2009; 4: e7076.
31. Martins-Taylor K, Nisler BS, Taapken SM, Compton T, Crandall L,Montgomery KD, Lalande M, Xu RH. Recurrent copy number variations in human induced pluripotent stem cells. Nat Biotechnol 2011; 29: 488-491.
32. Masaki H, Ishikawa T, Takahashi S, Okumura M, Sakai N, Haga M,Kominami K, Migita H, McDonald F, Shimada F, Sakurada K. Heterogeneity of pluripotent marker gene expression in colonies generated in human iPS cell induction culture. Stem Cell Res 2007; 1: 105-115.
33. Mayshar Y, Ben-David U, Lavon N, Biancotti JC, Yakir B, Clark AT,Plath K, Lowry WE, Benvenisty N. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010; 7: 521-531.
34. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. The homeoprotein nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003; 113: 631-642.
35. Nishino K, Toyoda M, Yamazaki-Inoue M, Fukawatase Y, Chikazawa E, Sakaguchi H, Akutsu H, Umezawa A. DNA methylation dynamics in human induced pluripotent stem cells over time. PLoS Genet 2011; 7: 1002085.
36. Niwa H, Miyazaki JI, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000; 24: 372-376.
37. Okumura-Nakanishi S, Saito M, Niwa H, Ishikawa F. Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem 2005; 280: 5307-5317.
38. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008; 451: 141-146.
39. Saretzki G, Walter T, Atkinson S, Passos JF, Bareth B, Keith WN, Stewart R, Hoare S, Stojkovic M, Armstrong L, von Zglinicki T, Lako M. Downregulation of multiple stress defense mechanisms during differentiation of human embryonic stem cells. Stem Cells 2008; 26: 455-464.
40. Shinagawa T, Takagi T, Tsukamoto D, Tomaru C, Huynh LM, Sivaraman P, Kumarevel T, Inoue K, Nakato R, Katou Y, Sado T, Takahashi S, Ogura A, Shirahige K, Ishii S. Histone variants enriched in oocytes enhance reprogramming to induced pluripotent stem cells. Cell Stem Cell 2014; 14: 217-227.
41. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, Barrandon O, Wray J, Yamanaka S, Chambers I, Smith A. Nanog is the gateway to the pluripotent ground state. Cell 2009; 138: 722-737.
42. Singh AM, Hamazaki T, Hankowski KE, Terada N. A heterogeneous expression pattern for nanog in embryonic stem cells. Stem Cells 2007; 25: 2534-2542.
43. Sousa EJ, Stuart HT, Bates LE, Ghorbani M, Nichols J, Dietmann S, Silva JCR. Exit from naive pluripotency induces a transient X chromosome inactivation-like state in males. Cell Stem Cell 2018; 22: 919-928.e6.
44. Sullivan S, Stacey GN, Akazawa C, Aoyama N, Baptista R, Bedford P, Bennaceur Griscelli A, Chandra A, Elwood N, Girard M, Kawamata S, Hanatani T, Latsis T, Lin S, Ludwig TE, Malygina T, Mack A, Mountford JC, Noggle S, Pereira LV, Price J, Sheldon M, Srivastava A, Stachelscheid H, Velayudhan SR, Ward NJ, Turner ML, Barry J, Song J. Quality control guidelines for clinical-grade human induced pluripotent stem cell lines. Regen Med 2018; 13: 859-866.
45. Štefková K, Procházková J, Pacherník J. Alkaline phosphatase in stem cells. Stem Cells Int 2015; 2015: 628368.
46. Taapken SM, Nisler BS, Newton MA, Sampsell-Barron TL, Leonhard KA, McIntire EM, Montgomery KD. Karotypic abnormalities in human induced pluripotent stem cells and embryonic stem cells. Nat Biotechnol 2011; 29: 313-314.
47. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-676.
48. Tomioka M, Nishimoto M, Miyagi S, Katayanagi T, Fukui N, Niwa H, Muramatsu M, Okuda A. Identification of Sox-2 regulatory region which is under the control of Oct-3/4–Sox-2 complex. Nucleic Acids Res 2002; 30: 3202.
49. Tulapurkar ME, Asiegbu BR, Singh IS, Hasday JD. Hyperthermia in the febrile range induces HSP72 expression proportional to exposure temperature but not to HSF-1 DNA-binding activity in human lung epithelial A549 cells. Cell Stress Chaperones 2009; 14: 499-508.
50. Wiley LA, Anfinson KR, Cranston CM, Kaalberg EE, Collins MM, Mullins RF, Stone EM, Tucker BA. Generation of xeno‐free, cGMP‐compliant patient‐specific iPSCs from skin biopsy. Curr Protoc Stem Cell Biol 2017; 42: 4A.12.1.
51. Willmann CA, Hemeda H, Pieper LA, Lenz M, Qin J, Joussen S, Sontag S, Wanek P, Denecke B, Schüler HM, Zenke M, Wagner W. To clone or not to clone? Induced pluripotent stem cells can be generated in bulk culture. PLoS One 2013; 8: e65324.
52. Vitale AM, Matigian NA, Ravishankar S, Bellette B, Wood SA, Wolvetang EJ, Mackay-Sim A. Variability in the generation of induced pluripotent stem cells: Importance for disease modeling. Stem Cells Transl Med 2012; 1: 641-650.
53. Vogler C, Huber C, Waldmann T, Ettig R, Braun L, Izzo A, Daujat S, Chassignet I, Lopez-Contreras AJ, Fernandez-Capetillo O, Dundr M, Rippe K, Längst G, Schneider R. Histone H2A C-terminus regulates chromatin dynamics, remodeling, and histone H1 binding. PLOS Genet 2010; 6: e1001234.
54. Yamanaka S. Pluripotent stem cell-based cell therapy – Promise and challenges. Cell Stem Cell 2020; 27: 523-531.
55. Ye H, Wang Q. Efficient generation of non-integration and feeder-free induced pluripotent stem cells from human peripheral blood cells by Sendai virus. Cell Physiol Biochem 2018; 50: 1318-1331.
56. Yokobayashi S, Okita K, Nakagawa M, Nakamura T, Yabuta Y, Yamamoto T, Saitou M. Clonal variation of human induced pluripotent stem cells for induction into the germ cell fate. Biol Reprod 2017; 96: 1154-1166.
57. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007; 318: 1917-1920.
58. Zeineddine D, Papadimou E, Chebli K, Gineste M, Liu J, Grey C, Thurig S, Behfar A, Wallace VA, Skerjanc IS, Pucéat M. Oct-3/4 dose dependently regulates specification of embryonic stem cells toward a cardiac lineage and early heart development. Dev Cell 2006; 11: 535-546.
Copyright: © 2024 Mossakowski Medical Research Centre Polish Academy of Sciences and the Polish Association of Neuropathologists. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (http://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
Quick links
© 2024 Termedia Sp. z o.o.
Developed by Bentus.