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Table 2 Summary of the procedures for reprogramming and the targeted functions in human pluripotent stem cells and their derivatives

From: Prevention of tumor risk associated with the reprogramming of human pluripotent stem cells

Cell Types


Function targeted

Status of tumorigenesis

Tumor treatment

Clinical trail


A. Chemical treatments


Inhibitors of stearoyl-CoA desaturase (SCD)1

Oleate = decreased Stearate and Palmitate = increased

Prevent teratoma


(No trial yet)

2013 [325]

 ESCs and EBCs

(N-oleoyl serinol) = ceramide analogue


OCT4 (+) / Prostate apoptosis response-4 (PAR-4) (+) = elimination

Human cancer cell lines

Brain tumor cell lines

Adenocarcinoma cell lines

Hepatocarcinoma cell lines

2002 [336]

2003 [337]



Inhibit ERV/ALR (sulfhydroxyl oxidase)

Impairs import of Mila40/Erv1 and TIM22

Block the teratoma formation


2013 [326]

 hPSCs, HiPSCs

Clostridium perfringens endotoxin (CPE)

Bound several Claudins including Claugin-6

Elimination of tumorigenic PSCs


2013 [333]

 hESCs, hiPSC-derived cells

Survivin inhibitor (Quercetin or YM155)

Cell death of undifferentiated stem cells, mitochondrial accumulation of p53

Prevent teratoma formation

Gastric cancer

2017 [338]


Digoxin and Lanatoside C

Cytotoxicity in undifferentiated hESCs

Tumor prevention in hESCs


2017 [339]



ER stress;



Inhibition of teratoma formation


2014 [340]

B. Immunological treatment


Anti-Claudin 6 (CLDN-6), Anti-CLDN-6 (+) cells removal, Anti-CLODN-6-Cytotoxic Ab, Anti-CLODN-6-Toxin CPE

Decrease the teratoma-formation

Inhibition of Teratoma


2013 [333]



H-type-1 glycan surface markers, SSEA-5-CD9, CD30, CD50, CD90 and CD200

Removal of cells with teratoma-potential from incompletely differentiated hESCs


2011 [323]


UEA-1+ and SSEA-4+

Fut1 and Fut 2 (fucosyl transferases)

Enrichment of PSCs


2011 [341]


mAb 84 cytotoxic antibody(Podocalyxin-like protein 1)

Kill undifferentiated hSCs

Removal of teratoma formation


2009 [331]

2008 [332]

 HPSCs derived neural precursor cells

Tra-1-60 (−), Tra-1-81 (−)

Removal of undifferentiated cells by Ab-nanogold

Inhibition of teratoma formation


2010 [342]

C. Genetic treatment


Survivin (BIRC5), YM155

Apoptosis in hESCs and teratoma formation

Removal of teratoma formation


2009 [328]


HSV-tk + cells were killed by ganciclovir

Kill HSV-tk (+) cells

Remove the tumor forming cells

HSV-tk + teratoma

2003 [330]


Nanog-3′ untranslated region with HSV-tk (+) gene

Kill HSV^tk (+) cells

Remove the tumor forming cells


2012 [343]

 Gastric cancer cells

Overexpression of JDP2, Oct4

BMP7 inhibition

Decreasing teratoma development

Gastric cancer

2017 [195]

 Neural cells from iPSCs

Pre-evaluation by transfer of iPSCs derived cells to primates

Pre-evaluation of tumor development

No tumor development

Spinal cord injury in marmoset model

2012 [344]

 Neural cells from iPSCs

Methylation analysis of iPSCs derived cells

Non-methylation status of CAT, PSMD5 genes

No tumor development

Nerval stem progenitors

hiPSC-NS/DCs in clinical model

2017 [303]

 Prostate cancer cells

Knock down of Oct4, Sox2

Tumor development screening after in vivo transfer

No tumor development

Prostate cancer


2010 [314]

 Cardiac progenitor cells from iPSCs

Inhibitors of DNA topoisomerase

Decreasing teratoma formation

Decreasing teratomas


iPSC-derivet cardiac regenerations

2014 [345]

 ES cells

CDK1 inhibitor treatment

Activation of p53-HOXA-MCL1 axis

Prevention of teratoma formation


2015 [346]


Inhibition of anti-apoptotic factor, treatment Survivin (YM155)

Pre-evaluation of tumor development

No teratoma formation in mice


2017 [347]


Introduction of suicide gene Caspase-9

Pre-evaluation of tumorigenic transformation

Avoid tumorigenic transformation

Injured spial cord of NOD/SCID mice

hiPS/NS/DCs in animal model

2017 [348]

2012 [344]

 Neuro-spheres from iPSCs

Pre-evaluation by transfer of iPSCs derived cells to mice

Pre-evaluation of tumor development

No tumor development

Spinal cord injury (SCI) patients tratment in animal model

hiPS/NS/DCs in animal model

2011 [349]

 Pancreatic ductal adenocarcinoma derived PDAC

* Tet-OSKM & MzrtTA

* Mir302-OCT4 * Episomal vector

Reduced tumorgenicity

TET2, SirT1, and Dot1L were decreased. TET1 upregulated & Tbx downregulated

Nanog is required. Tra-1-80 decreased

Reprogrammed pancreatic ductal adenocarcinoma (PDAC)-Tumergenesis

2019 [350]

 Ischemic Cardiomyopathy cells

EZH2, FoxM1 epigenetic repressed in PRC2

KLF15 decreased

DNA methylation on targetsof KLF15 Epigenetic regulator suppressed metabolic reprogramming of ICM

KLF15 repression

Ischemic cardiomyopathy


2019 [351]

 Ovarian cancer cells


Open chromatin

H3K79 methylation

Ovarian cancer cells-Reprogramming

2018 [352]

 Pediatric cancer derived iPSCs

Dnmt3a ablation

De novo ICR-preferred CGI hypermethylation ICR-CpG islands

Cancer repressed

In vivo pluripotency

2017 [353]