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Induced Pluripotent Stem Cells and Induced Pluripotent Cancer Cells in Cancer Disease Modeling

  • Dandan Zhu
  • Celine Shuet Lin Kong
  • Julian A. Gingold
  • Ruiying ZhaoEmail author
  • Dung-Fang LeeEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1119)

Abstract

In 2006, Noble Prize laureate Shinya Yamanaka discovered that a set of transcription factors can reprogram terminally differentiated somatic cells to a pluripotent stem cell state. Since then, induced pluripotent stem cells (iPSCs) have come into the public spotlight. Amidst a growing field of promising clinical uses of iPSCs in recent years, cancer disease modeling has emerged as a particularly promising and rapidly translatable application of iPSCs. Technological advances in genome editing over the past few years have facilitated increasingly rapid progress in generation of iPSCs with clearly defined genetic backgrounds to complement existing patient-derived models. Improved protocols for differentiation of iPSCs, engineered iPSCs and embryonic stem cells (ESCs) now permit the study of disease biology in the majority of somatic cell types. Here, we highlight current efforts to create patient-derived iPSC disease models to study various cancer types. We review the advantages and current challenges of using iPSCs in cancer disease modeling.

Keywords

Cancer disease model Genome editing Induced pluripotent cancer cells Induced pluripotent stem cells Reprogramming 

Abbreviations

AML

acute myeloid leukemia

APC

adenomatous polyposis cell

CML

chronic myeloid leukemia

COs

colorectal organoids

ER

estrogen receptor

ESCs

embryonic stem cells

FAP

familial adenomatous polyposis

HBOC

hereditary breast and ovarian cancer

iPCCs

induced pluripotent cancer cells

iPSCs

induced pluripotent stem cells

JMML

juvenile myelomonocytic leukemia

LFS

Li-Fraumeni syndrome

LSC

leukemic stem cells

MDS

Myelodysplastic syndrome

MSCs

mesenchymal stem cells

NS

Noonan syndrome

PDAC

pancreatic ductal adenocarcinoma

PR

progesterone receptor

sgRNA

single guide RNA

TALEN

transcription activator-like effector nuclease

ZFN

zinc finger nuclease

Notes

Acknowledgements

D.-F.L. is the CPRIT scholar in Cancer Research and supported by NIH Pathway to Independence Award R00 CA181496 and CPRIT Award RR160019.

Conflicts of Interest

Authors declare no conflicts of interest.

References

  1. Aaltonen LA, Peltomaki P, Leach FS, Sistonen P, Pylkkanen L, Mecklin JP, Jarvinen H, Powell SM, Jen J, Hamilton SR et al (1993) Clues to the pathogenesis of familial colorectal cancer. Science 260(5109):812–816CrossRefGoogle Scholar
  2. Abyzov A, Mariani J, Palejev D, Zhang Y, Haney MS, Tomasini L, Ferrandino AF, Rosenberg Belmaker LA, Szekely A, Wilson M, Kocabas A, Calixto NE, Grigorenko EL, Huttner A, Chawarska K, Weissman S, Urban AE, Gerstein M, Vaccarino FM (2012) Somatic copy number mosaicism in human skin revealed by induced pluripotent stem cells. Nature 492(7429):438–442.  https://doi.org/10.1038/nature11629 CrossRefPubMedPubMedCentralGoogle Scholar
  3. An MC, Zhang N, Scott G, Montoro D, Wittkop T, Mooney S, Melov S, Ellerby LM (2012) Genetic correction of Huntington’s disease phenotypes in induced pluripotent stem cells. Cell Stem Cell 11(2):253–263.  https://doi.org/10.1016/j.stem.2012.04.026 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Ang YS, Rivas RN, Ribeiro AJS, Srivas R, Rivera J, Stone NR, Pratt K, Mohamed TMA, Fu JD, Spencer CI, Tippens ND, Li M, Narasimha A, Radzinsky E, Moon-Grady AJ, Yu H, Pruitt BL, Snyder MP, Srivastava D (2016) Disease model of GATA4 mutation reveals transcription factor cooperativity in human cardiogenesis. Cell 167(7):1734–1749 e1722.  https://doi.org/10.1016/j.cell.2016.11.033 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Anokye-Danso F, Trivedi CM, Juhr D, Gupta M, Cui Z, Tian Y, Zhang Y, Yang W, Gruber PJ, Epstein JA, Morrisey EE (2011) Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8(4):376–388.  https://doi.org/10.1016/j.stem.2011.03.001 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Aoi T, Yae K, Nakagawa M, Ichisaka T, Okita K, Takahashi K, Chiba T, Yamanaka S (2008) Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 321(5889):699–702.  https://doi.org/10.1126/science.1154884 CrossRefPubMedGoogle Scholar
  7. Apostolou E, Hochedlinger K (2013) Chromatin dynamics during cellular reprogramming. Nature 502(7472):462–471.  https://doi.org/10.1038/nature12749 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Ban H, Nishishita N, Fusaki N, Tabata T, Saeki K, Shikamura M, Takada N, Inoue M, Hasegawa M, Kawamata S, Nishikawa S (2011) Efficient generation of transgene-free human induced pluripotent stem cells (iPSCs) by temperature-sensitive Sendai virus vectors. Proc Natl Acad Sci U S A 108(34):14234–14239.  https://doi.org/10.1073/pnas.1103509108 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brennan CW, Verhaak RG, McKenna A, Campos B, Noushmehr H, Salama SR, Zheng S, Chakravarty D, Sanborn JZ, Berman SH, Beroukhim R, Bernard B, Wu CJ, Genovese G, Shmulevich I, Barnholtz-Sloan J, Zou L, Vegesna R, Shukla SA, Ciriello G, Yung WK, Zhang W, Sougnez C, Mikkelsen T, Aldape K, Bigner DD, Van Meir EG, Prados M, Sloan A, Black KL, Eschbacher J, Finocchiaro G, Friedman W, Andrews DW, Guha A, Iacocca M, O’Neill BP, Foltz G, Myers J, Weisenberger DJ, Penny R, Kucherlapati R, Perou CM, Hayes DN, Gibbs R, Marra M, Mills GB, Lander E, Spellman P, Wilson R, Sander C, Weinstein J, Meyerson M, Gabriel S, Laird PW, Haussler D, Getz G, Chin L, Network TR (2013) The somatic genomic landscape of glioblastoma. Cell 155(2):462–477.  https://doi.org/10.1016/j.cell.2013.09.034 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Briggs JA, Sun J, Shepherd J, Ovchinnikov DA, Chung TL, Nayler SP, Kao LP, Morrow CA, Thakar NY, Soo SY, Peura T, Grimmond S, Wolvetang EJ (2013) Integration-free induced pluripotent stem cells model genetic and neural developmental features of down syndrome etiology. Stem Cells 31(3):467–478.  https://doi.org/10.1002/stem.1297 CrossRefPubMedGoogle Scholar
  11. Carvajal-Vergara X, Sevilla A, D’Souza SL, Ang YS, Schaniel C, Lee DF, Yang L, Kaplan AD, Adler ED, Rozov R, Ge Y, Cohen N, Edelmann LJ, Chang B, Waghray A, Su J, Pardo S, Lichtenbelt KD, Tartaglia M, Gelb BD, Lemischka IR (2010) Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 465(7299):808–812.  https://doi.org/10.1038/nature09005 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chao MP, Gentles AJ, Chatterjee S, Lan F, Reinisch A, Corces MR, Xavy S, Shen J, Haag D, Chanda S, Sinha R, Morganti RM, Nishimura T, Ameen M, Wu H, Wernig M, Wu JC, Majeti R (2017) Human AML-iPSCs reacquire leukemic properties after differentiation and model clonal variation of disease. Cell Stem Cell 20(3):329–344 e327.  https://doi.org/10.1016/j.stem.2016.11.018 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Chen J, McKay RM, Parada LF (2012) Malignant glioma: lessons from genomics, mouse models, and stem cells. Cell 149(1):36–47.  https://doi.org/10.1016/j.cell.2012.03.009 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Cheng L, Hansen NF, Zhao L, Du Y, Zou C, Donovan FX, Chou BK, Zhou G, Li S, Dowey SN, Ye Z, Program NCS, Chandrasekharappa SC, Yang H, Mullikin JC, Liu PP (2012) Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 10(3):337–344.  https://doi.org/10.1016/j.stem.2012.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823.  https://doi.org/10.1126/science.1231143 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Corbin AS, Agarwal A, Loriaux M, Cortes J, Deininger MW, Druker BJ (2011) Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J Clin Invest 121(1):396–409.  https://doi.org/10.1172/JCI35721 CrossRefPubMedGoogle Scholar
  17. Crespo M, Vilar E, Tsai SY, Chang K, Amin S, Srinivasan T, Zhang T, Pipalia NH, Chen HJ, Witherspoon M, Gordillo M, Xiang JZ, Maxfield FR, Lipkin S, Evans T, Chen S (2017) Colonic organoids derived from human induced pluripotent stem cells for modeling colorectal cancer and drug testing. Nat Med 23(7):878–884CrossRefGoogle Scholar
  18. De Los Angeles A, Ferrari F, Xi R, Fujiwara Y, Benvenisty N, Deng H, Hochedlinger K, Jaenisch R, Lee S, Leitch HG, Lensch MW, Lujan E, Pei D, Rossant J, Wernig M, Park PJ, Daley GQ (2015) Hallmarks of pluripotency. Nature 525(7570):469–478.  https://doi.org/10.1038/nature15515 CrossRefPubMedGoogle Scholar
  19. Devine MJ, Ryten M, Vodicka P, Thomson AJ, Burdon T, Houlden H, Cavaleri F, Nagano M, Drummond NJ, Taanman JW, Schapira AH, Gwinn K, Hardy J, Lewis PA, Kunath T (2011) Parkinson’s disease induced pluripotent stem cells with triplication of the alpha-synuclein locus. Nat Commun 2:440.  https://doi.org/10.1038/ncomms1453 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Doulatov S, Vo LT, Macari ER, Wahlster L, Kinney MA, Taylor AM, Barragan J, Gupta M, McGrath K, Lee HY, Humphries JM, Devine A, Narla A, Alter BP, Beggs AH, Agarwal S, Ebert BL, Gazda HT, Lodish HF, Sieff CA, Schlaeger TM, Zon LI, Daley GQ (2017) Drug discovery for Diamond-Blackfan anemia using reprogrammed hematopoietic progenitors. Sci Transl Med 9(376):eaah5645.  https://doi.org/10.1126/scitranslmed.aah5645 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Druker BJ, Guilhot F, O’Brien SG, Gathmann I, Kantarjian H, Gattermann N, Deininger MW, Silver RT, Goldman JM, Stone RM, Cervantes F, Hochhaus A, Powell BL, Gabrilove JL, Rousselot P, Reiffers J, Cornelissen JJ, Hughes T, Agis H, Fischer T, Verhoef G, Shepherd J, Saglio G, Gratwohl A, Nielsen JL, Radich JP, Simonsson B, Taylor K, Baccarani M, So C, Letvak L, Larson RA, Investigators I (2006) Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 355(23):2408–2417.  https://doi.org/10.1056/NEJMoa062867 CrossRefGoogle Scholar
  22. Funato K, Major T, Lewis PW, Allis CD, Tabar V (2014) Use of human embryonic stem cells to model pediatric gliomas with H3.3K27M histone mutation. Science 346(6216):1529–1533.  https://doi.org/10.1126/science.1253799 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Fusaki N, Ban H, Nishiyama A, Saeki K, Hasegawa M (2009) 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 85(8):348–362CrossRefGoogle Scholar
  24. Futreal PA, Liu Q, Shattuck-Eidens D, Cochran C, Harshman K, Tavtigian S, Bennett LM, Haugen-Strano A, Swensen J, Miki Y et al (1994) BRCA1 mutations in primary breast and ovarian carcinomas. Science 266(5182):120–122CrossRefGoogle Scholar
  25. Gingold J, Zhou R, Lemischka IR, Lee DF (2016) Modeling Cancer with pluripotent stem cells. Trends Cancer 2(9):485–494.  https://doi.org/10.1016/j.trecan.2016.07.007 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gordge PC, Hulme MJ, Clegg RA, Miller WR (1996) Elevation of protein kinase A and protein kinase C activities in malignant as compared with normal human breast tissue. Eur J Cancer 32A(12):2120–2126CrossRefGoogle Scholar
  27. Guenther MG, Frampton GM, Soldner F, Hockemeyer D, Mitalipova M, Jaenisch R, Young RA (2010) Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 7(2):249–257.  https://doi.org/10.1016/j.stem.2010.06.015 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Guha P, Morgan JW, Mostoslavsky G, Rodrigues NP, Boyd AS (2017) Lack of immune response to differentiated cells derived from syngeneic induced pluripotent stem cells. Cell Stem Cell 21(1):144–148.  https://doi.org/10.1016/j.stem.2017.03.012 CrossRefPubMedGoogle Scholar
  29. Hockemeyer D, Jaenisch R (2016) Induced pluripotent stem cells meet genome editing. Cell Stem Cell 18(5):573–586.  https://doi.org/10.1016/j.stem.2016.04.013 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hu K, Yu J, Suknuntha K, Tian S, Montgomery K, Choi KD, Stewart R, Thomson JA, Slukvin II (2011) Efficient generation of transgene-free induced pluripotent stem cells from normal and neoplastic bone marrow and cord blood mononuclear cells. Blood 117(14):e109–e119.  https://doi.org/10.1182/blood-2010-07-298331 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hussein SM, Batada NN, Vuoristo S, Ching RW, Autio R, Narva E, Ng S, Sourour M, Hamalainen R, Olsson C, Lundin K, Mikkola M, Trokovic R, Peitz M, Brustle O, Bazett-Jones DP, Alitalo K, Lahesmaa R, Nagy A, Otonkoski T (2011) Copy number variation and selection during reprogramming to pluripotency. Nature 471(7336):58–62.  https://doi.org/10.1038/nature09871 CrossRefPubMedGoogle Scholar
  32. Israel MA, Yuan SH, Bardy C, Reyna SM, Mu Y, Herrera C, Hefferan MP, Van Gorp S, Nazor KL, Boscolo FS, Carson CT, Laurent LC, Marsala M, Gage FH, Remes AM, Koo EH, Goldstein LS (2012) Probing sporadic and familial Alzheimer’s disease using induced pluripotent stem cells. Nature 482(7384):216–220.  https://doi.org/10.1038/nature10821 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Itzhaki I, Maizels L, Huber I, Zwi-Dantsis L, Caspi O, Winterstern A, Feldman O, Gepstein A, Arbel G, Hammerman H, Boulos M, Gepstein L (2011) Modelling the long QT syndrome with induced pluripotent stem cells. Nature 471(7337):225–229.  https://doi.org/10.1038/nature09747 CrossRefPubMedGoogle Scholar
  34. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K (2009) Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458(7239):771–775.  https://doi.org/10.1038/nature07864 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Karakikes I, Termglinchan V, Wu JC (2014) Human-induced pluripotent stem cell models of inherited cardiomyopathies. Curr Opin Cardiol 29(3):214–219.  https://doi.org/10.1097/HCO.0000000000000049 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kim D, Kim CH, Moon JI, Chung YG, Chang MY, Han BS, Ko S, Yang E, Cha KY, Lanza R, Kim KS (2009) Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 4(6):472–476.  https://doi.org/10.1016/j.stem.2009.05.005 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kim J, Hoffman JP, Alpaugh RK, Rhim AD, Reichert M, Stanger BZ, Furth EE, Sepulveda AR, Yuan CX, Won KJ, Donahue G, Sands J, Gumbs AA, Zaret KS (2013) An iPSC line from human pancreatic ductal adenocarcinoma undergoes early to invasive stages of pancreatic cancer progression. Cell Rep 3(6):2088–2099.  https://doi.org/10.1016/j.celrep.2013.05.036 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kondo T, Asai M, Tsukita K, Kutoku Y, Ohsawa Y, Sunada Y, Imamura K, Egawa N, Yahata N, Okita K, Takahashi K, Asaka I, Aoi T, Watanabe A, Watanabe K, Kadoya C, Nakano R, Watanabe D, Maruyama K, Hori O, Hibino S, Choshi T, Nakahata T, Hioki H, Kaneko T, Naitoh M, Yoshikawa K, Yamawaki S, Suzuki S, Hata R, Ueno S, Seki T, Kobayashi K, Toda T, Murakami K, Irie K, Klein WL, Mori H, Asada T, Takahashi R, Iwata N, Yamanaka S, Inoue H (2013) Modeling Alzheimer’s disease with iPSCs reveals stress phenotypes associated with intracellular Abeta and differential drug responsiveness. Cell Stem Cell 12(4):487–496.  https://doi.org/10.1016/j.stem.2013.01.009 CrossRefGoogle Scholar
  39. Kooreman NG, Kim Y, de Almeida PE, Termglinchan V, Diecke S, Shao NY, Wei TT, Yi H, Dey D, Nelakanti R, Brouwer TP, Paik DT, Sagiv-Barfi I, Han A, Quax PHA, Hamming JF, Levy R, Davis MM, Wu JC (2018) Autologous iPSC-based vaccines elicit anti-tumor responses in vivo. Cell Stem Cell 22(4):501–513 e507.  https://doi.org/10.1016/j.stem.2018.01.016 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kotini AG, Chang CJ, Boussaad I, Delrow JJ, Dolezal EK, Nagulapally AB, Perna F, Fishbein GA, Klimek VM, Hawkins RD, Huangfu D, Murry CE, Graubert T, Nimer SD, Papapetrou EP (2015) Functional analysis of a chromosomal deletion associated with myelodysplastic syndromes using isogenic human induced pluripotent stem cells. Nat Biotechnol 33(6):646–655.  https://doi.org/10.1038/nbt.3178 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kotini AG, Chang CJ, Chow A, Yuan H, Ho TC, Wang T, Vora S, Solovyov A, Husser C, Olszewska M, Teruya-Feldstein J, Perumal D, Klimek VM, Spyridonidis A, Rampal RK, Silverman L, Reddy EP, Papaemmanuil E, Parekh S, Greenbaum BD, Leslie CS, Kharas MG, Papapetrou EP (2017) Stage-specific human induced pluripotent stem cells map the progression of myeloid transformation to transplantable leukemia. Cell Stem Cell 20(3):315–328 e317.  https://doi.org/10.1016/j.stem.2017.01.009 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kriks S, Shim JW, Piao J, Ganat YM, Wakeman DR, Xie Z, Carrillo-Reid L, Auyeung G, Antonacci C, Buch A, Yang L, Beal MF, Surmeier DJ, Kordower JH, Tabar V, Studer L (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease. Nature 480(7378):547–551.  https://doi.org/10.1038/nature10648 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 (2011) 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 8(1):106–118.  https://doi.org/10.1016/j.stem.2010.12.003 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lee G, Papapetrou EP, Kim H, Chambers SM, Tomishima MJ, Fasano CA, Ganat YM, Menon J, Shimizu F, Viale A, Tabar V, Sadelain M, Studer L (2009) Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461(7262):402–406.  https://doi.org/10.1038/nature08320 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lee DF, Su J, Kim HS, Chang B, Papatsenko D, Zhao R, Yuan Y, Gingold J, Xia W, Darr H, Mirzayans R, Hung MC, Schaniel C, Lemischka IR (2015) Modeling familial cancer with induced pluripotent stem cells. Cell 161(2):240–254CrossRefGoogle Scholar
  46. Li FP, Fraumeni JF Jr (1969) Soft-tissue sarcomas, breast cancer, and other neoplasms. A familial syndrome? Ann Intern Med 71(4):747–752CrossRefGoogle Scholar
  47. Lin YH, Jewell BE, Gingold J, Lu L, Zhao R, Wang LL, Lee DF (2017) Osteosarcoma: molecular pathogenesis and iPSC modeling. Trends Mol Med 23(8):737–755.  https://doi.org/10.1016/j.molmed.2017.06.004 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Lowry WE, Richter L, Yachechko R, Pyle AD, Tchieu J, Sridharan R, Clark AT, Plath K (2008) Generation of human induced pluripotent stem cells from dermal fibroblasts. Proc Natl Acad Sci U S A 105(8):2883–2888.  https://doi.org/10.1073/pnas.0711983105 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Maherali N, Sridharan R, Xie W, Utikal J, Eminli S, Arnold K, Stadtfeld M, Yachechko R, Tchieu J, Jaenisch R, Plath K, Hochedlinger K (2007) Directly reprogrammed fibroblasts show global epigenetic remodeling and widespread tissue contribution. Cell Stem Cell 1(1):55–70.  https://doi.org/10.1016/j.stem.2007.05.014 CrossRefPubMedGoogle Scholar
  50. Mali P, Chou BK, Yen J, Ye Z, Zou J, Dowey S, Brodsky RA, Ohm JE, Yu W, Baylin SB, Yusa K, Bradley A, Meyers DJ, Mukherjee C, Cole PA, Cheng L (2010) Butyrate greatly enhances derivation of human induced pluripotent stem cells by promoting epigenetic remodeling and the expression of pluripotency-associated genes. Stem Cells 28(4):713–720.  https://doi.org/10.1002/stem.402 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Matano M, Date S, Shimokawa M, Takano A, Fujii M, Ohta Y, Watanabe T, Kanai T, Sato T (2015) Modeling colorectal cancer using CRISPR-Cas9-mediated engineering of human intestinal organoids. Nat Med 21(3):256–262.  https://doi.org/10.1038/nm.3802 CrossRefPubMedGoogle Scholar
  52. Mayshar Y, Ben-David U, Lavon N, Biancotti JC, Yakir B, Clark AT, Plath K, Lowry WE, Benvenisty N (2010) Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 7(4):521–531.  https://doi.org/10.1016/j.stem.2010.07.017 CrossRefPubMedGoogle Scholar
  53. Moad M, Pal D, Hepburn AC, Williamson SC, Wilson L, Lako M, Armstrong L, Hayward SW, Franco OE, Cates JM, Fordham SE, Przyborski S, Carr-Wilkinson J, Robson CN, Heer R (2013) A novel model of urinary tract differentiation, tissue regeneration, and disease: reprogramming human prostate and bladder cells into induced pluripotent stem cells. Eur Urol 64(5):753–761.  https://doi.org/10.1016/j.eururo.2013.03.054 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Moretti A, Bellin M, Welling A, Jung CB, Lam JT, Bott-Flugel L, Dorn T, Goedel A, Hohnke C, Hofmann F, Seyfarth M, Sinnecker D, Schomig A, Laugwitz KL (2010) Patient-specific induced pluripotent stem-cell models for long-QT syndrome. N Engl J Med 363(15):1397–1409.  https://doi.org/10.1056/NEJMoa0908679 CrossRefPubMedGoogle Scholar
  55. Mulero-Navarro S, Sevilla A, Roman AC, Lee DF, D’Souza SL, Pardo S, Riess I, Su J, Cohen N, Schaniel C, Rodriguez NA, Baccarini A, Brown BD, Cave H, Caye A, Strullu M, Yalcin S, Park CY, Dhandapany PS, Yongchao G, Edelmann L, Bahieg S, Raynal P, Flex E, Tartaglia M, Moore KA, Lemischka IR, Gelb BD (2015) Myeloid dysregulation in a human induced pluripotent stem cell model of PTPN11-Associated juvenile myelomonocytic leukemia. Cell Rep 13(3):504–515CrossRefGoogle Scholar
  56. Nagase H, Miyoshi Y, Horii A, Aoki T, Ogawa M, Utsunomiya J, Baba S, Sasazuki T, Nakamura Y (1992) Correlation between the location of germ-line mutations in the APC gene and the number of colorectal polyps in familial adenomatous polyposis patients. Cancer Res 52(14):4055–4057PubMedGoogle Scholar
  57. Nakagawa M, Koyanagi M, Tanabe K, Takahashi K, Ichisaka T, Aoi T, Okita K, Mochiduki Y, Takizawa N, Yamanaka S (2008) Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 26(1):101–106.  https://doi.org/10.1038/nbt1374 CrossRefPubMedGoogle Scholar
  58. Narsinh KH, Jia F, Robbins RC, Kay MA, Longaker MT, Wu JC (2011) Generation of adult human induced pluripotent stem cells using nonviral minicircle DNA vectors. Nat Protoc 6(1):78–88.  https://doi.org/10.1038/nprot.2010.173 CrossRefPubMedGoogle Scholar
  59. Nguyen HN, Byers B, Cord B, Shcheglovitov A, Byrne J, Gujar P, Kee K, Schule B, Dolmetsch RE, Langston W, Palmer TD, Pera RR (2011) LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 8(3):267–280.  https://doi.org/10.1016/j.stem.2011.01.013 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Noonan JA (1968) Hypertelorism with Turner phenotype. A new syndrome with associated congenital heart disease. Am J Dis Child 116(4):373–380CrossRefGoogle Scholar
  61. Nsair A, MacLellan WR (2011) Induced pluripotent stem cells for regenerative cardiovascular therapies and biomedical discovery. Adv Drug Deliv Rev 63(4–5):324–330.  https://doi.org/10.1016/j.addr.2011.01.013 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Oishi K, Zhang H, Gault WJ, Wang CJ, Tan CC, Kim IK, Ying H, Rahman T, Pica N, Tartaglia M, Mlodzik M, Gelb BD (2009) Phosphatase-defective LEOPARD syndrome mutations in PTPN11 gene have gain-of-function effects during Drosophila development. Hum Mol Genet 18(1):193–201.  https://doi.org/10.1093/hmg/ddn336 CrossRefPubMedGoogle Scholar
  63. Okita K, Nakagawa M, Hyenjong H, Ichisaka T, Yamanaka S (2008) Generation of mouse induced pluripotent stem cells without viral vectors. Science 322(5903):949–953.  https://doi.org/10.1126/science.1164270 CrossRefPubMedGoogle Scholar
  64. Papapetrou EP (2016) Patient-derived induced pluripotent stem cells in cancer research and precision oncology. Nat Med 22(12):1392–1401.  https://doi.org/10.1038/nm.4238 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, Daley GQ (2008a) Disease-specific induced pluripotent stem cells. Cell 134(5):877–886.  https://doi.org/10.1016/j.cell.2008.07.041 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ (2008b) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451(7175):141–146.  https://doi.org/10.1038/nature06534 CrossRefPubMedGoogle Scholar
  67. Rashid ST, Corbineau S, Hannan N, Marciniak SJ, Miranda E, Alexander G, Huang-Doran I, Griffin J, Ahrlund-Richter L, Skepper J, Semple R, Weber A, Lomas DA, Vallier L (2010) Modeling inherited metabolic disorders of the liver using human induced pluripotent stem cells. J Clin Invest 120(9):3127–3136.  https://doi.org/10.1172/JCI43122 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Raya A, Rodriguez-Piza I, Guenechea G, Vassena R, Navarro S, Barrero MJ, Consiglio A, Castella M, Rio P, Sleep E, Gonzalez F, Tiscornia G, Garreta E, Aasen T, Veiga A, Verma IM, Surralles J, Bueren J, Izpisua Belmonte JC (2009) Disease-corrected haematopoietic progenitors from Fanconi anaemia induced pluripotent stem cells. Nature 460(7251):53–59.  https://doi.org/10.1038/nature08129 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Richard JP, Maragakis NJ (2015) Induced pluripotent stem cells from ALS patients for disease modeling. Brain Res 1607:15–25.  https://doi.org/10.1016/j.brainres.2014.09.017 CrossRefPubMedGoogle Scholar
  70. Roberts AE, Allanson JE, Tartaglia M, Gelb BD (2013) Noonan syndrome. Lancet 381(9863):333–342.  https://doi.org/10.1016/S0140-6736(12)61023-X CrossRefPubMedPubMedCentralGoogle Scholar
  71. Rowley JD (1973) Letter: a new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 243(5405):290–293CrossRefGoogle Scholar
  72. Sancho-Martinez I, Nivet E, Xia Y, Hishida T, Aguirre A, Ocampo A, Ma L, Morey R, Krause MN, Zembrzycki A, Ansorge O, Vazquez-Ferrer E, Dubova I, Reddy P, Lam D, Hishida Y, Wu MZ, Esteban CR, O’Leary D, Wahl GM, Verma IM, Laurent LC, Izpisua Belmonte JC (2016) Establishment of human iPSC-based models for the study and targeting of glioma initiating cells. Nat Commun 7:10743.  https://doi.org/10.1038/ncomms10743 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Schwank G, Koo BK, Sasselli V, Dekkers JF, Heo I, Demircan T, Sasaki N, Boymans S, Cuppen E, van der Ent CK, Nieuwenhuis EE, Beekman JM, Clevers H (2013) Functional repair of CFTR by CRISPR/Cas9 in intestinal stem cell organoids of cystic fibrosis patients. Cell Stem Cell 13(6):653–658.  https://doi.org/10.1016/j.stem.2013.11.002 CrossRefGoogle Scholar
  74. Seki T, Yuasa S, Oda M, Egashira T, Yae K, Kusumoto D, Nakata H, Tohyama S, Hashimoto H, Kodaira M, Okada Y, Seimiya H, Fusaki N, Hasegawa M, Fukuda K (2010) Generation of induced pluripotent stem cells from human terminally differentiated circulating T cells. Cell Stem Cell 7(1):11–14.  https://doi.org/10.1016/j.stem.2010.06.003 CrossRefPubMedGoogle Scholar
  75. Serwold T, Hochedlinger K, Inlay MA, Jaenisch R, Weissman IL (2007) Early TCR expression and aberrant T cell development in mice with endogenous prerearranged T cell receptor genes. J Immunol 179(2):928–938CrossRefGoogle Scholar
  76. Sexton AN, Regalado SG, Lai CS, Cost GJ, O’Neil CM, Urnov FD, Gregory PD, Jaenisch R, Collins K, Hockemeyer D (2014) Genetic and molecular identification of three human TPP1 functions in telomerase action: recruitment, activation, and homeostasis set point regulation. Genes Dev 28(17):1885–1899.  https://doi.org/10.1101/gad.246819.114 CrossRefPubMedPubMedCentralGoogle Scholar
  77. Soldner F, Laganiere J, Cheng AW, Hockemeyer D, Gao Q, Alagappan R, Khurana V, Golbe LI, Myers RH, Lindquist S, Zhang L, Guschin D, Fong LK, Vu BJ, Meng X, Urnov FD, Rebar EJ, Gregory PD, Zhang HS, Jaenisch R (2011) Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146(2):318–331.  https://doi.org/10.1016/j.cell.2011.06.019 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Soyombo AA, Wu Y, Kolski L, Rios JJ, Rakheja D, Chen A, Kehler J, Hampel H, Coughran A, Ross TS (2013) Analysis of induced pluripotent stem cells from a BRCA1 mutant family. Stem Cell Rep 1(4):336–349.  https://doi.org/10.1016/j.stemcr.2013.08.004 CrossRefGoogle Scholar
  79. Sperling AS, Gibson CJ, Ebert BL (2017) The genetics of myelodysplastic syndrome: from clonal haematopoiesis to secondary leukaemia. Nat Rev Cancer 17(1):5–19.  https://doi.org/10.1038/nrc.2016.112 CrossRefPubMedGoogle Scholar
  80. Stadtfeld M, Hochedlinger K (2010) Induced pluripotency: history, mechanisms, and applications. Genes Dev 24(20):2239–2263.  https://doi.org/10.1101/gad.1963910 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Stadtfeld M, Nagaya M, Utikal J, Weir G, Hochedlinger K (2008) Induced pluripotent stem cells generated without viral integration. Science 322(5903):945–949.  https://doi.org/10.1126/science.1162494 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Stricker SH, Feber A, Engstrom PG, Caren H, Kurian KM, Takashima Y, Watts C, Way M, Dirks P, Bertone P, Smith A, Beck S, Pollard SM (2013) Widespread resetting of DNA methylation in glioblastoma-initiating cells suppresses malignant cellular behavior in a lineage-dependent manner. Genes Dev 27(6):654–669.  https://doi.org/10.1101/gad.212662.112 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Subramanyam D, Lamouille S, Judson RL, Liu JY, Bucay N, Derynck R, Blelloch R (2011) Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol 29(5):443–448.  https://doi.org/10.1038/nbt.1862 CrossRefPubMedPubMedCentralGoogle Scholar
  84. Suknuntha K, Ishii Y, Tao L, Hu K, McIntosh BE, Yang D, Swanson S, Stewart R, Wang JYJ, Thomson J, Slukvin I (2015) Discovery of survival factor for primitive chronic myeloid leukemia cells using induced pluripotent stem cells. Stem Cell Res 15(3):678–693.  https://doi.org/10.1016/j.scr.2015.10.015 CrossRefPubMedPubMedCentralGoogle Scholar
  85. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676CrossRefGoogle Scholar
  86. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872.  https://doi.org/10.1016/j.cell.2007.11.019 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Tu J, Huo Z, Liu M, Wang D, Xu A, Zhou R, Zhu D, Gingold J, Shen J, Zhao R, Lee DF (2018) Generation of human embryonic stem cell line with heterozygous RB1 deletion by CRIPSR/Cas9 nickase. Stem Cell Res 28:29–32.  https://doi.org/10.1016/j.scr.2018.01.021 CrossRefPubMedPubMedCentralGoogle Scholar
  88. Turner N, Tutt A, Ashworth A (2004) Hallmarks of ‘BRCAness’ in sporadic cancers. Nat Rev Cancer 4(10):814–819.  https://doi.org/10.1038/nrc1457 CrossRefPubMedGoogle Scholar
  89. Visvader JE (2011) Cells of origin in cancer. Nature 469(7330):314–322.  https://doi.org/10.1038/nature09781 CrossRefPubMedGoogle Scholar
  90. Vizcardo R, Masuda K, Yamada D, Ikawa T, Shimizu K, Fujii S, Koseki H, Kawamoto H (2013) Regeneration of human tumor antigen-specific T cells from iPSCs derived from mature CD8(+) T cells. Cell Stem Cell 12(1):31–36.  https://doi.org/10.1016/j.stem.2012.12.006 CrossRefPubMedGoogle Scholar
  91. Warren L, Manos PD, Ahfeldt T, Loh YH, Li H, Lau F, Ebina W, Mandal PK, Smith ZD, Meissner A, Daley GQ, Brack AS, Collins JJ, Cowan C, Schlaeger TM, Rossi DJ (2010) Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 7(5):618–630.  https://doi.org/10.1016/j.stem.2010.08.012 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M, Hochedlinger K, Bernstein BE, Jaenisch R (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448(7151):318–324.  https://doi.org/10.1038/nature05944 CrossRefPubMedGoogle Scholar
  93. Woltjen K, Michael IP, Mohseni P, Desai R, Mileikovsky M, Hamalainen R, Cowling R, Wang W, Liu P, Gertsenstein M, Kaji K, Sung HK, Nagy A (2009) piggyBac transposition reprograms fibroblasts to induced pluripotent stem cells. Nature 458(7239):766–770.  https://doi.org/10.1038/nature07863 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Xu A, Zhou R, Tu J, Huo Z, Zhu D, Wang D, Gingold JA, Mata H, Rao PH, Liu M, Mohamed AMT, Kong CSL, Jewell BE, Xia W, Zhao R, Hung MC, Lee DF (2018) Establishment of a human embryonic stem cell line with homozygous TP53 R248W mutant by TALEN mediated gene editing. Stem Cell Res 29:215–219.  https://doi.org/10.1016/j.scr.2018.04.013 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Yamanaka S (2010) Patient-specific pluripotent stem cells become even more accessible. Cell Stem Cell 7(1):1–2.  https://doi.org/10.1016/j.stem.2010.06.009 CrossRefPubMedGoogle Scholar
  96. Yazawa M, Hsueh B, Jia X, Pasca AM, Bernstein JA, Hallmayer J, Dolmetsch RE (2011) Using induced pluripotent stem cells to investigate cardiac phenotypes in Timothy syndrome. Nature 471(7337):230–234.  https://doi.org/10.1038/nature09855 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Yi F, Liu GH, Izpisua Belmonte JC (2012) Human induced pluripotent stem cells derived hepatocytes: rising promise for disease modeling, drug development and cell therapy. Protein Cell 3(4):246–250.  https://doi.org/10.1007/s13238-012-2918-4 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Ying H, Dey P, Yao W, Kimmelman AC, Draetta GF, Maitra A, Depinho RA (2016) Genetics and biology of pancreatic ductal adenocarcinoma. Genes Dev 30(4):355–385.  https://doi.org/10.1101/gad.275776.115 CrossRefPubMedPubMedCentralGoogle Scholar
  99. Yoshida Y, Yamanaka S (2010) Recent stem cell advances: induced pluripotent stem cells for disease modeling and stem cell-based regeneration. Circulation 122(1):80–87.  https://doi.org/10.1161/CIRCULATIONAHA.109.881433 CrossRefPubMedGoogle Scholar
  100. Young MA, Larson DE, Sun CW, George DR, Ding L, Miller CA, Lin L, Pawlik KM, Chen K, Fan X, Schmidt H, Kalicki-Veizer J, Cook LL, Swift GW, Demeter RT, Wendl MC, Sands MS, Mardis ER, Wilson RK, Townes TM, Ley TJ (2012) Background mutations in parental cells account for most of the genetic heterogeneity of induced pluripotent stem cells. Cell Stem Cell 10(5):570–582.  https://doi.org/10.1016/j.stem.2012.03.002 CrossRefPubMedPubMedCentralGoogle Scholar
  101. 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 (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920.  https://doi.org/10.1126/science.1151526 CrossRefGoogle Scholar
  102. Zhang X, Cruz FD, Terry M, Remotti F, Matushansky I (2013) Terminal differentiation and loss of tumorigenicity of human cancers via pluripotency-based reprogramming. Oncogene 32(18):2249–2260., 2260 e2241–2221.  https://doi.org/10.1038/onc.2012.237 CrossRefPubMedGoogle Scholar
  103. Zhao Y, Yin X, Qin H, Zhu F, Liu H, Yang W, Zhang Q, Xiang C, Hou P, Song Z, Liu Y, Yong J, Zhang P, Cai J, Liu M, Li H, Li Y, Qu X, Cui K, Zhang W, Xiang T, Wu Y, Zhao Y, Liu C, Yu C, Yuan K, Lou J, Ding M, Deng H (2008) Two supporting factors greatly improve the efficiency of human iPSC generation. Cell Stem Cell 3(5):475–479.  https://doi.org/10.1016/j.stem.2008.10.002 CrossRefPubMedGoogle Scholar
  104. Zhao T, Zhang ZN, Rong Z, Xu Y (2011) Immunogenicity of induced pluripotent stem cells. Nature 474(7350):212–215.  https://doi.org/10.1038/nature10135 CrossRefPubMedGoogle Scholar
  105. Zhou W, Freed CR (2009) Adenoviral gene delivery can reprogram human fibroblasts to induced pluripotent stem cells. Stem Cells 27(11):2667–2674.  https://doi.org/10.1002/stem.201 CrossRefPubMedGoogle Scholar
  106. Zhou H, Wu S, Joo JY, Zhu S, Han DW, Lin T, Trauger S, Bien G, Yao S, Zhu Y, Siuzdak G, Scholer HR, Duan L, Ding S (2009) Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4(5):381–384.  https://doi.org/10.1016/j.stem.2009.04.005 CrossRefPubMedGoogle Scholar
  107. Zhou R, Xu A, Gingold J, Strong LC, Zhao R, Lee DF (2017) Li-Fraumeni syndrome disease model: a platform to develop precision Cancer therapy targeting oncogenic p53. Trends Pharmacol Sci 38(10):908–927.  https://doi.org/10.1016/j.tips.2017.07.004 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Zhou R, Xu A, Wang D, Zhu D, Mata H, Huo Z, Tu J, Liu M, Mohamed AMT, Jewell BE, Gingold J, Xia W, Rao PH, Hung MC, Zhao R, Lee DF (2018) A homozygous p53 R282W mutant human embryonic stem cell line generated using TALEN-mediated precise gene editing. Stem Cell Res 27:131–135.  https://doi.org/10.1016/j.scr.2018.01.035 CrossRefPubMedGoogle Scholar
  109. Zwaan CM, Kolb EA, Reinhardt D, Abrahamsson J, Adachi S, Aplenc R, De Bont ES, De Moerloose B, Dworzak M, Gibson BE, Hasle H, Leverger G, Locatelli F, Ragu C, Ribeiro RC, Rizzari C, Rubnitz JE, Smith OP, Sung L, Tomizawa D, van den Heuvel-Eibrink MM, Creutzig U, Kaspers GJ (2015) Collaborative efforts driving progress in pediatric acute myeloid leukemia. J Clin Oncol 33(27):2949–2962.  https://doi.org/10.1200/JCO.2015.62.8289 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Department of Integrative Biology and Pharmacology, McGovern Medical SchoolThe University of Texas Health Science Center at HoustonHoustonUSA
  2. 2.Women’s Health Institute, Cleveland Clinic FoundationClevelandUSA
  3. 3.The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical SciencesHoustonUSA
  4. 4.Center for Stem Cell and Regenerative Medicine, The Brown Foundation Institute of Molecular Medicine for the Prevention of Human DiseasesThe University of Texas Health Science Center at HoustonHoustonUSA
  5. 5.Center for Precision Health, School of Biomedical Informatics and School of Public HealthThe University of Texas Health Science Center at HoustonHoustonUSA

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