Cellular reprogramming: A small molecule perspective

Current Opinion in Cell Biology

Volumn 24, Issue 6, 2012, Pages 784-792

  Nie, Baoming ^a   Wang, Haixia ^a   Laurent, Timothy ^a   Ding, Sheng ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 [3 (1 ADAMANTYL) 4 HYDROXYPHENYL] 2 NAPHTHOIC ACID; KRUPPEL LIKE FACTOR 4; LIVER RECEPTOR HOMOLOG 1; MICRORNA; NUCLEAR RECEPTOR ESRRB; OCTAMER TRANSCRIPTION FACTOR 4; ORPHAN NUCLEAR RECEPTOR; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG;

CELL AGING; CELL LINEAGE; CELL STRESS; CHROMATIN ASSEMBLY AND DISASSEMBLY; COPY NUMBER VARIATION; DNA DAMAGE; DNA REPAIR; EMBRYONIC STEM CELL; EPIGENETICS; EPITHELIAL MESENCHYMAL TRANSITION; GLYCOLYSIS; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SOMATIC CELL;

ANIMALS; CELL AGING; CELL LINEAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; EPITHELIAL-MESENCHYMAL TRANSITION; GLYCOLYSIS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; NUCLEAR REPROGRAMMING; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

HARNESS;

EID: 84871935467     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2012.08.010     Document Type: Review

References (73)

1. Okita K., Matsumura Y., Sato Y., Okada A., Morizane A., Okamoto S., Hong H., Nakagawa M., Tanabe K., Tezuka K. A more efficient method to generate integration-free human iPS cells. Nat Methods 2011, 8:409-412.
2. Zhou H., Wu S., Joo J.Y., Zhu S., Han D.W., Lin T., Trauger S., Bien G., Yao S., Zhu Y., et al. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 2009, 4:381-384.
3. Kim D., Kim C.H., Moon J.I., Chung Y.G., Chang M.Y., Han B.S., Ko S., Yang E., Cha K.Y., Lanza R., et al. Generation of human induced pluripotent stem cells by direct delivery of reprogramming proteins. Cell Stem Cell 2009, 4:472-476.
4. Warren L., Manos P.D., Ahfeldt T., Loh Y.H., Li H., Lau F., Ebina W., Mandal P.K., Smith Z.D., Meissner A. Highly efficient reprogramming to pluripotency and directed differentiation of human cells with synthetic modified mRNA. Cell Stem Cell 2010, 7:618-630.
5. Ohi Y., Qin H., Hong C., Blouin L., Polo J.M., Guo T., Qi Z., Downey S.L., Manos P.D., Rossi D.J. Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat Cell Biol 2011, 13:541-549.
6. Xu H., Yi B.A., Wu H., Bock C., Gu H., Lui K.O., Park J.-H.C., Shao Y., Riley A.K., Domian I.J., et al. Highly efficient derivation of ventricular cardiomyocytes from induced pluripotent stem cells with a distinct epigenetic signature. Cell Res 2012, 22:142-154.
7. Bar-Nur O., Russ Holger A., Efrat S., Benvenisty N. Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell 2011, 9:17-23.
8. Lee S.B., Seo D., Choi D., Park K.-Y., Holczbauer A., Marquardt J.U., Conner E.A., Factor V.M., Thorgeirsson S.S. Contribution of hepatic lineage stage-specific donor memory to the differential potential of induced mouse pluripotent stem cells. Stem Cells 2012, 30:997-1007.
9. Lister R., Pelizzola M., Kida Y.S., Hawkins R.D., Nery J.R., Hon G., Antosiewicz-Bourget J., O'Malley R., Castanon R., Klugman S., et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 2011, 471:68-73.
10. Marion R.M., Strati K., Li H., Murga M., Blanco R., Ortega S., Fernandez-Capetillo O., Serrano M., Blasco M.A. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009, 460:1149-1153.
11. Ramos-Mejia V., Munoz-Lopez M., Garcia-Perez J.L., Menendez P. iPSC lines that do not silence the expression of the ectopic reprogramming factors may display enhanced propensity to genomic instability. Cell Res 2010, 20:1092-1095.
12. Pasi C.E., Dereli-Oz A., Negrini S., Friedli M., Fragola G., Lombardo A., Van Houwe G., Naldini L., Casola S., Testa G., et al. Genomic instability in induced stem cells. Cell Death Differ 2011, 18:745-753.
13. Hussein S.M., Batada N.N., Vuoristo S., Ching R.W., Autio R., Narva E., Ng S., Sourour M., Hamalainen R., Olsson C., et al. Copy number variation and selection during reprogramming to pluripotency. Nature 2011, 471:58-62.
14. Gore A., Li Z., Fung H.L., Young J.E., Agarwal S., Antosiewicz-Bourget J., Canto I., Giorgetti A., Israel M.A., Kiskinis E., et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011, 471:63-67.
15. Laurent L.C., Ulitsky I., Slavin I., Tran H., Schork A., Morey R., Lynch C., Harness J.V., Lee S., Barrero M.J., et al. 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.
16. Li W., Jiang K., Ding S. Concise review: a chemical approach to control cell fate and function. Stem Cells 2012, 30:61-68.
17. Zhu S.Y., Wei W.G., Ding S. Chemical strategies for stem cell biology and regenerative medicine. Annu Rev Biomed Eng 2011, 13:73-90.
18. Feng B., Ng J.H., Heng J.C., Ng H.H. Molecules that promote or enhance reprogramming of somatic cells to induced pluripotent stem cells. Cell Stem Cell 2009, 4:301-312.
19. Li R., Liang J., Ni S., Zhou T., Qing X., Li H., He W., Chen J., Li F., Zhuang Q., et al. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010, 7:51-63.
20. Samavarchi-Tehrani P., Golipour A., David L., Sung H.K., Beyer T.A., Datti A., Woltjen K., Nagy A., Wrana J.L. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell 2010, 7:64-77.
21. Lin T., Ambasudhan R., Yuan X., Li W., Hilcove S., Abujarour R., Lin X., Hahm H.S., Hao E., Hayek A., et al. A chemical platform for improved induction of human iPSCs. Nat Methods 2009, 6:805-808.
22. Xu Y., Zhu X., Hahm H.S., Wei W., Hao E., Hayek A., Ding S. Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci U S A 2010, 107:8129-8134.
23. Ichida J.K., Blanchard J., Lam K., Son E.Y., Chung J.E., Egli D., Loh K.M., Carter A.C., Di Giorgio F.P., Koszka K., et al. A small-molecule inhibitor of tgf-Beta signaling replaces sox2 in reprogramming by inducing nanog. Cell Stem Cell 2009, 5:491-503.
24. Subramanyam D., Lamouille S., Judson R.L., Liu J.Y., Bucay N., Derynck R., Blelloch R. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells. Nat Biotechnol 2011, 29:443-448.
25. Utikal J., Polo J.M., Stadtfeld M., Maherali N., Kulalert W., Walsh R.M., Khalil A., Rheinwald J.G., Hochedlinger K. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 2009, 460:1145-1148.
26. 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. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 2009, 23:2134-2139.
27. Esteban M.A., Wang T., Qin B., Yang J., Qin D., Cai J., Li W., Weng Z., Chen J., Ni S., et al. Vitamin C enhances the generation of mouse and human induced pluripotent stem cells. Cell Stem Cell 2010, 6:71-79.
28. Wang T., Chen K., Zeng X., Yang J., Wu Y., Shi X., Qin B., Zeng L., Esteban M.A., Pan G., et al. The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell 2011, 9:575-587.
29. Zhu S., Li W., Zhou H., Wei W., Ambasudhan R., Lin T., Kim J., Zhang K., Ding S. Reprogramming of human primary somatic cells by OCT4 and chemical compounds. Cell Stem Cell 2010, 7:651-655.
30. Zhang J., Khvorostov I., Hong J.S., Oktay Y., Vergnes L., Nuebel E., Wahjudi P.N., Setoguchi K., Wang G., Do A., et al. UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 2011, 30:4860-4873.
31. Muller L.U., Milsom M.D., Harris C.E., Vyas R., Brumme K.M., Parmar K., Moreau L.A., Schambach A., Park I.H., London W.B., et al. Overcoming reprogramming resistance of Fanconi anemia cells. Blood 2012, 119:5449-5457.
32. Cheng L., Hansen N.F., Zhao L., Du Y., Zou C., Donovan F.X., Chou B.K., Zhou G., Li S., Dowey S.N., et al. Low incidence of DNA sequence variation in human induced pluripotent stem cells generated by nonintegrating plasmid expression. Cell Stem Cell 2012, 10:337-344.
33. Prigione A., Lichtner B., Kuhl H., Struys E.A., Wamelink M., Lehrach H., Ralser M., Timmermann B., Adjaye J. Human induced pluripotent stem cells harbor homoplasmic and heteroplasmic mitochondrial DNA Mutations while maintaining human embryonic stem cell-like metabolic reprogramming. Stem Cells 2011, 29:1338-1348.
34. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., He C., Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
35. Koh K.P., Yabuuchi A., Rao S., Huang Y., Cunniff K., Nardone J., Laiho A., Tahiliani M., Sommer C.A., Mostoslavsky G., et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011, 8:200-213.
36. Fong Y.W., Inouye C., Yamaguchi T., Cattoglio C., Grubisic I., Tjian R. A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells. Cell 2011, 147:120-131.
37. Meshorer E., Misteli T. Chromatin in pluripotent embryonic stem cells and differentiation. Nat Rev Mol Cell Biol 2006, 7:540-546.
38. Gaspar-Maia A., Alajem A., Polesso F., Sridharan R., Mason M.J., Heidersbach A., Ramalho-Santos J., McManus M.T., Plath K., Meshorer E., et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 2009, 460:863-868.
39. Singhal N., Graumann J., Wu G.M., Arauzo-Bravo M.J., Han D.W., Greber B., Gentile L., Mann M., Scholer H.R. Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 2010, 141:943-955.
40. Stadtfeld M., Apostolou E., Akutsu H., Fukuda A., Follett P., Natesan S., Kono T., Shioda T., Hochedlinger K. Aberrant silencing of imprinted genes on chromosome 12qF1 in mouse induced pluripotent stem cells. Nature 2010, 465:175-181.
41. Liu L., Luo G.Z., Yang W., Zhao X., Zheng Q., Lv Z., Li W., Wu H.J., Wang L., Wang X.J., et al. Activation of the imprinted Dlk1-Dio3 region correlates with pluripotency levels of mouse stem cells. J Biol Chem 2010, 285:19483-19490.
42. Carey B.W., Markoulaki S., Hanna J.H., Faddah D.A., Buganim Y., Kim J., Ganz K., Steine E.J., Cassady J.P., Creyghton M.P., et al. Reprogramming factor stoichiometry influences the epigenetic state and biological properties of induced pluripotent stem cells. Cell Stem Cell 2011, 9:588-598.
43. Stadtfeld M., Apostolou E., Ferrari F., Choi J., Walsh R.M., Chen T., Oi S., Kim S.Y., Bestor T., Shioda T., et al. Ascorbic acid prevents loss of Dlk1-Dio3 imprinting and facilitates generation of all-iPS cell mice from terminally differentiated B cells. Nat Genet 2012, 44:398-405.
44. Yuan X., Wan H., Zhao X., Zhu S., Zhou Q., Ding S. Brief report: combined chemical treatment enables Oct4-induced reprogramming from mouse embryonic fibroblasts. Stem Cells 2011, 29:549-553.
45. Li Y.Q., Zhang Q.A., Yin X.L., Yang W.F., Du Y.Y., Hou P.P., Ge J.A., Liu C., Zhang W.Q., Zhang X., et al. Generation of iPSCs from mouse fibroblasts with a single gene, Oct4, and small molecules. Cell Res 2011, 21:196-204.
46. Heng J.C.D., Feng B., Han J.Y., Jiang J.M., Kraus P., Ng J.H., Orlov Y.L., Huss M., Yang L., Lufkin T., et al. The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 2010, 6:167-174.
47. Mullen E.M., Gu P., Cooney A.J. Nuclear receptors in regulation of mouse ES cell pluripotency and differentiation. PPAR Res 2007, 2007:61563.
48. Wang W., Yang J., Liu H., Lu D., Chen X.F., Zenonos Z., Campos L.S., Rad R., Guo G., Zhang S.J., et al. Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1. Proc Natl Acad Sci U S A 2011, 108:18283-18288.
49. Ivanova N., Dobrin R., Lu R., Kotenko I., Levorse J., DeCoste C., Schafer X., Lun Y., Lemischka I.R. Dissecting self-renewal in stem cells with RNA interference. Nature 2006, 442:533-538.
50. Feng B., Jiang J., Kraus P., Ng J.H., Heng J.C., Chan Y.S., Yaw L.P., Zhang W., Loh Y.H., Han J., et al. Reprogramming of fibroblasts into induced pluripotent stem cells with orphan nuclear receptor Esrrb. Nat Cell Biol 2009, 11:197-203.
51. Davis R.L., Weintraub H., Lassar A.B. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 1987, 51:987-1000.
52. Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Sudhof T.C., Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
53. Yoo A.S., Sun A.X., Li L., Shcheglovitov A., Portmann T., Li Y., Lee-Messer C., Dolmetsch R.E., Tsien R.W., Crabtree G.R. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 2011, 476:228-231.
54. Pang Z.P., Yang N., Vierbuchen T., Ostermeier A., Fuentes D.R., Yang T.Q., Citri A., Sebastiano V., Marro S., Sudhof T.C., et al. Induction of human neuronal cells by defined transcription factors. Nature 2011, 476:220-223.
55. Ambasudhan R., Talantova M., Coleman R., Yuan X., Zhu S., Lipton S.A., Ding S. Direct reprogramming of adult human fibroblasts to functional neurons under defined conditions. Cell Stem Cell 2011, 9:113-118.
56. Pfisterer U., Kirkeby A., Torper O., Wood J., Nelander J., Dufour A., Bjorklund A., Lindvall O., Jakobsson J., Parmar M. Direct conversion of human fibroblasts to dopaminergic neurons. Proc Natl Acad Sci U S A 2011, 108:10343-10348.
57. Caiazzo M., Dell'Anno M.T., Dvoretskova E., Lazarevic D., Taverna S., Leo D., Sotnikova T.D., Menegon A., Roncaglia P., Colciago G., et al. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 2011, 476:224-227.
58. Son E.Y., Ichida J.K., Wainger B.J., Toma J.S., Rafuse V.F., Woolf C.J., Eggan K. Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 2011, 9:205-218.
59. Qiang L., Fujita R., Yamashita T., Angulo S., Rhinn H., Rhee D., Doege C., Chau L., Aubry L., Vanti W.B., et al. Directed conversion of Alzheimer's disease patient skin fibroblasts into functional neurons. Cell 2011, 146:359-371.
60. Ieda M., Fu J.D., Delgado-Olguin P., Vedantham V., Hayashi Y., Bruneau B.G., Srivastava D. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010, 142:375-386.
61. Song K., Nam Y.J., Luo X., Qi X., Tan W., Huang G.N., Acharya A., Smith C.L., Tallquist M.D., Neilson E.G., et al. Heart repair by reprogramming non-myocytes with cardiac transcription factors. Nature 2012, 485:599-604.
62. Feng R., Desbordes S.C., Xie H., Tillo E.S., Pixley F., Stanley E.R., Graf T. PU.1 and C/EBPalpha/beta convert fibroblasts into macrophage-like cells. Proc Natl Acad Sci U S A 2008, 105:6057-6062.
63. Huang P., He Z., Ji S., Sun H., Xiang D., Liu C., Hu Y., Wang X., Hui L. Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 2011, 475:386-389.
64. Sekiya S., Suzuki A. Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 2011, 475:390-393.
65. Pournasr B., Khaloughi K., Salekdeh G.H., Totonchi M., Shahbazi E., Baharvand H. Concise review: alchemy of biology: generating desired cell types from abundant and accessible cells. Stem Cells 2011, 29:1933-1941.
66. Graf T. Historical origins of transdifferentiation and reprogramming. Cell Stem Cell 2011, 9:504-516.
67. Zhou Q., Brown J., Kanarek A., Rajagopal J., Melton D.A. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008, 455:627-632.
68. Qian L., Huang Y., Spencer C.I., Foley A., Vedantham V., Liu L., Conway S.J., Fu J.D., Srivastava D. In vivo reprogramming of murine cardiac fibroblasts into induced cardiomyocytes. Nature 2012, 485:593-598.
69. Ladewig J., Mertens J., Kesavan J., Doerr J., Poppe D., Glaue F., Herms S., Wernet P., Kogler G., Muller F.J., et al. Small molecules enable highly efficient neuronal conversion of human fibroblasts. Nat Methods 2012, 9:575-578.
70. Efe J.A., Hilcove S., Kim J., Zhou H., Ouyang K., Wang G., Chen J., Ding S. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol 2011, 13:215-222.
71. Kim J., Efe J.A., Zhu S., Talantova M., Yuan X., Wang S., Lipton S.A., Zhang K., Ding S. Direct reprogramming of mouse fibroblasts to neural progenitors. Proc Natl Acad Sci U S A 2011, 108:7838-7843.
72. Thier M., Worsdorfer P., Lakes Y.B., Gorris R., Herms S., Opitz T., Seiferling D., Quandel T., Hoffmann P., Nothen M.M., et al. Direct conversion of fibroblasts into stably expandable neural stem cells. Cell Stem Cell 2012, 10:473-479.
73. Han D.W., Tapia N., Hermann A., Hemmer K., Hoing S., Arauzo-Bravo M.J., Zaehres H., Wu G., Frank S., Moritz S., et al. Direct reprogramming of fibroblasts into neural stem cells by defined factors. Cell Stem Cell 2012, 10:465-472.