Myc maintains embryonic stem cell pluripotency and self-renewal

Differentiation

Volumn 80, Issue 1, 2010, Pages 9-19

  Varlakhanova, Natalia V ^a,b   Cotterman, Rebecca F ^a,b   deVries, Wilhelmine N ^c   Morgan, Judy ^c   Donahue, Leah Rae ^c   Murray, Stephen ^c   Knowles, Barbara B ^d   Knoepfler, Paul S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SHRINERS HOSPITALS FOR CHILDREN NORTHERN CALIFORNIA   (United States)

^c JACKSON LABORATORY   (United States)

^d INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

Author keywords

Embryonic stem cells; iPS cells; Myc; Pluripotency; Self renewal

Indexed keywords

MYC PROTEIN; BIOLOGICAL MARKER; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, MOUSE; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL RENEWAL; CELL SURVIVAL; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; GENETIC TRANSDUCTION; GENOTYPE; HOMOZYGOSITY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; ANIMAL EMBRYO; CELL PROLIFERATION; CYTOLOGY; DNA MICROARRAY; EMBRYO DEVELOPMENT; ENZYME IMMUNOASSAY; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; ONCOGENE MYC; PHYSIOLOGY; REGENERATION; WESTERN BLOTTING;

ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; GENES, MYC; IMMUNOENZYME TECHNIQUES; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEINS C-MYC; REGENERATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

IPS; MURINAE;

EID: 77954142510     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1016/j.diff.2010.05.001     Document Type: Article

References (60)

1. Amanullah A., Liebermann D.A., Hoffman B. p53-independent apoptosis associated with c-Myc-mediated block in myeloid cell differentiation. Oncogene 2000, 19:2967-2977.
2. Ambros V. The functions of animal microRNAs. Nature 2004, 431:350-355.
3. Bechard M., Dalton S. Subcellular localization of glycogen synthase kinase 3beta controls embryonic stem cell self-renewal. Mol. Cell. Biol. 2009, 29:2092-2104.
4. Cai K.Q., Capo-Chichi C.D., Rula M.E., Yang D.H., Xu X.X. Dynamic GATA6 expression in primitive endoderm formation and maturation in early mouse embryogenesis. Dev. Dyn. 2008, 237:2820-2829.
5. Cartwright P., McLean C., Sheppard A., Rivett D., Jones K., Dalton S. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 2005, 132:885-896.
6. Chamberlain S.J., Yee D., Magnuson T. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 2008, 26:1496-1505.
7. Chang T.C., Yu D., Lee Y.S., Wentzel E.A., Arking D.E., West K.M., Dang C.V., Thomas-Tikhonenko A., Mendell J.T. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 2008, 40:43-50.
8. Charron J., Malynn B.A., Fisher P., Stewart V., Jeannotte L., Goff S.P., Robertson E.J., Alt F.W. Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes Dev. 1993, 6:2248-2257.
9. Chen C.Z., Li L., Lodish H.F., Bartel D.P. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004, 303:83-86.
10. Cotterman, R., Knoepfler, P.S., 2009. N-Myc regulates expression of pluripotency genes in neuroblastoma including lif, klf2, klf4, and lin28b. PLoS One 4, e5799.
11. Cotterman R., Jin V.X., Krig S.R., Lemen J.M., Wey A., Farnham P.J., Knoepfler P.S. N-Myc regulates a widespread euchromatic program in the human genome partially independent of its role as a classical transcription factor. Cancer Res. 2008, 68:9654-9662.
12. Davis A.C., Wims M., Spotts G.D., Hann S.R., Bradley A. A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev. 1993, 7:671-682.
13. de Alboran I.M., O'Hagan R.C., Gartner F., Malynn B., Davidson L., Rickert R., Rajewsky K., DePinho R.A., Alt F.W. Analysis of C-MYC function in normal cells via conditional gene- targeted mutation. Immunity 2001, 14:45-55.
14. Douglas N.C., Jacobs H., Bothwell A.L., Hayday A.C. Defining the specific physiological requirements for c-Myc in T cell development. Nat. Immunol. 2001, 2:307-315.
15. Dubois N.C., Adolphe C., Ehninger A., Wang R.A., Robertson E.J., Trumpp A. Placental rescue reveals a sole requirement for c-Myc in embryonic erythroblast survival and hematopoietic stem cell function. Development 2008, 135:2455-2465.
16. Gaspar-Maia A., Alajem A., Polesso F., Sridharan R., Mason M.J., Heidersbach A., Ramalho-Santos J., McManus M.T., Plath K., Meshorer E., Ramalho-Santos M. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 2009, 460:863-868.
17. Gibson J.D., Jakuba C.M., Boucher N., Holbrook K.A., Carter M.G., Nelson C.E. Single-cell transcript analysis of human embryonic stem cells. Integr. Biol. (Cambridge) 2009, 1:540-551.
18. Gradwohl G., Dierich A., LeMeur M., Guillemot F. Neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proc. Natl. Acad. Sci. USA 2000, 97:1607-1611.
19. Guccione E., Martinato F., Finocchiaro G., Luzi L., Tizzoni L., Dall' Olio V., Zardo G., Nervi C., Bernard L., Amati B. Myc-binding-site recognition in the human genome is determined by chromatin context. Nat. Cell Biol. 2006, 8:764-770.
20. Hann S.R., Eisenman R.N. Proteins encoded by the human c-myc oncogene: differential expression in neoplastic cells. Mol. Cell Biol. 1984, 4:2486-2497.
21. Hatton K.S., Mahon K., Chin L., Chiu F.C., Lee H.W., Peng D., Morgenbesser S.D., Horner J., DePinho R.A. Expression and activity of L-myc in normal mouse development. Mol. Cell. Biol. 1996, 16:1794-1804.
22. He T.-C., Sparks A.B., Rago C., Hermeking H., Zawel L., Da Costa L.T., Morin P.J., Vogelstein B., Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 1998, 281:1509-1512.
23. Hoebeeck J., Speleman F., Vandesompele J. Real-time quantitative PCR as an alternative to Southern blot or fluorescence in situ hybridization for detection of gene copy number changes. Methods Mol. Biol. 2007, 353:205-226.
24. Ivey K.N., Muth A., Arnold J., King F.W., Yeh R.F., Fish J.E., Hsiao E.C., Schwartz R.J., Conklin B.R., Bernstein H.S., Srivastava D. MicroRNA regulation of cell lineages in mouse and human embryonic stem cells. Cell Stem Cell 2008, 2:219-229.
25. Knoepfler P.S., Cheng P.F., Eisenman R.N. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev. 2002, 16:2699-2712.
26. Knoepfler P.S., Zhang X.Y., Cheng P.F., Gafken P.R., McMahon S.B., Eisenman R.N. Myc influences global chromatin structure. Embo J. 2006, 25:2723-2734.
27. Krichevsky A.M., Sonntag K.C., Isacson O., Kosik K.S. Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 2006, 24:857-864.
28. Laurenti E., Varnum-Finney B., Wilson A., Ferrero I., Blanco-Bose W.E., Ehninger A., Knoepfler P.S., Cheng P.F., MacDonald H.R., Eisenman R.N., Bernstein I.D., Trumpp A. Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity. Cell Stem Cell 2008, 3:611-624.
29. Lin C.H., Jackson A.L., Guo J., Linsley P.S., Eisenman R.N. Myc-regulated microRNAs attenuate embryonic stem cell differentiation. EMBO J. 2009, 28:3157-3170.
30. Malynn B.A., de Alboran I.M., O'Hagan R.C., Bronson R., Davidson L., DePinho R.A., Alt F.W. N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation. Genes Dev. 2000, 14:1390-1399.
31. Marhin W.W., Chen J., Facchini L.M., Fornace A.J., Penn L.Z. Myc represses the growth arrest gene gadd45. Oncogene 1997, 14:2825-2834.
32. Marson A., Foreman R., Chevalier B., Bilodeau S., Kahn M., Young R.A., Jaenisch R. Wnt signaling promotes reprogramming of somatic cells to pluripotency. Cell Stem Cell 2008, 3:132-135.
33. Martinato F., Cesaroni M., Amati B., Guccione E. Analysis of Myc-induced histone modifications on target chromatin. PLoS One 2008, 3:e3650.
34. Meyer N., Penn L.Z. Reflecting on 25 years with MYC. Nat. Rev. Cancer 2008, 8:976-990.
35. Moens C.B., Auerbach A.B., Conlon R.A., Joyner A.L., Rossant J. A targeted mutation reveals a role for N-myc in branching morphogenesis in the embryonic mouse lung. Genes Dev. 1992, 6:691-704.
36. Morrisey E.E., Tang Z., Sigrist K., Lu M.M., Jiang F., Ip H.S., Parmacek M.S. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 1998, 12:3579-3590.
37. Murchison E.P., Partridge J.F., Tam O.H., Cheloufi S., Hannon G.J. Characterization of dicer-deficient murine embryonic stem cells. Proc. Natl. Acad. Sci. USA 2005, 102:12135-12140.
38. Nagy A., Moens C., Ivanyi E., Pawling J., Gertsenstein M., Hadjantonakis A.K., Pirity M., Rossant J. Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles. Curr. Biol. 1998, 8:661-664.
39. Nakagawa M., Koyanagi M., Tanabe K., Takahashi K., Ichisaka T., Aoi T., Okita K., Mochiduki Y., Takizawa N., Yamanaka S. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat. Biotechnol. 2008, 26:101-106.
40. O'Shea K.S. Self-renewal vs. differentiation of mouse embryonic stem cells. Biol. Reprod. 2004, 71:1755-1765.
41. Okita K., Ichisaka T., Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature 2007.
42. Peterkin T., Gibson A., Patient R. GATA-6 maintains BMP-4 and Nkx2 expression during cardiomyocyte precursor maturation. EMBO J. 2003, 22:4260-4273.
43. Sawai S., Shimono A., Hanaoka K., Kondoh H. Embryonic lethality resulting from disruption of both N-myc alleles in mouse zygotes. New Biol. 1991, 3:861-869.
44. Scandura J.M., Boccuni P., Massague J., Nimer S.D. Transforming growth factor beta-induced cell cycle arrest of human hematopoietic cells requires p57KIP2 up-regulation. Proc. Natl. Acad. Sci. USA 2004, 101:15231-15236.
45. Sridharan R., Tchieu J., Mason M.J., Yachechko R., Kuoy E., Horvath S., Zhou Q., Plath K. Role of the murine reprogramming factors in the induction of pluripotency. Cell 2009, 136:364-377.
46. Stanton B.R., Perkins A.S., Tessarollo L., Sassoon D.A., Parada L.F. Loss of N-myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes Dev. 1992, 6:2235-2247.
47. Su X., Gopalakrishnan V., Stearns D., Aldape K., Lang F.F., Fuller G., Snyder E., Eberhart C.G., Majumder S. Abnormal expression of REST/NRSF and Myc in neural stem/progenitor cells causes cerebellar tumors by blocking neuronal differentiation. Mol. Cell Biol. 2006, 26:1666-1678.
48. Sumi T., Tsuneyoshi N., Nakatsuji N., Suemori H. Apoptosis and differentiation of human embryonic stem cells induced by sustained activation of c-Myc. Oncogene 2007, 26:5564-5576.
49. Takahashi K., Okita K., Nakagawa M., Yamanaka S. Induction of pluripotent stem cells from fibroblast cultures. Nat. Protocols 2007, 2:3081-3089.
50. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006.
51. Trumpp A., Refaeli Y., Oskarsson T., Gasser S., Murphy M., Martin G.R., Bishop J.M. c-Myc regulates mammalian body size by controlling cell number but not cell size. Nature 2001, 414:768-773.
52. Wang H., Mannava S., Grachtchouk V., Zhuang D., Soengas M.S., Gudkov A.V., Prochownik E.V., Nikiforov M.A. c-Myc depletion inhibits proliferation of human tumor cells at various stages of the cell cycle. Oncogene 2008, 27:1905-1915.
53. Wang J., Wang H., Li Z., Wu Q., Lathia J.D., McLendon R.E., Hjelmeland A.B., Rich J.N. c-Myc is required for maintenance of glioma cancer stem cells. PLoS ONE 2008, 3:e3769.
54. Wang Y., Baskerville S., Shenoy A., Babiarz J.E., Baehner L., Blelloch R. Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation. Nat. Genet. 2008, 40:1478-1483.
55. Wang Y., Blelloch R. Cell cycle regulation by MicroRNAs in embryonic stem cells. Cancer Res. 2009, 69:4093-4096.
56. Wilson A., Murphy M.J., Oskarsson T., Kaloulis K., Bettess M.D., Oser G.M., Pasche A.C., Knabenhans C., Macdonald H.R., Trumpp A. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 2004, 18:2747-2763.
57. Wong D.J., Liu H., Ridky T.W., Cassarino D., Segal E., Chang H.Y. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2008, 2:333-344.
58. Wu S., Cetinkaya C., Munoz-Alonso M.J., von der Lehr N., Bahram F., Beuger V., Eilers M., Leon J., Larsson L.G. Myc represses differentiation-induced p21CIP1 expression via Miz-1-dependent interaction with the p21 core promoter. Oncogene 2003, 22:351-360.
59. Yamanaka S. Elite and stochastic models for induced pluripotent stem cell generation. Nature 2009, 460:49-52.
60. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., Slukvin, Thomson J.A. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.