Myc increases self-renewal in neural progenitor cells through Miz-1

Journal of Cell Science

Volumn 121, Issue 23, 2008, Pages 3941-3950

  Kerosuo, Laura ^a   Piltti, Katja ^a   Fox, Heli ^a   Angers Loustau, Alexandre ^a   Häyry, Valtteri ^a   Eilers, Martin ^b   Sariola, Hannu ^a,c   Wartiovaara, Kirmo ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Miz 1; Myc; Neural progenitor; Oncogene; Self renewal; Stem cell

Indexed keywords

BINDING PROTEIN; MYC PROTEIN; PROTEIN MIZ 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN TISSUE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENETIC TRANSDUCTION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NEURAL STEM CELL; NONHUMAN; PLOIDY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WILD TYPE;

ANIMALS; BINDING SITES; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; FLUORESCENT ANTIBODY TECHNIQUE; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MODELS, BIOLOGICAL; NEURONS; PROTO-ONCOGENE PROTEINS C-MYC; STEM CELLS;

EID: 59349110287     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.024802     Document Type: Article

References (62)

1. Adhikary, S., Peukert, K., Karsunky, H., Beuger, V., Lutz, W., Elsasser, H. P., Moroy, T. and Eilers, M. (2003). Miz1 is required for early embryonic development during gastrulation. Mol. Cell. Biol. 23, 7648-7657.
2. Arnold, I. and Watt, F. M. (2001). c-myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr. Biol. 11, 558-568.
3. Beer, S., Zetterberg, A., Ihrie, R. A., McTaggart, R. A., Yang, Q., Bradon, N., Arvanitis, C., Attardi, L. D., Feng, S., Ruebner, B. et al. (2004). Developmental context determines latency of MYC-induced tumorigenesis. PLoS Biol. 2, e332.
4. Betschinger, J., Mechtler, K. and Knoblich, J. A. (2006). Asymmetric segregation of the tumor suppressor brat regulates self-renewal in drosophila neural stem cells. Cell 124, 1241-1253.
5. Bettess, M. D., Dubois, N., Murphy, M. J., Dubey, C., Roger, C., Robine, S. and Trumpp, A. (2005). c-myc is required for the formation of intestinal crypts but dispensable for homeostasis of the adult intestinal epithelium. Mol. Cell. Biol. 25, 7868-7878.
6. Bhardwaj, R. D., Curtis, M. A., Spalding, K. L., Buchholz, B. A., Fink, D., Bjork-Eriksson, T., Nordborg, C., Gage, F. H., Druid, H., Eriksson, P. S. et al. (2006). Neocortical neurogenesis in humans is restricted to development. Proc. Natl. Acad. Sci. USA 103, 12564-12568.
7. Cartwright, P., McLean, C., Sheppard, A., Rivett, D., Jones, K. and Dalton, S. (2005). LIF/STAT3 controls ES cell self-renewal and pluripotency by a myc-dependent mechanism. Development 132, 885-896.
8. Charron, J., Malynn, B. A., Fisher, P., Stewart, V., Jeannotte, L., Goff, S. P., Robertson, E. J. and Alt, F. W. (1992). Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes Dev. 6, 2248-2257.
9. Coller, H. A., Grandori, C., Tamayo, P., Colbert, T., Lander, E. S., Eisenman, R. N. and Golub, T. R. (2000). Expression analysis with oligonucleotide microarrays reveals that MYC regulates genes involved in growth, cell cycle, signaling, and adhesion. Proc. Natl. Acad. Sci. USA 97, 3260-3265.
10. Collins, V. P. (1995). Gene amplification in human gliomas. Glia 15, 289-296.
11. Dang, C. V., O'Donnell, K. A., Zeller, K. I., Nguyen, T., Osthus, R. C. and Li, F. (2006). The c-myc target gene network. Semin. Cancer Biol. 16, 253-264.
12. Davis, A. C., Wims, M., Spotts, G. D., Hann, S. R. and Bradley, A. (1993). A null c-myc mutation causes lethality before 10.5 days of gestation in homozygotes and reduced fertility in heterozygous female mice. Genes Dev. 7, 671-682.
13. Eberhart, C. G., Kratz, J., Wang, Y., Summers, K., Stearns, D., Cohen, K., Dang, C. V. and Burger, P. C. (2004). Histopathological and molecular prognostic markers in medulloblastoma: C-myc, N-myc, TrkC, and anaplasia. J. Neuropathol. Exp. Neurol. 63, 441-449.
14. Fasano, C. A., Dimos, J. T., Ivanova, N. B., Lowry, N., Lemischka, I. R. and Temple, S. (2007). shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 1, 87-99.
15. Frye, M., Gardner, C., Li, E. R., Arnold, I. and Watt, F. M. (2003). Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development 130, 2793-2808.
16. Fults, D., Pedone, C., Dai, C. and Holland, E. C. (2002). MYC expression promotes the proliferation of neural progenitor cells in culture and in vivo. Neoplasia 4, 32-39.
17. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438.
18. Gandarillas, A. and Watt, F. M. (1997). c-myc promotes differentiation of human epidermal stem cells. Genes Dev. 11, 2869-2882.
19. Gebhardt, A., Frye, M., Herold, S., Benitah, S. A., Braun, K., Samans, B., Watt, F. M., Elsasser, H. P. and Eilers, M. (2006). Myc regulates keratinocyte adhesion and differentiation via complex formation with Miz1. J. Cell Biol. 172, 139-149.
20. Grandori, C., Cowley, S. M., James, L. P. and Eisenman, R. N. (2000). The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol. 16, 653-699.
21. Guney, I., Wu, S. and Sedivy, J. M. (2006). Reduced c-myc signaling triggers telomere-independent senescence by regulating bmi-1 and p16(INK4a). Proc. Natl. Acad. Sci. USA 103, 3645-3650.
22. Haggerty, T. J., Zeller, K. I., Osthus, R. C., Wonsey, D. R. and Dang, C. V. (2003). A strategy for identifying transcription factor binding sites reveals two classes of genomic c-Myc targets. Proc. Natl. Acad. Sci. USA 100, 5313-5318.
23. Herold, S., Wanzel, M., Beuger, V., Frohme, C., Beul, D., Hillukkala, T., Syvaoja, J., Saluz, H. P., Haenel, F. and Eilers, M. (2002). Negative regulation of the mammalian UV response by myc through association with miz-1. Mol. Cell 10, 509-521.
24. Hirvonen, H., Makela, T. P., Sandberg, M., Kalimo, H., Vuorio, E. and Alitalo, K. (1990). Expression of the myc proto-oncogenes in developing human fetal brain. Oncogene 5, 1787-1797.
25. Huntly, B. J. and Gilliland, D. G. (2005). Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat. Rev. Cancer. 5, 311-321.
26. Knoepfler, P. S., Cheng, P. F. and Eisenman, R. N. (2002). N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev. 16, 2699-2712.
27. Lassman, A. B., Dai, C., Fuller, G. N., Vickers, A. J. and Holland, E. C. (2004). Overexpression of c-MYC promotes an undifferentiated phenotype in cultured astrocytes and allows elevated ras and akt signaling to induce gliomas from GFAP-expressing cells in mice. Neuron Glia Biol. 1, 157-163.
28. Levens, D. L. (2003). Reconstructing MYC. Genes Dev. 17, 1071-1077.
29. Li, L. and Neaves, W. B. (2006). Normal stem cells and cancer stem cells: the niche matters. Cancer Res. 66, 4553-4557.
30. Malynn, B. A., de Alboran, I. M., O'Hagan, R. C., Bronson, R., Davidson, L., DePinho, R. A. and Alt, F. W. (2000). N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation. Genes Dev. 14, 1390-1399.
31. Meyer, N., Kim, S. S. and Penn, L. Z. (2006). The oscar-worthy role of myc in apoptosis. Semin. Cancer Biol. 16, 275-287.
32. Molofsky, A. V., He, S., Bydon, M., Morrison, S. J. and Pardal, R. (2005). Bmi-1 promotes neural stem cell self-renewal and neural development but not mouse growth and survival by repressing the p16Ink4a and p19Arf senescence pathways. Genes Dev. 19, 1432-1437.
33. Moore, K. A. and Lemischka, I. R. (2006). Stem cells and their niches. Science 311, 1880-1885.
34. Morrison, S. J. and Kimble, J. (2006). Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441, 1068-1074.
35. Morshead, C. M., Craig, C. G. and van der Kooy, D. (1998). In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 125, 2251-2261.
36. Murphy, M. J., Wilson, A. and Trumpp, A. (2005). More than just proliferation: Myc function in stem cells. Trends Cell Biol. 15, 128-137.
37. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144.
38. Okita, K., Ichisaka, T. and Yamanaka, S. (2007). Generation of germline-competent induced pluripotent stem cells. Nature 448, 313-317.
39. Pardal, R., Molofsky, A. V., He, S. and Morrison, S. J. (2005). Stem cell self-renewal and cancer cell proliferation are regulated by common networks that balance the activation of proto-oncogenes and tumor suppressors. Cold Spring Harb. Symp. Quant. Biol. 70, 177-185.
40. Pelengaris, S., Littlewood, T., Khan, M., Elia, G. and Evan, G. (1999). Reversible activation of c-myc in skin: induction of a complex neoplastic phenotype by a single oncogenic lesion. Mol. Cell 3, 565-577.
41. Piltti, K., Kerosuo, L., Hakanen, J., Eriksson, M., Angers-Loustau, A., Leppa, S., Salminen, M., Sariola, H. and Wartiovaara, K. (2006). E6/E7 oncogenes increase and tumor suppressors decrease the proportion of self-renewing neural progenitor cells. Oncogene 25, 4880-4889.
42. Reynolds, B. A. and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
43. Scadden, D. T. (2006). The stem-cell niche as an entity of action. Nature 441, 1075-1079.
44. Schwab, M. (2004). MYCN in neuronal tumours. Cancer Lett. 204, 179-187.
45. Semsei, I., Ma, S. Y. and Cutler, R. G. (1989). Tissue and age specific expression of the myc proto-oncogene family throughout the life span of the C57BL/6J mouse strain. Oncogene 4, 465-471.
46. Seoane, J., Le, H. V. and Massague, J. (2002). Myc suppression of the p21(Cip1) cdk inhibitor influences the outcome of the p53 response to DNA damage. Nature 419, 729-734.
47. Singh, S. K., Hawkins, C., Clarke, I. D., Squire, J. A., Bayani, J., Hide, T., Henkelman, R. M., Cusimano, M. D. and Dirks, P. B. (2004). Identification of human brain tumour initiating cells. Nature 432, 396-401.
48. Staller, P., Peukert, K., Kiermaier, A., Seoane, J., Lukas, J., Karsunky, H., Moroy, T., Bartek, J., Massague, J., Hanel, F. et al. (2001). Repression of p15INK4b expression by myc through association with miz-1. Nat. Cell Biol. 3, 392-399.
49. Stanton, B. R., Perkins, A. S., Tessarollo, L., Sassoon, D. A. and Parada, L. F. (1992). Loss of N-myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes Dev. 6, 2235-2247.
50. Stearns, D., Chaudhry, A., Abel, T. W., Burger, P. C., Dang, C. V. and Eberhart, C. G. (2006). c-myc overexpression causes anaplasia in medulloblastoma. Cancer Res. 66, 673-681.
51. Su, X., Gopalakrishnan, V., Stearns, D., Aldape, K., Lang, F. F., Fuller, G., Snyder, E., Eberhart, C. G. and Majumder, S. (2006). Abnormal expression of REST/NRSF and myc in neural stem/progenitor cells causes cerebellar tumors by blocking neuronal differentiation. Mol. Cell. Biol. 26, 1666-1678.
52. Suhonen, J. O., Peterson, D. A., Ray, J. and Gage, F. H. (1996). Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383, 624-627.
53. Takahashi, K. and Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676.
54. Taupin, P. and Gage, F. H. (2002). Adult neurogenesis and neural stem cells of the central nervous system in mammals. J. Neurosci. Res. 69, 745-749.
55. Toma, J. G., Akhavan, M., Fernandes, K. J., Barnabe-Heider, F., Sadikot, A., Kaplan, D. R. and Miller, F. D. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol. 3, 778-784.
56. Vermes, I., Haanen, C., Steffens-Nakken, H. and Reutelingsperger, C. (1995). A novel assay for apoptosis. flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled annexin V. J. Immunol. Methods 184, 39-51.
57. Wade, M. and Wahl, G. M. (2006). c-myc, genome instability, and tumorigenesis: the devil is in the details. Curr. Top. Microbiol. Immunol. 302, 169-203.
58. Weber, A., Marquardt, J., Elzi, D., Forster, N., Starke, S., Glaum, A., Yamada, D., Defossez, P. A., Delrow, J., Eisenman, R. N. et al. (2008). Zbtb4 represses transcription of P21CIP1 and controls the cellular response to p53 activation. EMBO J. 27, 1563-1574.
59. Wernig, M., Meissner, A., Foreman, R., Brambrink, T., Ku, M., Hochedlinger, K., Bernstein, B. E. and Jaenisch, R. (2007). In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448, 318-324.
60. Wilson, A., Murphy, M. J., Oskarsson, T., Kaloulis, K., Bettess, M. D., Oser, G. M., Pasche, A. C., Knabenhans, C., Macdonald, H. R. and Trumpp, A. (2004). c-myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 18, 2747-2763.
61. Zhang, R., Zhang, Z., Zhang, C., Zhang, L., Robin, A., Wang, Y., Lu, M. and Chopp, M. (2004). Stroke transiently increases subventricular zone cell division from asymmetric to symmetric and increases neuronal differentiation in the adult rat. J. Neurosci. 24, 5810-5815.
62. Zimmerman, K. A., Yancopoulos, G. D., Collum, R. G., Smith, R. K., Kohl, N. E., Denis, K. A., Nau, M. M., Witte, O. N., Toran-Allerand, D. and Gee, C. E. (1986). Differential expression of myc family genes during murine development. Nature 319, 780-783.