Neural precursor cycling at sonic speed: N-Myc pedals, GSK-3 brakes

Cell Cycle

Volumn 5, Issue 1, 2006, Pages 47-52

  Knoepfler, Paul S ^a   Kenney, Anna Marie ^b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cell cycle; Cerebellum; Insulin like growth factor; Medulloblastoma; N myc; Progenitor cells; Stem cells

Indexed keywords

CYCLIN DEPENDENT KINASE ACTIVATING KINASE; SOMATOMEDIN; SONIC HEDGEHOG PROTEIN;

BRAIN DEVELOPMENT; BRAIN TUMOR; CANCER; CELL COUNT; CELL CULTURE; CELL CYCLE; CELL MATURATION; CENTRAL NERVOUS SYSTEM; CEREBELLUM; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE AMPLIFICATION; GENE EXPRESSION; GENE FUNCTION; GROWTH DISORDER; HUMAN; MEDULLOBLASTOMA; MITOSIS; NONHUMAN; ONCOGENE C MYB; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; VELOCITY;

ERINACEIDAE;

EID: 33645211987     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.1.2292     Document Type: Review

References (84)

1. Pettmann B, Henderson CE. Neuronal cell death. Neuron 1998; 20:633-47.
2. Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci 1991; 14:453-501.
3. Wechsler-Reya R, Scott MP. The developmental biology of brain tumors. Annu Rev Neurosci 2001; 24:385-428.
4. Altman J, Bayer SA. Development of the cerebellar system in relation toits eveolution, structure, and functions. Boca Raton, FLA: CRC Press, 1997.
5. Dahmane N, Ruiz-i-Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 1999; 126:3089-100.
6. Wallace VA. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 1999; 9:445-8.
7. Wechsler-Reya RJ, Scott MP. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog [see comments]. Neuron 1999; 22:103-14.
8. D'Mello SR, Borodezt K, Soltoff SP. Insulin-like growth factor and potassium depolarization maintain neuronal survival by distinct pathways: Possible involvement of PI 3-kinase in IGF-1 signaling. J Neurosci 1997; 17:1548-60.
9. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, Segal RA, Kaplan DR, and Greenberg ME. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 1997; 275:661-5.
10. 1 cyclin expression and sustained cell cycle progression in mammalian neuronal precursors [In Process Citation]. Mol Cell Biol 2000; 20:9055-67.
11. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME, Kim JY, Goumnerova LC, Black PM, Lau C, Allen JC, Zagzag D, Olson JM, Curran T, Wetmore C, Biegel JA, Poggio T, Mukherjee S, Rifkin R, Califano A, Stolovitzky G, Louis DN, Mesirov JP, Lander ES, and Golub TR. Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 2002; 415:436-42.
12. Raffel C, Jenkins RB, Frederick L, Hebrink D, Alderete B, Fults DW, and James CD. Sporadic medulloblastomas contain PTCH mutations. Cancer Res 1997; 57:842-5.
13. Reifenberger J, Wolter M, Weber RG, Megahed M, Ruzicka T, Lichter P, and Reifenberger G. Missense mutations in SMOH in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res 1998; 58:1798-803.
14. Xie J, Johnson RL, Zhang X, et al. Mutations of the PATCHED gene in several types of sporadic extracutaneous tumors. Cancer Res 1997; 57:2369-72.
15. Xie J, Johnson RL, Zhang X, Bare JW, Waldman FM, Cogen PH, Menon AG, Warren RS, Chen LC, Scott MP, and Epstein EH Jr. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998; 391:90-2.
16. Weiner HL, Bakst R, Hurlbert MS, Ruggiero J, Ahn E, Lee WS, Stephen D, Zagzag D, Joyner AL, and Turnbull DH. Induction of medulloblastomas in mice by sonic hedgehog, independent of Gli1. Cancer Res 2002; 62:6385-9.
17. Pietsch T, Waha A, Koch A, Kraus J, Albrecht S, Tonn J, Sorensen N, Berthold F, Henk B, Schmandt N, Wolf HK, von Deimling A, Wainwright B, Chenevix-Trench G, Wiestler OD, and Wicking C. Medulloblastomas of the desmoplastic variant carry mutations of the human homologue of Drosophila patched. Cancer Res 1997; 57:2085-8.
18. Goodrich LV, Milenkovic L, Higgins KM, Scott MP. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 1997; 277:1109-13.
19. Rao G, Pedone CA, Valle LD, Reiss K, Holland EC, Fults DW. Sonic hedgehog and insulin-like growth factor signaling synergize to induce medulloblastoma formation from nestin-expressing neural progenitors in mice. Oncogene 2004; 23:6156-62.
20. Wetmore C, Eberhart DE, Curran T. The normal patched allele is expressed in medulloblastomas from mice with heterozygous germ-line mutation of patched. Cancer Res 2000; 60:2239-46.
21. Rao G, Pedone CA, Coffin CM, Holland EC, Fults DW. c-Myc enhances sonic hedgehog-induced medulloblastoma formation from nestin-expressing neural progenitors in mice. Neoplasia 2003; 5:198-204.
22. Provias JP, Becker LE. Cellular and molecular pathology of medulloblastoma. J Neurooncol 1996; 29:35-43.
23. Kenney AM, Cole MD, Rowitch DH. Nmyc upregulation by sonic hedgehog signaling promotes proliferation in developing cerebellar granule neuron precursors. Development 2003; 130:15-28.
24. Kenney AM, Widlund HR, Rowitch DH. Hedgehog and PI-3 kinase signaling converge on Nmyc1 to promote cell cycle progression in cerebellar neuronal precursors. Development 2004; 131:217-28.
25. Oliver TG, Grasfeder LL, Carroll AL, Kaiser C, Gillingham CL, Lin SM, Wickramasinghe R, Scott MP, and Wechsler-Reya RJ. Transcriptional profiling of the Sonic hedgehog response: A critical role for N-myc in proliferation of neuronal precursors. Proc Natl Acad Sci USA 2003; 100:7331-6.
26. Henriksson M, Luscher B. Proteins of the Myc network: Essential regulators of cell growth and differentiation. Adv Cancer Res 1996; 68:109-182.
27. Nesbit CE, Tersak JM, Prochownik EV. MYC oncogenes and human neoplastic disease. Oncogene 1999; 18:3004-16.
28. Knoepfler PS, Cheng PF, Eisenman RN. N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 2002; 16:2699-712.
29. Bouchard C, Thieke K, Maier A, Saffrich R, Hanley-Hyde J, Ansorge W, Reed S, Sicinski P, Bartek J, and Eilers M. Direct induction of cyclin D2 by Myc contributes to cell cycle progression and sequestration of p27. Embo J 1999; 18:5321-33.
30. Gartel AL, Shchors K. Mechanisms of c-myc-mediated transcriptional repression of growth arrest genes. Exp Cell Res 2003; 283:17-21.
31. Huard JM, Forster CC, Carter ML, Sicinski P, Ross ME. Cerebellar histogenesis is disturbed in mice lacking cyclin D2. Development 1999; 126:1927-35.
32. Miyazawa K, Himi T, Garcia V, Yamagishi H, Sato S, Ishizaki Y. A role for p27/Kip1 in the control of cerebellar granule cell precursor proliferation. J Neurosci 2000; 20:5756-63.
33. Zindy F, Soares H, Herzog KH, Morgan J, Sherr CJ, Roussel MF. Expression of INK4 inhibitors of cyclin D-dependent kinases during mouse brain development. Cell Growth Differ 1997; 8:1139-50.
34. Ciemerych MA, Kenney AM, Sicinska E, Kalaszczynska I, Bronson RT, Rowitch DH, Gardner H, and Sicinski P. Development of mice expressing a single D-type cyclin. Genes Dev 2002; 16:3277-89.
35. Zindy F, Nilsson LM, Nguyen L, Meunier C, Smeyne RJ, Rehg JE, Eberhart C, Sherr CJ, and Roussel MF. Hemangiosarcomas, medulloblastomas, and other tumors in Ink4c/p53-null mice. Cancer Res 2003; 63:5420-7.
36. Kimura H, Stephen D, Joyner A, Curran T. Gli1 is important for medulloblastoma formation in Ptc1+/- mice. Oncogene 2005; 24:4026-36.
37. Hatton KS, Mahon K, Chin L, Chiu FC, Lee HW, Peng D, Morgenbesser SD, Horner J, and DePinho RA. Expression and activity of L-Myc in normal mouse development. Mol Cell Biol 1996; 16:1794-804.
38. Bigner SH, Friedman HS, Vogelstein B, Oakes WJ, Bigner DD. Amplification of the c-myc gene in human medulloblastoma cell lines and xenografts. Cancer Res 1990; 50:2347-50.
39. Garson JA, Pemberton LF, Sheppard PW, Varndell IM, Coakham HB, Kemshead JT. N-myc gene expression and oncoprotein characterisation in medulloblastoma. Br J Cancer 1989; 59:889-94.
40. MacGregor DN, Ziff EB. Elevated c-myc expression in childhood medulloblastomas. Pediatr Res 1990; 28:63-8.
41. Tomlinson FH, Jenkins RB, Scheithauer BW, Keelan PA, Ritland S, Parisi JE, Cunningham J, and Olsen KD. Aggressive medulloblastoma with high-level N-myc amplification. Mayo Clin Proc 1994; 69:359-65.
42. Charron J, Malynn BA, Fisher P, Stewart V, Jeannotte L, Goff SP, Robertson EJ, and Alt FW. Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes Dev 1992; 6:2248-57.
43. Sawai S, Shimono A, Wakamatsu Y, Palmes C, Hanaoka K, Kondoh H. Defects of embryonic organogenesis resulting from targeted disruption of the N-myc gene in the mouse. Development 1993; 117:1445-55.
44. Stanton BR, Perkins AS, Tessarollo L, Sassoon DA, Parada LF. Loss of N-myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes Dev 1992; 6:2235-47.
45. van Bokhoven H, Celli J, van Reeuwijk J, Rinne T, Glaudemans B, van Beusekom E, Rieu P, Newbury-Ecob RA, Chiang C, and Brunner HG. MYCN haploinsufficiency is associated with reduced brain size and intestinal atresias in Feingold syndrome. Nat Genet 2005; 37:465-7.
46. Hann SR, Abrams HD, Rohrschneider LR, Eisenman RN. Proteins encoded by v-myc and c-myc oncogenes: Identification and localization in acute leukemia virus transformants and bursal lymphoma cell lines. Cell 1983; 34:789-98.
47. Kamemura K, Hayes BK, Comer FI, Hart GW. Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: Alternative glycosylation/phosphorylation of THR-58, a known mutational hot spot of c-Myc in lymphomas, is regulated by mitogens. J Biol Chem 2002; 277:19229-35.
48. Vervoorts J, Luscher-Firzlaff JM, Rottmann S, Lilischkis R, Walsemann G, Dohmann K, Austen M, and Luscher B. Stimulation of c-MYC transcriptional activity and acetylation by recruitment of the cofactor CBP. EMBO Rep 2003; 4:484-90.
49. Gregory MA, Hann SR. c-Myc proteolysis by the ubiquitin-proteasome pathway: Stabilization of c-Myc in Burkitt's lymphoma cells. Mol Cell Biol 2000; 20:2423-35.
50. Gregory MA, Qi Y, Hann SR. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J Biol Chem 2003; 278:51606-12.
51. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev 2000; 14:2501-14.
52. Welcker M, Orian A, Jin J, Grim JA, Harper JW, Eisenman RN, and Clurman BE. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci USA 2004; 101:9085-90.
53. Herbst A, Salghetti SE, Kim SY, Tansey WP. Multiple cell-type-specific elements regulate Myc protein stability. Oncogene 2004; 23:3863-71.
54. Lutterbach B, Hann SR. Overexpression of c-Myc and cell immortalization alters c-Myc phosphorylation. Oncogene 1997; 14:967-75.
55. 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; 132:885-96.
56. Henriksson M, Bakardjiev A, Klein G, Luscher B. Phosphorylation sites mapping in the N-terminal domain of c-myc modulate its transforming potential. Oncogene 1993; 8:3199-209.
57. Lutterbach B, Hann SR. Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis. Mol Cell Biol 1994; 14:5510-22.
58. Pulverer BJ, Fisher C, Vousden K, Littlewood T, Evan G, Woodgett JR. Site-specific modulation of c-Myc cotransformation by residues phosphorylated in vivo. Oncogene 1994; 9:59-70.
59. Saksela K, Makela TP, Hughes K, Woodgett JR, Alitalo K. Activation of protein kinase C increases phosphorylation of the L-myc trans-activator domain at a GSK-3 target site. Oncogene 1992; 7:347-53.
60. Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, Ishida N, Okumura F, Nakayama K, and Nakayama KI. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. Embo J 2004; 23:2116-25.
61. Welcker M, Singer J, Loeb KR, Grim J, Bloecher A, Gurien-West M, Clurman BE, and Roberts JM. Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol Cell 2003; 12:381-92.
62. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev 1998; 12:3499-511.
63. Ye P, Xing Y, Dai Z, D'Ercole AJ. In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: Evidence that IGF-I increases proliferation of granule cell progenitors. Brain Res Dev Brain Res 1996; 95:44-54.
64. Beck KD, Powell-Braxton L, Widmer HR, Valverde J, Hefti F. Igf1 gene disruption results in reduced brain size, CNS hypomyelination, and loss of hippocampal granule and striatal parvalbumin-containing neurons. Neuron 1995; 14:717-30.
65. Mill P, Mo R, Hu MC, Dagnino L, Rosenblum ND, Hui CC. Shh controls epithelial proliferation via independent pathways that converge on N-Myc. Dev Cell 2005; 9:293-303.
66. Niklinski J, Claassen G, Meyers C, Gregory MA, Allegra CJ, Kaye FJ, Hann SR, and Zajac-Kaye M. Disruption of Myc-tubulin interaction by hyperphosphorylation of c-Myc during mitosis or by constitutive hyperphosphorylation of mutant c-Myc in Burkitt's lymphoma. Mol Cell Biol 2000; 20:5276-84.
67. Hoang AT, Lutterbach B, Lewis BC, Yano T, Chou TY, Barrett JF, Raffeld M, Hann SR, and Dang CV. A link between increased transforming activity of lymphoma-derived MYC mutant alleles, their defective regulation by p107, and altered phosphorylation of the c-Myc transactivation domain. Mol Cell Biol 1995; 15:4031-42.
68. Lutterbach B, Hann SR. c-Myc transactivation domain-associated kinases: Questionable role for map kinases in c-Myc phosphorylation. J Cell Biochem 1999; 72:483-91.
69. Noguchi K, Kitanaka C, Yamana H, Kokubu A, Mochizuki T, Kuchino Y. Regulation of c-Myc through phosphorylation at Ser-62 and Ser-71 by c-Jun N-terminal kinase. J Biol Chem 1999; 274:32580-7.
70. Yeh E, Cunningham M, Arnold H, Chasse D, Monteith T, Ivaldi G, Hahn WC, Stukenberg PT, Shenolikar S, Uchida T, Counter CM, Nevins JR, Means AR, and Sears R. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat Cell Biol 2004; 6:308-18.
71. Sjostrom SK, Finn G, Hahn WC, Rowitch DH, Kenney AM. The cdk1 complex plays a prime role in regulating N-myc phosphorylation and turnover in neural precursors. Dev Cell 2005; 9:327-38.
72. Marigo V, Davey RA, Zuo Y, Cunningham JM, Tabin CJ. Biochemical evidence that patched is the Hedgehog receptor. Nature 1996; 384:176-9.
73. Zhao Q, Kho A, Kenney AM, Yuk Di DI, Kohane I, Rowitch DH. Identification of genes expressed with temporal-spatial restriction to developing cerebellar neuron precursors by a functional genomic approach. Proc Natl Acad Sci USA 2002; 99:5704-9.
74. Barnes EA, Kong M, Ollendorff V, Donoghue DJ. Patched1 interacts with cyclin B1 to regulate cell cycle progression. Embo J 2001; 20:2214-23.
75. Yin XY, Grove L, Datta NS, Katula K, Long MW, Prochownik EV. Inverse regulation of cyclin B1 by c-Myc and p53 and induction of tetraploidy by cyclin B1 overexpression. Cancer Res 2001; 61:6487-93.
76. Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cordon-Cardo C, Cleveland JL, Tansey WP, and Lowe SW. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 2005; 436:807-11.
77. Del Valle L, Enam S, Lassak A, Wang JY, Croul S, Khalil, K, and Reiss K. Insulin-like growth factor I receptor activity in human medulloblastomas. Clin Cancer Res 2002; 8:1822-30.
78. Hartmann W, Koch A, Brune H, Waha A, Schuller U, Dani I, Denkhaus D, Langmann W, Bode U, Wiestler OD, Schilling K, and Pietsch T. Insulin-like growth factor II is involved in the proliferation control of medulloblastoma and its cerebellar precursor cells. Am J Pathol 2005; 166:1153-62.
79. Wang JY, Del Valle L, Gordon J, Rubini M, Romano G, Croul S, Peruzzi F, Khalili K, and Reiss K. Activation of the IGF-IR system contributes to malignant growth of human and mouse medulloblastomas. Oncogene 2001; 20:3857-68.
80. Leung C, Lingbeek M, Shakhova O, Liu J, Tanger E, Saremaslani P, Van Lohuizen M, and Marino S. Bmi1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004; 428:337-41.
81. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell 1991;65:737-52.
82. Berman DM, Karhadkar SS, Hallahan AR, Pritchard JI, Eberhart CG, Watkins DN, Chen JK, Cooper MK, Taipale J, Olson JM, and Beachy PA. Medulloblastoma growth inhibition by hedgehog pathway blockade. Science 2002; 297:1559-61.
83. Romer JT, Kimura H, Magdaleno S, Sasai K, Fuller C, Baines H, Connelly M, Stewart CF, Gould S, Rubin LL, and Curran T. Suppression of the Shh pathway using a small molecule inhibitor eliminates medulloblastoma in Ptc1(+/-)p53(-/-) mice. Cancer Cell 2004; 6:229-40.
84. Reiss K. Insulin-like growth factor-I receptor - A potential therapeutic target in medulloblastomas. Expert Opin Ther Targets 2002; 6:539-44.