Drosophila brat and human ortholog TRIM3 maintain stem cell equilibrium and suppress brain tumorigenesis by attenuating notch nuclear transport

Cancer Research

Volumn 76, Issue 8, 2016, Pages 2443-2452

  Mukherjee, Subhas ^a   Tucker Burden, Carol ^a   Zhang, Changming ^a   Moberg, Kenneth ^a   Read, Renee ^a   Hadjipanayis, Costas ^b   Brat, Daniel J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KARYOPHERIN; NOTCH RECEPTOR; NOTCH1 RECEPTOR; SMALL INTERFERING RNA; TRIPARTITE MOTIF PROTEIN 3; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; BRAT PROTEIN, DROSOPHILA; CARRIER PROTEIN; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; TRIM3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CANCER; CANCER INHIBITION; CANCER STEM CELL; CELL DIVISION; CELL NUCLEUS; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; DISEASE MODEL; DROSOPHILA; GLIOMA CELL; HUMAN; HUMAN CELL; NEUROBLAST; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RNA INTERFERENCE; UPREGULATION; ANIMAL; BRAIN TUMOR; CARCINOGENESIS; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN NEOPLASMS; CARCINOGENESIS; CARRIER PROTEINS; CELL NUCLEUS; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; HUMANS; NEOPLASTIC STEM CELLS; PROTEIN TRANSPORT; RECEPTORS, NOTCH; RNA INTERFERENCE;

EID: 84970951252     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-2299     Document Type: Article

References (43)

1. Mukherjee S, Kong J, Brat DJ. Cancer stem cell division: when the rules of asymmetry are broken. Stem Cells Dev 2015;24:405-16.
2. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, et al. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 2004;64:7011-21.
3. Johannessen TC, Wang J, Skaftnesmo KO, Sakariassen PO, Enger PO, Petersen K, et al. Highly infiltrative brain tumours show reduced chemosensitivity associated with a stem cell-like phenotype. Neuropathol Appl Neurobiol 2009;35:380-93.
4. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003;63:5821-8.
5. Chen G, Kong J, Tucker-Burden C, Anand M, Rong Y, Rahman F, et al. Human Brat ortholog TRIM3 is a tumor suppressor that regulates asymmetric cell division in glioblastoma. Cancer Res 2014;74:4536-48.
6. Caussinus E, Gonzalez C. Induction of tumor growth by altered stem-cell asymmetric division inDrosophila melanogaster.Nat Genet 2005;37:1125-9.
7. Arama E, Dickman D, Kimchie Z, Shearn A, Lev Z. Mutations in the betapropeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain. Oncogene 2000;19:3706-16.
8. Knoblich JA. Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 2010;11:849-60.
9. Liu J, Sato C, CerlettiM,Wagers A. Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr TopicsDev Biol 2010;92:367-409.
10. Ellisen LW, Bird J, West DC, Soreng AL, Reynolds TC, Smith SD, et al. TAN- 1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 1991;66: 649-61.
11. Boulay JL, Miserez AR, Zweifel C, Sivasankaran B, Kana V, Ghaffari A, et al. Loss of NOTCH2 positively predicts survival in subgroups of human glial brain tumors. PLoS One 2007;2:e576.
12. Solecki DJ, Liu XL, Tomoda T, Fang Y, Hatten ME. Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 2001;31:557-68.
13. Nagao M, SugimoriM, Nakafuku M. Cross talk between notch and growth factor/cytokine signaling pathways in neural stem cells. Mol Cell Biol 2007;27:3982-94.
14. Stockhausen MT, Kristoffersen K, Poulsen HS. The functional role of Notch signaling in human gliomas. Neuro Oncol 2010;12:199-211.
15. Baron M. Endocytic routes to Notch activation. Semin Cell Dev Biol 2012;23:437-42.
16. Nakahara J, Kanekura K, Nawa M, Aiso S, Suzuki N. Abnormal expression of TIP30 and arrested nucleocytoplasmic transport within oligodendrocyte precursor cells in multiple sclerosis. J Clin Invest 2009; 119:169-81.
17. Sachan N, Mishra AK, Mutsuddi M, Mukherjee A. The Drosophila importin- alpha3 is required for nuclear import of notch in vivo and it displays synergistic effects with notch receptor on cell proliferation. PLoS One 2013;8:e68247.
18. Huenniger K, Kramer A, Soom M, Chang I, Kohler M, Depping R, et al. Notch1 signaling ismediated by importins alpha 3, 4, and 7. Cell Mol Life Sci 2010;67:3187-96.
19. Yan Y, Denef N, Schupbach T. The vacuolar proton pump, V-ATPase, is required for notch signaling and endosomal trafficking inDrosophila. Dev Cell 2009;17:387-402.
20. Yedvobnick B, Kumar A, Chaudhury P, Opraseuth J, Mortimer N, Bhat KM. Differential effects of Drosophila mastermind on asymmetric cell fate specification and neuroblast formation. Genetics 2004;166: 1281-9.
21. Bian XL, Rosas-Acosta G, Wu YC, Wilson VG. Nuclear import of bovine papillomavirus type 1 E1 protein is mediated by multiple alpha importins and is negatively regulated by phosphorylation near a nuclear localization signal. J Virol 2007;81:2899-908.
22. Wodarz A, Ramrath A, Kuchinke U, Knust E. Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 1999;402: 544-7.
23. Ostrom QT, Gittleman H, Farah P, Ondracek A, Chen Y, Wolinsky Y, et al. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2006-2010. Neuro Oncol 2013;15Suppl 2:ii1-56.
24. Heimans JJ, TaphoornMJ. Impact of brain tumour treatment on quality of life. J Neurol 2002;249:955-60.
25. Osoba D, Brada M, Prados MD, Yung WK. Effect of disease burden on health-related quality of life in patients with malignant gliomas. Neuro Oncol 2000;2:221-8.
26. Bowman SK, Rolland V, Betschinger J, Kinsey KA, Emery G, Knoblich JA. The tumor suppressors Brat and Numb regulate transit-amplifying neuroblast lineages in Drosophila. Dev Cell 2008;14:535-46.
27. Komori H, Xiao Q, McCartney BM, Lee CY. Brain tumor specifies intermediate progenitor cell identity by attenuating beta-catenin/Armadillo activity. Development 2014;141:51-62.
28. Couturier L, Vodovar N, Schweisguth F. Endocytosis by Numb breaks Notch symmetry at cytokinesis. Nat Cell Biol 2012;14:131-9.
29. Lee SJ, Matsuura Y, Liu SM, Stewart M. Structural basis for nuclear import complex dissociation by RanGTP. Nature 2005;435:693-6.
30. Liu Y, Raheja R, Yeh N, Ciznadija D, Pedraza AM, Ozawa T, et al. TRIM3, a tumor suppressor linked to regulation of p21(Waf1/Cip1.). Oncogene 2014;33:308-15.
31. Koch U, Lehal R, Radtke F. Stem cells living with a Notch. Development 2013;140:689-704.
32. Chapouton P, Skupien P, Hesl B, Coolen M, Moore JC, Madelaine R, et al. Notch activity levels control the balance between quiescence and recruitment of adult neural stem cells. J Neurosci 2010;30:7961-74.
33. Gallahan D, Callahan R. Mammary tumorigenesis in feral mice: identification of a new int locus in mouse mammary tumor virus (Czech II)- induced mammary tumors. J Virol 1987;61:66-74.
34. Uyttendaele H, Marazzi G, Wu G, Yan Q, Sassoon D, Kitajewski J. Notch4/int-3, a mammary proto-oncogene, is an endothelial cell-specific mammalian Notch gene. Development 1996;122:2251-9.
35. Weijzen S, Rizzo P, Braid M, Vaishnav R, Jonkheer SM, Zlobin A, et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat Med 2002;8:979-86.
36. Zagouras P, Stifani S, Blaumueller CM, Carcangiu ML, Artavanis-Tsakonas S. Alterations in Notch signaling in neoplastic lesions of the human cervix. Proc Natl Acad Sci U S A 1995;92:6414-8.
37. Kandachar V, Roegiers F. Endocytosis and control of Notch signaling. Curr Opin Cell Biol 2012;24:534-40.
38. Bello B, Reichert H, Hirth F. The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila. Development 2006;133:2639-48.
39. Homem CC, Steinmann V, Burkard TR, Jais A, Esterbauer H, Knoblich JA. Ecdysone and mediator change energy metabolism to terminate proliferation in Drosophila neural stem cells. Cell 2014;158:874-88.
40. Jeffries S, Capobianco AJ. Neoplastic transformation by Notch requires nuclear localization. Mol Cell Biol 2000;20:3928-41.
41. Matamales M, Girault JA. Signaling from the cytoplasm to the nucleus in striatal medium-sized spiny neurons. Front Neuroanat 2011;5:37.
42. Wilson A, Radtke F. Multiple functions of Notch signaling in self-renewing organs and cancer. FEBS Lett 2006;580:2860-8.
43. Devgan V, Mammucari C, Millar SE, Brisken C, Dotto GP. p21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev 2005;19:1485-95.