Mir-17~92 Governs Motor Neuron Subtype Survival by Mediating Nuclear PTEN

Cell Reports

Volumn 11, Issue 8, 2015, Pages 1305-1318

  Tung, Ying Tsen ^a   Lu, Ya Lin ^a   Peng, Kuan Chih ^a,b   Yen, Ya Ping ^a,c   Chang, Mien ^a   Li, Joye ^d   Jung, Heekyung ^e   Thams, Sebastian ^f   Huang, Yuan Ping ^f   Hung, Jui Hung ^d   Chen, Jun An ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

^e NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NewYork Presbyterian Hospital   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; HOX PROTEIN; HOXC6 PROTEIN; HOXC9 PROTEIN; MICRORNA; MICRORNA 17; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KLHDC5; PROTEIN NDFIP1; PROTEIN UBE3B; PROTEIN UBE3C; TRANSCRIPTOME; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE NEDD4; UNCLASSIFIED DRUG; MIRN17 MICRORNA, MOUSE; PTEN PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BINDING SITE; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; GENE OVEREXPRESSION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; LIMB INNERVATING LATERAL MOTOR COLUMN MOTOR NEURON; MOLECULAR DYNAMICS; MONOUBIQUITINATION; MOTONEURON; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; SPINAL GANGLION; TRANSCRIPTION REGULATION; UBIQUITINATION; UPREGULATION; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; MICE; MICE, KNOCKOUT; MICRORNAS; MOTOR NEURONS; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES;

EID: 84929958029     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.04.050     Document Type: Article

References (60)

1. Asli N.S., Kessel M. Spatiotemporally restricted regulation of generic motor neuron programs by miR-196-mediated repression of Hoxb8. Dev. Biol. 2010, 344:857-868.
2. Bassi C., Ho J., Srikumar T., Dowling R.J., Gorrini C., Miller S.J., Mak T.W., Neel B.G., Raught B., Stambolic V. Nuclear PTEN controls DNA repair and sensitivity to genotoxic stress. Science 2013, 341:395-399.
3. Bian S., Hong J., Li Q., Schebelle L., Pollock A., Knauss J.L., Garg V., Sun T. MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. Cell Rep. 2013, 3:1398-1406.
4. Burek M.J., Oppenheim R.W. Programmed cell death in the developing nervous system. Brain Pathol. 1996, 6:427-446.
5. Buss R.R., Gould T.W., Ma J., Vinsant S., Prevette D., Winseck A., Toops K.A., Hammarback J.A., Smith T.L., Oppenheim R.W. Neuromuscular development in the absence of programmed cell death: phenotypic alteration of motoneurons and muscle. J.Neurosci. 2006, 26:13413-13427.
6. Buss R.R., Sun W., Oppenheim R.W. Adaptive roles of programmed cell death during nervous system development. Annu. Rev. Neurosci. 2006, 29:1-35.
7. Chen J.A., Wichterle H. Apoptosis of limb innervating motor neurons and erosion of motor pool identity upon lineage specific dicer inactivation. Front Neurosci 2012, 6:69.
8. Chen J.A., Chu S.T., Amaya E. Maintenance of motor neuron progenitors in Xenopus requires a novel localized cyclin. EMBO Rep. 2007, 8:287-292.
9. Chen J.A., Huang Y.P., Mazzoni E.O., Tan G.C., Zavadil J., Wichterle H. Mir-17-3p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron 2011, 69:721-735.
10. Dalla Torre di Sanguinetto S.A., Dasen J.S., Arber S. Transcriptional mechanisms controlling motor neuron diversity and connectivity. Curr. Opin. Neurobiol. 2008, 18:36-43.
11. Dasen J.S. Transcriptional networks in the early development of sensory-motor circuits. Curr. Top. Dev. Biol. 2009, 87:119-148.
12. Dasen J.S., Jessell T.M. Hox networks and the origins of motor neuron diversity. Curr. Top. Dev. Biol. 2009, 88:169-200.
13. Dasen J.S., Tice B.C., Brenner-Morton S., Jessell T.M. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 2005, 123:477-491.
14. Dasen J.S., De Camilli A., Wang B., Tucker P.W., Jessell T.M. Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 2008, 134:304-316.
15. Dekkers M.P., Barde Y.A. Developmental biology. Programmed cell death in neuronal development. Science 2013, 340:39-41.
16. Dekkers M.P., Nikoletopoulou V., Barde Y.A. Cell biology in neuroscience: Death of developing neurons: new insights and implications for connectivity. J.Cell Biol. 2013, 203:385-393.
17. Dessaud E., Yang L.L., Hill K., Cox B., Ulloa F., Ribeiro A., Mynett A., Novitch B.G., Briscoe J. Interpretation of the sonic hedgehog morphogen gradient by a temporal adaptation mechanism. Nature 2007, 450:717-720.
18. Dessaud E., McMahon A.P., Briscoe J. Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 2008, 135:2489-2503.
19. Di Giorgio F.P., Carrasco M.A., Siao M.C., Maniatis T., Eggan K. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci. 2007, 10:608-614.
20. Dimos J.T., Rodolfa K.T., Niakan K.K., Weisenthal L.M., Mitsumoto H., Chung W., Croft G.F., Saphier G., Leibel R., Goland R., et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 2008, 321:1218-1221.
21. Ernfors P., Lee K.F., Jaenisch R. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature 1994, 368:147-150.
22. Goh C.P., Putz U., Howitt J., Low L.H., Gunnersen J., Bye N., Morganti-Kossmann C., Tan S.S. Nuclear trafficking of Pten after brain injury leads to neuron survival not death. Exp. Neurol. 2014, 252:37-46.
23. Grimson A., Farh K.K., Johnston W.K., Garrett-Engele P., Lim L.P., Bartel D.P. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 2007, 27:91-105.
24. Groszer M., Erickson R., Scripture-Adams D.D., Lesche R., Trumpp A., Zack J.A., Kornblum H.I., Liu X., Wu H. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene invivo. Science 2001, 294:2186-2189.
25. Hamburger V. History of the discovery of neuronal death in embryos. J.Neurobiol. 1992, 23:1116-1123.
26. He L., Thomson J.M., Hemann M.T., Hernando-Monge E., Mu D., Goodson S., Powers S., Cordon-Cardo C., Lowe S.W., Hannon G.J., Hammond S.M. A microRNA polycistron as a potential human oncogene. Nature 2005, 435:828-833.
27. Howitt J., Lackovic J., Low L.H., Naguib A., Macintyre A., Goh C.P., Callaway J.K., Hammond V., Thomas T., Dixon M., et al. Ndfip1 regulates nuclear Pten import invivo to promote neuronal survival following cerebral ischemia. J.Cell Biol. 2012, 196:29-36.
28. Huang W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
29. Jung H., Mazzoni E.O., Soshnikova N., Hanley O., Venkatesh B., Duboule D., Dasen J.S. Evolving Hox activity profiles govern diversity inlocomotor systems. Dev. Cell 2014, 29:171-187.
30. Kanning K.C., Kaplan A., Henderson C.E. Motor neuron diversity in development and disease. Annu. Rev. Neurosci. 2010, 33:409-440.
31. Kaplan A., Spiller K.J., Towne C., Kanning K.C., Choe G.T., Geber A., Akay T., Aebischer P., Henderson C.E. Neuronal matrix metalloproteinase-9 is a determinant of selective neurodegeneration. Neuron 2014, 81:333-348.
32. Kreis P., Leondaritis G., Lieberam I., Eickholt B.J. Subcellular targeting and dynamic regulation of PTEN: implications for neuronal cells and neurological disorders. Front. Mol. Neurosci. 2014, 7:23.
33. Mazzoni E.O., Mahony S., Peljto M., Patel T., Thornton S.R., McCuine S., Reeder C., Boyer L.A., Young R.A., Gifford D.K., Wichterle H. Saltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals. Nat. Neurosci. 2013, 16:1191-1198.
34. Mu P., Han Y.C., Betel D., Yao E., Squatrito M., Ogrodowski P., de Stanchina E., D'Andrea A., Sander C., Ventura A. Genetic dissection of the miR-17~92 cluster of microRNAs in Myc-induced B-cell lymphomas. Genes Dev. 2009, 23:2806-2811.
35. Mund T., Pelham H.R. Regulation of PTEN/Akt and MAP kinase signaling pathways by the ubiquitin ligase activators Ndfip1 and Ndfip2. Proc. Natl. Acad. Sci. USA 2010, 107:11429-11434.
36. Nikoletopoulou V., Lickert H., Frade J.M., Rencurel C., Giallonardo P., Zhang L., Bibel M., Barde Y.A. Neurotrophin receptors TrkA and TrkC cause neuronal death whereas TrkB does not. Nature 2010, 467:59-63.
37. Ning K., Drepper C., Valori C.F., Ahsan M., Wyles M., Higginbottom A., Herrmann T., Shaw P., Azzouz M., Sendtner M. PTEN depletion rescues axonal growth defect and improves survival in SMN-deficient motor neurons. Hum. Mol. Genet. 2010, 19:3159-3168.
38. Olive V., Bennett M.J., Walker J.C., Ma C., Jiang I., Cordon-Cardo C., Li Q.J., Lowe S.W., Hannon G.J., He L. miR-19 is a key oncogenic component of mir-17-92. Genes Dev. 2009, 23:2839-2849.
39. Olive V., Jiang I., He L. mir-17-92, a cluster of miRNAs in the midst of the cancer network. Int. J. Biochem. Cell Biol. 2010, 42:1348-1354.
40. Olive V., Sabio E., Bennett M.J., De Jong C.S., Biton A., McGann J.C., Greaney S.K., Sodir N.M., Zhou A.Y., Balakrishnan A., et al. A component of the mir-17-92 polycistronic oncomir promotes oncogene-dependent apoptosis. eLife 2013, 2:e00822.
41. Oppenheim R.W. The neurotrophic theory and naturally occurring motoneuron death. Trends Neurosci. 1989, 12:252-255.
42. Oppenheim R.W. Cell death during development of the nervous system. Annu. Rev. Neurosci. 1991, 14:453-501.
43. Otaegi G., Pollock A., Hong J., Sun T. MicroRNA miR-9 modifies motor neuron columns by a tuning regulation of FoxP1 levels in developing spinal cords. J.Neurosci. 2011, 31:809-818.
44. Philippidou P., Dasen J.S. Hox genes: choreographers in neural development, architects of circuit organization. Neuron 2013, 80:12-34.
45. Raff M.C. Social controls on cell survival and cell death. Nature 1992, 356:397-400.
46. Raoul C., Henderson C.E., Pettmann B. Programmed cell death of embryonic motoneurons triggered through the Fas death receptor. J.Cell Biol. 1999, 147:1049-1062.
47. Rousso D.L., Gaber Z.B., Wellik D., Morrisey E.E., Novitch B.G. Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 2008, 59:226-240.
48. Song M.S., Carracedo A., Salmena L., Song S.J., Egia A., Malumbres M., Pandolfi P.P. Nuclear PTEN regulates the APC-CDH1 tumor-suppressive complex in a phosphatase-independent manner. Cell 2011, 144:187-199.
49. Song M.S., Salmena L., Pandolfi P.P. The functions and regulation of the PTEN tumour suppressor. Nat. Rev. Mol. Cell Biol. 2012, 13:283-296.
50. Southwell D.G., Paredes M.F., Galvao R.P., Jones D.L., Froemke R.C., Sebe J.Y., Alfaro-Cervello C., Tang Y., Garcia-Verdugo J.M., Rubenstein J.L., et al. Intrinsically determined cell death of developing cortical interneurons. Nature 2012, 491:109-113.
51. Taylor A.R., Gifondorwa D.J., Robinson M.B., Strupe J.L., Prevette D., Johnson J.E., Hempstead B., Oppenheim R.W., Milligan C.E. Motoneuron programmed cell death in response to proBDNF. Dev. Neurobiol. 2012, 72:699-712.
52. Trotman L.C., Wang X., Alimonti A., Chen Z., Teruya-Feldstein J., Yang H., Pavletich N.P., Carver B.S., Cordon-Cardo C., Erdjument-Bromage H., et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 2007, 128:141-156.
53. Van Themsche C., Leblanc V., Parent S., Asselin E. X-linked inhibitor of apoptosis protein (XIAP) regulates PTEN ubiquitination, content, and compartmentalization. J.Biol. Chem. 2009, 284:20462-20466.
54. Ventura A., Young A.G., Winslow M.M., Lintault L., Meissner A., Erkeland S.J., Newman J., Bronson R.T., Crowley D., Stone J.R., et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 2008, 132:875-886.
55. Wichterle H., Lieberam I., Porter J.A., Jessell T.M. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002, 110:385-397.
56. Xiao C., Srinivasan L., Calado D.P., Patterson H.C., Zhang B., Wang J., Henderson J.M., Kutok J.L., Rajewsky K. Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat. Immunol. 2008, 9:405-414.
57. Yaginuma H., Tomita M., Takashita N., McKay S.E., Cardwell C., Yin Q.W., Oppenheim R.W. A novel type of programmed neuronal death in the cervical spinal cord of the chick embryo. J.Neurosci. 1996, 16:3685-3703.
58. Zhang S., Taghibiglou C., Girling K., Dong Z., Lin S.Z., Lee W., Shyu W.C., Wang Y.T. Critical role of increased PTEN nuclear translocation in excitotoxic and ischemic neuronal injuries. J.Neurosci. 2013, 33:7997-8008.
59. Zhang Y., Ueno Y., Liu X.S., Buller B., Wang X., Chopp M., Zhang Z.G. The MicroRNA-17-92 cluster enhances axonal outgrowth in embryonic cortical neurons. J.Neurosci. 2013, 33:6885-6894.
60. Kirby J., Ning K., Ferraiuolo L., Heath P.R., Ismail A., Kuo S.W., Valori C.F., Cox L., Sharrack B., Wharton S.B., et al. Phosphatase and tensin homologue/protein kinase B pathway linked to motor neuron survival in humansuperoxide dismutase 1-related amyotrophic lateral sclerosis. Brain 2011, 134:506-517.