Global analysis of gene expression in NGF-deprived sympathetic neurons identifies molecular pathways associated with cell death

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Kristiansen, Mark ^a   Menghi, Francesca ^a   Hughes, Rosie ^a   Hubank, Mike ^a   Ham, Jonathan ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CEP 11004; ENZYME INHIBITOR; MIXED LINEAGE KINASE; NERVE GROWTH FACTOR; PROTEIN C JUN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL LEVEL; CONTROLLED STUDY; DDIT3 GENE; DNA MICROARRAY; DOWN REGULATION; GENE; GENE ACTIVATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE TARGETING; GENOME ANALYSIS; MXI1 GENE; NDRG1 GENE; NERVE CELL CULTURE; NONHUMAN; RAT; REAL TIME POLYMERASE CHAIN REACTION; SYMPATHETIC NERVE CELL; TRIB3 GENE; TXNIP GENE; ADRENERGIC SYSTEM; ANIMAL; BINDING SITE; CYTOLOGY; EXON; GENETICS; METABOLISM; NERVE CELL; PROMOTER REGION; UPREGULATION; VALIDATION STUDY;

ANIMALS; BINDING SITES; CELL DEATH; DOWN-REGULATION; EXONS; GENE EXPRESSION PROFILING; NERVE GROWTH FACTOR; NEURONS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-JUN; RATS; REAL-TIME POLYMERASE CHAIN REACTION; SYMPATHETIC NERVOUS SYSTEM; UP-REGULATION;

EID: 80455158292     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-551     Document Type: Article

References (65)

1. Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci 1991, 14:453-501. 10.1146/annurev.ne.14.030191.002321, 2031577.
2. Jacobson MD, Weil M, Raff MC. Programmed cell death in animal development. Cell 1997, 88:347-54. 10.1016/S0092-8674(00)81873-5, 9039261.
3. Buss RR, Sun W, Oppenheim RW. Adaptive roles of programmed cell death during nervous system development. Annu Rev Neurosci 2006, 29:1-35. 10.1146/annurev.neuro.29.051605.112800, 16776578.
4. Yuan J, Yankner BA. Apoptosis in the nervous system. Nature 2000, 407:802-809. 10.1038/35037739, 11048732.
5. Deckwerth TL, Johnson EM. Temporal analysis of events associated with programmed cell death (apoptosis) of sympathetic neurons deprived of nerve growth factor. J Cell Biol 1993, 123:1207-22. 10.1083/jcb.123.5.1207, 2119882, 7503996.
6. Edwards SN, Tolkovsky AM. Characterization of apoptosis in cultured rat sympathetic neurons after nerve growth factor withdrawal. J Cell Biol 1994, 124(4):537-546. 10.1083/jcb.124.4.537, 2119915, 8106551.
7. Deshmukh M, Johnson EM. Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 1998, 21:695-705. 10.1016/S0896-6273(00)80587-5, 9808457.
8. Neame SJ, Rubin LL, Philpott KL. Blocking cytochrome c activity within intact neurons inhibits apoptosis. J Cell Biol 1998, 142:1583-93. 10.1083/jcb.142.6.1583, 2141762, 9744886.
9. Putcha GV, Johnson EM. Men are worms: neuronal cell death in C elegans and vertebrates. Cell Death Differ 2004, 11(1):38-48. 10.1038/sj.cdd.4401352, 14647239.
10. Wright KM, Vaughn AE, Deshmukh M. Apoptosome dependent caspase-3 activation pathway is non-redundant and necessary for apoptosis in sympathetic neurons. Cell Death Differ 2007, 14(3):625-633. 10.1038/sj.cdd.4402024, 16932756.
11. Conradt B. Genetic control of programmed cell death during animal development. Annu Rev Genet 2009, 43:493-523. 10.1146/annurev.genet.42.110807.091533, 2806233, 19886811.
12. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, Johnson EM. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 1998, 106:829-844.
13. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM. Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 1994, 127:1717-27. 10.1083/jcb.127.6.1717, 2120296, 7798322.
14. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, Rubin LL. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 1995, 14:927-39. 10.1016/0896-6273(95)90331-3, 7748560.
15. Lipscomb EA, Sarmiere PD, Crowder RJ, Freeman RS. Expression of the SM-20 gene promotes death in nerve growth factor-dependent sympathetic neurons. J Neurochem 1999, 73(1):429-432.
16. Putcha GV, Moulder KL, Golden JP, Bouillet P, Adams JA, Strasser A, Johnson EM. Induction of BIM, a proapoptotic BH3-only BCL-2 family member, is critical for neuronal apoptosis. Neuron 2001, 29(3):615-628. 10.1016/S0896-6273(01)00238-0, 11301022.
17. Whitfield J, Neame SJ, Paquet L, Bernard O, Ham J. Dominant-negative c-Jun promotes neuronal survival by reducing BIM expression and inhibiting mitochondrial cytochrome c release. Neuron 2001, 29:629-43. 10.1016/S0896-6273(01)00239-2, 11301023.
18. Palmada M, Kanwal S, Rutkoski NJ, Gustafson-Brown C, Johnson RS, Wisdom R, Carter BD. c-jun is essential for sympathetic neuronal death induced by NGF withdrawal but not by p75 activation. J Cell Biol 2002, 158(3):453-461. 10.1083/jcb.200112129, 2173823, 12163468.
19. Besirli CG, Wagner EF, Johnson EM. The limited role of NH2-terminal c-Jun phosphorylation in neuronal apoptosis: identification of the nuclear pore complex as a potential target of the JNK pathway. J Cell Biol 2005, 170(3):401-411. 10.1083/jcb.200501138, 2171472, 16061693.
20. Jacobs WB, Govoni G, Ho D, Atwal JK, Barnabe-Heider F, Keyes WM, Mills AA, Miller FD, Kaplan DR. p63 is an essential pro-apoptotic protein during neural development. Neuron 2005, 48(5):743-756. 10.1016/j.neuron.2005.10.027, 16337913.
21. Wyttenbach A, Tolkovsky AM. The BH3-only protein Puma is both necessary and sufficient for neuronal apoptosis induced by DNA damage in sympathetic neurons. J Neurochem 2006, 96(5):1213-1226. 10.1111/j.1471-4159.2005.03676.x, 16478523.
22. Bishop T, Gallagher D, Pascual A, Lygate CA, de Bono JP, Nicholls LG, Ortega-Saenz P, Oster H, Wijeyekoon B, Sutherland AI, Grosfeld A, Aragones J, Schneider M, van Geyte K, Teixeira D, Diez-Juan A, Lopez-Barneo J, Channon KM, Maxwell PH, Pugh CW, Davies AM, Carmeliet P, Ratcliffe PJ. Abnormal sympathoadrenal development and systemic hypotension in PHD3-/- mice. Mol Cell Biol 2008, 28(10):3386-3400. 10.1128/MCB.02041-07, 2423159, 18332118.
23. Schlisio S, Kenchappa RS, Vredeveld LC, George RE, Stewart R, Greulich H, Shahriari K, Nguyen NV, Pigny P, Dahia PL, Pomeroy SL, Maris JM, Look AT, Meyerson M, Peeper DS, Carter BD, Kaelin WG. The kinesin KIF1Bbeta acts downstream from EglN3 to induce apoptosis and is a potential 1p36 tumor suppressor. Genes Dev 2008, 22(7):884-893. 10.1101/gad.1648608, 2279200, 18334619.
24. Kristiansen M, Hughes R, Patel P, Jacques TS, Clark AR, Ham J. Mkp1 is a c-Jun target gene that antagonises JNK-dependent apoptosis in sympathetic neurons. J Neurosci 2010, 30(32):10820-10832. 10.1523/JNEUROSCI.2824-10.2010, 3044878, 20702711.
25. Virdee K, Bannister AJ, Hunt SP, Tolkovsky AM. Comparison between the timing of JNK activation, c-Jun phosphorylation, and onset of death commitment in sympathetic neurones. J Neurochem 1997, 69:550-61.
26. Whitfield J, Babij C, Rubin LL, Ham J. Role of the Jun kinase pathway in the regulation of c-Jun expression and apoptosis in sympathetic neurons. J Neurosci 1998, 18:1713-1724.
27. Eilers A, Whitfield J, Shah B, Spadoni C, Desmond H, Ham J. Direct inhibition of c-Jun N-terminal kinase in sympathetic neurones prevents c-jun promoter activation and NGF withdrawal-induced death. J Neurochem 2001, 76(5):1439-1454. 10.1046/j.1471-4159.2001.00150.x, 11238729.
28. Harding TC, Xue L, Bienemann A, Haywood D, Dickens M, Tolkovsky AM, Uney JB. Inhibition of JNK by overexpression of the JNK binding domain of JIP-1 prevents apoptosis in sympathetic neurons. J Biol Chem 2001, 276(7):4531-4534. 10.1074/jbc.C000815200, 11121395.
29. Mota M, Reeder M, Chernoff J, Bazenet CE. Evidence for a role of mixed lineage kinases in neuronal apoptosis. J Neurosci 2001, 21:4949-4957.
30. Xu Z, Maroney AC, Dobrzanski P, Kukekov NV, Greene LA. The MLK family mediates c-Jun N-terminal kinase activation in neuronal apoptosis. Mol Cell Biol 2001, 21:4713-4724. 10.1128/MCB.21.14.4713-4724.2001, 87148, 11416147.
31. Freeman RS, Estus S, Johnson EM. Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of Cyclin D1 during programmed cell death. Neuron 1994, 12(2):343-355. 10.1016/0896-6273(94)90276-3, 8110463.
32. Imaizumi K, Tsuda M, Imai Y, Wanaka A, Takagi T, Tohyama M. Molecular cloning of a novel polypeptide, DP5, induced during programmed neuronal death. J Biol Chem 1997, 272(30):18842-18848. 10.1074/jbc.272.30.18842, 9228060.
33. Kojima S, Mayumi-Matsuda K, Suzuki H, Sakata T. Molecular cloning of rat GADD45γ, gene induction and its role during neuronal cell death. FEBS Letts 1999, 446:313-317.
34. Towers E, Gilley J, Randall R, Hughes R, Kristiansen M, Ham J. The proapoptotic dp5 gene is a direct target of the MLK-JNK-c-Jun pathway in sympathetic neurons. Nucleic Acids Res 2009, 37:3044-3060. 10.1093/nar/gkp175, 2685101, 19304750.
35. Mayumi-Matsuda K, Kojima S, Suzuki H, Sakata T. Identification of a novel kinase- like gene induced during neuronal cell death. Biochem Biophys Res Commun 1999, 258(2):260-264. 10.1006/bbrc.1999.0576, 10329375.
36. Franklin JL. Redox regulation of the intrinsic pathway in neuronal apoptosis. Antioxid Redox Signalling 2011, 14(8):1437-1448.
37. Desagher S, Severac D, Lipkin A, Bernis C, Ritchie W, Le Digarcher A, Journot L. Genes regulated in neurons undergoing transcription-dependent apoptosis belong to signaling pathways rather than the apoptotic machinery. J Biol Chem 2005, 280(7):5693-5702.
38. Lassot I, Robbins I, Kristiansen M, Rahmeh R, Jaudon F, Magiera MM, Mora S, Vanhille L, Lipkin A, Pettmann B, Ham J, Desagher S. Trim17, a novel E3 ubiquitin-ligase, initiates neuronal apoptosis. Cell Death Differ 2010, 17(12):1928-1941. 10.1038/cdd.2010.73, 3016602, 20559321.
39. Jiang X, Kim HE, Shu H, Zhao Y, Zhang H, Kofron J, Donnelly J, Burns D, Ng SC, Rosenberg S, Wang X. Distinctive roles of PHAP proteins and prothymosin-alpha in a death regulatory pathway. Science 2003, 299(5604):223-226. 10.1126/science.1076807, 12522243.
40. Kirkland RA, Franklin JL. Evidence for redox regulation of cytochrome c release during programmed neuronal death: antioxidant effects of protein synthesis and caspase inhibition. J Neurosci 2001, 21(6):1949-1963.
41. Prieto-Alamo MJ, Jurado J, Gallardo-Madueno R, Monje-Casas F, Holmgren A, Pueyo C. Transcriptional regulation of glutaredoxin and thioredoxin pathways and related enzymes in response to oxidative stress. J Biol Chem 2000, 275(18):13398-13405. 10.1074/jbc.275.18.13398, 10788450.
42. Nordberg J, Arner ES. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 2001, 31(11):1287-1312. 10.1016/S0891-5849(01)00724-9, 11728801.
43. Nishiyama A, Matsui M, Iwata S, Hirota K, Masutani H, Nakamura H, Takagi Y, Sono H, Gon Y, Yodoi J. Identification of thioredoxin-binding protein/vitamin D(3) up- regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem 1999, 274(31):21645-21650. 10.1074/jbc.274.31.21645, 10419473.
44. Junn E, Han SH, Im JY, Yang Y, Cho EW, Um HD, Kim DK, Lee KW, Han PL, Rhee SG, Choi I. Vitamin D3 up-regulated protein 1 mediates oxidative stress via suppressing the thioredoxin function. J Immuno 2000, 164(12):6287-6295.
45. Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 2006, 13(3):385-392. 10.1038/sj.cdd.4401778, 16397584.
46. Smith MI, Deshmukh M. Endoplasmic reticulum stress-induced apoptosis requires bax for commitment and Apaf-1 for execution in primary neurons. Cell Death Differ 2007, 1(5):1011-1019.
47. Breckenridge DG, Germain M, Mathai JP, Nguyen M, Shore GC. Regulation of apoptosis by endoplasmic reticulum pathways. Oncogene 2003, 22(53):8608-8618. 10.1038/sj.onc.1207108, 14634622.
48. Rao RV, Ellerby HM, Bredesen DE. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004, 11(4):372-380. 10.1038/sj.cdd.4401378, 14765132.
49. Guyton KZ, Xu Q, Holbrook NJ. Induction of the mammalian stress response gene GADD153 by oxidative stress: role of AP-1 element. Biochem J 1996, 314(Part 2):547-554. 1217084, 8670069.
50. Maytin EV, Ubeda M, Lin JC, Habener JF. Stress-inducible transcription factor CHOP/gadd153 induces apoptosis in mammalian cells via p38 kinase-dependent and -independent mechanisms. Exp Cell Res 2001, 267(2):193-204. 10.1006/excr.2001.5248, 11426938.
51. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 1998, 12(7):982-995. 10.1101/gad.12.7.982, 316680, 9531536.
52. Gotoh T, Terada K, Oyadomari S, Mori M. hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell Death Differ 2004, 11(4):390-402. 10.1038/sj.cdd.4401369, 14752510.
53. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. TRB3, a novel ER stress- inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 2005, 24(6):1243-1255. 10.1038/sj.emboj.7600596, 556400, 15775988.
54. Puthalakath H, O'Reilly LA, Gunn P, Lee L, Kelly PN, Huntington ND, Hughes PD, Michalak EM, McKimm-Breschkin J, Motoyama N, Gotoh T, Akira S, Bouillet P, Strasser A. ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 2007, 129(7):1337-1349. 10.1016/j.cell.2007.04.027, 17604722.
55. Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, Cregan SP. Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP- mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 2010, 30(50):16938-16948. 10.1523/JNEUROSCI.1598-10.2010, 21159964.
56. Gilley J, Coffer PJ, Ham J. FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 2003, 162(4):613-622. 10.1083/jcb.200303026, 2173804, 12913110.
57. Hughes R, Kristiansen M, Lassot I, Desagher S, Mantovani R, Ham J. NF-Y is essential for expression of the proapoptotic bim gene in sympathetic neurons. Cell Death Differ 2011, 18(6):937-947. 10.1038/cdd.2010.166, 21164521.
58. Delpuech O, Griffiths B, East P, Essafi A, Lam EW, Burgering B, Downward J, Schulze A. Induction of Mxi1-SR alpha by FOXO3a contributes to repression of Myc- dependent gene expression. Mol Cell Biol 2007, 27(13):4917-4930. 10.1128/MCB.01789-06, 1951505, 17452451.
59. Schreiber-Agus N, DePinho RA. Repression by the Mad(Mxi1)-Sin3 complex. Bioessays 1998, 20(10):808-818. 10.1002/(SICI)1521-1878(199810)20:10<808::AID-BIES6>3.0.CO;2-U, 9819568.
60. Wartiovaara K, Barnabe-Heider F, Miller FD, Kaplan DR. N-myc promotes survival and induces S-phase entry of postmitotic sympathetic neurons. J Neurosci 2002, 22(3):815-824.
61. Whitfield J, Neame SJ, Ham J. Methods for culturing primary sympathetic neurons and for determining neuronal viability. Methods Mol Biol 2004, 282:157-168.
62. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004, 3:Article3.
63. Huang da W, Lempicki RA. Systemic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2008, 4(1):44-57.
64. Hughes R, Gilley J, Kristiansen M, Ham J. The MEK-ERK pathway negatively regulates bim expression through the 3' UTR in sympathetic neurons. BMC Neurosci 2011, 12(1):69. 10.1186/1471-2202-12-69, 3146425, 21762482.
65. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25(4):402-408. 10.1006/meth.2001.1262, 11846609.