Alterations in G1 to S phase cell-cycle regulators during amyotrophic lateral sclerosis

American Journal of Pathology

Volumn 162, Issue 3, 2003, Pages 823-835

  Ranganathan, Srikanth ^a   Bowser, Robert ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; CYCLIN D; CYCLIN DEPENDENT KINASE; CYCLINE; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL LOSS; CONTROLLED STUDY; CYTOPLASM; FEMALE; GLIA; HUMAN; HUMAN TISSUE; MALE; MOTONEURON; MOTOR CORTEX; NERVE CELL NECROSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SENSORY CORTEX; SPINAL CORD; UPREGULATION;

EID: 0037372292     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63879-5     Document Type: Article

References (74)

1. Chou SM: Pathology of motor system disorder. Motor Neuron Disease, Biology and Management. Edited by PN Leigh, M Swash. London, Springer-Verlag, 1995, pp 53-92
2. Eisen A, Weber M: The motor cortex and amyotrophic lateral sclerosis. Muscle Nerve 2001, 24:564-573
3. Rosen DR, Siddique TS, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng H-X, Rahmani Z, Krizus A, McKenna-Yasek D, Cayabyab A, Gaston SM, Berger R, Tanzi RE, Halperin JJ, Herzfeldt B, Van den Bergh R, Hung W-Y, Bird T, Deng G, Mulder DW, Smyth C, Laing NG, Soriano E, Pericak-Vance MA, Haines J, Rouleau GA, Gusella JS, Horvitz HR, Brown Jr RH: Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62
4. Rosen DR, Bowling AC, Patterson D, Usdin TB, Sapp P, Mezey E, McKenna-Yasek D, O'Regan JP, Rahman Z, Ferrante RJ, Brownstein MJ, Kowall NW, Beal MF, Horvitz HR, Brown Jr RH: A frequent ala 4 to val superoxide dismutase-1 mutation is associated with a rapidly progressive familial amyotrophic lateral sclerosis. Hum Mol Genet 1994, 3:981-987
5. Yang Y, Hentati A, Deng HX, Dabbagh O, Sasaki T, Hirano M, Hung WY, Ouahchi K, Yan J, Azim AC, Cole N, Gascon G, Yagmour A, Ben-Hamida M, Pericak-Vance M, Hentati F, Siddique T: The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat Genet 2001, 29:160-165
6. Hadano S, Hand CK, Osuga H, Yanagisawa Y, Otomo A, Devon RS, Miyamoto N, Showguchi-Miyata J, Okada Y, Singaraja R, Figlewicz DA, Kwiatkowski T, Hosler BA, Sagie T, Skaug J, Nasir J, Brown Jr RH, Scherer SW, Rouleau GA, Hayden MR, Ikeda JE: A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat Genet 2001, 29:166-173
7. Kunst CB, Messer L, Gordon J, Haines J, Patterson D: Genetic mapping of a mouse modifier gene that can prevent ALS onset. Genomics 2000, 70:181-189
8. Cleveland DW, Rothstein JD: From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2001, 2:806-819
9. Kruman II, Pedersen WA, Springer JE, Mattson MP: ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp Neurol 1999, 160:28-39
10. Shaw PJ, Egget CJ: Molecular factors underlying selective vulnerability of motor neurons to neurodegeneration in amyotrophic lateral sclerosis. J Neurol 2000, 247(Suppl 1):1/17-1/27
11. Tu P-H, Gurney ME, Julien J-P, Lee VM-Y, Trojanowski JQ: Oxidative stress, mutant SOD-1 and neurofilament pathology in transgenic mouse models of motor neuron disease. Lab Invest 1997, 76:441-456
12. Kong J, Xu Z: Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J Neurosci 1998, 18:3241-3250
13. Lee MK, Marszalek JR, Cleveland DW: A mutant neurofilament subunit causes massive, selective motor neuron death: implications for the pathogenesis of human motor neuron disease. Neuron 1994, 13:975-988
14. Martin JE: Neurotrophic factors and neurodegeneration. Motor Neuron Disease, Biology and Management. Edited by PN Leigh, M Swash, London, Springer-Verlag, 1995, pp 241-258
15. Mu X, He J, Anderson DW, Trojanowski JQ, Springer JE: Altered expression of bcl-2 and bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann Neurol 1996, 40:379-386
16. Copani A, Uberti D, Sortino MA, Bruno V, Nicoletti F, Memo M: Activation of cell-cycle-associated proteins in neuronal death: a mandatory or dispensable path? Trends Neurosci 2001, 24:25-31
17. Ross ME: Cell division and the nervous system: regulating the cycle from neural differentiation to death. Trends Neurosci 1996, 19:62-68
18. Freeman RS: The cell cycle and neuronal cell death. Cell Death and Diseases of the Nervous System. Edited by Koliatsos VE, Ratan RR. New Jersey, Humana Press Inc., 1999, pp 103-119
19. Heintz N: Cell death and the cell cycle: a relationship between transformation and neurodegeneration? Trends Biochem Sci 1993, 18:157-159
20. Weinberg RA: The retinoblastoma protein and cell cycle control. Cell 1995, 81:323-330
21. Jacks T, Fazeli A, Schmitt EM, Bronson RT, Goodell MA, Weinberg RA: Effects of an Rb mutation in the mouse. Nature 1992, 359:295-300
22. Lee EY-HP, Chang C-Y, Hu N, Wang Y-CJ, Lai C-C, Herrup K, Lee W-H, Bradley A: Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 1992, 359:288-294
23. Tsai KY, Hu Y, Macleod KF, Crowley D, Yamasaki L, Jacks T: Mutation of E2F-1 suppresses apoptosis and inappropriate S phase entry and extends survival of Rb-deficient mouse embryos. Mol Cell 1998, 2:293-304
24. Jordan-Sciutto K, Rhodes J, Bowser R: Altered subcellular distribution of transcriptional regulators in response to Aβ peptide and during Alzheimer disease. Mech Ageing Dev 2001, 123:11-20
25. Jordan-Sciutto KL, Malaiyandi LM, Bowser R: Altered distribution of cell cycle transcriptional regulators during Alzheimer disease. J Neuropathol Exp Neurol 2002, 61:358-367
26. Park DS, Farinelli SE, Greene LA: Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J Biol Chem 1996, 271:8161-8169
27. Park DS, Morris EJ, Greene LA, Geller HM: G1/S cell cycle blockers and inhibitors of cyclin-dependent kinases suppress camptothecin-induced neuronal apoptosis. J Neurosci 1997, 17:1256-1270
28. Park DS, Levine B, Ferrari G, Greene LA: Cyclin dependent kinase inhibitors and dominant negative cyclin dependent kinase 4 and 6 promote survival of NGF-deprived sympathetic neurons. J Neurosci 1997, 17:8975-8983
29. Park DS, Morris EJ, Padmanabhan J, Shelanski ML, Geller HM, Greene LA: Cyclin-dependent kinases participate in death of neurons evoked by DNA-damaging agents. J Cell Biol 1998, 143:457-467
30. Park DS, Morris EJ, Stefanis L, Troy CM, Shelanski ML, Geller HM, Greene LA: Multiple pathways of neuronal death induced by DNA-damaging agents, NGF deprivation, and oxidative stress J Neurosci 1998, 18:830-840
31. Park DS, Morris EJ, Bremner R, Keramaris E, Padmanabhan J, Rosenbaum M, Shelanski ML, Geller HM, Greene LA: Involvement of retinoblastoma family members and E2F/DP complexes in the death of neurons evoked by DNA damage. J Neurosci 2000, 20:3104-3114
32. O'Hare MJ, Hou ST, Morris EJ, Cregan SP, Xu Q, Slack RS, Park DS: Induction and modulation of cerebellar granule neuron death by E2F-1. J Biol Chem 2000, 275:25358-25364
33. Padmanabhan J, Park DS, Greene LA, Shelanski ML: Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J Neurosci 1999, 19;8747-8756
34. Giovanni A, Wirtz-Brugger F, Keramaris E, Slack R, Park DS: Involvement of cell cycle elements, cyclin-dependent kinases, pRb, and E2F-DP, in beta-amyloid-induced neuronal death. J Biol Chem 1999, 274:19011-19016
35. Giovanni A, Keramaris E, Morris EJ, Hou ST, O'Hare M, Dyson N, Robertson GS, Slack RS, Park DS: E2F1 mediates death of B-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase 3. J Biol Chem 2000, 275:11553-11560
36. Ilzecka J, Stelmasiak Z, Dobosz B: Interleukin-1beta converting enzyme/caspase-1 (ICE/caspase-1) and soluble APO-1/Fas/CD 95 receptor in amyotrophic lateral sclerosis patients. Acta Neurol Scand 2001, 103:255-258
37. Pasinelli P, Houseweart MK, Brown Jr RH, Cleveland DW: Caspase-1 and -3 are sequentially activated in motor neuron death in Cu, Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2000, 97:13901-13906
38. Yi FH, Lautrette C, Vermot-Desroches C, Bordessoule D, Couratier P, Wijdenes J, Preud'homme JL, Jauberteau MO: In vitro induction of neuronal apoptosis by anti-Fas antibody-containing sera from amyotrophic lateral sclerosis patients. J Neuroimmunol 2000, 109:211-220
39. Dyson N: The regulation of E2F by pRb-family proteins. Genes Dev 1998, 12:2245-2262
40. Black AR, Azizkhan-Clifford J: Regulation of E2F: a family of transcriptional factors involved in proliferation control. Gene 1999, 237:281-302
41. Chellappan SP, Heibert S, Mudryj M, Horowitz JM, Nevins JR: The E2F transcription factor is a cellular target for the RB protein. Cell 1991, 65:1053-1061
42. Thomas LB, Gates DJ, Richfield EK, O'Brien TF, Schweitzer JB, Steindler DA: DNA end labeling (TUNEL) in Huntington's disease and other neuropathological conditions. Exp Neurol 1995, 133:265-272
43. Li WP, Chan WY, Lai HW, Yew DT: Terminal dUTP nick end labeling (TUNEL) positive cells in the different regions of the brain in normal aging and Alzheimer patients. J Mol Neurosci 1997, 8:75-82
44. Martin LJ: Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism. J Neuropathol Exp Neurol 1999, 58:459-471
45. Bar-Peled O, Knudson M, Korsmeyer SJ, Rothstein JD: Motor neuron degeneration is attenuated in bax-deficient neurons in vitro. J Neurosci Res 1999, 55:542-556
46. Timsit S, Rivera S, Ouaghi P, Guischard F, Tremblay E, Ben-Ari Y, Khrestchatisky M: Increased cyclin D1 in vulnerable neurons in the hippocampus after ischaemia and epilepsy: a modulator of in vivo programmed cell death? Eur J Neurosci 1999, 11:263-278
47. Dobashi Y, Shoji M, Noguchi T, Kondo E, Katayama K, Kameya T: A novel apoptotic cascade mediated by CDK4 in rat pheochromocytoma PC12 cells. Biochem Biophys Res Commun 1999, 260:806-812
48. Li M, Ona VO, Guegan C, Chen M, Jackson-Lewis V, Andrews LJ, Olszewski AJ, Stieg PE, Lee JP, Przedborski S, Friedlander RM: Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000, 288:335-339
49. Vukosavic S, Stefanis L, Jackson-Lewis V, Guégan C, Romero N, Chen C, Dubois-Dauphin M, Przedborski S: Delaying caspase activation by bcl-2: a clue to disease retardation in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 2000, 20:9119-9125
50. Trinh E, Boutillier AL, Loeffler JP: Regulation of the retinoblastoma-dependent Mdm2 and E2F-1 signaling pathways during neuronal apoptosis. Mol Cell Neurosci 2001, 17:342-353
51. Sathasivam S, Ince PG, Shaw PJ: Apoptosis in amyotrophic lateral sclerosis: a review of the evidence. Neuropathol Appl Neurobiol 2001, 27:257-274
52. Macleod KF, Hu Y, Jacks T: Loss of Rb activates both p53-dependent and independent cell death pathways in the developing mouse nervous system. EMBO J 1996, 15:6178-6188
53. Phillips AC, Bates S, Ryan KM, Helin K, Vousden KH: Induction of DNA synthesis and apoptosis are separable functions of E2F-1. Genes Dev 1997, 11:1853-1863
54. Jordan-Sciutto K, Dragich JM, Bowser R: DNA binding activity of the fetal Alz-50 clone1 (FAC1) protein is enhanced by phosphorylation. Biochem Biophys Res Comm 1999, 260:785-789
55. Ranganathan S, Scudiere S, Bowser R: Hyperphosphorylation of the retinoblastoma gene product and altered subcellular distribution of E2F-1 in Alzheimer disease and amyotrophic lateral sclerosis. J Alzheimer Dis 2001, 3:377-385
56. Yang Y, Geldmacher DS, Herrup K: DNA replication precedes neuronal cell death in Alzheimer disease. J Neurosci 2001, 21:2661-2668
57. Vincent I, Jicha G, Rosado M, Dickson DW: Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer disease brain. J Neurosci 1997, 17:3588-3598
58. McShea A, Harris P, Webster K, Wahl A, Smith M: Abnormal expression of the cell cycle regulators p16 and cdk4 in Alzheimer disease. Am J Pathol 1997, 150:1933-1939
59. Jordan-Sciutto K, Wang G, Murphy-Corb M, Wiley C: Induction of cell cycle regulators in simian immunodeficiency virus encephalitis. Am J Pathol 2000, 157:497-507
60. Verona R, Moberg K, Estes S, Starz M, Vernon JP, Lees JA: E2F activity is regulated by cell cycle-dependent changes in subcellular localization. Mol Cell Biol 1997, 17:7268-7282
61. Lowe J: New pathological findings in amyotrophic lateral sclerosis. J Neurol Sci 1994, 124:38-51
62. Migheli A, Attanasio A, Schiffer D: Ubiquitin and neurofilament expression in anterior horn cells in amyotrophic lateral sclerosis: possible clues to the pathogenesis. Neuropathol Appl Neurobiol 1994, 20:282-289
63. He BP, Wen W, Strong MJ: Activated microglia (BV-2) facilitation of TNF-α-mediated motor neuron death in vitro. J Neuroimmunol 2002, 128:31-38
64. Qin X, Livingston DM, Kaelin WGJ, Adams PD: Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc Natl Acad Sci USA 1994, 91:10918-10922
65. Stiewe T, Putzer BM: Role of the p53-homologue p73 in E2F1-induced apoptosis. Nat Genet 2000, 26:464-469
66. Irwin M, Marin MC, Phillips AC, Seelan RS, Smith DI, Liu W, Flores ER, Tsai KY, Jacks T, Vousden KH, Kaelin Jr WG: Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 2000, 407:645-648
67. Stewart B, Phillips AC, Clark PA, Stott F, Peters G, Ludwig RL, Vousden KH: p14ARF links the tumor suppressors RB and p53. Nature 1998, 395:124-125
68. Moroni MC, Hickman ES, Denchi EL, Caprara G, Colli E, Cecconi F, Muller H, Helin K: Apaf-1 is a transcriptional target for E2F and p53. Nat Cell Biol 2001, 3:552-558
69. Luciakova K, Barath P, Li R, Zaid A, Nelson BD: Activity of the human cytochrome c1 promoter is modulated by E2F. Biochem J 2000, 351:251-256
70. Martin LJ: P53 is abnormally elevated and active in the CNS of patients with amyotrophic lateral sclerosis. Neurobiol Dis 2000, 7:613-622
71. Miyashita T, Reed JC: Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995, 80:293-299
72. Phillips AC, Ernst MK, Bates S, Rice NR, Vousden KH: E2F-1 potentiates cell death by blocking antiapoptotic signaling pathways. Mol Cell 1999, 4:771-781
73. Khursigara G, Orlinick JR, Chao MV: Association of the p75 neurotrophin receptor with TRAF6. J Biol Chem 1999, 274:2597-2600
74. Ye X, Mehlen P, Rabizadeh S, VanArsdale T, Zhang H, Shin H, Wang JJ, Leo E, Zapata J, Hauser CA, Reed JC, Bredesen DE: TRAF family proteins interact with the common neurotrophin receptor and modulate apoptosis induction. J Biol Chem 1999, 274:30202-30208