The catalytic subunit of telomerase protects neurons against amyloid β- peptide-induced apoptosis

Journal of Neurochemistry

Volumn 75, Issue 1, 2000, Pages 117-124

  Zhu, Haiyan ^a   Fu, Weiming ^a   Mattson, Mark P ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

3' Azido 2',3' dideoxythymidine; Alzheimer's disease; Caspase; Mitochondrial transmembrane potential; Reverse transcriptase

Indexed keywords

AMYLOID BETA PROTEIN; TELOMERASE; THYMIDINE DERIVATIVE;

ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME SUBUNIT; GENE OVEREXPRESSION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOUSE; NERVE CELL; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; APOPTOSIS; CATALYTIC DOMAIN; CELLS, CULTURED; DNA-BINDING PROTEINS; EMBRYO; ENZYME INHIBITORS; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICE; MITOCHONDRIA; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; OXIDATIVE STRESS; PC12 CELLS; RATS; RNA; TELOMERASE;

ANIMALIA;

EID: 0034086553     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0750117.x     Document Type: Article

References (62)

1. Adamec E., Vonsattel J. P., and Nixon R. A. (1999) DNA strand breaks in Alzheimer's disease. Brain Res. 849, 67-77.
2. Aloyz R. S., Bamji S. X., Pozniak C. D., Toma J. G., Atwal J., Kaplan D. R., and Miller F. D. (1998) p53 is essential for developmental neuron death as regulated by the TrkA and p75 neurotrophin receptors. J. Cell Biol. 143, 1691-1703.
3. Behl C., Davis J. B., Lesley R., and Schubert D. (1994) Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77, 817-827.
4. Bodnar A. G., Ouellette M., Frolkis M., Holt S. E., Chiu C. P., Morin G. B., Harley C. B., Shay J. W., Lichtsteiner S., and Wright W. E. (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279, 349-352.
5. Bohr V. A. and Anson R. M. (1995) DNA damage, mutation and fine structure DNA repair in aging. Mutat. Res. 338, 25-34.
6. Broccoli D., Smogorzewska A., Chong L., and de Lange T. (1997) Human telomeres contain two distinct Myb-related proteins, TRFI and TRF2. Nat. Genet. 17, 231-239.
7. Chan S. L., Griffin W. S. T., and Mattson M. P. (1999) Evidence for caspase-mediated cleavage of AMPA receptor subunits in neuronal apoptosis and in Alzheimer's disease. J. Neurosci. Res. 57, 315-323.
8. Chin L., Artandi S. E., Shen Q., Tam A., Lee S. L., Gottlieb G. J., Greider C. W., and DePinho R. A. (1999) p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97, 527-538.
9. Cregan S. P., MacLaurin J. G., Craig C. G., Robertson G. S., Nicholson D. W., Park D. S., and Slack R. S. (1999) Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. J. Neurosci. 19, 7860-7869.
10. Crumrine R. C., Thomas A. L., and Morgan P. F. (1994) Attenuation of p53 expression protects against focal ischemic damage in transgenic mice. J. Cereb. Blood Flow Metab. 14, 887-891.
11. de la Monte S. M., Sohn Y. K., and Wands J. R. (1997) Correlates of p53- and Fas (CD95)-mediated apoptosis in Alzheimer's disease. J. Neurol. Sci. 152, 73-83.
12. Deng G., Su J. H., Ivins K. J., Van Houten B., and Cotman C. W. (1999) Bcl-2 facilitates recovery from DNA damage after oxidative stress. Exp. Neurol. 159, 309-318.
13. Feng J., Funk W. D., Wang S. S., Weinricn S. L., Avilion A. A., Chiu C. P., Adams R. R., Chang E., Allsopp R. C., Yu J., Le S., West M. D., Harley C. B., Andrews W. H., Greider C. W., and Villeponteau B. (1995) The RNA component of human telomerase. Science 269, 1236-1241.
14. Fu W., Begley J. G., Killen M. W., and Mattson M. P. (1999) Antiapoptotic role of telomerase in pheochromocytoma cells. J. Biol. Chem. 274, 7264-7271.
15. Fu W., Killen M., Pandita T., and Mattson M. P. (2000) The catalytic subunit of telomerase is expressed in developing brain neurons and serves a cell survival-promoting function. J. Mol. Neurosci. 14, 3-15.
16. Gomez D. E., Tejera A. M., and Olivero O. A. (1998) Irreversible telomere shortening by 3′-azido-2′,3′-dideoxythymidine (AZT) treatment. Biochem. Biophys. Res. Commun. 246, 107-110.
17. Goodman Y. and Mattson M. P. (1994) Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury. Exp. Neurol. 128, 1-12.
18. Greenberg R. A., Allsopp R. C., Chin L., Morin G. B., and DePinho R. A. (1998) Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation. Oncogene 16, 1723-1730.
19. Greider C. W. (1998) Telomerase activity, cell proliferation, and cancer. Proc. Natl. Acad. Sci. USA 95, 90-92.
20. Greider C. W. and Blackburn E. H. (1989) A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature 337, 331-337.
21. Guo Q., Sopher B. L., Pham D. G., Furukawa K., Robinson N., Martin G. M., and Mattson M. P. (1997) Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid β-peptide: involvement of calcium and oxyradicals. J. Neurosci. 17, 4212-4222.
22. Guo Q., Fu W., Xie J., Luo H., Sells S. F., Geddes J. W., Bondada V., Rangnekar V., and Mattson M. P. (1998) Par-4 is a novel mediator of neuronal degeneration associated with the pathogenesis of Alzheimer's disease. Nat. Med. 4, 957-962.
23. Guo Q., Sebastian L., Sopher B. L., Miller M. W., Ware C. B., Martin G. M., and Mattson M. P. (1999) Increased vulnerability of hippocampal neurons from presenilin-1 mutant knock-in mice to amyloid β-peptide toxicity: central roles of superoxide production and caspase activation. J. Neurochem. 72, 1019-1029.
24. Hahn W. C., Stewart S. A., Brooks M. W., York S. G., Eaton E., Kurachi A., Beijersbergen R. L., Knoll J. H., Meyerson M., and Weinberg R. A. (1999) Inhibition of telomerase limits the growth of human cancer cells. Nat. Med. 5, 1164-1170.
25. Harley C. B. (1991) Telomere loss: mitotic clock or genetic time bomb? Mutat. Res. 256, 271-282.
26. Harrington L., Zhou W., McPhail T., Oulton R., Yeung D. S., Mar V., Bass M. B., and Robinson M. O. (1997) Human telomerase contains evolutionarily conserved catalytic and structural subunits. Genes Dev. 11, 3109-3115.
27. Jordan J., Galindo M. F., Prehn J. H., Weichselbaum R. R., Beckett M., Ghadge G. D., Roos R. P., Leiden J. M., and Miller R. J. (1997) p53 expression induces apoptosis in hippocampal pyramidal neuron cultures. J. Neurosci. 17, 1397-1405.
28. Karlseder J., Broccoli D., Dai Y., Hardy S., and de Lange T. (1999) p53-and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283, 1321-1325.
29. Keller J. N., Pang Z., Geddes J. W., Begley J. G., Germeyer A., Waeg G., and Mattson M. P. (1997) Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: role of the lipid peroxidation product 4-hydroxynonenal. J. Neurochem. 69, 273-284.
30. Keller J. N., Kindy M. S., Holtsberg F. W., St Clair D. K., Yen H. C., Germeyer A., Steiner S. M., Bruce-Keller A. J., Hutchins J. B., and Mattson M. P. (1998) Mitochondrial MnSOD prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation and mitochondrial dysfunction. J. Neurosci. 18, 687-697.
31. Kim N. W., Piatyszek M. A., Prowse K. R., Harley C. B., West M. D., Ho P. L. C., Coviello G. M., Wright W. E., Weinrich S. L., and Shay J. W. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015.
32. Kruman I., Bruce-Keller A. J., Bredesen D. W., Waeg G., and Mattson M. P. (1997) Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J. Neurosci. 17, 5089-5100.
33. LaFerla F. M., Hall C. K., Ngo L., and Jay G. (1996) Extracellular deposition of beta-amyloid upon p53-dependent neuronal cell death in transgenic mice. J. Clin. Invest. 98, 1626-1632.
34. Le W. D., Colom L. V., Xie W. J., Smith R. G., Alexianu M., and Appel S. H. (1995) Cell death induced by β-amyloid 1-40 in MES 23.5 hybrid clone: the role of nitric oxide and NMDA-gated channel activation leading to apoptosis. Brain Res. 686, 49-60.
35. Li H., Cao Y., Berndt M. C., Funder J. W., and Liu J. P. (1999a) Molecular interactions between telomerase and the tumor suppressor protein p53 in vitro. Oncogene 18, 6785-6794.
36. Li P. F., Dietz R., and von Harsdorf R. (1999b) p53 regulates mitochondrial membrane potential through reactive oxygen species and induces cytochrome c-independent apoptosis blocked by Bcl-2. EMBO J. 18, 6027-6036.
37. Lingner J., Hughes T. R., Shevchenko A., Mann M., Lundblad V., and Cech T. R. (1997) Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561-567.
38. Liu J. P. (1999) Studies of the molecular mechanisms in the regulation of telomerase activity. FASEB J. 13, 2091-2104.
39. Loo D., Copani A., Pike C., Whittemore E., Walencewicz A., and Cotman C. W. (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
40. 2+ homeostasis and cell death. J. Neurosci. 15, 6239-6249.
41. Mark R. J., Lovell M. A., Markesbery W. R., Uchida K., and Mattson M. P. (1997) A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68, 255-264.
42. Masliah E., Mallory M., Alford M., Tanaka S., and Hansen L. A. (1998) Caspase dependent DNA fragmentation might be associated with excitotoxicity in Alzheimer disease. J. Neuropathol. Exp. Neurol. 57, 1041-1052.
43. Mattson M. P. (1997) Cellular actions of β-amyloid precursor protein, and its soluble and fibrillogenic peptide derivatives. Physiol. Rev. 77, 1081-1132.
44. Mattson M. P., Cheng B., Davis D., Bryant K., Lieberburg I., and Rydel R. E. (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12, 376-389.
45. Mattson M. P., Goodman Y., Luo H., Fu W., and Furukawa K. (1997) Activation of NF-κB protects hippocampal neurons against oxidative stress-induced apoptosis: evidence for induction of Mn-SOD and suppression of peroxynitrite production and protein tyrosine nitration. J. Neurosci. Res. 49, 681-697.
46. Mattson M. P., Partin J., and Begley J. G. (1998) Amyloid β-peptide induces apoptosis-related events in synapses and dendrites. Brain Res. 807, 167-176.
47. Murakami J., Nagai N., Shigemasa K., and Ohama K. (1999) Inhibition of telomerase activity and cell proliferation by a reverse transcriptase inhibitor in gynaecological cancer cell lines. Eur. J. Cancer 35, 1027-1034.
48. Reichman T. W., Albanell J., Wang X., Moore M. A. S., and Studzinski G. P. (1997) Downregulation of telomerase activity in HL60 cells by differentiating agents is accompanied by increased expression of telomerase-associated protein. J. Cell. Biochem. 67, 13-23.
49. Rhyu M. S. (1995) Telomeres, telomerase and immortality. J. Natl. Cancer Inst. 87, 884-894.
50. Sharma H. W., Sokoloski J. A., Perez J. R., Maltese J. Y., Sartorelli A. C., Stein C. A., Nichols G., Khaled Z., Telang N. T., and Narayanan R. (1995) Differentiation of immortal cells inhibits telomerase activity. Proc. Natl. Acad. Sci. USA 92, 12343-12346.
51. Smale G., Nichols N. R., and Brady D. R. (1994) Evidence for apoptotic cell death in Alzheimer's disease. Exp. Neurol. 133, 225-230.
52. Strahl C. and Blackburn E. H. (1996) Effects of reverse transcriptase inhibitors on telomere length and telomerase activity in two immortalized human cell lines. Mol. Cell. Biol. 16, 53-65.
53. Su J. H., Anderson A. J., Cummings B., and Cotman C. W. (1994) Immunocytochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529-2533.
54. Su J. H., Deng G., and Cotman C. W. (1997) Neuronal DNA damage precedes tangle formation and is associated with up-regulation of nitrotyrosine in Alzheimer's disease brain. Brain Res. 774, 193-199.
55. Torp R., Su J. H., Deng G., and Cotman C. W. (1998) GADD45 is induced in Alzheimer's disease, and protects against apoptosis in vitro. Neurobiol. Dis. 5, 245-252.
56. Tortosa A., Lopez E., and Ferrer I. (1998) Bcl-2 and Bax protein expression in Alzheimer's disease. Acta Neuropathol. (Berl.) 95, 407-412.
57. van Steensel B. and de Lange T. (1997) Control of telomere length by the human telomeric protein TRF1. Nature 385, 740-743.
58. Xiang H., Kinoshita Y., Knudson C. M., Korsmeyer S. J., Schwartzkroin P. A., and Morrison R. S. (1998) Bax involvement in p53-mediated neuronal cell death. J. Neurosci. 18, 1363-1373.
59. Yegorov Y. E., Chernov D. N., Akimov S. S., Bolsheva N. L., Krayevsky A. A., and Zelenin A. V. (1996) Reverse transcriptase inhibitors suppress telomerase function and induce senescence-like processes in cultured mouse fibroblasts. FEBS Lett. 389, 115-118.
60. Zhang J., Pieper A., and Snyder S. H. (1995) Poly(ADP-ribose) synthetase activation: an early indicator of neurotoxic DNA damage. J. Neurochem. 65, 1411-1414.
61. Zhang S., Liu J., Saafi E. L., and Cooper G. J. (1999) Induction of apoptosis by human amylin in RINm5F islet beta-cells is associated with enhanced expression of p53 and p21WAF1/CIP1. FEBS Lett. 455, 315-320.
62. Zhu J., Wang H., Bishop J. M., and Blackburn E. H. (1999) Telomerase extends the lifespan of virus-transformed human cells without net telomere lengthening. Proc. Natl. Acad. Sci. USA 96, 3723-3728.