Human amylin induces 'apoptotic' pattern of gene expression concomitant with cortical neuronal apoptosis

Journal of Neurochemistry

Volumn 71, Issue 2, 1998, Pages 506-516

  Tucker, H Michael ^a   Rydel, Russell E ^b   Wright, Sarah ^b   Estus, Steven ^a,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Athena Neurosciences Inc   (United States)

^c NONE   (United States)

Author keywords

Alzheimer's disease; Amylin; Amyloid ; Apoptosis; c jun

Indexed keywords

AMYLIN; PROTEIN C FOS; TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; CHROMATIN CONDENSATION; CONCENTRATION RESPONSE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; NEUROTOXICITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; SEQUENCE HOMOLOGY;

EID: 0031754613     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.71020506.x     Document Type: Article

References (60)

1. Anderson A. J., Pike C. J., and Cotman C. W. (1995) Differential induction of immediate early gene proteins in cultured neurons by β-amyloid (Aβ): association of c-jun with Aβ-induced apoptosis. J. Neurochem. 65, 1487-1498.
2. Ankarcrona M., Dypbukt J., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., and Nicotera P. (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
3. Arispe N., Pollard H. B., and Rojas E. (1994) Beta-amyloid Ca (2+)-channel hypothesis for neuronal death in Alzheimer's disease. Mol. Cell. Biochem. 2, 119-125.
4. Baeuerle P. A. and Henkel P. (1994) Function and activation of NF-kappaB in the immune system. Annu. Rev. Immunol. 12, 141-179.
5. Baker S. J. and Reddy E. P. (1996) Transducers of life and death: TNF receptor superfamily and associated proteins. Oncogene 12, 1-9.
6. Beaumont K., Kenny M. A., Young A. A., and Rink T. J. (1993) High affinity amylin binding sites in rat brain. Mol. Pharmacol. 44, 493-497.
7. Behl C., Davis J. B., Klier F. G., and Schubert D. (1994a) Amyloid beta peptide induces necrosis rather than apoptosis. Brain Res. 645, 254-264.
8. Behl C, Davis J. B., Lesley R., and Schubert D. (1994b) Hydrogen peroxide mediates amyloid beta protein toxicity. Cell 77, 817-827.
9. Boldin M. P., Goncharov T. M., Goltsev Y. V., and Wallach D. (1996) Involvement of MACH, a novel MORT1 /FADD-interacting protease, in Fas/APO-1 and TNF receptor-induced cell death. Cell 85, 803-815.
10. Brewer G. J., Torricelli J. R., Evege E. K., and Price P. J. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
11. Chinnaiyan A. M., Tepper C. G., Seidin M. F., O'Rourke K., Kischkel F. C., Hellbardt S., Krammer P. H., Peter M. E., and Dixit V. M. (1996) FADD/MORT 1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271, 4961-4965.
12. Cooper G. J. S., Willis A. C., Clark A., Turner R. C., Sim R. B., and Reid K. B. M. (1987) Purification and characterization of a peptide from amyloid-rich pancreases of type 2 diabetic patients. Proc. Natl. Acad. Sci. USA 84, 8628-8632.
13. Cort J., Liu Z., Lee G., Harris S. M., Prickett K. S., Gaeta L. S. L., and Anderson N. H. (1994) β-structure in human amylin and two designer β-peptides: CD and NMR spectroscopic comparisons suggest soluble β-oligomers and the absence of significant populations of β-strand dimers. Biockem. Biophys. Res. Commun. 204, 1088-1095.
14. Deshmukh M. and Johnson E. M. (1997) Staurosporine-induced sympathetic neuronal death: comparison with the NGF deprivation-induced PCD pathway. Soc. Neurosci. Abstr. 23, 1986.
15. Dragunow M., Young D., Hughes P., MacGibbon G., Lawlor P., Singleton K., Sirimanne E., Beilharz E., and Gluckman P. (1993) Is c-Jun involved in nerve cell death following status epilepticus and hypoxic-ischaemic brain injury? Mol. Brain Res. 18, 347-352.
16. Edwards B. J.-A. and Morley J. E. (1992) Amylin. Life Sci. 51, 1899-1912.
17. Estus S. (1997) Optimization and validation of RT-PCR as a tool to analyze apoptotic gene expression, in NeuroMethods: Apoptosis Techniques and Protocols (Poirier J., ed), pp. 67-84. Humana Press, Totowa, New Jersey.
18. Estus S., Zaks W., Freeman R., Gruda M., Bravo R., and Johnson E. (1994) Altered gene expression in neurons during programmed cell death; identification of c-jun as necessary for neuronal apoptosis. J. Cell Biol. 127, 1717-1727.
19. Estus S., Tucker H. M., Bose S., Wright S., Brigham E. F., Wogulis M., and Rydel R. E. (1997a) Comparison of altered gene expression in rat and human fetal neurons during neuronal death induced by amyloid-β-protein treatment. Soc. Neurosci. Abstr. 23, 1628.
20. Estus S., Tucker H. M., van Rooyen C., Wright S., Brigham E., Wogulis M., and Rydel R. E. (1997b) Aggregated amyloid-β protein induces cortical neuronal apoptosis and concomitant "apoptotic" pattern of gene induction. J. Neurosci. 17, 7736-7745.
21. Forloni G., Chiesa R., Smiroldo S., Verga L., Salmona M., Tagliavini F., and Angeretti N. (1993) Apoptosis mediated neurotoxicity induced by chronic application of β amyloid fragment 25-35. Neuroreport 4, 523-526.
22. Fraser P. E., Ngyyuen J. T., Inouye H., Surewicz W. K., Selkoe D. J., Podlisny M. B., and Kirschner D. A. (1992) Fibril formation by primate, rodent and Dutch-hemorrhagic analogues of Alzheimer amyloid beta-protein. Biochemistry 31, 10716-10723.
23. Fraser S. P., Sun Y.-H., Chong Y. H., and Djamgoz M. B. A. (1996) Membrane currents induced in Xenopus oocytes by the C-terminal fragment of the β-amyloid precursor protein. J. Neurochem. 66, 2034-2040.
24. Freeman R. S., Estus S., and Johnson E. M. Jr. (1994) Analysis of cell cycle-related gene expression in postmitotic neurons: selective induction of cyclin D1 during programmed cell death. Neuron 12, 343-355.
25. Gavrieli Y., Sherman Y., and Ben-Sasson S. A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
26. Gillardon F., Skutella T., Uhlmann E., Holsboer F., Zimmermann M., and Behl C. (1996) Activation of c-Fos contributes to amyloid beta-peptide-induced neurotoxicity. Brain Res. 706, 169-172.
27. Golde T. E., Estus S., Usiak M., Younkin L. H., and Younkin S. G. (1990) Expression of beta amyloid protein precursor mRNAs: recognition of a novel alternatively spliced form and quantitation in Alzheimer's disease using PCR. Neuron 4, 253-267.
28. Goto K., Ishige A., Sekiguchi K., Iizuka S., Sugimoto A., and Yuzurihara M. (1990) Effects of cycloheximide on delayed neuronal death in rat hippocampus. Brain Res. 534, 299-302.
29. Ham J., Babij C., Whitfield J., Pfarr C. M., Lallemand D., Yaniv M., and Rubin L. L. (1995) A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14, 927-939.
30. Hensley K., Carney J. M., Mattson M. P., Aksenova M., Harris M., Wu J. F., Floyd R. A., and Butterfield D. A. (1994) A model for beta-amyloid aggregation and neurotoxicity based on free radical generation by the peptide: relevance to Alzheimer disease. Proc. Natl. Acad. Sci. USA 91, 3270-3274.
31. Herdegen T., Skene P., and Bahr M. (1997) The c-Jun transcription factor - bipotential mediator of neuronal death, survival and regeneration. Trends Neurosci. 20, 227-231.
32. Hilbich C., Kisters-Woike B., Reed J., Masters C. L., and Beyreuther K. (1992) Substitutions of hydrophobic amino acids reduce the amyloidogenicity of Alzheimer's disease βA4 peptides. J. Mol. Biol. 228, 460-473.
33. Lassmann H., Bancher C., Breitschopf H., Wegiel J., Bobinski M., Jellinger K., and Wisniewski H. M. (1995) Cell death in Alzheimer's disease evaluated by DNA fragmentation in situ. Acta Neuropathol. (Berl.) 89, 35-41.
34. Linnik M. D., Zobrist R. H., and Hatfield M. D. (1993) Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24, 2002-2009.
35. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., 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.
36. Lorenzo A., Razzaboni B., Weir G. C., and Yankner B. A. (1994) Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368, 756-760.
37. MacManus J. P., Buchan A. M., Hill J. E., Rasquinha I., and Preston E. (1993) Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164, 89-92.
38. MacManus J. P., Hill I. E., Huang Z. G., Rasquinha I., Xue D., and Buchan A. M. (1994) DNA damage consistent with apoptosis in transient ischaemic neocortex. Neuroreport 5, 493-496.
39. Mattson M. P., Tomaselli K. J., and Rydel R. E. (1993) Calcium-destabilizing and neurodegenerative effects of aggregated beta-amyloid peptide are attenuated by basic FGF. Brain Res. 621, 35-49.
40. May P. C., Boggs L, N., and Fuson K. S. (1993) Neurotoxicity of human amylin in rat primary hippocampal cultures: similarity to Alzheimer's disease amyloid-β neurotoxicity. J. Neurochem. 61, 2330-2333.
41. McDonnell S. E., Kerr L. D., and Matrisian L. M. (1990) Epidermal growth factor stimulation of stromelysin mRNA in rat fibroblasts requires induction of proto-oncogenes c-fos and c-jun and activation of protein kinase C. Mol. Cell. Biol. 10, 4284-4293.
42. McLean L. R. and Balasubramaniam A. (1992) Promotion of β-structure by interaction of diabetes associated polypeptide (amylin) with phosphatidylcholine. Biochim. Biophrs. Acta 1122, 317-320.
43. Miller T. M. and Johnson E. M. (1996) Metabolic and genetic analysis of apoptosis in potassium/serum-deprived rat cerebellar granule cells. J. Neurosci. 16, 7487-7495.
44. Mirzabekov T., Lin M. C., Yuan W. L., Marshall P. J., Carman M., Tomaselli K., Lieberburg I., and Kagan B. L. (1994) Channel formation in planar lipid bilayers by a neurotoxic fragment of the beta amyloid peptide. Biochem. Biophys. Res. Commun. 202, 1142-1148.
45. Mirzabekov T. A., Lin M., and Kagen B. L. (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem. 271, 1988-1992.
46. Mulder H., Leckstrom A., Uddman R., Ekblad E., Westermark P., and Sundler F. (1995) Islet amyloid polypeptide (amylin) is expressed in sensory neurons. J. Neumsci. 15, 7625-7632.
47. Nogawa S., Zhang F., Ross M. E., and Iadecola C. (1997) Cyclooxygenase-2 gene expression in neurons contributes to ischemic brain damage. J. Neurosci. 17, 2746-2755.
48. Pike C., Walencewicz A., Glabe C., and Cotman C. (1991) In vitro aging of β-amyloid protein causes peptide aggregation and neurotoxicity. Brain Res. 563, 311-314.
49. Pike C. J., Burdick D., Walencewicz A. J., Glabe C. G., and Cotman C. W. (1993) Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13, 1676-1687.
50. Portera-Cailliau C., Hedreen J. C., Price D. L., and Koliatsos V. E. (1995) Evidence for apoptotic cell death in Huntington disease and excitotoxic animal models. J. Neurosci. 15, 3775-3787.
51. Schmedtje J. F., Ji Y. S., Liu W. L., DuBois R. N., and Runge M. S. (1997) Hypoxia induces cyclooxygenase-2 via the NF-kappaB p65 transcription factor in human vascular endothelial cells. J. Biol. Chem. 272, 601-608.
52. Schubert D., Behl C., Lesley R., Brack A., Dargusch R., Sagara Y., and Kimura H. (1995) Amyloid peptides are toxic via a common oxidative mechanism. Proc. Natl. Acad. Sci. USA 92, 1989-1993.
53. Shigeno T. (1990) Reduction of delayed neuronal death by inhibition of protein synthesis. Neurosci. Lett 120, 117-119.
54. Simmons L. K., May P. C., Tomaselli K. J., Rydel R. E., Fuson K. S., Brigham E. F., Wright S., Lieberburg I., Becker G. W., and Brems D. N. (1994) Secondary structure of amyloid beta peptide correlates with neurotoxic activity in vitro. Mol. Pharmacol. 45, 373-379.
55. Su J. H., Anderson A. J., Cummings B. J., and Cotman C. W. (1994) Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5, 2529-2533.
56. Trejo J., Massamiri T., Deng T., Dewji N. N., Bayney R. M., and Brown J. H. (1994) A direct role for protein kinase C and the transcription factor Jun/AP-1 in the regulation of the Alzheimer's beta-amyloid precursor protein gene. J. Biol. Chem. 269, 21692-21699.
57. Wanaka A., Johnson E. M. Jr., and Milbrandt J. (1990) Localization of FGF receptor mRNA in the adult rat central nervous system by in situ hybridization. Neuron 5, 267-281.
58. Weil M., Jacobson M. D., Coles H. S., Davies T. J., Gardner R. L., Raff K. D., and Raff M. C. (1996) Constitutive expression of the machinery for programmed cell death. J. Cell Biol. 133, 1053-1059.
59. Westermark P., Wernstedt C., Wilander E., Hayden D. W., O'Brien T. D., and Johnson K. H. (1987) Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. USA 84, 3881-3885.
60. Xia Z., Dickens M., Raingeaud J., Davis R. J., and Greenberg M. E. (1995) Opposing effects of ERK and JNK-p38 MAP kinases on apoptosis. Science 270, 1326-1331.