Home LiteratureArticle Details
PMID: 10662826 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Presenilin-1 mutation increases neuronal vulnerability to focal ischemia in vivo and to hypoxia and glucose deprivation in cell culture: involvement of perturbed calcium homeostasis.

Mattson MP, Zhu H, Yu J, Kindy MS

Abstract

Many cases of early-onset inherited Alzheimer's disease (AD) are caused by mutations in the presenilin-1 (PS1) gene. Studies of cultured neural cells suggest that PS1 mutations result in perturbed cellular calcium homeostasis and may thereby render neurons vulnerable to apoptosis. In light of evidence that metabolic impairment plays a role in AD, that cerebral ischemia may be a risk factor for AD, and that individuals with AD have increased morbidity and mortality after stroke, we examined the impact of a PS1 mutation on neuronal vulnerability to ischemic injury. We report that the extent of brain injury after focal cerebral ischemia reperfusion is increased, and behavioral outcome is worsened, in PS1 mutant knock-in mice compared to wild-type mice. Cultured cortical neurons from PS1 mutant mice exhibit increased vulnerability to glucose deprivation and chemical hypoxia compared to their wild-type counterparts. Calcium imaging studies demonstrated enhanced elevation of intracellular calcium levels after glucose deprivation and chemical hypoxia in neurons from PS1 mutant mice. Agents that block calcium release from IP(3)- and ryanodine-sensitive stores (xestospongin and dantrolene, respectively) protected against the endangering action of the PS1 mutation. Our data suggest that presenilin mutations may promote neuronal degeneration in AD by increasing the sensitivity of neurons to age-related ischemia-like conditions. The data further suggest that drugs that stabilize endoplasmic reticulum calcium homeostasis may prove effective in suppressing the neurodegenerative process in AD patients.

MeSH Terms
Alzheimer Disease/genetics Animals Apoptosis Blood Pressure Calcium/metabolism Carbon Dioxide/blood Cell Hypoxia Cells, Cultured Cerebrovascular Circulation Dantrolene/pharmacology Embryo, Mammalian Genetic Predisposition to Disease Glucose/physiology Heart Rate Homeostasis Hypoglycemia Ischemic Attack, Transient/genetics,physiopathology Membrane Proteins/deficiency,genetics,physiology Mice Mice, Knockout Neocortex/cytology,physiology,physiopathology Neurons/cytology,drug effects,physiology Oxygen/blood Partial Pressure Presenilin-1 Sodium Cyanide/pharmacology
Chemicals
Membrane Proteins Presenilin-1 Carbon Dioxide Dantrolene Glucose Sodium Cyanide Oxygen Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Mattson M P
Sanders-Brown Research Center on Aging, Department of Anatomy, University of Kentucky, Lexington, Kentucky 40536, USA. mattsonm@grc.nia.nih.gov
Zhu H
Yu J
Kindy M S
References (52)
52 references, click to expand
  1. Xestospongins: potent membrane permeable blockers of the inositol 1,4,5-trisphosphate receptor.
    Neuron. 1997 Sep;19(3):723-33 PMID: 9331361
  2. Activation of K+ channels and suppression of neuronal activity by secreted beta-amyloid-precursor protein.
    Nature. 1996 Jan 4;379(6560):74-8 PMID: 8538744
  3. Dantrolene protects against ischemic, delayed neuronal death in gerbil brain.
    Neurosci Lett. 1993 Aug 6;158(1):105-8 PMID: 8233063
  4. beta-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity.
    J Neurosci. 1992 Feb;12(2):376-89 PMID: 1346802
  5. Ischemia-induced neuronal apoptosis.
    Curr Opin Neurobiol. 1996 Oct;6(5):667-72 PMID: 8937832
  6. Dementia after ischemic stroke: a population-based study in Rochester, Minnesota (1960-1984)
    Neurology. 1996 Jan;46(1):154-9 PMID: 8559366
  7. Familial Alzheimer's disease-linked presenilin 1 variants elevate Abeta1-42/1-40 ratio in vitro and in vivo.
    Neuron. 1996 Nov;17(5):1005-13 PMID: 8938131
  8. Brain infarction and the clinical expression of Alzheimer disease. The Nun Study.
    JAMA. 1997 Mar 12;277(10):813-7 PMID: 9052711
  9. Excitotoxicity and excitoprotection in vitro.
    Adv Neurol. 1996;71:1-30; discussion 30-5 PMID: 8790786
  10. Alzheimer's presenilin mutation sensitizes neural cells to apoptosis induced by trophic factor withdrawal and amyloid beta-peptide: involvement of calcium and oxyradicals.
    J Neurosci. 1997 Jun 1;17(11):4212-22 PMID: 9151738
  11. The Alzheimer's disease-associated presenilins are differentially phosphorylated proteins located predominantly within the endoplasmic reticulum.
    Mol Med. 1996 Nov;2(6):673-91 PMID: 8972483
  12. Light and electron microscopic localization of presenilin-1 in primate brain.
    J Neurosci. 1997 Mar 15;17(6):1971-80 PMID: 9045726
  13. Expression and analysis of presenilin 1 in a human neuronal system: localization in cell bodies and dendrites.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9223-8 PMID: 8799182
  14. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1.
    Nature. 1996 Oct 24;383(6602):710-3 PMID: 8878479
  15. Differential immunohistochemical localization of inositol 1,4,5-trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain.
    J Neurosci. 1993 Jul;13(7):3051-63 PMID: 8392539
  16. Stroke risk factors and stroke prevention.
    Semin Neurol. 1998;18(4):429-40 PMID: 9932614
  17. Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice.
    J Neurochem. 1999 Mar;72(3):1030-9 PMID: 10037474
  18. Neurotrophic factors [activity-dependent neurotrophic factor (ADNF) and basic fibroblast growth factor (bFGF)] interrupt excitotoxic neurodegenerative cascades promoted by a PS1 mutation.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4125-30 PMID: 10097174
  19. Alzheimer's disease.
    N Engl J Med. 1986 Apr 10;314(15):964-73 PMID: 2870433
  20. Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the beta-amyloid precursor protein.
    Neuron. 1993 Feb;10(2):243-54 PMID: 8094963
  21. Caffeine-induced calcium release from internal stores in cultured rat sensory neurons.
    Neuroscience. 1993 Dec;57(3):845-59 PMID: 8309540
  22. Diagnosis and treatment of Alzheimer disease and related disorders. Consensus statement of the American Association for Geriatric Psychiatry, the Alzheimer's Association, and the American Geriatrics Society.
    JAMA. 1997 Oct 22-29;278(16):1363-71 PMID: 9343469
  23. Alteration of second messenger systems after transient cerebral ischemia in gerbils: protective effect of pentobarbital and an autoradiographic analysis.
    Neurosci Lett. 1991 Sep 2;130(1):57-60 PMID: 1749517
  24. Neuroprotective effects of gelsolin during murine stroke.
    J Clin Invest. 1999 Feb;103(3):347-54 PMID: 9927495
  25. Widespread neuronal expression of the presenilin-1 early-onset Alzheimer's disease gene in the murine brain.
    Am J Pathol. 1996 Jun;148(6):1797-806 PMID: 8669467
  26. Secreted forms of beta-amyloid precursor protein protect hippocampal neurons against amyloid beta-peptide-induced oxidative injury.
    Exp Neurol. 1994 Jul;128(1):1-12 PMID: 8070512
  27. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease.
    Nat Med. 1996 Aug;2(8):864-70 PMID: 8705854
  28. Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knock-in mice.
    Nat Med. 1999 Jan;5(1):101-6 PMID: 9883847
  29. Dantrolene is cytoprotective in two models of neuronal cell death.
    J Neurochem. 1996 Dec;67(6):2390-8 PMID: 8931471
  30. NGF and bFGF protect rat hippocampal and human cortical neurons against hypoglycemic damage by stabilizing calcium homeostasis.
    Neuron. 1991 Dec;7(6):1031-41 PMID: 1662517
  31. Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death.
    J Neurosci. 1984 Jul;4(7):1884-91 PMID: 6737044
  32. Dantrolene prevents glutamate cytotoxicity and Ca2+ release from intracellular stores in cultured cerebral cortical neurons.
    J Neurochem. 1991 Mar;56(3):1075-8 PMID: 1671584
  33. Human and rodent Alzheimer beta-amyloid peptides acquire distinct conformations in membrane-mimicking solvents.
    Eur J Biochem. 1993 Jan 15;211(1-2):249-57 PMID: 8425535
  34. Secreted beta-amyloid precursor protein counteracts the proapoptotic action of mutant presenilin-1 by activation of NF-kappaB and stabilization of calcium homeostasis.
    J Biol Chem. 1998 May 15;273(20):12341-51 PMID: 9575187
  35. Rodent models of cerebral ischemia.
    Stroke. 1989 Dec;20(12):1627-42 PMID: 2688195
  36. Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells.
    Nat Med. 1996 Feb;2(2):224-9 PMID: 8574969
  37. Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase.
    Science. 1994 Sep 23;265(5180):1883-5 PMID: 7522345
  38. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction.
    J Neurosci. 1998 Jan 15;18(2):687-97 PMID: 9425011
  39. Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives.
    Physiol Rev. 1997 Oct;77(4):1081-132 PMID: 9354812
  40. Growth factors prevent mitochondrial dysfunction, loss of calcium homeostasis, and cell injury, but not ATP depletion in hippocampal neurons deprived of glucose.
    Exp Neurol. 1993 May;121(1):1-13 PMID: 8495704
  41. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury.
    J Neurosci. 1993 Aug;13(8):3510-24 PMID: 8101871
  42. Amyloid, the presenilins and Alzheimer's disease.
    Trends Neurosci. 1997 Apr;20(4):154-9 PMID: 9106355
  43. Secreted forms of beta-amyloid precursor protein protect against ischemic brain injury.
    J Neurochem. 1994 Aug;63(2):781-4 PMID: 8035204
  44. Presenilins, the endoplasmic reticulum, and neuronal apoptosis in Alzheimer's disease.
    J Neurochem. 1998 Jan;70(1):1-14 PMID: 9422341
  45. Identification and neuron specific expression of the S182/presenilin I protein in human and rodent brains.
    J Neurosci Res. 1996 Aug 01;45(3):308-20 PMID: 8841992
  46. Alzheimer's PS-1 mutation perturbs calcium homeostasis and sensitizes PC12 cells to death induced by amyloid beta-peptide.
    Neuroreport. 1996 Dec 20;8(1):379-83 PMID: 9051814
  47. Alpha-secretase-derived product of beta-amyloid precursor protein is decreased by presenilin 1 mutations linked to familial Alzheimer's disease.
    J Neurochem. 1997 Dec;69(6):2494-9 PMID: 9375682
  48. Early postischemic dantrolene-induced amelioration of poly(ADP-ribose) polymerase-related bioenergetic failure in neonatal rat brain slices.
    J Cereb Blood Flow Metab. 1998 Dec;18(12):1346-56 PMID: 9850147
  49. Cellular and molecular mechanisms underlying perturbed energy metabolism and neuronal degeneration in Alzheimer's and Parkinson's diseases.
    Ann N Y Acad Sci. 1999;893:154-75 PMID: 10672236
  50. Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptors.
    Nat Med. 1996 Jul;2(7):788-94 PMID: 8673925
  51. Calcium, free radicals, and excitotoxic neuronal death in primary cell culture.
    Methods Cell Biol. 1995;46:187-216 PMID: 7541884
  52. The effects of additional pathology on the cognitive deficit in Alzheimer disease.
    J Neuropathol Exp Neurol. 1997 Feb;56(2):165-70 PMID: 9034370
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
0270-6474
Published
2000-02-15
Pages
1358-64
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6772370
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com