The inhalation anesthetic isoflurane induces a vicious cycle of apoptosis and amyloid β-protein accumulation

Journal of Neuroscience

Volumn 27, Issue 6, 2007, Pages 1247-1254

  Xie, Zhongcong ^a   Dong, Yuanlin ^a   Maeda, Uta ^a   Moir, Robert D ^a   Xia, Weiming ^b   Culley, Deborah J ^c   Crosby, Gregory ^c   Tanzi, Rudolph E ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

A ; Alzheimer's disease; Anesthesia; Apoptosis; APP; Isoflurane

Indexed keywords

AMYLOID BETA PROTEIN; BETA SECRETASE; CASPASE 3; CHELATING AGENT; CLIOQUINOL; GAMMA SECRETASE; ISOFLURANE; PROTEINASE;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RELEASE; GLIOMA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; ANESTHETICS, INHALATION; APOPTOSIS; ASPARTIC ENDOPEPTIDASES; CASPASE 3; CELL LINE, TUMOR; CHELATING AGENTS; CLIOQUINOL; COPPER; CYSTEINE PROTEINASE INHIBITORS; ENZYME ACTIVATION; GANGLIOGLIOMA; HUMANS; ISOFLURANE; NEUROGLIA; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; RECOMBINANT FUSION PROTEINS; ZINC;

EID: 33847001623     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5320-06.2007     Document Type: Article

References (53)

1. Cherny RA, Atwood CS, Xilinas ME, Gray DN, Jones WD, McLean CA, Barnham KJ, Volitakis I, Fraser FW, Kim Y, Huang X, Goldstein LE, Moir RD, Lim JT, Beyreuther K, Zheng H, Tanzi RE, Masters CL, Bush AI (2001) Treatment with a copper-zinc chelator markedly and rapidly inhibits beta-amyloid accumulation in Alzheimer's disease transgenic mice. Neuron 30:665-676.
2. De Felice FG, Vieira MN, Saraiva LM, Figueroa-Villar JD, Garcia-Abreu J, Liu R, Chang L, Klein WL, Ferreira ST (2004) Targeting the neurotoxic species in Alzheimer's disease: inhibitors of Abeta oligomerization. FASEB J 18:1366-1372.
3. Eckenhoff RG, Johansson JS, Wei H, Carnini A, Kang B, Wei W, Pidikiti R, Keller JM, Eckenhoff MF (2004) Inhaled anesthetic enhancement of amyloid-beta oligomerization and cytotoxicity. Anesthesiology 101:703-709.
4. Florent S, Malaplate-Armand C, Youssef I, Kriem B, Koziel V, Escanye MC, Fifre A, Sponne I, Leininger-Muller B, Olivier JL, Pillot T, Oster T (2006) Docosahexaenoic acid prevents neuronal apoptosis induced by soluble amyloid-beta oligomers. J Neurochem 96:385-395.
5. Francis R, McGrath G, Zhang J, Ruddy DA, Sym M, Apfeld J, Nicoll M, Maxwell M, Hai B, Ellis MC, Parks AL, Xu W, Li J, Gurney M, Myers RL, Himes CS, Hiebsch R, Ruble C, Nye JS, Curtis D (2002) aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev Cell 3:85-97.
6. Galli C, Piccini A, Ciotti MT, Castellani L, Calissano P, Zaccheo D, Tabaton M (1998) Increased amyloidogenic secretion in cerebellar granule cells undergoing apoptosis. Proc Natl Acad Sci USA 95:1247-1252.
7. Gervais FG, Xu D, Robertson GS, Vaillancourt JP, Zhu Y, Huang J, LeBlanc A, Smith D, Rigby M, Shearman MS, Clarke EE, Zheng H, Van Der Ploeg LH, Ruffolo SC, Thornberry NA, Xanthoudakis S, Zamboni RJ, Roy S, Nicholson DW (1999) Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 97:395-406.
8. Glenner GG, Wong CW (1984) Alzheimer's disease and Down's syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122:1131-1135.
9. Grace EA, Rabiner CA, Busciglio J (2002) Characterization of neuronal dystrophy induced by fibrillar amyloid beta: implications for Alzheimer's disease. Neuroscience 114:265-273.
10. Gu Y, Misonou H, Sato T, Dohmae N, Takio K, Ihara Y (2001) Distinct intramembrane cleavage of the beta-amyloid precursor protein family resembling gamma-secretase-like cleavage of Notch. J Biol Chem 276:35235-35238.
11. Guo Q, Sopher BL, Furukawa K, Pham DG, Robinson N, Martin GM, Mattson MP (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.
12. Holtzman DM, Deshmukh M (1997) Caspases: a treatment target for neurodegenerative disease? Nat Med 3:954-955.
13. Jendroska K, Hoffmann OM, Patt S (1997) Amyloid beta peptide and precursor protein (APP) in mild and severe brain ischemia. Ann NY Acad Sci 826:401-405.
14. Kalaria RN (2000) The role of cerebral ischemia in Alzheimer's disease. Neurobiol Aging 21:321-330.
15. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489.
16. Kim HJ, Chae SC, Lee DK, Chromy B, Lee SC, Park YC, Klein WL, Krafft GA, Hong ST (2003) Selective neuronal degeneration induced by soluble oligomeric amyloid beta protein. FASEB J 17:118-120.
17. Kindler CH, Eilers H, Donohoe P, Ozer S, Bickler PE (1999) Volatile anesthetics increase intracellular calcium in cerebrocortical and hippocampal neurons. Anesthesiology 90:1137-1145.
18. Kokmen E, Whisnant JP, O'Fallon WM, Chu CP, Beard CM (1996) Dementia after ischemic stroke: a population-based study in Rochester, Minnesota (1960-1984). Neurology 46:154-159.
19. Kriem B, Sponne I, Fifre A, Malaplate-Armand C, Lozac'h-Pillot K, Koziel V, Yen-Potin FT, Bihain B, Oster T, Olivier JL, Pillot T (2005) Cytosolic phospholipase A2 mediates neuronal apoptosis induced by soluble oligomers of the amyloid-beta peptide. FASEB J 19:85-87.
20. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
21. LeBlanc A (1995) Increased production of 4 kDa amyloid β peptide in serum deprived human primary neuron cultures: possible involvement of apoptosis. J Neurosci 15:7837-7846.
22. LeBlanc A, Liu H, Goodyer C, Bergeron C, Hammond J (1999) Caspase-6 role in apoptosis of human neurons, amyloidogenesis, and Alzheimer's disease. J Biol Chem 274:23426-23436.
23. Li YM, Lai MT, Xu M, Huang Q, DiMuzio-Mower J, Sardana MK, Shi XP, Yin KC, Shafer JA, Gardell SJ (2000) Presenilin 1 is linked with gamma-secretase activity in the detergent solubilized state. Proc Natl Acad Sci USA 97:6138-6143.
24. Lorenzo A, Yankner BA (1994) Beta-amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc Natl Acad Sci USA 91:12243-12247.
25. Lunkes A, Trottier Y, Mandel JL (1998) Pathological mechanisms in Huntington's disease and other polyglutamine expansion diseases. Essays Biochem 33:149-163.
26. 2+ homeostasis and cell death. J Neurosci 15:6239-6249.
27. Mattson MP, Chan SL (2003) Neuronal and glial calcium signaling in Alzheimer's disease. Cell Calcium 34:385-397.
28. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992) β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389.
29. Nagy Z, Esiri MM, Jobst KA, Morris JH, King EM, McDonald B, Joachim C, Litchfield S, Barnetson L, Smith AD (1997) The effects of additional pathology on the cognitive deficit in Alzheimer disease. J Neuropathol Exp Neurol 56:165-170.
30. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, Yuan J, Moskowitz MA (1998) Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 18:3659-3668.
31. Pike CJ, Burdick D, Walencewicz AJ, Glabe CG, Cotman CW (1993) Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J Neurosci 13:1676-1687.
32. Pillot T, Drouet B, Queille S, Labeur C, Vandekerchkhove J, Rosseneu M, Pincon-Raymond M, Chambaz J (1999) The nonfibrillar amyloid beta-peptide induces apoptotic neuronal cell death: involvement of its C-terminal fusogenic domain. J Neurochem 73:1626-1634.
33. Sastre M, Steiner H, Fuchs K, Capell A, Multhaup G, Condron MM, Teplow DB, Haass C (2001) Presenilin-dependent gamma-secretase processing of beta-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch. EMBO Rep 2:835-841.
34. Snowdon DA, Greiner LH, Mortimer JA, Riley KP, Greiner PA, Markesbery WR (1997) Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA 277:813-817.
35. Sodhi CP, Rampalli S, Perez RG, Koo EH, Quinn B, Gottardi-Littell NR (2004) The endocytotic pathway is required for increased A beta 42 secretion during apoptosis. Brain Res Mol Brain Res 128:201-211.
36. Soto C, Sigurdsson EM, Morelli L, Kumar RA, Castano EM, Frangione B (1998) Beta-sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy. Nat Med 4:822-826.
37. Sponne I, Fifre A, Drouet B, Klein C, Koziel V, Pincon-Raymond M, Olivier JL, Chambaz J, Pillot T (2003) Apoptotic neuronal cell death induced by the non-fibrillar amyloid-beta peptide proceeds through an early reactive oxygen species-dependent cytoskeleton perturbation. J Biol Chem 278:3437-3445.
38. Steiner H, Winkler E, Edbauer D, Prokop S, Basset G, Yamasaki A, Kostka M, Haass C (2002) PEN-2 is an integral component of the gamma-secretase complex required for coordinated expression of presenilin and nicastrin. J Biol Chem 277:39062-39065.
39. Tanzi RE, Bertram L (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120:545-555.
40. Tesco G, Koh YH, Tanzi RE (2003) Caspase activation increases beta-amyloid generation independently of caspase cleavage of the beta-amyloid precursor protein (APP). J Biol Chem 278:46074-46080.
41. Thornberry NA (1998) Caspases: key mediators of apoptosis. Chem Biol 5:R97-R103.
42. Walsh DM, Klyubin I, Fadeeva JV, Rowan MJ, Selkoe DJ (2002) Amyloid-beta oligomers: their production, toxicity and therapeutic inhibition. Biochem Soc Trans 30:552-557.
43. Wang HW, Pasternak JF, Kuo H, Ristic H, Lambert MP, Chromy B, Viola KL, Klein WL, Stine WB, Krafft GA, Trommer BL (2002) Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res 924:133-140.
44. Wei H, Kang B, Wei W, Liang G, Meng QC, Li Y, Eckenhoff RG (2005) Isoflurane and sevoflurane affect cell survival and BCL-2/BAX ratio differently. Brain Res 1037:139-147.
45. Xie Z, Tanzi RE (2006) Alzheimer's disease and post-operative cognitive dysfunction. Exp Gerontol 41:346-359.
46. Xie Z, Moir RD, Romano DM, Tesco G, Kovacs DM, Tanzi RE (2004) Hypocapnia induces caspase-3 activation and increases abeta production. Neurodegener Dis 1:29-37.
47. Xie Z, Romano DM, Tanzi RE (2005a) Effects of RNAi-mediated silencing of PEN-2, APH-1a, and nicastrin on wild-type vs FAD mutant forms of presenilin 1. J Mol Neurosci 25:67-77.
48. Xie Z, Romano DM, Tanzi RE (2005b) RNA interference-mediated silencing of X11alpha and X11beta attenuates amyloid beta-protein levels via differential effects on beta-amyloid precursor protein processing. J Biol Chem 280:15413-15421.
49. Xie Z, Dong Y, Maeda U, Alfille P, Culley DJ, Crosby G, Tanzi RE (2006a) The common inhalation anesthetic isoflurane induces apoptosis and increases amyloid beta protein levels. Anesthesiology 104:988-994.
50. Xie Z, Dong Y, Maeda U, Moir R, Inouye SK, Culley DJ, Crosby G, Tanzi RE (2006b) Isoflurane-induced apoptosis: a potential pathogenic link between delirium and dementia. J Gerontol A Biol Sci Med Sci 61A:1300-1306.
51. Yoo AS, Cheng I, Chung S, Grenfell TZ, Lee H, Pack-Chung E, Handler M, Shen J, Xia W, Tesco G, Saunders AJ, Ding K, Frosch MP, Tanzi RE, Kim TW (2000) Presenilin-mediated modulation of capacitative calcium entry. Neuron 27:561-572.
52. Yu C, Kim SH, Ikeuchi T, Xu H, Gasparini L, Wang R, Sisodia SS (2001) Characterization of a presenilin-mediated amyloid precursor protein carboxyl-terminal fragment gamma. Evidence for distinct mechanisms involved in gamma-secretase processing of the APP and Notch1 transmembrane domains. J Biol Chem 276:43756-43760.
53. Yu G, Nishimura M, Arawaka S, Levitan D, Zhang L, Tandon A, Song YQ, Rogaeva E, Chen F, Kawarai T, Supala A, Levesque L, Yu H, Yang DS, Holmes E, Milman P, Liang Y, Zhang DM, Xu DH, Sato C, et al. (2000) Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature 407:48-54.