Familial amyloid precursor protein mutants cause caspase-6-dependent but amyloid b-peptide-independent neuronal degeneration in primary human neuron cultures

Cell Death and Disease

Volumn 1, Issue 11, 2010, Pages

  Sivananthan, S N ^a,b   Lee, A W ^a,b   Goodyer, C G ^b   Le Blanc, A C ^a,b  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Amyloid peptide; Amyloid precursor protein; Caspase 6; Neurodegeneration

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; CASPASE 6; ENHANCED GREEN FLUORESCENT PROTEIN; TAU PROTEIN; UBIQUITIN; BENZYLOXYCARBONYL VALYL ASPARTIC ACID FLUOROMETHYL KETONE; BENZYLOXYCARBONYL-VALYL-ASPARTIC ACID FLUOROMETHYL KETONE; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PEPTIDE CHLOROMETHYL KETONE; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CELL DEATH; HUMAN; HUMAN CELL; MUTAGENESIS; NERVE CELL CULTURE; NERVE CELL DEGENERATION; NERVE FIBER DEGENERATION; PRIORITY JOURNAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; GENETICS; METABOLISM; NERVE CELL; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT;

ALZHEIMER DISEASE; AMINO ACID CHLOROMETHYL KETONES; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; CASPASE 6; CELL DIFFERENTIATION; CELLS, CULTURED; GREEN FLUORESCENT PROTEINS; HUMANS; LUMINESCENT PROTEINS; NERVE DEGENERATION; NEUROGENESIS; NEURONS; RECOMBINANT FUSION PROTEINS; TAU PROTEINS; UBIQUITIN;

EID: 79958855476     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2010.74     Document Type: Article

References (44)

1. Albrecht S, Bogdanovic N, Ghetti B, Winblad B, LeBlanc AC. Caspase-6 activation in familial alzheimer disease brains carrying amyloid precursor protein or presenilin I or presenilin II mutations. J Neuropathol Exp Neurol 2009; 68: 1282-1293.
2. Albrecht S, Bourdeau M, Bennett D, Mufson EJ, Bhattacharjee M, LeBlanc AC. Activation of caspase-6 in aging and mild cognitive impairment. Am J Pathol 2007; 170: 1200-1209. (Pubitemid 47339328)
3. Guo H, Albrecht S, Bourdeau M, Petzke T, Bergeron C, LeBlanc AC. Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer's disease. Am J Pathol 2004; 165: 523-531. (Pubitemid 38971382)
4. Klaiman G, Petzke TL, Hammond J, LeBlanc AC. Targets of caspase-6 activity in human neurons and Alzheimer disease. Mol Cell Proteomics 2008; 7: 1541-1555.
5. Bertram L, Tanzi RE. Thirty years of Alzheimer's disease genetics: the implications of systematic meta-analyses. Nat Rev Neurosci 2008; 9: 768-778.
6. Rovelet-Lecrux A, Hannequin D, Raux G, Le Meur N, Laquerriere A, Vital A et al. APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy. Nat Genet 2006; 38: 24-26. (Pubitemid 43011878)
7. McPhie DL, Golde T, Eckman CB, Yager D, Brant JB, Neve RL. Beta-secretase cleavage of the amyloid precursor protein mediates neuronal apoptosis caused by familial Alzheimer's disease mutations. Brain Res Mol Brain Res 2001; 97: 103-113. (Pubitemid 34020715)
8. Giambarella U, Murayama Y, Ikezu T, Fujita T, Nishimoto I. Potential CRE suppression by familial Alzheimer's mutants of APP independent of adenylyl cyclase regulation. FEBS Lett 1997; 412: 97-101. (Pubitemid 27310008)
9. Yamatsuji T, Okamoto T, Takeda S, Murayama Y, Tanaka N, Nishimoto I. Expression of V642 APP mutant causes cellular apoptosis as Alzheimer trait-linked phenotype. EMBO J 1996; 15: 498-509. (Pubitemid 26044563)
10. Eckert A, Steiner B, Marques C, Leutz S, Romig H, Haass C et al. Elevated vulnerability to oxidative stress-induced cell death and activation of caspase-3 by the Swedish amyloid precursor protein mutation. J Neurosci Res 2001; 64: 183-192.
11. Selkoe DJ, Podlisny MB. Deciphering the genetic basis of Alzheimer's disease. Annu Rev Genomics Hum Genet 2002; 3: 67-99. (Pubitemid 35217431)
12. Gervais FG, Xu D, Robertson GS, Vaillancourt JP, Zhu Y, Huang J et al. Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 1999; 97: 395-406.
13. LeBlanc A, Liu H, Goodyer C, Bergeron C, Hammond J. Caspase-6 role in apoptosis of human neurons, amyloidogenesis, and Alzheimer's disease. J Biol Chem 1999; 274: 23426-23436.
14. Srinivasula SM, Fernandes-Alnemri T, Zangrilli J, Robertson N, Armstrong RC, Wang L et al. The Ced-3/interleukin 1beta converting enzyme-like homolog Mch6 and the lamincleaving enzyme Mch2alpha are substrates for the apoptotic mediator CPP32. J Biol Chem 1996; 271: 27099-27106. (Pubitemid 26359130)
15. Klaiman G, Champagne N, LeBlanc AC. Self-activation of caspase-6 in vitro and in vivo: caspase-6 activation does not induce cell death in HEK293T cells. Biochim Biophys Acta 2009; 1793: 592-601.
16. Kang JJ, Schaber MD, Srinivasula SM, Alnemri ES, Litwack G, Hall DJ et al. Cascades of mammalian caspase activation in the yeast Saccharomyces cerevisiae. J Biol Chem 1999; 274: 3189-3198. (Pubitemid 29075408)
17. Allsopp TE, McLuckie J, Kerr LE, Macleod M, Sharkey J, Kelly JS. Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis. Cell Death Differ 2000; 7: 984-993.
18. Doostzadeh-Cizeron J, Yin S, Goodrich DW. Apoptosis induced by the nuclear death domain protein p84N5 is associated with caspase-6 and NF-kappa B activation. J Biol Chem 2000; 275: 25336-25341.
19. Cowling V, Downward J. Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Differ 2002; 9: 1046-1056.
20. Zhang Y, Goodyer C, LeBlanc A. Selective and protracted apoptosis in human primary neurons microinjected with active caspase-3, -6, -7, and -8. J Neurosci 2000; 20: 8384-8389.
21. Nikolaev A, McLaughlin T, O'Leary DD, Tessier-Lavigne M. APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 2009; 457: 981-989.
22. LeBlanc AC. The role of apoptotic pathways in Alzheimer's disease neurodegeneration and cell death. Curr Alzheimer Res 2005; 2: 389-402.
23. van de Craen M, de Jonghe C, van den Brande I, Declercq W, van Gassen G, van Criekinge W et al. Identification of caspases that cleave presenilin-1 and presenilin-2. Five presenilin-1 (PS1) mutations do not alter the sensitivity of PS1 to caspases. FEBS Lett 1999; 445: 149-154. (Pubitemid 29101551)
24. Dickson DW. The pathogenesis of senile plaques. J Neuropathol Exp Neurol 1997; 56: 321-339. (Pubitemid 27465015)
25. Perry G, Kawai M, Tabaton M, Onorato M, Mulvihill P, Richey P et al. Neuropil threads of Alzheimer's disease show a marked alteration of the normal cytoskeleton. J Neurosci 1991; 11: 1748-1755.
26. Stokin GB, Goldstein LS. Axonal transport and Alzheimer's disease. Annu Rev Biochem 2006; 75: 607-627. (Pubitemid 44118045)
27. Salehi A, Delcroix JD, Belichenko PV, Zhan K, Wu C, Valletta JS et al. Increased APP expression in a mouse model of Down's syndrome disrupts NGF transport and causes cholinergic neuron degeneration. Neuron 2006; 51: 29-42. (Pubitemid 43963336)
28. Wirths O, Weis J, Kayed R, Saido TC, Bayer TA. Age-dependent axonal degeneration in an Alzheimer mouse model. Neurobiol Aging 2007; 28: 1689-1699. (Pubitemid 47393589)
29. Nishimura I, Uetsuki T, Dani SU, Ohsawa Y, Saito I, Okamura H et al. Degeneration in vivo of rat hippocampal neurons by wild-type Alzheimer amyloid precursor protein overexpressed by adenovirus-mediated gene transfer. J Neurosci 1998; 18: 2387-2398. (Pubitemid 28141788)
30. Gotz J, Ittner LM, Kins S. Do axonal defects in tau and amyloid precursor protein transgenic animals model axonopathy in Alzheimer's disease? J Neurochem 2006; 98: 993-1006. (Pubitemid 44127777)
31. Lazarov O, Morfini GA, Lee EB, Farah MH, Szodorai A, DeBoer SR et al. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: revisited. J Neurosci 2005; 25: 2386-2395. (Pubitemid 40322280)
32. Simon AM, Schiapparelli L, Salazar-Colocho P, Cuadrado-Tejedor M, Escribano L, Lopez de Maturana R et al. Overexpression of wild-type human APP in mice causes cognitive deficits and pathological features unrelated to Abeta levels. Neurobiol Dis 2009; 33: 369-378.
33. Stokin GB, Almenar-Queralt A, Gunawardena S, Rodrigues EM, Falzone T, Kim J et al. Amyloid precursor protein-induced axonopathies are independent of amyloid-beta peptides. Hum Mol Genet 2008; 17: 3474-3486.
34. Citron M, Teplow DB, Selkoe DJ. Generation of amyloid beta protein from its precursor is sequence specific. Neuron 1995; 14: 661-670.
35. Paradis E, Douillard H, Koutroumanis M, Goodyer C, LeBlanc A. Amyloid βpeptide of Alzheimer's disease downregulates Bcl-2 and upregulates Bax expression in human neurons. J Neurosci 1996; 16: 7533-7539. (Pubitemid 26389692)
36. LeBlanc A. Increased production of 4 kDa amyloid beta peptide in serum deprived human primary neuron cultures: possible involvement of apoptosis. J Neurosci 1995; 15: 7837-7846.
37. Esposito L, Gan L, Yu GQ, Essrich C, Mucke L. Intracellularly generated amyloid-beta peptide counteracts the antiapoptotic function of its precursor protein and primes proapoptotic pathways for activation by other insults in neuroblastoma cells. J Neurochem 2004; 91: 1260-1274. (Pubitemid 39658553)
38. Luo JJ, Wallace W, Riccioni T, Ingram DK, Roth GS, Kusiak JW. Death of PC12 cells and hippocampal neurons induced by adenoviral-mediated FAD human amyloid precursor protein gene expression. J Neurosci Res 1999; 55: 629-642. (Pubitemid 29117621)
39. Zhao B, Chrest FJ, Horton Jr WE, Sisodia SS, Kusiak JW. Expression of mutant amyloid precursor proteins induces apoptosis in PC12 cells. J Neurosci Res 1997; 47: 253-263. (Pubitemid 27066759)
40. Small SA, Duff K. Linking Abeta and tau in late-onset Alzheimer's disease: a dual pathway hypothesis. Neuron 2008; 60: 534-542.
41. Gomez-Isla T, Hollister R, West H, Mui S, Growdon J, Petersen R et al. Neuronal loss correlated with but exceeds neurofibrillary tangles in Alzheimer0s disease. Ann Neurol 1996; 41: 17-24.
42. Oyama F, Kotliarova S, Harada A, Ito M, Miyazaki H, Ueyama Y et al. Gem GTPase and tau: morphological changes induced by gem GTPase in CHO cells are antagonized by tau. J Biol Chem 2004; 279: 27272-27277. (Pubitemid 38812566)
43. Bergink S, Severijnen LA, Wijgers N, Sugasawa K, Yousaf H, Kros JM et al. The DNA repair-ubiquitin-associated HR23 proteins are constituents of neuronal inclusions in specific neurodegenerative disorders without hampering DNA repair. Neurobiol Dis 2006; 23: 708-716. (Pubitemid 44234106)
44. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A. Selective cytotoxicity of intracellular amyloid β peptide1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol 2002; 156: 519-529. (Pubitemid 34839899)