Apoptosis and in vitro Alzheimer disease neuronal models

Communicative and Integrative Biology

Volumn 2, Issue 2, 2009, Pages 163-169

  Calissano, P ^a,b   Matrone, C ^a   Amadoro, G ^a  

^a CNR   (Italy)

^b EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

Author keywords

Alzheimer disease; Amyloid beta; Apoptosis; Caspase; Neurotrophin; Tau protein

Indexed keywords

ANIMALIA;

EID: 67650508325     PISSN: None     EISSN: 19420889     Source Type: Journal    
DOI: 10.4161/cib.7704     Document Type: Review

References (130)

1. Selkoe DJ. Alzheimer's disease: genes, proteins and therapy. Physiol Rev 2001; 81:741-66.
2. Shen Y, He P, Zhong Z, McAllister C, Lindholm K. Distinct destructive signal pathways of neuronal death in Alzheimer's disease. Trends Mol Med 2006; 12:574-9.
3. Salehi A, Delcroix JD, Mobley WC. Traffic at the intersection of neurotrophic factor signalling and neurodegeneration. Trends Neurosci 2003; 26:73-80.
4. Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002; 297:353-6.
5. Blurton-Jones M, Laferla FM. Pathways by which Abeta facilitates tau pathology. Curr Alzheimer Res 2006; 3:437-48.
6. Mattson MP. Apoptosis in neurodegenerative disorders. Nat Rev Mol Cell Biol 2000; 1:120-9.
7. Mattson MP, Magnus T. Ageing and neuronal vulnerability. Nat Rev Neurosci 2006; 7:278-94.
8. Schulte-Herbrüggen O, Braun A, Rochlitzer S, Jockers-Scherübl MC, Hellweg R. Neurotrophic factors-a tool for therapeutic strategies in neurological, neuropsychiatric and neuroimmunological diseases? Curr Med Chem 2007; 14:2318-29.
9. Canu N, Calissano P. In vitro cultured neurons for molecular studies correlating apoptosis with events related to Alzheimer disease. Cerebellum 2003; 2:270-8.
10. Shimohama S. Apoptosis in Alzheimer's disease-an update. Apoptosis 2000; 5:9-16.
11. Behl C. Apoptosis and Alzheimer's disease. J Neural Transm 2000; 107:1325-44.
12. Kitamura Y, Shimohama S, Kamoshima W, Ota T, Matsuoka Y, Nomura Y, et al. Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's disease. Brain Res 1998; 780:260-9.
13. Su JH, Deng G, Cotman CW. Bax protein expression is increased in Alzheimer's brain: correlations with DNA damage, Bcl-2 expression and brain pathology. J Neuropathol Exp Neurol 1997; 56:86-93.
14. Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Brück W, Jellinger K, et al. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death. Am J Pathol 1999; 155:1459-66.
15. Selznick LA, Holtzman DM, Han BH, Gökden M, Srinivasan AN, Johnson EM Jr, et al. In situ immunodetection of neuronal caspase-3 activation in Alzheimer disease. J Neuropathol Exp Neurol 1999; 58:1020-6.
16. 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; 165:523-31.
17. Rohn TT, Head E, Nesse WH, Cotman CW, Cribbs DH. Activation of caspase-8 in the Alzheimer's disease brain. Neurobiol Dis 2001; 8:1006-16.
18. Rohn TT, Rissman RA, Davis MC, Kim YE, Cotman CW, Head E. Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Caspase-9 activation and caspase cleavage of tau in the Alzheimer's disease brain. Neurobiol Dis 2002; 11:341-54.
19. Wu CK, Thal L, Pizzo D, Hansen L, Masliah E, Geula C. Apoptotic signals within the basal forebrain cholinergic neurons in Alzheimer's disease. Exp Neurol 2005; 195:484-96.
20. 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; 170:1200-9.
21. Suzuki T, Nishiyama K, Yamamoto A, Inazawa J, Iwaki T, Yamada T, et al. Molecular cloning of a novel apoptosis-related gene, human Nap1 (NCKAP1), and its possible relation to Alzheimer disease. Genomics 2000; 63:246-54.
22. Cribbs DH, Poon WW, Rissman RA, Blurton-Jones M. Caspase-mediated degeneration in Alzheimer's disease. Am J Pathol 2004; 165:353-5.
23. Gastard MC, Troncoso JC, Koliatsos VE. Caspase activation in the limbic cortex of subjects with early Alzheimer's disease. Ann Neurol 2003; 54:393-8.
24. Louneva N, Cohen JW, Han LY, Talbot K, Wilson RS, Bennett DA, et al. Caspase 3 is enriched in postsynaptic densities and increased in Alzheimer's disease. Am J Pathol 2008; 173:1488-95.
25. Su JH, Kesslak JP, Head E, Cotman CW. Caspase-cleaved amyloid precursor protein and activated caspase-3 are co-localized in the granules of granulovacuolar degeneration in Alzheimer's disease and Down's syndrome brain. Acta Neuropathol 2002; 104:1-6.
26. Wai MS, Liang Y, Shi C, Cho EY, Kung HF, Yew DT. Co-localization of hyperphosphorylated tau and caspases in the brainstem of Alzheimer's disease patients. Biogerontology 2008; In press.
27. 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.
28. Lu DC, Rabizadeh S, Chandra S, Shayya RF, Ellerby LM, Ye X, et al. A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor. Nat Med 2000; 6:397-404.
29. Tesco G, Koh YH, Kang EL, Cameron AN, Das S, Sena-Esteves M, et al. Depletion of GGA3 stabilizes BACE and enhances beta-secretase activity. Neuron 2007; 54:721-37.
30. Marín N, Romero B, Bosch-Morell F, Llansola M, Felipo V, Romá J, et al. Beta-amyloidinduced activation of caspase-3 in primary cultures of rat neurons. Mech Ageing Dev 2000; 119:63-7.
31. Loo DT, Copani A, Pike CJ, Whittemore ER, Walencewicz AJ, Cotman CW. Apoptosis is induced by beta-amyloid in cultured nervous system neurons Proc Natl Acad Sci USA 1993; 90:7951-5.
32. Uetsuki T, Takemoto K, Nishimura I, Okamoto M, Niinobe M, Momoi T, et al. Activation of neuronal caspase-3 by intracellular accumulation of wild-type Alzheimer amyloid precursor protein. J Neurosci 1999; 19:6955-64.
33. Nishimura I, Uetsuki T, Kuwako K, Hara T, Kawakami T, Aimoto S, et al. Cell death induced by a caspase-cleaved transmembrane fragment of the Alzheimer amyloid precursor protein. Cell Death Differ 2002; 9:199-208.
34. Chan SL, Mattson MP. Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 1999; 58:167-90.
35. Glabe C. Intracellular mechanisms of amyloid accumulation and pathogenesis in Alzheimer's disease. J Mol Neurosci 2001; 17:137-45.
36. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003; 39:409-21.
37. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, et al. ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 2004; 304:448-52.
38. Du H, Guo L, Fang F, Chen D, Sosunov AA, McKhann GM, et al. Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat Med 2008; 14:1097-105.
39. Oddo S. The ubiquitin-proteasome system in Alzheimer's disease. J Cell Mol Med 2008; 12:363-73.
40. Song S, Lee H, Kam TI, Tai ML, Lee JY, Noh JY, et al. E2-25K/Hip-2 regulates caspase-12 in ER stress-mediated Abeta neurotoxicity. J Cell Biol 2008; 82:675-84.
41. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 2000; 403:98-103.
42. Ivins KJ, Thornton PL, Rohn TT, Cotman CW. Neuronal apoptosis induced by beta-amyloid is mediated by caspase-8. Neurobiol Dis 1999; 6:440-9.
43. Giovanni A, Keramaris E, Morris EJ, Hou ST, O'Hare M, Dyson N, et al. E2F1 mediates death of B-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase 3. J Biol Chem 2000; 275:11553-60.
44. Troy CM, Rabacchi SA, Friedman WJ, Frappier TF, Brown K, Shelanski ML. Caspase-2 mediates neuronal cell death induced by beta-amyloid. J Neurosci 2000; 20:1386-92.
45. Wei Z, Song MS, MacTavish D, Jhamandas JH, Kar S. Role of calpain and caspase in beta-amyloid-induced cell death in rat primary septal cultured neurons. Neuropharmacology 2008; 54:721-33.
46. 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; 274:23426-36.
47. Weidemann A, Paliga K, Dürrwang U, Reinhard FB, Schuckert O, Evin G, et al. Proteolytic processing of the Alzheimer's disease amyloid precursor protein within its cytoplasmic domain by caspase-like proteases. J Biol Chem 1999; 274:5823-9.
48. Abrahamson EE, Ikonomovic MD, Ciallella JR, Hope CE, Paljug WR, Isanski BA, et al. Caspase inhibition therapy abolishes brain trauma-induced increases in Abeta peptide: implications for clinical outcome. Exp Neurol 2006; 197:437-50.
49. Hook VY, Kindy M, Hook G. Inhibitors of cathepsin B improve memory and reduce beta-amyloid in transgenic Alzheimer disease mice expressing the wild-type, but not the Swedish mutant, beta-secretase site of the amyloid precursor protein. J Biol Chem 2008; 283:7745-53.
50. Trinchese F, Fa' M, Liu S, Zhang H, Hidalgo A, Schmidt SD, et al. Inhibition of calpains improves memory and synaptic transmission in a mouse model of Alzheimer disease J Clin Invest 2008; 118:2796-807.
51. Dickson DW. Apoptotic mechanisms in Alzheimer neurofibrillary degeneration: cause or effect? J Clin Invest 2004; 114:23-7.
52. García-Sierra F, Mondragón-Rodríguez S, Basurto-Islas G. Truncation of tau protein and its pathological significance in Alzheimer's disease. J Alzheimers Dis 2008; 14:401-9.
53. Cotman CW, Poon WW, Rissman RA, Blurton-Jones M. The role of caspase cleavage of tau in Alzheimer disease neuropathology. J Neuropathol Exp Neurol 2005; 64:104-12.
54. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, et al. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 2003; 100:10032-7.
55. Cho JH, Johnson GV. Glycogen synthase kinase 3 beta induces caspase-cleaved tau aggregation in situ. J Biol Chem 2004; 279:54716-23.
56. Fasulo L, Ugolini G, Visintin M, Bradbury A, Brancolini C, Verzillo V, et al. The neuronal microtubule-associated protein tau is a substrate for caspase-3 and an effector of apoptosis. J Neurochem 2000; 75:624-33.
57. Chung CW, Song YH, Kim IK, Yoon WJ, Ryu BR, Jo DG, et al. Proapoptotic effects of tau cleavage product generated by caspase-3. Neurobiol Dis 2001; 8:162-72.
58. Ramalho RM, Viana RJ, Castro RE, Steer CJ, Low WC, Rodriguez CM. Apoptosis in transgenic mice expressing the P301L mutated form of human tau. Mol Med 2008; 1485:309-17.
59. Rohn TT, Vyas V, Hernandez-estrada T, Nichol KE, Christie LA, Head E. Lack of pathology in a triple transgenic mouse model of Alzheimer's disease after overexpression of the anti-apoptotic protein bcl-2. J Neurosci 2008; 28:3051-9.
60. Zilkova M, Koson P, Zilka N. The hunt for dying neurons: insight into the neuronal loss in Alzheimer's disease. Bratisl Lek Listy 2006; 107:366-73.
61. Yuan J. Divergence from a dedicated cellular suicide mechanism: exploring the evolution of cell death. Mol Cell 2006; 23:1-12.
62. Bredesen DE, Rao RV, Mehlen P. Cell death in the nervous system. Nature 2006; 443:796-802.
63. D'Mello SR, Galli C, Ciotti T, Calissano P. Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 1993; 90:10989-93.
64. Galli C, Meucci O, Scorziello A, Werge TM, Calissano P, Schettini G. Apoptosis in cerebellar granule cells is blocked by high KCl, forskolin and IGF-1 through distinct mechanisms of action: the involvement of intracellular calcium and RNA synthesis. J Neurosci 1995; 15:1172-9.
65. Borsello T, Di Luzio A, Ciotti MT, Calissano P, Galli C. Granule neuron DNA damage following deafferentation in adult rats cerebellar cortex: a lesion model. Neuroscience 2000; 95:163-71.
66. Nardi N, Avidan G, Daily D, Zilkha-Falb R, Barzilai A. Biochemical and temporal analysis of events associated with apoptosis induced by lowering the extracellular potassium concentration in mouse cerebellar granule neurons. J Neurochem 1997; 68:750-9.
67. Schulz JB, Beinroth S, Weller M, Wüllner U, Klockgether T. Endonucleolytic DNA fragmentation is not required for apoptosis of cultured rat cerebellar granule neurons. Neurosci Lett 1998; 245:9-12.
68. Armstrong RC, Aja TJ, Hoang KD, Gaur S, Bai X, Alnemri ES, Litwack G, Karanewsky DS, Fritz LC, Tomaselli KJ. Activation of the CED3/ICE-related protease CPP32 in cerebellar granule neurons undergoing apoptosis but not necrosis. J Neurosci 1997; 17:553-62.
69. Eldadah BA, Yakovlev AG, Faden AI. The role of CED-3-related cysteine proteases in apoptosis of cerebellar granule cells. J Neurosci 1997; 17:6105-13.
70. Eldadah BA, Ren RF, Faden AI. Ribozyme-mediated inhibition of caspase-3 protects cerebellar granule cells from apoptosis induced by serum-potassium deprivation. J Neurosci 2000; 20:179-86.
71. D'Mello SR, Kuan CY, Flavell RA, Rakic P. Caspase-3 is required for apoptosis-associated DNA fragmentation but not for cell death in neurons deprived of potassium. J Neurosci Res 2000; 59:24-31.
72. Gerhardt E, Kügler S, Leist M, Beier C, Berliocchi L, Volbracht C, et al. Cascade of caspase activation in potassium-deprived cerebellar granule neurons: targets for treatment with peptide and protein inhibitors of apoptosis. Mol Cell Neurosci 2001; 4:717-31.
73. Canu N, Dus L, Barbato C, Ciotti MT, Brancolini C, Rinaldi AM, et al. Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis. J Neurosci 1998; 18:7061-74.
74. Canu N, Tufi R, Serafino AL, Amadoro G, Ciotti MT, Calissano P. Role of the autophagiclysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J Neurochem 2005; 92:1228-42.
75. Kaasik A, Rikk T, Piirsoo A, Zharkovsky T, Zharkovsky A. Upregulation of lysosomal cathepsin L and autophagy during neuronal death induced by reduced serum and potassium. Eur J Neurosci 2005; 22:1023-31.
76. Amadoro G, Pieri M, Ciotti MT, Carunchio I, Canu N, Calissano P, et al. Substance P provides neuroprotection in cerebellar granule cells through Akt and MAPK/Erk activation: evidence for the involvement of the delayed rectifier potassium current. Neuropharmacology 2007; 52:1366-77.
77. Kubo T, Nonomura T, Enokido Y, Hatanaka H. Brain-derived neurotrophic factor (BDNF) can prevent apoptosis of rat cerebellar granule neurons in culture. Brain Res Dev Brain Res 1995; 85:249-58.
78. D'Mello SR, Borodezt K, Soltoff SP. Insulin-like growth factor and potassium depolarization maintain neuronal survival by distinct pathways: possible involvement of PI 3-kinase in IGF-1 signaling. J Neurosci 1997; 17:1548-60.
79. Journot L, Villalba M, Bockaert J. PACAP-38 protects cerebellar granule cells from apoptosis. Ann NY Acad Sci 1998; 865:100-10.
80. Dudek H, Datta SR, Franke TF, Birnbaum MJ, Yao R, Cooper GM, et al. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 1997; 275:661-5.
81. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96:857-68.
82. Kienlen Campard P, Crochemore C, René F, Monnier D, Koch B, Loeffler JP. DNA PACAP type I receptor activation promotes cerebellar neuron survival through the cAMP/PKA signaling pathway. Cell Biol 1997; 16:323-33.
83. Villalba M, Bockaert J, Journot L. Pituitary adenylate cyclase-activating polypeptide (PACAP-38) protects cerebellar granule neurons from apoptosis by activating the mitogen-activated protein kinase (MAP kinase) pathway. J Neurosci 1997; 17:83-90.
84. Galli C, Piccini A, Ciotti MT, Castellani L, Calissano P, Zaccheo D, et al. Increased amyloidogenic secretion in cerebellar granule cells undergoing apoptosis. Proc Natl Acad Sci USA 1998; 95:1247-52.
85. Piccini A, Ciotti MT, Vitolo OV, Calissano P, Tabaton M, Galli C. Endogenous APP derivatives oppositely modulate apoptosis through an autocrine loop. Neuroreport 2000; 11:1375-9.
86. De Berardinis M, Ciotti MT, Amadoro G, Galli C, Calissano P. Transfer of the apoptotic message in sister cultures of cerebellar neurons. Neuroreport 2001; 12:2137-40.
87. Atlante A, Gagliardi S, Marra E, Calissano P. Neuronal apoptosis in rats is accompanied by rapid impairment of cellular respiration and is prevented by scavengers of reactive oxygen species. Neurosci Lett 1998; 245:127-30.
88. Atlante A, Bobba A, Calissano P, Passarella S, Marra E. The apoptosis/necrosis transition in cerebellar granule cells depends on the mutual relationship of the antioxidant and the proteolytic systems which regulate ROS production and cytochrome c release en route to death. J Neurochem 2003; 84:960-71.
89. Atlante A, Passarella S. Detection of reactive oxygen species in primary cultures of cerebellar granule cells Brain Res Brain Res Protoc 1999; 4:266-70.
90. Schulz JB, Weller M, Klockgether T. Potassium deprivation-induced apoptosis of cerebellar granule neurons: a sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. J Neurosci 1996; 16:4696-706.
91. Levi-Montalcini R. Nerve growth Factor. Science 1975; 187:113.
92. Boissière F, Hunot S, Faucheux B, Hersh LB, Agid Y, Hirsch EC. Trk neurotrophin receptors in cholinergic neurons of patients with Alzheimer's disease. Dement Geriatr Cogn Disord 1997; 8:1-8.
93. Chu Y, Cochran EJ, Bennett DA, Mufson EJ, Kordower JH. Downregulation of trkA mRNA within nucleus basalis neurons in individuals with mild cognitive impairment and Alzheimer's disease. J Comp Neurol 2001; 437:296-307.
94. Ginsberg SD, Che S, Wuu J, Counts SE, Mufson EJ. Downregulation of trk but not p75NTR gene expression in single cholinergic basal forebrain neurons mark the progression of Alzheimer's disease. J Neurochem 2006; 97:475-87.
95. Mufson EJ, Lavine N, Jaffar S, Kordower JH, Quirion R, Saragovi HU. Reduction in p140-TrkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease. Exp Neurol 1997; 146:91-103.
96. Mufson EJ, Ma SY, Cochran EJ, Bennett DA, Beckett LA, Jaffar S, et al. Loss of nucleus basalis neurons containing trkA immunoreactivity in individuals with mild cognitive impairment and early Alzheimer's disease. J Comp Neurol 2000; 427:19-30.
97. Salehi A, Verhaagen J, Dijkhuizen PA, Swaab DF. Co-localization of high-affinity neurotrophin receptors in nucleus basalis of Meynert neurons and their differential reduction in Alzheimer's disease. Neuroscience 1996; 75:373-87.
98. Counts SE, Nadeem M, Wuu J, Ginsberg SD, Saragovi HU, Mufson EJ. Reduction of cortical TrkA but not p75(NTR) protein in early-stage Alzheimer's disease. Ann Neurol 2004; 56:520-31.
99. Hock C, Heese K, Hulette C, Rosenberg C, Otten U. Region-specific neurotrophin imbalances in Alzheimer disease: decreased levels of brain-derived neurotrophic factor and increased levels of nerve growth factor in hippocampus and cortical areas. Arch Neurol 2000; 57:846-51.
100. Savaskan E, Müller-Spahn F, Olivieri G, Bruttel S, Otten U, Rosenberg C, et al. Alterations in trk A, trk B and trk C receptor immunoreactivities in parietal cortex and cerebellum in Alzheimer's disease. Eur Neurol 2000; 44:172-80.
101. Costantini C, Weindruch R, Della Valle G, Puglielli L. A TrkA-to-p75NTR molecular switch activates amyloid beta-peptide generation during aging. Biochem J 2005; 391:59-67.
102. Costantini C, Scrable H, Puglielli L. An aging pathway controls the TrkA to p75NTR receptor switch and amyloid beta-peptide generation. EMBO J 2006; 25:1997-2006.
103. Costantini C, Rossi F, Formaggio E, Bernardoni R, Cecconi D, Della-Bianca V. Characterization of the signaling pathway downstream p75 neurotrophin receptor involved in beta-amyloid peptide-dependent cell death. J Mol Neurosci 2005; 25:141-56.
104. Schliebs R. Basal forebrain cholinergic dysfunction in Alzheimer's disease-interrelationship with beta-amyloid, inflammation and neurotrophin signaling. Neurochem Res 2005; 30:895-908.
105. Yeo TT, Chua-Couzens J, Butcher LL, Bredesen DE, Cooper JD, Valletta JS, et al. Absence of p75NTR causes increased basal forebrain cholinergic neuron size, choline acetyltransferase activity, and target innervation. J Neurosci 1997; 17:7594-605.
106. Volosin M, Song W, Almeida RD, Kaplan DR, Hempstead BL, Friedman WJ. Interaction of survival and death signaling in basal forebrain neurons: roles of neurotrophins and proneurotrophins. J Neurosci 2006; 26:7756-66.
107. Yaar M, Arble BL, Stewart KB, Qureshi NH, Kowall NW, Gilchrest BA. p75 (NTR) antagonistic cyclic peptide decreases the size of beta amyloid-Induced brain inflammation. Cell Mol Neurobiol 2008; 28:1027-31.
108. Sotthibundhu A, Sykes AM, Fox B, Underwood CK, Thangnipon W, Coulson EJ. Betaamyloid (1-42) induces neuronal death through the p75 neurotrophin receptor. J Neurosci 2008; 28:3941-6.
109. Ge YW, Lahiri DK. Regulation of promoter activity of the APP gene by cytokines and growth factors: implications in Alzheimer's disease. Ann NY Acad Sci 2002; 973:463-7.
110. Rossner S, Ueberham U, Schliebs R, Perez-Polo JR, Bigl V. p75 and TrkA receptor signaling independently regulate amyloid precursor protein mRNA expression, isoform composition and protein secretion in PC12 cells. J Neurochem 1998; 71:757-66.
111. Fisher A, Heldman E, Gurwitz D, Haring R, Karton Y, Meshulam H, et al. M1 agonists for the treatment of Alzheimer's disease. Novel properties and clinical update. Ann NY Acad Sci 1996; 777:189-96.
112. Tatebayashi Y, Haque N, Tung YC, Iqbal K, Grundke-Iqbal I. Role of tau phosphorylation by glycogen synthase kinase-3beta in the regulation of organelle transport. J Cell Sci 2004; 117:1653-63.
113. Nuydens R, Dispersyn G, de Jong M, van den Kieboom G, Borgers M, Geerts H. Aberrant tau phosphorylation and neurite retraction during NGF deprivation in PC12 cells. Biochem Biophys Res Commun 1997; 240:687-91.
114. Shelton SB, Johnson GV. Tau and HMW tau phosphorylation and compartmentalization in apoptotic neuronal PC12 cells. J Neurosci Res 2001; 66:203-13.
115. Corsetti V, Amadoro G, Gentile A, Capsoni S, Ciotti MT, Cencioni MT, et al. Identification of a caspase-derived N-terminal tau fragment in cellular and animal Alzheimer's disease models. Mol Cell Neurosci 2008; 38:381-92.
116. Amadoro G, Ciotti MT, Costanzi M, Cestari V, Calissano P, Canu N. NMDA receptor mediates tau-induced neurotoxicity by calpain and ERK/MAPK activation. Proc Natl Acad Sci USA 2006; 103:2892-7.
117. Babu JR, Geetha T, Wooten MW. Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J Neurochem 2005; 94:192-203.
118. Niewiadomska G, Baksalerska-Pazera M, Riedel G. Altered cellular distribution of phosphotau proteins coincides with impaired retrograde axonal transport in neurons of aged rats. Ann NY Acad Sci 2005; 1048:287-95.
119. Niewiadomska G, Baksalerska-Pazera M, Riedel G. Cytoskeletal transport in the aging brain: focus on the cholinergic system. Rev Neurosci 2006; 17:581-618.
120. Ruberti F, Capsoni S, Comparini A, Di Daniel E, Franzot J, Gonfloni S, et al. Phenotypic knockout of nerve growth factor in adult transgenic mice reveals severe deficits in basal fore-brain cholinergic neurons, cell death in the spleen and skeletal muscle dystrophy. J Neurosci 2000; 20:2589-601.
121. Capsoni S, Cattaneo A. On the molecular basis linking nerve growth factor (NGF) to Alzheimer's disease. Cell Mol Neurobiol 2006; 26:619-33.
122. Tuszynski MH, Thal L, Pay M, Salmon DP, U HS, Bakay R, et al. A phase 1 clinical trial of nerve growth factor gene therapy for Alzheimer disease. Nat Med 2005; 11:551-5.
123. Cattaneo A, Capsoni S, Paoletti F. Towards non invasive nerve growth factor therapies for Alzheimer's disease. J Alzheimers Dis 2008; 15:255-83.
124. Matrone C, Di Luzio A, Meli G, D'Aguanno S, Severini C, Ciotti MT, et al. Activation of the amyloidogenic route by NGF deprivation induces apoptotic death in PC12 cells. J Alzheimers Dis 2008; 13:81-96.
125. Matrone C, Ciotti MT, Mercanti D, Marolda R, Calissano P. NGF and BDNF signaling control amyloidogenic route and Ab production in hippocampal neurons. Proc Natl Acad Sci USA 2008; 105:13138-43.
126. Park DS, Morris EJ, Stefanis L, Troy CM, Shelanski ML, Geller HM, et al. Multiple pathways of neuronal death induced by DNA-damaging agents, NGF deprivation and oxidative stress. J Neurosci 1998; 18:830-40.
127. Troy CM, Rabacchi SA, Hohl JB, Angelastro JM, Greene LA, Shelanski ML. Death in the balance: alternative participation of the caspase-2 and -9 pathways in neuronal death induced by nerve growth factor deprivation. J Neurosci 2001; 21:5007-16.
128. Perini G, Della-Bianca V, Politi V, Della Valle G, Dal-Pra I, et al. Role of p75 neurotrophin receptor in the neurotoxicity by beta-amyloid peptides and synergistic effect of inflammatory cytokines. J Exp Med 2002; 195:907-18. Erratum in: J Exp Med 2002; 195:1231.
129. Rametti A, Esclaire F, Yardin C, Terro F. Linking alterations in tau phosphorylation and cleavage during neuronal apoptosis. J Biol Chem 2004; 279:54518-28.
130. Bhat RV, Leonov S, Luthman J, Scott CW, Lee CM. Interactions between GSK3beta and caspase signalling pathways during NGF deprivation induced cell death. J Alzheimers Dis 2002; 4:291-30.