Zebrafish lacking Alzheimer presenilin enhancer 2 (Pen-2) demonstrate excessive p53-dependent apoptosis and neuronal loss

Journal of Neurochemistry

Volumn 96, Issue 5, 2006, Pages 1423-1440

  Campbell, William A ^a   Yang, Hongwei ^a   Zetterberg, Henrik ^a   Baulac, Stéphanie ^a   Sears, Jacqueline A ^a   Liu, Tianming ^b   Wong, Stephen T C ^b   Zhong, Tao P ^c   Xia, Weiming ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d HARVARD INSTITUTES OF MEDICINE   (United States)

Author keywords

secretase; Alzheimer's disease; Pen 2; Presenilin; Zebrafish

Indexed keywords

AMYLOID BETA PROTEIN; ANTERIOR PHARYNX DEFECTIVE 1 PROTEIN; ANTISENSE OLIGODEOXYNUCLEOTIDE; GAMMA SECRETASE; ISLET 1 PROTEIN; MORPHOLINE DERIVATIVE; NICASTRIN; NOTCH RECEPTOR; PRESENILIN ENHANCER 2; PROTEIN; PROTEIN P53; PROTEIN SUBUNIT; TUBULIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL LOSS; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EXTRACHROMOSOMAL INHERITANCE; GENE LOSS; NERVE CELL DIFFERENTIATION; NERVE CELL LOSS; NEURAL STEM CELL; NONHUMAN; NOTCH INTRACELLULAR DOMAIN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; ZEBRA FISH;

ALZHEIMER DISEASE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BODY PATTERNING; CELL COUNT; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; EMBRYO, NONMAMMALIAN; FISH PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN SITU NICK-END LABELING; INDOLES; MEMBRANE PROTEINS; NEURONS; OLIGONUCLEOTIDES, ANTISENSE; PRESENILIN-2; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P53; ZEBRAFISH; ZEBRAFISH PROTEINS;

ANIMALIA; DANIO RERIO;

EID: 33645101015     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.03648.x     Document Type: Article

References (88)

1. Alberici A. Moratto D. Benussi L. et al. 1999 Presenilin 1 protein directly interacts with Bcl-2 JBiolChem 274 30 764 30 769
2. Alves da Costa C. Paitel E. Mattson MP. Amson R. Telerman A. Ancolio K. Checler F. 2002 Wild-type and mutated presenilins 2 trigger p53-dependent apoptosis and down-regulate presenilin 1 expression in HEK293 human cells and in murine neurons ProcNatl AcadSciUSA 99 4043 4048
3. Alves da Costa C. Mattson MP. Ancolio K. Checler F. 2003 The C-terminal fragment of presenilin 2 triggers p53-mediated staurosporine-induced apoptosis, a function independent of the presenilinase-derived N-terminal counterpart JBiolChem 278 12 064 12 069
4. Amson R. Lassalle JM. Halley H. et al. 2000 Behavioral alterations associated with apoptosis and down-regulation of presenilin 1 in the brains of p53-deficient mice ProcNatl AcadSciUSA 97 5346 5350
5. Arawaka S. Hasegawa H. Tandon A. et al. 2002 The levels of mature glycosylated nicastrin are regulated and correlate with γ-secretase processing of amyloid β-precursor protein JNeurochem 83 1065 1071
6. Baulac S. Lavoie M. Kimberly W. Strahle J. Wolfe M. Selkoe D. Xia W. 2003 Functional γ-secretase complex assembly in Golgi/trans-Golgi network: interactions among presenilin, nicastrin, Aph1, Pen-2 and γ-secretase substrates NeurobiolDis 14 194 204
7. Berghmans S. Murphey RD. Wienholds E. et al. 2005 tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors ProcNatl AcadSciUSA 102 407 412
8. Bergman A. Hansson EM. Pursglove SE. Farmery MR. Lannfelt L. Lendahl U. Lundkvist J. Naslund J. 2004 Pen-2 is sequestered in the endoplasmic reticulum and subjected to ubiquitylation and proteasome-mediated degradation in the absence of presenilin JBiolChem 279 16 744 16 753
9. Bernardos RL. Lentz SI. Wolfe MS. Raymond PA. 2005 Notch-Δ signaling is required for spatial patterning and Muller glia differentiation in the zebrafish retina DevBiol 278 381 395
10. Borchelt DR. Thinakaran G. Eckman CB. et al. 1996 Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo Neuron 17 1005 1013
11. Campbell W. Iskandar M-K. Reed M. Xia W. 2002 Endoproteolysis of presenilin in vitro: inhibition by γ-secretase inhibitors Biochemistry 41 3372 3379
12. Campbell W. Reed ML. Strahle J. Wolfe MS. Xia Wq13 2003 Presenilin endoproteolysis mediated by an aspartyl protease activity pharmacologically distinct from γ-secretase JNeurochem 85 1563 1574
13. Chen F. Tandon ASN. Gu YJ. et al. 2003 Presenilin 1 and presenilin 2 have differential effects on the stability and maturation of nicastrin in mammalian brain JBiolChem 278 19 974 19 979
14. Chipuk JE. Kuwana T. Bouchier-Hayes L. Droin NM. Newmeyer DD. Schuler M. Green DR. 2004 Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis Science 303 1010 1014
15. Clarke PG. 1985 Neuronal death during development in the isthmo-optic nucleus of the chick: sustaining role of afferents from the tectumq14 JCompNeurol 234 365 379
16. Clarke JD. Hayes BP. Hunt SP. Roberts A. 1984 Sensory physiology, anatomy and immunohistochemistry of Rohon-Beard neurones in embryos of Xenopus laevis JPhysiol 348 511 525
17. Cowan WM. Fawcett JW. O'Leary DD. Stanfield BB. 1984 Regressive events in neurogenesis Science 225 1258 1265
18. Crystal AS. Morais VA. Fortna RR. Carlin D. Pierson TC. Wilson CA. Lee VM. Doms RW. 2004 Presenilin modulates Pen-2 levels post-translationally by protecting it from proteasomal degradation Biochemistry 43 3555 3563
19. De Strooper B. 2003 Aph-1, Pen-2, and nicastrin with presenilin generate an active γ-secretase complex Neuron 38 9 12
20. De Strooper B. Annaert W. Cupers P. et al. 1999 A presenilin-1-dependent γ-secretase-like protease mediates release of Notch intracellular domain Nature 398 518 522
21. Derer P. Derer M. 1990 Cajal-Retzius cell ontogenesis and death in mouse brain visualized with horseradish peroxidase and electron microscopy Neuroscience 36 839 856
22. Dumont P. Leu JI. Della Pietra AC. 3rd, George DL. Murphy M. 2003 The codon 72 polymorphic variants of p53 have markedly different apoptotic potential NatGenet 33 357 365
23. Edbauer D. Winkler E. Regula JT. Pesold B. Steiner H. Haass C. 2003 Reconstitution of γ-secretase activity NatCell Biol 7 7
24. Ericson J. Thor S. Edlund T. Jessell TM. Yamada T. 1992 Early stages of motor neuron differentiation revealed by expression of homeobox gene islet-1 Science 256 1555 1560
25. Fei P. El-Deiry WS. 2003 P53 and radiation responses Oncogene 22 5774 5783
26. Fortna RR. Crystal AS. Morais VA. Pijak DS. Lee VM. Doms RW. 2004 Membrane topology and nicastrin-enhanced endoproteolysis of APH-1, a component of the γ-secretase complex JBiolChem 279 3685 3693
27. Fraering PC. LaVoie MJ. Ye W. Ostaszewski BL. Kimberly WT. Selkoe DJ. Wolfe MS. 2004 Detergent-dependent dissociation of active γ-secretase reveals an interaction between Pen-2 and PS1-NTF and offers a model for subunit organization within the complex Biochemistry 43 323 333
28. Francis R. McGrath G. Zhang J. et al. 2002 aph-1 and pen-2 are required for Notch pathway signaling, γ-secretase cleavage of bAPP and presenilin protein accumulation DevCell 3 85 97
29. Geling A. Steiner H. Willem M. Bally-Cuif L. Haass C. 2002 A γ-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish EMBO Report 3 688 694
30. Groth C. Nornes S. McCarty R. Tamme R. Lardelli M. 2002 Identification of a second presenilin gene in zebrafish with similarity to the human Alzheimer's disease gene presenilin2 DevGenes Evol 212 486 490
31. Gu Y. Chen F. Sanjo N. et al. 2003 APH-1 interacts with mature and immature forms of presenilins and nicastrin and may play a role in maturation of presenilin-nicastrin complexes JBiolChem 278 7374 7380
32. Guo Y. Livne-Bar I. Zhou L. Boulianne GL. 1999 Drosophila presenilin is required for neuronal differentiation and affects notch subcellular localization and signaling JNeurosci 19 8435 8442
33. Handler M. Yang X. Shen J. 2000 Presenilin-1 regulates neuronal differentiation during neurogenesis Development 127 2593 2606
34. Hasegawa H. Sanjo N. Chen F. et al. 2004 Both the sequence and length of the C terminus of PEN-2 are critical for intermolecular interactions and function of presenilin complexes JBiolChem 279 46 455 46 463
35. Henion PD. Raible DW. Beattie CE. Stoesser KL. Weston JA. Eisen JS. 1996 Screen for mutations affecting development of zebrafish neural crest DevGenet 18 11 17
36. Hu Y. Fortini M. 2003 Different cofactor activities in γ-secretase assembly: evidence for a nicastrin-Aph-1 subcomplex JCell Biol 161 685 690
37. Inoue A. Takahashi M. Hatta K. Hotta Y. Okamoto H. 1994 Developmental regulation of islet-1 mRNA expression during neuronal differentiation in embryonic zebrafish DevDyn 199 1 11
38. Itoh M. Kim CH. Palardy G. et al. 2003 Mind bomb is a ubiquitin ligase that is essential for efficient activation of Notch signaling by Delta DevCell 4 67 82
39. Jackman WR. Langeland JA. Kimmel CB. 2000 Islet reveals segmentation in the Amphioxus hindbrain homolog DevBiol 220 16 26
40. Johnstone RW. Ruefli AA. Lowe SW. 2002 Apoptosis: a link between cancer genetics and chemotherapy Cell 108 153 164
41. Kim SH. Sisodia SS. 2005 A sequence within the first transmembrane domain of PEN-2 is critical for PEN-2-mediated endoproteolysis of presenilin 1 JBiolChem 280 1992 2001
42. Kimberly WT. LaVoie MJ. Ostaszewski BL. Ye W. Wolfe MS. Selkoe DJ. 2002 Complex N-linked glycosylated nicastrin associates with active γ-secretase and undergoes tight cellular regulation JBiolChem 277 35 113 35 117
43. Kimberly W. LaVoie M. Ostaszewski BL. Ye W. Wolfe MS. Selkoe DJ. 2003 γ-Secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2 ProcNatl AcadSciUSA 100 6382 6387
44. Kimmel CB. Ballard WW. Kimmel SR. Ullmann B. Schilling TF. 1995 Stages of embryonic development of the zebrafish DevDyn 203 253 310
45. Korzh V. Edlund T. Thor S. 1993 Zebrafish primary neurons initiate expression of the LIM homeodomain protein Isl-1 at the end of gastrulation Development 118 417 425
46. Kovacs DM. Mancini R. Henderson J. Na SJ. Schmidt SD. Kim TW. Tanzi RE. 1999 Staurosporine-induced activation of caspase-3 is potentiated by presenilin 1 familial Alzheimer's disease mutations in human neuroglioma cells JNeurochem 73 2278 2285
47. Langheinrich U. Hennen E. Stott G. Vacun G. 2002 Zebrafish as a model organism for the identification and characterization of drugs and genes affecting p53 signaling CurrBiol 12 2023 2028
48. LaVoie MJ. Fraering PC. Ostaszewski BL. Ye W. Kimberly WT. Wolfe MS. Selkoe DJ. 2003 Assembly of the γ-secretase complex involves early formation of an intermediate subcomplex of Aph-1 and nicastrin JBiolChem 278 37 213 37 222
49. Lee S. Shah S. Li HYuC. Han W. Yu G. 2002 Mammalian APH-1 interacts with presenilin and nicastrin, and is required for intramembrane proteolysis of APP and Notch JBiolChem 277 45 013 45 019 q15
50. Leem JY. Vijayan S. Han P. Cai D. Machura M. Lopes KO. Veselits ML. Xu H. Thinakaran G. 2002 Presenilin 1 is required for maturation and cell surface accumulation of nicastrin JBiolChem 277 19 236 19 240
51. Leimer U. Lun K. Romig H. Walter J. Grunberg J. Brand M. Haass C. 1999 Zebrafish (Danio rerio) presenilin promotes aberrant amyloid β-peptide production and requires a critical aspartate residue for its function in amyloidogenesis Biochemistry 38 13 602 13 609
52. Leu JI. Dumont P. Hafey M. Murphy ME. George DL. 2004 Mitochondrial p53 activates Bak and causes disruption of a Bak-Mcl1 complex NatCell Biol 6 443 450
53. Liu TX. Howlett NG. Deng M. Langenau DM. Hsu K. Rhodes J. Kanki JP. D'Andrea AD. Look AT. 2003 Knockdown of zebrafish Fancd2 causes developmental abnormalities via p53-dependent apoptosis DevCell 5 903 914
54. Luo WJ. Wang H. Li H. Kim BS. Shah S. Lee HJ. Thinakaran G. Kim TW. Yu G. Xu H. 2003 PEN-2 and APH-1 coordinately regulate proteolytic processing of presenilin 1 JBiolChem 278 7850 7854
55. Metcalfe WK. Myers PZ. Trevarrow B. Bass MB. Kimmel CB. 1990 Primary neurons that express the L2/HNK-1 carbohydrate during early development in the zebrafish Development 110 491 504
56. Mihara M. Erster S. Zaika A. Petrenko O. Chittenden T. Pancoska P. Moll UM. 2003 p53 has a direct apoptogenic role at the mitochondria MolCell 11 577 590
57. Miyashita T. Reed JC. 1995 Tumor suppressor p53 is a direct transcriptional activator of the human bax gene Cell 80 293 299
58. Morais VA. Crystal AS. Pijak DS. Carlin D. Costa J. Lee VM. Doms RW. 2003 The transmembrane domain region of nicastrin mediates direct interactions with APH-1 and the γ-secretase complex JBiolChem 278 43 284 43 291
59. Nakano K. Vousden KH. 2001 PUMA, a novel proapoptotic gene, is induced by p53 MolCell 7 683 694
60. Nornes S. Groth C. Camp E. Ey P. Lardelli M. 2003 Developmental control of presenilin1 expression, endoproteolysis, and interaction in zebrafish embryos ExpCell Res 289 124 132
61. Oda E. Ohki R. Murasawa H. Nemoto J. Shibue T. Yamashita T. Tokino T. Taniguchi T. Tanaka N. 2000 Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis Science 288 1053 1058
62. Oppenheim RW. 1991 Cell death during development of the nervous system AnnuRevNeurosci 14 453 501
63. Passer BJ. Pellegrini L. Vito P. Ganjei JK. D'Adamio L. 1999 Interaction of Alzheimer's presenilin-1 and presenilin-2 with Bcl-X (L). A potential role in modulating the threshold of cell death JBiolChem 274 24 007 24 013
64. 299 and occur as stable N- and C-terminal fragments in normal and Alzheimer brain tissue NeurobiolDis 3 325 337
65. Prokop S. Shirotani K. Edbauer D. Haass C. Steiner H. 2004 Requirement of PEN-2 for stabilization of the presenilin N-/C-terminal fragment heterodimer within the γ-secretase complex JBiolChem 279 23 255 23 261
66. Prokop S. Haass C. Steiner H. 2005 Length and overall sequence of the PEN-2 C-terminal domain determines its function in the stabilization of presenilin fragments JNeurochem 94 57 62
67. Roperch JP. Alvaro V. Prieur S. et al. 1998 Inhibition of presenilin 1 expression is promoted by p53 and p21WAF-1 and results in apoptosis and tumor suppression NatMed 4 835 838
68. Sax JK. Fei P. Murphy ME. Bernhard E. Korsmeyer SJ. El-Deiry WS. 2002 BID regulation by p53 contributes to chemosensitivity NatCell Biol 4 842 849
69. Selkoe DJ. 2004 Alzheimer's disease: mechanistic understanding predicts novel therapies AnnInternMed 140 627 638
70. Serneels L. Dejaegere T. Craessaerts K. et al. 2005 Differential contribution of the three Aph1 genes to γ-secretase activity in vivo ProcNatl AcadSciUSA 102 1719 1724
71. Shen J. Bronson RT. Chen DF. Xia W. Selkoe DJ. Tonegawa S. 1997 Skeletal and CNS defects in presnilin-1 deficient mice Cell 89 629 639
72. 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 γ-secretase complex required for coordinated expression of presenilin and nicastrin JBiolChem 277 39 062 39 065
73. Takasugi N. Tomita T. Hayashi I. Tsuruoka M. Niimura M. Takahashi Y. Thinakaran G. Iwatsubo T. 2003 The role of presenilin cofactors in the γ-secretase complex Nature 422 438 441
74. Thinakaran G. Borchelt DR. Lee MK. et al. 1996 Endoprotreolysis of presenilin 1 and accumulation of processed derivatives in vivo Neuron 17 181 190
75. Thisse C. Thisse B. Schilling TF. Postlethwait JH. 1993 Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail, and no tail mutant embryos Development 119 1203 1215
76. Thor S. Thomas JB. 1997 The Drosophila islet gene governs axon pathfinding and neurotransmitter identity Neuron 18 397 409
77. Tomita T. Katayama R. Takikawa R. Iwatsubo T. 2002 Complex N-glycosylated form of nicastrin is stabilized and selectively bound to presenilin fragments FEBS Lett 520 117 121
78. Vogelstein B. Lane D. Levine AJ. 2000 Surfing the p53 network Nature 408 307 310
79. Westerfield M. 1994 The Zebrafish Book, pp. q16 10 16 University of Oregon Press Eugene, OR
80. Williams JA. Barrios A. Gatchalian C. Rubin L. Wilson SW. Holder N. 2000 Programmed cell death in zebrafish Rohon-Beard neurons is influenced by TrkC1/NT-3 signaling DevBiol 226 220 230
81. Wolfe MS. Xia W. Ostaszewski BL. Diehl TS. Kimberly WT. Selkoe DJ. 1999 Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity Nature 398 513 517
82. Xia W. Wolfe M. 2003 Intramembrane proteolysis by presenilin and presenilin-like proteases JCell Sci 116 2839 2844
83. Xie Z. Romano DM. Kovacs DM. Tanzi RE. 2004 Effects of RNA interference-mediated silencing of γ-secretase complex components on cell sensitivity to caspase-3 activation JBiolChem 279 34 130 34 137
84. Xu X. Shi YC. Gao W. Mao G. Zhao G. Agrawal S. Chisolm GM. Sui D. Cui MZ. 2002 The novel presenilin-1-associated protein is a proapoptotic mitochondrial protein JBiolChem 277 48 913 48 922
85. Yang D-S. Tandon A. Chen F. et al. 2002 Mature glycosylation and trafficking of nicastrin modulate its binding to presenilins JBiolChem 277 28 135 28 142
86. Yang X. Klein R. Tian X. Cheng HT. Kopan R. Shen J. 2004 Notch activation induces apoptosis in neural progenitor cells through a p53-dependent pathway DevBiol 269 81 94
87. Zhang L. Lee J. Song L. Sun X. Shen J. Terracina G. Parker EM. 2005 Characterization of the reconstituted γ-secretase complex from Sf9 cells co-expressing presenilin 1, nicastrin, aph-1a, and pen-2 Biochemistry 44 4450 4457
88. Zhang Z. Hartmann H. Do VM. et al. 1998 Destabilization of β-catenin by mutations in presenilin-1 potentiates neuronal apoptosis Nature 395 698 702