In vivo manifestation of Notch related phenotypes in zebrafish treated with Alzheimer's amyloid reducing γ-secretase inhibitors

Journal of Neurochemistry

Volumn 113, Issue 5, 2010, Pages 1200-1209

  Yang, Ting ^a   Arslanova, Dilyara ^a   Xu, Xiaoyin ^b   Li, Yue Ming ^c   Xia, Weiming ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Alzheimer; Amyloid; Notch; Secretase; Zebrafish

Indexed keywords

AMYLOID BETA PROTEIN; CELL PROTEIN; GAMMA SECRETASE INHIBITOR; GAMMA SECRETASE INHIBITOR 18; GAMMA SECRETASE INHIBITOR A; N [N (3,5 DIFLUOROPHENACETYL ALANYL)] S PHENYLGLYCINE TERT BUTYL ESTER; NOTCH RECEPTOR; PROTEIN HER6; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENCY; DRUG SAFETY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOPATHY; GENE TARGETING; IN SITU HYBRIDIZATION; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ZEBRA FISH;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELLS, CULTURED; DIPEPTIDES; EMBRYO, NONMAMMALIAN; HEART RATE; IN SITU HYBRIDIZATION; PHENOTYPE; PIGMENTATION; PROTEASE INHIBITORS; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; ZEBRAFISH;

ANIMALIA; DANIO RERIO; VERTEBRATA;

EID: 77951905218     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06681.x     Document Type: Article

References (46)

1. Campbell W., Wolfe M. Xia W. (2005) Assays for amyloid precursor protein γ-secretase activity, in Amyloid Precursor Protein, A Practical Approach (Xia W. Xu H., eds pp. 51 68. CRC Press
2. Campbell W. A., Yang H. W., Zetterberg H., Baulac S., Sears J. A., Liu T., Wong S. T. C., Zhong T. P. Xia W. (2006) Zebrafish lacking Alzheimer Presenilin Enhancer 2 (Pen-2) demonstrate excessive p53 dependent apoptosis and neuronal loss. J. Neurochem. 96, 1423 1440.
3. Chen F., Hasegawa H., Schmitt-Ulms G. et al. (2006) TMP21 is a presenilin complex component that modulates gamma-secretase but not epsilon-secretase activity. Nature 440, 1208 1212.
4. De Strooper B., Saftig P., Craessaerts K., Vanderstichele H., Gundula G., Annaert W., Von Figura K. Van Leuven F. (1998) Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391, 387 390. (Pubitemid 28093512)
5. De Strooper B., Annaert W., Cupers P. et al. (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398, 518 522. (Pubitemid 129523590)
6. van Eeden F. J., Granato M., Schach U. et al. (1996) Mutations affecting somite formation and patterning in the zebrafish, Danio rerio. Development 123, 153 164. (Pubitemid 27056744)
7. Esler W. P., Kimberly W., Ostaszewski B., Ye W., Diehl T., Selkoe D. Wolfe M. S. (2002) Activity dependent isolation of the presenilin-g-secretase complex reveals nicastrin and a g substrate. Proc. Natl Acad. Sci. USA 99, 2720 2725. (Pubitemid 34240527)
8. Fan X., Matsui W., Khaki L., Stearns D., Chun J., Li Y. M. Eberhart C. G. (2006) Notch pathway inhibition depletes stem-like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 66, 7445 7452. (Pubitemid 44289197)
9. Fraering P. C., LaVoie M. J., Ye W., Ostaszewski B. L., Kimberly W. T., Selkoe D. J. Wolfe M. S. (2004) Detergent-dependent dissociation of active gamma-secretase reveals an interaction between Pen-2 and PS1-NTF and offers a model for subunit organization within the complex. Biochemistry 43, 323 333. (Pubitemid 38082554)
10. Francis R., McGrath G., Zhang J. et al. (2002) aph-1 and pen-2 are required for Notch pathway signaling, g-secretase cleavage of bAPP and presenilin protein accumulation. Dev. Cell 3, 85 97. (Pubitemid 34778398)
11. Geling A., Steiner H., Willem M., Bally-Cuif L. Haass C. (2002) A gamma-secretase inhibitor blocks Notch signaling in vivo and causes a severe neurogenic phenotype in zebrafish. EMBO Rep. 3, 688 694.
12. Hardy J. Selkoe D. J. (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297, 353 356. (Pubitemid 34790756)
13. 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. J. Biol. Chem. 279, 46455 46463. (Pubitemid 39518288)
14. Holtzinger A. Evans T. (2005) Gata4 regulates the formation of multiple organs. Development 132, 4005 4014. (Pubitemid 41410262)
15. Hong L., Koelsch G., Lin X., Wu S., Terzyan S., Ghosh A. K., Zhang X. C. Tang J. (2000) Structure of the protease domain of memapsin 2 (beta-secretase) complexed with inhibitor. Science 290, 150 153.
16. Isoo N., Sato C., Miyashita H., Shinohara M., Takasugi N., Morohashi Y., Tsuji S., Tomita T. Iwatsubo T. (2007) Abeta42 overproduction associated with structural changes in the catalytic pore of gamma-secretase: common effects of Pen-2 N-terminal elongation and fenofibrate. J. Biol. Chem. 282, 12388 12396. (Pubitemid 47100594)
17. Jiang Y. J., Brand M., Heisenberg C. P. et al. (1996) Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio. Development 123, 205 216. (Pubitemid 27056748)
18. Johnson-Wood K., Lee M., Motter R. et al. (1997) Amyloid precursor protein processing and A beta42 deposition in a transgenic mouse model of Alzheimer disease. Proc. Natl Acad. Sci. USA 94, 1550 1555. (Pubitemid 27087889)
19. Kim S. H. Sisodia S. S. (2005) A sequence within the first transmembrane domain of PEN-2 is critical for PEN-2-mediated endoproteolysis of presenilin 1. J. Biol. Chem. 280, 1992 2001.
20. Kukar T. L., Ladd T. B., Bann M. A. et al. (2008) Substrate-targeting gamma-secretase modulators. Nature 453, 925 929.
21. Lazarov V. K., Fraering P. C., Ye W., Wolfe M. S., Selkoe D. J. Li H. (2006) Electron microscopic structure of purified, active gamma-secretase reveals an aqueous intramembrane chamber and two pores. Proc. Natl Acad. Sci. USA 103, 6889 6894.
22. Lee S., Shah S., Li H., Yu C., Han W. Yu G. (2002) Mammalian APH-1 Interacts with Presenilin and Nicastrin, and is Required for Intramembrane Proteolysis of APP and Notch. J. Biol. Chem. 277, 45013 45019.
23. Lewis S. J., Smith A. L., Neduvelil J. G. et al. (2005) A novel series of potent gamma-secretase inhibitors based on a benzobicyclo[4.2.1]nonane core. Bioorg. Med. Chem. Lett. 15, 373 378. (Pubitemid 39647153)
24. Li T., Ma G., Cai H., Price D. L. Wong P. C. (2003) Nicastrin is required for assembly of presenilinγ-secretase complexes to mediate Notch signaling and for processing and trafficking of beta-amyloid precursor protein in mammals. J. Neurosci. 23, 3272 3277. (Pubitemid 36531968)
25. Netzer W. J., Dou F., Cai D. et al. (2003) Gleevec inhibits beta-amyloid production but not Notch cleavage. Proc. Natl Acad. Sci. USA 100, 12444 12449. Epub 12003 Oct 12441. (Pubitemid 37271579)
26. Petit A., Pasini A., Alves Da Costa C. et al. (2003) JLK isocoumarin inhibitors: selective gamma-secretase inhibitors that do not interfere with notch pathway in vitro or in vivo. J. Neurosci. Res. 74, 370 377. (Pubitemid 37362813)
27. Placanica L., Tarassishin L., Yang G., Peethumnongsin E., Kim S. H., Zheng H., Sisodia S. Li Y. M. (2009) PEN2 and presenilin-1 modulate the dynamic equilibrium of presenilin-1 and presenilin-2 gamma -secretase complexes. J. Biol. Chem. 284 (5 2967 2977.
28. Searfoss G. H., Jordan W. H., Calligaro D. O. et al. (2003) Adipsin, a biomarker of gastrointestinal toxicity mediated by a functional gamma-secretase inhibitor. J. Biol. Chem. 278, 46107 46116.
29. Seiffert D., Bradley J. D., Rominger C. M. et al. (2000) Presenilin-1 and -2 are molecular targets for gamma-secretase inhibitors. J. Biol. Chem. 275, 34086 34091.
30. Selkoe D. J. (1999) Translating cell biology into therapeutic advances in Alzheimer's disease. Nature 399 (Supp A23 A31.
31. Serneels L., Dejaegere T., Craessaerts K. et al. (2005) Differential contribution of the three Aph1 genes to gamma-secretase activity in vivo. Proc. Natl Acad. Sci. USA 102, 1719 1724. (Pubitemid 40209234)
32. Shah S., Lee S. F., Tabuchi K. et al. (2005) Nicastrin functions as a gamma-secretase-substrate receptor. Cell 122, 435 447.
33. Shelton C. C., Zhu L., Chau D., Yang L., Wang R., Djaballah H., Zheng H. Li Y. M. (2009) Modulation of gamma-secretase specificity using small molecule allosteric inhibitors. Proc. Natl Acad. Sci. USA 106, 20228 20233.
34. Shirotani K., Edbauer D., Capell A., Schmitz J., Steiner H. Haass C. (2003) gamma-Secretase activity is associated with a conformational change of nicastrin. J. Biol. Chem. 278, 16474 16477. (Pubitemid 36799505)
35. Siman R. Velji J. (2003) Localization of presenilin-nicastrin complexes and gamma-secretase activity to the trans-Golgi network. J. Neurochem. 84, 1143 1153. (Pubitemid 36330666)
36. Tian Y., Bassit B., Chau D. Li Y. M. (2010) An APP inhibitory domain containing the Flemish mutation residue modulates gamma-secretase activity for Abeta production. Nat. Struct. Mol. Biol. 17, 151 158.
37. Weggen S., Eriksen J. L., Das P. et al. (2001) A subset of NSAIDs lower amyloidogenic Abeta42 independently of cyclooxygenase activity. Nature 414, 212 216. (Pubitemid 33051236)
38. Wolfe M. S., Xia W., Ostaszewski B. L., Diehl T. S., Kimberly W. T. Selkoe D. J. (1999) Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity. Nature 398, 513 517. (Pubitemid 129523589)
39. Wong G. T., Manfra D., Poulet F. M. et al. (2004) Chronic treatment with the gamma-secretase inhibitor LY-411,575 inhibits beta-amyloid peptide production and alters lymphopoiesis and intestinal cell differentiation. J. Biol. Chem. 279, 12876 12882. Epub 12004 Jan 12876. (Pubitemid 38445862)
40. Xia W. (2001) Amyloid metabolism and secretases in Alzheimer's disease. Curr. Neurol. Neurosci. Rep. 1, 422 427.
41. Xia W. Wolfe M. (2003) Intramembrane proteolysis by presenilin and presenilin-like proteases. J. Cell Sci. 116, 2839 2844. (Pubitemid 36926973)
42. Yang T., Arslanova D., Gu Y., Augelli-Szafran C. Xia W. (2008) Quantification of gamma-secretase modulation differentiates inhibitor compound selectivity between two substrates Notch and amyloid precursor protein. Mol. Brain 1, 15.
43. Yu G., Nishimura M., Arawaka S. et al. (2000) Nicastrin modulates presenilin-mediated notch&glp-1 signal transduction and betaAPP processing. Nature 407, 48 54.
44. Zetterberg H., Campbell W. A., Yang H. W. Xia W. (2006) The cytosolic loop of the gamma-secretase component presenilin enhancer 2 (Pen-2) protects zebrafish embryos from apoptosis. J. Biol. Chem. 281, 11933 11939. (Pubitemid 43855456)
45. Zhong T. P., Childs S., Leu J. P. Fishman M. C. (2001) Gridlock signalling pathway fashions the first embryonic artery. Nature 414, 216 220. (Pubitemid 33051237)
46. Zon L. I. Peterson R. T. (2005) In vivo drug discovery in the zebrafish. Nat. Rev. Drug Discov. 4, 35 44.