Mice lacking both presenilin genes exhibit early embryonic patterning defects

Genes and Development

Volumn 13, Issue 21, 1999, Pages 2801-2810

  Donoviel, Dorit B ^a   Hadjantonakis, Anna Katerina ^a   Ikeda, Masaki ^b   Zheng, Hui ^c,e   Hyslop, Peter St George ^b   Bernstein, Alan ^a,d  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c MERCK RESEARCH LABORATORIES   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Alzheimer's Disease; Notch; Presenilin; Somite segmentation

Indexed keywords

PRESENILIN 1; PRESENILIN 2;

ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; MESENCHYME CELL; MOUSE; NEURAL TUBE; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL;

ANIMALS; BODY PATTERNING; EMBRYONIC AND FETAL DEVELOPMENT; GENE TARGETING; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; PRESENILIN-1; PRESENILIN-2; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

INVERTEBRATA; MAMMALIA; RODENTIA; VERTEBRATA;

EID: 0032728957     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.21.2801     Document Type: Article

References (71)

1. Akanawa, C., Y. Sasai, S. Nakanishi, and R. Kageyama. 1992. Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J. Biol. Chem. 267: 21879-21885.
2. Anafi, M., F. Kiefer, G.D. Gish, G. Mbamalu, N.N. Iscove, and T. Pawson. 1997. SH2/SH3 adaptor proteins can link tyrosine kinases to a ste20-related protein kinase, HPK1. J. Biol. Chem. 272: 27804-27811.
3. Artavanis-Tsakonas, S., M.D. Rand, and R.J. Lake. 1999. Notch signaling: Cell fate control and signal integration in development. Science 284: 770-776.
4. Baumeister, R., U. Leimer, I. Zweckbronner, C. Jakubek, J. Grunberg, and C. Haass. 1997. Human presenilin-1, but not familial Alzheimer's disease (FAD) mutants, facilitate Caenorhabditis elegans Notch signalling independently of proteolytic processing. Genes Funct. 1: 149-159.
5. Berezovska, O., M.Q. Xia, and B.T. Hyman. 1998. Notch is expressed in adult brain, is coexpressed with presenilin-1, and is altered in Alzheimer disease. J. Neuropathol. Exp. Neurol. 57: 738-745.
6. Bettenhausen, B., M. Hrabe de Angelis, D. Simon, J.L. Guenet, and A. Gossler. 1995. Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 121: 2407-2418.
7. Blacker, D. and R.E. Tanzi. 1998. The genetics of Alzheimer disease: Current status and future prospects. Arch. Neurol. 55: 294-296.
8. Buxbaum, I.D., E.K. Choi, Y. Luo, C. Lilliehook, A.C. Crowley, D.E. Merriam, and W. Wasco. 1998. Calsenilin: A calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment. Nat. Med. 4: 1177-1181.
9. Chartier-Harlin, M.C., F. Crawford, H. Houlden, A. Warren, D. Hughes, L. Fidani, A. Goate, M. Rossor, P. Roques, J. Hardy et al. 1991. Early-onset Alzheimer's disease caused by mutations at codon 717 of the beta-amyloid precursor protein gene. Nature 353: 844-846.
10. Chen, Z.F. and R.R. Behringer. 1995. twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes & Dev. 9: 686-699.
11. Conlon, R.A. and J. Rossant. 1992. Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116: 357-368.
12. Conlon, R.A., A.G. Reaume, and J. Rossant. 1995. Notch1 is required for the coordinate segmentation of somites. Development 121: 1533-1545.
13. Cook, D.G., J.C. Sung, T.E. Golde, K.M. Felsenstein, B.S. Wojczyk, R.E. Tanzi, J.Q. Trojanowski, V.M. Lee, and R.W. Doms. 1996. Expression and analysis of presenilin 1 in a human neuronal system: Localization in cell bodies and dendrites. Proc. Natl. Acad. Sci. 93: 9223-9228.
14. Dale, J.K., C. Vesque, T.J. Lints, T.K. Sampath, A. Furley, J. Dodd, and M. Placzek. 1997. Cooperation of BMP7 and SHH in the induction of forebrain ventral midline cells by prechordal mesoderm. Cell 90: 257-269.
15. Davis, J.A., S. Naruse, H. Chen, C. Eckman, S. Younkin, D.L. Price, D.R. Borchelt, S.S. Sisodia, and P.C. Wong. 1998. An Alzheimer's disease-linked PS1 variant rescues the developmental abnormalities of PS1-deficient embryos. Neuron 20: 603-609.
16. de la Pompa, J.L., A. Wakeham, K.M. Correia, E. Samper, S. Brown, R.J. Aguilera, T. Nakano, T. Honjo, T.W. Mak, J. Rossant, and R.A. Conlon. 1997. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124: 1139-1148.
17. De Strooper, B., M. Beullens, B. Contreras, L. Levesque, K. Craessaerts, B. Cordell, D. Moechars, M. Bollen, P. Fraser, P. St George Hyslop, and F. Van Leuven. 1997. Phosphorylation, subcellular localization, and membrane orientation of the Alzheimer's disease-associated presenilins. J. Biol. Chem. 272: 3590-3598.
18. De Strooper, B., P. Saftig, K. Craessaerts, H. Vanderstichele, G. Guhde, W. Annaert, K. Von Figura, and F. Van Leuven. 1998. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391: 387-390.
19. De Strooper, B., W. Annaert, P. Cupers, P. Saftig, K. Craessaerts, J.S. Mumm, E.H. Schroeter, V. Schrijvers, M.S. Wolfe, W.J. Ray, A. Goate, and R. Kopan. 1999. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398: 518-522.
20. Dewji, N.N. and S.J. Singer. 1997. Cell surface expression of the Alzheimer disease-related presenilin proteins. Proc. Natl. Acad. Sci. 94: 9926-9931.
21. Doan, A., G. Thinakaran, D.R. Borchelt, H.H. Slunt, T. Ratovitsky, M. Podlisny, D.J. Selkoe, M. Seeger, S.E. Gandy, D.L. Price, and S.S. Sisodia. 1996. Protein topology of presenilin 1. Neuron 17: 1023-1030.
22. Duff, K., C. Eckman, C. Zehr, X. Yu, C.M. Prada, J. Perez-tur, M. Hutton, L. Buee, Y. Harigaya, D. Yager et al. 1996. Increased amyloid-beta42(43) in brains of mice expressing mutant presenilin 1. Nature 383: 710-713.
23. Dumanchin, C., C. Czech, D. Campion, M.H. Cuif, T. Poyot, C. Martin, F. Charbonnier, B. Goud, L. Pradier, and T. Frebourg. 1999. Presenilins interact with Rab11, a small GTPase involved in the regulation of vesicular transport. Hum. Mol. Genet. 8: 1263-1269.
24. Echelard, Y., D.J. Epstein, B. St-Jacques, L. Shen, J. Mohler, J.A. McMahon, and A.P. McMahon. 1993. Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75: 1417-1430.
25. Ensini, M., T.N. Tsuchida, H.G. Belting, and T.M, Jessell. 1998. The control of rostrocaudal pattern in the developing spinal cord: Specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 125: 969-982.
26. Evrard, Y.A., Y. Lun, A. Aulehla, L. Gan, and R.L. Johnson. 1998. lunatic fringe is an essential mediator of somite segmentation and patterning. Nature 394: 377-381.
27. Hayat, M. 1974. Principles and techniques of scanning electron microscopy: Biological applications. Van Nostrand Rienhold, New York, NY.
28. Kovacs, D.M., H.J. Fausett, K.J. Page, T.W. Kim, R.D. Moir, D.E. Merriam, R.D. Hollister, O.G. Hallmark, R. Mancini, K.M. Felsenstein et al. 1996. Alzheimer-associated presenilins 1 and 2: Neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nat. Med. 2: 224-229.
29. Lee, M.K., H.H. Slunt, L.J. Martin, G. Thinakaran, G. Kim, S.E. Gandy, M. Seeger, E. Koo, D.L. Price, and S.S. Sisodia. 1996. Expression of presenilin 1 and 2 (PS1 and PS2) in human and murine tissues. J. Neurosci. 16: 7513-7525.
30. Levesque, G., G. Yu, M. Nishimura, D.M. Zhang, L. Levesque, H. Yu, D. Xu, Y. Liang, E. Rogaeva, M. Ikeda et al. 1999. Presenilins interact with armadillo proteins including neural-specific plakophilin-related protein and beta-catenin. J. Neurochem. 72: 999-1008.
31. Levitan, D. and I. Greenwald. 1995. Facilitation of lin-12-mediated signalling by sel12, a Caenorhabditis elegans S182 Alzheimer's disease gene. Nature 377: 351-354.
32. Levitan, D., T.G. Doyle, D. Brousseau, M.K. Lee, G. Thinakaran, H.H. Slunt, S.S. Sisodia, and I. Greenwald. 1996. Assessment of normal and mutant human presenilin function in Caenorhabditis elegans. Proc. Natl. Acad. Sci. 93: 14940-14944.
33. Levy-Lahad, E., W. Wasco, P. Poorkaj, D.M. Romano, J. Oshima, W.H. Pettingell, C.E. Yu, P.D. Jondro, S.D. Schmidt, K. Wang et al. 1995. Candidate gene for the chromosome 1 familial Alzheimer's disease locus. Science 269: 973-977.
34. Li, J., M. Xu, H. Zhou, I. Ma, and H. Potter. 1997. Alzheimer presenilins in the nuclear membrane, interphase kinetochores, and centrosomes suggest a role in chromosome segregation. Cell 90: 917-927.
35. Li, X. and I. Greenwald. 1996. Membrane topology of the C. elegans SEL-12 presenilin. Neuron 17: 1015-1021.
36. _. 1997. HOP-1, a Caenorhabditis elegans presenilin, appears to be functionally redundant with SEL-12 presenilin and to facilitate LIN-12 and GLP-1 signaling. Proc. Natl. Acad. Sci. 94: 12204-12209.
37. _. 1998. Additional evidence for an eight-transmembrane-domain topology for Caenorhabditis elegans and human presenilins. Proc. Natl. Acad. Sci. 95: 7109-7114.
38. Lu, F.M. and S.E. Lux. 1996. Constitutively active human Notch1 binds to the transcription factor CBF1 and stimulates transcription through a promoter containing a CBF1-responsive element. Proc. Natl. Acad. Sci. 93: 5663-5667.
39. Mansouri, A., Y. Yokota, R. Wehr, N.G. Copeland, N.A. Jenkins, and P. Gruss. 1997. Paired-related murine homeobox gene expressed in the developing sclerotome, kidney, and nervous system. Dev. Dyn.210: 53-65.
40. Matsuno, K., M.J. Go, X. Sun, D.S. Eastman, and S. Artavanis-Tsakonas. 1997. Suppressor of Hairless-independent events in Notch signaling imply novel pathway elements. Development 124: 4265-4273.
41. Murayama, M., S. Tanaka, J. Palacino, O. Murayama, T. Honda, X. Sun, K. Yasutake, N. Nihonmatsu, B. Wolozin, and A. Takashima. 1998. Direct association of presenilin-1 with beta-catenin. FEES Lett. 433: 73-77.
42. Murrell, J., M. Farlow, B. Ghetti, and M.D. Benson. 1991. A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 254: 97-99.
43. Nishimura, M., G. Yu, G. Levesque, D.M. Zhang, L. Ruel, F. Chen, P. Milman, E. Holmes, Y. Liang, T. Kawarai et al. 1999a. Presenilin mutations associated with Alzheimer disease cause defective intracellular trafficking of beta-catenin, a component of the presenilin protein complex. Nat. Med. 5: 164-169.
44. Nishimura, M., G. Yu, and P.H. St George-Hyslop. 1999b. Biology of presenilins as causative molecules for Alzheimer disease. Clin. Genet. 55: 219-225.
45. Ohtsuka, T., M. Ishibashi, G. Gradwohl, S. Nakanishi, F. Guillemot, and R. Kageyama. 1999. Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J. 18: 2196-2207.
46. Oka, C., T. Nakano, A. Wakeham, J.L. de la Pompa, C. Mori, T. Sakai, S. Okazaki, M. Kawaichi, K. Shiota, T.W. Mak, and T. Honjo. 1995. Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development 121: 3291-3301.
47. Oyama, F., N. Sawamura, K. Kobayashi, M. Morishima-Kawashima, T. Kuramochi, M. Ito, T. Tomita, K. Maruyama, T.C. Saido, T. Iwatsubo et al. 1998. Mutant presenilin 2 transgenic mouse: Effect on an age-dependent increase of amyloid beta-protein 42 in the brain. J. Neurochem. 71: 313-322.
48. Pirity, M., A.K. Hadjantonakis, and A. Nagy. 1998. Embryonic stem cells, creating transgenic animals. Methods Cell Biol. 57: 279-293.
49. Qian, S., P. Jiang, X.M. Guan, G. Singh, M.E. Trumbauer, H. Yu, H.Y. Chen, L.H. Van de Ploeg, and H. Zheng. 1998. Mutant human presenilin 1 protects presenilin 1 null mouse against embryonic lethality and elevates Abetal-42/43 expression. Neuron 20: 611-617.
50. Ray, W.J., M. Yao, P. Nowotny, J. Mumm, W. Zhang, J.Y. Wu, R. Kopan, and A.M. Goate. 1999. Evidence for a physical interaction between presenilin and Notch. Proc. Natl. Acad. Sci. 96: 3263-3268.
51. Rogaev, E.I., R. Sherrington, E.A. Rogaeva, G. Levesque, M. Ikeda, Y. Liang, H. Chi, C. Lin, K. Holman, T. Tsuda et al. 1995. Familial Alzheimer's disease in kindreds with missense mutations in a gene on chromosome 1 related to the Alzheimer's disease type 3 gene. Nature 376: 775-778.
52. Shen, J., R.T. Bronson, D.F. Chen, W. Xia, D.J. Selkoe, and S. Tonegawa. 1997. Skeletal and CNS defects in Presenilin-1-deficient mice. Cell 89: 629-639.
53. Sherrington, R., E.I. Rogaev, Y. Liang, E.A. Rogaeva, G. Levesque, M. Ikeda, H. Chi, C. Lin, G. Li, K. Holman et al. 1995. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375: 754-760.
54. Smine, A., X. Xu, K. Nishiyama, T. Katada, P. Gambetti, S.P. Yadav, X. Wu, Y.C. Shi, S. Yasuhara, V. Homburger, and T. Okamoto. 1998. Regulation of brain G-protein go by Alzheimer's disease gene presenilin-1. J. Biol. Chem. 273: 16281-16288.
55. Stabler, S.M., L.L. Ostrowski, S.M. Janicki, and M.J. Monteiro. 1999. A myristoylated calcium-binding protein that preferentially interacts with the Alzheimer's disease presenilin 2 protein. J. Cell. Biol. 145: 1277-1292.
56. Struhl, G. and I. Greenwald. 1999. Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398: 522-525.
57. Takashima, A., M. Murayama, O. Murayama, T. Kohno, T. Honda, K. Yasutake, N. Nihonmatsu, M. Mercken, H. Yamaguchi, S. Sugihara, and B. Wolozin. 1998. Presenilin 1 associates with glycogen synthase kinase-3beta and its substrate tau. Proc. Natl. Acad. Sci. 95: 9637-9641.
58. Tamura, K., Y. Taniguchi, S. Minoguchi, T. Sakai, T. Tun, T. Furukawa, and T. Honjo. 1995. Physical interaction between a novel domain of the receptor Notch and the transcription factor RBP-J kappa/Su(H). Curr. Biol. 5: 1416-1423.
59. Thinakaran, G., D.R. Borchelt, M.K. Lee, H.H. Slunt, L. Spitzer, G. Kim, T. Ratovitsky, F. Davenport, C. Nordstedt, M. Seeger et al. 1996. Endoproteolysis of presenilin 1 and accumulation of processed derivatives in vivo. Neuron 17: 181-190.
60. Walter, J., A. Capell, J. Grunberg, B. Pesold, A. Schindzielorz, R. Prior, M.B. Podlisny, P. Fraser, P.S. Hyslop, D.J. Selkoe, and C. Haass. 1996. The Alzheimer's disease-associated presenilins are differentially phosphorylated proteins located predominantly within the endoplasmic reticulum. Mol. Med. 2: 673-691.
61. Weidemann, A., K. Paliga, U. Durrwang, C. Czech, G. Evin, C.L. Masters, and K. Beyreuther. 1997. Formation of stable complexes between two Alzheimer's disease gene products: presenilin-2 and beta-amyloid precursor protein. Nat. Med. 3: 328-332.
62. Westlund, B., D. Parry, R. Clover, M. Basson, and C.D. Johnson. 1999. Reverse genetic analysis of Caenorhabditis elegans presenilins reveals redundant but unequal roles for sel-12 and hop-1 in Notch-pathway signaling. Proc. Natl. Acad. Sci. 96: 2497-2502.
63. Wolfe, M.S., W. Xia, B.L. Ostaszewski, T.S. Diehl, W.T. Kimberly, and D.J. Selkoe. 1999. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398: 513-517.
64. Wong, P.C., H. Zheng, H. Chen, M.W. Becher, D.J. Sirinathsinghji, M.E. Trumbauer, H.Y. Chen, D.L. Price, L.H. Van der Ploeg, and S.S. Sisodia. 1997. Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm. Nature 387: 288-292.
65. Xia, W., J. Zhang, R. Perez, E.H. Koo, and D.J. Selkoe. 1997. Interaction between amyloid precursor protein and presenilins in mammalian cells: Implications for the pathogenesis of Alzheimer disease. Proc. Natl. Acad. Sci. 94: 8208-8213.
66. Ye, Y., N. Lukinova, and M.E. Fortini. 1999. Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature 398: 525-529.
67. Yu, G., F. Chen, G. Levesque, M. Nishimura, D.M. Zhang, L. Levesque, E. Rogaeva, D. Xu, Y. Liang, M. Duthie, P.H. St George-Hyslop, and P.E. Fraser. 1998. The presenilin 1 protein is a component of a high molecular weight intracellular complex that contains beta-catenin. J. Biol. Chem. 273: 16470-16475.
68. Zhang, N. and T. Gridley. 1998. Defects in somite formation in lunatic fringe-deficient mice. Nature 394: 374-377.
69. Zhang, W., S.W. Han, D.W. McKeel, A. Goate, and J.Y. Wu. 1998a. Interaction of presenilins with the filamin family of actin-binding proteins. J. Neurosci. 18: 914-922.
70. Zhang, Z., H. Hartmann, V.M. Do, D. Abramowski, C. Sturchler-Pierrat, M. Staufenbiel, B. Sommer, M. van de Wetering, H. Clevers, P. Saftig, B. De Strooper, X. He, and B.A. Yankner. 1998b. Destabilization of beta-catenin by mutations in presenilin-1 potentiates neuronal apoptosis. Nature 395: 698-702.
71. Zhou, J., U. Liyanage, M. Medina, C. Ho, A.D. Simmons, M. Lovett, and K.S. Kosik. 1997. Presenilin 1 interaction in the brain with a novel member of the Armadillo family. Neuroreport 8: 2085-2090.