Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-like protein 2

Journal of Neuroscience

Volumn 25, Issue 5, 2005, Pages 1219-1225

  Wang, Pei ^a,f   Yang, Guang ^b   Mosier, Dennis R ^a,c   Chang, Paul ^d   Zaidi, Tahire ^a   Gong, Yan Dao ^b   Zhao, Nan Ming ^b   Dominguez, Bertha ^e   Lee, Kuo Fen ^e   Gan, Wen Biao ^d   Zheng, Hui ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TSINGHUA UNIVERSITY   (China)

^c MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Knock out mice; Neuromuscular junction; Synaptic transmission; Synaptic vesicles

Indexed keywords

AMYLOID PRECURSOR PROTEIN; AMYLOID PRECURSOR PROTEIN LIKE PROTEIN 2; BIOLOGICAL MARKER; CHOLINERGIC RECEPTOR; NEUROTRANSMITTER; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; EMBRYO; INCIDENCE; MOUSE; NERVE ENDING; NERVE SPROUTING; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; SYNAPSE VESICLE;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; DIAPHRAGM; MICE; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; MOTOR ENDPLATE; MUSCLE PROTEINS; NECK MUSCLES; NEUROMUSCULAR JUNCTION; PHENOTYPE; RECEPTORS, CHOLINERGIC; RECEPTORS, PRESYNAPTIC; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 13944274830     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4660-04.2005     Document Type: Article

References (40)

1. Akaaboune M, Allinquant B, Farza H, Roy K, Magoul R, Fiszman M, Festoff BW, Hantai D (2000) Developmental regulation of amyloid precursor protein at the neuromuscular junction in mouse skeletal muscle. Mol Cell Neurosci 15:355-367.
2. Brandon EP, Lin W, D'Amour KA, Pizzo DP, Dominguez B, Sugiura Y, Thode S, Ko CP, Thal LJ, Gage FH, Lee KF (2003) Aberrant patterning of neuromuscular synapses in choline acetyltransferase-deficient mice. J Neurosci 23:539-549.
3. Cao X, Sudhof TC (2001) A transcriptionally [correction of transcriptively] active complex of APP with Fe65 and histone acetyltransferase Tip60. Science 293:115-120.
4. Daigle I, Li C (1993) apl-1, a Caenorhabditis elegans gene encoding a protein related to the human beta-amyloid protein precursor. Proc Natl Acad Sci USA 90:12045-12049.
5. Dawson GR, Seabrook GR, Zheng H, Smith DW, Graham S, O'Dowd G, Bowery BJ, Boyce S, Trumbauer ME, Chen HY, Van der Ploeg LH, Sirinathsinghji DJ (1999) Age-related cognitive deficits, impaired long-term potentiation and reduction in synaptic marker density in mice lacking the beta-amyloid precursor protein [In Process Citation]. Neuroscience 90:1-13.
6. De Strooper B (2003) Aph-1, Pen-2, and nicastrin with presenilin generate an active gamma-secretase complex. Neuron 38:9-12.
7. Donoviel DB, Hadjantonakis AK, Ikeda M, Zheng H, Hyslop PS, Bernstein A (1999) Mice lacking both presenilin genes exhibit early embryonic patterning defects [In Process Citation]. Genes Dev 13:2801-2810.
8. Gunawardena S, Goldstein LS (2001) Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32:389-401.
9. Heber S, Herms J, Gajic V, Hainfellner J, Aguzzi A, Rulicke T, von Kretzschmar H, von Koch C, Sisodia S, Tremml P, Lipp HP, Wolfer DP, Muller U (2000) Mice with combined gene knock-outs reveal essential and partially redundant functions of amyloid precursor protein family members. J Neurosci 20:7951-7963.
10. Herreman A, Hartmann D, Annaert W, Saftig P, Craessaerts K, Serneels L, Umans L, Schrijvers V, Checler F, Vanderstichele H, Baekelandt V, Dressel R, Cupers P, Huylebroeck D, Zwijsen A, Van Leuven F, De Strooper B (1999) Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency [In Process Citation]. Proc Natl Acad Sci USA 96:11872-11877.
11. Jin LW, Ninomiya H, Roch JM, Schubert D, Masliah E, Otero DA, Saitoh T (1994) Peptides containing the RERMS sequence of amyloid beta/A4 protein precursor bind cell surface and promote neurite extension. J Neurosci 14:5461-5470.
12. Kamal A, Stokin GB, Yang Z, Xia CH, Goldstein LS (2000) Axonal transport of amyloid precursor protein is mediated by direct binding to the kinesin light chain subunit of kinesin-I. Neuron 28:449-459.
13. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing beta-secretase and presenilin-1 requires APP. Nature 414:643-648.
14. Kirazov E, Kirazov L, Bigl V, Schliebs R (2001) Ontogenetic changes in protein level of amyloid precursor protein (APP) in growth cones and synaptosomes from rat brain and prenatal expression pattern of APP mRNA isoforms in developing rat embryo. Int J Dev Neurosci 19:287-296.
15. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, Beyreuther K, Fischer P, Masters CL, Price DL (1990) Precursor of amyloid protein in Alzheimer disease undergoes fast anterograde axonal transport. Proc Natl Acad Sci USA 87:1561-1565.
16. Lin W, Burgess RW, Dominguez B, Pfaff SL, Sanes JR, Lee KF (2001) Distinct roles of nerve and muscle in postsynaptic differentiation of the neuromuscular synapse. Nature 410:1057-1064.
17. Masliah E, Terry R (1993) The role of synaptic proteins in the pathogenesis of disorders of the central nervous system. Brain Pathol 3:77-85.
18. Misgeld T, Burgess RW, Lewis RM, Cunningham JM, Lichtman JW, Sanes JR (2002) Roles of neurotransmitter in synapse formation: development of neuromuscular junctions lacking choline acetyltransferase. Neuron 36:635-648.
19. Moya KL, Benowitz LI, Schneider GE, Allinquant B (1994) The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol 161:597-603.
20. Ohsawa I, Takamura C, Morimoto T, Ishiguro M, Kohsaka S (1999) Amino-terminal region of secreted form of amyloid precursor protein stimulates proliferation of neural stem cells. Eur J Neurosci 11:1907-1913.
21. Phinney AL, Calhoun ME, Wolfer DP, Lipp HP, Zheng H, Jucker M (1999) Aged APP-null mice exhibit a learning impairment which is not mediated by a loss of hippocampal neuron or synaptic bouton number. Neuroscience 90:1207-1216.
22. Rosen DR, Martin-Morris L, Luo LQ, White K (1989) A Orosophila gene encoding a protein resembling the human beta-amyloid protein precursor. Proc Natl Acad Sci USA 86:2478-2482.
23. Rossjohn J, Cappai R, Feil SC, Henry A, McKinstry WJ, Galatis D, Hesse L, Multhaup G, Beyreuther K, Masters CL, Parker MW (1999) Crystal structure of the N-terminal, growth factor-like domain of Alzheimer amyloid precursor protein. Nat Struct Biol 6:327-331.
24. Sanes JR, Lichtman JW (1999) Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 22:389-442.
25. Schubert W, Prior R, Weidemann A, Dircksen H, Multhaup G, Masters CL, Beyreuther K (1991) Localization of Alzheimer beta A4 amyloid precursor protein at central and peripheral synaptic sites. Brain Res 563:184-194.
26. Seabrook GR, Smith DW, Bowery BJ, Easter A, Reynolds T, Fitzjohn SM, Morton RA, Zheng H, Dawson GR, Sirinathsinghji DJ, Davies CH, Collingridge GL, Hill RG (1999) Mechanisms contributing to the deficits in hippocampal synaptic plasticity in mice lacking amyloid precursor protein [In Process Citation]. Neuropharmacology 38:349-359.
27. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
28. Shigematsu K, McGeer PL, McGeer EG (1992) Localization of amyloid precursor protein in selective postsynaptic densities of rat cortical neurons. Brain Res 592:353-357.
29. Sisodia SS, Koo EH, Hoffman PN, Perry G, Price DL (1993) Identification and transport of full-length amyloid precursor proteins in rat peripheral nervous system. J Neurosci 13:3136-3142.
30. Slunt HH, Thinakaran G, Von Koch C, Lo AC, Tanzi RE, Sisodia SS (1994) Expression of a ubiquitous, cross-reactive homologue of the mouse beta-amyloid precursor protein (APP). J Biol Chem 269:2637-2644.
31. Tanzi RE, Gusella JF, Watkins PC, Bruns GA, St George-Hyslop P, Van Keuren ML, Patterson D, Pagan S, Kurnit DM, Neve RL (1987) Amyloid beta protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus. Science 235:880-884.
32. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R (1991) Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580.
33. Torroja L, Packard M, Gorczyca M, White K, Budnik V (1999) The Drosophila β-amyloid precursor protein homolog promotes synapse differentiation at the neuromuscular junction. J Neurosci 19:7793-7803.
34. 2+ channels. Proc Natl Acad Sci USA 100:3491-3496.
35. von Koch CS, Zheng H, Chen H, Trumbauer M, Thinakaran G, van der Ploeg LH, Price DL, Sisodia SS (1997) Generation of APLP2 KO mice and early postnatal lethality in APLP2/APP double KO mice. Neurobiol Aging 18:661-669.
36. Wasco W, Bupp K, Magendantz M, Gusella JF, Tanzi RE, Solomon F (1992) Identification of a mouse brain cDNA that encodes a protein related to the Alzheimer disease-associated amyloid beta protein precursor. Proc Natl Acad Sci USA 89:10758-10762.
37. Wasco W, Gurubhagavatula S, Paradis MD, Romano DM, Sisodia SS, Hyman BT, Neve RL, Tanzi RE (1993) Isolation and characterization of APLP2 encoding a homologue of the Alzheimer's associated amyloid beta protein precursor. Nat Genet 5:95-100.
38. Xia X, Wang P, Sun X, Soriano S, Shum WK, Yamaguchi H, Trumbauer ME, Takashima A, Koo EH, Zheng H (2002) The aspartate-257 of presenilin 1 is indispensable for mouse development and production of {beta}-amyloid peptides through {beta}-catenin-independent mechanisms. Proc Natl Acad Sci USA 99:8760-8765.
39. Yamazaki T, Selkoe DJ, Koo EH (1995) Trafficking of cell surface beta-amyloid precursor protein: retrograde and transcytotic transport in cultured neurons. J Cell Biol 129:431-442.
40. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJ, Hopkins R, Smith DW, Heavens RP, Dawson GR, Boyce S, Conner MW, et al. (1995) Beta-amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81:525-531.