Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: Revisited

Journal of Neuroscience

Volumn 25, Issue 9, 2005, Pages 2386-2395

  Lazarov, Orly ^a   Morfini, Gerardo A ^b   Lee, Edward B ^c   Farah, Mohamed H ^d   Szodorai, Anita ^e   DeBoer, Scott R ^b   Koliatsos, Vassilis E ^d   Kins, Stefan ^e   Lee, Virginia M Y ^c   Wong, Philip C ^d   Price, Donald L ^d   Brady, Scott T ^b   Sisodia, Sangram S ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Alzheimer's disease; APP; Axonal transport; Kinesin 1; Presenilin; Proteolysis

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; GAMMA SECRETASE; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEIN; KINESIN; MEMBRANE PROTEIN; PRESENILIN 1; PRESENILIN 2; PROTEIN TYROSINE KINASE; TYROSINE KINASE RECEPTOR;

ANIMAL TISSUE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME BINDING; FRACTIONATION; HETEROZYGOSITY; HOMOZYGOSITY; IMMUNOPRECIPITATION; MEMBRANE VESICLE; MOUSE; NERVE FIBER TRANSPORT; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN ISOLATION; REVIEW; SCIATIC NERVE; TRANSGENIC MOUSE;

AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ENDOPEPTIDASES; AXONS; BLOTTING, WESTERN; BRAIN; CLONING, MOLECULAR; ENDOPEPTIDASES; GENE EXPRESSION; GLUTATHIONE TRANSFERASE; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KINESIN; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PRESENILIN-1; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; RECEPTOR PROTEIN-TYROSINE KINASES; RECOMBINANT FUSION PROTEINS; SCIATIC NERVE; SCIATIC NEUROPATHY;

EID: 20044396527     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3089-04.2005     Document Type: Review

References (48)

1. Borchelt DR, Thinakaran G, Eckman CB, Lee MK, Davenport F, Ratovitsky T, Prada CM, Kim G, Seekins S, Yager D, Slunt HH, Wang R, Seeger M, Levey AI, Gandy SE, Copeland NG, Jenkins NA, Price DL, Younkin SG, Sisodia SS (1996) Familial Alzheimer's disease-linked presenilin 1 variants elevate Aβ1-42/1-40 ratio in vitro and in vivo. Neuron 17:1005-1013.
2. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, Copeland NG, Price DL, Sisodia SS (1997) Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 19:939-945.
3. Bowman AB, Kamal A, Ritchings BW, Philp AV, McGrail M, Gindhart JG, Goldstein LS (2000) Kinesin-dependent axonal transport is mediated by the Sunday Driver (SYD) protein. Cell 103:583-594.
4. Brady ST, Pfister KK, Bloom GS (1990) A monoclonal antibody against kinesin inhibits both anterograde and retrograde fast axonal transport in squid axoplasm. Proc Natl Acad Sci USA 87:1061-1065.
5. Buxbaum JD, Thinakaran G, Koliatsos V, O'Callahan J, Slunt HH, Price DL, Sisodia SS (1998) Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J Neurosci 18:9629-9637.
6. Cai H, Wang Y, McCarthy D, Wen H, Borchelt DR, Price DL, Wong PC (2001) BACE1 is the major β-secretase for generation of Aβ peptides by neurons. Nat Neurosci 4:233-234.
7. De Strooper B (2003) APH-1, PEN-2, and nicastrin with presenilin generate an active γ-secretase complex. Neuron 38:9-12.
8. Elluru RG, Bloom GS, Brady ST (1995) Fast axonal transport of kinesin in the rat visual system: functionality of kinesin heavy chain isoforms. Mol Biol Cell 6:21-40.
9. Haass C, Lemere CA, Capell A, Citron M, Seubert P, Schenk D, Lannfelt L, Selkoe DJ (1995) The Swedish mutation causes early-onset Alzheimer's disease by β-secretase cleavage within the secretory pathway. Nat Med 1:1291-1296.
10. Hilbich C, Monning U, Grund C, Masters CL, Beyreuther K (1993) Amyloid-like properties of peptides flanking the epitope of amyloid precursor protein-specific monoclonal antibody 22C11. J Biol Chem 268:26571-26577.
11. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
12. Kaether C, Skehel P, Dotti CG (2000) Axonal membrane proteins are transported in distinct carriers: a two-color video microscopy study in cultured hippocampal neurons. Mol Biol Cell 11:1213-1224.
13. 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.
14. Kamal A, Almenar-Queralt A, LeBlanc JF, Roberts EA, Goldstein LS (2001) Kinesin-mediated axonal transport of a membrane compartment containing β-secretase and presenilin-1 requires APP. Nature 414:643-648.
15. Kanai Y, Okada Y, Tanaka Y, Harada A, Terada S, Hirokawa N (2000) KIF5C, a novel neuronal kinesin enriched in motor neurons. J Neurosci 20:6374-6384.
16. Kesavapany S, Banner SJ, Lau KF, Shaw CE, Miller CC, Cooper JD, McLoughlin DM (2002) Expression of the Fe65 adapter protein in adult and developing mouse brain. Neuroscience 115:951-960.
17. Kim SH, Lah JJ, Thinakaran G, Levey A, Sisodia SS (2000) Subcellular localization of presenilins: association with a unique membrane pool in cultured cells. Neurobiol Dis 7:99-117.
18. Kim SH, Leem JY, Lah JJ, Slunt HH, Levey AI, Thinakaran G, Sisodia SS (2001) Multiple effects of aspartate mutant presenilin 1 on the processing and trafficking of amyloid precursor protein. J Biol Chem 276: 43343-43350.
19. 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.
20. Lamb BT, Bardel KA, Kulnane LS, Anderson JJ, Holtz G, Wagner SL, Sisodia SS, Hoeger EJ (1999) Amyloid production and deposition in mutant amyloid precursor protein and presenilin-1 yeast artificial chromosome transgenic mice. Nat Neurosci 2:695-697.
21. Lazarov O, Lee M, Peterson DA, Sisodia SS (2002) Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 22:9785-9793.
22. Lee EB, Zhang B, Liu K, Greenbaum EA, Doms RW, Trojanowski JQ, Lee VM (2005) BACE overexpression alters the subcellular processing of APP and inhibits Aβ deposition in vivo. J Cell Biol 168:291-302.
23. Lee MK, Borchelt DR, Kim G, Thinakaran G, Slunt HH, Ratovitski T, Martin LJ, Kittur A, Gandy S, Levey AI, Jenkins N, Copeland N, Price DL, Sisodia SS (1997) Hyperaccumulation of FAD-linked presenilin 1 variants in vivo. Nat Med 3:756-760.
24. Leopold PL, McDowall AW, Pfister KK, Bloom GS, Brady ST (1992) Association of kinesin with characterized membrane-bounded organelles. Cell Motil Cytoskeleton 23:19-33.
25. Li JY, Pfister KK, Brady S, Dahlstrom A (1999) Axonal transport and distribution of immunologically distinct kinesin heavy chains in rat neurons. J Neurosci Res 58:226-241.
26. Marcinkiewicz M, Seidah NG (2000) Coordinated expression of β-amyloid precursor protein and the putative β-secretase BACE and α-secretase ADAM10 in mouse and human brain. J Neurochem 75:2133-2143.
27. Matsuda S, Yasukawa T, Homma Y, Ito Y, Niikura T, Hiraki T, Hirai S, Ohno S, Kita Y, Kawasumi M, Kouyama K, Yamamoto T, Kyriakis JM, Nishimoto I (2001) c-Jun N-terminal kinase (JNK)-interacting protein-1b/ islet-brain-1 scaffolds Alzheimer's amyloid precursor protein with JNK. J Neurosci 21:6597-6607.
28. Morfini G, Tsai MY, Szebenyi G, Brady ST (2001) Approaches to study interactions between kinesin motors and membranes. Methods Mol Biol 164:147-162.
29. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST (2002) Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J 21:281-293.
30. Papp H, Pakaski M, Kasa P (2002) Presenilin-1 and the amyloid precursor protein are transported bidirectionally in the sciatic nerve of adult rat. Neurochem Int 41:429-435.
31. Pfister KK, Wagner MC, Stenoien DL, Brady ST, Bloom GS (1989) Monoclonal antibodies to kinesin heavy and light chains stain vesicle-like structures, but not microtubules, in cultured cells. J Cell Biol 108:1453-1463.
32. Price DL, Sisodia SS (1998) Mutant genes in familial Alzheimer's disease and transgenic models. Annu Rev Neurosci 21:479-505.
33. Rahman A, Kamal A, Roberts EA, Goldstein LS (1999) Defective kinesin heavy chain behavior in mouse kinesin light chain mutants. J Cell Biol 146:1277-1288.
34. Selkoe DJ (2001) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81:741-766.
35. Sheng JG, Price DL, Koliatsos VE (2002) Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Aβ amyloidosis. J Neurosci 22:9794-9799.
36. Shi XP, Tugusheva K, Bruce JE, Lucka A, Wu GX, Chen-Dodson E, Price E, Li Y, Xu M, Huang Q, Sardana MK, Hazuda DJ (2003) β-secretase cleavage at amino acid residue 34 in the amyloid β peptide is dependent upon γ-secretase activity. J Biol Chem 278:21286-21294.
37. 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.
38. Stenoien DL, Brady ST (1997) Immunochemical analysis of kinesin light chain function. Mol Biol Cell 8:675-689.
39. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N (1998) Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93:1147-1158.
40. Thinakaran G, Teplow DB, Siman R, Greenberg B, Sisodia SS (1996) Metabolism of the "Swedish" amyloid precursor protein variant in neuro2a (N2a) cells. Evidence that cleavage at the "β-secretase" site occurs in the Golgi apparatus. J Biol Chem 271:9390-9397.
41. Thinakaran G, Harris CL, Ratovitski T, Davenport F, Slunt HH, Price DL, Borchelt DR, Sisodia SS (1997) Evidence that levels of presenilins (PS1 and PS2) are coordinately regulated by competition for limiting cellular factors. J Biol Chem 272:28415-28422.
42. Tsai MY, Morfini G, Szebenyi G, Brady ST (2000) Release of kinesin from vesicles by hsc70 and regulation of fast axonal transport. Mol Biol Cell 11:2161-2173.
43. Tu PH, Elder G, Lazzarini RA, Nelson D, Trojanowski JQ, Lee VM (1995) Overexpression of the human NFM subunit in transgenic mice modifies the level of endogenous NFL and the phosphorylation state of NFH subunits. J Cell Biol 129:1629-1640.
44. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, Rapoport TA, Margolis B (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J Cell Biol 152:959-970.
45. Ward BM, Moss B (2004) Vaccinia virus A36R membrane protein provides a direct link between intracellular enveloped virions and the microtubule motor kinesin. J Virol 78:2486-2493.
46. Weidemann A, Konig G, Bunke D, Fischer P, Salbaum JM, Masters CL, Beyreuther K (1989) Identification, biogenesis, and localization of precursors of Alzheimer's disease A4 amyloid protein. Cell 57:115-126.
47. Wisniewski TP, Tanzi CL, Gindhart JG (2003) The Drosophila kinesin-I associated protein YETI binds both kinesin subunits. Biol Cell 95:595-602.
48. Zheng H, Jiang M, Trumbauer ME, Sirinathsinghji DJ, Hopkins R, Smith DW, Heavens RP, Dawson GR, Boyce S, Conner MW, Stevens KA, Slunt HH, Sisodia SS, Chen HY, Van der Ploeg LH (1995) β-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell 81:525-531.