Decreasing the expression of PICALM reduces endocytosis and the activity of β-secretase: Implications for Alzheimer's disease

BMC Neuroscience

Volumn 17, Issue 1, 2016, Pages

  Thomas, Rhian S ^a   Henson, Alex ^a   Gerrish, Amy ^b,c   Jones, Lesley ^b   Williams, Julie ^b   Kidd, Emma J ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^c BIRMINGHAM CHILDREN S HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid precursor protein; Clathrin mediated endocytosis; PICALM; C terminal fragment; Secretase

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; MEMBRANE PROTEIN; PHOSPHATIDYLINOSITOL BINDING CLATHRIN ASSEMBLY PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; APP PROTEIN, HUMAN; CLATHRIN ASSEMBLY PROTEIN; CLATHRIN HEAVY CHAIN; ISOPROTEIN; MESSENGER RNA; PEPTIDE FRAGMENT; PICALM PROTEIN, HUMAN; SECRETASE; SMALL INTERFERING RNA;

ALZHEIMER DISEASE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN SECRETION; SINGLE NUCLEOTIDE POLYMORPHISM; WESTERN BLOTTING; BRAIN; DEFICIENCY; FLOW CYTOMETRY; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; BLOTTING, WESTERN; BRAIN; CELL LINE, TUMOR; CLATHRIN HEAVY CHAINS; ENDOCYTOSIS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOHISTOCHEMISTRY; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; PEPTIDE FRAGMENTS; PROTEIN ISOFORMS; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSFERRIN;

EID: 84978726671     PISSN: None     EISSN: 14712202     Source Type: Journal    
DOI: 10.1186/s12868-016-0288-1     Document Type: Article

References (59)

1. Lambert JC, Heath S, Even G, Campion D, Sleegers K, Hiltunen M, Combarros O, Zelenika D, Bullido MJ, Tavernier B, et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet. 2009;41:1094-9.
2. Harold D, Abraham R, Hollingworth P, Sims R, Gerrish A, Hamshere ML, Pahwa JS, Moskvina V, Dowzell K, Williams A, et al. Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nat Genet. 2009;41:1088-93.
3. Jones L, Lambert JC, Wang L-S, Choi SH, Harold D, Vedernikov A, Escott-Price V. Convergent genetic and expression data implicate immunity in Alzheimer's disease. Alzheimer's Dement. 2015;11:658-71.
4. Lambert JC, Ibrahim-Verbaas CA, Harold D, Naj AC, Sims R, Bellenguez C, DeStafano AL, Bis JC, Beecham GW, Grenier-Boley B, et al. Meta-analysis of 74,046 individuals identifies 11 new susceptibility loci for Alzheimer's disease. Nat Genet. 2013;45:1452-8.
5. Seshadri S, Fitzpatrick AL, Ikram MA, DeStefano AL, Gudnason V, Boada M, Bis JC, Smith AV, Carassquillo MM, Lambert JC, et al. Genome-wide analysis of genetic loci associated with Alzheimer disease. JAMA J Am Med Assoc. 2010;303:1832-40.
6. Hardy J, Allsop D. Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci. 1991;12:383-8.
7. Koo EH, Squazzo SL, Selkoe DJ, Koo CH. Trafficking of cell-surface amyloid beta-protein precursor. I. Secretion, endocytosis and recycling as detected by labeled monoclonal antibody. J Cell Sci. 1996;109:991-8.
8. Yamazaki T, Koo EH, Selkoe DJ. Trafficking of cell-surface amyloid beta-protein precursor. II. Endocytosis, recycling and lysosomal targeting detected by immunolocalization. J Cell Sci. 1996;109:999-1008.
9. Sinha S, Anderson JP, Barbour R, Basi GS, Caccavello R, Davis D, Doan M, Dovey HF, Frigon N, Hong J, et al. Purification and cloning of amyloid precursor protein beta-secretase from human brain. Nature. 1999;402:537-40.
10. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science. 1999;286:735-41.
11. Yan R, Bienkowski MJ, Shuck ME, Miao H, Tory MC, Pauley AM, Brashier JR, Stratman NC, Mathews WR, Buhl AE, et al. Membrane-anchored aspartyl protease with Alzheimer's disease beta-secretase activity. Nature. 1999;402:533-7.
12. Citron M. Strategies for disease modification in Alzheimer's disease. Nat Rev Neurosci. 2004;5:677-85.
13. Edbauer D, Winkler E, Regula JT, Pesold B, Steiner H, Haass C. Reconstitution of gamma-secretase activity. Nat Cell Biol. 2003;5:486-8.
14. Kimberly WT, LaVoie MJ, Ostaszewski BL, Ye W, Wolfe MS, Selkoe DJ. Gamma-secretase is a membrane protein complex comprised of presenilin, nicastrin, Aph-1, and Pen-2. Proc Natl Acad Sci USA. 2003;100:6382-7.
15. Takasugi N, Tomita T, Hayashi I, Tsuruoka M, Niimura M, Takahashi Y, Thinakaran G, Iwatsubo T. The role of presenilin cofactors in the gamma-secretase complex. Nature. 2003;422:438-41.
16. Allinson TM, Parkin ET, Turner AJ, Hooper NM. ADAMs family members as amyloid precursor protein alpha-secretases. J Neurosci Res. 2003;74:342-52.
17. Asai M, Hattori C, Szabo B, Sasagawa N, Maruyama K, Tanuma S, Ishiura S. Putative function of ADAM9, ADAM10, and ADAM17 as APP alpha-secretase. Biochem Biophys Res Commun. 2003;301:231-5.
18. Grbovic OM, Mathews PM, Jiang Y, Schmidt SD, Dinakar R, Summers-Terio NB, Ceresa BP, Nixon RA, Cataldo AM. Rab5-stimulated up-regulation of the endocytic pathway increases intracellular beta-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Abeta production. J Biol Chem. 2003;278:31261-8.
19. Thomas RS, Lelos MJ, Good MA, Kidd EJ. Clathrin-mediated endocytic proteins are upregulated in the cortex of the Tg2576 mouse model of Alzheimer's disease-like amyloid pathology. Biochem Biophys Res Commun. 2011;415:656-61.
20. Cataldo AM, Barnett JL, Pieroni C, Nixon RA. Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: neuropathologic evidence for a mechanism of increased beta-amyloidogenesis. J Neurosci. 1997;17:6142-51.
21. Cataldo AM, Peterhoff CM, Troncoso JC, Gomez-Isla T, Hyman BT, Nixon RA. Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am J Pathol. 2000;157:277-86.
22. Carey RM, Balcz BA, Lopez-Coviella I, Slack BE. Inhibition of dynamin-dependent endocytosis increases shedding of the amyloid precursor protein ectodomain and reduces generation of amyloid beta protein. BMC Cell Biol. 2005;6:30.
23. Cirrito JR, Kang JE, Lee J, Stewart FR, Verges DK, Silverio LM, Bu G, Mennerick S, Holtzman DM. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron. 2008;58:42-51.
24. Meyerholz A, Hinrichsen L, Groos S, Esk PC, Brandes G, Ungewickell EJ. Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic. 2005;6:1225-34.
25. Barral S, Bird T, Goate A, Farlow MR, Diaz-Arrastia R, Bennett DA, Graff-Radford N, Boeve BF, Sweet RA, Stern Y, et al. Genotype patterns at PICALM, CR1, BIN1, CLU, and APOE genes are associated with episodic memory. Neurology. 2012;78:1464-71.
26. D'Angelo F, Vignaud H, Di Martino J, Salin B, Devin A, Cullin C, Marchal C. A yeast model for amyloid-beta aggregation exemplifies the role of membrane trafficking and PICALM in cytotoxicity. Dis Models Mech. 2013;6:206-16.
27. Parikh I, Fardo DW, Estus S. Genetics of PICALM expression and Alzheimer's disease. PLoS One. 2014;9:e91242.
28. Kok EH, Luoto T, Haikonen S, Goebeler S, Haapasalo H, Karhunen PJ. CLU, CR1 and PICALM genes associate with Alzheimer's-related senile plaques. Alzheimers Res Ther. 2011;3:12.
29. Ando K, Brion JP, Stygelbout V, Suain V, Authelet M, Dedecker R, Chanut A, Lacor P, Lavaur J, Sazdovitch V, et al. Clathrin adaptor CALM/PICALM is associated with neurofibrillary tangles and is cleaved in Alzheimer's brains. Acta Neuropathol. 2013;125:861-78.
30. NCBI reference sequence database. http://www.ncbi.nlm.nih.gov/refseq/. Accessed 5 Oct 15.
31. Gibbs JR, van der Brug MP, Hernandez DG, Traynor BJ, Nalls MA, Lai SL, Arepalli S, Dillman A, Rafferty IP, Troncoso J, et al. Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet. 2010;6:e1000952.
32. Trabzuni D, Ryten M, Walker R, Smith C, Imran S, Ramasamy A, Weale ME, Hardy J. Quality control parameters on a large dataset of regionally dissected human control brains for whole genome expression studies. J Neurochem. 2011;119:275-82.
33. Dreyling MH, Martinez-Climent JA, Zheng M, Mao J, Rowley JD, Bohlander SK. The t(10;11)(p13;q14) in the U937 cell line results in the fusion of the AF10 gene and CALM, encoding a new member of the AP-3 clathrin assembly protein family. Proc Natl Acad Sci USA. 1996;93:4804-9.
34. Jones L, Harold D, Williams J. Genetic evidence for the involvement of lipid metabolism in Alzheimer's disease. Biochim Biophys Acta. 2010;1801:754-61.
35. Tebar F, Bohlander SK, Sorkin A. Clathrin assembly lymphoid myeloid leukemia (CALM) protein: localization in endocytic-coated pits, interactions with clathrin, and the impact of overexpression on clathrin-mediated traffic. Mol Biol Cell. 1999;10:2687-702.
36. Baig S, Joseph SA, Tayler H, Abraham R, Owen MJ, Williams J, Kehoe PG, Love S. Distribution and expression of picalm in Alzheimer disease. J Neuropathol Exp Neurol. 2010;69:1071-7.
37. Huang F, Khvorova A, Marshall W, Sorkin A. Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem. 2004;279:16657-61.
38. Scotland PB, Heath JL, Conway AE, Porter NB, Armstrong MB, Walker JA, Klebig ML, Lavau CP, Wechsler DS. The PICALM protein plays a key role in iron homeostasis and cell proliferation. PLoS One. 2012;7:e44252.
39. Kanatsu K, Morohashi Y, Suzuki M, Kuroda H, Watanabe T, Tomita T, Iwatsubo T. Decreased CALM expression reduces Abeta42 to total Abeta ratio through clathrin-mediated endocytosis of gamma-secretase. Nat Commun. 2014;5:3386.
40. Harel A, Wu F, Mattson MP, Morris CM, Yao PJ. Evidence for CALM in directing VAMP2 trafficking. Traffic. 2008;9:417-29.
41. Xiao Q, Gil SC, Yan P, Wang Y, Han S, Gonzales E, Perez R, Cirrito JR, Lee JM. Role of phosphatidylinositol clathrin assembly lymphoid-myeloid leukemia (PICALM) in intracellular amyloid precursor protein (APP) processing and amyloid plaque pathogenesis. J Biol Chem. 2012;287:21279-89.
42. Lu L, Hong WJ. From endosomes to the trans-Golgi network. Semin Cell Dev Biol. 2014;31:30-9.
43. Miller SE, Sahlender DA, Graham SC, Honing S, Robinson MS, Peden AA, Owen DJ. The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell. 2011;147:1118-31.
44. Al Soraj M, He L, Peynshaert K, Cousaert J, Vercauteren D, Braeckmans K, De Smedt SC, Jones AT. siRNA and pharmacological inhibition of endocytic pathways to characterize the differential role of macropinocytosis and the actin cytoskeleton on cellular uptake of dextran and cationic cell penetrating peptides octaarginine (R8) and HIV-Tat. J Controll Release. 2012;161:132-41.
45. Koo EH, Squazzo SL. Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J Biol Chem. 1994;269:17386-9.
46. Vecchi M, Polo S, Poupon V, van de Loo JW, Benmerah A, Di Fiore PP. Nucleocytoplasmic shuttling of endocytic proteins. J Cell Biol. 2001;153:1511-7.
47. Mercer JL, Argus JP, Crabtree DM, Keenan MM, Wilks MQ, Chi J-TA, Bensinger SJ, Lavau CP, Wechsler DS. Modulation of PICALM levels perturbs cellular cholesterol homeostasis. PLoS One. 2015;10:e0129776.
48. Tian Y, Chang JC, Fan EY, Flajolet M, Greengard P. Adaptor complex AP2/PICALM, through interaction with LC3, targets Alzheimer's APP-CTF for terminal degradation via autophagy. Proc Natl Acad Sci USA. 2013;110:17071-6.
49. Bali J, Gheinani AH, Zurbriggen S, Rajendran L. Role of genes linked to sporadic Alzheimer's disease risk in the production of beta-amyloid peptides. Proc Natl Acad Sci USA. 2012;109:15307-11.
50. Wu F, Matsuoka Y, Mattson MP, Yao PJ. The clathrin assembly protein AP180 regulates the generation of amyloid-beta peptide. Biochem Biophys Res Commun. 2009;385:247-50.
51. Jiang Y, Mullaney KA, Peterhoff CM, Che S, Schmidt SD, Boyer-Boiteau A, Ginsberg SD, Cataldo AM, Mathews PM, Nixon RA. Alzheimer's-related endosome dysfunction in Down syndrome is Abeta-independent but requires APP and is reversed by BACE-1 inhibition. Proc Natl Acad Sci USA. 2010;107:1630-5.
52. Kim S, Sato Y, Mohan PS, Peterhoff C, Pensalfini A, Rigoglioso A, Jiang Y, Nixon RA. Evidence that the rab5 effector APPL1 mediates APP-betaCTF-induced dysfunction of endosomes in Down syndrome and Alzheimer's disease. Mol Psychiatry. 2015;. doi: 10.1038/mp.2015.97.
53. Ihara Y, Morishima-Kawashima M, Nixon R. The ubiquitin-proteasome system and the autophagic-lysosomal system in Alzheimer disease. Cold Spring Harbour Perspect Med. 2012;2:a006361.
54. Laird FM, Cai HB, Savonenko AV, Farah MH, He KW, Melnikova T, Wen HJ, Chiang HC, Xu GL, Koliatsos VE, et al. BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J Neurosci. 2005;25:11693-709.
55. McConlogue L, Buttini M, Anderson JP, Brigham EF, Chen KS, Freedman SB, Games D, Johnson-Wood K, Lee M, Zeller M, et al. Partial reduction of BACE1 has dramatic effects on Alzheimer plaque and synaptic pathology in APP transgenic mice. J Biol Chem. 2007;282:26326-34.
56. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402-8.
57. Thomas RS, Liddell JE, Murphy LS, Pache DM, Kidd EJ. An antibody to the beta-secretase cleavage site on amyloid-beta-protein precursor inhibits amyloid-beta production. J Alzheimers Dis. 2006;10:379-90.
58. Thomas RS, Liddell JE, Kidd EJ. Anti-amyloid precursor protein immunoglobulins inhibit amyloid-beta production by steric hindrance. FEBS J. 2011;278:167-78.
59. Thomas RS, Hvoslef-Eide M, Good MA, Kidd EJ. Inhibition of amyloid-beta production by anti-amyloid precursor protein antibodies in primary mouse cortical neurones. NeuroReport. 2013;24:1058-61.