Defective Transcytosis of APP and Lipoproteins in Human iPSC-Derived Neurons with Familial Alzheimer's Disease Mutations

Cell Reports

Volumn 17, Issue 3, 2016, Pages 759-773

  Woodruff, Grace ^a   Reyna, Sol M ^a   Dunlap, Mariah ^a   Van Der Kant, Rik ^a   Callender, Julia A ^a   Young, Jessica E ^a   Roberts, Elizabeth A ^a   Goldstein, Lawrence S B ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; APP; endocytosis; FAD; iPSC; PS1; transcytosis

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PRESENILIN 1; RAB11 PROTEIN; LRP1 PROTEIN, HUMAN; MESSENGER RNA; RAB PROTEIN; SECRETASE;

ALZHEIMER DISEASE; ARTICLE; AXON; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FAMILIAL ALZHEIMER DISEASE; FAMILIAL DISEASE; GENE MUTATION; HUMAN; HUMAN CELL; INDUCED PLURIPOTENT STEM CELL; NERVE CELL; PRIORITY JOURNAL; TRANSCYTOSIS; ANTAGONISTS AND INHIBITORS; GENETICS; METABOLISM; MUTATION; PATHOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; AXONS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; LIPOPROTEINS, LDL; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MUTATION; NEURONS; PRESENILIN-1; RAB GTP-BINDING PROTEINS; RNA, MESSENGER; TRANSCYTOSIS;

EID: 84992223540     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.09.034     Document Type: Article

References (64)

1. Alzheimer's Association. 2014 Alzheimer's disease facts and figures. Alzheimers Dement 10 (2014), e47–e92.
2. Anderson, E., Maday, S., Sfakianos, J., Hull, M., Winckler, B., Sheff, D., Fölsch, H., Mellman, I., Transcytosis of NgCAM in epithelial cells reflects differential signal recognition on the endocytic and secretory pathways. J. Cell Biol. 170 (2005), 595–605.
3. Ascaño, M., Richmond, A., Borden, P., Kuruvilla, R., Axonal targeting of Trk receptors via transcytosis regulates sensitivity to neurotrophin responses. J. Neurosci. 29 (2009), 11674–11685.
4. Barres, B.A., Smith, S.J., Cholesterol—making or breaking the synapse. Science 294 (2001), 1296–1297.
5. Buggia-Prévot, V., Fernandez, C.G., Riordan, S., Vetrivel, K.S., Roseman, J., Waters, J., Bindokas, V.P., Vassar, R., Thinakaran, G., Axonal BACE1 dynamics and targeting in hippocampal neurons: a role for Rab11 GTPase. Mol. Neurodegener., 9, 2014, 1.
6. Burns, M., Gaynor, K., Olm, V., Mercken, M., LaFrancois, J., Wang, L., Mathews, P.M., Noble, W., Matsuoka, Y., Duff, K., Presenilin redistribution associated with aberrant cholesterol transport enhances beta-amyloid production in vivo. J. Neurosci. 23 (2003), 5645–5649.
7. Cai, D., Leem, J.Y., Greenfield, J.P., Wang, P., Kim, B.S., Wang, R., Lopes, K.O., Kim, S.H., Zheng, H., Greengard, P., et al. Presenilin-1 regulates intracellular trafficking and cell surface delivery of β-amyloid precursor protein. J. Biol. Chem. 278 (2003), 3446–3454.
8. Cataldo, A.M., Peterhoff, C.M., Troncoso, J.C., Gomez-Isla, T., Hyman, B.T., Nixon, R.A., Endocytic pathway abnormalities precede amyloid β deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am. J. Pathol. 157 (2000), 277–286.
9. Cataldo, A., Rebeck, G.W., Ghetri, B., Hulette, C., Lippa, C., Van Broeckhoven, C., van Duijn, C., Cras, P., Bogdanovic, N., Bird, T., et al. Endocytic disturbances distinguish among subtypes of Alzheimer's disease and related disorders. Ann. Neurol. 50 (2001), 661–665.
10. Chang, K.-A., Suh, Y.-H., Pathophysiological roles of amyloidogenic carboxy-terminal fragments of the beta-amyloid precursor protein in Alzheimer's disease. J. Pharmacol. Sci. 97 (2005), 461–471.
11. Chen, Y., Durakoglugil, M.S., Xian, X., Herz, J., ApoE4 reduces glutamate receptor function and synaptic plasticity by selectively impairing ApoE receptor recycling. Proc. Natl. Acad. Sci. USA 107 (2010), 12011–12016.
12. Coen, K., Flannagan, R.S., Baron, S., Carraro-Lacroix, L.R., Wang, D., Vermeire, W., Michiels, C., Munck, S., Baert, V., Sugita, S., et al. Lysosomal calcium homeostasis defects, not proton pump defects, cause endo-lysosomal dysfunction in PSEN-deficient cells. J. Cell Biol. 198 (2012), 23–35.
13. Dumanchin, C., Czech, C., Campion, D., Cuif, M.H., Poyot, T., Martin, C., Charbonnier, F., Goud, B., Pradier, L., Frebourg, T., Presenilins interact with Rab11, a small GTPase involved in the regulation of vesicular transport. Hum. Mol. Genet. 8 (1999), 1263–1269.
14. Fonseca, A.C.R.G., Resende, R., Oliveira, C.R., Pereira, C.M.F., Cholesterol and statins in Alzheimer's disease: current controversies. Exp. Neurol. 223 (2010), 282–293.
15. Gandy, S., Zhang, Y.W., Ikin, A., Schmidt, S.D., Bogush, A., Levy, E., Sheffield, R., Nixon, R.A., Liao, F.F., Mathews, P.M., et al. Alzheimer's presenilin 1 modulates sorting of APP and its carboxyl-terminal fragments in cerebral neurons in vivo. J. Neurochem. 102 (2007), 619–626.
16. Gatz, M., Reynolds, C.A., Fratiglioni, L., Johansson, B., Mortimer, J.A., Berg, S., Fiske, A., Pedersen, N.L., Role of genes and environments for explaining Alzheimer disease. Arch. Gen. Psychiatry 63 (2006), 168–174.
17. Ginsberg, S.D., Alldred, M.J., Counts, S.E., Cataldo, A.M., Neve, R.L., Jiang, Y., Wuu, J., Chao, M.V., Mufson, E.J., Nixon, R.A., Che, S., Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression. Biol. Psychiatry 68 (2010), 885–893.
18. Guo, Q., Li, H., Gaddam, S.S.K., Justice, N.J., Robertson, C.S., Zheng, H., Amyloid precursor protein revisited: neuron-specific expression and highly stable nature of soluble derivatives. J. Biol. Chem. 287 (2012), 2437–2445.
19. Karch, C.M., Goate, A.M., Alzheimer's disease risk genes and mechanisms of disease pathogenesis. Biol. Psychiatry 77 (2015), 43–51.
20. Kim, S., Sato, Y., Mohan, P.S., Peterhoff, C., Pensalfini, A., Rigoglioso, A., Jiang, Y., Nixon, R.A., Evidence that the rab5 effector APPL1 mediates APP-βCTF-induced dysfunction of endosomes in Down syndrome and Alzheimer's disease. Mol. Psychiatry 21 (2015), 1–10.
21. Kounnas, M.Z., Moir, R.D., Rebeck, G.W., Bush, A.I., Argraves, W.S., Tanzi, R.E., Hyman, B.T., Strickland, D.K., LDL receptor-related protein, a multifunctional ApoE receptor, binds secreted β-amyloid precursor protein and mediates its degradation. Cell 82 (1995), 331–340.
22. Lane-Donovan, C., Philips, G.T., Herz, J., More than cholesterol transporters: lipoprotein receptors in CNS function and neurodegeneration. Neuron 83 (2014), 771–787.
23. Lazo, O.M., Gonzalez, A., Ascaño, M., Kuruvilla, R., Couve, A., Bronfman, F.C., BDNF regulates Rab11-mediated recycling endosome dynamics to induce dendritic branching. J. Neurosci. 33 (2013), 6112–6122.
24. Lee, J.-H., Yu, W.H., Kumar, A., Lee, S., Mohan, P.S., Peterhoff, C.M., Wolfe, D.M., Martinez-Vicente, M., Massey, A.C., Sovak, G., et al. Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141 (2010), 1146–1158.
25. 2+ homeostasis via TRPML1 by regulating vATPase-mediated lysosome acidification. Cell Rep. 12 (2015), 1430–1444.
26. Leem, J.Y., Saura, C.A., Pietrzik, C., Christianson, J., Wanamaker, C., King, L.T., Veselits, M.L., Tomita, T., Gasparini, L., Iwatsubo, T., et al. A role for presenilin 1 in regulating the delivery of amyloid precursor protein to the cell surface. Neurobiol. Dis. 11 (2002), 64–82.
27. Liu, C.-C., Kanekiyo, T., Xu, H., Bu, G., Apolipoprotein E and Alzheimer disease: risk, mechanisms, and therapy. Nat. Rev, Neurol. 9 (2013), 106–118.
28. Mauch, D.H., Nägler, K., Schumacher, S., Göritz, C., Müller, E.C., Otto, A., Pfrieger, F.W., CNS synaptogenesis promoted by glia-derived cholesterol. Science 294 (2001), 1354–1357.
29. Maxfield, F.R., Role of endosomes and lysosomes in human disease. Cold Spring Harb. Perspect. Biol., 6, 2014, a016931.
30. McBrayer, M., Nixon, R.A., Lysosome and calcium dysregulation in Alzheimer's disease: partners in crime. Biochem. Soc. Trans. 41 (2013), 1495–1502.
31. Nägler, K., Mauch, D.H., Pfrieger, F.W., Glia-derived signals induce synapse formation in neurones of the rat central nervous system. J. Physiol. 533 (2001), 665–679.
32. Neely, K.M., Green, K.N., LaFerla, F.M., Presenilin is necessary for efficient proteolysis through the autophagy-lysosome system in a γ-secretase-independent manner. J. Neurosci. 31 (2011), 2781–2791.
33. Niederst, E.D., Reyna, S.M., Goldstein, L.S.B., Axonal amyloid precursor protein and its fragments undergo somatodendritic endocytosis and processing. Mol. Biol. Cell 26 (2015), 205–217.
34. Nixon, R.A., Yang, D.-S., Autophagy failure in Alzheimer's disease-locating the primary defect. Neurobiol. Dis. 43 (2011), 38–45.
35. Peric, A., Annaert, W., Early etiology of Alzheimer's disease: tipping the balance toward autophagy or endosomal dysfunction?. Acta Neuropathol. 129 (2015), 363–381.
36. Pfrieger, F.W., Role of cholesterol in synapse formation and function. Biochim. Biophys. Acta 1610 (2003), 271–280.
37. Pierrot, N., Tyteca, D., D'auria, L., Dewachter, I., Gailly, P., Hendrickx, A., Tasiaux, B., Haylani, L.E., Muls, N., N'kuli, F., et al. Amyloid precursor protein controls cholesterol turnover needed for neuronal activity. EMBO Mol. Med. 5 (2013), 608–625.
38. Pietrzik, C.U., Busse, T., Merriam, D.E., Weggen, S., Koo, E.H., The cytoplasmic domain of the LDL receptor-related protein regulates multiple steps in APP processing. EMBO J. 21 (2002), 5691–5700.
39. Sakane, H., Yamamoto, H., Kikuchi, A., LRP6 is internalized by Dkk1 to suppress its phosphorylation in the lipid raft and is recycled for reuse. J. Cell Sci. 123 (2010), 360–368.
40. Selfridge, A., Hyun, N., Chiang, C.-C., Reyna, S.M., Weissmiller, A.M., Shi, L.Z., Preece, D., Mobley, W.C., Berns, M.W., Rat embryonic hippocampus and induced pluripotent stem cell derived cultured neurons recover from laser-induced subaxotomy. Neurophotonics, 2, 2015, 015006.
41. Sherrington, R., Rogaev, E.I., Liang, Y., Rogaeva, E.A., Levesque, G., Ikeda, M., Chi, H., Lin, C., Li, G., Holman, K., et al. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease. Nature 375 (1995), 754–760.
42. Sinha, S., Lieberburg, I., Cellular mechanisms of beta-amyloid production and secretion. Proc. Natl. Acad. Sci. USA 96 (1999), 11049–11053.
43. Spires-Jones, T.L., Hyman, B.T., The intersection of amyloid beta and tau at synapses in Alzheimer's disease. Neuron 82 (2014), 756–771.
44. Stokin, G.B., Almenar-Queralt, A., Gunawardena, S., Rodrigues, E.M., Falzone, T., Kim, J., Lillo, C., Mount, S.L., Roberts, E.A., McGowan, E., et al. Amyloid precursor protein-induced axonopathies are independent of amyloid-β peptides. Hum. Mol. Genet. 17 (2008), 3474–3486.
45. Svennerholm, L., Gottfries, C.G., Membrane lipids, selectively diminished in Alzheimer brains, suggest synapse loss as a primary event in early-onset form (type I) and demyelination in late-onset form (type II). J. Neurochem. 62 (1994), 1039–1047.
46. Szpankowski, L., Encalada, S.E., Goldstein, L.S.B., Subpixel colocalization reveals amyloid precursor protein-dependent kinesin-1 and dynein association with axonal vesicles. Proc. Natl. Acad. Sci. USA 109 (2012), 8582–8587.
47. Takahashi, M., Murate, M., Fukuda, M., Sato, S.B., Ohta, A., Kobayashi, T., Cholesterol controls lipid endocytosis through Rab11. Mol. Biol. Cell 18 (2007), 2667–2677.
48. Tamboli, I.Y., Prager, K., Thal, D.R., Thelen, K.M., Dewachter, I., Pietrzik, C.U., St George-Hyslop, P., Sisodia, S.S., De Strooper, B., Heneka, M.T., et al. Loss of gamma-secretase function impairs endocytosis of lipoprotein particles and membrane cholesterol homeostasis. J. Neurosci. 28 (2008), 12097–12106.
49. Taylor, A.M., Blurton-Jones, M., Rhee, S.W., Cribbs, D.H., Cotman, C.W., Jeon, N.L., A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat. Methods 2 (2005), 599–605.
50. Toyn, J.H., Ahlijanian, M.K., Interpreting Alzheimer's disease clinical trials in light of the effects on amyloid-β. Alzheimers Res. Ther., 6, 2014, 14.
51. Treusch, S., Hamamichi, S., Goodman, J.L., Matlack, K.E.S., Chung, C.Y., Baru, V., Shulman, J.M., Parrado, A., Bevis, B.J., Valastyan, J.S., et al. Functional links between Aβttoxicity, endocytic trafficking, and Alzheimer's disease risk factors in yeast. Science 334 (2011), 1241–1245.
52. Udayar, V., Buggia-Prévot, V., Guerreiro, R.L., Siegel, G., Rambabu, N., Soohoo, A.L., Ponnusamy, M., Siegenthaler, B., Bali, J., Simons, M., et al., AESG. A paired RNAi and RabGAP overexpression screen identifies Rab11 as a regulator of β-amyloid production. Cell Rep. 5 (2013), 1536–1551.
53. Ullrich, O., Reinsch, S., Urbé, S., Zerial, M., Parton, R.G., Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135 (1996), 913–924.
54. von Bartheld, C.S., Axonal transport and neuronal transcytosis of trophic factors, tracers, and pathogens. J. Neurobiol. 58 (2004), 295–314.
55. Vossel, K.A., Xu, J.C., Fomenko, V., Miyamoto, T., Suberbielle, E., Knox, J.A., Ho, K., Kim, D.H., Yu, G.-Q., Mucke, L., Tau reduction prevents Aβ-induced axonal transport deficits by blocking activation of GSK3β. J. Cell Biol. 209 (2015), 419–433.
56. Weissmiller, A.M., Natera-Naranjo, O., Reyna, S.M., Pearn, M.L., Zhao, X., Nguyen, P., Cheng, S., Goldstein, L.S.B., Tanzi, R.E., Wagner, S.L., et al. A γ-secretase inhibitor, but not a γ-secretase modulator, induced defects in BDNF axonal trafficking and signaling: evidence for a role for APP. PLoS ONE, 10, 2015, e0118379.
57. Welz, T., Wellbourne-Wood, J., Kerkhoff, E., Orchestration of cell surface proteins by Rab11. Trends Cell Biol. 24 (2014), 407–415.
58. Wilson, J.M., de Hoop, M., Zorzi, N., Toh, B.H., Dotti, C.G., Parton, R.G., EEA1, a tethering protein of the early sorting endosome, shows a polarized distribution in hippocampal neurons, epithelial cells, and fibroblasts. Mol. Biol. Cell 11 (2000), 2657–2671.
59. Wolozin, B., Cholesterol and the biology of Alzheimer's disease. Neuron 41 (2004), 7–10.
60. Woodruff, G., Young, J.E., Martinez, F.J., Buen, F., Gore, A., Kinaga, J., Li, Z., Yuan, S.H., Zhang, K., Goldstein, L.S.B., The presenilin-1 ΔE9 mutation results in reduced γ-secretase activity, but not total loss of PS1 function, in isogenic human stem cells. Cell Rep. 5 (2013), 974–985.
61. Yamakawa, H., Yagishita, S., Futai, E., Ishiura, S., β-Secretase inhibitor potency is decreased by aberrant β-cleavage location of the “Swedish Mutant” amyloid precursor protein. J Biol Chem. 285 (2010), 1634–1642.
62. Yap, C.C., Wisco, D., Kujala, P., Lasiecka, Z.M., Cannon, J.T., Chang, M.C., Hirling, H., Klumperman, J., Winckler, B., The somatodendritic endosomal regulator NEEP21 facilitates axonal targeting of L1/NgCAM. J. Cell Biol. 180 (2008), 827–842.
63. Zhang, M., Haapasalo, A., Kim, D.Y., Ingano, L.A., Pettingell, W.H., Kovacs, D.M., Presenilin/gamma-secretase activity regulates protein clearance from the endocytic recycling compartment. FASEB J. 20 (2006), 1176–1178.
64. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., O'Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 11929–11947.