Presenilin Deficiency or Lysosomal Inhibition Enhances Wnt Signaling through Relocalization of GSK3 to the Late-Endosomal Compartment

Cell Reports

Volumn 2, Issue 5, 2012, Pages 1316-1328

  Dobrowolski, Radek ^a,c   Vick, Philipp ^a   Ploper, Diego ^a   Gumper, Iwona ^b   Snitkin, Harriet ^b   Sabatini, David D ^b   De Robertis, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

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

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CHLOROQUINE; ESCRT PROTEIN; FRIZZLED PROTEIN; GLYCOGEN SYNTHASE KINASE 3; PRESENILIN; TAU PROTEIN; WNT PROTEIN;

ARTICLE; BIOACCUMULATION; CELL COMPARTMENTALIZATION; CELL STRUCTURE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; ENDOSOME; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME STABILITY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

3T3 CELLS; ANIMALS; ANTIGENS, CD63; ANTIMALARIALS; BETA CATENIN; CELL LINE; CHLOROQUINE; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HELA CELLS; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; LYSOSOMES; MACROLIDES; MICE; MULTIVESICULAR BODIES; PRESENILINS; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TAU PROTEINS; WNT PROTEINS;

EID: 84870407757     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.09.026     Document Type: Article

References (52)

1. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol. 2009, 10:468-477.
2. Biechele T.L., Moon R.T. Assaying β-catenin/TCF transcription with β-catenin/TCF transcription-based reporter constructs. Methods Mol. Biol. 2008, 468:99-110.
3. Bilic J., Huang Y.L., Davidson G., Zimmermann T., Cruciat C.M., Bienz M., Niehrs C. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science 2007, 316:1619-1622.
4. Blitzer J.T., Nusse R. A critical role for endocytosis in Wnt signaling. BMC Cell Biol. 2006, 7:28.
5. Boonen R.A., van Tijn P., Zivkovic D. Wnt signaling in Alzheimer's disease: up or down, that is the question. Ageing Res. Rev. 2009, 8:71-82.
6. Brundin P., Melki R., Kopito R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat. Rev. Mol. Cell Biol. 2010, 11:301-307.
7. Bucci C., Thomsen P., Nicoziani P., McCarthy J., van Deurs B. Rab7: a key to lysosome biogenesis. Mol. Biol. Cell 2000, 11:467-480.
8. Cadigan K.M., Peifer M. Wnt signaling from development to disease: insights from model systems. Cold Spring Harb. Perspect. Biol. 2009, 1:a002881.
9. Clevers H., Nusse R. Wnt/β-catenin signaling and disease. Cell 2012, 149:1192-1205.
10. Cruciat C.M., Ohkawara B., Acebron S.P., Karaulanov E., Reinhard C., Ingelfinger D., Boutros M., Niehrs C. Requirement of prorenin receptor and vacuolar H+-ATPase-mediated acidification for Wnt signaling. Science 2010, 327:459-463.
11. Davidson G., Shen J., Huang Y.L., Su Y., Karaulanov E., Bartscherer K., Hassler C., Stannek P., Boutros M., Niehrs C. Cell cycle control of wnt receptor activation. Dev. Cell 2009, 17:788-799.
12. de Calignon A., Polydoro M., Suárez-Calvet M., William C., Adamowicz D.H., Kopeikina K.J., Pitstick R., Sahara N., Ashe K.H., Carlson G.A., et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 2012, 73:685-697.
13. De Ferrari G.V., Moon R.T. The ups and downs of Wnt signaling in prevalent neurological disorders. Oncogene 2006, 25:7545-7553.
14. De Strooper B., Annaert W. Novel research horizons for presenilins and γ-secretases in cell biology and disease. Annu. Rev. Cell Dev. Biol. 2010, 26:235-260.
15. Dobrowolski R., De Robertis E.M. Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles. Nat. Rev. Mol. Cell Biol. 2012, 13:53-60.
16. Escola J.-M., Kleijmeer M.J., Stoorvogel W., Griffith J.M., Yoshie O., Geuze H.J. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 1998, 273:20121-20127.
17. Hall A.C., Lucas F.R., Salinas P.C. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell 2000, 100:525-535.
18. Hardy J. The amyloid hypothesis for Alzheimer's disease: a critical reappraisal. J. Neurochem. 2009, 110:1129-1134.
19. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992, 256:184-185.
20. Huotari J., Helenius A. Endosome maturation. EMBO J. 2011, 30:3481-3500.
21. Kang D.E., Soriano S., Xia X., Eberhart C.G., De Strooper B., Zheng H., Koo E.H. Presenilin couples the paired phosphorylation of beta-catenin independent of axin: implications for beta-catenin activation in tumorigenesis. Cell 2002, 110:751-762.
22. Kategaya L.S., Changkakoty B., Biechele T., Conrad W.H., Kaykas A., Dasgupta R., Moon R.T. Bili inhibits Wnt/beta-catenin signaling by regulating the recruitment of axin to LRP6. PLoS ONE 2009, 4:e6129.
23. Katzmann D.J., Odorizzi G., Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 2002, 3:893-905.
24. Kfoury N., Holmes B.B., Jiang H., Holtzman D.M., Diamond M.I. Trans-cellular propagation of Tau aggregation by fibrillar species. J. Biol. Chem. 2012, 287:19440-19451.
25. Kim N.G., Xu C., Gumbiner B.M. Identification of targets of the Wnt pathway destruction complex in addition to β-catenin. Proc. Natl. Acad. Sci. USA 2009, 106:5165-5170.
26. Kwan K.M., Kirschner M.W. A microtubule-binding Rho-GEF controls cell morphology during convergent extension of Xenopus laevis. Development 2005, 132:4599-4610.
27. 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 2010, 141:1146-1158.
28. Li V.S., Ng S.S., Boersema P.J., Low T.Y., Karthaus W.R., Gerlach J.P., Mohammed S., Heck A.J., Maurice M.M., Mahmoudi T., Clevers H. Wnt signaling through inhibition of β-catenin degradation in an intact Axin1 complex. Cell 2012, 149:1245-1256.
29. Liu L., Drouet V., Wu J.W., Witter M.P., Small S.A., Clelland C., Duff K. Trans-synaptic spread of tau pathology in vivo. PLoS ONE 2012, 7:e31302.
30. MacDonald B.T., Tamai K., He X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell 2009, 17:9-26.
31. Maretto S., Cordenonsi M., Dupont S., Braghetta P., Broccoli V., Hassan A.B., Volpin D., Bressan G.M., Piccolo S. Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 2003, 100:3299-3304.
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. 2011, 31:2781-2791.
33. Niehrs C., Shen J. Regulation of Lrp6 phosphorylation. Cell. Mol. Life Sci. 2010, 67:2551-2562.
34. Niehrs C., Acebron S.P. Mitotic and mitogenic Wnt signalling. EMBO J. 2012, 31:2705-2713.
35. Nixon R.A., Yang D.S. Autophagy failure in Alzheimer's disease-locating the primary defect. Neurobiol. Dis. 2011, 43:38-45.
36. Nixon R.A., Yang D.S., Lee J.H. Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 2008, 4:590-599.
37. Rajendran L., Honsho M., Zahn T.R., Keller P., Geiger K.D., Verkade P., Simons K. Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc. Natl. Acad. Sci. USA 2006, 103:11172-11177.
38. Sahu R., Kaushik S., Clement C.C., Cannizzo E.S., Scharf B., Follenzi A., Potolicchio I., Nieves E., Cuervo A.M., Santambrogio L. Microautophagy of cytosolic proteins by late endosomes. Dev. Cell 2011, 20:131-139.
39. Sardiello M., Palmieri M., di Ronza A., Medina D.L., Valenza M., Gennarino V.A., Di Malta C., Donaudy F., Embrione V., Polishchuk R.S., et al. A gene network regulating lysosomal biogenesis and function. Science 2009, 325:473-477.
40. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 1991, 6:487-498.
41. Soriano S., Kang D.E., Fu M., Pestell R., Chevallier N., Zheng H., Koo E.H. Presenilin 1 negatively regulates beta-catenin/T cell factor/lymphoid enhancer factor-1 signaling independently of beta-amyloid precursor protein and notch processing. J. Cell Biol. 2001, 152:785-794.
42. Sorkin A., von Zastrow M. Endocytosis and signalling: intertwining molecular networks. Nat. Rev. Mol. Cell Biol. 2009, 10:609-622.
43. Taelman V.F., Dobrowolski R., Plouhinec J.L., Fuentealba L.C., Vorwald P.P., Gumper I., Sabatini D.D., De Robertis E.M. Wnt signaling requires sequestration of glycogen synthase kinase 3 inside multivesicular endosomes. Cell 2010, 143:1136-1148.
44. Takahashi R.H., Milner T.A., Li F., Nam E.E., Edgar M.A., Yamaguchi H., Beal M.F., Xu H., Greengard P., Gouras G.K. Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am. J. Pathol. 2002, 161:1869-1879.
45. Vella L.J., Sharples R.A., Nisbet R.M., Cappai R., Hill A.F. The role of exosomes in the processing of proteins associated with neurodegenerative diseases. Eur. Biophys. J. 2008, 37:323-332.
46. Veeman M.T., Slusarski D.C., Kaykas A., Louie S.H., Moon R.T. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 2003, 13:680-685.
47. Wegner C.S., Malerød L., Pedersen N.M., Progida C., Bakke O., Stenmark H., Brech A. Ultrastructural characterization of giant endosomes induced by GTPase-deficient Rab5. Histochem. Cell Biol. 2010, 133:41-55.
48. Wibo M., Poole B. Protein degradation in cultured cells. II. The uptake of chloroquine by rat fibroblasts and the inhibition of cellular protein degradation and cathepsin B1. J. Cell Biol. 1974, 63:430-440.
49. Wollert T., Hurley J.H. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 2010, 464:864-869.
50. Yamamoto H., Komekado H., Kikuchi A. Caveolin is necessary for Wnt-3a-dependent internalization of LRP6 and accumulation of beta-catenin. Dev. Cell 2006, 11:213-223.
51. Zeng X., Huang H., Tamai K., Zhang X., Harada Y., Yokota C., Almeida K., Wang J., Doble B., Woodgett J., et al. Initiation of Wnt signaling: control of Wnt coreceptor Lrp6 phosphorylation/activation via frizzled, dishevelled and axin functions. Development 2008, 135:367-375.
52. Zhang X., Garbett K., Veeraraghavalu K., Wilburn B., Gilmore R., Mirnics K., Sisodia S.S. A role for presenilins in autophagy revisited: normal acidification of lysosomes in cells lacking PSEN1 and PSEN2. J. Neurosci. 2012, 32:8633-8648.