Presenilins Form ER Ca2+ Leak Channels, a Function Disrupted by Familial Alzheimer's Disease-Linked Mutations

Cell

Volumn 126, Issue 5, 2006, Pages 981-993

  Tu, Huiping ^a   Nelson, Omar ^a   Bezprozvanny, Arseny ^a   Wang, Zhengnan ^a   Lee, Sheu Fen ^a   Hao, Yi Heng ^a   Serneels, Lutgarde ^b   De Strooper, Bart ^b   Yu, Gang ^a   Bezprozvanny, Ilya ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CATION CHANNEL; DIVALENT CATION; FLAVINE ADENINE NUCLEOTIDE; MUTANT PROTEIN; PRESENILIN 1; PRESENILIN 2;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EMBRYO; ARTICLE; CALCIUM CONDUCTANCE; CALCIUM SIGNALING; CONTROLLED STUDY; EMBRYO; EMBRYO CELL; ENDOPLASMIC RETICULUM; FIBROBLAST; LIPID BILAYER; MOUSE; MUTANT; MUTATION; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

EID: 33748140720     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.06.059     Document Type: Article

References (41)

1. Annaert W.G., Levesque L., Craessaerts K., Dierinck I., Snellings G., Westaway D., George-Hyslop P.S., Cordell B., Fraser P., and De Strooper B. Presenilin 1 controls gamma-secretase processing of amyloid precursor protein in pre-golgi compartments of hippocampal neurons. J. Cell Biol. 147 (1999) 277-294
2. Arispe N., Rojas E., and Pollard H.B. Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. USA 90 (1993) 567-571
3. Begley J.G., Duan W., Chan S., Duff K., and Mattson M.P. Altered calcium homeostasis and mitochondrial dysfunction in cortical synaptic compartments of presenilin-1 mutant mice. J. Neurochem. 72 (1999) 1030-1039
4. Camello C., Lomax R., Petersen O.H., and Tepikin A.V. Calcium leak from intracellular stores-the enigma of calcium signalling. Cell Calcium 32 (2002) 355-361
5. Cedazo-Minguez A., Popescu B.O., Ankarcrona M., Nishimura T., and Cowburn R.F. The presenilin 1 deltaE9 mutation gives enhanced basal phospholipase C activity and a resultant increase in intracellular calcium concentrations. J. Biol. Chem. 277 (2002) 36646-36655
6. De Strooper B., Saftig P., Craessaerts K., Vanderstichele H., Guhde G., Annaert W., Von Figura K., and Van Leuven F. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 391 (1998) 387-390
7. Herms J., Schneider I., Dewachter I., Caluwaerts N., Kretzschmar H., and Van Leuven F. Capacitive calcium entry is directly attenuated by mutant presenilin-1, independent of the expression of the amyloid precursor protein. J. Biol. Chem. 278 (2003) 2484-2489
8. Herreman A., Serneels L., Annaert W., Collen D., Schoonjans L., and De Strooper B. Total inactivation of gamma-secretase activity in presenilin-deficient embryonic stem cells. Nat. Cell Biol. 2 (2000) 461-462
9. Hofer A.M. Measurement of free [Ca2+] changes in agonist-sensitive internal stores using compartmentalized fluorescent indicators. Methods Mol. Biol. 114 (1999) 249-265
10. Ito E., Oka K., Etcheberrigaray R., Nelson T.J., McPhie D.L., Tofel-Grehl B., Gibson G.E., and Alkon D.L. Internal Ca2+ mobilization is altered in fibroblasts from patients with Alzheimer disease. Proc. Natl. Acad. Sci. USA 91 (1994) 534-538
11. Kasri N.N., Kocks S.L., Verbert L., Hebert S.S., Callewaert G., Parys J.B., Missiaen L., and De Smedt H. Up-regulation of inositol 1,4,5-trisphosphate receptor type 1 is responsible for a decreased endoplasmic-reticulum Ca(2+) content in presenilin double knock-out cells. Cell Calcium 40 (2006) 41-51
12. Khachaturian Z.S. Calcium, membranes, aging, and Alzheimer's disease. Introduction and overview. Ann. N Y Acad. Sci. 568 (1989) 1-4
13. LaFerla F.M. Calcium dyshomeostasis and intracellular signalling in Alzheimer's disease. Nat. Rev. Neurosci. 3 (2002) 862-872
14. Laudon H., Hansson E.M., Melen K., Bergman A., Farmery M.R., Winblad B., Lendahl U., von Heijne G., and Naslund J. A nine-transmembrane domain topology for presenilin 1. J. Biol. Chem. 280 (2005) 35352-35360
15. Leissring M.A., Parker I., and LaFerla F.M. Presenilin-2 mutations modulate amplitude and kinetics of inositol 1, 4,5-trisphosphate-mediated calcium signals. J. Biol. Chem. 274 (1999) 32535-32538
16. Leissring M.A., Paul B.A., Parker I., Cotman C.W., and LaFerla F.M. Alzheimer's presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes. J. Neurochem. 72 (1999) 1061-1068
17. Leissring M.A., LaFerla F.M., Callamaras N., and Parker I. Subcellular mechanisms of presenilin-mediated enhancement of calcium signaling. Neurobiol. Dis. 8 (2001) 469-478
18. Leissring M.A., Murphy M.P., Mead T.R., Akbari Y., Sugarman M.C., Jannatipour M., Anliker B., Muller U., Saftig P., De Strooper B., et al. A physiologic signaling role for the gamma -secretase-derived intracellular fragment of APP. Proc. Natl. Acad. Sci. USA 99 (2002) 4697-4702
19. Lomax R.B., Camello C., Van Coppenolle F., Petersen O.H., and Tepikin A.V. Basal and physiological Ca(2+) leak from the endoplasmic reticulum of pancreatic acinar cells. Second messenger-activated channels and translocons. J. Biol. Chem. 277 (2002) 26479-26485
20. Mattson M.P., LaFerla F.M., Chan S.L., Leissring M.A., Shepel P.N., and Geiger J.D. Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders. Trends Neurosci. 23 (2000) 222-229
21. Nyabi O., Bentahir M., Horre K., Herreman A., Gottardi-Littell N., Van Broeckhoven C., Merchiers P., Spittaels K., Annaert W., and De Strooper B. Presenilins mutated at Asp-257 or Asp-385 restore Pen-2 expression and Nicastrin glycosylation but remain catalytically inactive in the absence of wild type Presenilin. J. Biol. Chem. 278 (2003) 43430-43436
22. Oakes S.A., Scorrano L., Opferman J.T., Bassik M.C., Nishino M., Pozzan T., and Korsmeyer S.J. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 102 (2005) 105-110
23. Pinton P., Ferrari D., Magalhaes P., Schulze-Osthoff K., Di Virgilio F., Pozzan T., and Rizzuto R. Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J. Cell Biol. 148 (2000) 857-862
24. Ris L., Dewachter I., Reverse D., Godaux E., and Van Leuven F. Capacitative calcium entry induces hippocampal long term potentiation in the absence of presenilin-1. J. Biol. Chem. 278 (2003) 44393-44399
25. Saura C.A., Choi S.Y., Beglopoulos V., Malkani S., Zhang D., Shankaranarayana Rao B.S., Chattarji S., Kelleher III R.J., Kandel E.R., Duff K., et al. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42 (2004) 23-36
26. Schneider I., Reverse D., Dewachter I., Ris L., Caluwaerts N., Kuiperi C., Gilis M., Geerts H., Kretzschmar H., Godaux E., et al. Mutant presenilins disturb neuronal calcium homeostasis in the brain of transgenic mice, decreasing the threshold for excitotoxicity and facilitating long-term potentiation. J. Biol. Chem. 276 (2001) 11539-11544
27. Serneels L., Dejaegere T., Craessaerts K., Horre K., Jorissen E., Tousseyn T., Hebert S., Coolen M., Martens G., Zwijsen A., et al. Differential contribution of the three Aph1 genes to gamma-secretase activity in vivo. Proc. Natl. Acad. Sci. USA 102 (2005) 1719-1724
28. Shah S., Lee S.F., Tabuchi K., Hao Y.H., Yu C., LaPlant Q., Ball H., Dann III C.E., Sudhof T., and Yu G. Nicastrin functions as a gamma-secretase-substrate receptor. Cell 122 (2005) 435-447
29. Smith I.F., Green K.N., and LaFerla F.M. Calcium dysregulation in Alzheimer's disease: recent advances gained from genetically modified animals. Cell Calcium 38 (2005) 427-437
30. Stutzmann G.E., Caccamo A., LaFerla F.M., and Parker I. Dysregulated IP3 signaling in cortical neurons of knock-in mice expressing an Alzheimer's-linked mutation in presenilin1 results in exaggerated Ca2+ signals and altered membrane excitability. J. Neurosci. 24 (2004) 508-513
31. Stutzmann G.E., Smith I., Caccamo A., Oddo S., Laferla F.M., and Parker I. Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer's disease mice. J. Neurosci. 26 (2006) 5180-5189
32. Takeda T., Asahi M., Yamaguchi O., Hikoso S., Nakayama H., Kusakari Y., Kawai M., Hongo K., Higuchi Y., Kashiwase K., et al. Presenilin 2 regulates the systolic function of heart by modulating Ca2+ signaling. FASEB J. 19 (2005) 2069-2071
33. Tandon A., and Fraser P. The presenilins. Genome Biol. 3 (2002) reviews3014
34. Tang T.-S., Tu H., Chan E.Y., Maximov A., Wang Z., Wellington C.L., Hayden M.R., and Bezprozvanny I. Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Neuron 39 (2003) 227-239
35. Tu H., Wang Z., and Bezprozvanny I. Modulation of mammalian inositol 1,4,5-trisphosphate receptor isoforms by calcium: a role of calcium sensor region. Biophys. J. 88 (2005) 1056-1069
36. Tu H., Wang Z., Nosyreva E., De Smedt H., and Bezprozvanny I. Functional characterization of mammalian inositol 1,4,5-trisphosphate receptor isoforms. Biophys. J. 88 (2005) 1046-1055
37. Van Coppenolle F., Vanden Abeele F., Slomianny C., Flourakis M., Hesketh J., Dewailly E., and Prevarskaya N. Ribosome-translocon complex mediates calcium leakage from endoplasmic reticulum stores. J. Cell Sci. 117 (2004) 4135-4142
38. Wolfe M.S., Xia W., Ostaszewski B.L., Diehl T.S., Kimberly W.T., and Selkoe D.J. Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity. Nature 398 (1999) 513-517
39. Woodbury D.J., and Miller C. Nystatin-induced liposome fusion: a versatile approach to ion channel reconstitution into planar bilayers. Biophys. J. 58 (1990) 833-839
40. Yoo A.S., Cheng I., Chung S., Grenfell T.Z., Lee H., Pack-Chung E., Handler M., Shen J., Xia W., Tesco G., et al. Presenilin-mediated modulation of capacitative calcium entry. Neuron 27 (2000) 561-572
41. Zweifach A., and Lewis R.S. The mitogen-regulated calcium current of T lymphocytes is activated by depletion of intracellular calcium stores. Proc. Natl. Acad. Sci. USA 90 (1993) 6295-6299