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Presenilin Transmembrane Domain 8 conserved AxxxAxxxG Motifs Are Required for the Activity of the γ-Secretase Complex.

Bibliographic reference Marinangeli, Claudia ; Tasiaux, Bernadette ; Opsomer, Rémi ; Hage, Salim ; Sodero, Alejandro ; et. al. Presenilin Transmembrane Domain 8 conserved AxxxAxxxG Motifs Are Required for the Activity of the γ-Secretase Complex.. In: Journal of Biological Chemistry, Vol. 290, no. 11, p. 7169-7184 (2015)
Permanent URL http://hdl.handle.net/2078.1/155939
  1. Sastre Magdalena, Steiner Harald, Fuchs Klaus, Capell Anja, Multhaup Gerd, Condron Margaret M, Teplow David B, Haass Christian, Presenilin-dependent γ-secretase processing of β-amyloid precursor protein at a site corresponding to the S3 cleavage of Notch, 10.1093/embo-reports/kve180
  2. Kopan Raphael, Ilagan Ma. Xenia G., The Canonical Notch Signaling Pathway: Unfolding the Activation Mechanism, 10.1016/j.cell.2009.03.045
  3. Kopan R., Notch Signaling, 10.1101/cshperspect.a011213
  4. Wolfe Michael S., Intramembrane-cleaving Proteases, 10.1074/jbc.r800039200
  5. Dries Daniel, Yu Gang, Assembly, Maturation, and Trafficking of the γ-Secretase Complex in Alzheimers Disease, 10.2174/156720508783954695
  6. Spasic Dragana, Annaert Wim, Building γ-secretase – the bits and pieces, 10.1242/jcs.015255
  7. Laudon Hanna, Hansson Emil M., Melén Karin, Bergman Anna, Farmery Mark R., Winblad Bengt, Lendahl Urban, von Heijne Gunnar, Näslund Jan, A Nine-transmembrane Domain Topology for Presenilin 1, 10.1074/jbc.m507217200
  8. Thinakaran Gopal, Borchelt David R, Lee Michael K, Slunt Hilda H, Spitzer Lia, Kim Grace, Ratovitsky Tamara, Davenport Frances, Nordstedt Christer, Seeger Mary, Hardy John, Levey Allan I, Gandy Samuel E, Jenkins Nancy A, Copeland Neal G, Price Donald L, Sisodia Sangram S, Endoproteolysis of Presenilin 1 and Accumulation of Processed Derivatives In Vivo, 10.1016/s0896-6273(00)80291-3
  9. Kimberly W. Taylor, Xia Weiming, Rahmati Talat, Wolfe Michael S., Selkoe Dennis J., The Transmembrane Aspartates in Presenilin 1 and 2 Are Obligatory for γ-Secretase Activity and Amyloid β-Protein Generation, 10.1074/jbc.275.5.3173
  10. Wolfe Michael S., Xia Weiming, Ostaszewski Beth L., Diehl Thekla S., Kimberly W. Taylor, Selkoe Dennis J., Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity, 10.1038/19077
  11. Wolfe Michael S., Toward the structure of presenilin/γ-secretase and presenilin homologs, 10.1016/j.bbamem.2013.04.015
  12. Gu Yongjun, Misonou Hiroaki, Sato Toru, Dohmae Naoshi, Takio Koji, Ihara Yasuo, Distinct Intramembrane Cleavage of the β-Amyloid Precursor Protein Family Resembling γ-Secretase-like Cleavage of Notch, 10.1074/jbc.c100357200
  13. Chau De-Ming, Crump Christina J., Villa Jennifer C., Scheinberg David A., Li Yue-Ming, Familial Alzheimer Disease Presenilin-1 Mutations Alter the Active Site Conformation of γ-secretase, 10.1074/jbc.m111.300483
  14. Wanngren Johanna, Lara Patricia, Öjemalm Karin, Maioli Silvia, Moradi Nasim, Chen Lu, Tjernberg Lars O., Lundkvist Johan, Nilsson IngMarie, Karlström Helena, Changed membrane integration and catalytic site conformation are two mechanisms behind the increased Aβ42/Aβ40 ratio by presenilin 1 familial Alzheimer-linked mutations, 10.1016/j.fob.2014.04.006
  15. Lu Peilong, Bai Xiao-chen, Ma Dan, Xie Tian, Yan Chuangye, Sun Linfeng, Yang Guanghui, Zhao Yanyu, Zhou Rui, Scheres Sjors H. W., Shi Yigong, Three-dimensional structure of human γ-secretase, 10.1038/nature13567
  16. Wolfe Michael S., Selkoe Dennis J., γ-Secretase: A Horseshoe Structure Brings Good Luck, 10.1016/j.cell.2014.06.043
  17. Lemmon, J. Biol. Chem, 267, 7683 (1992)
  18. Smith Steven O., Song David, Shekar Srinivasan, Groesbeek Michel, Ziliox Martine, Aimoto Saburo, Structure of the Transmembrane Dimer Interface of Glycophorin A in Membrane Bilayers†, 10.1021/bi010357v
  19. Senes Alessandro, Engel Donald E, DeGrado William F, Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs, 10.1016/j.sbi.2004.07.007
  20. Senes A., Ubarretxena-Belandia I., Engelman D. M., The C --H***O hydrogen bond: A determinant of stability and specificity in transmembrane helix interactions, 10.1073/pnas.161280798
  21. Eilers M., Shekar S. C., Shieh T., Smith S. O., Fleming P. J., Internal packing of helical membrane proteins, 10.1073/pnas.97.11.5796
  22. Eilers Markus, Patel Ashish B., Liu Wei, Smith Steven O., Comparison of Helix Interactions in Membrane and Soluble α-Bundle Proteins, 10.1016/s0006-3495(02)75613-0
  23. Pardossi-Piquard Raphaëlle, Checler Frédéric, The physiology of the β-amyloid precursor protein intracellular domain AICD : AICD production, regulation, degradation and function, 10.1111/j.1471-4159.2011.07475.x
  24. Dawson Jessica P, Weinger Joshua S, Engelman Donald M, Motifs of serine and threonine can drive association of transmembrane helices, 10.1006/jmbi.2001.5353
  25. Adamian Larisa, Liang Jie, Interhelical hydrogen bonds and spatial motifs in membrane proteins: Polar clamps and serine zippers, 10.1002/prot.10071
  26. Smith Steven O., Eilers Markus, Song David, Crocker Evan, Ying Weiwen, Groesbeek Michel, Metz Guenter, Ziliox Martine, Aimoto Saburo, Implications of Threonine Hydrogen Bonding in the Glycophorin A Transmembrane Helix Dimer, 10.1016/s0006-3495(02)75590-2
  27. Beel A. J., Sanders C. R., Substrate specificity of γ-secretase and other intramembrane proteases, 10.1007/s00018-008-7462-2
  28. Kienlen-Campard Pascal, Tasiaux Bernadette, Van Hees Joanne, Li Mingli, Huysseune Sandra, Sato Takeshi, Fei Jeffrey Z., Aimoto Saburo, Courtoy Pierre J., Smith Steven O., Constantinescu Stefan N., Octave Jean-Noël, Amyloidogenic Processing but Not Amyloid Precursor Protein (APP) Intracellular C-terminal Domain Production Requires a Precisely Oriented APP Dimer Assembled by Transmembrane GXXXG Motifs, 10.1074/jbc.m707142200
  29. Sato T., Tang T.-c., Reubins G., Fei J. Z., Fujimoto T., Kienlen-Campard P., Constantinescu S. N., Octave J.-N., Aimoto S., Smith S. O., A helix-to-coil transition at the  -cut site in the transmembrane dimer of the amyloid precursor protein is required for proteolysis, 10.1073/pnas.0812261106
  30. Tang Tzu-Chun, Hu Yi, Kienlen-Campard Pascal, El Haylani Laetitia, Decock Marie, Van Hees Joanne, Fu Ziao, Octave Jean-Noel, Constantinescu Stefan N., Smith Steven O., Conformational Changes Induced by the A21G Flemish Mutation in the Amyloid Precursor Protein Lead to Increased Aβ Production, 10.1016/j.str.2013.12.012
  31. Munter Lisa-Marie, Voigt Philipp, Harmeier Anja, Kaden Daniela, Gottschalk Kay E, Weise Christoph, Pipkorn Rüdiger, Schaefer Michael, Langosch Dieter, Multhaup Gerd, GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of Aβ42, 10.1038/sj.emboj.7601616
  32. Araki Wataru, Saito Shinya, Takahashi-Sasaki Noriko, Shiraishi Hirohisa, Komano Hiroto, Murayama Kiyoko S., Characterization of APH-1 Mutants With a Disrupted Transmembrane GxxxG Motif, 10.1385/jmn:29:1:35
  33. Lee Sheu-Fen, Shah Sanjiv, Yu Cong, Wigley W. Christian, Li Harry, Lim Myungsil, Pedersen Kia, Han Weiping, Thomas Philip, Lundkvist Johan, Hao Yi-Heng, Yu Gang, A Conserved GXXXG Motif in APH-1 Is Critical for Assembly and Activity of the γ-Secretase Complex, 10.1074/jbc.m309745200
  34. Funamoto Satoru, Morishima-Kawashima Maho, Tanimura Yu, Hirotani Naoko, Saido Takaomi C., Ihara Yasuo, Truncated Carboxyl-Terminal Fragments of β-Amyloid Precursor Protein Are Processed to Amyloid β-Proteins 40 and 42†, 10.1021/bi049399k
  35. Niimura Manabu, Isoo Noriko, Takasugi Nobumasa, Tsuruoka Makiko, Ui-Tei Kumiko, Saigo Kaoru, Morohashi Yuichi, Tomita Taisuke, Iwatsubo Takeshi, Aph-1 Contributes to the Stabilization and Trafficking of the γ-Secretase Complex through Mechanisms Involving Intermolecular and Intramolecular Interactions, 10.1074/jbc.m409829200
  36. Liu Wei, Eilers Markus, Patel Ashish B., Smith Steven O., Helix Packing Moments Reveal Diversity and Conservation in Membrane Protein Structure, 10.1016/j.jmb.2004.02.001
  37. Sobhanifar S., Schneider B., Lohr F., Gottstein D., Ikeya T., Mlynarczyk K., Pulawski W., Ghoshdastider U., Kolinski M., Filipek S., Guntert P., Bernhard F., Dotsch V., Structural investigation of the C-terminal catalytic fragment of presenilin 1, 10.1073/pnas.1000778107
  38. Oh Young S., Turner R. James, Topology of the C-Terminal Fragment of Human Presenilin 1, 10.1021/bi0509494
  39. Shiraishi Hirohisa, Marutani Toshihiro, Wang Hua-Qin, Maeda Yasuhiro, Kurono Yukihisa, Takashima Akihiko, Araki Wataru, Nishimura Masaki, Yanagisawa Katsuhiko, Komano Hiroto, Reconstitution of γ-secretase by truncated presenilin (PS) fragments revealed that PS C-terminal transmembrane domain is critical for formation of γ-secretase complex : γ-secretase complex by truncated presenilin, 10.1111/j.1365-2443.2005.00914.x
  40. Watanabe Naoto, Takagi Shizuka, Tominaga Aya, Tomita Taisuke, Iwatsubo Takeshi, Functional Analysis of the Transmembrane Domains of Presenilin 1 : PARTICIPATION OF TRANSMEMBRANE DOMAINS 2 AND 6 IN THE FORMATION OF INITIAL SUBSTRATE-BINDING SITE OF γ-SECRETASE, 10.1074/jbc.m110.101287
  41. Sato C., Takagi S., Tomita T., Iwatsubo T., The C-Terminal PAL Motif and Transmembrane Domain 9 of Presenilin 1 Are Involved in the Formation of the Catalytic Pore of the  -Secretase, 10.1523/jneurosci.1163-08.2008
  42. Aldudo J., Bullido M.J., Valdivieso F., DGGE method for the mutational analysis of the coding and proximal promoter regions of the Alzheimer's disease presenilin-1 gene: Two novel mutations, 10.1002/(sici)1098-1004(199911)14:5<433::aid-humu10>3.0.co;2-k
  43. Octave Jean-Noël, Essalmani Rachid, Tasiaux Bernadette, Menager Jean, Czech Christian, Mercken Luc, The Role of Presenilin-1 in the γ-Secretase Cleavage of the Amyloid Precursor Protein of Alzheimer's Disease, 10.1074/jbc.275.3.1525
  44. Ben Khalifa N., Tyteca D., Marinangeli C., Depuydt M., Collet J.-F., Courtoy P. J., Renauld J.-C., Constantinescu S., Octave J.-N., Kienlen-Campard P., Structural features of the KPI domain control APP dimerization, trafficking, and processing, 10.1096/fj.11-190207
  45. Qi-Takahara Y., Longer Forms of Amyloid   Protein: Implications for the Mechanism of Intramembrane Cleavage by  -Secretase, 10.1523/jneurosci.1575-04.2005
  46. Hébert Sébastien S, Serneels Lutgarde, Tolia Alexandra, Craessaerts Katleen, Derks Carmen, Filippov Mikhail A, Müller Ulrike, De Strooper Bart, Regulated intramembrane proteolysis of amyloid precursor protein and regulation of expression of putative target genes, 10.1038/sj.embor.7400704
  47. Kopan R., Schroeter E. H., Weintraub H., Nye J. S., Signal transduction by activated mNotch: importance of proteolytic processing and its regulation by the extracellular domain., 10.1073/pnas.93.4.1683
  48. Cao X., A Transcriptively Active Complex of APP with Fe65 and Histone Acetyltransferase Tip60, 10.1126/science.1058783
  49. Huysseune Sandra, Kienlen-Campard Pascal, Octave Jean-Noël, Fe65 does not stabilize AICD during activation of transcription in a luciferase assay, 10.1016/j.bbrc.2007.06.186
  50. Hage Salim, Marinangeli Claudia, Stanga Serena, Octave Jean-Noël, Quetin-Leclercq Joëlle, Kienlen-Campard Pascal, Gamma-Secretase Inhibitor Activity of aPterocarpus erinaceusExtract, 10.1159/000355557
  51. Xia W., Zhang J., Perez R., Koo E. H., Selkoe D. J., Interaction between amyloid precursor protein and presenilins in mammalian cells: Implications for the pathogenesis of Alzheimer disease, 10.1073/pnas.94.15.8208
  52. Campeau Eric, Ruhl Victoria E., Rodier Francis, Smith Corey L., Rahmberg Brittany L., Fuss Jill O., Campisi Judith, Yaswen Paul, Cooper Priscilla K., Kaufman Paul D., A Versatile Viral System for Expression and Depletion of Proteins in Mammalian Cells, 10.1371/journal.pone.0006529
  53. Salmon Patrick, Trono Didier, Production and Titration of Lentiviral Vectors, 10.1002/0471142905.hg1210s54
  54. Wang Lie-Feng, Zhang Ru, Xie Xin, Development of a High-Throughput Assay for Screening of γ-Secretase Inhibitor with Endogenous Human, Mouse or Drosophila γ-Secretase, 10.3390/molecules14093589
  55. Berechid Bridget E., Kitzmann Magali, Foltz Daniel R., Roach Arthur H., Seiffert Dietmar, Thompson Lorin A., Olson Richard E., Bernstein Alan, Donoviel Dorit B., Nye Jeffrey S., Identification and Characterization of Presenilin-independent Notch Signaling, 10.1074/jbc.m108238200
  56. Takami M., Nagashima Y., Sano Y., Ishihara S., Morishima-Kawashima M., Funamoto S., Ihara Y.,  -Secretase: Successive Tripeptide and Tetrapeptide Release from the Transmembrane Domain of  -Carboxyl Terminal Fragment, 10.1523/jneurosci.2362-09.2009
  57. Wolfe Michael S., Esler William P., Kimberly W. Taylor, Ostaszewski Beth L., Diehl Thekla S., Moore Chad L., Tsai Jui-Yi, Rahmati Talat, Xia Weiming, Selkoe Dennis J., 10.1038/35017062
  58. Wolfe Michael S., De Los Angeles Joseph, Miller Duane D., Xia Weiming, Selkoe Dennis J., Are Presenilins Intramembrane-Cleaving Proteases? Implications for the Molecular Mechanism of Alzheimer's Disease†, 10.1021/bi991080q
  59. De Strooper Bart, Saftig Paul, Craessaerts Katleen, Vanderstichele Hugo, Guhde Gundula, Annaert Wim, Von Figura Kurt, Van Leuven Fred, 10.1038/34910
  60. Berezovska O., Familial Alzheimer's Disease Presenilin 1 Mutations Cause Alterations in the Conformation of Presenilin and Interactions with Amyloid Precursor Protein, 10.1523/jneurosci.0364-05.2005
  61. De Strooper Bart, Herreman An, Serneels Lutgarde, Annaert Wim, Collen Desiré, Schoonjans Luc, 10.1038/35017105
  62. De Strooper Bart, Annaert Wim, Cupers Philippe, Saftig Paul, Craessaerts Katleen, Mumm Jeffrey S., Schroeter Eric H., Schrijvers Vincent, Wolfe Michael S., Ray William J., Goate Alison, Kopan Raphael, A presenilin-1-dependent γ-secretase-like protease mediates release of Notch intracellular domain, 10.1038/19083
  63. Fukumori A., Fluhrer R., Steiner H., Haass C., Three-Amino Acid Spacing of Presenilin Endoproteolysis Suggests a General Stepwise Cleavage of  -Secretase-Mediated Intramembrane Proteolysis, 10.1523/jneurosci.1443-10.2010
  64. Edbauer D., Winkler E., Haass C., Steiner H., Presenilin and nicastrin regulate each other and determine amyloid  -peptide production via complex formation, 10.1073/pnas.132277899
  65. Bentahir Mostafa, Nyabi Omar, Verhamme Jan, Tolia Alexandra, Horre Katrien, Wiltfang Jens, Esselmann Hermann, Strooper Bart, Presenilin clinical mutations can affect gamma-secretase activity by different mechanisms, 10.1111/j.1471-4159.2005.03578.x
  66. Nyabi Omar, Pype Stefan, Mercken Marc, Herreman An, Saftig Paul, Craessaerts Katleen, Serneels Lutgarde, Annaert Wim, De Strooper Bart, No endogenous Aβ production in presenilin-deficient fibroblasts, 10.1038/ncb0702-e164a
  67. Matsumura Nobutaka, Takami Mako, Okochi Masayasu, Wada-Kakuda Satoko, Fujiwara Hitomi, Tagami Shinji, Funamoto Satoru, Ihara Yasuo, Morishima-Kawashima Maho, γ-Secretase Associated with Lipid Rafts : MULTIPLE INTERACTIVE PATHWAYS IN THE STEPWISE PROCESSING OF β-CARBOXYL-TERMINAL FRAGMENT, 10.1074/jbc.m113.510131
  68. Osenkowski Pamela, Li Hua, Ye Wenjuan, Li Dongyang, Aeschbach Lorene, Fraering Patrick C., Wolfe Michael S., Selkoe Dennis J., Li Huilin, Cryoelectron Microscopy Structure of Purified γ-Secretase at 12 Å Resolution, 10.1016/j.jmb.2008.10.078
  69. Dovey H. F., John V., Anderson J. P., Chen L. Z., De Saint Andrieu P., Fang L. Y., Freedman S. B., Folmer B., Goldbach E., Holsztynska E. J., Hu K. L., Johnson-Wood K. L., Kennedy S. L., Kholodenko D., Knops J. E., Latimer L. H., Lee M., Liao Z., Lieberburg I. M., Motter R. N., Mutter L. C., Nietz J., Quinn K. P., Sacchi K. L., Seubert P. A., Shopp G. M., Thorsett E. D., Tung J. S., Wu J., Yang S., Yin C. T., Schenk D. B., May P. C., Altstiel L. D., Bender M. H., Boggs L. N., Britton T. C., Clemens J. C., Czilli D. L., Dieckman-McGinty D. K., Droste J. J., Fuson K. S., Gitter B. D., Hyslop P. A., Johnstone E. M., Li W-Y., Little S. P., Mabry T. E., Miller F. D., Ni B., Nissen J. S., Porter W. J., Potts B. D., Reel J. K., Stephenson D., Su Y., Shipley L. A., Whitesitt C. A., Yin T., Audia J. E., Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain : γ-secretase inhibitors reduce Aβ levels in PDAPP mouse brain, 10.1046/j.1471-4159.2001.00012.x
  70. Shearman Mark S., Beher Dirk, Clarke Earl E., Lewis Huw D., Harrison Tim, Hunt Peter, Nadin Alan, Smith Adrian L., Stevenson Graeme, Castro José L., L-685,458, an Aspartyl Protease Transition State Mimic, Is a Potent Inhibitor of Amyloid β-Protein Precursor γ-Secretase Activity, 10.1021/bi0005456
  71. Cao Xinwei, Südhof Thomas C., Dissection of Amyloid-β Precursor Protein-dependent Transcriptional Transactivation, 10.1074/jbc.m402248200
  72. De Strooper, EMBO J, 14, 4932 (1995)
  73. Leem Jae Yoon, Saura Carlos A., Pietrzik Claus, Christianson John, Wanamaker Christian, King LaShaunda T., Veselits Margaret L., Tomita Taisuke, Gasparini Laura, Iwatsubo Takeshi, Xu Huaxi, Green William N., Koo Edward H., Thinakaran Gopal, A Role for Presenilin 1 in Regulating the Delivery of Amyloid Precursor Protein to the Cell Surface, 10.1006/nbdi.2002.0546
  74. Herreman A., gamma-Secretase activity requires the presenilin-dependent trafficking of nicastrin through the Golgi apparatus but not its complex glycosylation, 10.1242/jcs.00292
  75. Knappenberger Katharine S., Tian Gaochao, Ye Xiaomei, Sobotka-Briner Cynthia, Ghanekar Smita V., Greenberg Barry D., Scott Clay W., Mechanism of γ-Secretase Cleavage Activation:  Is γ-Secretase Regulated through Autoinhibition Involving the Presenilin-1 Exon 9 Loop?, 10.1021/bi036072v
  76. Jozwiak Krzysztof, Krzysko Krystiana A., Bojarski Lukasz, Gacia Magdalena, Filipek Slawomir, Molecular Models of the Interface between Anterior Pharynx-Defective Protein 1 (APH-1) and Presenilin Involving GxxxG Motifs, 10.1002/cmdc.200700189
  77. Weggen Sascha, Beher Dirk, Molecular consequences of amyloid precursor protein and presenilin mutations causing autosomal-dominant Alzheimer's disease, 10.1186/alzrt107
  78. Hardy J., The Amyloid Hypothesis of Alzheimer's Disease: Progress and Problems on the Road to Therapeutics, 10.1126/science.1072994
  79. Weidemann Andreas, Eggert Simone, Reinhard Friedrich B. M., Vogel Markus, Paliga Krzysztof, Baier Gottfried, Masters Colin L., Beyreuther Konrad, Evin Geneviève, A Novel ɛ-Cleavage within the Transmembrane Domain of the Alzheimer Amyloid Precursor Protein Demonstrates Homology with Notch Processing†, 10.1021/bi015794o
  80. Pinnix Inga, Musunuru Usha, Tun Han, Sridharan Arati, Golde Todd, Eckman Christopher, Ziani-Cherif Chewki, Onstead Luisa, Sambamurti Kumar, A Novel γ-Secretase Assay Based on Detection of the Putative C-terminal Fragment-γ of Amyloid β Protein Precursor, 10.1074/jbc.m005968200
  81. Sato T., Diehl T. S., Narayanan S., Funamoto S., Ihara Y., De Strooper B., Steiner H., Haass C., Wolfe M. S., Active  -Secretase Complexes Contain Only One of Each Component, 10.1074/jbc.m705248200
  82. Hardy J., Higgins G., Alzheimer's disease: the amyloid cascade hypothesis, 10.1126/science.1566067