ER-associated degradation regulates Alzheimer's amyloid pathology and memory function by modulating γ-secretase activity

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Zhu, Bing ^a   Jiang, LuLin ^a   Huang, Timothy ^a   Zhao, Yingjun ^a   Liu, Tongfei ^a   Zhong, Yongwang ^b   Li, Xiaoguang ^a   Campos, Alexandre ^a   Pomeroy, Kenneth ^a   Masliah, Eliezer ^c   Zhang, Dongxian ^a   Xu, Huaxi ^a,d  

^a BURNHAM INSTITUTE   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d XIAMEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; GAMMA SECRETASE; MEMBRALIN; MESSENGER RNA; NICASTRIN; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG; AMYLOID PRECURSOR PROTEIN; C19ORF6 PROTEIN, HUMAN; MEMBRANE PROTEIN; NERVE PROTEIN; NICASTRIN PROTEIN; PROTEIN BINDING; SECRETASE; SMALL INTERFERING RNA;

BRAIN; CELL ORGANELLE; CONTROL SYSTEM; DISEASE INCIDENCE; ENZYME; ENZYME ACTIVITY; HOMEOSTASIS; MEMORY; NERVOUS SYSTEM DISORDER; PATHOLOGY; PROTEIN; PROTEOMICS; QUALITY CONTROL;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME SUBSTRATE; FLUORESCENCE RESONANCE ENERGY TRANSFER; MEMORY; MEMORY DISORDER; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NONHUMAN; PATHOGENESIS; PROTEIN DEGRADATION; PROTEOMICS; ANIMAL; BRAIN; C3H MOUSE; C57BL MOUSE; CELL LINE; COGNITIVE DEFECT; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; FEMALE; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN FOLDING; RNA INTERFERENCE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BRAIN; CELL LINE; COGNITIVE DYSFUNCTION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; FEMALE; HEK293 CELLS; HUMANS; MALE; MEMBRANE GLYCOPROTEINS; MEMORY; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PROTEIN BINDING; PROTEIN FOLDING; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 85034230452     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-01799-4     Document Type: Article

References (51)

1. Tu, S., Okamoto, S., Lipton, S. A., & Xu, H. Oligomeric Abeta-induced synaptic dysfunction in Alzheimer?s disease. Mol. Neurodegener. 9, 48 (2014
2. Li, Y., et al. Structural biology of presenilin 1 complexes. Mol. Neurodegener. 9, 59 (2014
3. Shah, S., et al. Nicastrin functions as a gamma-secretase-substrate receptor. Cell 122, 435-447 (2005
4. Haapasalo, A., & Kovacs, D. M. The many substrates of presenilin/gammasecretase. J. Alzheimers Dis. 25, 3-28 (2011
5. Vetrivel, K. S., Zhang, Y. W., Xu, H., & Thinakaran, G. Pathological and physiological functions of presenilins. Mol. Neurodegener. 1, 4 (2006
6. Lemus, L., & Goder, V. Regulation of endoplasmic reticulum-Associated protein degradation (ERAD) by ubiquitin. Cells 3, 824-847 (2014
7. Meusser, B., Hirsch, C., Jarosch, E., & Sommer, T. ERAD: the long road to destruction. Nat. Cell. Biol. 7, 766-772 (2005
8. Ruggiano, A., Foresti, O., & Carvalho, P. Quality control: ER-Associated degradation: protein quality control and beyond. J. Cell. Biol. 204, 869-879 (2014
9. Nishitoh, H., et al. ALS-linked mutant SOD1 induces ER stress- And ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev. 22, 1451-1464 (2008
10. Al-Saif, A., Bohlega, S., & Al-Mohanna, F. Loss of ERLIN2 function leads to juvenile primary lateral sclerosis. Ann. Neurol. 72, 510-516 (2012
11. Deng, H. X., et al. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature. 477, 211-215 (2011
12. Meyer, H., & Weihl, C. C. The VCP/p97 system at a glance: connecting cellular function to disease pathogenesis. J. Cell. Sci. 127, 3877-3883 (2014
13. Omura, T., Kaneko, M., Okuma, Y., Matsubara, K., & Nomura, Y. Endoplasmic reticulum stress and Parkinson?s disease: the role of HRD1 in averting apoptosis in neurodegenerative disease. Oxidat Med Cell Longev 2013, 239854 (2013
14. Christianson, J. C., et al. Defining human ERAD networks through an integrative mapping strategy. Nat. Cell. Biol. 14, 93-105 (2012
15. Sato, B. K., Schulz, D., Do, P. H., & Hampton, R. Y. Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol. Cell. 34, 212-222 (2009
16. Bernasconi, R., Galli, C., Calanca, V., Nakajima, T., & Molinari, M. Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates. J. Cell. Biol. 188, 223-235 (2010
17. Zattas, D., Adle, D. J., Rubenstein, E. M., & Hochstrasser, M. N-Terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Mol. Biol. Cell. 24, 890-900 (2013
18. Zhong, X., et al. AAA ATPase p97/valosin-containing protein interacts withgp78, a ubiquitin ligase for endoplasmic reticulum-Associated degradation. J. Biol. Chem. 279, 45676-45684 (2004
19. Andersson, O., & von Euler, G. Characterization and expression of the gene encoding membralin, an evolutionary conserved protein expressed in the central nervous system. Brain. Res. Gene. Expr. Patterns. 1, 205-212 (2002
20. Yang, B., et al. The critical role of membralin in postnatal motor neuron survival and disease. eLife 4, doi: 10.7554/eLife.06500 (2015
21. Salminen, A., Kauppinen, A., Suuronen, T., Kaarniranta, K., & Ojala, J. ER stress in Alzheimer?s disease: a novel neuronal trigger for inflammation and Alzheimer?s pathology. J. Neuroinflamm. 6, 41 (2009
22. Ma, T., et al. Suppression of eIF2alpha kinases alleviates Alzheimer?s diseaserelated plasticity and memory deficits. Nat. Neurosci. 16, 1299-1305 (2013
23. Scheper, W., & Hoozemans, J. J. The unfolded protein response in neurodegenerative diseases: a neuropathological perspective. Acta. Neuropathol. 130, 315-331 (2015
24. Desikan, R. S., et al. Genetic assessment of age-Associated Alzheimer disease risk: Development and validation of a polygenic hazard score. PLoS medicine 14, e1002258 (2017
25. Humphries, C., et al. Alzheimer disease (AD) specific transcription, DNA methylation and splicing in twenty AD associated loci. Mol. Cell. Neurosci. 67, 37-45 (2015
26. Verveer, P. J., Rocks, O., Harpur, A. G., & Bastiaens, P. I. Imaging protein interactions by FRET microscopy: FRET measurements by acceptor photobleaching. CSH Protocols 2006, doi: 10.1101/pdb.prot4598 (2006
27. Matthews, D. R., et al. A multi-functional imaging approach to high-content protein interaction screening. PLoS. ONE. 7, e33231 (2012
28. Zhong, Y., & Fang, S. Live cell imaging of protein dislocation from the endoplasmic reticulum. J. Biol. Chem. 287, 28057-28066 (2012
29. Opattova, A., Cente, M., Novak, M., & Filipcik, P. The ubiquitin proteasome system as a potential therapeutic target for treatment of neurodegenerative diseases. Gen. Physiol. Biophys. 34, 337-352 (2015
30. Dennissen, F. J., Kholod, N., & van Leeuwen, F. W. The ubiquitin proteasome system in neurodegenerative diseases: culprit, accomplice or victim?. Prog. Neurobiol. 96, 190-207 (2012
31. Zhang, Y. W., et al. Nicastrin is critical for stability and trafficking but not association of other presenilin/gamma-secretase components. J. Biol. Chem. 280, 17020-17026 (2005
32. Leem, J. Y., et al. Presenilin 1 is required for maturation and cell surface accumulation of nicastrin. J. Biol. Chem. 277, 19236-19240 (2002
33. Edbauer, D., Winkler, E., Haass, C., & Steiner, H. Presenilin and nicastrin regulate each other and determine amyloid beta-peptide production via complex formation. Proc. Natl Acad. Sci. USA 99, 8666-8671 (2002
34. Sato, T., et al. Active gamma-secretase complexes contain only one of each component. J. Biol. Chem. 282, 33985-33993 (2007
35. Wang, X., et al. Sorting nexin 27 regulates Abeta production through modulating gamma-secretase activity. Cell reports 9, 1023-1033 (2014
36. Tian, Y., Bassit, B., Chau, D., & Li, Y. M. An APP inhibitory domain containing the Flemish mutation residue modulates gamma-secretase activity for Abeta production. Nat. Struct. Mol. Biol. 17, 151-158 (2010
37. Chau, D. M., Crump, C. J., Villa, J. C., Scheinberg, D. A., & Li, Y. M. Familial Alzheimer disease presenilin-1 mutations alter the active site conformation of gamma-secretase. J. Biol. Chem. 287, 17288-17296 (2012
38. Chen, Y. C., et al. Identification and characterization of membralin, a novel tumor-Associated gene, in ovarian carcinoma. Biochim. Biophys. Acta. 1730, 96-102 (2005
39. Chishti, M. A., et al. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J. Biol. Chem. 276, 21562-21570 (2001
40. Zemoura, K., et al. Endoplasmic reticulum-Associated degradation controls cell surface expression of gamma-Aminobutyric acid, type B receptors. J. Biol. Chem. 288, 34897-34905 (2013
41. Sun, S., et al. IRE1alpha is an endogenous substrate of endoplasmic-reticulumassociated degradation. Nat. Cell. Biol. 17, 1546-1555 (2015
42. Wang, Y., et al. SPFH1 and SPFH2 mediate the ubiquitination and degradation of inositol 1, 4, 5-Trisphosphate receptors in muscarinic receptor-expressing HeLa cells. Biochim. Biophys. Acta. 1793, 1710-1718 (2009
43. van den Boomen, D. J., et al. TMEM129 is a Derlin-1 associated ERAD E3 ligase essential for virus-induced degradation of MHC-I. Proc. Natl Acad. Sci. USA 111, 11425-11430 (2014
44. Brettschneider, J., Del Tredici, K., Lee, V. M., & Trojanowski, J. Q. Spreading of pathology in neurodegenerative diseases: a focus on human studies. Nat. Rev. Neurosci. 16, 109-120 (2015
45. Huang, Y., & Mucke, L. Alzheimer mechanisms and therapeutic strategies. Cell 148, 1204-1222 (2012
46. Teranishi, Y., et al. Erlin-2 is associated with active gamma-secretase in brain and affects amyloid beta-peptide production. Biochem. Biophys. Res. Commun. 424, 476-481 (2012
47. Tanabe, C., et al. The ubiquitin ligase synoviolin up-regulates amyloid beta production by targeting a negative regulator of gamma-secretase, Rer1, for degradation. J. Biol. Chem. 287, 44203-44211 (2012
48. Yan, L., et al. RPS23RG1 reduces Abeta oligomer-induced synaptic and cognitive deficits. Sci. Rep. 6, 18668 (2016
49. Attar, A., et al. A shortened barnes maze protocol reveals memory deficits at 4-months of age in the triple-Transgenic mouse model of alzheimer?s disease. PLoS. ONE 8, e80355 (2013
50. Zhao, Y., et al. Appoptosin-mediated caspase cleavage of tau contributes to progressive supranuclear palsy pathogenesis. Neuron. 87, 963-975 (2015
51. Wang, X., et al. Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in Down?s syndrome. Nat. Med. 19, 473-480 (2013