Interactions between N-linked glycosylation and polymerisation of neuroserpin within the endoplasmic reticulum

FEBS Journal

Volumn 282, Issue 23, 2015, Pages 4565-4579

  Moriconi, Claudia ^a   Ordoñez, Adriana ^b   Lupo, Giuseppe ^c   Gooptu, Bibek ^d   Irving, James A ^e   Noto, Rosina ^f   Martorana, Vincenzo ^f   Manno, Mauro ^f   Timpano, Valentina ^a   Guadagno, Noemi A ^a   Dalton, Lucy ^b   Marciniak, Stefan J ^b   Lomas, David A ^e   Miranda, Elena ^a,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f CNR   (Italy)

Author keywords

conformational disease; neurodegeneration; protein aggregation; serpin; serpinopathies

Indexed keywords

ASPARAGINE; MUTANT PROTEIN; NEUROSERPIN; PROTEASOME; BIOPOLYMER; NEUROPEPTIDE; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ARTICLE; BRAIN DISEASE; CARBOXY TERMINAL SEQUENCE; DEMENTIA; DISEASE MODEL; ENDOPLASMIC RETICULUM; ENZYME LINKED IMMUNOSORBENT ASSAY; FAMILIAL ENCEPHALOPATHY WITH NEUROSERPIN INCLUSION BODY; METABOLOMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN POLYMERIZATION; SITE DIRECTED MUTAGENESIS; TRANSIENT TRANSFECTION; WESTERN BLOTTING; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; CELL CULTURE; CHLOROCEBUS AETHIOPS; COS CELL LINE; GENETICS; GLYCOSYLATION; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; PC12 CELL LINE; POLYMERIZATION; RAT;

AMINO ACID SEQUENCE; ANIMALS; BIOPOLYMERS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HUMANS; MODELS, MOLECULAR; MUTATION; NEUROPEPTIDES; PC12 CELLS; POLYMERIZATION; RATS; SERPINS;

EID: 84954490076     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13517     Document Type: Article

References (41)

1. Galliciotti G, &, Sonderegger P, (2006) Neuroserpin. Front Biosci 11, 33-45.
2. Miranda E, &, Lomas DA, (2006) Neuroserpin: a serpin to think about. Cell Mol Life Sci 63, 709-722.
3. Caccia S, Ricagno S, &, Bolognesi M, (2010) Molecular bases of neuroserpin function and pathology. Biomol Concepts 1, 117-130.
4. Davis RL, Shrimpton AE, Holohan PD, Bradshaw C, Feiglin D, Collins GH, Sonderegger P, Kinter J, Becker LM, Lacbawan F, et al,. (1999) Familial dementia caused by polymerization of mutant neuroserpin. Nature 401, 376-379.
5. Davis RL, Shrimpton AE, Carrell RW, Lomas DA, Gerhard L, Baumann B, Lawrence DA, Yepes M, Kim TS, Ghetti B, et al,. (2002) Association between conformational mutations in neuroserpin and onset and severity of dementia. Lancet 359, 2242-2247.
6. Coutelier M, Andries S, Ghariani S, Dan B, Duyckaerts C, van Rijckevorsel K, Raftopoulos C, Deconinck N, Sonderegger P, Scaravilli F, et al,. (2008) Neuroserpin mutation causes electrical status epilepticus of slow-wave sleep. Neurology 71, 64-66.
7. Hagen MC, Murrell JR, Delisle MB, Andermann E, Andermann F, Guiot MC, &, Ghetti B, (2011) Encephalopathy with neuroserpin inclusion bodies presenting as progressive myoclonus epilepsy and associated with a novel mutation in the Proteinase Inhibitor 12 gene. Brain Pathol 21, 575-582.
8. Miranda E, Römisch K, &, Lomas DA, (2004) Mutants of neuroserpin that cause dementia accumulate as polymers within the endoplasmic reticulum. J Biol Chem 279, 28283-28291.
9. Miranda E, MacLeod I, Davies MJ, Pérez J, Römisch K, Crowther DC, &, Lomas DA, (2008) The intracellular accumulation of polymeric neuroserpin explains the severity of the dementia FENIB. Hum Mol Genet 17, 1527-1539.
10. Davies MJ, Miranda E, Roussel BD, Kaufman RJ, Marciniak SJ, &, Lomas DA, (2009) Neuroserpin polymers activate NF-κB by a calcium signaling pathway that is independent of the unfolded protein response. J Biol Chem 284, 18202-18209.
11. Kroeger H, Miranda E, MacLeod I, Pérez J, Crowther DC, Marciniak SJ, &, Lomas DA, (2009) Endoplasmic reticulum-associated degradation (ERAD) and autophagy cooperate to degrade polymerogenic mutant serpins. J Biol Chem 284, 22793-22802.
12. Roussel BD, Newton TM, Malzer E, Simecek N, Haq I, Thomas SE, Burr ML, Lehner PJ, Crowther DC, Marciniak SJ, et al,. (2013) Sterol metabolism regulates neuroserpin polymer degradation in the absence of the unfolded protein response in the dementia FENIB. Hum Mol Genet 22, 4616-4626.
13. Ying Z, Wang H, Fan H, &, Wang G, (2011) The endoplasmic reticulum (ER)-associated degradation system regulates aggregation and degradation of mutant neuroserpin. J Biol Chem 286, 20835-20844.
14. Krueger SR, Ghisu GP, Cinelli P, Gschwend TP, Osterwalder T, Wolfer DP, &, Sonderegger P, (1997) Expression of neuroserpin, an inhibitor of tissue plasminogen activator, in the developing and adult nervous system of the mouse. J Neurosci 17, 8984-8996.
15. Schrimpf SP, Bleiker AJ, Brecevic L, Kozlov SV, Berger P, Osterwalder T, Krueger SR, Schinzel A, &, Sonderegger P, (1997) Human neuroserpin (PI12): cDNA cloning and chromosomal localization to 3q26. Genomics 40, 55-62.
16. Schipanski A, Oberhauser F, Neumann M, Lange S, Szalay B, Krasemann S, van Leeuwen FW, Galliciotti G, &, Glatzel M, (2014) The lectin OS-9 delivers mutant neuroserpin to endoplasmic reticulum associated degradation in familial encephalopathy with neuroserpin inclusion bodies. Neurobiol Aging 35, 2394-2403.
17. Ferris SP, Kodali VK, &, Kaufman RJ, (2014) Glycoprotein folding and quality-control mechanisms in protein-folding diseases. Dis Model Mech 7, 331-341.
18. Lawless MW, Greene CM, Mulgrew A, Taggart CC, O'Neill SJ, &, McElvaney NG, (2004) Activation of endoplasmic reticulum-specific stress responses associated with the conformational disease Z α1-antitrypsin deficiency. J Immunol 172, 5722-5726.
19. Hidvegi T, Schmidt BZ, Hale P, &, Perlmutter DH, (2005) Accumulation of mutant α1-antitrypsin Z in the endoplasmic reticulum activates caspases-4 and -12, NFκB, and BAP31 but not the unfolded protein response. J Biol Chem 280, 39002-39015.
20. 1-antitrypsin deficiency. Hepatology 57, 2049-2060.
21. Irving JA, Haq I, Dickens JA, Faull SV, &, Lomas DA, (2014) Altered native stability is the dominant basis for susceptibility of alpha1-antitrypsin mutants to polymerization. Biochem J 460, 103-115.
22. Sciaky N, Presley J, Smith C, Zaal KJ, Cole N, Moreira JE, Terasaki M, Siggia E, &, Lippincott-Schwartz J, (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J Cell Biol 139, 1137-1155.
23. Osterwalder T, Contartese J, Stoeckli ET, Kuhn TB, &, Sonderegger P, (1996) Neuroserpin, an axonally secreted serine protease inhibitor. EMBO J 15, 2944-2953.
24. Gooptu B, &, Lomas DA, (2009) Conformational pathology of the serpins: themes, variations, and therapeutic strategies. Annu Rev Biochem 78, 147-176.
25. Lomas DA, &, Carrell RW, (2002) Serpinopathies and the conformational dementias. Nat Rev Genet 3, 759-768.
26. 1-antitrypsin: implications for disease and drug design. J Mol Biol 387, 857-868.
27. Bager R, Johansen JS, Jensen JK, Stensballe A, Jendroszek A, Buxbom L, Sørensen HP, &, Andreasen PA, (2013) Protein conformational change delayed by steric hindrance from an N-linked glycan. J Mol Biol 425, 2867-2877.
28. Shental-Bechor D, &, Levy Y, (2008) Effect of glycosylation on protein folding: a close look at thermodynamic stabilization. Proc Natl Acad Sci USA 105, 8256-8261.
29. Takehara S, Zhang J, Yang X, Takahashi N, Mikami B, &, Onda M, (2010) Refolding and polymerization pathways of neuroserpin. J Mol Biol 403, 751-762.
30. Samandari T, &, Brown JL, (1993) A study of the effects of altering the sites for N-glycosylation in α-1-proteinase inhibitor variants M and S. Protein Sci 2, 1400-1410.
31. Belorgey D, Irving JA, Ekeowa UI, Freeke J, Roussel BD, Miranda E, Pérez J, Robinson CV, Marciniak SJ, Crowther DC, et al,. (2011) Characterisation of serpin polymers in vitro and in vivo. Methods 53, 255-266.
32. Sato T, Sako Y, Sho M, Momohara M, Suico MA, Shuto T, Nishitoh H, Okiyoneda T, Kokame K, Kaneko M, et al,. (2012) STT3B-dependent posttranslational N-glycosylation as a surveillance system for secretory protein. Mol Cell 47, 99-110.
33. Belorgey D, Crowther DC, Mahadeva R, &, Lomas DA, (2002) Mutant neuroserpin (S49P) that causes familial encephalopathy with neuroserpin inclusion bodies is a poor proteinase inhibitor and readily forms polymers in vitro. J Biol Chem 277, 17367-17373.
34. Pratt T, Sharp L, Nichols J, Price DJ, &, Mason JO, (2000) Embryonic stem cells and transgenic mice ubiquitously expressing a tau-tagged green fluorescent protein. Dev Biol 228, 19-28.
35. Noto R, Santangelo MG, Levantino M, Cupane A, Mangione MR, Parisi D, Ricagno S, Bolognesi M, Manno M, &, Martorana V, (2015) Functional and dysfunctional conformers of human neuroserpin characterized by optical spectroscopies and molecular dynamics. Biochim Biophys Acta 1854, 110-117.
36. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, &, Ferrin TE, (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
37. Humphrey W, Dalke A, &, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14 33-38, 27-28.
38. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al,. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947-2948.
39. Tamura K, Stecher G, Peterson D, Filipski A, &, Kumar S, (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30, 2725-2729.
40. Sayers EW, Barrett T, Benson DA, Bryant SH, Canese K, Chetvernin V, Church DM, DiCuccio M, Edgar R, Federhen S, et al,. (2009) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37, D5-15.
41. Takehara S, Onda M, Zhang J, Nishiyama M, Yang X, Mikami B, &, Lomas DA, (2009) The 2.1-A crystal structure of native neuroserpin reveals unique structural elements that contribute to conformational instability. J Mol Biol 388, 11-20.