The tempered polymerization of human neuroserpin

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Noto, Rosina ^a   Santangelo, Maria Grazia ^b   Ricagno, Stefano ^c   Mangione, Maria Rosalia ^a   Levantino, Matteo ^b   Pezzullo, Margherita ^c   Martorana, Vincenzo ^a   Cupane, Antonio ^b   Bolognesi, Martino ^c   Manno, Mauro ^a  

^a CNR   (Italy)

^b UNIVERSITY OF PALERMO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; NEUROSERPIN; POLYMER; SERINE PROTEINASE INHIBITOR; TRYPTOPHAN; NEUROPEPTIDE;

ARTICLE; CONTROLLED STUDY; FRAGMENTATION REACTION; HEAT STRESS; HIGH TEMPERATURE; LIGHT SCATTERING; POLYMERIZATION; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN FAMILY; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY; WILD TYPE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; KINETICS; PHYSIOLOGY; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; TEMPERATURE;

HUMANS; KINETICS; MODELS, MOLECULAR; NEUROPEPTIDES; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SERPINS; TEMPERATURE;

EID: 84857869206     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032444     Document Type: Article

References (62)

1. Silverman GA, Bird PI, Carrell RW, Church FC, Coughlin PB, et al. (2001) The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, novel functions, mechanism of inhibition and a revised nomenclature. J Biol Chem 276: 33293-33296.
2. Gooptu B, Lomas DA, (2009) Conformational pathology of the serpins: themes, variations and therapeutic strategies. Annu Rev Biochem 78: 147-176.
3. Gettins PGW, (2002) Serpin Structure, Mechanism, and Function. Chem Rev 102: 4751-4803.
4. Huntington JA, Read RJ, Carrell RW, (2000) Structure of a serpin-protease complex shows inhibition by deformation. Nature 407: 923-926.
5. Whisstock JC, Bottomley SP, (2006) Molecular gymnastic: serpin structure, folding and misfolding. Curr Opin Struct Biol 16: 761-768.
6. Caccia S, Ricagno S, Bolognesi M, (2010) Molecular bases of neuroserpin function and pathology. BioMol Concepts 1: 117-130.
7. Cabrita LD, Bottomley SP, (2004) How do proteins avoid becoming too stable? Biophysical studies into metastable proteins. Eur Biophys J 33: 83-88.
8. Gooptu B, Hazes B, Chang WSW, Dafforn TR, Carrell RW, et al. (2000) Inactive conformation of the serpin α1-antichymotrypsin indicates two-stage insertion of the reactive loop: Implications for inhibitory function and conformational disease. Proc Natl Acad Sci USA 97: 67-72.
9. Lomas DA, Evans DL, Finch JT, Carrell RW, (1992) The mechanism of Z α1-antitrypsin accumulation in the liver. Nature 357: 605-607.
10. Davies MJ, Miranda E, Roussel BD, Kaufman RJ, Marciniak SJ, et al. (2009) Neuroserpin Polymers Activate NFB by a Calcium Signaling Pathway That Is Independent of the Unfolded Protein Response. J Biol Chem 284: 18202-18209.
11. Carrell RW, Lomas DA, (1997) Conformational disease. The Lancet 350: 134-138.
12. Hastings GA, Coleman TA, Haudenschild CC, Stefansson S, Smith EP, et al. (1997) Neuroserpin, a brain-associated inhibitor of tissue plasminogen activator is localized primarily in neurones. J Biol Chem 272: 33062-33067.
13. Miranda E, Lomas DA, (2006) Neuroserpin: a serpin to think about. Cell Mol Life Sci 63: 709-722.
14. Kinghorn KJ, Crowther DC, Sharp LK, Nerelius C, Davis RL, et al. (2006) Neuroserpin binds Aβ and is a neuroprotective component of amyloid plaques in Alzheimer disease. J Biol Chem 281: 29268-29277.
15. Chiou A, Hagglof P, Orte A, Chen AY, Dunne PD, et al. (2009) Probing neuroserpin polymerization and interaction with amyloid-β peptides using single molecule fluorescence. Biophys J 97: 2306-2315.
16. Davis RL, Shrimpton AE, Holohan PD, Bradshaw C, Feiglin D, et al. (1999) Familial dementia caused by polymerization of mutant neuroserpin. Nature 401: 376-379.
17. Belorgey D, Crowther DC, Mahadeva R, Lomas DA, (2002) Mutant neuroserpin (Ser49Pro) that causes the familial dementia FENIB is a poor proteinase inhibitor and readily forms polymers in vitro. J Biol Chem 277: 17367-17373.
18. Belorgey D, Sharp LK, Crowther DC, Onda M, Johansson J, et al. (2004) Neuroserpin Portland (Ser52Arg) is trapped as an inactive intermediate that rapidly forms polymers: implications for the epilepsy seen in the dementia FENIB. Eur J Biochem 71: 3360-3367.
19. Onda M, Belorgey D, Sharp LK, Lomas DA, (2005) Latent S49P neuroserpin forms polymers in the dementia familial encephalopathy with neuroserpin inclusion bodies. J Biol Chem 280: 1373513741.
20. Davis RL, Shrimpton AE, Carrell RW, Lomas DA, Gerhard L, et al. (2002) Association between conformational mutations in neuroserpin and onset and severity of dementia. Lancet 359: 2242-2247.
21. Miranda E, Romisch K, Lomas DA, (2004) Mutants of neuroserpin that cause dementia accumulate as polymers within the endoplasmic reticulum. J Biol Chem 279: 28283-28291.
22. Miranda E, MacLeod I, Davies MJ, Perez J, Romisch K, et al. (2008) The intracellular accumulation of polymeric neuroserpin explains the severity of the dementia FENIB. Hum Mol Genet 17: 1527-1539.
23. Ricagno S, Caccia S, Sorrentino G, Antonini G, Bolognesi M, (2009) Human Neuroserpin: Structure and Time-Dependent Inhibition. J Mol Biol 388: 109-121.
24. Carrell RW, Lomas DA, (2002) α1-antitrypsin deficiency- A model for conformational diseases. Nature 407: 923-926.
25. Ricagno S, Pezzullo M, Barbiroli A, Manno M, Levantino M, et al. (2010) Two Latent and Two Hyperstable Polymeric Forms of Human Neuroserpin. Biophys J 99: 3402-3411.
26. Santangelo MG, Noto R, Levantino M, Cupane A, Ricagno S, et al. (2012) On the molecular structure of neuroserpin polymers. Proteins 80: 8-13.
27. Belorgey D, Hagglof P, Onda M, Lomas DA, (2010) pH dependent stability of neuroserpin is mediated by histidines 119 and 138; Implications for the control of β-sheet A and polymerization. Methods 53: 255-266.
28. Dafforn TR, Mahadeva R, Elliott PR, Sivasothy P, Lomas DA, (1999) A kinetic mechanism for the polymerization of α1-antitrypsin. J Biol Chem 274: 9548-9555.
29. Sivasothy P, Dafforn TR, Gettins PGW, Lomas DA, (2000) Pathogenic α1-Antitrypsin Polymers Are Formed by Reactive Loop-β- Sheet A Linkage. J Biol Chem 275: 33663-33668.
30. Miranda E, Perez J, Ekeowa UI, Hadzic N, Kalsheker N, et al. (2010) Conformational specificity of polymers of α1-antitrypsin that are associated with liver disease. Hepatology 52: 1078-1088.
31. Ekeowa UI, Freeke J, Miranda E, Gooptu B, Bush MF, et al. (2010) Defining the mechanism of polymerization in the serpinopathies. Proc Natl Acad Sci USA 107: 17146-17151.
32. Tsutsui Y, Kuri B, Sengupta T, Wintrode PL, (2008) The structural basis of serpin polymerization studied by hydrogen/deuterium exchange and mass spectrometry. J Biol Chem 283: 30804-30811.
33. Yamasaki M, Li W, Johnson DJ, Huntington JA, (2008) Crystal structure of a stable dimer reveals the molecular basis of serpin polymerization. Nature 455: 1255-1258.
34. Yamasaki M, Sendall TJ, Pearce MC, Whisstock JC, Huntington JA, (2011) Molecular basis of α1-antitrypsin deficiency revealed by the structure of a domain-swapped trimer. EMBO reports 12: 1011-1017.
35. Purkayastha P, Klemke JW, Lavender S, Oyola R, Cooperman BS, et al. (2005) α1-Antitrypsin Polymerization: A fluorescence Correlation Spectroscopy Study. Biochemistry 44: 2642-2649.
36. Xue WF, Hellewell AL, Gosal WS, Homans SW, Hewitt EW, et al. (2009) Fibril Fragmentation Enhances Amyloid Cytotoxicity. J Biol Chem 284: 34272-34282.
37. Carlier MF, Melki R, Pantaloni D, Hill TL, Chen Y, (1987) Synchronous oscillations in microtubule polymerization. Proc Natl Acad Sci USA 84: 5257-5261.
38. Barker-Carlson K, Lawrence DA, Schwartz BS, (2002) Acyl-Enzyme Complexes between Tissue-type Plasminogen Activator and Neuroserpin are Short-Lived in Vitro. J Biol Chem 49: 46852-46857.
39. Manno M, Craparo EF, Martorana V, Bulone D, San Biagio PL, (2006) Kinetics of insulin aggregation: Disentanglement of amyloid fibrillation from large-size cluster formation. Biophys J 90: 4585-4591.
40. Berne BJ, Pecora R, (1976) Dynamic Light Scattering New York Wiley. Interscience.
41. Carrotta R, Manno M, Giordano FM, Longo A, Portale G, et al. (2009) Protein stability modulated by a conformational effector: effects of trifluoroethanol on bovine serum albumin. Phys Chem Chem Phys 11: 4007-4018.
42. Frisken BJ, (2001) Revisiting the method of cumulants for the analysis of dynamic light-scattering data. Appl Opt 40: 4087-4091.
43. Cipelletti L, Manley S, Ball RC, Weitz DA, (2000) Universal Aging Features in the Restructuring of Fractal Colloidal Gels. Phys Rev Lett 84: 2275-2278.
44. Carrotta R, Manno M, Bulone D, Martorana V, San Biagio PL, (2005) Protofibril Formation of Amyloid β-Protein at Low pH via a Noncooperative Elongation Mechanism. J Biol Chem 280: 30001-30008.
45. de Gennes PG, (1979) Scaling Concepts in Polymer Physics Ithaca and London Cornell University Press.
46. Manno M, Craparo EF, Podestà A, Bulone D, Carrotta R, et al. (2007) Kinetics of Different Processes in Human Insulin Amyloid Formation. J Mol Biol 366: 258-274.
47. Andersen CB, Yagi H, Manno M, Martorana V, Ban T, et al. (2009) Branching in Amyloid Fibril Growth. Biophys J 96: 1529-1536.
48. Ferrone F, (1999) Analysis of protein aggregation kinetics. In: Wetzel R, editors. Methods in Enzymology San Diego Elsevier Academic Press pp. 256-274.
49. Knowles TPJ, Waudby CA, Devlin GL, Cohen SIA, Aguzzi A, et al. (2009) An Analytical Solution to the Kinetics of Breakable Filament Assembly. Science 326: 1533-1537.
50. Lakowicz JR, (1999) Principles of Fluorescence Spectroscopy New York Kluwer Academic/Plenum Publishers.
51. D'Amico M, Raccosta S, Cannas M, Martorana V, Manno M, (2011) Existence of Metastable Intermediate Lysozyme Conformation Highlights the Role of Alcohols in Altering Protein Stability. J Phys Chem B 115: 4078-4087.
52. Krishnan B, Gierasch LM, (2011) Dynamic local unfolding in the serpin α-1 antitrypsin provides a mechanism for loop insertion and polymerization. Nature Struct Mol Biol 18: 222-227.
53. Oosawa F, Asakura S, (1975) Thermodynamics of the Polymerization of Proteins London Academic Press.
54. Flyvbjerg H, Jobs E, Leibler S, (1996) Kinetics of self-assembling microtubules: An inverse problem in biochemistry. Proc Natl Acad Sci USA 93: 5975-5979.
55. Andrews JM, Roberts CJ, (2007) A Lumry-Eyring Nucleated Polymerization Model of Protein Aggregation Kinetics: 1. Aggregation with Pre-Equilibrated Unfolding. J Phys Chem B 111: 7897-7913.
56. Taylor TW, Sorensen CM, (1987) Moment analysis of the cluster-size-distribution approach to scaling during coagulation. Phys Rev A 36: 5415-5419.
57. Olivier BJ, Sorensen CM, (1990) Variable aggregation rates in colloidal gold: Kernel homogeneity dependence on aggregant concentration. Phys Rev A 41: 2093-2100.
58. Vigil RD, Ziff RM, (1989) On the Stability of Coagulation-Fragmentation Population Balances. J Colloid Interface Sci 133: 257-264.
59. Sorensen CM, Zhang HX, Taylor TW, (1987) Cluster-Size Evolution on a Coagulation-Fragmentation System. Phys Rev Lett 59: 363-366.
60. Chen Y, Hill TL, (1987) Theoretical studies oscillations in microtubule polymerization. Proc Natl Acad Sci USA 84: 8419-8423.
61. Marx A, Mandelkow E, (1994) A model of microtubule oscillations. Eur Biophys J 22: 405-421.
62. Jobs E, Wolf DE, Flyvbjerg H, (1997) Modeling Microtubule Oscillation. Phys Rev Lett 79: 519-522.