High-resolution structure of a BRICHOS domain and its implications for anti-amyloid chaperone activity on lung surfactant protein C

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 7, 2012, Pages 2325-2329

  Willander, Hanna ^a   Askarieh, Glareh ^a,b   Landreh, Michael ^c   Westermark, Per ^d   Nordling, Kerstin ^a,c   Keränen, Henrik ^d   Hermansson, Erik ^a,c   Hamvas, Aaron ^e   Noge, Lawrence M ^f   Bergman, Tomas ^c   Saenz, Alejandra ^g   Casals, Cristina ^g   Åqvist, Johan ^d   Jörnvall, Hans ^c   Berglund, Helena ^c   Presto, Jenny ^a,c   Knight, Stefan D ^a   Johansson, Jan ^a,c  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UNIVERSITY OF OSLO   (Norway)

^c KAROLINSKA INSTITUTE   (Sweden)

^d UPPSALA UNIVERSITY   (Sweden)

^e ST LOUIS CHILDREN S HOSPITAL   (United States)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

sheet aggregates; Discordant helix; Interstitial lung disease; SFTPC mutations; Transmembrane segment

Indexed keywords

AMYLOID; ASPARTIC ACID; CHAPERONE; LUNG SURFACTANT; PROTEIN C; SURFACTANT PROTEIN PROPROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BRICHOS DOMAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; IN VIVO STUDY; LUNG PARENCHYMA; MASS SPECTROMETRY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN;

AMINO ACID SEQUENCE; AMYLOID; CRYSTALLOGRAPHY, X-RAY; LUNG; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; PULMONARY SURFACTANT-ASSOCIATED PROTEIN C;

EID: 84857129641     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114740109     Document Type: Article

References (30)

1. Mulugeta S, Beers MF (2006) Surfactant protein C: its unique properties and emerging immunomodulatory role in the lung. Microbes Infect 8:2317-2323. (Pubitemid 44311585)
2. Beers MF, Kim CY, Dodia C, Fisher AB (1994) Localization, synthesis, and processing of surfactant protein SP-C in rat lung analyzed by epitope-specific antipeptide antibodies. J Biol Chem 269:20318-20328. (Pubitemid 24260429)
3. Johansson J, Szyperski T, Curstedt T, Wüthrich K (1994) The NMR structure of the pulmonary surfactant-associated polypeptide SP-C in an apolar solvent contains a valyl-rich α-helix. Biochemistry 33:6015-6023. (Pubitemid 24184607)
4. Mingarro I, Nilsson I, Whitley P, von Heijne G (2000) Different conformations of nascent polypeptides during translocation across the ER membrane. BMC Cell Biol 1, Available at http://www.biomedcentral.com/1471-2121/ 1/3.
5. Kallberg Y, Gustafsson M, Persson B, Thyberg J, Johansson J (2001) Prediction of amyloid fibril-forming proteins. J Biol Chem 276:12945-12950.
6. Hedlund J, Johansson J, Persson B (2009) BRICHOS - a superfamily of multidomain proteins with diverse functions. BMC Res Notes 11, Available at http://www.biomedcentral.com/1756-0500/2/180.
7. Nogee LM, et al. (2001) A mutation in the surfactant protein C gene associated with familial interstitial lung disease. N Engl J Med 344:573-579. (Pubitemid 32167871)
8. Wert SE, Whitsett JA, Nogee LM (2009) Genetic disorders of surfactant dysfunction. Pediatr Dev Pathol 12:253-274.
9. Sanchez-Pulido L, Devos D, Valencia A (2002) BRICHOS: a conserved domain in proteins associated with dementia, respiratory distress and cancer. Trends Biochem Sci 27:329-332. (Pubitemid 34756511)
10. Johansson H, Nerelius C, Nordling K, Johansson J (2009) Preventing amyloid formation by catching unfolded transmembrane segments. J Mol Biol 389:227-229.
11. Nerelius C, et al. (2008) Mutations linked to interstitial lung disease can abrogate anti-amyloid function of prosurfactant protein C. Biochem J 41:201-209.
12. Casals C, et al. (2008) C-terminal, endoplasmic reticulum-lumenal domain of prosurfactant protein C - structural features and membrane interactions. FEBS J 275:536-547.
13. Wang WJ, Russo SJ, Mulugeta S, Beers MF (2002) Biosynthesis of surfactant protein C (SP-C). Sorting of SP-C proprotein involves homomeric association via a signal anchor domain. J Biol Chem 277:19929-19937. (Pubitemid 34967514)
14. Fitzen M, et al. (2009) Peptide-binding specificity of the prosurfactant protein C Brichos domain analyzed by electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom 184:3591-3598.
15. Johansson H, Nordling K, Weaver TE, Johansson J (2006) The Brichos domain-containing C-terminal part of pro-surfactant protein C binds to an unfolded poly-val transmembrane segment. J Biol Chem 281:21032-21039. (Pubitemid 44115444)
16. Sipe JD, et al. (2010) Amyloid fibril protein nomenclature: 2010 recommendations from the nomenclature committee of the International Society of Amyloidosis. Amyloid 17:101-104.
17. Westermark P (2011) Subcutaneous adipose tissue biopsy for amyloid protein studies. Amyloid Proteins: Methods and Protocols, eds EM Sigurdsson, M Calero, and M Gasset (Springer Science and Business Media, NY), in press, 2nd Ed.
18. Willander H, Hermansson E, Johansson J, Presto J (2011) BRICHOS domain associated with lung fibrosis, dementia and cancer - a chaperone that prevents amyloid fibril formation? FEBS J 278:3893-3904.
19. Sandberg A, et al. (2010) Stabilization of neurotoxic Alzheimer amyloid-β oligomers by protein engineering. Proc Natl Acad Sci USA 107:15595-15600.
20. Yu L, et al. (2009) Structural characterization of a soluble amyloid β-peptide oligomer. Biochemistry 48:1870-1877.
21. Peng S, Fitzen M, Jörnvall H, Johansson J (2010) The extracellular domain of Bri2 (ITM2B) binds the ABri peptide (1-23) and amyloid β-peptide (Aβ1-40). Implications for Bri2 effects on processing of amyloid precursor protein and Aβ aggregation. Biochem Biophys Res Commun 393:356-361.
22. Nerelius C, Gustafsson M, Nordling K, Larsson A, Johansson J (2009) Anti-amyloid activity of the C-terminal domain of proSP-C against amyloid β-peptide and medin. Biochemistry 48:778-786.
23. Zavialov AV, et al. (2003) Structure and biogenesis of the capsular F1 antigen from Yersinia pestis: preserved folding energy drives fiber formation. Cell 113:587-596. (Pubitemid 36694184)
24. Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842-846. (Pubitemid 41486706)
25. Zavialov AV, Knight SD (2007) A novel self-capping mechanism controls aggregation of periplasmic chaperone Caf1M. Mol Microbiol 64:153-164. (Pubitemid 46435038)
26. Barral JM, Broadley SA, Schaffar G, Hartl FU (2004) Roles of molecular chaperones in protein misfolding diseases. Semin Cell Dev Biol 15:17-29. (Pubitemid 38177364)
27. Bonini NM (2002) Chaperoning brain degeneration. Proc Natl Acad Sci USA 99:16407-16411.
28. Johansson H, Eriksson M, Nordling K, Presto J, Johansson J (2009) The Brichos domain of prosurfactant protein C can hold and fold a transmembrane segment. Protein Sci 18:1175-1182.
29. Persson A, et al. (2006) Lactadherin binds to elastin - a starting point for medin amyloid formation? Amyloid 13:78-85.
30. Westermark GT, Johnson KH, Westermark P (1999) Staining methods for identification of amyloid in tissue. Meth Enzymol 309:3-25. (Pubitemid 29446438)