Journal of Structural Biology

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Journal of Structural Biology This Number Completes Volume 191 ISSN 1047-8477 Volume 191, Number 3, September 2015 Journal of Structural Biology CoverFinal.indd 1 8/17/15 12:22 PM JOURNAL OF STRUCTURAL BIOLOGY Editors-in-Chief Alasdair C. Steven Wolfgang Baumeister Silver Spring, Maryland, USA Max-Planck-Institut fu¨r Biochemie D-82152 Martinsried bei Mu¨nchen, Germany Associate Editors Bridget Carragher Bauke W. Dijkstra Andrei Lupas The Scripps Research Institute Groningen University, Max-Planck-Institut fuer La Jolla, California Groningen, The Netherlands Entwicklungsbiologie Tuebingen, Germany Daniel J. Mu¨ ller Rajan Sankaranarayanan Stephen Weiner Eidgenossische Technische Hochschule Centre for Cellular and Molecular Biology Weizmann Institute of Science Basel, Switzerland Hyderabad, India Rehovot, Israel Editorial Board Ueli Aebi Nick Grishin Michael Radermacher Maurice E. Mu¨ ller Institute Southwestern Medical Center University of Vermont Basel, Switzerland Dallas, Texas Burlington, Vermont Linda Amos Dorit Hanein Zihe Rao MRC Laboratory of Molecular Biology The Burnham Institute Tsinghua University Cambridge, United Kingdom La Jolla, California Beijing, China Albert J.R. Heck Tim Baker Ivan Raska University of California Utrecht University Utrecht, The Netherlands Academy of Sciences of the Czech Republic San Diego, California Prague, Czech Republic Harald Herrmann Adriaan Bax German Cancer Research Center Felix Rey National Institute of Diabetes and Heidelberg, Germany Institut Pasteur Digestive and Kidney Diseases (NIDDK) Paris, France Bethesda, Maryland Anthony Hyman MPI for Molecular Cell Biology, Dresden, Germany Elia Beniash Michael Sattler University of Pittsburgh John Johnson European Molecular Biology Laboratory Pittsburgh, Pennsylvania The Scripps Research Institute, La Jolla, California Heidelberg, Germany Alain Brisson Andrey Kajava Markus Sauer Institut Europe´en de Chimie et Biologie Centre de Recherches de Biochimie University Wuerzburg Bordeaux, France Macromoleculaire Montpellier, France Wuerzburg, Germany Susan Buchanan Masahide Kikkawa IIme Schlichting University of Tokyo National Institutes of Health MIP fu¨ r Medizinische Forschung Tokyo, Japan Bethesda, Maryland Heidelberg, Germany Abraham Koster Sarah Butcher Leiden University Medical Center Petra Schwille University of Helsinki Leiden, The Netherlands Technische Universita¨t Dresden Helsinki, Finland Dresden, Germany Carolyn Larabell Jose-Maria Carazo University of California J. Squire Spanish National Center for Biotechnology San Francisco, California University of Bristol Madrid, Spain Steven Ludtke Bristol, United Kingdom Jose´ L. Carrascosa Baylor College of Medicine Murray Stewart Centro Nacional de Biotecnologı´a Houston, Texas MRC Laboratory of Molecular Biology Madrid, Spain M. Madan Babu Cambridge, United Kingdom Henri Chanzy Medical Research Council (MRC) Cambridge Centre de Recherches sur les England, UK Lukas Tamm University of Virginia Macromole´cules Ve´ge´tales Francois Major Grenoble, France Charlottesville, Virginia Universite´ de Montreal Quebec, Canada James Conway Ronald A. Milligan Kenneth A. Taylor Florida State University University of Pittsburgh The Scripps Research Institute Tallahassee, Florida Pittsburgh, Pennsylvania La Jolla, California Adrian Elcock Tom Misteli Leann Tilley University of Iowa National Institutes of Health/ University of Melbourne Iowa City, Iowa National Cancer Institute Melbourne, Victoria, Australia Bethesda, Maryland Jan Ellenberg Thomas Walz European Molecular Biology Laboratory Andrea Musacchio Harvard Medical School Heidelberg, Germany Max Planck Institute of Molecular Physiology Boston, Massachussetts Dortmund, Germany Andreas Engel Paul Wingfield Delft University of Technology, Eva Nogales NIAMS-NIH Delft, The Netherlands University of California Bethesda, Maryland Berkeley, California Joachim Frank Derak N. Woolfson Wadsworth Center Rau´ l Padro´n University of Bristol Albany, New York Venezuelan Institute for Scientific Research (IVIC) Bristol, United Kingdom Caracas, Venezuela Peter Fratzl David A.D. Parry Ulrich Zachariae University of DundeeDundee MPI of Colloids and Interfaces Massey University Scotland, UK Golm, Germany Palmerston North, New Zealand Robert M. Glaeser Dr. Anastassis Perrakis Dr. Martin Zacharias Technische Universita¨t Mu¨ nchen University of California Netherlands Cancer Institute Garching, Germany Berkeley, California Amsterdam, The Netherlands Founding Editor: F.S. Sjo¨strand Journal of Structural Biology 191 (2015) 272–280 Contents lists available at ScienceDirect Journal of Structural Biology journal homepage: www.elsevier.com/locate/yjsbi Exploring the ‘aggregation-prone’ core of human Cystatin C: A structural study ⇑ Paraskevi L. Tsiolaki, Nikolaos N. Louros, Stavros J. Hamodrakas, Vassiliki A. Iconomidou Department of Cell Biology and Biophysics, Faculty of Biology, University of Athens, Panepistimiopolis, Athens 157 01, Greece article info abstract Article history: Amyloidogenic proteins like human Cystatin C (hCC) have been shown to form dimers and oligomers by Received 8 May 2015 exchange of subdomains of the monomeric proteins. Normally, the hCC monomer, a low molecular type 2 Received in revised form 21 July 2015 Cystatin, consists of 120 amino acid residues and functions as an inhibitor of cysteine proteases. The Accepted 30 July 2015 oligomerization of hCC is involved in the pathophysiology of a rare form of amyloidosis namely Available online 31 July 2015 Icelandic hereditary cerebral amyloid angiopathy, in which an L68Q mutant is deposited as amyloid in brain arteries of young adults. In order to find the shortest stretch responsible to drive the fibril formation Keywords: of hCC, we have previously demonstrated that the LQVVR peptide forms amyloid fibrils, in vitro (Tsiolaki Human Cystatin C et al., 2015). Predictions by AMYLPRED, an amyloidogenic determinant prediction algorithm developed in Hereditary Cystatin C Amyloid Angiopathy Stefin our lab, led us to synthesize and experimentally study two additional predicted peptides derived from 3D-domain swapping hCC. Along with our previous findings, in this work, we reveal that these peptides self-assemble, in a ‘Aggregation-prone’ peptides similar way, into amyloid-like fibrils in vitro, as electron microscopy, X-ray fiber diffraction, ATR FT-IR Amyloid fibrils spectroscopy and Congo red staining studies have shown. Further to our experimental results, all three peptides seem to have a fundamental contribution in forming the ‘‘aggregation-prone’’ core of human Cystatin C. Ó 2015 Published by Elsevier Inc. 1. Introduction Cystatin, expressed in all nucleated human cells (Abrahamson et al., 1986; Grubb, 2000). It is found in all tissues and body fluids Under appropriate conditions, proteins or peptides undergo (Abrahamson et al., 1986) and it is present at particularly high con- conformational changes leading from their soluble forms into centrations in cerebrospinal fluid (Abrahamson et al., 1987; Grubb ordered fibrillar aggregates, called amyloid fibrils. To date, 30 dif- and Lofberg, 1982). ferent proteins can form amyloids and although there is no appar- hCC, belonging to the papain (C1) and legumain (C13) families ent homology in their primary sequence or their 3D structure, they (Grubb, 2000; Henskens et al., 1996; Turk and Bode, 1991), can do share the propensity to self-assemble and form insoluble fibrils. normally inhibit cysteine proteases by an ideal binding epitope The pathological consequences of the formation of amyloid fibrils resulting from the characteristic Cystatin fold (Fig. 1B). This confor- are implicated in a wide range of divergent neurodegenerative dis- mation is composed of a polypeptide that folds into a five-stranded eases such as Alzheimer’s, Parkinson’s, Creutzfeldt-Jacob’s and b-sheet (b1tob5 b-strands), which partially wraps around a cen- Huntington’s disease and many more, known as amyloidoses tral a-helix (a1 helix). The N-terminal segment and the two hair- (Sipe et al., 2012). pin loops L1 and L2 build the edge of the protein, which binds Human Cystatin C (hCC), a 120-aminoacid protein (Fig. 1A) into the active site of cysteine proteases and blocks their prote- (Abrahamson et al., 1987), belongs to the Cystatin super-family olytic activity (Bode et al., 1988)(Fig. 1B, Supplementary Fig. S1). (Barrett, 1986; Turk and Bode, 1991) and is a secretory type 2 In 2010, Koladziejczyk et al., created a monomer-stabilized human Cystatin C with an engineered disulfide bond [(L47C)-(G69C)] (Kolodziejczyk et al., 2010) and revealed for the first time the Abbreviations: hCC, human Cystatin C; HCCAA, Hereditary Cystatin C Amyloid Angiopathy; ATR FT-IR spectroscopy, attenuated total reflectance Fourier-transform canonical structure features of hCC (Supplementary Fig. S1). spectroscopy. Aggregation and oligomerization of hCC accelerates a rare form ⇑ Corresponding author. of amyloidosis, called Hereditary Cystatin C Cerebral Amyloid E-mail addresses: [email protected] (P.L. Tsiolaki), [email protected] Angiopathy (Icelandic Cerebral Angiopathy, HCCAA) (N.N. Louros), [email protected] (S.J. Hamodrakas), [email protected] (Gudmundsson et al., 1972). This angiopathy is an autosomal (V.A. Iconomidou). http://dx.doi.org/10.1016/j.jsb.2015.07.013 1047-8477/Ó 2015 Published by Elsevier Inc. P.L. Tsiolaki et al. / Journal of Structural Biology 191 (2015) 272–280 273 Fig. 1. Amino acid sequence and native structure of human Cystatin C (hCC). (A) A representation of the polypeptide sequence of human Cystatin C, which normally
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