Prevalence and Pathology of Amyloid in Atherosclerotic Arteries
2006; Lippincott Williams & Wilkins; Volume: 26; Issue: 3 Linguagem: Inglês
10.1161/01.atv.0000201930.10103.be
ISSN1524-4636
AutoresChristoph Röcken, J. Tautenhahn, Frank Bühling, Daniela Sachwitz, Steffi Vöckler, Andreas Goette, Thomas Bürger,
Tópico(s)Cell Adhesion Molecules Research
ResumoHomeArteriosclerosis, Thrombosis, and Vascular BiologyVol. 26, No. 3Prevalence and Pathology of Amyloid in Atherosclerotic Arteries Free AccessLetterPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissionsDownload Articles + Supplements ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toSupplementary MaterialsFree AccessLetterPDF/EPUBPrevalence and Pathology of Amyloid in Atherosclerotic Arteries Christoph Röcken, Jörg Tautenhahn, Frank Bühling, Daniela Sachwitz, Steffi Vöckler, Andreas Goette and Thomas Bürger Christoph RöckenChristoph Röcken From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. , Jörg TautenhahnJörg Tautenhahn From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. , Frank BühlingFrank Bühling From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. , Daniela SachwitzDaniela Sachwitz From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. , Steffi VöcklerSteffi Vöckler From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. , Andreas GoetteAndreas Goette From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. and Thomas BürgerThomas Bürger From the Departments of Pathology (C.R., D.S., S.V.), General Surgery (J.T.), and Immunology (F.B.), Otto-von-Guericke-University Magdeburg, Germany; the Department of Clinical and Laboratory Medicine (F.B.), Cottbus, Germany; the Division of Cardiology (A.G.), of the Otto-von-Guericke-University Magdeburg, Germany; and the Diakonissen Krankenhaus (T.B.), Kassel, Germany. Originally published1 Mar 2006https://doi.org/10.1161/01.ATV.0000201930.10103.beArteriosclerosis, Thrombosis, and Vascular Biology. 2006;26:676–677To the Editor:Apolipoprotein AI (AApoAI)–associated amyloidosis is characterized by the deposition of apolipoprotein AI (apoAI) and occurs as a hereditary and a nonhereditary form. Hereditary AApoAI amyloidosis is a systemic disease leading to the deposition of amyloid in various organs and tissues and is caused by germline mutations in the APOA1 gene. Nonhereditary AApoAI amyloid is far more prevalent and characterized by deposits of nonvariant protein in atherosclerotic arteries.1–3 Despite being linked to the most common cause of morbidity and mortality in Western societies, nonhereditary AApoAI amyloid has achieved only little attention.1–4 It shares several striking similarities with secondary or reactive AA amyloidosis. Nonhereditary AApoAI amyloid occurs in the background of a local chronic inflammatory reaction, it originates from an apolipoprotein that largely associates with high-density lipoproteins (HDLs), and apoAI-containing HDL is endocytosed and retroendocytosed by macrophages, which, in themselves, are able to form amyloid in vitro. Finally, AApoAI amyloidosis is characterized by the deposition of proteolytic fragments of the precursor protein, leading us to speculate that proteolysis is involved in the pathogenesis of AApoAI amyloid.1,3 The aim of this study was to gain further insights into the pathology of nonhereditary AApoAI amyloid.See coverThe prevalence and spatial distribution of amyloid, macrophages, cathepsin B (CathB), cathepsin K (CathK), cathepsin L (CathL), and carboxy methyl lysine (CML) was studied using carotid artery specimens obtained from a consecutive series of all 225 patients undergoing carotid endarterectomy with polyester patch angioplasty (Table I, available online at http://atvb.ahajournals.org) during the period from 1997 to 2003. All patients were scheduled for elective therapeutic endarterectomy and gave written informed consent in the surgical procedure. Patient characteristics were retrieved from hospital records. This study was in accordance with the guidelines of the ethics committee of the University of Magdeburg. Tissue samples were formalin fixed and paraffin embedded. Deparaffinized serial sections were stained with hematoxylin and eosin, Elastic van Gieson stain, and Congo Red. Immunostaining was performed with specific antibodies directed against apoAI, CathB, CathK, CathL, CD68, CML, serum amyloid A (SAA), and transthyretin as described previously.5–7 In vitro degradation experiments with apoAI-enriched HDL apolipoproteins (purchased from Calbiochem) were performed using recombinant human CathB (1.5 μmol/L final concentration), Cath K (3.0 μmol/L), and CathL (0.15 μmol/L and 30 nmol/L).5–7 Degradation was performed at 37°C for 10, 30, 120, or 240 minutes at pH 5.5. Proteins were resolved in polyacrylamide gels and visualized by Coomassie blue staining.5 Enzymatic activity was studied in 6 unfixed carotid artery specimens (2 with and 4 without intimal amyloid).Table I summarizes the patients' characteristics. Amyloid was found in the intima and in atherosclerotic plaques in 122 (54%) patients (Figure; Table I). Download figureDownload PowerPointCarotid artery specimens from a patient with symptomatic carotid artery stenosis. Green birefringent amyloid deposits were found in Congo red–stained specimens (Congo red), which were immunoreactive for apoAI (arrow). Note abundant apoAI immunostaining in the surrounding nonamyloidotic plaque area. CathL was found in all arteries, being the most abundant cysteine protease in macrophages of atherosclerotic arteries, and was also found extracellularly. Congo red staining in polarized light; immunostaining with anti-apoAI and anti-CathL antibodies; hematoxylin counterstain. Original magnifications ×200. In vitro degradation experiments using native apoAI-enriched HDL apolipoproteins were performed with CathL (30 nmol/L) for 10 minutes, 30 minutes, 2 hours, and 4 hours. Incubation for 4 hours at 37°C in the presence of proteases and E64 served as a control. NP denotes no protease added. SDS-PAGE and Coomassie blue staining.Patients with amyloid were significantly older than patients without amyloid (P<0.001). The presence of amyloid correlated only with triglyceride levels. Fifty-one amyloid-containing specimens were subjected to immunohistochemical staining with anti–apoAI– and anti–SAA-antibodies. Extracellular apoAI immunoreactivity was most prominent as diffuse staining in atherosclerotic plaques and rarely in the arterial media. In addition, macrophages and foam cells commonly stained for apoAI. In 45 (88%) arteries, amyloid deposits clearly stained with the anti-apoAI antibody (Figure). In six (12%) specimens, amyloid could no longer be discerned in the anti–apoAI-immunostained sections. SAA was not detected in any specimen. The presence and distribution of CML was studied in 20 specimens with amyloid and was detected in every specimen. CML was not found within amyloid. However, it was interesting to note that amyloid deposits were always surrounded by CML immunoreactivity. Twenty-four resection specimens were studied for CD68-immunoreactive macrophages and the spatial distribution of cysteine proteases, including 16 specimens with and 8 without amyloid. CD68-immunoreactive macrophages and CathB were found in every specimen. CathB was present in macrophages (83% of the patients), multinucleated histiocytic giant cells (MGCs; 13%), endothelial cells (4%), and myocytes (4%). Extracellular immunostaining was also commonly observed. CathK was found in 11 (69%) amyloidotic and 6 (63%) nonamyloidotic arteries and was the least commonly found cysteine protease. CathK was also present in macrophages (46%), MGCs (13%), and myocytes (54%). CathL was expressed in all arteries, being present in macrophages (100%), MGCs (17%), and extracellularly (Figure). Almost all macrophages stained for CathL, whereas only a small fraction was immunoreactive for CathB and CathK. CathL was the most abundant cysteine protease in macrophages of atherosclerotic arteries. The pattern of immunostaining for cysteine proteases did not show any differences between amyloidotic and nonamyloidotic arteries. Next, we studied enzymatic activity by fluorospectroscopy (excitation 345 nm, emission 440 nm; Spectramax Gemini Dual-Scanning Microplate Spectrofluorometer, Molecular Devices Cooperation) using a Z-R-R-AMC (CathB), Z-G-P-R-AMC (CathK), or Z-F-R-AMC (CathL; all Bachem) fluorogenic substrate. CathB (Vmax/mg=6.83±4.99) and CathL (Vmax/mg=15.70±10.47) activity was found in every carotid artery specimen. CathK activity (Vmax/mg=6.73±3.79) was detectable in 3 carotid artery specimens, including 1 with intimal amyloid deposits. We then examined whether native human apoAI obtained commercially is susceptible to degradation by cysteine proteases. All 3 proteases were found to be potentially able to degrade apoAI at a concentrations of 30 nmol/L (CathL), 0.15 μmol/L (CathL), 1.5 μmol/L (CathB), and 3 μmol/L (CathK) generating differently sized protein and peptide fragments. No degradation was observed in the absence of active protease or in the presence of a cysteine protease inhibitor (E64).After investigating a large unselected series of resection specimens, we show here that amyloid is a common pathological change in atherosclerotic carotid arteries. The occurrence of amyloid correlated significantly with patient age. Because atherosclerosis was more prevalent than amyloid leads to the conjecture that atherosclerosis precedes or promotes the formation of amyloid. The majority of our patients tested had apoAI-immunoreactive amyloid deposits, consistent with the known origin of intimal amyloid. Despite being common, little is known about the pathogenesis and significance of nonhereditary AApoAI amyloid in atherosclerotic arteries. Serum levels of apoAI correlate inversely to the risk and severity of coronary artery disease, and therefore, it is unlikely that high apoAI–serum levels precede the development of amyloid. However, apoAI is present in atherosclerotic arteries already at an early stage,8,9 and the amount of apoAI correlates with patient age and the severity of atherosclerosis.8 These findings indicate that apoAI is enriched in atherosclerotic arteries leading to a high local concentration, which, on its own, is known to increase the risk of amyloid formation. In support of this notion, we found abundant apoAI immunoreactivity outside the amyloid deposits.A hallmark of atherosclerosis is the post-translational modification of proteins and lipids by advanced-glycation end products (AGEs). The biological effect of AGEs is mediated, at least partly, by the receptor of AGEs (RAGE). Yan et al10 have shown that canceling out the activation of cellular RAGE delayed the onset of reactive amyloidosis in mice, thus describing a putative pathophysiological pathway by which AGEs may influence amyloid formation. In this study, we show that amyloid-containing arteries are rich in CML, a distinct, chemically characterized type of AGE. Thus, AGEs may also be involved in the pathology of nonhereditary AApoAI amyloid.Apart from the primary structure, local or systemic protein concentrations, and the presence of AGEs, other factors contribute to the pathology of amyloid and amyloidoses, including proteolysis of the precursor protein and amyloid deposits, as well as macrophages. We believe that we are the first to show the presence of proteolytically active CathB, CathK, and CathL in atherosclerotic arteries, which have been shown previously to also be potentially involved in the pathology and pathogenesis of AA- and immunoglobulin-derived AL amyloid.5,7 Interestingly, and sharing another similarity with other forms of amyloid,6 we also found CathK-immunoreactive MGCs in amyloidotic arteries. CathK belongs to the most active human elastases described until now and probably represents an enhanced specific proteolytic capability of histiocytic cells.11 Furthermore, we show that all 3 proteases are able to degrade apoAI, generating intermediate-sized fragments, some having a molecular weight similar to AApoAI amyloid proteins.With an increasing knowledge about conformational diseases, it has become evident that protein misfoldings and aggregates can be pathogenic.12 Amyloid in atherosclerotic plaques might be just the tip of an iceberg. Large amounts of aging proteins in the plaque are prone to a multitude of conformational changes and formation of supramolecular structures, not all of which necessarily have to form amyloid to gain a pathologic function. In this respect, atherosclerosis may share similarities with Alzheimer disease. Further studies into this topic are warranted.This work was supported by grants from the Deutsche Forschungsgemeinschaft (grant RO1173/3-3), Bonn Bad-Godesberg, Germany. The authors thank Dr Rosemarie Kientsch-Engel (Roche Diagnostics GmbH; Penzberg, Germany) for kindly providing the anti-CML antibody and Dr Robert Menard (Biotechnology Research Institute, NRCC; Montreal, Canada) for kindly providing recombinant human cathepsin B and L.FootnotesCorrespondence to Prof Dr med Christoph Röcken, Department of Pathology, Charité University Hospital, Schumannstr. 20/21, D-10117 Berlin, Germany. E-mail [email protected] References 1 Mucchiano GI, Haggqvist B, Sletten K, Westermark P. Apolipoprotein A-1-derived amyloid in atherosclerotic plaques of the human aorta. J Pathol. 2001; 193: 270–275.CrossrefMedlineGoogle Scholar2 Mucchiano GI, Jonasson L, Haggqvist B, Einarsson E, Westermark P. Apolipoprotein A-I-derived amyloid in atherosclerosis. Its association with plasma levels of apolipoprotein A-I and cholesterol. Am J Clin Pathol. 2001; 115: 298–303.CrossrefMedlineGoogle Scholar3 Westermark P, Mucchiano G, Marthin T, Johnson KH, Sletten K. Apolipoprotein A1-derived amyloid in human aortic atherosclerotic plaques. Am J Pathol. 1995; 147: 1186–1192.MedlineGoogle Scholar4 Mucchiano G, Cornwell GGI, Westermark P. Senile aortic amyloid. Evidence for two distinct forms of localized deposits. Am J Pathol. 1992; 140: 871–877.MedlineGoogle Scholar5 Bohne S, Sletten K, Menard R, Bühling F, Vockler S, Wrenger E, Roessner A, Röcken C. Cleavage of AL amyloid proteins and AL amyloid deposits by cathepsins B, K, and L. J Pathol. 2004; 203: 528–537.CrossrefMedlineGoogle Scholar6 Röcken C, Stix B, Brömme D, Ansorge S, Roessner A, Bühling F. A putative role for cathepsin K in degradation of AA and AL amyloidosis. Am J Pathol. 2001; 158: 1029–1038.CrossrefMedlineGoogle Scholar7 Röcken C, Menard R, Bühling F, Vöckler S, Raynes J, Stix B, Krüger S, Roessner A, Kähne T. Proteolysis of serum amyloid A and AA amyloid proteins by cysteine proteases: cathepsin B generates AA amyloid proteins and cathepsin L may prevent their formation. Ann Rheum Dis. 2005; 64: 808–815.CrossrefMedlineGoogle Scholar8 Ishikawa Y, Ishii T, Akasaka Y, Masuda T, Strong JP, Zieske AW, Takei H, Malcom GT, Taniyama M, Choi-Miura NH, Tomita M. Immunolocalization of apolipoproteins in aortic atherosclerosis in American youths and young adults: findings from the PDAY study. Atherosclerosis. 2001; 158: 215–225.CrossrefMedlineGoogle Scholar9 Vollmer E, Brust J, Roessner A, Bosse A, Burwikel F, Kaesberg B, Harrach B, Robenek H, Bocker W. Distribution patterns of apolipoproteins A1, A2, and B in the wall of atherosclerotic vessels. Virchows Arch A. 1991; 419: 79–88.CrossrefGoogle Scholar10 Yan SD, Zhu HJ, Zhu AP, Golabek A, Du H, Roher A, Yu J, Soto C, Schmidt AM, Stern D, Kindy M. Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med. 2000; 6: 643–651.CrossrefMedlineGoogle Scholar11 Bühling F, Reisenauer A, Gerber A, Krüger S, Weber E, Brömme D, Roessner A, Ansorge S, Welte T, Röcken C. Cathepsin K—a marker of macrophage differentiation? J Pathol. 2001; 195: 375–382.CrossrefMedlineGoogle Scholar12 Merlini G, Bellotti V. Molecular mechanisms of amyloidosis. N Engl J Med. 2003; 349: 583–596.CrossrefMedlineGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Lewkowicz E and Gursky O (2022) Dynamic protein structures in normal function and pathologic misfolding in systemic amyloidosis, Biophysical Chemistry, 10.1016/j.bpc.2021.106699, 280, (106699), Online publication date: 1-Jan-2022. Ushio N, Chambers J, Watanabe K, Kayano M and Uchida K (2021) Age-Related Arteriolar Changes With Lipid and Amyloid Deposits in the Gonads of Dogs, Veterinary Pathology, 10.1177/0300985821996670, 58:3, (558-567), Online publication date: 1-May-2021. Tasaki M, Lavatelli F, Obici L, Obayashi K, Miyamoto T, Merlini G, Palladini G, Ando Y and Ueda M (2021) Age-related amyloidosis outside the brain: A state-of-the-art review, Ageing Research Reviews, 10.1016/j.arr.2021.101388, 70, (101388), Online publication date: 1-Sep-2021. Beyene S, Yacob O, Melaku G, Hideo-Kajita A, Kuku K, Brathwaite E, Wilson V, Dan K, Kadakkal A, Sheikh F, Mohammed S and Garcia-Garcia H (2021) Comparison of Patterns of Coronary Artery Disease in Patients With Heart Failure by Cardiac Amyloidosis Status, Cardiovascular Revascularization Medicine, 10.1016/j.carrev.2020.09.026, 27, (31-35), Online publication date: 1-Jun-2021. Witkowski A, Carta S, Lu R, Yokoyama S, Rubartelli A and Cavigiolio G (2019) Oxidation of methionine residues in human apolipoprotein A-I generates a potent pro-inflammatory molecule, Journal of Biological Chemistry, 10.1074/jbc.RA118.005663, 294:10, (3634-3646), Online publication date: 1-Mar-2019. Gorbenko G, Trusova V, Deligeorgiev T, Gadjev N, Mizuguchi C and Saito H (2019) Two-step FRET as a tool for probing the amyloid state of proteins, Journal of Molecular Liquids, 10.1016/j.molliq.2019.111675, 294, (111675), Online publication date: 1-Nov-2019. Miyoshi N (2018) Biochemical properties of cholesterol aldehyde secosterol and its derivatives, Journal of Clinical Biochemistry and Nutrition, 10.3164/jcbn.17-109, 62:2, (107-114), . Gorbenko G, Trusova V, Mizuguchi C and Saito H (2018) Lipid Bilayer Interactions of Amyloidogenic N-Terminal Fragment of Apolipoprotein A-I Probed by Förster Resonance Energy Transfer and Molecular Dynamics Simulations, Journal of Fluorescence, 10.1007/s10895-018-2267-7, 28:5, (1037-1047), Online publication date: 1-Sep-2018. Gaglione R, Smaldone G, Di Girolamo R, Piccoli R, Pedone E and Arciello A (2018) Cell milieu significantly affects the fate of AApoAI amyloidogenic variants: predestination or serendipity?, Biochimica et Biophysica Acta (BBA) - General Subjects, 10.1016/j.bbagen.2017.11.018, 1862:3, (377-384), Online publication date: 1-Mar-2018. Townsend D, Hughes E, Akien G, Stewart K, Radford S, Rochester D and Middleton D (2018) Epigallocatechin-3-gallate remodels apolipoprotein A-I amyloid fibrils into soluble oligomers in the presence of heparin, Journal of Biological Chemistry, 10.1074/jbc.RA118.002038, 293:33, (12877-12893), Online publication date: 1-Aug-2018. Witkowski A, Chan G, Boatz J, Li N, Inoue A, Wong J, Wel P and Cavigiolio G (2018) Methionine oxidized apolipoprotein A‐I at the crossroads of HDL biogenesis and amyloid formation, The FASEB Journal, 10.1096/fj.201701127R, 32:6, (3149-3165), Online publication date: 1-Jun-2018. Jayaraman S, Sánchez-Quesada J and Gursky O (2017) Triglyceride increase in the core of high-density lipoproteins augments apolipoprotein dissociation from the surface: Potential implications for treatment of apolipoprotein deposition diseases, Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, 10.1016/j.bbadis.2016.10.010, 1863:1, (200-210), Online publication date: 1-Jan-2017. Townsend D, Hughes E, Hussain R, Siligardi G, Baldock S, Madine J and Middleton D (2017) Heparin and Methionine Oxidation Promote the Formation of Apolipoprotein A-I Amyloid Comprising α-Helical and β-Sheet Structures, Biochemistry, 10.1021/acs.biochem.6b01120, 56:11, (1632-1644), Online publication date: 21-Mar-2017. Ryan T, Griffin M, McGillivray D, Knott R, Wood K, Masters C, Kirby N and Curtain C (2016) Apolipoprotein C-II Adopts Distinct Structures in Complex with Micellar and Submicellar Forms of the Amyloid-Inhibiting Lipid-Mimetic Dodecylphosphocholine, Biophysical Journal, 10.1016/j.bpj.2015.11.007, 110:1, (85-94), Online publication date: 1-Jan-2016. Das M, Wilson C, Mei X, Wales T, Engen J and Gursky O (2016) Structural Stability and Local Dynamics in Disease-Causing Mutants of Human Apolipoprotein A-I: What Makes the Protein Amyloidogenic?, Journal of Molecular Biology, 10.1016/j.jmb.2015.10.029, 428:2, (449-462), Online publication date: 1-Jan-2016. Zheng L, Wu T, Zeng C, Li X, Li X, Wen D, Ji T, Lan T, Xing L, Li J, He X and Wang L (2016) SAP deficiency mitigated atherosclerotic lesions in ApoE−/− mice, Atherosclerosis, 10.1016/j.atherosclerosis.2015.11.009, 244, (179-187), Online publication date: 1-Jan-2016. Miyoshi N (2016) Chemical alterations and regulations of biomolecules in lifestyle-related diseases, Bioscience, Biotechnology, and Biochemistry, 10.1080/09168451.2016.1141037, 80:6, (1046-1053), Online publication date: 2-Jun-2016. Das M and Gursky O (2015) Amyloid-Forming Properties of Human Apolipoproteins: Sequence Analyses and Structural Insights Lipids in Protein Misfolding, 10.1007/978-3-319-17344-3_8, (175-211), . Chowhan R, Dar T and Singh L (2015) Proteopathies: Biological, Molecular and Clinical Perspectives Proteostasis and Chaperone Surveillance, 10.1007/978-81-322-2467-9_8, (139-169), . Rauschecker M, Cologna S, Xekouki P, Nilubol N, Shamburek R, Merino M, Backlund P, Yergey A, Kebebew E, Balow J, Stratakis C and Abraham S (2015) Clinical Case Report: LECT2-Associated Adrenal Amyloidosis, AACE Clinical Case Reports, 10.4158/EP13443.CR, 1:1, (e59-e67), Online publication date: 1-Dec-2016. Rasool M, Malik A, Manan A, Sultana M, Qazi M and Pushparaj P (2015) Protein Folding: From Normal Cellular Function to Pathophysiology Proteostasis and Chaperone Surveillance, 10.1007/978-81-322-2467-9_5, (89-103), . Miyoshi N, Iuliano L, Tomono S and Ohshima H (2014) Implications of cholesterol autoxidation products in the pathogenesis of inflammatory diseases, Biochemical and Biophysical Research Communications, 10.1016/j.bbrc.2013.12.107, 446:3, (702-708), Online publication date: 1-Apr-2014. Das M, Mei X, Jayaraman S, Atkinson D and Gursky O (2014) Amyloidogenic mutations in human apolipoprotein A-I are not necessarily destabilizing - a common mechanism of apolipoprotein A-I misfolding in familial amyloidosis and atherosclerosis, FEBS Journal, 10.1111/febs.12809, 281:11, (2525-2542), Online publication date: 1-Jun-2014. Adachi E, Kosaka A, Tsuji K, Mizuguchi C, Kawashima H, Shigenaga A, Nagao K, Akaji K, Otaka A and Saito H (2013) The extreme N-terminal region of human apolipoprotein A-I has a strong propensity to form amyloid fibrils, FEBS Letters, 10.1016/j.febslet.2013.11.031, 588:3, (389-394), Online publication date: 31-Jan-2014. Wilck N and Ludwig A (2014) Targeting the Ubiquitin-Proteasome System in Atherosclerosis: Status Quo, Challenges, and Perspectives, Antioxidants & Redox Signaling, 10.1089/ars.2013.5805, 21:17, (2344-2363), Online publication date: 10-Dec-2014. Adachi E, Nakajima H, Mizuguchi C, Dhanasekaran P, Kawashima H, Nagao K, Akaji K, Lund-Katz S, Phillips M and Saito H (2013) Dual Role of an N-terminal Amyloidogenic Mutation in Apolipoprotein A-I, Journal of Biological Chemistry, 10.1074/jbc.M112.428052, 288:4, (2848-2856), Online publication date: 1-Jan-2013. Wong Y, Binger K, Howlett G and Griffin M (2012) Identification of an amyloid fibril forming peptide comprising residues 46-59 of apolipoprotein A-I, FEBS Letters, 10.1016/j.febslet.2012.05.007, 586:13, (1754-1758), Online publication date: 21-Jun-2012. Shishido S, Varahan S, Yuan K, Li X and Fleming S (2012) Humoral innate immune response and disease, Clinical Immunology, 10.1016/j.clim.2012.06.002, 144:2, (142-158), Online publication date: 1-Aug-2012. Teoh C, Bekard I, Asimakis P, Griffin M, Ryan T, Dunstan D and Howlett G (2011) Shear Flow Induced Changes in Apolipoprotein C-II Conformation and Amyloid Fibril Formation, Biochemistry, 10.1021/bi2002482, 50:19, (4046-4057), Online publication date: 17-May-2011. Schwartz R, Borissoff J, Spronk H and ten Cate H (2011) The Hemostatic System as a Modulator of Atherosclerosis, New England Journal of Medicine, 10.1056/NEJMra1011670, 364:18, (1746-1760), Online publication date: 5-May-2011. Teoh C, Griffin M and Howlett G (2011) Apolipoproteins and amyloid fibril formation in atherosclerosis, Protein & Cell, 10.1007/s13238-011-1013-6, 2:2, (116-127), Online publication date: 1-Feb-2011. Wong Y, Binger K, Howlett G and Griffin M (2010) Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I, Proceedings of the National Academy of Sciences, 10.1073/pnas.0910136107, 107:5, (1977-1982), Online publication date: 2-Feb-2010. Wall J (2010) Immunotherapy in Secondary and Light-Chain Amyloidosis Protein Misfolding Diseases, 10.1002/9780470572702.ch42, (917-932) Kristen A, Schnabel P, Winter B, Helmke B, Longerich T, Hardt S, Koch A, Sack F, Katus H, Linke R and Dengler T (2010) High prevalence of amyloid in 150 surgically removed heart valves—a comparison of histological and clinical data reveals a correlation to atheroinflammatory conditions, Cardiovascular Pathology, 10.1016/j.carpath.2009.04.005, 19:4, (228-235), Online publication date: 1-Jul-2010. Bassi N, Zampieri S, Ghirardello A, Tonon M, Zen M, Cozzi F and Doria A (2008) Pentraxins, Anti-pentraxin Antibodies, and Atherosclerosis, Clinical Reviews in Allergy & Immunology, 10.1007/s12016-008-8098-6, 37:1, (36-43), Online publication date: 1-Aug-2009. Herczenik E and Gebbink M (2008) Molecular and cellular aspects of protein misfolding and disease, The FASEB Journal, 10.1096/fj.07-099671, 22:7, (2115-2133), Online publication date: 1-Jul-2008. Herrmann J, Soares S, Lerman L and Lerman A (2008) Potential Role of the Ubiquitin-Proteasome System in Atherosclerosis, Journal of the American College of Cardiology, 10.1016/j.jacc.2008.02.047, 51:21, (2003-2010), Online publication date: 1-May-2008. Shin T, Isas J, Hsieh C, Kayed R, Glabe C, Langen R and Chen J (2008) Formation of soluble amyloid oligomers and amyloid fibrils by the multifunctional protein vitronectin, Molecular Neurodegeneration, 10.1186/1750-1326-3-16, 3:1, Online publication date: 1-Dec-2008. Bochicchio B, Pepe A and Tamburro A (2007) Elastic fibers and amyloid deposition in vascular tissue, Future Neurology, 10.2217/14796708.2.5.523, 2:5, (523-536), Online publication date: 1-Sep-2007. Wilson L, Mok Y, Binger K, Griffin M, Mertens H, Lin F, Wade J, Gooley P and Howlett G (2007) A Structural Core Within Apolipoprotein C-II Amyloid Fibrils Identified Using Hydrogen Exchange and Proteolysis, Journal of Molecular Biology, 10.1016/j.jmb.2006.12.040, 366:5, (1639-1651), Online publication date: 1-Mar-2007. Stewart C, Haw A, Lopez R, McDonald T, Callaghan J, McConville M, Moore K, Howlett G and O'Brien K (2007) Serum amyloid P colocalizes with apolipoproteins in human atheroma: functional implications, Journal of Lipid Research, 10.1194/jlr.M700098-JLR200, 48:10, (2162-2171), Online publication date: 1-Oct-2007. Gunzburg M, Perugini M and Howlett G (2007) Structural Basis for the Recognition and Cross-linking of Amyloid Fibrils by Human Apolipoprotein E, Journal of Biological Chemistry, 10.1074/jbc.M706425200, 282:49, (35831-35841), Online publication date: 1-Dec-2007. Howlett G and Moore K (2006) Untangling the role of amyloid in atherosclerosis, Current Opinion in Lipidology, 10.1097/01.mol.0000245260.63505.4f, 17:5, (541-547), Online publication date: 1-Oct-2006. Röcken C and Ernst J (2006) Amyloiddiagnostik bei rheumatischen ErkrankungenAmyloid diagnostics in rheumatic diseases, Der Pathologe, 10.1007/s00292-006-0861-y, 27:6, (422-430), Online publication date: 1-Nov-2006. Röcken C, Fändrich M, Stix B, Tannert A, Hortschansky P, Reinheckel T, Saftig P, Kähne T, Menard R, Ancsin J and Bühling F (2006) Cathepsin protease activity modulates amyloid load in extracerebral amyloidosis, The Journal of Pathology, 10.1002/path.2076, 210:4, (478-487), Online publication date: 1-Dec-2006. March 2006Vol 26, Issue 3 Advertisement Article InformationMetrics https://doi.org/10.1161/01.ATV.0000201930.10103.bePMID: 16484604 Originally publishedMarch 1, 2006 PDF download Advertisement
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