2,852
Views
6
CrossRef citations to date
0
Altmetric
Review Articles

The amyloid proteome: a systematic review and proposal of a protein classification system

&
Pages 526-542 | Received 24 Dec 2020, Accepted 31 May 2021, Published online: 27 Jul 2021

References

  • Adachi M, Kitamura M, Muta K, Maekawa A, Uramatsu T, Tadokoro M, Funakoshi S, Hisano S, Kuwahara N, Shimizu A, et al. 2020. IgM monoclonal gammopathy with heavy-and-light-chain amyloidosis resembling fibrillary glomerulonephritis determined by tandem mass spectrometry: a case report. BMC Nephrol. 21:195.
  • Alexander MP, Dasari S, Vrana JA, Riopel J, Valeri AM, Markowitz GS, Hever A, Bijol V, Larsen CP, Cornell LD, et al. 2018. Congophilic fibrillary glomerulonephritis: a case series. Am J Kidney Dis. 72:325–336. eng.
  • Ancsin JB, Kisilevsky R. 1999. The heparin/heparan sulfate-binding site on apo-serum amyloid A. J Biol Chem. 274:7172–7181.
  • Baranova IN, Bocharov AV, Vishnyakova TG, Kurlander R, Chen Z, Fu D, Arias IM, Csako G, Patterson AP, Eggerman TL. 2010. CD36 is a novel Serum Amyloid A (SAA) receptor mediating SAA binding and SAA-induced signaling in human and rodent cells. J Biol Chem. 285:8492–8506. eng.
  • Baumgart J-V, Stuhlmann-Laeisz C, Hegenbart U, Nattenmüller J, Schönland S, Krüger S, Behrens H-M, Röcken C. 2018. Local vs. systemic pulmonary amyloidosis-impact on diagnostics and clinical management. Virchows Arch. 473:627–637. eng.
  • Benson MD, Buxbaum JN, Eisenberg DS, Merlini G, Saraiva MJM, Sekijima Y, Sipe JD, Westermark P. 2020. Amyloid nomenclature 2020: update and recommendations by the International Society of Amyloidosis (ISA) nomenclature committee. Amyloid. 27:217–222.
  • Bogie JFJ, Dierckx T, Erens C, Grajchen E, Haidar M, Hardonnière K, Hendriks JJA, Hendrix S, Kerdine-Römer S, Broeckhoven JV, et al. 2020. CD36-mediated uptake of myelin debris by macrophages and microglia reduces neuroinflammation. J Neuroinflammation. 17:224. eng.
  • Brambilla F, Lavatelli F, Di Silvestre D, Valentini V, Palladini G, Merlini G, Mauri P. 2013. Shotgun protein profile of human adipose tissue and its changes in relation to systemic amyloidoses. J Proteome Res. 12:5642–5655.
  • Brambilla F, Lavatelli F, Di Silvestre D, Valentini V, Rossi R, Palladini G, Obici L, Verga L, Mauri P, Merlini G. 2012. Reliable typing of systemic amyloidoses through proteomic analysis of subcutaneous adipose tissue. Blood. 119:1844–1847.
  • Bristow CL, Boackle RJ. 1986. Evidence for the binding of human serum amyloid P component to C1q and Fabγ. Mol Immunol. 23(10):1045–1052.
  • Butler PJG, Tennent GA, Pepys MB. 1990. Pentraxin-chromatin interactions: serum amyloid P component specifically displaces H1-type histones and solubilizes native long chromatin. J Exp Med. 172:13–18. eng.
  • Chiti F, Dobson CM. 2017. Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu Rev Biochem. 86:27–68.
  • Cohen AD, Comenzo RL. 2010. Systemic light-chain amyloidosis: advances in diagnosis, prognosis, and therapy. Hematology Am Soc Hematol Educ Program. 2010:287–294. eng.
  • Coker AR, Purvis A, Baker D, Pepys MB, Wood SP. 2000. Molecular chaperone properties of serum amyloid P component. FEBS Lett. 473(2):199–202.
  • Comenzo RL. 2014. LECT2 makes the amyloid list. Blood. 123:1436–1437.
  • Dallacasagrande V, Hajjar KA. 2020. Annexin A2 in inflammation and host defense. Cells. 9(6):1499.
  • Damy T, Plante-Bordeneuve V, Dogan A. 2014. Characterization of untyped cardiac amyloidosis by mass spectrometry in a patient with Gly6Ser transthyretin polymorphism in fatal cardiogenic shock. Arch Cardiovasc Dis. 107:706–708.
  • Dasari S, Alexander MP, Vrana JA, Theis JD, Mills JR, Negron V, Sethi S, Dispenzieri A, Highsmith WE, Jr., Nasr SH, et al. 2018. DnaJ heat shock protein family B member 9 is a novel biomarker for fibrillary GN. J Am Soc Nephrol. 29:51–56.
  • Dasari S, Amin MS, Kurtin PJ, Vrana JA, Theis JD, Grogg KL, Alexander MP, Nasr SH, Fervenza FC, Leung N, et al. 2016. Clinical, biopsy, and mass spectrometry characteristics of renal apolipoprotein A-IV amyloidosis. Kidney Int. 90:658–664.
  • Dasari S, Theis JD, Vrana JA, Rech KL, Dao LN, Howard MT, Dispenzieri A, Gertz MA, Hasadsri L, Highsmith WE, et al. 2020. Amyloid typing by mass spectrometry in clinical practice: a comprehensive review of 16,175 samples. Mayo Clin Proc. 95(9):1852–1864.
  • Dobri A-M, Dudău M, Enciu A-M, Hinescu ME. 2021. CD36 in alzheimer's disease: an overview of molecular mechanisms and therapeutic targeting. Neuroscience. 453:301–311.
  • Dogan A. 2017. Amyloidosis: insights from proteomics. Annu Rev Pathol Mech Dis. 12:277–304.
  • Doll S, Dreßen M, Geyer PE, Itzhak DN, Braun C, Doppler SA, Meier F, Deutsch M-A, Lahm H, Lange R, et al. 2017. Region and cell-type resolved quantitative proteomic map of the human heart. Nat Commun. 8:1469.
  • D’Souza A, Theis J, Quint P, Kyle R, Gertz M, Zeldenrust S, Vrana J, Dogan A, Dispenzieri A. 2013. Exploring the amyloid proteome in immunoglobulin-derived lymph node amyloidosis using laser microdissection/tandem mass spectrometry. Am J Hematol. 88:577–580.
  • D’Souza A, Theis JD, Vrana JA, Dogan A. 2014. Pharmaceutical amyloidosis associated with subcutaneous insulin and enfuvirtide administration. Amyloid. 21:71–75.
  • Efebera YA, Sturm A, Baack EC, Hofmeister CC, Satoskar A, Nadasdy T, Nadasdy G, Benson DM, Gillmore JD, Hawkins PN, et al. 2014. Novel gelsolin variant as the cause of nephrotic syndrome and renal amyloidosis in a large kindred. Amyloid. 21:110–112.
  • Emsley J, White HE, O'Hara BP, Oliva G, Srinivasan N, Tickle IJ, Blundell TL, Pepys MB, Wood SP. 1994. Structure of pentameric human serum amyloid P component. Nature. 367:338–345.
  • Freudenthaler S, Hegenbart U, Schönland S, Behrens H-M, Krüger S, Röcken C. 2016. Amyloid in biopsies of the gastrointestinal tract-a retrospective observational study on 542 patients. Virchows Arch. 468(5):569–577.
  • Gabelica V, Shvartsburg AA, Afonso C, Barran P, Benesch JLP, Bleiholder C, Bowers MT, Bilbao A, Bush MF, Campbell JL, et al. 2019. Recommendations for reporting ion mobility Mass Spectrometry measurements. Mass Spectrom Rev. 38:291–320.
  • Garnier S. 2018. viridis: Default Color Maps from 'matplotlib'. [place unknown]: [publisher unknown]. R package version 0.5.1; [accessed 2020 Oct 4]. https://cran.r-project.org/package=viridis.
  • Glatz JFC, Luiken JJFP. 2018. Dynamic role of the transmembrane glycoprotein CD36 (SR-B2) in cellular fatty acid uptake and utilization. J Lipid Res. 59:1084–1093.
  • Greene MJ, Sam F, Soo Hoo PT, Patel RS, Seldin DC, Connors LH. 2011. Evidence for a functional role of the molecular chaperone clusterin in amyloidotic cardiomyopathy. Am J Pathol. 178:61–68.
  • Gu Z, Eils R, Schlesner M. 2016. Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics. 32:2847–2849.
  • Gu Z, Gu L, Eils R, Schlesner M, Brors B. 2014. circlize implements and enhances circular visualization in R. Bioinformatics. 30:2811–2812.
  • Hajishengallis G, Reis ES, Mastellos DC, Ricklin D, Lambris JD. 2017. Novel mechanisms and functions of complement. Nat Immunol. 18:1288–1298.
  • Hashimoto T, Serrano-Pozo A, Hori Y, Adams KW, Takeda S, Banerji AO, Mitani A, Joyner D, Thyssen DH, Bacskai BJ, et al. 2012. Apolipoprotein E, especially apolipoprotein E4, increases the oligomerization of amyloid β peptide. J Neurosci. 32(43):15181–15192.
  • Helder MRK, Schaff HV, Nishimura RA, Gersh BJ, Dearani JA, Ommen SR, Mereuta OM, Theis JD, Dogan A, Edwards WD. 2014. Impact of incidental amyloidosis on the prognosis of patients with hypertrophic cardiomyopathy undergoing septal myectomy for left ventricular outflow tract obstruction. Am J Cardiol. 114(9):1396–1399.
  • Horike K, Takeda A, Tsujita M, Goto N, Watarai Y, Uchida K, Katayama A, Nishihira M, Shimizu A, Nozu K, et al. 2018. Two novel APOA1 gene mutations in a Japanese renal transplant recipient with recurrent apolipoprotein A-I related amyloidosis. Nephrology. 23 (Suppl 2):17–21.
  • Ikegawa M, Nirasawa T, Kakuda N, Miyasaka T, Kuzuhara Y, Murayama S, Ihara Y. 2019. Visualization of Amyloid β deposits in the human brain with matrix-assisted laser desorption/ionization imaging mass spectrometry. J Vis Exp.
  • Jasra SK, Badian C, Macri I, Ra P. 2012. Recognition of early myocardial infarction by immunohistochemical staining with cardiac troponin-I and complement C9. J Forensic Sci. 57(6):1595–1600.
  • Jenkins CP, Cardona DM, Bowers JN, Oliai BR, Allan RW, Normann SJ. 2010. The utility of C4d, C9, and troponin T immunohistochemistry in acute myocardial infarction. Arch Pathol Lab Med. 134:256–263.
  • Ke PC, Zhou R, Serpell LC, Riek R, Knowles TPJ, Lashuel HA, Gazit E, Hamley IW, Davis TP, Fändrich M, et al. 2020. Half a century of amyloids: past, present and future. Chem Soc Rev. 49:5473–5509.
  • Kedia N, Arhzaouy K, Pittman SK, Sun Y, Batchelor M, Weihl CC, Bieschke J. 2019. Desmin forms toxic, seeding-competent amyloid aggregates that persist in muscle fibers. Proc Natl Acad Sci USA. 116:16835–16840.
  • Khan T, Muise ES, Iyengar P, Wang ZV, Chandalia M, Abate N, Zhang BB, Bonaldo P, Chua S, Scherer PE. 2009. Metabolic dysregulation and adipose tissue fibrosis: role of collagen VI. Mol Cell Biol. 29:1575–1591.
  • Kisilevsky R. 2000. The relation of proteoglycans, serum amyloid P and apo E to amyloidosis current status, 2000. Amyloid. 7:23–25.
  • Klein CJ, Vrana JA, Theis JD, Dyck PJ, Dyck PJB, Spinner RJ, Mauermann ML, Bergen HR, III, Zeldenrust SR, Dogan A. 2011. Mass spectrometric-based proteomic analysis of amyloid neuropathy type in nerve tissue. Arch Neurol. 68:195–199.
  • Klimtchuk ES, Prokaeva T, Frame NM, Abdullahi HA, Spencer B, Dasari S, Cui H, Berk JL, Kurtin PJ, Connors LH, et al. 2018. Unusual duplication mutation in a surface loop of human transthyretin leads to an aggressive drug-resistant amyloid disease. Proc Natl Acad Sci USA. 115:E6428–E6436.
  • Kourelis TV, Dasari SS, Dispenzieri A, Maleszewski JJ, Redfield MM, Fayyaz AU, Grogan M, Ramirez-Alvarado M, Abou Ezzeddine OF, McPhail ED. 2020. A proteomic atlas of cardiac amyloid plaques. CardioOncology. 2:632–643.
  • Krance SH, Wu C-Y, Zou Y, Mao H, Toufighi S, He X, Pakosh M, Swardfager W. 2019. The complement cascade in Alzheimer's disease: a systematic review and meta-analysis. Mol Psychiatry.
  • Lavatelli F, Perlman DH, Spencer B, Prokaeva T, McComb ME, Théberge R, Connors LH, Bellotti V, Seldin DC, Merlini G, et al. 2008. Amyloidogenic and associated proteins in systemic amyloidosis proteome of adipose tissue. Mol Cell Proteomics. 7:1570–1583.
  • Lee K-W, Lee D-H, Son H, Kim Y-S, Park J-Y, Roh G-S, Kim H-J, Kang S-S, Cho G-J, Choi W-S. 2009. Clusterin regulates transthyretin amyloidosis. Biochem Biophys Res Commun. 388:256–260.
  • Lepelletier F-X, Mann DMA, Robinson AC, Pinteaux E, Boutin H. 2017. Early changes in extracellular matrix in Alzheimer's disease. Neuropathol Appl Neurobiol. 43:167–182.
  • Lundgren DH, Hwang S-I, Wu L, Han DK. 2014. Role of spectral counting in quantitative proteomics. Expert Rev Proteomics. 7:39–53.
  • Mahmood S, Bridoux F, Venner CP, Sachchithanantham S, Gilbertson JA, Rowczenio D, Wagner T, Sayed R, Patel K, Fontana M, et al. 2015. Natural history and outcomes in localised immunoglobulin light-chain amyloidosis: a long-term observational study. Lancet Haematol. 2(6):e241–e250.
  • Mangione PP, Mazza G, Gilbertson JA, Rendell NB, Canetti D, Giorgetti S, Frenguelli L, Curti M, Rezk T, Raimondi S, et al. 2017. Increasing the accuracy of proteomic typing by decellularisation of amyloid tissue biopsies. J Proteomics. 165:113–118.
  • Mantovani A, Garlanda C, Doni A, Bottazzi B. 2008. Pentraxins in innate immunity: from C-reactive protein to the long pentraxin PTX3. J Clin Immunol. 28:1–13.
  • Martinez JR, Dhawan A, Farach-Carson MC. 2018. Modular proteoglycan perlecan/HSPG2: mutations, Phenotypes, and Functions. Genes. 9(11):556.
  • Merlini G, Bellotti V. 2003. Molecular mechanisms of amyloidosis. N Engl J Med. 349:583–596.
  • Merlini G, Seldin DC, Gertz MA. 2011. Amyloidosis: Pathogenesis and new therapeutic options. J Clin Oncol. 29:1924–1933.
  • Miller DV, Dogan A, Sethi S. 2010. New-onset proteinuria with massive amorphous glomerular deposits. Am J Kidney Dis. 55:749–754.
  • Müller-Eberhard HJ. 1985. The killer molecule of complement. J Invest Dermatol. 85:47s–52s.
  • Narayan P, Orte A, Clarke RW, Bolognesi B, Hook S, Ganzinger KA, Meehan S, Wilson MR, Dobson CM, Klenerman D. 2011. The extracellular chaperone clusterin sequesters oligomeric forms of the amyloid-β(1-40) peptide. Nat Struct Mol Biol. 19:79–83.
  • Nasr SH, Dasari S, Hasadsri L, Theis JD, Vrana JA, Gertz MA, Muppa P, Zimmermann MT, Grogg KL, Dispenzieri A, et al. 2017. Novel type of renal amyloidosis derived from apolipoprotein-CII. J Am Soc Nephrol. 28:439–445.
  • Nasr SH, Dogan A, Larsen CP. 2015. Leukocyte cell-derived chemotaxin 2-associated amyloidosis: a recently recognized disease with distinct clinicopathologic characteristics. Clin J Am Soc Nephrol. 10:2084–2093.
  • Noursadeghi M, Bickerstaff MC, Gallimore JR, Herbert J, Cohen J, Pepys MB. 2000. Role of serum amyloid P component in bacterial infection: Protection of the host or protection of the pathogen. Proc Natl Acad Sci USA. 97:14584–14589.
  • Oskarsson ME, Paulsson JF, Schultz SW, Ingelsson M, Westermark P, Westermark GT. 2015. In vivo seeding and cross-seeding of localized amyloidosis: a molecular link between type 2 diabetes and alzheimer disease. Am J Pathol. 185(3):834–846.
  • Otaka Y, Nakazato Y, Tsutsui T, Tamura J. 2019. Cardiac involvement in heavy and light chain amyloidosis: a case report and literature review. Medicine. 98:e17999.
  • Pepys MB, Booth DR, Hutchinson WL, Gallimore JR, Collins IM, Hohenester E. 1997. Amyloid P component. A Critical Review. Amyloid. 4(4):274–295.
  • Pepys MB, Butler PJG. 1987. Serum amyloid P component is the major calcium-dependent specific DNA binding protein of the serum. Biochem Biophys Res Commun. 148(1):308–313.
  • Pepys MB, Dyck RF, Fc de B, Skinner M, Cohen AS. 1979. Binding of serum amyloid P-component (SAP) by amyloid fibrils. Clin Exp Immunol. 38:284–293.
  • Pepys MB, Herbert J, Hutchinson WL, Tennent GA, Lachmann HJ, Gallimore JR, Lovat LB, Bartfai T, Alanine A, Hertel C, et al. 2002. Targeted pharmacological depletion of serum amyloid P component for treatment of human amyloidosis. Nature. 417:254–259.
  • Pepys MB. 2018. The pentraxins 1975-2018: serendipity, diagnostics and drugs. Front Immunol. 9:2382.
  • Picken MM. 2015. Proteomics and mass spectrometry in the diagnosis of renal amyloidosis. Clin Kidney J. 8(6):665–672.
  • Poulsen ET, Pedersen KW, Marzeda AM, Enghild JJ. 2017. Serum amyloid P Component (SAP) interactome in human plasma containing physiological calcium levels. Biochemistry. 56:896–902.
  • Pozzi A, Yurchenco PD, Iozzo RV. 2017. The nature and biology of basement membranes. Matrix Biol. 57-58:1–11.
  • Puchtler H, Sweat F, Levine M. 1962. On the binding of congo red by amyloid. J Histochem Cytochem. 10(3):355–364.
  • R Core Team 2020. R: A language and environment for statistical computing. R 4.0.0. Vienna, Austria: R Foundation for Statistical Computing. https://www.r-project.org/.
  • Ravindran A, Grogg KL, Domaas DA, Go RS. 2016. Polyclonal localized light chain amyloidosis—a distinct entity? Clin Lymphoma Myeloma Leuk. 16:588–592.
  • Renner B, Tong HH, Laskowski J, Jonscher K, Goetz L, Woolaver R, Hannan J, Li YX, Hourcade D, Pickering MC, et al. 2016. Annexin A2 enhances complement activation by inhibiting factor H. J Immunol. 196:1355–1365.
  • Richards DB, Cookson LM, Barton SV, Liefaard L, Lane T, Hutt DF, Ritter JM, Fontana M, Moon JC, Gillmore JD, et al. 2018. Repeat doses of antibody to serum amyloid P component clear amyloid deposits in patients with systemic amyloidosis. Sci Transl Med. 10(422):eaan3128.
  • Richards DB, Cookson LM, Berges AC, Barton SV, Lane T, Ritter JM, Fontana M, Moon JC, Pinzani M, Gillmore JD, et al. 2015. Therapeutic clearance of amyloid by antibodies to serum amyloid P component. N Engl J Med. 373:1106–1114.
  • Ricklin D, Hajishengallis G, Yang K, Lambris JD. 2010. Complement: a key system for immune surveillance and homeostasis. Nat Immunol. 11:785–797.
  • Rodriguez FJ, Gamez JD, Vrana JA, Theis JD, Giannini C, Scheithauer BW, Parisi JE, Lucchinetti CF, Pendlebury WW, Bergen HR, III, et al. 2008. Immunoglobulin derived depositions in the nervous system: novel mass spectrometry application for protein characterization in formalin-fixed tissues. Lab Invest. 88:1024–1037.
  • Rowczenio D, Dogan A, Theis JD, Vrana JA, Lachmann HJ, Wechalekar AD, Gilbertson JA, Hunt T, Gibbs SDJ, Sattianayagam PT, et al. 2011. Amyloidogenicity and clinical phenotype associated with five novel mutations in apolipoprotein A-I. Am J Pathol. 179:1978–1987.
  • Sethi S, Dasari S, Plaisier E, Ronco P, Nasr SH, Brocheriou I, Theis JD, Vrana JA, Zimmermann MT, Quint PS, et al. 2018. Apolipoprotein CII amyloidosis associated with p.Lys41Thr mutation. Kidney Int Rep. 3:1193–1201.
  • Sethi S, Fervenza FC, Miller D, Norby S, Leung N. 2010. Recurrence of amyloidosis in a kidney transplant. Am J Kidney Dis. 56:394–398.
  • Sethi S, Theis JD, Leung N, Dispenzieri A, Nasr SH, Fidler ME, Cornell LD, Gamez JD, Vrana JA, Dogan A. 2010. Mass spectrometry-based proteomic diagnosis of renal immunoglobulin heavy chain amyloidosis. Clin J Am Soc Nephrol. 5:2180–2187.
  • Sethi S, Theis JD, Quint P, Maierhofer W, Kurtin PJ, Dogan A, Highsmith EW. Jr. 2013. Renal amyloidosis associated with a novel sequence variant of gelsolin. Am J Kidney Dis. 61(1):161–166.
  • Sethi S, Theis JD, Shiller SM, Nast CC, Harrison D, Rennke HG, Vrana JA, Dogan A. 2012. Medullary amyloidosis associated with apolipoprotein A-IV deposition. Kidney Int. 81:201–206.
  • Sethi S, Theis JD, Vrana JA, Fervenza FC, Sethi A, Qian Q, Quint P, Leung N, Dogan A, Nasr SH. 2013. Laser microdissection and proteomic analysis of amyloidosis, cryoglobulinemic GN, fibrillary GN, and immunotactoid glomerulopathy. Clin J Am Soc Nephrol. 8:915–921.
  • Sidiqi MH, McPhail ED, Theis JD, Dasari S, Vrana JA, Drosou ME, Leung N, Hayman S, Rajkumar SV, Warsame R, et al. 2019. Two types of amyloidosis presenting in a single patient: a case series. Blood Cancer J. 9(3):1924.
  • Sjöberg AP, Trouw LA, Blom AM. 2009. Complement activation and inhibition: a delicate balance. Trends Immunol. 30:83–90.
  • Sridharan M, Highsmith WE, Kurtin PJ, Zimmermann MT, Theis JD, Dasari S, Dingli D. 2018. A patient with hereditary ATTR and a novel AGel p.Ala578Pro amyloidosis. Mayo Clin Proc. 93:1678–1682.
  • Stuhlmann-Laeisz C, Schönland SO, Hegenbart U, Oschlies I, Baumgart J-V, Krüger S, Röcken C. 2019. AL amyloidosis with a localized B cell neoplasia. Virchows Arch. 474:353–363.
  • Sun W, Sun J, Zou L, Shen K, Zhong D, Zhou D, Sun W, Li J. 2015. The successful diagnosis and typing of systemic amyloidosis using a microwave-assisted filter-aided fast sample preparation method and LC/MS/MS analysis. PLoS One. 10:e0127180.
  • Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, et al. 2019. STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 47:D607–D613.
  • Theis JD, Dasari S, Vrana JA, Kurtin PJ, Dogan A. 2013. Shotgun-proteomics-based clinical testing for diagnosis and classification of amyloidosis. J Mass Spectrom. 48:1067–1077.
  • UniProt Consortium. 2019. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res. 47:D506–D515.
  • Vrana JA, Gamez JD, Madden BJ, Theis JD, Bergen HR, III, Dogan A. 2009. Classification of amyloidosis by laser microdissection and mass spectrometry-based proteomic analysis in clinical biopsy specimens. Blood. 114:4957–4959.
  • Vrana JA, Theis JD, Dasari S, Mereuta OM, Dispenzieri A, Zeldenrust SR, Gertz MA, Kurtin PJ, Grogg KL, Dogan A. 2014. Clinical diagnosis and typing of systemic amyloidosis in subcutaneous fat aspirates by mass spectrometry-based proteomics. Haematologica. 99:1239–1247.
  • Wickham H, Averick M, Bryan J, Chang W, McGowan L, François R, Grolemund G, Hayes A, Henry L, Hester J, et al. 2019. Welcome to the Tidyverse. JOSS. 4(43):1686.
  • Wickham H. 2016. ggplot2: elegant graphics for data analysis. Cham: Springer. p. 140. p. (Use R!). https://ggplot2.tidyverse.org/.
  • Wilson MR, Yerbury JJ, Poon S. 2008. Potential roles of abundant extracellular chaperones in the control of amyloid formation and toxicity. Mol Biosyst. 4:42–52.
  • Winter M, Tholey A, Kristen A, Röcken C. 2017. MALDI mass spectrometry imaging: a novel tool for the identification and classification of amyloidosis. Proteomics. 17(22):1700236.
  • Winter M, Tholey A, Krüger S, Schmidt H, Röcken C. 2015. MALDI-mass spectrometry imaging identifies vitronectin as a common constituent of amyloid deposits. J Histochem Cytochem. 63:772–779.
  • Wisniewski T, Drummond E. 2020. APOE-amyloid interaction: therapeutic targets. Neurobiol Dis. 138:104784.
  • Yang X, Okamura DM, Lu X, Chen Y, Moorhead J, Varghese Z, Ruan XZ. 2017. CD36 in chronic kidney disease: novel insights and therapeutic opportunities. Nat Rev Nephrol. 13:769–781.
  • Yerbury JJ, Poon S, Meehan S, Thompson B, Kumita JR, Dobson CM, Wilson MR. 2007. The extracellular chaperone clusterin influences amyloid formation and toxicity by interacting with prefibrillar structures. Faseb J. 21:2312–2322.