Multi-omic analyses in Abyssinian cats with primary renal amyloid deposits.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
16 04 2021
Historique:
received: 28 04 2020
accepted: 19 03 2021
entrez: 17 4 2021
pubmed: 18 4 2021
medline: 20 11 2021
Statut: epublish

Résumé

The amyloidoses constitute a group of diseases occurring in humans and animals that are characterized by abnormal deposits of aggregated proteins in organs, affecting their structure and function. In the Abyssinian cat breed, a familial form of renal amyloidosis has been described. In this study, multi-omics analyses were applied and integrated to explore some aspects of the unknown pathogenetic processes in cats. Whole-genome sequences of two affected Abyssinians and 195 controls of other breeds (part of the 99 Lives initiative) were screened to prioritize potential disease-associated variants. Proteome and miRNAome from formalin-fixed paraffin-embedded kidney specimens of fully necropsied Abyssinian cats, three affected and three non-amyloidosis-affected were characterized. While the trigger of the disorder remains unclear, overall, (i) 35,960 genomic variants were detected; (ii) 215 and 56 proteins were identified as exclusive or overexpressed in the affected and control kidneys, respectively; (iii) 60 miRNAs were differentially expressed, 20 of which are newly described. With omics data integration, the general conclusions are: (i) the familial amyloid renal form in Abyssinians is not a simple monogenic trait; (ii) amyloid deposition is not triggered by mutated amyloidogenic proteins but is a mix of proteins codified by wild-type genes; (iii) the form is biochemically classifiable as AA amyloidosis.

Identifiants

pubmed: 33863921
doi: 10.1038/s41598-021-87168-0
pii: 10.1038/s41598-021-87168-0
pmc: PMC8052419
doi:

Substances chimiques

Amyloidogenic Proteins 0
MicroRNAs 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

8339

Investigateurs

Reuben M Buckley (RM)
Danielle Aberdein (D)
Paulo C Alves (PC)
Asa Ohlsson Andersson (AO)
Gregory S Barsh (GS)
Rebecca R Bellone (RR)
Tomas F Bergström (TF)
Adam R Boyko (AR)
Jeffrey A Brockman (JA)
Margret L Casal (ML)
Marta G Castelhano (MG)
Ottmar Distl (O)
Nicholas H Dodman (NH)
N Matthew Ellinwood (NM)
Jonathan E Fogle (JE)
Oliver P Forman (OP)
Dorian J Garrick (DJ)
Edward I Ginns (EI)
Bianca Haase (B)
Jens Häggström (J)
Robert J Harvey (RJ)
Daisuke Hasegawa (D)
Isabel Hernandez (I)
Marjo K Hytönen (MK)
Maria Kaukonen (M)
Christopher B Kaelin (CB)
Tomoki Kosho (T)
Emilie Leclerc (E)
Teri L Lear (TL)
Tosso Leeb (T)
Ronald H L Li (RHL)
Hannes Lohi (H)
Mark A Magnuson (MA)
Richard Malik (R)
Shrinivasrao P Mane (SP)
John S Munday (JS)
William J Murphy (WJ)
Niels C Pedersen (NC)
Simon M Peterson-Jones (SM)
Max F Rothschild (MF)
Clare Rusbridge (C)
Beth Shapiro (B)
Joshua A Stern (JA)
William F Swanson (WF)
Karen A Terio (KA)
Rory J Todhunter (RJ)
Wesley C Warren (WC)
Elizabeth A Wilcox (EA)
Julia H Wildschutte (JH)
Yoshihiko Yu (Y)
Leslie A Lyons (LA)

Références

Holub, D. et al. Mass spectrometry amyloid typing is reproducible across multiple organ sites. BioMed Res. Int. 2019, 1–9 (2019).
doi: 10.1155/2019/3689091
Benson, M. D. et al. Amyloid nomenclature 2018: recommendations by the International Society of Amyloidosis (ISA) nomenclature committee. Amyloid 25, 215–219 (2018).
pubmed: 30614283 doi: 10.1080/13506129.2018.1549825
Merlini, G. et al. Effects of Tafamidis on Transthyretin stabilization and clinical outcomes in patients with non-Val30Met Transthyretin amyloidosis. J. Cardiovasc. Trans. Res. 6, 1011–1020 (2013).
doi: 10.1007/s12265-013-9512-x
Allsop, D. & Mayes, J. Amyloid β-peptide and Alzheimer’s disease. Essays Biochem. 56, 99–110 (2014).
pubmed: 25131589 doi: 10.1042/bse0560099
Elitok, O. M., Elitok, B. & Unver, O. Renal amyloidosis in cattle with inflammatory diseases. J. Vet. Intern. 22, 450–455 (2008).
doi: 10.1111/j.1939-1676.2008.0059.x
Ménsua, C. et al. Pathology of AA amyloidosis in domestic sheep and goats. Vet. Pathol. 40, 71–80 (2003).
pubmed: 12627715 doi: 10.1354/vp.40-1-71
Rideout, B. A. et al. Renal medullary amyloidosis in Dorcas gazelles. Vet. Pathol. 26, 129–135 (1989).
pubmed: 2711570 doi: 10.1177/030098588902600205
Schulze, C. et al. Generalized AA-amyloidosis in Siberian tigers (Panthera tigris altaica) with predominant renal medullary amyloid deposition. Vet. Pathol. 35, 70–74 (1998).
pubmed: 9545138 doi: 10.1177/030098589803500108
Williams, J. H., Van Wilpe, E. & Momberg, M. Renal medullary AA amyloidosis, hepatocyte dissociation and multinucleated hepatocytes in a 14-year-old free-ranging lioness (Panthera leo). J. S. Afr. Vet. Assoc. 76, 90–98 (2005).
pubmed: 16108528 doi: 10.4102/jsava.v76i2.404
Garner, M. M., Raymond, J. T., O’Brien, T. D., Nordhausen, R. W. & Russell, W. C. Amyloidosis in the black-footed ferret (Mustela nigripes). J. Zoo Wildlife Med. 38, 32–41 (2007).
doi: 10.1638/06-023.1
Guo, J.-T., Aldrich, C. E., Mason, W. S. & Pugh, J. C. Characterization of serum amyloid A protein mRNA expression and secondary amyloidosis in the domestic duck. Proc. Natl. Acad. Sci. 93, 14548–14553 (1996).
pubmed: 8962089 doi: 10.1073/pnas.93.25.14548 pmcid: 26170
Ovelgönne, J. H., Landman, W. J., Gruys, E., Gielkens, A. L. & Peeters, B. P. Identical amyloid precursor proteins in two breeds of chickens which differ in susceptibility to develop amyloid arthropathy. Amyloid 8, 41–51 (2001).
pubmed: 11293824 doi: 10.3109/13506120108993813
Andel, A. C. J., Gruys, E., Kroneman, J. & Veerkamp, J. Amyloid in the horse: a report of nine cases. Equine Vet. J. 20, 277–285 (1988).
pubmed: 3168988 doi: 10.1111/j.2042-3306.1988.tb01524.x
Østevik, L., Gunnes, G., de Souza, G. A., Wien, T. N. & Sørby, R. Nasal and ocular amyloidosis in a 15-year-old horse. Acta Vet. Scand. 56, 50 (2014).
pubmed: 25159190 pmcid: 4223893 doi: 10.1186/s13028-014-0050-6
Platz, S. J., Breuer, W., Geisel, O., Linke, R. P. & Hermanns, W. Identification of λ light chain amyloid in eight canine and two feline extramedullary plasmacytomas. J. Comp. Pathol. 116, 45–54 (1997).
pubmed: 9076599 doi: 10.1016/S0021-9975(97)80042-4
Segev, G. et al. Renal amyloidosis in dogs: a retrospective study of 91 cases with comparison of the disease between Shar-Pei and non-Shar-Pei dogs. J. Vet. Intern. Med. 26, 259–268 (2012).
pubmed: 22268374 doi: 10.1111/j.1939-1676.2011.00878.x
Olsson, M. et al. Thorough investigation of a canine Autoinflammatory Disease (AID) confirms one main risk locus and suggests a modifier locus for amyloidosis. PLoS ONE 8, e75242 (2013).
pubmed: 24130694 pmcid: 3793984 doi: 10.1371/journal.pone.0075242
Zhang, B. et al. Characterization of the cheetah serum amyloid A1 Gene: critical role and functional polymorphism of a cis-acting element. J. Hered. 99, 355–363 (2008).
pubmed: 18375929 doi: 10.1093/jhered/esn015
Terio, K. A., O’Brien, T., Lamberski, N., Famula, T. R. & Munson, L. Amyloidosis in Black-footed Cats (Felis nigripes). Vet. Pathol. 45, 393–400 (2008).
pubmed: 18487501 doi: 10.1354/vp.45-3-393
Chew, D. J., DiBartola, S. P., Boyce, J. T. & Gasper, P. W. Renal amyloidosis in related Abyssinian cats. J. Am. Vet. Med. Assoc. 181, 139–142 (1982).
pubmed: 7118693
Boyce, J. T., DiBartola, S. P., Chew, D. J. & Gasper, P. W. Familial renal amyloidosis in Abyssinian cats. Vet. Pathol. 21, 33–38 (1984).
pubmed: 6710810 doi: 10.1177/030098588402100106
van der Linde-Sipman, J. S., Niewold, T. A., Tooten, P. C. J., de Neijs-Backer, M. & Gruys, E. Generalized AA-amyloidosis in Siamese and Oriental cats. Vet. Immunol. Immunop. 56, 1–10 (1997).
doi: 10.1016/S0165-2427(96)05717-0
Niewold, T. A., van der Linde-Sipman, J. S., Murphy, C., Tooten, P. C. & Gruys, E. Familial amyloidosis in cats: Siamese and Abyssinian AA proteins differ in primary sequence and pattern of deposition. Amyloid 6, 205–209 (1999).
pubmed: 10524286 doi: 10.3109/13506129909007328
van Rossum, M. et al. Analysis of cDNA sequences of feline SAAs. Amyloid 11, 38–43 (2004).
pubmed: 15185497 doi: 10.1080/13506120410001676836
DiBartola, S. P., Benson, M. D., Dwulet, F. E. & Cornacoff, J. B. Isolation and characterization of amyloid protein AA in the Abyssinian cat. Lab. Invest. 52, 485–489 (1985).
pubmed: 3990242
Kluve-Beckerman, B., Dwulet, F. E., DiBartonla, S. P. & Benson, M. D. Primary structures of dog and cat amyloid A proteins: comparison to human AA. Comp. Biochem. Phy. B 94, 175–183 (1989).
doi: 10.1016/0305-0491(89)90030-8
Johnson, K. H. et al. Amino acid sequence variations in protein AA of cats with high and low incidences of AA amyloidosis. Comp. Biochem. Physiol. B 94, 765–768 (1989).
pubmed: 2605915 doi: 10.1016/0305-0491(89)90162-4
Lavatelli, F. & Vrana, J. A. Proteomic typing of amyloid deposits in systemic amyloidoses. Amyloid 18, 177–182 (2011).
pubmed: 22080761 doi: 10.3109/13506129.2011.630762
Vrana, J. A. et al. Classification of amyloidosis by laser microdissection and mass spectrometry-based proteomic analysis in clinical biopsy specimens. Blood 114, 4957–4959 (2009).
pubmed: 19797517 doi: 10.1182/blood-2009-07-230722
Klein, C. J. et al. Mass spectrometric-based proteomic analysis of amyloid neuropathy type in nerve tissue. Arch. Neurol. 68, 1 (2011).
doi: 10.1001/archneurol.2010.261
Rowczenio, D. et al. Amyloidogenicity and clinical phenotype associated with five novel mutations in apolipoprotein A-I. Am. J. Pathol. 179, 1978–1987 (2011).
pubmed: 21820994 pmcid: 3181365 doi: 10.1016/j.ajpath.2011.06.024
Sethi, S. et al. Medullary amyloidosis associated with apolipoprotein A-IV deposition. Kidney Int. 81, 201–206 (2012).
pubmed: 21900878 doi: 10.1038/ki.2011.316
Weng, L. et al. Dysregulation of miRNAs in AL amyloidosis. Amyloid 18, 128–135 (2011).
pubmed: 21834602 pmcid: 5615404 doi: 10.3109/13506129.2011.588977
Patel, N. et al. MicroRNAs can regulate human APP levels. Mol. Neurodegener. 3, 10 (2008).
pubmed: 18684319 pmcid: 2529281 doi: 10.1186/1750-1326-3-10
Ichii, O. et al. MicroRNA expression profiling of cat and dog kidneys. Res. Vet. Sci. 96, 299–303 (2014).
pubmed: 24530019 doi: 10.1016/j.rvsc.2014.01.003
Weber, K., Rostert, N., Bauersachs, S. & Wess, G. Serum microRNA profiles in cats with hypertrophic cardiomyopathy. Mol. Cell. Biochem. 402, 171–180 (2015).
pubmed: 25573325 doi: 10.1007/s11010-014-2324-8
Cong, W. et al. Global miRNA expression profiling of domestic cat livers following acute Toxoplasma gondii infection. Oncotarget 8, 1 (2017).
doi: 10.18632/oncotarget.16108
Sun, J. et al. MicroRNA profile analysis of a feline kidney cell line before and after infection with mink enteritis virus. Gene 539, 224–229 (2014).
pubmed: 24525403 doi: 10.1016/j.gene.2014.01.074
Laganà, A. et al. Discovery and characterization of the feline miRNAome. Sci. Rep. 7, 9263 (2017).
pubmed: 28835705 pmcid: 5569061 doi: 10.1038/s41598-017-10164-w
Wright, J. R., Calkins, E. & Humphrey, R. L. Potassium permanganate reaction in amyloidosis. Lab. Invest. 36, 274–281 (1977).
pubmed: 839739
Gandolfi, B. et al. COLQ variant associated with Devon Rex and Sphynx feline hereditary myopathy. Anim. Genet. 46, 711–715 (2015).
pubmed: 26374066 pmcid: 4637250 doi: 10.1111/age.12350
Buckley, R. M. et al. Werewolf, there wolf: variants in Hairless associated with hypotrichia and roaning in the Lykoi cat breed. Genes 11, 682 (2020).
pmcid: 7348984 doi: 10.3390/genes11060682
Buckley, R. M. et al. A new domestic cat genome assembly based on long sequence reads empowers feline genomic medicine and identifies a novel gene for dwarfism. PLoS Genet. 16, e1008926 (2020).
pubmed: 33090996 pmcid: 7581003 doi: 10.1371/journal.pgen.1008926
McLaren, W. et al. The Ensembl Variant Effect Predictor. Genome Biol. 17, 122 (2016).
pubmed: 27268795 pmcid: 4893825 doi: 10.1186/s13059-016-0974-4
Vernocchi, V. et al. Sperm ubiquitination in epididymal feline semen. Theriogenology 82, 636–642 (2014).
pubmed: 24999010 doi: 10.1016/j.theriogenology.2014.06.002
Tedeschi, G. et al. Protein pattern of Xenopus laevis embryos grown in simulated microgravity. Cell Biol. Int. 35, 249–258 (2011).
pubmed: 20946105 doi: 10.1042/CBI20100248
Galli, A. et al. Cluster-assembled zirconia substrates promote long-term differentiation and functioning of human islets of Langerhans. Sci. Rep. 8, 9979 (2018).
pubmed: 29967323 pmcid: 6028636 doi: 10.1038/s41598-018-28019-3
Migliaccio, O. et al. Living in future ocean acidification, physiological adaptive responses of the immune system of sea urchins resident at a CO2 vent system. Sci. Total Environ. 672, 938–950 (2019).
pubmed: 30981169 doi: 10.1016/j.scitotenv.2019.04.005
Mi, H., Muruganujan, A., Casagrande, J. T. & Thomas, P. D. Large-scale gene function analysis with the PANTHER classification system. Nat. Protoc. 8, 1551–1566 (2013).
pubmed: 23868073 pmcid: 6519453 doi: 10.1038/nprot.2013.092
Huang, D. W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009).
doi: 10.1038/nprot.2008.211
Tedeschi, G. et al. Proteomic profile of maternal-aged blastocoel fluid suggests a novel role for ubiquitin system in blastocyst quality. J. Assist. Reprod. Genet. 34, 225–238 (2017).
pubmed: 27924460 doi: 10.1007/s10815-016-0842-x
Vizcaíno, J. A. et al. 2016 update of the PRIDE database and its related tools. Nucl. Acids Res. 44, D447-456 (2016).
pubmed: 26527722 doi: 10.1093/nar/gkv1145
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet j. 17, 10 (2011).
doi: 10.14806/ej.17.1.200
Friedländer, M. R., Mackowiak, S. D., Li, N., Chen, W. & Rajewsky, N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucl. Acids Res. 40, 37–52 (2012).
pubmed: 21911355 doi: 10.1093/nar/gkr688
Griffiths-Jones, S. miRBase: microRNA sequences, targets and gene nomenclature. Nucl. Acids Res. 34, D140–D144 (2006).
pubmed: 16381832 doi: 10.1093/nar/gkj112
Fan, Y. et al. miRNet - dissecting miRNA-target interactions and functional associations through network-based visual analysis. Nucl. Acids Res. 44, W135–W141 (2016).
pubmed: 27105848 doi: 10.1093/nar/gkw288 pmcid: 4987881
Riffo-Campos, Á., Riquelme, I. & Brebi-Mieville, P. Tools for sequence-based miRNA target prediction: what to choose?. Int. J. Mol. Sci. 17, 1987 (2016).
pmcid: 5187787 doi: 10.3390/ijms17121987
Moszyńska, A., Gebert, M., Collawn, J. F. & Bartoszewski, R. SNPs in microRNA target sites and their potential role in human disease. Open Biol. 7, 170019 (2017).
pubmed: 28381629 pmcid: 5413909 doi: 10.1098/rsob.170019
Tasaki, M. et al. Effect of age and sex differences on wild-type transthyretin amyloid formation in familial amyloidotic polyneuropathy: a proteomic approach. Int. J. Cardiol 170, 69–74 (2013).
pubmed: 24182678 doi: 10.1016/j.ijcard.2013.10.033
Lipinski, M. J. et al. The ascent of cat breeds: genetic evaluations of breeds and worldwide random-bred populations. Genomics 91, 12–21 (2008).
pubmed: 18060738 doi: 10.1016/j.ygeno.2007.10.009
Ugurlu, S., Egeli, B. H., Bolayirli, I. M. & Ozdogan, H. Soluble TREM-1 levels in Familial Mediterranean Fever related AA-amyloidosis. Immunol. Invest. 22, 1–9 (2020).
Mereuta, O. M. et al. Systemic AA amyloidosis as a unique manifestation of a combined mutation of TNFRSF1A and MEFV genes. Amyloid 20, 122–126 (2013).
pubmed: 23461592 doi: 10.3109/13506129.2013.775119
Awdishu, L. et al. Identification of maltase glucoamylase as a biomarker of acute kidney injury in patients with cirrhosis. Crit. Care Res. Pract. 2019, 1–8 (2019).
doi: 10.1155/2019/5912804
Zhou, W. et al. FAN1 mutations cause karyomegalic interstitial nephritis, linking chronic kidney failure to defective DNA damage repair. Nat. Genet. 44, 910–915 (2012).
pubmed: 22772369 pmcid: 3412140 doi: 10.1038/ng.2347
Picken, M. M. Non-light-chain immunoglobulin amyloidosis: time to expand or refine the spectrum to include light+heavy chain amyloidosis?. Kidney Int. 83, 353–356 (2013).
pubmed: 23446254 doi: 10.1038/ki.2012.433
Eulitz, M., Weiss, D. T. & Solomon, A. Immunoglobulin heavy-chain-associated amyloidosis. Proc Natl Acad Sci USA 87, 6542–6546 (1990).
pubmed: 2118650 doi: 10.1073/pnas.87.17.6542 pmcid: 54572
Paltrinieri, S., Sironi, G., Giori, L., Faverzani, S. & Longeri, M. Changes in serum and urine SAA concentrations and qualitative and quantitative proteinuria in Abyssinian cats with familial amyloidosis: a five-year longitudinal study (2009–2014). J. Vet. Intern. Med. 29, 505–512 (2015).
pubmed: 25776129 pmcid: 4895502 doi: 10.1111/jvim.12561
Simons, J. P. et al. Pathogenetic mechanisms of amyloid A amyloidosis. Proc. Natl. Acad. Sci. 110, 16115–16120 (2013).
pubmed: 23959890 doi: 10.1073/pnas.1306621110 pmcid: 3791773
Westermark, G. T., Fändrich, M. & Westermark, P. AA amyloidosis: pathogenesis and targeted therapy. Annu Rev Pathol. 10, 321–344 (2015).
pubmed: 25387054 doi: 10.1146/annurev-pathol-020712-163913
Brandan, E. & Inestrosa, N. C. Extracellular matrix components and amyloid in neuritic plaques of Alzheimer’s disease. Gen. Pharmacol. 24, 1063–1068 (1993).
pubmed: 8270163 doi: 10.1016/0306-3623(93)90350-7
Bronfman, F. C., Soto, C., Tapia, L., Tapia, V. & Inestrosa, N. C. Extracellular matrix regulates the amount of the beta-amyloid precursor protein and its amyloidogenic fragments. J. Cell. Physiol. 166, 360–369 (1996).
pubmed: 8591996 doi: 10.1002/(SICI)1097-4652(199602)166:2<360::AID-JCP14>3.0.CO;2-F
Clark, E. A. & Brugge, J. S. Integrins and signal transduction pathways: the road taken. Science 268, 233–239 (1995).
pubmed: 7716514 doi: 10.1126/science.7716514
Exley, C. ATP-promoted amyloidosis of an amyloid beta peptide. NeuroReport 8, 3411–3414 (1997).
pubmed: 9351682 doi: 10.1097/00001756-199710200-00043
Gastineau, D. A., Gertz, M. A., Daniels, T. M., Kyle, R. A. & Bowie, E. J. Inhibitor of the thrombin time in systemic amyloidosis: a common coagulation abnormality. Blood 77, 2637–2640 (1991).
pubmed: 1904284 doi: 10.1182/blood.V77.12.2637.2637
Choufani, E. B. et al. Acquired factor X deficiency in patients with amyloid light-chain amyloidosis: incidence, bleeding manifestations, and response to high-dose chemotherapy. Blood 97, 1885–1887 (2001).
pubmed: 11238135 doi: 10.1182/blood.V97.6.1885
Liu, L., Komatsu, H., Murray, I. V. J. & Axelsen, P. H. Promotion of amyloid beta protein misfolding and fibrillogenesis by a lipid oxidation product. J. Mol. Biol. 377, 1236–1250 (2008).
pubmed: 18304576 doi: 10.1016/j.jmb.2008.01.057
Pathak, B. K., Mondal, S., Banerjee, S., Ghosh, A. N. & Barat, C. Sequestration of ribosome during protein aggregate formation: contribution of ribosomal RNA. Sci. Rep. 7, 42017 (2017).
pubmed: 28169307 pmcid: 5294636 doi: 10.1038/srep42017
Xu, G., Stevens, S. M., Moore, B. D., McClung, S. & Borchelt, D. R. Cytosolic proteins lose solubility as amyloid deposits in a transgenic mouse model of Alzheimer-type amyloidosis. Hum. Mol. Genet. 22, 2765–2774 (2013).
pubmed: 23512986 pmcid: 3690965 doi: 10.1093/hmg/ddt121
Huang, Y., Ren, H. T., Xiong, J. L., Gao, X. C. & Sun, X. H. Identification and characterization of known and novel microRNAs in three tissues of Chinese giant salamander base on deep sequencing approach. Genomics 109, 258–264 (2017).
pubmed: 28476431 doi: 10.1016/j.ygeno.2017.04.007
Adams, D., Koike, H., Slama, M. & Coelho, T. Hereditary transthyretin amyloidosis: a model of medical progress for a fatal disease. Nat. Rev. Neurol. 15, 387–404 (2019).
pubmed: 31209302 doi: 10.1038/s41582-019-0210-4
Winter, R., Kühn, U., Hause, G. & Schwarz, E. Polyalanine-independent conformational conversion of nuclear poly(A)-binding protein 1 (PABPN1). J. Biol. Chem. 287, 22662–22671 (2012).
pubmed: 22570486 pmcid: 3391145 doi: 10.1074/jbc.M112.362327
Stix, B. et al. Proteolysis of AA amyloid fibril proteins by matrix metalloproteinases-1, -2, and -3. Am. J. Pathol. 159, 561–570 (2001).
pubmed: 11485914 pmcid: 1850551 doi: 10.1016/S0002-9440(10)61727-0
Struck, A. K. et al. Complex segregation analysis of familial amyloidosis in Oriental shorthair cats. Vet J. 265, 105552 (2020).
pubmed: 33129552 doi: 10.1016/j.tvjl.2020.105552
Miyazaki, S., Kadota, A., Mitsui, I. & Murakami, T. Amyloid signature proteins in feline amyloidosis. J. Comp. Pathol. 177, 10–17 (2020).
pubmed: 32505236 doi: 10.1016/j.jcpa.2020.03.007

Auteurs

Francesca Genova (F)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Simona Nonnis (S)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Elisa Maffioli (E)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Gabriella Tedeschi (G)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Maria Giuseppina Strillacci (MG)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Michela Carisetti (M)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Giuseppe Sironi (G)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy.

Francesca Anna Cupaioli (FA)

Institute of Biomedical Technologies, National Research Council of Italy (CNR-ITB), 20090, Segrate, Italy.

Noemi Di Nanni (N)

Institute of Biomedical Technologies, National Research Council of Italy (CNR-ITB), 20090, Segrate, Italy.

Alessandra Mezzelani (A)

Institute of Biomedical Technologies, National Research Council of Italy (CNR-ITB), 20090, Segrate, Italy.

Ettore Mosca (E)

Institute of Biomedical Technologies, National Research Council of Italy (CNR-ITB), 20090, Segrate, Italy.

Christopher R Helps (CR)

Langford Vets, University of Bristol, Langford, BS40 5DU, UK.

Peter A J Leegwater (PAJ)

Department of Clinical Sciences of Companion Animals, Utrecht University, 3508 TD, Utrecht, The Netherlands.

Laetitia Dorso (L)

Pathology Service for Large Animals, Ecole Nationale Vétérinaire Oniris, 44300, Nantes, France.

Maria Longeri (M)

Department of Veterinary Medicine, University of Milan, 26900, Lodi, Italy. maria.longeri@unimi.it.

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