MALDI MSI Reveals the Spatial Distribution of Protein Markers in Tracheobronchial Lymph Nodes and Lung of Pigs after Respiratory Infection
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CEITEC 2020 (LQ1601)
Ministry of Education, Youth and Sports of the Czech Republic
AF-IGA-2018-tym005
IGA TP MENDELU
RO0518
Ministry of Agriculture of the Czech Republic
PubMed
33287430
PubMed Central
PMC7730995
DOI
10.3390/molecules25235723
PII: molecules25235723
Knihovny.cz E-zdroje
- Klíčová slova
- Actinobacillus pleuropneumoniae, CD163, MALDI MSI, interleukin 1β, lungs infection, pig model, protegrin‑4 precursor,
- MeSH
- Actinobacillus pleuropneumoniae patogenita MeSH
- antigeny diferenciační myelomonocytární metabolismus MeSH
- biologické markery metabolismus MeSH
- bronchy metabolismus MeSH
- CD antigeny metabolismus MeSH
- infekce bakteriemi rodu Actinobacillus metabolismus mikrobiologie MeSH
- infekce dýchací soustavy metabolismus mikrobiologie MeSH
- interleukin-1beta metabolismus MeSH
- kationické antimikrobiální peptidy metabolismus MeSH
- lymfatické uzliny metabolismus MeSH
- plíce metabolismus MeSH
- prasata MeSH
- receptory buněčného povrchu metabolismus MeSH
- spektrometrie hmotnostní - ionizace laserem za účasti matrice metody MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antigeny diferenciační myelomonocytární MeSH
- biologické markery MeSH
- CD antigeny MeSH
- CD163 Antigen MeSH
- interleukin-1beta MeSH
- kationické antimikrobiální peptidy MeSH
- protegrin-4 MeSH Prohlížeč
- receptory buněčného povrchu MeSH
Respiratory infections are a real threat for humans, and therefore the pig model is of interest for studies. As one of a case for studies, Actinobacillus pleuropneumoniae (APP) caused infections and still worries many pig breeders around the world. To better understand the influence of pathogenic effect of APP on a respiratory system-lungs and tracheobronchial lymph nodes (TBLN), we aimed to employ matrix-assisted laser desorption/ionization time-of-flight mass spectrometry imaging (MALDI-TOF MSI). In this study, six pigs were intranasally infected by APP and two were used as non-infected control, and 48 cryosections have been obtained. MALDI-TOF MSI and immunohistochemistry (IHC) were used to study spatial distribution of infectious markers, especially interleukins, in cryosections of porcine tissues of lungs (necrotic area, marginal zone) and tracheobronchial lymph nodes (TBLN) from pigs infected by APP. CD163, interleukin 1β (IL‑1β) and a protegrin-4 precursor were successfully detected based on their tryptic fragments. CD163 and IL‑1β were confirmed also by IHC. The protegrin-4 precursor was identified by MALDI-TOF/TOF directly on the tissue cryosections. CD163, IL‑1β and protegrin‑4 precursor were all significantly (p < 0.001) more expressed in necrotic areas of lungs infected by APP than in marginal zone, TBLN and in control lungs.
Central European Institute of Technology Brno University of Technology 612 00 Brno Czech Republic
Central European Institute of Technology Mendel University in Brno 613 00 Brno Czech Republic
Department of Immunology Veterinary Research Institute 621 00 Brno Czech Republic
Zobrazit více v PubMed
Li R.W., Wang J.F., Liu L.B., Zhang R.X., Hao X.P., Han Q.G., Wang J.C., Yuan W.Z. Direct detection of Actinobacillus pleuropneumoniae in swine lungs and tonsils by real-time recombinase polymerase amplification assay. Mol. Cell. Probes. 2019;45:14–18. doi: 10.1016/j.mcp.2019.03.007. PubMed DOI
Pereira M.F., Rossi C.C., Seide L.E., Martins S., Dolinski C.D., Bazzolli D.M.S. Antimicrobial resistance, biofilm formation and virulence reveal Actinobacillus pleuropneumoniae strains’ pathogenicity complexity. Res. Vet. Sci. 2018;118:498–501. doi: 10.1016/j.rvsc.2018.05.003. PubMed DOI
Aper D., Frombling J., Bagcioglu M., Ehling-Schulz M., Hennig-Pauka I. Comparison of metabolic adaptation and biofilm formation of Actinobacillus pleuropneumoniae field isolates from the upper and lower respiratory tract of swine with respiratory disease. Vet. Microbiol. 2020;240 doi: 10.1016/j.vetmic.2019.108532. PubMed DOI
Loera-Muro A., Angulo C. New trends in innovative vaccine development against Actinobacillus pleuropneumoniae. Vet. Microbiol. 2018;217:66–75. doi: 10.1016/j.vetmic.2018.02.028. PubMed DOI
Ondrackova P., Leva L., Kucerova Z., Vicenova M., Mensikova M., Faldyna M. Distribution of porcine monocytes in different lymphoid tissues and the lungs during experimental Actinobacillus pleuropneumoniae infection and the role of chemokines. Vet. Res. 2013;44:98. doi: 10.1186/1297-9716-44-98. PubMed DOI PMC
Kowal K., Silver R., Sławińska E., Bielecki M., Chyczewski L., Kowal-Bielecka O. CD163 and its role in inflammation. Folia Histochem. Cytobiol. 2011;49:365–374. doi: 10.5603/FHC.2011.0052. PubMed DOI
Faldyna M., Nechvatalova K., Sinkora J., Knotigova P., Leva L., Krejci J., Toman M. Experimental Actinobacillus pleuropneumoniae infection in piglets with different types and levels of specific protection: Immunophenotypic analysis of lymphocyte subsets in the circulation and respiratory mucosal lymphoid tissue. Vet. Immunol. Immunopathol. 2005;107:143–152. doi: 10.1016/j.vetimm.2005.04.007. PubMed DOI
Sassu E.L., Ladinig A., Talker S.C., Stadler M., Knecht C., Stein H., Frömbling J., Richter B., Spergser J., Ehling-Schulz M., et al. Frequency of Th17 cells correlates with the presence of lung lesions in pigs chronically infected with Actinobacillus pleuropneumoniae. Vet. Res. 2017;48:4. doi: 10.1186/s13567-017-0411-z. PubMed DOI PMC
Auger E., Deslandes V., Ramjeet M., Contreras I., Nash J.H.E., Harel J., Gottschalk M., Olivier M., Jacques M. Host-pathogen interactions of Actinobacillus pleuropneumoniae with porcine lung and tracheal epithelial cells. Infect. Immun. 2009;77:1426–1441. doi: 10.1128/IAI.00297-08. PubMed DOI PMC
Konze S.A., Abraham W.R., Goethe E., Surges E., Kuypers M.M.M., Hoeltig D., Meens J., Vogel C., Stiesch M., Valentin-Weigand P., et al. Link between heterotrophic carbon fixation and virulence in the porcine lung pathogen Actinobacillus pleuropneumoniae. Infect. Immun. 2019;87 doi: 10.1128/IAI.00768-18. PubMed DOI PMC
Xie F., Li G., Zhou L., Zhang Y., Cui N., Liu S., Wang C. Attenuated Actinobacillus pleuropneumoniae double-deletion mutant S-8∆clpP/apxIIC confers protection against homologous or heterologous strain challenge. BMC Vet. Res. 2017;13:14. doi: 10.1186/s12917-016-0928-9. PubMed DOI PMC
Hedegaard J., Skovgaard K., Mortensen S., Sorensen P., Jensen T.K., Hornshoj H., Bendixen C., Heegaard P.M.H. Molecular characterisation of the early response in pigs to experimental infection with Actinobacillus pleuropneumoniae using cDNA microarrays. Acta Vet. Scand. 2007;49 doi: 10.1186/1751-0147-49-11. PubMed DOI PMC
Ondrackova P., Nechvatalova K., Kucerova Z., Leva L., Dominguez J., Faldyna M. Porcine mononuclear phagocyte subpopulations in the lung, blood and bone marrow: Dynamics during inflammation induced by Actinobacillus pleuropneumoniae. Vet. Res. 2010;41 doi: 10.1051/vetres/2010035. PubMed DOI PMC
Baraldi T.G., Cruz N.R.N., Pereira D.A., Galdeano J.V.B., Gatto I.R.H., Silva A.F.D., Panzardi A., Linhares D.C.L., Mathias L.A., de Oliveira L.G. Antibodies against Actinobacillus pleuropneumoniae, Mycoplasma hyopneumoniae and influenza virus and their relationships with risk factors, clinical signs and lung lesions in pig farms with one-site production systems in Brazil. Prev. Vet. Med. 2019;171 doi: 10.1016/j.prevetmed.2019.104748. PubMed DOI
Czyzewska-Dors E., Dors A., Kwit K., Stasiak E., Pomorska-Mol M. Pig lung immune cytokine response to the swine influenza virus and the Actinobacillus pleuropneumoniae infection. J. Vet. Res. 2017;61:259–265. doi: 10.1515/jvetres-2017-0036. PubMed DOI PMC
Lassen B., Geldhof P., Halli O., Vlaminck J., Oliviero C., Orro T., Heinonen M. Anti-Ascaris suum IgG antibodies in fattening pigs with different respiratory conditions. Vet. Parasitol. 2019;265:85–90. doi: 10.1016/j.vetpar.2018.12.005. PubMed DOI
Hoeltig D., Rohde J., Frase R., Nietfeld F., Waldmann K.H., Valentin-Weigand P., Meens J. Multi-organ spreading of Actinobacillus pleuropneumoniae serovar 7 in weaned pigs during the first week after experimental infection. Vet. Res. 2018;49 doi: 10.1186/s13567-018-0592-0. PubMed DOI PMC
Do T., Jarosova R., Smidova L., Guran R., Ondrackova P., Faldyna M., Sladek Z., Zitka O. MALDI-TOF MSI method for determining spatial distribution of infection markers in pulmonary tissues of pigs; Proceedings of the MendelNet 2018—Proceedings of 25th International PhD Students Conference; Brno, Czech Republic. 7–8 November 2018; pp. 495–500.
Jarosova R., Do T., Tesarova B., Smidova V., Guran R., Ondrackova P., Faldyna M., Sladek Z., Zitka O. Determining spatial distribution of interleukin-1β as an infection marker in pulmonary porcine tissues; Proceedings of the MendelNet 2019—Proceedings of 26th International PhD Students Conference; Brno, Czech Republic. 6–7 November 2019; pp. 459–464.
Angel P.M., Caprioli R.M. Matrix-assisted laser desorption ionization imaging mass spectrometry: In situ molecular mapping. Biochemistry. 2013;52:3818–3828. doi: 10.1021/bi301519p. PubMed DOI PMC
Sun C.L., Liu W., Mu Y., Wang X. 1,1′-binaphthyl-2,2′-diamine as a novel MALDI matrix to enhance the in situ imaging of metabolic heterogeneity in lung cancer. Talanta. 2020;209 doi: 10.1016/j.talanta.2019.120557. PubMed DOI
Aichler M., Walch A. MALDI Imaging mass spectrometry: Current frontiers and perspectives in pathology research and practice. Lab. Investig. 2015;95:422–431. doi: 10.1038/labinvest.2014.156. PubMed DOI
Cazares L.H., Troyer D.A., Wang B., Drake R.R., Semmes O.J. MALDI tissue imaging: From biomarker discovery to clinical applications. Anal. Bioanal. Chem. 2011;401:17–27. doi: 10.1007/s00216-011-5003-6. PubMed DOI PMC
Lin L.E., Chen C.L., Huang Y.C., Chung H.H., Lin C.W., Chen K.C., Peng Y.J., Ding S.T., Wang M.Y., Shen T.L., et al. Precision biomarker discovery powered by microscopy image fusion-assisted high spatial resolution ambient ionization mass spectrometry imaging. Anal. Chim. Acta. 2020;1100:75–87. doi: 10.1016/j.aca.2019.11.014. PubMed DOI
Boskamp T., Lachmund D., Casadonte R., Hauberg-Lotte L., Kobarg J.H., Kriegsmann J., Maass P. Using the chemical noise background in MALDI mass spectrometry imaging for mass alignment and calibration. Anal. Chem. 2020;92:1301–1308. doi: 10.1021/acs.analchem.9b04473. PubMed DOI
Maslov D.R., Svirkova A., Allmaier G., Marchetti-Deschamann M., Pavelic S.K. Optimization of MALDI-TOF mass spectrometry imaging for the visualization and comparison of peptide distributions in dry-cured ham muscle fibers. Food Chem. 2019;283:275–286. doi: 10.1016/j.foodchem.2018.12.126. PubMed DOI
Dufresne M., Patterson N.H., Norris J.L., Caprioli R.M. Combining salt doping and matrix sublimation for high spatial resolution MALDI imaging mass spectrometry of neutral lipids. Anal. Chem. 2019;91:12928–12934. doi: 10.1021/acs.analchem.9b02974. PubMed DOI
Shi R., Dai X., Li W.F., Lu F., Liu Y., Qu H.H., Li H., Chen Q.Y., Tian H., Wu E.H., et al. Hydroxyl-group-dominated graphite dots reshape laser desorption/ionization mass spectrometry for small biomolecular analysis and imaging. ACS Nano. 2017;11:9500–9513. doi: 10.1021/acsnano.7b05328. PubMed DOI
Norris J.L., Caprioli R.M. Analysis of tissue specimens by matrix-assisted laser desorption/ionization imaging mass spectrometry in biological and clinical research. Chem. Rev. 2013;113:2309–2342. doi: 10.1021/cr3004295. PubMed DOI PMC
Jung J. Recent advances of MALDI-mass spectrometry imaging in cancer research. Mass Spectrom. Lett. 2019;10:71–78. doi: 10.5478/msl.2019.10.3.71. DOI
Vanickova L., Guran R., Kollár S., Emri G., Krizkova S., Do T., Heger Z., Zitka O., Adam V. Mass spectrometric imaging of cysteine rich proteins in human skin. Int. J. Biol. Macromol. 2019;125:270–277. doi: 10.1016/j.ijbiomac.2018.11.272. PubMed DOI
Guran R., Vanickova L., Horak V., Krizkova S., Michalek P., Heger Z., Zitka O., Adam V. MALDI MSI of MeLiM melanoma: Searching for differences in protein profiles. PLoS ONE. 2017;12:e0189305. doi: 10.1371/journal.pone.0189305. PubMed DOI PMC
Holzlechner M., Strasser K., Zareva E., Steinhäuser L., Birnleitner H., Beer A., Bergmann M., Oehler R., Marchetti-Deschmann M. In situ characterization of tissue-resident immune cells by MALDI mass spectrometry imaging. J. Proteome Res. 2017;16:65–76. doi: 10.1021/acs.jproteome.6b00610. PubMed DOI
Skytthe M.K., Graversen J.H., Moestrup S.K. Targeting of CD163(+) macrophages in inflammatory and malignant diseases. Int. J. Mol. Sci. 2020;21:5497. doi: 10.3390/ijms21155497. PubMed DOI PMC
De Macedo C.S., Anderson D.M., Schey K.L. MALDI (matrix assisted laser desorption ionization) imaging mass spectrometry (IMS) of skin: Aspects of sample preparation. Talanta. 2017;174:325–335. doi: 10.1016/j.talanta.2017.06.018. PubMed DOI
Mutuku S.M., Trim P.J., Prabhala B.K., Irani S., Bremert K.L., Logan J.M., Brooks D.A., Stahl J., Centenera M.M., Snel M.F., et al. Evaluation of small molecule drug uptake in patient-derived prostate cancer explants by mass spectrometry. Sci. Rep. 2019;9:15008. doi: 10.1038/s41598-019-51549-3. PubMed DOI PMC
Hoffmann F., Umbreit C., Krüger T., Pelzel D., Ernst G., Kniemeyer O., Guntinas-Lichius O., Berndt A., von Eggeling F. Identification of proteomic markers in head and neck cancer using MALDI–MS imaging, LC–MS/MS, and immunohistochemistry. Proteom. Clin. Appl. 2019;13:1700173. doi: 10.1002/prca.201700173. PubMed DOI
Kriegsmann M., Zgorzelski C., Casadonte R., Schwamborn K., Muley T., Winter H., Eichhorn M., Eichhorn F., Warth A., Deininger S.O., et al. Mass spectrometry imaging for reliable and fast classification of non-small cell lung cancer subtypes. Cancers. 2020;12:2704. doi: 10.3390/cancers12092704. PubMed DOI PMC
Gour S., Kumar V., Singh A., Gadhave K., Goyal P., Pandey J., Giri R., Yadav J.K. Mammalian antimicrobial peptide protegrin-4 self assembles and forms amyloid-like aggregates: Assessment of its functional relevance. J. Pept. Sci. Off. Publ. Eur. Pept. Soc. 2019;25:e3151. doi: 10.1002/psc.3151. PubMed DOI
Myers M.J., Baarsch M.J., Murtaugh M.P. Effects of pentoxifylline on inflammatory cytokine expression and acute pleuropneumonia in swine. Immunobiology. 2002;205:17–34. doi: 10.1078/0171-2985-00108. PubMed DOI
Balaji R., Wright K.J., Turner J.L., Hill C.M., Dritz S.S., Fenwick B., Carroll J.A., Zannelli M.E., Beausang L.A., Minton J.E. Circulating cortisol, tumor necrosis factor-alpha interleukin-1β, and interferon-gamma in pigs infected with Actinobacillus pleuropneumoniae. J. Anim. Sci. 2002;80:202–207. doi: 10.2527/2002.801202x. PubMed DOI
Zeng F., Dong R., Zhao C.C., Liu D.W., Zheng E.Q., Song C.X., Wu Z.F., Li Z.C. Constitutive expression of antimicrobial peptide PR-39 in transgenic mice significantly enhances resistance to bacterial infection and promotes growth. Transgenic Res. 2018;27:409–422. doi: 10.1007/s11248-018-0084-z. PubMed DOI
Perregaux D.G., Bhavsar K., Contillo L., Shi J.S., Gabel C.A. Antimicrobial peptides initiate IL-1 beta posttranslational processing: A novel role beyond innate immunity. J. Immunol. 2002;168:3024–3032. doi: 10.4049/jimmunol.168.6.3024. PubMed DOI
Dayao D.A.E., Gibson J.S., Blackall P.J., Turni C. Antimicrobial resistance genes in Actinobacillus pleuropneumoniae, Haemophilus parasuis and Pasteurella multocida isolated from Australian pigs. Aust. Vet. J. 2016;94:227–231. doi: 10.1111/avj.12458. PubMed DOI
Ranade S.S., Ramalingam R. A review on bioactive porcine peptide, protegrin-1. Int. J. Pept. Res. 2020;26:1493–1501. doi: 10.1007/s10989-019-09955-8. DOI
Burkard C., Opriessnig T., Mileham A.J., Stadejek T., Ait-Ali T., Lillico S.G., Whitelaw C.B.A., Archibald A.L. Pigs Lacking the scavenger receptor cysteine-rich domain 5 of CD163 are resistant to porcine reproductive and respiratory syndrome virus 1 infection. J. Virol. 2018;92:e00415–e00418. doi: 10.1128/JVI.00415-18. PubMed DOI PMC
Crayne C.B., Albeituni S., Nichols K.E., Cron R.Q. The immunology of macrophage activation syndrome. Front. Immunol. 2019;10 doi: 10.3389/fimmu.2019.00119. PubMed DOI PMC
Chen C., Perry T.L., Chitko-McKown C.G., Smith A.D., Cheung L.M., Beshah E., Urban J.F., Dawson H.D. The regulatory actions of retinoic acid on M2 polarization of porcine macrophages. Dev. Comp. Immunol. 2019;98:20–33. doi: 10.1016/j.dci.2019.03.020. PubMed DOI
McGonagle D., Sharif K., O’Regan A., Bridgewood C. The role of cytokines including interleukin-6 in COVID-19 induced pneumonia and macrophage activation syndrome-like disease. Autoimmun. Rev. 2020;19 doi: 10.1016/j.autrev.2020.102537. PubMed DOI PMC
Merad M., Martin J.C. Pathological inflammation in patients with COVID-19: A key role for monocytes and macrophages. Nat. Rev. Immunol. 2020;20:355–362. doi: 10.1038/s41577-020-0331-4. PubMed DOI PMC
Xu X.L., Han M.F., Li T.T., Sun W., Wang D.S., Fu B.Q., Zhou Y.G., Zheng X.H., Yang Y., Li X.Y., et al. Effective treatment of severe COVID-19 patients with tocilizumab. Proc. Natl. Acad. Sci. USA. 2020;117:10970–10975. doi: 10.1073/pnas.2005615117. PubMed DOI PMC
Tang Y.J., Liu J.J., Zhang D.Y., Xu Z.H., Ji J.J., Wen C.P. Cytokine Storm in COVID-19: The Current evidence and treatment strategies. Front. Immunol. 2020;11:13. doi: 10.3389/fimmu.2020.01708. PubMed DOI PMC
Suckau D., Resemann A., Schuerenberg M., Hufnagel P., Franzen J., Holle A. A novel MALDI LIFT-TOF/TOF mass spectrometer for proteomics. Anal. Bioanal. Chem. 2003;376:952–965. doi: 10.1007/s00216-003-2057-0. PubMed DOI
Kaya I., Michno W., Brinet D., Iacone Y., Zanni G., Blennow K., Zetterberg H., Hanrieder J. Histology-compatible MALDI mass spectrometry based imaging of neuronal lipids for subsequent immunofluorescent staining. Anal. Chem. 2017;89:4685–4694. doi: 10.1021/acs.analchem.7b00313. PubMed DOI