Neutrophil metalloproteinase driven spleen damage hampers infection control of trypanosomiasis.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
05 09 2023
05 09 2023
Historique:
received:
13
01
2023
accepted:
18
08
2023
medline:
7
9
2023
pubmed:
6
9
2023
entrez:
5
9
2023
Statut:
epublish
Résumé
Recent blood transcriptomic analysis of rhodesiense sleeping sickness patients has revealed that neutrophil signature genes and activation markers constitute the top indicators of trypanosomiasis-associated inflammation. Here, we show that Trypanosoma brucei infection results in expansion and differentiation of four splenic neutrophil subpopulations, including Mki67
Identifiants
pubmed: 37669943
doi: 10.1038/s41467-023-41089-w
pii: 10.1038/s41467-023-41089-w
pmc: PMC10480172
doi:
Substances chimiques
Metalloproteases
EC 3.4.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
5418Informations de copyright
© 2023. Springer Nature Limited.
Références
Büscher, P., Cecchi, G., Jamonneau, V. & Priotto, G. Human African trypanosomiasis. Lancet 390, 2397–2409 (2017).
pubmed: 28673422
Kennedy, P. G. Clinical features, diagnosis, and treatment of human African trypanosomiasis (sleeping sickness). Lancet Neurol. 12, 186–194 (2013).
pubmed: 23260189
Pays, E., Radwanska, M. & Magez, S. The pathogenesis of African trypanosomiasis. Annu. Rev. Pathol. Mech. Dis. 18, 19–45 (2023).
Moon, S. et al. Detrimental effect of Trypanosoma brucei brucei infection on memory B cells and host ability to recall protective B-cell responses. J. Infect. Dis. 26, 528–540 (2022).
Nguyen, H. T. T., Guevarra, R. B., Magez, S. & Radwanska, M. Single-cell transcriptome profiling and the use of AID deficient mice reveal that B cell activation combined with antibody class switch recombination and somatic hypermutation do not benefit the control of experimental trypanosomosis. PLoS Pathog. 17, e1010026 (2021).
pubmed: 34762705
pmcid: 8610246
Quintana, J. F. et al. Single cell and spatial transcriptomic analyses reveal microglia-plasma cell crosstalk in the brain during Trypanosoma brucei infection. Nat. Commun. 13, 5752 (2022).
pubmed: 36180478
pmcid: 9525673
Trindade, S. et al. Trypanosoma brucei parasites occupy and functionally adapt to the adipose tissue in mice. Cell Host Microbe 8, 837–848 (2016).
De Vlaminck, K. et al. Differential plasticity and fate of brain-resident and recruited macrophages during the onset and resolution of neuroinflammation. Immunity 8, 2085–2102.e9 (2022).
Briggs, E. M., Rojas, F., McCulloch, R., Matthews, K. R. & Otto, T. D. Single-cell transcriptomic analysis of bloodstream Trypanosoma brucei reconstructs cell cycle progression and developmental quorum sensing. Nat. Commun. 12, 5268 (2021).
pubmed: 34489460
pmcid: 8421343
Mabille, D. et al. Impact of pulmonary African trypanosomes on the immunology and function of the lung. Nat. Commun. 13, 7083 (2022).
pubmed: 36400767
pmcid: 9674601
Stockdale, C., Swiderski, M. R., Barry, J. D. & McCulloch, R. Antigenic variation in Trypanosoma brucei: joining the DOTs. PLoS Biol. 6, e185 (2008).
pubmed: 18666832
pmcid: 2486309
Lecordier, L. et al. The Trypanosoma brucei KIFC1 kinesin ensures the fast antibody clearance required for parasite infectivity. Iscience 23, 101476 (2020).
pubmed: 32889430
pmcid: 7479354
Bartossek, T. et al. Structural basis for the shielding function of the dynamic trypanosome variant surface glycoprotein coat. Nat. Microbiol. 2, 1523–1532 (2017).
pubmed: 28894098
Engstler, M. et al. Hydrodynamic flow-mediated protein sorting on the cell surface of trypanosomes. Cell 131, 505–515 (2007).
pubmed: 17981118
Radwanska, M. et al. Trypanosomiasis-induced B cell apoptosis results in loss of protective anti-parasite antibody responses and abolishment of vaccine-induced memory responses. PLoS Pathog. 4, e1000078 (2008).
pubmed: 18516300
pmcid: 2386555
Bockstal, V. et al. T. brucei infection reduces B lymphopoiesis in bone marrow and truncates compensatory splenic lymphopoiesis through transitional B-cell apoptosis. PLoS Pathog. 7, e1002089 (2011).
pubmed: 21738467
pmcid: 3128123
Macleod, O. J. et al. Invariant surface glycoprotein 65 of Trypanosoma brucei is a complement C3 receptor. Nat. Commun. 13, 5085 (2022).
pubmed: 36038546
pmcid: 9424271
La Greca, F., Haynes, C., Stijlemans, B., De Trez, C. & Magez, S. Antibody‐mediated control of Trypanosoma vivax infection fails in the absence of tumour necrosis factor. Parasite Immunol. 36, 271–276 (2014).
pubmed: 24697754
Deleeuw, V. et al. Trypanosoma brucei brucei causes a rapid and persistent influx of neutrophils in the spleen of infected mice. Parasite Immunol. 41, e12664 (2019).
pubmed: 31325372
pmcid: 6771705
Caljon, G. et al. Neutrophils enhance early Trypanosoma brucei infection onset. Sci. Rep. 8, 11203 (2018).
pubmed: 30046157
pmcid: 6060092
Papayannopoulos, V. Neutrophil extracellular traps in immunity and disease. Nat. Rev. Immunol. 18, 134–147 (2018).
pubmed: 28990587
Naish, E. et al. The formation and function of the neutrophil phagosome. Immunol. Rev. 314, 158–180 (2023).
pubmed: 36440666
Rosales, C. Neutrophil: a cell with many roles in inflammation or several cell types. Front. Physiol. 9, 113 (2018).
pubmed: 29515456
pmcid: 5826082
Lee, I. T., Lin, C. C., Wu, Y. C. & Yang, C. M. TNF‐α induces matrix metalloproteinase‐9 expression in A549 cells: role of TNFR1/TRAF2/PKCα‐dependent signaling pathways. J. Cell Physiol. 224, 454–464 (2010).
pubmed: 20333651
Sheshachalam, A., Srivastava, N., Mitchell, T., Lacy, P. & Eitzen, G. Granule protein processing and regulated secretion in neutrophils. Front. Immunol. 5, 448 (2014).
pubmed: 25285096
pmcid: 4168738
Cabral-Pacheco, G. A. et al. The roles of matrix metalloproteinases and their inhibitors in human diseases. Int. J. Mol. Sci. 21, 9739 (2020).
pubmed: 33419373
pmcid: 7767220
Tiberti, N. et al. New biomarkers for stage determination in Trypanosoma brucei rhodesiense sleeping sickness patients. Clin. Transl. Med. 2, 1 (2013).
pubmed: 23369533
pmcid: 3561069
Mulindwa, J., Matovu, E., Enyaru, J. & Clayton, C. Blood signatures for second stage human African trypanosomiasis: a transcriptomic approach. BMC Med. Genomics 13, 14 (2020).
pubmed: 32000760
pmcid: 6993467
Lin, M. et al. Matrix metalloproteinase-8 facilitates neutrophil migration through the corneal stromal matrix by collagen degradation and production of the chemotactic peptide Pro-Gly-Pro. Am. J. Path. 173, 144–153 (2008).
pubmed: 18556780
pmcid: 2438292
Lokmic, Z. et al. The extracellular matrix of the spleen as a potential organizer of immune cell compartments. Semin. Immunol. 20, 4–13 (2008).
pubmed: 18243017
Zhang, J., Sun, Y. & Zheng, J. The state of art of extracellular traps in protozoan infections. Front. Immunol. 12, 770246 (2021).
pubmed: 34970259
pmcid: 8712655
Grob, D. et al. Trypanosoma brucei brucei induces polymorphonuclear neutrophil activation and neutrophil extracellular traps release. Front. Immunol. 11, 559561 (2020).
pubmed: 33193328
pmcid: 7649812
Zhang, K. et al. Trypanosoma brucei lipophosphoglycan induces the formation of neutrophil extracellular traps and reactive oxygen species burst via toll-like receptor 2, toll-like receptor 4, and c-Jun N-terminal kinase activation. Front. Microbiol. 12, 713531 (2021).
pubmed: 34394064
pmcid: 8355521
Nicolás-Ávila, J. Á., Adrover, J. M. & Hidalgo, A. Neutrophils in homeostasis, immunity, and cancer. Immunity 46, 15–28 (2017).
pubmed: 28099862
Evrard, M. et al. Developmental analysis of bone marrow neutrophils reveals populations specialized in expansion, trafficking, and effector functions. Immunity 48, 364–379 (2018).
pubmed: 29466759
Grieshaber-Bouyer, R. et al. The neutrotime transcriptional signature defines a single continuum of neutrophils across biological compartments. Nat. Commun. 12, 2856 (2021).
pubmed: 34001893
pmcid: 8129206
Xie, X. et al. Single-cell transcriptome profiling reveals neutrophil heterogeneity in homeostasis and infection. Nat. Immunol. 21, 1119–1133 (2020).
pubmed: 32719519
pmcid: 7442692
Nguyen, H. T. T., Radwanska, M. & Magez, S. Tipping the balance between erythroid cell differentiation and induction of anemia in response to the inflammatory pathology associated with chronic trypanosome infections. Front. Immunol. 13, 1051647 (2022).
pubmed: 36420267
pmcid: 9676970
Nguyen H. T. T., Magez S. & Radwanska M. From helping to regulating—a transcriptomic profile of Ifng
Kwok, I. et al. Combinatorial single-cell analyses of granulocyte-monocyte progenitor heterogeneity reveals an early uni-potent neutrophil progenitor. Immunity 53, 303–318 (2020).
pubmed: 32579887
Ren, Y. et al. The type I interferon-IRF7 axis mediates transcriptional expression of Usp25 gene. J. Biol. Chem. 291, 13206–13215 (2016).
pubmed: 27129230
pmcid: 4933234
Meixner, A., Karreth, F., Kenner, L., Penninger, J. M. & Wagner, E. F. Jun and JunD-dependent functions in cell proliferation and stress response. Cell Death Differ. 17, 1409–1419 (2010).
pubmed: 20300111
Gierlikowska, B., Stachura, A., Gierlikowski, W. & Demkov, U. Phagocytosis, degranulation, and extracellular traps released by neutrophils—the current knowledge, pharmacological modulation and future prospects. Front. Farmacol. 12, 666732 (2021).
Dibbert, B. et al. Cytokine-mediated Bax deficiency and consequent delayed neutrophil apoptosis: a general mechanism to accumulate effector cells in inflammation. Proc. Natl Acad. Sci. USA 96, 13330–13335 (1999).
pubmed: 10557320
pmcid: 23947
Jabłońska-Trypuć, A., Matejczyk, M. & Rosochacki, S. Matrix metalloproteinases (MMPs), the main extracellular matrix (ECM) enzymes in collagen degradation, as a target for anticancer drugs. J. Enzym. Inhib. Med. Chem. 31, 177–183 (2016).
Bonnans, C., Chou, J. & Werb, Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 15, 786–801 (2014).
pubmed: 25415508
pmcid: 4316204
Browaeys, R., Saelens, W. & Saeys, Y. NicheNet: modeling intercellular communication by linking ligands to target genes. Nat. Methods 17, 159–162 (2020).
pubmed: 31819264
Coquery, C. M. & Erickson, L. D. Regulatory roles of the tumor necrosis factor receptor BCMA. Crit. Rev. Immunol. 32, 287–305 (2012).
pubmed: 23237506
pmcid: 3548317
Zhang, Y., Li, J., Zhang, Y. M., Zhang, X. M. & Tao, J. Effect of TACI signaling on humoral immunity and autoimmune diseases. J. Immunol. Res. 2015, 247426 (2015).
pubmed: 25866827
pmcid: 4381970
Oliveira, F. L. et al. Galectin-3 regulates peritoneal B1-cell differentiation into plasma cells. Glycobiology 11, 1248–1258 (2009).
Gorina, R., Lyck, R., Vestweber, D. & Engelhardt, B. β2 integrin-mediated crawling on endothelial ICAM-1 and ICAM-2 is a prerequisite for transcellular neutrophil diapedesis across the inflamed blood-brain barrier. J. Immunol. 192, 324–337 (2014).
pubmed: 24259506
Siekacz, K. et al. Soluble ITGaM and ITGb2 integrin subunits are involved in long-term pulmonary complications after COVID-19 infection. J. Clin. Med. 12, 342 (2023).
pubmed: 36615143
pmcid: 9821073
Boumiza, S. et al. MMPs and TIMPs levels are correlated with anthropometric parameters, blood pressure, and endothelial function in obesity. Sci. Rep. 11, 20052 (2021).
pubmed: 34625635
pmcid: 8501083
Forsblom, E., Tervahartiala, T., Ruotsalainen, E., Järvinen, A. & Sorsa, T. Matrix metalloproteinase MMP-8, TIMP-1 and MMP-8/TIMP-1 ratio in plasma in methicillin-sensitive Staphylococcus aureus bacteremia. PLoS ONE 16, e0252046 (2021).
pubmed: 34043679
pmcid: 8158883
Papayannopoulos, V., Metzler, K. D., Hakkim, A. & Zychlinsky, A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 191, 677–691 (2010).
pubmed: 20974816
pmcid: 3003309
Giaglis, S. et al. Multimodal regulation of NET formation in pregnancy: progesterone antagonizes the pro-NETotic effect of estrogen and G-CSF. Front. Immunol. 7, 565 (2016).
pubmed: 27994595
pmcid: 5136684
Metzler, K. D., Goosmann, C., Lubojemska, A., Zychlinsky, A. & Papayannopoulos, V. A myeloperoxidase-containing complex regulates neutrophil elastase release and actin dynamics during NETosis. Cell Rep. 8, 883–896 (2014).
pubmed: 25066128
pmcid: 4471680
Dyugovskaya, L., Polyakov, A., Cohen-Kaplan, V., Lavie, P. & Lavie, L. Bax/Mcl-1 balance affects neutrophil survival in intermittent hypoxia and obstructive sleep apnea: effects of p38MAPK and ERK1/2 signaling. J. Transl. Med. 10, 211 (2012).
pubmed: 23088735
pmcid: 3543281
Murphy, M. P. & Caraher, E. Mcl-1 is vital for neutrophil survival. Immunol. Res. 62, 225–233 (2015).
pubmed: 25929430
Ai, Z. Revealing key regulators of neutrophil function during inflammation by re-analysing single-cell RNA-seq. PloS ONE 17, e0276460 (2022).
pubmed: 36269754
pmcid: 9586406
Charzewski, Ł., Krzyśko, K. A. & Lesyng, B. Structural characterisation of inhibitory and non-inhibitory MMP-9–TIMP-1 complexes and implications for regulatory mechanisms of MMP-9. Sci. Rep. 11, 13376 (2021).
pubmed: 34183752
pmcid: 8238946
Thirkettle, S. et al. Matrix metalloproteinase 8 (collagenase 2) induces the expression of interleukins 6 and 8 in breast cancer cells. J. Biol. Chem. 288, 16282–16294 (2013).
pubmed: 23632023
pmcid: 3675567
Garratt, L. W. et al. Matrix metalloproteinase activation by free neutrophil elastase contributes to bronchiectasis progression in early cystic fibrosis. Eur. Respir. J. 46, 384–394 (2015).
pubmed: 25929954
Rydzynska, Z., Pawlik, B., Krzyzanowski, D., Mlynarski, W. & Madzio, J. Neutrophil elastase defects in congenital neutropenia. Front. Immunol. 12, 653932 (2021).
pubmed: 33968054
pmcid: 8100030
Ren, Z., Spaargaren, M. & Pals, S. T. Syndecan-1 and stromal heparan sulfate proteoglycans: key moderators of plasma cell biology and myeloma pathogenesis. Blood 137, 1713–1718 (2021).
pubmed: 33512430
pmcid: 8405055
McCarron, M. J., Park, P. W. & Fooksman, D. R. CD138 mediates selection of mature plasma cells by regulating their survival. Blood 129, 2749–2759 (2017).
pubmed: 28381397
pmcid: 5437827
Yang, N. & Friedl, A. Syndecan-1-induced ECM fiber alignment requires integrin αvβ3 and syndecan-1 ectodomain and heparan sulfate chains. PloS ONE11, e0150132 (2016).
pubmed: 26909794
pmcid: 4766302
Song, J. et al. Extracellular matrix of secondary lymphoid organs impacts on B-cell fate and survival. Proc. Natl Acad. Sci. USA 110, E2915–E2924 (2013).
pubmed: 23847204
pmcid: 3732919
Schrock, D. C. et al. Pivotal role for αV integrins in sustained Tfh support of the germinal center response for long-lived plasma cell generation. Proc. Natl Acad. Sci. USA 116, 4462–4470 (2019).
pubmed: 30770452
pmcid: 6410787
Young, M. D. & Behjati, S. SoupX removes ambient RNA contamination from droplet-based single-cell RNA sequencing data. Gigascience 9, giaa151 (2020).
pubmed: 33367645
pmcid: 7763177
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).
pubmed: 29608179
pmcid: 6700744
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902 (2019).
pubmed: 31178118
pmcid: 6687398
Kimmel, J. C., Hwang, A. B., Scaramozza, A., Marshall, W. F. & Brack, A. S. Aging induces aberrant state transition kinetics in murine muscle stem cells. Development 147, dev183855 (2020).
pubmed: 32198156
pmcid: 7225128
Aran, D. et al. Reference-based analysis of lung single-cell sequencing reveals a transitional profibrotic macrophage. Nat. Immunol. 20, 163–172 (2019).
pubmed: 30643263
pmcid: 6340744
Satija, R., Farrell, J. A., Gennert, D., Schier, A. F. & Regev, A. Spatial reconstruction of single-cell gene expression data. Nat. Biotechnol. 33, 495–502 (2015).
pubmed: 25867923
pmcid: 4430369
Trapnell, C. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381–386 (2014).
pubmed: 24658644
pmcid: 4122333
Korsunsky, I. et al. Fast, sensitive and accurate integration of single-cell data with Harmony. Nat. Methods 12, 1289–1296 (2019).