Dissecting thrombus-directed chemotaxis and random movement in neutrophil near-thrombus motion in flow chambers.
Chemotaxis
Hemostasis
Neutrophils
Platelets
Thromboinflammation
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
20 May 2024
20 May 2024
Historique:
received:
23
11
2023
accepted:
08
05
2024
medline:
20
5
2024
pubmed:
20
5
2024
entrez:
19
5
2024
Statut:
epublish
Résumé
Thromboinflammation is caused by mutual activation of platelets and neutrophils. The site of thromboinflammation is determined by chemoattracting agents release by endothelium, immune cells, and platelets. Impaired neutrophil chemotaxis contributes to the pathogenesis of Shwachman-Diamond syndrome (SDS). In this hereditary disorder, neutrophils are known to have aberrant chemoattractant-induced F-actin properties. Here, we aim to determine whether neutrophil chemotaxis could be analyzed using our previously developed ex vivo assay of the neutrophils crawling among the growing thrombi. Adult and pediatric healthy donors, alongside with pediatric patients with SDS, were recruited for the study. Thrombus formation and granulocyte movement in hirudinated whole blood were visualized by fluorescent microscopy in fibrillar collagen-coated parallel-plate flow chambers. Alternatively, fibrinogen, fibronectin, vWF, or single tumor cells immobilized on coverslips were used. A computational model of chemokine distribution in flow chamber with a virtual neutrophil moving in it was used to analyze the observed data. The movement of healthy donor neutrophils predominantly occurred in the direction and vicinity of thrombi grown on collagen or around tumor cells. For SDS patients or on coatings other than collagen, the movement was characterized by randomness and significantly reduced velocities. Increase in wall shear rates to 300-500 1/s led to an increase in the proportion of rolling neutrophils. A stochastic algorithm simulating leucocyte chemotaxis movement in the calculated chemoattractant field could reproduce the experimental trajectories of moving neutrophils for 72% of cells. In samples from healthy donors, but not SDS patients, neutrophils move in the direction of large, chemoattractant-releasing platelet thrombi growing on collagen.
Sections du résumé
BACKGROUND
BACKGROUND
Thromboinflammation is caused by mutual activation of platelets and neutrophils. The site of thromboinflammation is determined by chemoattracting agents release by endothelium, immune cells, and platelets. Impaired neutrophil chemotaxis contributes to the pathogenesis of Shwachman-Diamond syndrome (SDS). In this hereditary disorder, neutrophils are known to have aberrant chemoattractant-induced F-actin properties. Here, we aim to determine whether neutrophil chemotaxis could be analyzed using our previously developed ex vivo assay of the neutrophils crawling among the growing thrombi.
METHODS
METHODS
Adult and pediatric healthy donors, alongside with pediatric patients with SDS, were recruited for the study. Thrombus formation and granulocyte movement in hirudinated whole blood were visualized by fluorescent microscopy in fibrillar collagen-coated parallel-plate flow chambers. Alternatively, fibrinogen, fibronectin, vWF, or single tumor cells immobilized on coverslips were used. A computational model of chemokine distribution in flow chamber with a virtual neutrophil moving in it was used to analyze the observed data.
RESULTS
RESULTS
The movement of healthy donor neutrophils predominantly occurred in the direction and vicinity of thrombi grown on collagen or around tumor cells. For SDS patients or on coatings other than collagen, the movement was characterized by randomness and significantly reduced velocities. Increase in wall shear rates to 300-500 1/s led to an increase in the proportion of rolling neutrophils. A stochastic algorithm simulating leucocyte chemotaxis movement in the calculated chemoattractant field could reproduce the experimental trajectories of moving neutrophils for 72% of cells.
CONCLUSIONS
CONCLUSIONS
In samples from healthy donors, but not SDS patients, neutrophils move in the direction of large, chemoattractant-releasing platelet thrombi growing on collagen.
Identifiants
pubmed: 38764040
doi: 10.1186/s12915-024-01912-2
pii: 10.1186/s12915-024-01912-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
115Subventions
Organisme : Russian Science Foundation
ID : 23-45-10039
Informations de copyright
© 2024. The Author(s).
Références
Hidalgo A, Chilvers ER, Summers C, Koenderman L. The neutrophil life cycle. Trends Immunol. 2019;40(7):584–97.
pubmed: 31153737
doi: 10.1016/j.it.2019.04.013
Puhr-Westerheide D, Schink SJ, Fabritius M, Mittmann L, Hessenauer MET, Pircher J, et al. Neutrophils promote venular thrombosis by shaping the rheological environment for platelet aggregation. Sci Rep. 2019;9(1):15932.
pubmed: 31685838
pmcid: 6828708
doi: 10.1038/s41598-019-52041-8
Margraf A, Ley K, Zarbock A. Neutrophil recruitment: from model systems to tissue-specific patterns. Trends Immunol. 2019;40(7):613–34.
pubmed: 31175062
pmcid: 6745447
doi: 10.1016/j.it.2019.04.010
Szatmary AC, Nossal R, Parent CA, Majumdar R. Modeling neutrophil migration in dynamic chemoattractant gradients: assessing the role of exosomes during signal relay. Mogilner A, editor. MBoC. 2017;28(23):3457–70.
Schattner M, Jenne CN, Negrotto S, Ho-Tin-Noe B. Editorial: Platelets and immune responses during thromboinflammation. Front Immunol. 2020;11:1079.
pubmed: 32547562
pmcid: 7270277
doi: 10.3389/fimmu.2020.01079
Tanguay JF, Geoffroy P, Dorval JF, Sirois M. Percutaneous endoluminal arterial cryoenergy improves vascular remodelling after angioplasty. Thromb Haemost. 2004;92(11):1114–21.
pubmed: 15543341
doi: 10.1160/TH04-06-0336
Darbousset R, Mezouar S, Dignat-George F, Panicot-Dubois L, Dubois C. Involvement of neutrophils in thrombus formation in living mice. Pathol Biol (Paris). 2014;62(1):1–9.
pubmed: 24485849
doi: 10.1016/j.patbio.2013.11.002
Engelmann B, Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat Rev Immunol. 2013;13(1):34–45.
pubmed: 23222502
doi: 10.1038/nri3345
Massberg S, Grahl L, von Bruehl ML, Manukyan D, Pfeiler S, Goosmann C, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med. 2010;16(8):887–96.
pubmed: 20676107
doi: 10.1038/nm.2184
An OI, Martyanov AA, Stepanyan MG, Boldova AE, Rumyantsev SA, Panteleev MA, et al. Platelets in COVID-19: “innocent by-standers” or active participants? Voprosy gematologii/onkologii i immunopatologii v pediatrii. 2021;20(1):184–91.
doi: 10.24287/1726-1708-2021-20-1-184-191
Sveshnikova A, Stepanyan M, Panteleev M. Platelet functional responses and signalling: the molecular relationship. Part 1: responses. Syst Biol Physiol Rep. 2021;1(1):20.
Jr JEI, Battinelli EM. Selective sorting of alpha-granule proteins. J Thromb Haemost. 2009;7:173–6.
doi: 10.1111/j.1538-7836.2009.03387.x
Parsons MEM, Szklanna PB, Guerrero JA, Wynne K, Dervin F, O’Connell K, et al. Platelet releasate proteome profiling reveals a core set of proteins with low variance between healthy adults. Proteomics. 2018;18(15): e1800219.
pubmed: 29932309
doi: 10.1002/pmic.201800219
Woulfe D, Yang J, Brass L. ADP and platelets: the end of the beginning. J Clin Invest. 2001;107(12):1503–5.
pubmed: 11413156
pmcid: 200202
doi: 10.1172/JCI13361
Labelle M, Begum S, Hynes RO. Platelets guide the formation of early metastatic niches. Proc Natl Acad Sci U S A. 2014;111(30):E3053-3061.
pubmed: 25024172
pmcid: 4121772
doi: 10.1073/pnas.1411082111
Bizios R, Lai L, Fenton JW, Malik AB. Thrombin-induced chemotaxis and aggregation of neutrophils. J Cell Physiol. 1986;128(3):485–90.
pubmed: 3745283
doi: 10.1002/jcp.1041280318
Levi M, van der Poll T. Coagulation and sepsis. Thromb Res. 2017;149:38–44.
pubmed: 27886531
doi: 10.1016/j.thromres.2016.11.007
Morozova DS, Martyanov AA, Obydennyi SI, Korobkin JJD, Sokolov AV, Shamova EV, et al. Ex vivo observation of granulocyte activity during thrombus formation. BMC Biol. 2022;20(1):32.
pubmed: 35125118
pmcid: 8819951
doi: 10.1186/s12915-022-01238-x
Kawashima N, Oyarbide U, Cipolli M, Bezzerri V, Corey SJ. Shwachman-Diamond syndromes: clinical, genetic, and biochemical insights from the rare variants. Haematologica. 2023;108(10):2594–605.
pubmed: 37226705
pmcid: 10543188
doi: 10.3324/haematol.2023.282949
Burroughs L, Woolfrey A, Shimamura A. Shwachman Diamond syndrome – a review of the clinical presentation, molecular pathogenesis, diagnosis, and treatment. Hematol Oncol Clin North Am. 2009;23(2):233–48.
pubmed: 19327581
pmcid: 2754297
doi: 10.1016/j.hoc.2009.01.007
Stepanovic V, Wessels D, Goldman FD, Geiger J, Soll DR. The chemotaxis defect of Shwachman-Diamond syndrome leukocytes. Cell Motil Cytoskeleton. 2004;57(3):158–74.
pubmed: 14743349
doi: 10.1002/cm.10164
Orelio C, Kuijpers TW. Shwachman-Diamond syndrome neutrophils have altered chemoattractant-induced F-actin polymerization and polarization characteristics. Haematologica. 2009;94(3):409–13.
pubmed: 19211642
pmcid: 2649349
doi: 10.3324/haematol.13733
Martinod K, Demers M, Fuchs TA, Wong SL, Brill A, Gallant M, et al. Neutrophil histone modification by peptidylarginine deiminase 4 is critical for deep vein thrombosis in mice. Proc Natl Acad Sci U S A. 2013;110(21):8674–9.
pubmed: 23650392
pmcid: 3666755
doi: 10.1073/pnas.1301059110
Sveshnikova A, Adamanskaya E, Panteleev M. Conditions for the implementation of the phenomenon of programmed death of neutrophils with the appearance of DNA extracellular traps (“NET-osis”) during thrombus formation. Pediatric Hematology/Oncology and Immunopathology. 2024;23(1):211–8.
doi: 10.24287/1726-1708-2024-23-1-211-218
Wyant T, Fedyk E, Abhyankar B. An overview of the mechanism of action of the monoclonal antibody vedolizumab. Journal of Crohn’s and Colitis. 2016;10(12):1437–44.
pubmed: 27252400
doi: 10.1093/ecco-jcc/jjw092
Sirotkina OV, Khaspekova SG, Zabotina AM, Shimanova YV, Mazurov AV. Effects of platelet glycoprotein IIb-IIIa number and glycoprotein IIIa Leu33Pro polymorphism on platelet aggregation and sensitivity to glycoprotein IIb-IIIa antagonists. Platelets. 2007;18(7):506–14.
pubmed: 17957566
doi: 10.1080/09537100701326739
Lämmermann T, Kastenmüller W. Concepts of GPCR -controlled navigation in the immune system. Immunol Rev. 2019;289(1):205–31.
pubmed: 30977203
pmcid: 6487968
doi: 10.1111/imr.12752
Hasçelik G, ŞLener B, Hasçelik Z. Effect of some anti-inflammatory drugs on human neutrophil chemotaxis. J Int Med Res. 1994;22(2):100–6.
pubmed: 8020636
doi: 10.1177/030006059402200206
Kendrick AA, Holliday MJ, Isern NG, Zhang F, Camilloni C, Huynh C, et al. The dynamics of interleukin-8 and its interaction with human CXC receptor I peptide. Protein Sci. 2014;23(4):464–80.
pubmed: 24442768
pmcid: 3970897
doi: 10.1002/pro.2430
Thomson AW, Lotze MT. The cytokine handbook. 4th ed. 1–1396. Amsterdam [etc.]: Academic press, an imprint of Elsevier science; 2003.
Joshi N, Kumar D, Poluri KM. Elucidating the molecular interactions of chemokine CCL2 orthologs with flavonoid baicalin. ACS Omega. 2020;5(35):22637–51.
pubmed: 32923824
pmcid: 7482410
doi: 10.1021/acsomega.0c03428
Cognasse F, Duchez AC, Audoux E, Ebermeyer T, Arthaud CA, Prier A, et al. Platelets as key factors in inflammation: focus on CD40L/CD40. Front Immunol. 2022;13: 825892.
pubmed: 35185916
pmcid: 8850464
doi: 10.3389/fimmu.2022.825892
Wang F. The signaling mechanisms underlying cell polarity and chemotaxis. Cold Spring Harb Perspect Biol. 2009;1(4): a002980.
pubmed: 20066099
pmcid: 2773618
doi: 10.1101/cshperspect.a002980
Kasper B, Brandt E, Bulfone-Paus S, Petersen F. Platelet factor 4 (PF-4)-induced neutrophil adhesion is controlled by src-kinases, whereas PF-4-mediated exocytosis requires the additional activation of p38 MAP kinase and phosphatidylinositol 3-kinase. Blood. 2004;103(5):1602–10.
pubmed: 14592823
doi: 10.1182/blood-2003-08-2802
Liu Z, Li L, Zhang H, Pang X, Qiu Z, Xiang Q, et al. Platelet factor 4 (PF4) and its multiple roles in diseases. Blood Reviews. 2023;101155.
Ward Y, Lake R, Faraji F, Sperger J, Martin P, Gilliard C, et al. Platelets promote metastasis via binding tumor CD97 leading to bidirectional signaling that coordinates transendothelial migration. Cell Rep. 2018;23(3):808–22.
pubmed: 29669286
pmcid: 6574118
doi: 10.1016/j.celrep.2018.03.092
SenGupta S, Hein LE, Parent CA. The recruitment of neutrophils to the tumor microenvironment is regulated by multiple mediators. Front Immunol. 2021;12: 734188.
pubmed: 34567000
pmcid: 8461236
doi: 10.3389/fimmu.2021.734188
Kovalenko TA, Panteleev MA, Sveshnikova AN. The role of tissue factor in metastasising, neoangiogenesis and hemostasis in cancer. Oncohematology. 2019;14(2):70–85.
doi: 10.17650/1818-8346-2019-14-2-70-85
Ananthanarayanan B, Kim Y, Kumar S. Elucidating the mechanobiology of malignant brain tumors using a brain matrix-mimetic hyaluronic acid hydrogel platform. Biomaterials. 2011;32(31):7913–23.
pubmed: 21820737
pmcid: 3159794
doi: 10.1016/j.biomaterials.2011.07.005
Astarita JL, Acton SE, Turley SJ. Podoplanin: emerging functions in development, the immune system, and cancer. Frontiers in Immunology. 2012;3(SEP):1–11.
Martyanov AA, Tesakov IP, Khachatryan LA, An OI, Boldova AE, Ignatova AA, et al. Platelet functional abnormalities in pediatric patients with kaposiform hemangioendothelioma/Kasabach-Merritt phenomenon. Blood Adv. 2023;7(17):4936–49.
pubmed: 37307200
pmcid: 10463204
doi: 10.1182/bloodadvances.2022009590
O’Sullivan JM, Preston RJS, Robson T, O’Donnell JS. emerging roles for von Willebrand factor in cancer cell biology. Semin Thromb Hemost. 2018;44(2):159–66.
pubmed: 29165741
doi: 10.1055/s-0037-1607352
Rankin EB, Erler J, Giaccia AJ. 3 - The cellular microenvironment and metastases. In: Niederhuber JE, Armitage JO, Doroshow JH, Kastan MB, Tepper JE, editors. Abeloff’s Clinical Oncology. 5th ed. Philadelphia: Churchill Livingstone; 2014. p. 40- 51.e4.
doi: 10.1016/B978-1-4557-2865-7.00003-5
Schönichen C, Montague SJ, Brouns SLN, Burston JJ, Cosemans JMEM, Jurk K, et al. Antagonistic roles of human platelet integrin αIIbβ3 and chemokines in regulating neutrophil activation and fate on arterial thrombi under flow. Arterioscler Thromb Vasc Biol. 2023;43(9):1700–12.
pubmed: 37409530
pmcid: 10443630
doi: 10.1161/ATVBAHA.122.318767
Weyrich AS, Elstad MR, McEver RP, McIntyre TM, Moore KL, Morrissey JH, et al. Activated platelets signal chemokine synthesis by human monocytes. J Clin Invest. 1996;97(6):1525–34.
pubmed: 8617886
pmcid: 507213
doi: 10.1172/JCI118575
Okajima K, Harada N, Kushimoto S, Uchiba M. Role of microthrombus formation in the development of ischemia/reperfusion-induced liver injury in rats. Thromb Haemost. 2002;88(9):473–80.
pubmed: 12353078
doi: 10.1055/s-0037-1613240
Stewart GJ. Neutrophils and deep venous thrombosis. Pathophysiol Haemost Thromb. 2009;23(Suppl. 1):127–40.
doi: 10.1159/000216922
Panteleev MA, Korin N, Reesink KD, Bark DL, Cosemans JMEM, Gardiner EE, et al. Wall shear rates in human and mouse arteries: Standardization of hemodynamics for in vitro blood flow assays: Communication from the ISTH SSC subcommittee on biorheology. J Thromb Haemost. 2021;19(2):588–95.
pubmed: 34396692
doi: 10.1111/jth.15174
Vicker MG, Lackie JM, Schill W. Neutrophil leucocyte chemotaxis is not induced by a spatial gradient of chemoattractant. J Cell Sci. 1986;84:263–80.
pubmed: 3805156
doi: 10.1242/jcs.84.1.263
Nelson AS, Myers KC. Diagnosis, treatment, and molecular pathology of Shwachman-Diamond syndrome. Hematol Oncol Clin North Am. 2018;32(4):687–700.
pubmed: 30047420
doi: 10.1016/j.hoc.2018.04.006
Dunster JL, Panteleev MA, Gibbins JM, Sveshnikova AN. Mathematical techniques for understanding platelet regulation and the development of new pharmacological approaches. Methods Mol Biol. 2018;1812:255–79.
pubmed: 30171583
doi: 10.1007/978-1-4939-8585-2_15
Belyaev AV, Dunster JL, Gibbins JM, Panteleev MA, Volpert V. Modeling thrombosis in silico: frontiers, challenges, unresolved problems and milestones. Phys Life Rev. 2018;26–27:57–95.
pubmed: 29550179
doi: 10.1016/j.plrev.2018.02.005
Kaneva VN, Dunster JL, Volpert V, Ataullahanov F, Panteleev MA, Nechipurenko DY. Modeling thrombus shell: linking adhesion receptor properties and macroscopic dynamics. Biophys J. 2021;120(2):334–51.
pubmed: 33472026
pmcid: 7840445
doi: 10.1016/j.bpj.2020.10.049
Mandel J, Casari M, Stepanyan M, Martyanov A, Deppermann C. Beyond hemostasis: platelet innate immune interactions and thromboinflammation. Int J Mol Sci. 2022;23(7):3868.
pubmed: 35409226
pmcid: 8998935
doi: 10.3390/ijms23073868
Metzemaekers M, Gouwy M, Proost P. Neutrophil chemoattractant receptors in health and disease: double-edged swords. Cell Mol Immunol. 2020;17(5):433–50.
pubmed: 32238918
pmcid: 7192912
doi: 10.1038/s41423-020-0412-0
Eash KJ, Means JM, White DW, Link DC. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood. 2009;113(19):4711–9.
pubmed: 19264920
pmcid: 2680371
doi: 10.1182/blood-2008-09-177287
Marin-Esteban V, Youn J, Beaupain B, Jaracz-Ros A, Barlogis V, Fenneteau O, et al. Biallelic CXCR2 loss-of-function mutations define a distinct congenital neutropenia entity. Haematol. 2021;107(3):765–9.
doi: 10.3324/haematol.2021.279254
Tokarev AA, Butylin AA, Ataullakhanov FI. Platelet adhesion from shear blood flow is controlled by near-wall rebounding collisions with erythrocytes. Biophys J. 2011;100(4):799–808.
pubmed: 21320422
pmcid: 3037552
doi: 10.1016/j.bpj.2010.12.3740
Matzner Y, Marx G, Drexler R, Eldor A. The inhibitory effect of heparin and related glycosaminoglycans on neutrophil chemotaxis. Thromb Haemost. 1984;52(2):134–7.
pubmed: 6084320
doi: 10.1055/s-0038-1661157
Nechipurenko DY, Receveur N, Yakimenko AO, Shepelyuk TO, Yakusheva AA, Kerimov RR, et al. Clot contraction drives the translocation of procoagulant platelets to thrombus surface. Arterioscler Thromb Vasc Biol. 2019;39(1):37–47.
pubmed: 30580561
doi: 10.1161/ATVBAHA.118.311390
Van Kruchten R, Cosemans JMEM, Heemskerk JWM. Measurement of whole blood thrombus formation using parallel-plate flow chambers - a practical guide. Platelets. 2012;23(3):229–42.
pubmed: 22502645
doi: 10.3109/09537104.2011.630848
Balabin FA. Quantitative assessment of heterogeneity of single platelet calcium responses to activation. Res Pract Thromb Haemost. 2021;5(Suppl 2):PB1027.
Crocker JC, Hoffman BD. Multiple-particle tracking and two-point microrheology in cells. Methods Cell Biol. 2007;83:141–78.
pubmed: 17613308
doi: 10.1016/S0091-679X(07)83007-X
Vitello DJ, Ripper RM, Fettiplace MR, Weinberg GL, Vitello JM. Blood density is nearly equal to water density: a validation study of the gravimetric method of measuring intraoperative blood loss. J Vet Med. 2015;2015:1–4.
doi: 10.1155/2015/152730
Nader E, Skinner S, Romana M, Fort R, Lemonne N, Guillot N, et al. Blood rheology: key parameters, impact on blood flow, role in sickle cell disease and effects of exercise. Front Physiol. 2019;10:1329.
pubmed: 31749708
pmcid: 6842957
doi: 10.3389/fphys.2019.01329
Farid H, Simoncelli EP. Optimally rotation-equivariant directional derivative kernels. In: Sommer G, Daniilidis K, Pauli J, editors. Computer Analysis of Images and Patterns. Berlin, Heidelberg: Springer Berlin Heidelberg; 1997. p. 207–14. (Goos G, Hartmanis J, Van Leeuwen J, editors. Lecture Notes in Computer Science; vol. 1296).
Mardia KV. Distribution theory for the von Mises-Fisher distribution and its application. In: Patil GP, Kotz S, Ord JK, editors. A Modern Course on Statistical Distributions in Scientific Work. Dordrecht: Springer, Netherlands; 1975. p. 113–30.
doi: 10.1007/978-94-010-1842-5_10
Schmid-Schönbein GW, Shih YY, Chien S. Morphometry of human leukocytes. Blood. 1980;56(5):866–75.
pubmed: 6775712
doi: 10.1182/blood.V56.5.866.866
Adamanskaya, E., Boldova, A., Korobkin, J., Sveshnikova A. The fields of the smears of a SDS patient and healthy donors. figshare https://figshare.com/articles/figure/The_fields_of_the_smears_of_a_SDS_patient_and_healthy_donors_Supplemented_materials_for_article_Dissecting_Thrombus-Directed_Chemotaxis_and_Random_Walk_in_Neutrophil_Near-Thrombus_Movement_in_Flow_Chambers_/25706400 (2024).
Boldova, A., Adamanskaya, E., Korobkin, J., Sveshnikova A. Fixed granulocytes from SDS patients and healthy donors in flow chamber. Figshare. https://figshare.com/articles/figure/Fixed_granulocytes_from_SDS_patients_and_healthy_donors_in_flow_chamber_Supplemented_materials_for_article_Dissecting_Thrombus-Directed_Chemotaxis_and_Random_Walk_in_Neutrophil_Near-Thrombus_Movement_in_Flow_Chambers_/25738761 (2024).
Korobkin, J., Adamanskaya, E., Sveshnikova A. Dissecting thrombus-directed chemotaxis and random movement in neutrophil near-thrombus motion in flow chambers. OSF. https://osf.io/863ud/ (2024).