Sulfenylome analysis of pathogen-inactivated platelets reveals the presence of cysteine oxidation in integrin signaling pathway and cytoskeleton regulation.
blood platelets
cysteine
post-translational modifications
proteomics
transfusion medicine
Journal
Journal of thrombosis and haemostasis : JTH
ISSN: 1538-7836
Titre abrégé: J Thromb Haemost
Pays: England
ID NLM: 101170508
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
18
05
2020
revised:
17
09
2020
accepted:
01
10
2020
pubmed:
14
10
2020
medline:
15
5
2021
entrez:
13
10
2020
Statut:
ppublish
Résumé
Essentials Cysteine oxidation to sulfenic acid plays a key role in redox regulation and signal transduction. Platelet sulfenylome was studied by quantitative proteomics in pathogen inactivated platelets. One hundred and seventy-four sulfenylated proteins were identified in resting platelets. Pathogen inactivation oxidized integrin βIII, which could activate the mitogen-activated protein kinases pathway. ABSTRACT: Background Cysteine-containing protein modifications are involved in numerous biological processes such redox regulation or signal transduction. During the preparation and storage of platelet concentrates, cell functions and protein regulations are impacted. In spite of several proteomic investigations, the platelet sulfenylome, ie, the proteins containing cysteine residues (R-SH) oxidized to sulfenic acid (R-SOH), has not been characterized. Methods A dimedone-based sulfenic acid tagging and enrichment coupled to a mass spectrometry identification workflow was developed to identify and quantify the sulfenic acid-containing proteins in platelet concentrates treated or not with an amotosalen/ultraviolet A (UVA) pathogen inactivation technique. Results One hundred and seventy-four sulfenylated proteins were identified belonging mainly to the integrin signal pathway and cytoskeletal regulation by Rho GTPase. The impact on pathogen inactivated platelet concentrates was weak compared to untreated ones where three sulfenylated proteins (myosin heavy chain 9, integrin βIII, and transgelin 2) were significantly affected by amotosalen/UVA treatment. Of particular interest, the reported oxidation of cysteine residues in integrin βIII is known to activate the receptor αIIbβIII. Following the pathogen inactivation, it might trigger the phosphorylation of p38MAPK and explain the lesions reported in the literature. Moreover, procaspase activating compound-1 (PAC-1) binding assays on platelet activation showed an increased response to adenosine diphosphate exacerbated by the tagging of proteins with dimedone. This result corroborates the hypothesis of an oxidation-triggered activation of αIIbβIII by the pathogen inactivation treatment. Conclusions The present work completes missing information on the platelet proteome and provides new insights on the effect of pathogen inactivation linked to integrin signaling and cytoskeleton regulation.
Identifiants
pubmed: 33047470
doi: 10.1111/jth.15121
pii: S1538-7836(22)00433-0
doi:
Substances chimiques
Integrins
0
Cysteine
K848JZ4886
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
233-247Informations de copyright
© 2020 International Society on Thrombosis and Haemostasis.
Références
Kaushansky K, Roth GJ. Megakaryocytes and platelets. In: Greer JP, Rodgers GM, Foerster J, Paraskevas F, Lukens JN, Glader B, eds. Wintrobe's Clinical Hematology, 11th ed. Philadelphia, PA: Pippincott Williams & Wilkins; 2004:605-650.
Patel P, Naik UP. Platelet MAPKs-a 20+year history: what do we really know? J Thromb Haemost. 2020;18 2087-2102. https://doi.org/10.1111/jth.14967
Aslan JE, McCarty OJT. Rho GTPases in platelet function. J Thromb Haemost. 2013;11:35-46. https://doi.org/10.1111/jth.12051
Sonego G, Abonnenc M, Tissot J-D, Prudent M, Lion N. Redox proteomics and platelet activation: understanding the redox proteome to improve platelet quality for transfusion. Int J Mol Sci. 2017;18:1-22.
Masselli E, Pozzi G, Vaccarezza M, et al. ROS in platelet biology: functional aspects and methodological insights. Int J Mol Sci. 2020;21:4866. https://doi.org/10.3390/ijms21144866
Carrim N, Arthur JF, Hamilton JR, et al. Thrombin-induced reactive oxygen species generation in platelets: a novel role for protease-activated receptor 4 and GPIbalpha. Redox Biol. 2015;6:640-647. https://doi.org/10.1016/j.redox.2015.10.009
Jang JY, Min JH, Chae YH, et al. Reactive oxygen species play a critical role in collagen-induced platelet activation via SHP-2 oxidation. Antioxid Redox Signal. 2014;20:2528-2540. https://doi.org/10.1089/ars.2013.5337
Rehder DS, Borges CR. Cysteine sulfenic acid as an intermediate in disulfide bond formation and nonenzymatic protein folding. Biochemistry. 2010;49:7748-7755. https://doi.org/10.1021/bi1008694
Dalle-Donne I, Rossi R, Colombo G, Giustarini D, Milzani A. Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem Sci. 2009;34:85-96. https://doi.org/10.1016/j.tibs.2008.11.002
Kettenhofen NJ, Wood MJ. Formation, reactivity, and detection of protein sulfenic acids. Chem Res Toxicol. 2010;23:1633-1646. https://doi.org/10.1021/tx100237w
Delobel J, Prudent M, Crettaz D, et al. Cysteine redox proteomics of the hemoglobin-depleted cytosolic fraction of stored red blood cells. Proteomics Clini Appl. 2016;10:883-893. https://doi.org/10.1002/prca.201500132
Paulsen CE, Carroll KS. Cysteine-mediated redox signaling: chemistry, biology, and tools for discovery. Chem Rev. 2013;113:4633-4679. https://doi.org/10.1021/cr300163e
Prudent M, Tissot JD, Lion N. Proteomics of blood and derived products: what's next? Expert Rev Proteomics. 2011;8:717-737.
Burkhart JM, Vaudel M, Gambaryan S, et al. The first comprehensive and quantitative analysis of human platelet protein composition allows the comparative analysis of structural and functional pathways. Blood. 2012;120:E73-E82. https://doi.org/10.1182/blood-2012-04-416594
Aloui C, Barlier C, Claverol S, et al. Differential protein expression of blood platelet components associated with adverse transfusion reactions. J Proteomics. 2019;194:25-36. https://doi.org/10.1016/j.jprot.2018.12.019
Qureshi AH, Chaoji V, Maiguel D, et al. Proteomic and phospho-proteomic profile of human platelets in basal, resting state: insights into integrin signaling. PLoS One. 2009;4:e7627. https://doi.org/10.1371/journal.pone.0007627
Garcia A, Prabhakar S, Hughan S, et al. Differential proteome analysis of TRAP-activated platelets: involvement of DOK-2 and phosphorylation of RGS proteins. Blood. 2004;103:2088-2095. https://doi.org/10.1182/blood-2003-07-2392
Beck F, Geiger J, Gambaryan S, et al. Temporal quantitative phosphoproteomics of ADP stimulation reveals novel central nodes in platelet activation and inhibition. Blood. 2017;129:E1-E12. https://doi.org/10.1182/blood-2016-05-714048
Pan J, Carroll KS. Chemical biology approaches to study protein cysteine sulfenylation. Biopolymers. 2014;101:165-172. https://doi.org/10.1002/bip.22255
Akter S, Carpentier S, Van Breusegem F, Messens J. Identification of dimedone-trapped sulfenylated proteins in plants under stress. Biochemistry and biophysics reports. 2017;9:106-113. https://doi.org/10.1016/j.bbrep.2016.11.014
Yang J, Gupta V, Carroll KS, Liebler DC. Site-specific mapping and quantification of protein S-sulphenylation in cells. Nat Commun. 2014;5:4776. https://doi.org/10.1038/ncomms5776
Paulsen CE, Truong TH, Garcia FJ, et al. Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat Chem Biol. 2012;8:57-64. https://doi.org/10.1038/nchembio.736
Prudent M, D'Alessandro A, Cazenave J-P, et al. Proteome changes in platelets after pathogen inactivation-an interlaboratory consensus. Transf Med Rev. 2014;28:72-83. https://doi.org/10.1016/j.tmrv.2014.02.002
Schubert P, Johnson L, Marks DC, Devine DV. UV-based pathogen inactivation systems: untangling the molecular targets activated in platelets. Front Med. 2018;5:129. https://doi.org/10.3389/fmed.2018.00129
Feys HB, Van Aelst B, Compernolle V. Biomolecular consequences of platelet pathogen inactivation methods. Transfus Med Rev. 2019;33:29-34. https://doi.org/10.1016/j.tmrv.2018.06.002
Schubert P, Coupland D, Culibrk B, Goodrich RP, Devine DV. Riboflavin and ultraviolet light treatment of platelets triggers p38MAPK signaling: inhibition significantly improves in vitro platelet quality after pathogen reduction treatment. Transfusion. 2013;53:3164-3173. https://doi.org/10.1111/trf.12173
Stivala S, Gobbato S, Infanti L, et al. Amotosalen/ultraviolet A pathogen inactivation technology reduces platelet activatability, induces apoptosis and accelerates clearance. Haematologica. 2017;102:1650-1660. https://doi.org/10.3324/haematol.2017.164137
Prudent M, Crettaz D, Delobel J, Tissot J-D, Lion N. Proteomic analysis of Intercept-treated platelets. J Proteomics. 2012;76:316-328. https://doi.org/10.1016/j.jprot.2012.07.008
Sonego G, Abonnenc M, Crettaz D, Lion N, Tissot JD, Prudent M. Irreversible oxidations of platelet proteins after riboflavin-UVB pathogen inactivation. Transfu Clin Biol. 2020;27:36-42. https://doi.org/10.1016/j.tracli.2018.12.001
Johnson L, Marks D. Treatment of platelet concentrates with the mirasol pathogen inactivation system modulates platelet oxidative stress and NF-kappaB activation. Transfus Med Hemother. 2015;42:167-173. https://doi.org/10.1159/000403245
Abonnenc M, Crettaz D, Marvin L, et al. Metabolomic profiling highlights oxidative damages in platelet concentrates treated for pathogen inactivation and shows protective role of urate. Metabolomics. 2016;12:188. https://doi.org/10.1007/s11306-016-1136-0
Abonnenc M, Crettaz D, Sonego G, Escolar G, Tissot JD, Prudent M. Towards the understanding of the UV light, riboflavin and additive solution contributions to the in vitro lesions observed in Mirasol(R)-treated platelets. Transfus Clin Biol. 2019;26:209-216. https://doi.org/10.1016/j.tracli.2019.09.001
Abonnenc M, Crettaz D, Tacchini P, et al. Antioxidant power as a quality control marker for completeness of amotosalen and ultraviolet A photochemical treatments in platelet concentrates and plasma units. Transfusion. 2016;56:1819-1827. https://doi.org/10.1111/trf.13638
Prudent M, Sonego G, Abonnenc M, Tissot J-D, Lion N. LC-MS/MS Analysis and comparison of oxidative damages on peptides induced by pathogen reduction technologies for platelets. J Am Soc Mass Spectr. 2014;25:651-661. https://doi.org/10.1007/s13361-013-0813-8
Abonnenc M, Sonego G, Crettaz D, et al. In vitro study of platelet function confirms the contribution of the ultraviolet B (UVB) radiation in the lesions observed in riboflavin/UVB-treated platelet concentrates. Transfusion. 2015;55:2219-2230. https://doi.org/10.1111/trf.13123
Abonnenc M, Sonego G, Kaiser-Guignard J, et al. In vitro evaluation of pathogen-inactivated buffy coat-derived platelet concentrates during storage: psoralen-based photochemical treatment step-by-step. Blood Transf. 2015;13:255-264. https://doi.org/10.2450/2014.0082-14
Yang J, Gupta V, Tallman KA, Porter NA, Carroll KS, Liebler DC. Global, in situ, site-specific analysis of protein S-sulfenylation. Nat Protoc. 2015;10:1022-1037. https://doi.org/10.1038/nprot.2015.062
Cox J, Neuhauser N, Michalski A, Scheltema RA, Olsen JV, Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J Proteome Res. 2011;10:1794-1805. https://doi.org/10.1021/pr101065j
Tyanova S, Temu T, Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11:2301-2319. https://doi.org/10.1038/nprot.2016.136
Cox J, Hein MY, Luber CA, Paron I, Nagaraj N, Mann M. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol Cell Proteomics. 2014;13:2513-2526. https://doi.org/10.1074/mcp.M113.031591
Schwanhausser B, Busse D, Li N, et al. Global quantification of mammalian gene expression control. Nature. 2011;473:337-342. https://doi.org/10.1038/nature10098
Devarie-Baez NO, Silva Lopez EI, Furdui CM. Biological chemistry and functionality of protein sulfenic acids and related thiol modifications. Free Radic Res. 2016;50:172-194. https://doi.org/10.3109/10715762.2015.1090571
Jang JY, Wang SB, Min JH, et al. Peroxiredoxin II is an antioxidant enzyme that negatively regulates collagen-stimulated platelet function. J Biol Chem. 2015;290:11432-11442. https://doi.org/10.1074/jbc.M115.644260
Flevaris P, Li ZY, Zhang GY, Zheng Y, Liu JL, Du XP. Two distinct roles of mitogen-activated protein kinases in platelets and a novel Rac1-MAPK-dependent integrin outside-in retractile signaling pathway. Blood. 2009;113:893-901. https://doi.org/10.1182/blood-2008-05-155978
Vanhoorelbeke K, Ulrichts H, Van de Walle G, Fontayne A, Deckmyn H. Inhibition of platelet glycoprotein Ib and its antithrombotic potential. Curr Pharm Design. 2007;13:2684-2697.
Schubert P, Culibrk B, Goodrich RP, Devine DV. Changes in the protein profiling triggered by riboflavin/UV treatment using quantitative proteomics: increase in cytoskeletal protein expression. Transfusion. 2012;52(suppl S3):19A-20A.
Hechler B, Ohlmann P, Chafey P, et al. Preserved functional and biochemical characteristics of platelet components prepared with amotosalen and ultraviolet A for pathogen inactivation. Transfusion. 2013;53:1187-1200. https://doi.org/10.1111/j.1537-2995.2012.03923.x
Marrocco C, D'Alessandro A, Girelli G, Zolla L. Proteomic analysis of platelets treated with gamma irradiation versus a commercial photochemical pathogen reduction technology. Transfusion. 2013;53:1808-1820. https://doi.org/10.1111/trf.12060
Mohr H, Steil L, Gravemann U, et al. A novel approach to pathogen reduction in platelet concentrates using short-wave ultraviolet light. Transfusion. 2009;49:2612-2624.
O'Dea EL, Kearns JD, Hoffmann A. UV as an amplifier rather than inducer of NF-kappaB activity. Mol Cell. 2008;30:632-641. https://doi.org/10.1016/j.molcel.2008.03.017
Chen Z, Schubert P, Culibrk B, Devine DV. p38MAPK is involved in apoptosis development in apheresis platelet concentrates after riboflavin and ultraviolet light treatment. Transfusion. 2015;55:848-857. https://doi.org/10.1111/trf.12905
Na BR, Kim HR, Piragyte I, et al. TAGLN2 regulates T cell activation by stabilizing the actin cytoskeleton at the immunological synapse. J Cell Biol. 2015;209:143-162. https://doi.org/10.1083/jcb.201407130
Levin J. Chapter 1-the evolution of mammalian platelets. In: Press A, (ed.). Platelets, 3rd ed.London: Academic Press; 2013:3-25.
Yan B, Smith JW. Mechanism of integrin activation by disulfide bond reduction. Biochemistry. 2001;40:8861-8867. https://doi.org/10.1021/bi002902i
Verhaar R, Dekkers DWC, De Cuyper IM, Ginsberg MH, de Korte D, Verhoeven AJ. UV-C irradiation disrupts platelet surface disulfide bonds and activates the platelet integrin alpha IIb beta 3. Blood. 2008;112:4935-4939. https://doi.org/10.1182/blood-2008-04-151043
Gong H, Shen B, Flevaris P, et al. G protein subunit Galpha13 binds to integrin alphaIIbbeta3 and mediates integrin "outside-in" signaling. Science. 2010;327:340-343. https://doi.org/10.1126/science.1174779
Flevaris P, Stojanovic A, Gong H, Chishti A, Welch E, Du X. A molecular switch that controls cell spreading and retraction. J Cell Biol. 2007;179:553-565. https://doi.org/10.1083/jcb.200703185
Picker SM, Tauszig ME, Gathof BS. Cell quality of apheresis-derived platelets treated with riboflavin-ultraviolet light after resuspension in platelet additive solution. Transfusion. 2012;52:510-516. https://doi.org/10.1111/j.1537-2995.2011.03323.x
Tynngård N, Johansson BM, Lindahl TL, Berlin G, Hansson M. Effects of intercept pathogen inactivation on platelet function as analysed by free oscillation rheometry. Transfus Apher Sci. 2008;38:85-88. https://doi.org/10.1016/j.transci.2007.12.012