411
Views
2
CrossRef citations to date
0
Altmetric
Plenary Article

Mapping densely packed αIIbβ3 receptors in murine blood platelets with expansion microscopy

ORCID Icon, , , ORCID Icon, ORCID Icon, , , , ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 849-858 | Received 13 Aug 2021, Accepted 14 Dec 2021, Published online: 02 Feb 2022

References

  • Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002;110:673–687. doi: 10.1016/S0092-8674(02)00971-6.
  • Campbell ID, Humphries MJ. Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol 2011;3:a004994–a004994. doi: 10.1101/cshperspect.a004994.
  • Shattil SJ, Kim C, Ginsberg MH. The final steps of integrin activation: the end game. Nat Rev Mol Cell Biol 2010;11:288–300. doi: 10.1038/nrm2871.
  • Durrant TN, van den Bosch MT, Hers I. Integrin αIIbβ3 outside-in signaling. Blood 2017;130:1607–1619. doi: 10.1182/blood-2017-03-773614.
  • Humphries JD, Byron A, Humphries MJ. Integrin ligands at a glance. J Cell Sci 2006;119:3901–3903. doi: 10.1242/jcs.03098.
  • Mackman N, Bergmeier W, Stouffer GA, Weitz JI. Therapeutic strategies for thrombosis: new targets and approaches. Nat Rev Drug Discov 2020;19:333–352. doi: 10.1038/s41573-020-0061-0.
  • Fong KP, Zhu H, Span LM, Moore DT, Yoon K, Tamura R, Yin H, DeGrado WF, Bennett JS . Directly activating the integrin αIIbβ3 initiates outside-in signaling by causing αIIbβ3 clustering. J Biol Chem 2016;291:11706–11716. doi: 10.1074/jbc.M116.716613.
  • Legate KR, Wickstrom SA, Fassler R. Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 2009;23:397–418. doi: 10.1101/gad.1758709.
  • Huang J, Li X, Shi X, Zhu M, Wang J, Huang S, Huang X, Wang H, Li L, Deng H, et al. Platelet integrin αIIbβ3: signal transduction, regulation, and its therapeutic targeting. J Hematol Oncol 2019;12:26. doi: 10.1186/s13045-019-0709-6.
  • Wagner C, Mascelli MA, Neblock DS, Weisman HF, Coller BS, Jordan RE . Analysis of GPIIb/IIIa receptor number by quantification of 7E3 binding to human platelets. Blood 1996;88:907–914. doi: 10.1182/blood.V88.3.907.907.
  • Coller BS, Shattil SJ. The GPIIb/IIIa (integrin αIIbβ3) odyssey: a technology-driven saga of a receptor with twists, turns, and even a Bend. Blood 2008;112:3011–3025. doi: 10.1182/blood-2008-06-077891.
  • Oheim M, Li D. Quantitative colocalisation imaging: concepts, measurements, and pitfalls. In: Shorte SL, and Frischknecht F, editors. Imaging cellular and molecular biological functions. Berlin Heidelberg: Springer; 2007. p. 117–155. doi: 10.1007/978-3-540-71331-9_5.
  • Pike JA, Styles IB, Rappoport JZ, Heath JK. Quantifying receptor trafficking and colocalization with confocal microscopy. Methods 2017;115:42–54. doi: 10.1016/j.ymeth.2017.01.005.
  • Schulze H, Stegner D. Imaging platelet biogenesis in vivo. Res Pract Thromb Haemost 2018;2:461–468. doi: 10.1002/rth2.12112.
  • Clark JC, Kavanagh DM, Watson S, Pike JA, Andrews RK, Gardiner EE, Poulter NS, Hill SJ, Watson SP. Adenosine and forskolin inhibit platelet aggregation by collagen but not the proximal signalling events. Thromb Haemost 2019;119:1124–1137. doi: 10.1055/s-0039-1688788.
  • Vangindertael J, Camacho R, Sempels W, Mizuno H, Dedecker P, Janssen KPF. An introduction to optical super-resolution microscopy for the adventurous biologist. Methods Appl Fluoresc 2018;6:022003. doi: 10.1088/2050-6120/aaae0c.
  • Levet F, Julien G, Galland R, Butler C, Beghin A, Chazeau A, Hoess P, Ries J, Giannone G, Sibarita J-B. A tessellation-based colocalization analysis approach for single-molecule localization microscopy. Nat Commun 2019;10:1–12. doi: 10.1038/s41467-019-10007-4.
  • Chen F, Tillberg PW, Boyden ES. Expansion microscopy. Science 2015;347:543–548. doi: 10.1126/science.1260088.
  • Wassie AT, Zhao Y, Boyden ES. Expansion microscopy: principles and uses in biological research. Nat Methods 2019;16:33–41. doi: 10.1038/s41592-018-0219-4.
  • Tillberg PW, Chen F, Piatkevich KD, Zhao Y, Yu -C-C, English BP, Gao L, Martorell A, Suk H-J, Yoshida F, et al. Protein-retention expansion microscopy of cells and tissues labeled using standard fluorescent proteins and antibodies. Nat Biotechnol 2016;34:987–992. doi: 10.1038/nbt.3625.
  • Truckenbrodt S, Sommer C, Rizzoli SO, Danzl JG. A practical guide to optimization in X10 expansion microscopy. Nat Protoc 2019;14:832–863. doi: 10.1038/s41596-018-0117-3.
  • Dunn KW, Kamocka MM, McDonald JH. A practical guide to evaluating colocalization in biological microscopy. Am J Physiol Physiol 2011;300:C723–C742. doi: 10.1152/ajpcell.00462.2010.
  • Manders EMM, Verbeek FJ, Aten JA. Measurement of co-localization of objects in dual-colour confocal images. J Microsc 1993;169:375–382. doi: 10.1111/j.1365-2818.1993.tb03313.x.
  • van Eeuwijk JMM, Stegner D, Lamb DJ, Kraft P, Beck S, Thielmann I, Kiefer F, Walzog B, Stoll G, Nieswandt B. The novel oral Syk inhibitor, Bl1002494, protects mice from arterial thrombosis and thrombo inflammatory brain infarction. Arterioscler Thromb Vasc Biol 2016;36:1247–1253. doi: 10.1161/ATVBAHA.115.306883.
  • Richter KN, Revelo NH, Seitz KJ, Helm MS, Sarkar D, Saleeb RS, D’Este E, Eberle J, Wagner E, Vogl C, et al. Glyoxal as an alternative fixative to formaldehyde in immunostaining and super‐resolution microscopy. EMBO J 2018;37:139–159. doi: 10.15252/embj.201695709.
  • Nieswandt B, Bergmeier W, Rackebrandt K, Gessner JE, Zirngibl H. Identification of critical antigen-specific mechanisms in the development of immune thrombocytopenic purpura in mice. Blood 2000;96:2520–2527. doi: 10.1182/blood.V96.7.2520.
  • Chozinski TJ, Halpern AR, Okawa H, Kim H-J, Tremel GJ, Wong ROL, Vaughan JC. Expansion microscopy with conventional antibodies and fluorescent proteins. Nat Methods 2016;13:485–488. doi: 10.1038/nmeth.3833.
  • Truckenbrodt S, Maidorn M, Crzan D, Wildhagen H, Kabatas S, Rizzoli SO. X10 expansion microscopy enables 25‐nm resolution on conventional microscopes. EMBO Rep 2018;19:e45836. doi: 10.15252/embr.201845836.
  • Arganda-Carreras I, Sorzano COS, Marabini R, Carazo JM, Ortiz-de-Solorzano C, Kybic J. Consistent and elastic registration of histological sections using vector-spline regularization. In:Beichel RR, Sonka M, editors. Computer vision approaches to medical image analysis. Berlin Heidelberg: Springer; 2006. p. 85–95. doi: 10.1007/11889762_8.
  • Heil HS, Schreiber B, Götz R, Emmerling M, Dabauvalle M-C, Krohne G, Höfling S, Kamp M, Sauer M, Heinze KG. Sharpening emitter localization in front of a tuned mirror. Light Sci Appl 2018;7:99. doi: 10.1038/s41377-018-0104-z.
  • Brunstein M, Oheim M. Dependence of descriptors of co-localization on microscope spatiotemporal resolution and the choice of regions of interest. Microsc Res Tech 2017;80:220–230. doi: 10.1002/jemt.22790.
  • Poulter NS, Pollitt AY, Owen DM, Gardiner EE, Andrews RK, Shimizu H, Ishikawa D, Bihan D, Farndale RW, Moroi M, et al. Clustering of glycoprotein VI (GPVI) dimers upon adhesion to collagen as a mechanism to regulate GPVI signaling in platelets. J Thromb Haemost 2017;15:549–564. doi: 10.1111/jth.13613.
  • Pallini C, Pike JA, O’Shea C, Andrews RK, Gardiner EE, Watson SP, Poulter NS. Immobilized collagen prevents shedding and induces sustained GPVI clustering and signaling in platelets. Platelets 2021;32:59–73. doi: 10.1080/09537104.2020.1849607.
  • Gaertner F, Ahmad Z, Rosenberger G, Fan S, Nicolai L, Busch B, Yavuz G, Luckner M, Ishikawa-Ankerhold H, Hennel R, et al. Migrating platelets are mechano-scavengers that collect and bundle bacteria. Cell 2017;171:1368–1382.e23. doi: 10.1016/j.cell.2017.11.001.
  • Nicolai L, Schiefelbein K, Lipsky S, Leunig A, Hoffknecht M, Pekayvaz K, Raude B, Marx C, Ehrlich A, Pircher J, et al. Vascular surveillance by haptotactic blood platelets in inflammation and infection. Nat Commun 2020;11:5778. doi: 10.1038/s41467-020-19515-0.
  • Gao M, Maraspini R, Beutel O, Zehtabian A, Eickholt B, Honigmann A, Ewers H. Expansion Stimulated Emission Depletion Microscopy (ExSTED). ACS Nano 2018;12:4178–4185. doi: 10.1021/acsnano.8b00776.
  • Ku T, Swaney J, Park J-Y, Albanese A, Murray E, Cho JH, Park Y-G, Mangena V, Chen J, Chung K. Multiplexed and scalable super-resolution imaging of three-dimensional protein localization in size-adjustable tissues. Nat Biotechnol 2016;34:973–981. doi: 10.1038/nbt.3641.
  • Gambarotto D, Zwettler FU, Le Guennec M, Schmidt-Cernohorska M, Fortun D, Borgers S, Heine J, Schloetel J-G, Reuss M, Unser M, et al. Imaging cellular ultrastructures using expansion microscopy (U-ExM). Nat Methods 2019;16:71–74. doi: 10.1038/s41592-018-0238-1.
  • Zwettler FU, Reinhard S, Gambarotto D, Bell TDM, Hamel V, Guichard P, Sauer M. Molecular resolution imaging by post-labeling expansion single-molecule localization microscopy (Ex-SMLM). Nat Commun 2020;11:3388. doi: 10.1038/s41467-020-17086-8.
  • Rayes J, Watson SP, Nieswandt B. Functional significance of the platelet immune receptors GPVI and CLEC-2. J Clin Invest 2019;129:12–23. doi: 10.1172/JCI122955.
  • Senis YA, Mazharian A, Mori J. Src family kinases: at the forefront of platelet activation. Blood 2014;124:2013–2024. doi: 10.1182/blood-2014-01-453134.
  • Lee FA, van Lier M, Relou IAM, Foley L, Akkerman J-WN, Heijnen HFG, Farndale RW. Lipid rafts facilitate the interaction of PECAM-1 with the glycoprotein VI-FcR γ-chain complex in human platelets. J Biol Chem 2006;281:39330–39338. doi: 10.1074/jbc.M607930200.
  • Battinelli EM, Thon JN, Okazaki R, Peters CG, Vijey P, Wilkie AR, Noetzli LJ, Flaumenhaft R, Italiano JE. Megakaryocytes package contents into separate a-granules that are differentially distributed in platelets. Blood Adv 2019;3:3092–3098. doi: 10.1182/bloodadvances.2018020834.
  • Pokrovskaya ID, Yadav S, Rao A, McBride E, Kamykowski JA, Zhang G, Aronova MA, Leapman RD, Storrie B. 3D ultrastructural analysis of α‐granule, dense granule, mitochondria, and canalicular system arrangement in resting human platelets. Res Pract Thromb Haemost 2020;4:72–85. doi: 10.1002/rth2.12260.
  • Halpern AR, Alas GCM, Chozinski TJ, Paredez AR, Vaughan JC. Hybrid structured illumination expansion microscopy reveals microbial cytoskeleton organization. ACS Nano 2017;11:12677–12686. doi: 10.1021/acsnano.7b07200.
  • Mahecic D, Testa I, Griffié J, Manley S. Strategies for increasing the throughput of super-resolution microscopies. Curr Opin Chem Biol 2019;51:84–91. doi: 10.1016/j.cbpa.2019.05.012.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.