Canalicular system reorganization during mouse platelet activation as revealed by 3D ultrastructural analysis

Irina D. Pokrovskaya, Michael Tobin, Rohan Desai, Smita Joshi, Jeffrey A. Kamykowski, Guofeng Zhang, Maria A. Aronova, Sidney W. Whiteheart, Richard D. Leapman, Brian Storrie

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

The canalicular system (CS) has been defined as: 1) an inward, invaginated membrane connector that supports entry into and exit from the platelet; 2) a static structure stable during platelet isolation; and 3) the major source of plasma membrane (PM) for surface area expansion during activation. Recent analysis from STEM tomography and serial block face electron microscopy has challenged the relative importance of CS as the route for granule secretion. Here, We used 3D ultrastructural imaging to reexamine the CS in mouse platelets by generating high-resolution 3D reconstructions to test assumptions 2 and 3. Qualitative and quantitative analysis of whole platelet reconstructions, obtained from immediately fixed or washed platelets fixed post-washing, indicated that CS, even in the presence of activation inhibitors, reorganized during platelet isolation to generate a more interconnected network. Further, CS redistribution into the PM at different times, post-activation, appeared to account for only about half the PM expansion seen in thrombin-activated platelets, in vitro, suggesting that CS reorganization is not sufficient to serve as a dominant membrane reservoir for activated platelets. In sum, our analysis highlights the need to revisit past assumptions about the platelet CS to better understand how this membrane system contributes to platelet function.

Original languageEnglish
Pages (from-to)97-104
Number of pages8
JournalPlatelets
Volume32
Issue number1
DOIs
StatePublished - 2021

Bibliographical note

Funding Information:
The Storrie laboratory was supported in part by National Institutes of Health grants R01 HL119393 and R56 HL119393. The Leapman laboratory was supported by the intramural program at NIBIB at the National Institutes of Health, Bethesda, MD. The Whiteheart laboratory was supported in part by National Institutes of Health grants HL56652 and HL138179, American Heart Association grant AHA16GRNT27620001, and a Veterans Affairs Merit Award to SWW and an American Heart Association predoctoral grant AHA15PRE25550020 to SJ;American Heart Association [AHA15PRE25550020,AHA16GRNT27620001];National Heart, Lung, and Blood Institute [R01 HL119393,R01 HL138179,R01HL56652,R56HL119393];U.S. Department of Veterans Affairs [Merit award to SWW]; The authors thank Carl Zeiss, Inc (Thornwood, NY) for performing the FIB-SEM imaging and Joel Mancusco of Zeiss for arranging this.

Publisher Copyright:
© 2020 Taylor & Francis Group, LLC.

Keywords

  • Canalicular system
  • electron microscopy
  • hemostasis
  • platelet granules
  • platelet organelles
  • platelet ultrastructure

ASJC Scopus subject areas

  • Hematology

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