Original Scientific Article
Emperipolesis: Sternal and femoral microenvironment induces megakaryiocyte emperipolesis in the Wistar strain
Damir Suljević * ,
Filip Filipić ,
Erna Islamagić

Mac Vet Rev 2019; 42 (1): 71 - 77

10.2478/macvetrev-2019-0012

Received: 18 January 2018

Received in revised form: 02 June 2018

Accepted: 04 July 2018

Available Online First: 04 February 2019

Published on: 15 March 2019

Correspondence: Damir Suljević, suljevic.damir@gmail.com
PDF HTML

Abstract

Emperipolesis is considered a physiological phenomena often present in various pathophysiological conditions, but its etiology is still unknown. In this study, we analyzed the number of megakaryocytes and the percentage of emperipoletic cells in the sternal and femoral bone marrow of Wistar rats. Five types in the thrombopoiesis lineage (megakaryoblasts, promegakaryocytes and megakaryocytes - acidophilic, basophilic and thrombocytogenic) were determined. Except for basophilic megakaryocytes, significant differences were found for number of thrombopoietic cells in the sternal and femoral bone marrow. A larger number of thrombocytogenic megakaryocytes were present in the sternal bone marrow. Emperipoletic cells were significantly present in the femoral compared to the sternal bone marrow. Emperipolesis was typical for lymphocytes and neutrophils individually, while emperipolesis with two or more cells within thrombopoietic cell was also present (1-7 %) and significant differences between the sternal and femoral bone marrow were detected. Emperipolesis was found in all analysed rats and it most commonly occured within mature megakaryocytes and rarely megakaryoblasts, while it was not recorded in the promegakaryocytes. The high incidence of megakaryocytes with emperopolesis in rats could be a consequence of “normal” cell retention in the cytoplasm of megakaryocytes while passing blood cells to circulation or related to haematopoietic response due to high incidence of inbreeding.

Keywords: bone marrow, emperipolesis, femur, megakaryocytes, Wistar strain


References

1. Gupta, N., Jadhav, K., Shah, V. (2017). Emperipolesis, entosis and cell cannibalism:Demystifying the cloud. J Oral Maxillofac Pathol. 21 (1):92–98.
https://doi.org/10.4103/0973-029X.203763 PMid:28479694 PMCid:PMC5406827
2. Raja, H., Subramanyam, S.G., Govindaraj, S., Babu, M.K. (2011). A rare cause of massive lymphadenopathy. Indian J Surg Oncol. 2 (3):212-214.
https://doi.org/10.1007/s13193-011-0102-6 PMid:22942615 PMCid:PMC3272174
3. Sable, M.N., Sehgal, K., Gadage, V.S., Subramanian, P.G., Gujral, S. (2009). Megakaryocytic emperipolesis:A histological finding in myelodysplastic syndrome. Indian J Pathol Microbiol. 52, 599–600. https://doi.org/10.4103/0377-4929.56153 PMid:19805998
4. Rastogi, V., Sharma, R., Misra, S.R., Yadav, L., Sharma, V. (2014). Emperipolesis –A Review. J Clin Diagn Res. 8 (12):ZM01–ZM02. https://doi.org/10.7860/JCDR/2014/10361.5299
5. Amita, K., Vijay Shankar, S., Abhishekh, M.G., Geethalakshmi, U. (2011). Emperipolesis in a case of adult T cell lymphoblastic lymphoma (mediastinal type) –Detected at FNAC and imprint cytology. Online J Health Allied Sci. 10, 11.
6. Vemuganti, G.K., Naik, M.N., Honavar, S.G. (2008). Rosaidorfman disease of the orbit. J Hematol Oncol. 1, 7. https://doi.org/10.1186/1756-−-1-7 PMid:18588698 PMCid:PMC2474646
7. Lee, W.B., Erm, S.K., Kim, K.Y., Becker, R.P. (1999). Emperipolesis of erythroblasts within Kupffer cells during hepatic hemopoiesis in human fetus. Anat Rec. 256, 158–164. https://doi.org/10.1002/(SICI)1097-0185(19991001)256:2<158::AID-AR6>3.0.CO;2-0
8. Dziecioł, J., Lemancewicz, D., Kłoczko, J., Bogusłowicz, W., Lebelt, A. (2001). Megakaryocytes emperipolesis in bone marrow of the patients with non-Hodgkin's lymphoma. Folia Histochem Cytobiol. 2 (39):142-143.
9. Poppema, S. (1978). Sternberg-Reed cells with intracytoplasmic lymphocytes. Phagocytosis or emperipolesis?Virchows Arch A Pathol Anat Histol. 380, 355–359.
https://doi.org/10.1007/BF00431321 PMid:153049
10. Xia, P., Wang, S., Guo, Z., Yao, X. (2008). Emperipolesis, entosis and beyond:Dance with fate. Cell Res. 18, 705–707. https://doi.org/10.1038/cr.2008.64 PMid:18521104
11. Sierro, F., Tay, S.S., Warren, A., Le Couteur, D.G., McCaughan, G.W., Bowen, D.G., Bertolino, P. (2015). Suicidal emperipolesis:a process leading to cell-in-cell structures, T cell clearance and immune homeostasis. Curr Mol Med. 15 (9):819-827. https://doi.org/10.2174/1566524015666151026102143 PMid:26511707
12. Mansour, A., Abou-Ezzi, G., Sitnicka, E., Jacobsen, S.E.W., Wakkach, A., Blin-Wakkach, C. (2012). Osteoclasts promote the formation of hematopoietic stem cell niches in the bone marrow. J Exp Med. 209 (3):537–549. https://doi.org/10.1084/jem.20110994 PMid:22351931 PMCid:PMC3302238
13. Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., Ito, K., Koh, G.Y., Suda, T. (2004). Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell. 118 (2):149–161. https://doi.org/10.1016/j.cell.2004.07.004 PMid:15260986
14. Kunisaki, Y., Bruns, I., Scheiermann, C., Ahmed, J., Pinho, S., Zhang, D., Mizoguchi, T., Wei, Q., Lucas, D., Ito, K., Mar, J.C., Bergman, A., Frenette, P.S. (2013). Nature. 502 (7473):637–643. https://doi.org/10.1038/nature12612 PMid:24107994 PMCid:PMC3821873
15. Becker, R.P., De Bruyn, P.P. (1976). The transmural passage of blood cells into myeloid sinusoids and the entry of platelets into the sinusoidal circulation;a scanning electron microscopic investigation. Am J Anat. 145 (2):183–205. https://doi.org/10.1002/aja.1001450204 PMid:1258805
16. Heazlewood, S.Y., Neaves, R.J., Williams, B., Haylock, D.N., Adams, T.E., Nilsson, S.K. (2013). Megakaryocytes co-localise with hemopoietic stem cells and release cytokines that up-regulate stem cell proliferation. Stem Cell Res. 11 (2):782–792. https://doi.org/10.1016/j.scr.2013.05.007 PMid:23792434
17. Hartwig, J., Italiano, J. (2003). The birth of the platelet. J Thromb Haemost. 1 (7):1580–1586. https://doi.org/10.1046/j.1538-7836.2003.00331.x PMid:12∈94
18. Shivdasani, R.A., Fujiwara, Y., McDevitt, M.A., Orkin, S.H. (1997). A lineage-selective knockout establishes the critical role of transcription factor GATA-1 in megakaryocyte growth and platelet development. EMBO J. 16 (13):3965–3973. https://doi.org/10.1093/emboj/16.13.3965 PMid:9233806 PMCid:PMC1170020
19. Rozman, C., Vives-Corrons, J.L. (1981). On the alleged diagnostic significance of megakaryocytic “phagocytosis“(emperipolesis). Br J Haematol. 48, 510.
https://doi.org/10.1111/j.1365-2141.1981.tb02745.x PMid:7196253
20. Tavassoli, M. (1986). Modulation of megakaryocyte emperipolesis by phlebotomy:Megakaryocytes as a component of marrow-blood barrier. Blood Cells. 12, 205-216. PMid:3790733
21. Centurione, L., Di Baldassarre, A., Zingariello, M., Bosco, D., Gatta, V., Rana, R.A., Langella, V., Di Virgilio, A., Vannucchi, A.M., Migliaccio, A.R. (2004). Increased and pathologic emperipolesis of neutrophils within megakaryocytes associated with marrow fibrosis in GATA-1(low) mice. Blood 104 (12):3573-3580. https://doi.org/10.1182/blood-2004-01-0193 PMid:15292068
22. Lee, K.P. (1989). Emperipolesis of hematopoietic cells within megakaryocytes in bone marrow of the rat. Vet Pathol. 26, 473-478. https://doi.org/10.1177/030098588902600603 PMid:2603328
23. Bobik, R., Dabrowski, Z. (1995). Emperipolesis of marrow cells within megakaryocytes in the bone marrow of sublethally irradiated mice. Ann Hematol. 70 (2):91-95.
https://doi.org/10.1007/BF01834387 PMid:7880931
24. De Pasquale, A., Paterlini, P., Quaglino, D., Quaglino, D. (1985). Emperipolesis ofgranulocytes within megakaryocytes. Br J Haematol. 60, 384-386.
https://doi.org/10.1111/j.1365-2141.1985.tb07429.x PMid:3↑22
25. Faree, M., Afzal, M. (2014). Evidence of inbreeding depression on height, weight, and body mass index:a population-based child cohort. Am J Hum Biol. 26 (6):784–795.
https://doi.org/10.1002/ajhb.22599 PMid:25130378
26. van Den Brandt, J., Kovács, P., Klöting, I. (2000). Metabolic variability among disease-resistant inbred rat strains and in comparison with wild rats (Rattus norvegicus). Clin Exp Pharmacol Physiol. 27 (10):793-795. https://doi.org/10.1046/j.1440-1681.2000.03336.x PMid:11022971


Copyright

© 2019 Suljević D. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Conflict of Interest Statement

The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 42, Issue 1, Pages 71-77, p-ISSN 1409-7621, e-ISSN 1857-7415, DOI: 10.2478/macvetrev-2019-0012, 2019