Annals of Hematology

, Volume 70, Issue 2, pp 91–95 | Cite as

Emperipolesis of marrow cells within megakaryocytes in the bone marrow of sublethally irradiated mice

  • R. Bobik
  • Z. Dabrowski
Original Article


The incidence of megakaryocytic emperipolesis was studied in the bone marrow of normal and X-irradiated mice. Two groups of mice received total body irradiation with a single dose of 5 Gy and one of the two groups had been treated with a radioprotective drug, ethiofos (WR-2721), before irradiation. Mice from a third group remained unexposed to irradiation and served as controls. The Wright-Giemsa stained bone marrow smears were analyzed every 5 days during a 30-day period, starting 1 day after irradiation. The number of megakaryocytes exhibiting the phenomenon was determined and expressed as an average value for every experimental group. The frequency of megakaryocytic emperipolesis was less than 15% of megakaryocytes from control smears but increased to 34% in mice that had only been irradiated and to 43% when mice were treated with WR-2721 before irradiation. In the last case, i.e., irradiation and treatment with a radioprotective drug, a positive correlation between the macrocytic megakaryocytes and elevated emperipolesis was noted. Under light microscopy, there were no signs of phagocytosis; engulfed cells remained unaltered with their normal structure intact. Granulocytic, erythroid, and lymphoid cells appeared to be the most frequent marrow cells engulfed by mature megakaryocytes. The number of incorporated cells in one megakaryocyte ranged from 1 to 3, though occasionally more than 6 were seen in macrocytic megakaryocytes. Based on our findings and on a review of the associated literature, we believe emperipolesis is an interesting cellular phenomenon related to the fast passage of marrow cells across the marrow-blood barrier, especially through the cytoplasm of megakaryocytes in response to an increased demand for cell delivery. The high demand for cell delivery which occurs after irradiation may cause certain mature bone marrow cells to take a transmegakaryocyte path to enter the circulation of the blood. Irradiation seems to have an immediate effect (observed after 24 h) on emperipolesis, suggesting that a humoral factor is involved in the pathogenesis.

Key words

Emperipolesis Megakaryocytes Sublethal irradiation WR-2721 (ethiofos) Bone marrow 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Aoki M, Tavassoli M (1981) Dynamics of red cell egress from bone marrow after blood letting. Br J Haematol 49:337–347PubMedGoogle Scholar
  2. 2.
    Bobik R (1993) Influence of X-irradiation and radioprotective drug on the megakaryocyte-platelet system of mice (in Polish). Doctoral dissertation, The Jagiellonian University, CracowGoogle Scholar
  3. 3.
    Beutler E (1984) Red cell metabolism. A manual of biochemical methods, 3rd edn. Grune and Stratton, New YorkGoogle Scholar
  4. 4.
    Breton-Gorius J (1981) On the alleged phagocytosis by megakaryocytes. Br J Haematol 47:653Google Scholar
  5. 5.
    Burkhardt R, Kleinknecht R, Jager R, Frish B, Mahl G, Bartl R (1984) Megakaryocytic emperipolesis — accidental or diagnostic sign? In: Lennert K, Hubner K (eds) Pathology of the bone marrow. G. Fischer, Stuttgart, pp 200–205Google Scholar
  6. 6.
    Calvo W, Alabi R, Nothdurft W, Fliedner TM (1994) Cytotoxic immigration of granulocytes into megakaryocytes as a late consequence of irradiation. Radiat Res 138:260–265PubMedGoogle Scholar
  7. 7.
    Cashell AW, Buss DH (1992) The frequency and significance of megakaryocytic emperipolesis in myeloproliferative and reactive states. Ann Hematol 64:273–276PubMedGoogle Scholar
  8. 8.
    Chiu T (1983) Megakaryocytes with intracytoplasmic blood cells. Am J Vet Res 45:769–770Google Scholar
  9. 9.
    Humble JG, Jayne WHW, Pulvertaft RJV (1956) Biological interaction between lymphocytes and other cells. Br J Haematol 2:283–294PubMedGoogle Scholar
  10. 10.
    Larsen TE (1970) Emperipolesis of granular leukocytes within megakaryocytes in human hemopoietic bone marrow. Am J Clin Pathol 53:485–489PubMedGoogle Scholar
  11. 11.
    Lee KP (1989) Emperipolesis of hematopoietic cells within megakaryocytes in bone marrow of the rat. Vet Pathol 26:473–478PubMedGoogle Scholar
  12. 12.
    Levine RF, Fedorko ME (1976) Isolation of intact megakaryocytes from guinea pig femoral marrow. Successful harvest made possible with inhibitors of platelet aggregation; enrichment achieved with a two-step separation technique. J Cell Biol 69:159–172PubMedGoogle Scholar
  13. 13.
    Migita M, Fukunaga Y, Watanabe A, Maruyama K, Ohta K, Kaneko K, Kaneda M, Kakinuma K, Yamatoto M (1992) Emperipolesis of neutrophils by megakaryocytes and thrombocytopenia observed in a case of Kostmann's syndrome during intravenous administration of high-dose rhg-CSF. Br J Haematol 80:413–415PubMedGoogle Scholar
  14. 14.
    Parmley RT, Kim TH, Austin RL, Avarado CS, Ragab AH (1982) Emperipolesis of neutrophils by dysmorphic megakaryocytes. Am J Hematol 13:303–311PubMedGoogle Scholar
  15. 15.
    Pasquale De A, Paterlini P, Quaglino D, Quaglino D (1985) Emperipolesis of granulocytes within megakaryocytes (letter). Br J Haematol 60:384–386PubMedGoogle Scholar
  16. 16.
    Richters A, Sherwin RP, Richters V (1971) The lymphocyte and human lung cancers. Cancer Res 31:214–222PubMedGoogle Scholar
  17. 17.
    Rozman C, Vives-Corrons (1981) On the alleged diagnostic significance of megakaryocytic ‘phagocytosis’ (emperipolesis) (letter). Br J Haematol 48:510PubMedGoogle Scholar
  18. 18.
    Sahebekhtiari HA, Tavassoli M (1976) Marrow cell uptake by megakaryocytes in routine bone marrow smears during blood loss. Scand J Haematol 16:13–17PubMedGoogle Scholar
  19. 19.
    Shamoto M (1981) Emperipolesis of hematopoietic cells in myelocytic leukemia. Virchows Arch [B] 35:283–290Google Scholar
  20. 20.
    Signal R, Belliveau RR (1988) Quantitation of megakaryocytes in normal bone marrow. Anal Quant Cytol Histol 10:33–36PubMedGoogle Scholar
  21. 21.
    Sobolewski S (1980) Phagocytosis by megakaryocytes in malignant disorders (abstract). Br J Haematol 45:173Google Scholar
  22. 22.
    Tavassoli M (1981) Emperipolesis by megakaryocytes in blood loss. Br J Haematol 49:660PubMedGoogle Scholar
  23. 23.
    Tavassoli M (1986) Modulation of megakaryocyte emperiolesis by phlebotomy: megakaryocytes as a component of marrow-blood barrier. Blood Cells 12:205–216PubMedGoogle Scholar
  24. 24.
    Tavassoli M, Aoki M (1989) Localization of megakaryocytes in the bone marrow. Blood Cells 15:3–14PubMedGoogle Scholar
  25. 25.
    Thiele J, Krech R, Choritz H, Georgii A (1984) Emperipolesis — a peculiar feature of megakaryocytes as evaluated in chronic myeloproliferative disease by morphometry and ultrastructure. Virchows Arch [B] 46:253–263Google Scholar
  26. 26.
    Thiele J, Schneidwer G, Hoeppner B, Wienhold S, Zankovich R, Fischer R (1988) Histomorphometry of bone marrow biopsies in chronic myeloproliferative disorders with associated thrombocytosis — features of significance for the diagnosis of primary (essential) thrombocythemia. Virchows Arch [A] 413:407–417Google Scholar
  27. 27.
    Weiss L (1970) Transmural cellular passage in vascular sinuses of rat bone marrow. Blood 36:189–208PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1995

Authors and Affiliations

  • R. Bobik
    • 1
  • Z. Dabrowski
    • 1
  1. 1.Division of Hematology and Toxicology, Department of Animal Physiology, Institute of ZoologyJagiellonian UniversityCracowPoland

Personalised recommendations