Home LiteratureArticle Details
PMID: 2201412 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

How do normal and leukemic white blood cells egress from the bone marrow? Morphological facts and biochemical riddles.

Blut ·Vol. 61 ·No. 1 ·1990-07-00 ·Pages 3-13

Petrides PE, Dittmann KH

Abstract

Under normal circumstances only mature granulocytes and monocytes cross the bone marrow sinus wall, a trilaminar structure consisting of endothelial cells, a discontinuous basal membrane and an adventitial cell layer in order to get access to the blood circulation. In leukemia, however, immature white blood cells are able to traverse the barrier and to appear in the blood stream. Very little is known about the regulatory processes which govern the egress of white blood cells in healthy individuals and their malignant counterparts in patients with leukemia. The results of the few studies performed to address this question in animal and human leukemias all agree that the extent to which adventitial cells (fibroblasts) cover the endothelium in bone marrow is drastically reduced. This implies altered interactions between the leukemic and adventitial cells and their extracellular matrix. We propose here a model to explain the egress of normal cells and their leukemic counterparts. It is based upon our own experimental data and the general at present limited knowledge of the subject. It is hoped that this model will stimulate further research into this important aspect of leukemogenesis.

MeSH Terms
Animals Biological Factors/physiology Bone Marrow/anatomy & histology Bone Marrow Cells Cell Adhesion/physiology Cell Movement/physiology Cytokines Humans Leukemia/pathology Leukocytes/physiology Models, Biological
Chemicals
Biological Factors Cytokines
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Petrides P E
Department of Medicine III, University of Munich Medical School Grosshadern, Federal Republic of Germany.
Dittmann K H
References (80)
80 references, click to expand
  1. Hemopoietic cell growth factors and their receptors.
    Annu Rev Biochem. 1989;58:45-77 PMID: 2549855
  2. The microcirculation of the bone marrow.
    Anat Rec. 1970 Sep;168(1):55-68 PMID: 4918907
  3. Microgranular acute promyelocytic leukemia: a proposed role for a greater deformability of the leukemic cell.
    Nouv Rev Fr Hematol. 1989;31(1):23-6 PMID: 2915920
  4. The type I insulin-like growth factor receptor is a motility receptor in human melanoma cells.
    J Biol Chem. 1989 Dec 25;264(36):21544-9 PMID: 2557332
  5. How cancer cells spread in the body.
    Science. 1989 Apr 14;244(4901):147-8 PMID: 2704994
  6. The transmural migration and release of blood cells in acute myelogenous leukemia.
    Am J Anat. 1977 Jun;149(2):247-67 PMID: 267427
  7. Kinetics of granulocytopoiesis.
    Clin Haematol. 1979 Jun;8(2):351-70 PMID: 385200
  8. Structural substrates of bone marrow function.
    Semin Hematol. 1981 Jul;18(3):179-93 PMID: 7025215
  9. Marrow cell egress: specificity of the site of penetration into the sinus.
    Blood. 1978 Nov;52(5):959-68 PMID: 698400
  10. Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins.
    Science. 1989 Mar 3;243(4895):1160-5 PMID: 2466335
  11. Studies of leukopoiesis: the technique of leukopheresis and the response of myeloid tissue in normal and irradiated dogs.
    J Lab Clin Med. 1955 Jun;45(6):881-905 PMID: 14381726
  12. Collagen heterogeneity in normal human bone marrow.
    Br J Haematol. 1981 Jun;48(2):287-91 PMID: 7016167
  13. Acute leukemia. A prototype of disseminated cancer.
    Cancer. 1984 May 15;53(10):2026-33 PMID: 6367932
  14. Colocalization of calcium-dependent protease II and one of its substrates at sites of cell adhesion.
    Cell. 1987 Nov 20;51(4):569-77 PMID: 2824061
  15. Increase in the number of fenestrae in mouse endothelial liver cells by altering the cytoskeleton with cytochalasin B.
    Hepatology. 1987 Nov-Dec;7(6):1230-8 PMID: 3679088
  16. Marrow adipose cells and hemopoiesis: an interpretative review.
    Exp Hematol. 1984 Feb;12(2):139-46 PMID: 6199224
  17. Mechanisms of leukocyte production and release. XII. A comparative assay of the leukocytosis-inducing factor (LIF) and the colony-stimulating factor (CSF).
    Proc Soc Exp Biol Med. 1974 Apr;145(4):1262-7 PMID: 4597274
  18. Leukemic cell-endothelial cell interactions in leukemic cell dissemination.
    Lab Invest. 1989 Jan;60(1):45-64 PMID: 2911183
  19. Transient versus permanent expression of cancer-related glycopeptides on normal versus leukemic myeloid cells coinciding with marrow egress.
    Blood. 1984 Jan;63(1):170-6 PMID: 6689948
  20. Ultrastructure of the sinus wall of murine bone marrow in myelogenous leukemia.
    Am J Anat. 1975 Mar;142(3):319-33 PMID: 1054534
  21. Cellular relationship in the rat bone marrow studied by freeze fracture and lanthanum impregnation thin-sectioning electron microscopy.
    J Ultrastruct Res. 1979 Dec;69(3):343-61 PMID: 513186
  22. Bone marrow sinus and cell egress in human leukaemia: a morphometric study of core biopsies using wide-field electron microscopy.
    Br J Haematol. 1986 Aug;63(4):737-47 PMID: 3460628
  23. Hormonal regulation of capillary fenestrae in the rat adrenal cortex: quantitative studies using objective lens staging scanning electron microscopy.
    Scan Electron Microsc. 1986;(Pt 4):1381-93 PMID: 3027881
  24. Endothelial cell proliferation in myelofibrosis.
    Br J Haematol. 1985 Aug;60(4):625-30 PMID: 3927969
  25. Transmural cellular passage in vascular sinuses of rat bone marrow.
    Blood. 1970 Aug;36(2):189-208 PMID: 5427454
  26. A scanning and transmission electron microscopic study on rat bone marrow sinuses and transmural migration of blood cells.
    Arch Histol Jpn. 1976 Mar;39(1):51-66 PMID: 938202
  27. Extracellular matrix of the marrow microenvironment.
    Br J Haematol. 1988 Sep;70(1):1-4 PMID: 3052566
  28. The marrow-blood barrier.
    Br J Haematol. 1979 Mar;41(3):297-302 PMID: 371662
  29. Endothelial diaphragmed fenestrae: in vitro modulation by phorbol myristate acetate.
    J Cell Biol. 1986 May;102(5):1965-70 PMID: 3700479
  30. The ultrastructure of the hemopoietic environment of the marrow: a review.
    Exp Hematol. 1981 Apr;9(4):391-410 PMID: 7016565
  31. Haemonectin, a bone marrow adhesion protein specific for cells of granulocyte lineage.
    Nature. 1987 Oct 22-28;329(6141):744-6 PMID: 3313047
  32. Identification of microfilaments in marrow sinus endothelial cells: their possible role in cell egress.
    J Ultrastruct Res. 1981 Mar;74(3):255-8 PMID: 6166753
  33. Heparan sulphate bound growth factors: a mechanism for stromal cell mediated haemopoiesis.
    Nature. 1988 Mar 24;332(6162):376-8 PMID: 2965305
  34. [The fine structure of rat bone marrow in the use of recent aldehyde fixation].
    Blut. 1966 Aug;13(5):291-304 PMID: 5329439
  35. Absence of tight junctions in endothelium of marrow sinuses: possible significance for marrow cell egress.
    Br J Haematol. 1979 Mar;41(3):303-7 PMID: 427035
  36. Chronic myelocytic leukemia: ultrastructural histopathology of bone marrow from patients in the chronic phase.
    Ultrastruct Pathol. 1984;6(4):307-17 PMID: 6592869
  37. The kinetics of neutrophilic leukocytes in health and in disease.
    Semin Hematol. 1967 Oct;4(4):359-86 PMID: 4864987
  38. Endocytosis, transfer tubules, and lysosomal activity in myeloid sinusoidal endothelium.
    J Ultrastruct Res. 1975 Nov;53(2):133-51 PMID: 172648
  39. An altered IGF-I receptor is present in human leukemic cells.
    J Biol Chem. 1990 Jun 5;265(16):9340-5 PMID: 1693149
  40. The structure of bone marrow. Functional interrelationships of vascular and hematopoietic compartments in experimental hemolytic anemia: an electron microscopic study.
    J Morphol. 1965 Nov;117(3):467-537 PMID: 5883927
  41. Newer concepts in leukocyte physiology and their clinical significance.
    AMA Arch Intern Med. 1957 Aug;100(2):183-9 PMID: 13443536
  42. Structure and function of the bone marrow and hematopoiesis.
    Hematol Oncol Clin North Am. 1988 Dec;2(4):495-511 PMID: 3065314
  43. The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats.
    Anat Rec. 1976 Oct;186(2):161-84 PMID: 984472
  44. Early hemopoietic and stromal precursor cells.
    Int Rev Cytol. 1986;102:271-313 PMID: 3533829
  45. Chemotactic activity of human recombinant granulocyte-macrophage colony-stimulating factor.
    Immunology. 1987 Mar;60(3):439-44 PMID: 3494669
  46. Increased activity of a specific sialyltransferase in chronic myelogenous leukemia.
    Blood. 1985 Nov;66(5):1068-71 PMID: 2413927
  47. The vascular bed of red bone marrow.
    J Ultrastruct Res. 1961 Mar;5:65-85 PMID: 13787795
  48. Interleukin-1 and tumor necrosis factor production in acute non-lymphoid leukemia.
    Eur J Haematol. 1989 Jan;42(1):16-23 PMID: 2783672
  49. The role of proteinases in cellular invasiveness.
    Biochim Biophys Acta. 1983 Dec 29;695(3-4):177-214 PMID: 6317025
  50. [Research on the vascular structure of the bone marrow of rats].
    Z Zellforsch Mikrosk Anat. 1956;45(3):328-38 PMID: 13402085
  51. Marrow stromal stem cells.
    J Cell Sci Suppl. 1988;10:63-76 PMID: 3077943
  52. The physiology of granulocytic cells in normal and leukemic states.
    Am J Med. 1960 May;28:711-25 PMID: 13812563
  53. In vitro homing of hemopoietic stem cells is mediated by a recognition system with galactosyl and mannosyl specificities.
    Proc Natl Acad Sci U S A. 1987 Jul;84(13):4485-9 PMID: 3474617
  54. Morphometric analysis of bone marrow sinus cell elements after induction of monomyelocytic leukemia in BALB/c mice.
    Anat Rec. 1989 Jul;224(3):331-5 PMID: 2782618
  55. Heparan sulfate degradation in tumor cell invasion and angiogenesis.
    Adv Exp Med Biol. 1988;233:201-10 PMID: 2464906
  56. New perspectives in cell adhesion: RGD and integrins.
    Science. 1987 Oct 23;238(4826):491-7 PMID: 2821619
  57. Cell surface molecule associated with lymphocyte homing is a ubiquitinated branched-chain glycoprotein.
    Science. 1986 Feb 21;231(4740):823-9 PMID: 3003913
  58. Proteolytic degradation of extracellular matrix in tumor invasion.
    Biochim Biophys Acta. 1987 Nov 25;907(3):191-217 PMID: 2823896
  59. Transforming growth factor-beta regulates growth as well as collagen and fibronectin synthesis of human marrow fibroblasts.
    Br J Haematol. 1989 Aug;72(4):486-91 PMID: 2789074
  60. Alteration of fibronectin receptors (integrins) in phorbol ester-treated human promonocytic leukemia cells.
    Cancer Res. 1988 Oct 15;48(20):5730-7 PMID: 2971431
  61. The importance of the Mac-1, LFA-1 glycoprotein family in monocyte and granulocyte adherence, chemotaxis, and migration into inflammatory sites: insights from an experiment of nature.
    Ciba Found Symp. 1986;118:102-26 PMID: 3525036
  62. Calcium-dependent cell-cell adhesion molecules (cadherins): subclass specificities and possible involvement of actin bundles.
    J Cell Biol. 1987 Dec;105(6 Pt 1):2501-10 PMID: 3320048
  63. Neutrophilia-inducing activity in plasma of neutropenic human beings.
    Blood. 1971 Jun;37(6):647-56 PMID: 5162310
  64. Ultrastructural studies of transmural migration of blood cells in the bone marrow of rats, mice and guinea pigs.
    Am J Anat. 1972 Dec;135(4):521-35 PMID: 4637868
  65. Secretion of interleukin-1 by acute myeloblastic leukemia cells in vitro induces endothelial cells to secrete colony stimulating factors.
    Blood. 1987 Oct;70(4):1218-21 PMID: 3498521
  66. The migration of blood cells of the bone marrow through the sinusoidal wall.
    J Morphol. 1971 Apr;133(4):417-37 PMID: 5103337
  67. Phorbol ester induces diaphragmed fenestrae in large vessel endothelium in vitro.
    Eur J Cell Biol. 1987 Aug;44(1):86-9 PMID: 3622535
  68. The histophysiology of bone marrow.
    Clin Orthop Relat Res. 1967 May-Jun;52:13-23 PMID: 6048905
  69. Mapping of the bone marrow sinus endothelium with lectins and glycosylated ferritins: identification of differentiated microdomains and their functional significance.
    J Ultrastruct Res. 1983 Sep;84(3):299-310 PMID: 6655780
  70. Adaptation of marrow sinus wall to fluctuation in the rate of cell delivery: studies in rabbits after blood-letting.
    Br J Haematol. 1977 Jan;35(1):25-32 PMID: 557982
  71. An electron microscopic study of the bone marrow of the rat in an experimental myelogenous leukemia.
    Blood. 1972 Jan;39(1):99-112 PMID: 4500506
  72. Bone marrow matrix modulation of HL-60 phenotype.
    Blood. 1987 Oct;70(4):1119-23 PMID: 3477298
  73. Lineage-specific requirement of c-abl function in normal hematopoiesis.
    Science. 1989 Sep 8;245(4922):1107-10 PMID: 2672339
  74. Vascular endothelial cells and granulopoiesis: interleukin-1 stimulates release of G-CSF and GM-CSF.
    Blood. 1988 Jan;71(1):99-103 PMID: 3257150
  75. Fibronectin-plasma membrane interaction in the adhesion of hemopoietic cells.
    J Cell Biol. 1986 Aug;103(2):429-37 PMID: 2942550
  76. Altered adhesive interactions with marrow stroma of haematopoietic progenitor cells in chronic myeloid leukaemia.
    Nature. 1987 Jul 23-29;328(6128):342-4 PMID: 3474529
  77. Strain MC29 avian leukosis virus. Myelocytoma, endothelioma, and renal growths: pathomorphological and ultrastructural aspects.
    J Natl Cancer Inst. 1967 Mar;38(3):251-85 PMID: 4290185
  78. 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. 1976 Feb;145(2):183-205 PMID: 1258805
  79. Some properties of marrow derived adherent cells in tissue culture.
    Blood. 1980 Dec;56(6):1006-12 PMID: 7002230
  80. Measurement of platelet and megakaryocyte interaction with the subendothelial extracellular matrix.
    Methods Enzymol. 1989;169:76-91 PMID: 2716534
Article Info
Journal
Blut
Abbr.
Blut
ISSN
0006-5242
DOI
10.1007/BF01739426
Published
1990-07-00
Pages
3-13
Language
English
Region
Germany
NLM ID
0173401
Subset
IM
External Links
PubMed source DOI: 10.1007/BF01739426
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2