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PMID: 8228819 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Macrophage colony-stimulating factor stimulates survival and chemotactic behavior in isolated osteoclasts.

The Journal of experimental medicine ·Vol. 178 ·No. 5 ·1993-11-01 ·Pages 1733-44

Fuller K, Owens JM, Jagger CJ, Wilson A, Moss R, Chambers TJ

Abstract

Macrophage colony-stimulating factor (M-CSF) is known to play an important role in osteoclast formation. However, its actions on mature cells have not been fully characterized. We now report that M-CSF dramatically stimulates osteoclastic motility and spreading; osteoclasts responded to a gradient of M-CSF with orientation, and random cell polarization occurred after isotropic exposure. M-CSF also supported the survival of osteoclasts by preventing apoptosis. Paradoxically, M-CSF inhibits bone resorption by isolated osteoclasts. We found that this was effected predominantly by reduction in the number of excavations. Thus, M-CSF showed a propensity to suppress resorption through a reduction in the proportion of cells that were resorbing bone. Our data suggest that apart from the established role of M-CSF in the provision of precursors for osteoclastic induction, a major role for M-CSF in bone resorption is to enhance osteoclastic survival, migration, and chemotaxis. It seems appropriate that during these processes resorptive functions should be suppressed. We suggest that M-CSF continues to modulate osteoclastic activity once osteoclasts are on resorptive sites, through regulation of the balance between resorption and migration, such that not only the quantity, but the spatial pattern of resorption can be controlled by adjacent M-CSF-secreting cells of osteoblastic lineage.

MeSH Terms
Animals Animals, Newborn Apoptosis/drug effects Bone Resorption Cell Survival/drug effects Cells, Cultured Chemotaxis/drug effects Humans Macrophage Colony-Stimulating Factor/pharmacology Mice Mice, Inbred Strains Microscopy, Electron Microscopy, Electron, Scanning Microscopy, Phase-Contrast Osteoclasts/cytology,drug effects,physiology,ultrastructure Rats Rats, Wistar Recombinant Proteins/pharmacology
Chemicals
Recombinant Proteins Macrophage Colony-Stimulating Factor
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Fuller K
Department of Histopathology, St. George's Hospital Medical School, London, United Kingdom.
Owens J M
Jagger C J
Wilson A
Moss R
Chambers T J
References (49)
49 references, click to expand
  1. Hematopoietic growth factors.
    J Clin Invest. 1987 Jun;79(6):1549-57 PMID: 3034976
  2. Macrophage colony stimulating factor (M-CSF) is essential for osteoclast formation in vitro.
    Biochem Biophys Res Commun. 1991 May 31;177(1):526-31 PMID: 2043138
  3. The effects of inhibitors of cysteine-proteinases and collagenase on the resorptive activity of isolated osteoclasts.
    Bone. 1987;8(5):305-13 PMID: 2827713
  4. Induction of monocyte migration by recombinant macrophage colony-stimulating factor.
    J Immunol. 1988 Jul 15;141(2):575-9 PMID: 3290341
  5. Human macrophage colony-stimulating factor inhibits bone resorption by osteoclasts disaggregated from rat bone.
    J Cell Physiol. 1988 Oct;137(1):199-203 PMID: 3262621
  6. Cellular and molecular mechanisms in the regulation and function of osteoclasts.
    Vitam Horm. 1991;46:41-86 PMID: 1660641
  7. An assessment of the prevalence of organic material on bone surfaces.
    Calcif Tissue Int. 1992 Feb;50(2):118-22 PMID: 1571829
  8. Derivation of osteoclasts from hematopoietic colony-forming cells in culture.
    J Bone Miner Res. 1992 Mar;7(3):353-62 PMID: 1585838
  9. Macrophage colony-stimulating factor (CSF-1) enhances invasiveness in CSF-1 receptor-positive carcinoma cell lines.
    Cancer Res. 1992 Jul 1;52(13):3661-6 PMID: 1535551
  10. Macrophage colony stimulating factor controls macrophage recruitment to the cycling mouse uterus.
    Dev Biol. 1992 Aug;152(2):336-43 PMID: 1644224
  11. Detection of transcripts for the receptor for macrophage colony-stimulating factor, c-fms, in murine osteoclasts.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9637-41 PMID: 1409676
  12. Delayed hematopoietic development in osteopetrotic (op/op) mice.
    J Exp Med. 1993 Jan 1;177(1):237-42 PMID: 8418205
  13. Transient recruitment of osteoclasts and expression of their function in osteopetrotic (op/op) mice by a single injection of macrophage colony-stimulating factor.
    J Bone Miner Res. 1993 Jan;8(1):45-50 PMID: 8427048
  14. Detection of collagenase mRNA in odontoclasts of bovine root-resorbing tissue by in situ hybridization.
    Calcif Tissue Int. 1993 Apr;52(4):325-30 PMID: 8467413
  15. Generation of osteoclast-inductive and osteoclastogenic cell lines from the H-2KbtsA58 transgenic mouse.
    Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5578-82 PMID: 8390670
  16. Leucocyte locomotion: behavioural mechanisms for accumulation.
    J Cell Sci Suppl. 1987;8:103-19 PMID: 3332656
  17. Sensory adaptation of leukocytes to chemotactic peptides.
    J Cell Biol. 1979 Aug;82(2):517-27 PMID: 479314
  18. Scanning electron microscopy of rachitic rat bone.
    Scan Electron Microsc. 1979;(2):513-20 PMID: 524022
  19. Stimulation of macrophage plasminogen activator activity by colony-stimulating factors.
    J Cell Physiol. 1980 Jun;103(3):435-45 PMID: 6967488
  20. Production of lymphocyte-activating factor (Interleukin 1) by macrophages activated with colony-stimulating factors.
    J Immunol. 1980 Sep;125(3):1302-5 PMID: 6774016
  21. Role of osteoblasts in hormonal control of bone resorption--a hypothesis.
    Calcif Tissue Int. 1981;33(4):349-51 PMID: 6271355
  22. Calcitonin alters behaviour of isolated osteoclasts.
    J Pathol. 1982 Jan;136(1):27-39 PMID: 7057295
  23. Survival of mononuclear phagocytes depends on a lineage-specific growth factor that the differentiated cells selectively destroy.
    Cell. 1982 Jan;28(1):71-81 PMID: 6978185
  24. Osteoblasts release osteoclasts from calcitonin-induced quiescence.
    J Cell Sci. 1982 Oct;57:247-60 PMID: 6759515
  25. The mononuclear phagocyte system of the mouse defined by immunohistochemical localization of antigen F4/80: macrophages of bone and associated connective tissue.
    J Cell Sci. 1984 Mar;66:189-94 PMID: 6378941
  26. The effect of calcium-regulating hormones and prostaglandins on bone resorption by osteoclasts disaggregated from neonatal rabbit bones.
    Endocrinology. 1985 Jan;116(1):234-9 PMID: 3880540
  27. Effect of substrate composition on bone resorption by rabbit osteoclasts.
    J Cell Sci. 1984 Aug;70:61-71 PMID: 6501437
  28. Sex differences in bone resorption: a scanning electron microscopic study of mouse parietal bones.
    Arch Histol Jpn. 1984 Oct;47(4):429-40 PMID: 6542771
  29. Osteoclasts: putative, surrogate and authentic.
    J Pathol. 1984 Dec;144(4):295-6 PMID: 6520653
  30. Abundant calcitonin receptors in isolated rat osteoclasts. Biochemical and autoradiographic characterization.
    J Clin Invest. 1986 Aug;78(2):355-60 PMID: 3016026
  31. Macrophage growth factor CSF-1 stimulates human monocyte production of interferon, tumor necrosis factor, and colony stimulating activity.
    J Immunol. 1986 Oct 1;137(7):2281-5 PMID: 2428865
  32. Osteoclasts and osteoblasts migrate in opposite directions in response to a constant electrical field.
    J Cell Physiol. 1986 Dec;129(3):283-8 PMID: 3782308
  33. Ability of polymorphonuclear leukocytes to orient in gradients of chemotactic factors.
    J Cell Biol. 1977 Nov;75(2 Pt 1):606-16 PMID: 264125
  34. Chemotaxis in eukaryotic cells: a focus on leukocytes and Dictyostelium.
    Annu Rev Cell Biol. 1988;4:649-86 PMID: 2848555
  35. Calcitonin receptors as markers for osteoclastic differentiation: correlation between generation of bone-resorptive cells and cells that express calcitonin receptors in mouse bone marrow cultures.
    Endocrinology. 1989 Sep;125(3):1606-12 PMID: 2547591
  36. Generation of osteoclasts from hemopoietic cells and a multipotential cell line in vitro.
    J Cell Physiol. 1989 Sep;140(3):478-82 PMID: 2777887
  37. The bone marrow-derived stromal cell lines MC3T3-G2/PA6 and ST2 support osteoclast-like cell differentiation in cocultures with mouse spleen cells.
    Endocrinology. 1989 Oct;125(4):1805-13 PMID: 2676473
  38. The osteoclast functional antigen, implicated in the regulation of bone resorption, is biochemically related to the vitronectin receptor.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1817-26 PMID: 2477382
  39. Apoptosis. The role of the endonuclease.
    Am J Pathol. 1990 Mar;136(3):593-608 PMID: 2156431
  40. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene.
    Nature. 1990 May 31;345(6274):442-4 PMID: 2188141
  41. Total absence of colony-stimulating factor 1 in the macrophage-deficient osteopetrotic (op/op) mouse.
    Proc Natl Acad Sci U S A. 1990 Jun;87(12):4828-32 PMID: 2191302
  42. Identification of plasminogen activator in osteoclasts.
    J Bone Miner Res. 1990 May;5(5):499-505 PMID: 2114731
  43. Macrophage-colony-stimulating factor (CSF-1) induces proliferation, chemotaxis, and reversible monocytic differentiation in myeloid progenitor cells transfected with the human c-fms/CSF-1 receptor cDNA.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5613-7 PMID: 2165597
  44. Colony stimulating factor-1 is a negative regulator of the macrophage respiratory burst.
    J Cell Physiol. 1990 Aug;144(2):190-6 PMID: 2199464
  45. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells.
    Proc Natl Acad Sci U S A. 1990 Sep;87(18):7260-4 PMID: 2169622
  46. Macrophage colony stimulating factor restores in vivo bone resorption in the op/op osteopetrotic mouse.
    Endocrinology. 1990 Nov;127(5):2592-4 PMID: 2146111
  47. Congenital osteoclast deficiency in osteopetrotic (op/op) mice is cured by injections of macrophage colony-stimulating factor.
    J Exp Med. 1991 Jan 1;173(1):269-72 PMID: 1985123
  48. Deficiency of osteoclasts in osteopetrotic mice is due to a defect in the local microenvironment provided by osteoblastic cells.
    Endocrinology. 1991 Apr;128(4):1792-6 PMID: 2004603
  49. Murine osteoblastlike cells and the osteogenic cell MC3T3-E1 release a macrophage colony-stimulating activity in culture.
    Calcif Tissue Int. 1987 Sep;41(3):151-6 PMID: 3117342
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1993-11-01
Pages
1733-44
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2191238
Subset
IM
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