Home LiteratureArticle Details
PMID: 8456940 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Macrophages and fibroblasts express embryonic fibronectins during cutaneous wound healing.

The American journal of pathology ·Vol. 142 ·No. 3 ·1993-03-00 ·Pages 793-801

Brown LF, Dubin D, Lavigne L, Logan B, Dvorak HF, Van de Water L

Abstract

Fibronectins (FN) comprise a family of adhesive glycoproteins that are prominent components of wound healing. These proteins arise by alternative splicing of a single gene transcript at three sites, termed EIIIA, EIIIB, and V. Extravasated plasma FN, which lacks the EIIIA and EIIIB domains, along with fibrin, comprise the "provisional" matrix that forms within minutes of tissue injury. By 2 days after cutaneous excisional wounding in rats, total FN messenger RNA (mRNA) expression is increased locally and dramatically within the surrounding dermis, in the subjacent muscle (panniculus carnosus) and, notably, at the wound margins. Moreover, in contrast to normal skin, 2-day wounds express EIIIA- and EIIIB-containing "embryonic" FN mRNAs. To identify the cells responsible for synthesizing the various FN isoforms, we performed in situ hybridization with probes for the various FN mRNAs. Collagen and lysozyme probes were employed to distinguish fibroblasts from macrophages. At early intervals (2 days) after wounding, macrophages were the principal cells that expressed FN mRNA. Moreover, many of these cells expressed embryonic FN mRNAs. At 7 to 10 days, when the wound defect was maturing, fibroblasts were the major cells synthesizing these embryonic FNs. It is widely accepted that wound macrophages phagocytose debris and provide degradative enzymes and cytokines essential for early stages of tissue repair. Our findings suggest an additional function for wound macrophages--synthesis of embryonic FNs providing an extracellular matrix that facilitates wound repair, perhaps by promoting cell migration.

MeSH Terms
Animals Base Sequence Embryo, Mammalian/metabolism Female Fibroblasts/metabolism Fibronectins/genetics,metabolism Macrophages/metabolism Mice Mice, Inbred BALB C Molecular Probes/genetics Molecular Sequence Data RNA Splicing RNA, Messenger/metabolism Rats Rats, Inbred Strains Skin/metabolism,pathology Wound Healing/physiology
Chemicals
Fibronectins Molecular Probes RNA, Messenger
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Brown L F
Department of Pathology, Beth Israel Hospital, Boston, MA 02215.
Dubin D
Lavigne L
Logan B
Dvorak H F
Van de Water L
References (45)
45 references, click to expand
  1. Action of fibrin-stabilizing factor on cold-insoluble globulin and alpha2-macroglobulin in clotting plasma.
    J Biol Chem. 1976 Mar 25;251(6):1639-45 PMID: 56335
  2. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  3. Fibronectin is produced by human macrophages.
    J Exp Med. 1980 Mar 1;151(3):602-13 PMID: 7359083
  4. Phagocytosis of gelatin-latex particles by a murine macrophage line is dependent on fibronectin and heparin.
    J Cell Biol. 1981 Jul;90(1):32-9 PMID: 7251676
  5. Human alveolar macrophage fibronectin: synthesis, secretion, and ultrastructural localization during gelatin-coated latex particle binding.
    J Cell Biol. 1981 Sep;90(3):711-20 PMID: 7287821
  6. In vivo co-distribution of fibronectin and actin fibers in granulation tissue: immunofluorescence and electron microscope studies of the fibronexus at the myofibroblast surface.
    J Cell Biol. 1984 Jun;98(6):2091-106 PMID: 6373789
  7. Monocytes and macrophages synthesize and secrete thrombospondin.
    Blood. 1985 Jan;65(1):79-84 PMID: 3965054
  8. Fibronectin and wound healing.
    J Cell Biochem. 1984;26(2):107-16 PMID: 6084665
  9. Secretory products of macrophages.
    J Clin Invest. 1987 Feb;79(2):319-26 PMID: 3543052
  10. Transforming growth factor-beta increases steady state levels of type I procollagen and fibronectin messenger RNAs posttranscriptionally in cultured human dermal fibroblasts.
    J Clin Invest. 1987 Apr;79(4):1285-8 PMID: 3470308
  11. Regulation of fibronectin and type I collagen mRNA levels by transforming growth factor-beta.
    J Biol Chem. 1987 May 15;262(14):6443-6 PMID: 3471760
  12. Identification of two distinct regions of the type III connecting segment of human plasma fibronectin that promote cell type-specific adhesion.
    J Biol Chem. 1987 May 15;262(14):6886-92 PMID: 3571291
  13. Expression and secretion of type beta transforming growth factor by activated human macrophages.
    Proc Natl Acad Sci U S A. 1987 Sep;84(17):6020-4 PMID: 2888109
  14. Newt epidermal cell migration in vitro and in vivo appears to involve Arg-Gly-Asp-Ser receptors.
    J Cell Sci. 1987 May;87 ( Pt 4):525-34 PMID: 3654790
  15. Multiple sites of alternative splicing of the rat fibronectin gene transcript.
    EMBO J. 1987 Sep;6(9):2573-80 PMID: 2445560
  16. Modulation of fibronectin gene expression in human mononuclear phagocytes.
    J Clin Invest. 1987 Dec;80(6):1720-7 PMID: 3680524
  17. Alternative splicing of chicken fibronectin in embryos and in normal and transformed cells.
    Mol Cell Biol. 1987 Dec;7(12):4297-307 PMID: 2830487
  18. Transforming growth factor beta stimulates the expression of fibronectin and of both subunits of the human fibronectin receptor by cultured human lung fibroblasts.
    J Biol Chem. 1988 Apr 5;263(10):4586-92 PMID: 2965146
  19. Cloning the human lysozyme cDNA: inverted Alu repeat in the mRNA and in situ hybridization for macrophages and Paneth cells.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6227-31 PMID: 3413092
  20. Mouse lysozyme M gene: isolation, characterization, and expression studies.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6232-6 PMID: 3413093
  21. Secreted phosphoproteins associated with neoplastic transformation: close homology with plasma proteins cleaved during blood coagulation.
    Cancer Res. 1988 Oct 15;48(20):5770-4 PMID: 3167835
  22. Fibronectin and its receptors.
    Annu Rev Biochem. 1988;57:375-413 PMID: 2972252
  23. Extracellular matrix assembly.
    Annu Rev Cell Biol. 1988;4:183-207 PMID: 2848551
  24. Endothelial cell behavior after denudation injury is modulated by transforming growth factor-beta1 and fibronectin.
    Lab Invest. 1989 Jun;60(6):755-65 PMID: 2659888
  25. Reappearance of an embryonic pattern of fibronectin splicing during wound healing in the adult rat.
    J Cell Biol. 1989 Aug;109(2):903-14 PMID: 2760116
  26. Patterns of fibronectin gene expression and splicing during cell migration in chicken embryos.
    Development. 1988 Nov;104(3):369-82 PMID: 3256468
  27. Secretory products of phagocytes.
    Curr Opin Immunol. 1988 Sep-Oct;1(1):47-55 PMID: 3077299
  28. Regrowth of arterial endothelium. Denudation with minimal trauma leads to complete endothelial cell regrowth.
    Lab Invest. 1989 Nov;61(5):556-63 PMID: 2811304
  29. Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo.
    Development. 1989 Jun;106(2):375-88 PMID: 2591321
  30. Transforming growth factor-beta regulates the splicing pattern of fibronectin messenger RNA precursor.
    FEBS Lett. 1990 Feb 12;261(1):175-8 PMID: 2307231
  31. Fibronectins: structure, functions and receptors.
    Curr Opin Cell Biol. 1989 Oct;1(5):956-63 PMID: 2534045
  32. Fibronectin matrix deposition and fibronectin receptor expression in healing and normal skin.
    J Invest Dermatol. 1990 Jun;94(6 Suppl):128S-134S PMID: 2161886
  33. Co-assembly of plasma and cellular fibronectins into fibrils in human fibroblast cultures.
    J Cell Biol. 1990 Jul;111(1):249-56 PMID: 2114411
  34. Changes in keratinocyte adhesion during terminal differentiation: reduction in fibronectin binding precedes alpha 5 beta 1 integrin loss from the cell surface.
    Cell. 1990 Oct 19;63(2):425-35 PMID: 2145076
  35. Activation of human keratinocyte migration on type I collagen and fibronectin.
    J Cell Sci. 1990 Jun;96 ( Pt 2):197-205 PMID: 2145292
  36. Macrophage heterogeneity occurs through a developmental mechanism.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1963-7 PMID: 1705715
  37. Tissue-specific splicing pattern of fibronectin messenger RNA precursor during development and aging in rat.
    J Cell Biol. 1991 Jun;113(5):1223-9 PMID: 2040649
  38. Cytokines in context.
    J Cell Biol. 1991 Jun;113(5):981-6 PMID: 2040651
  39. The alternative splicing of fibronectin pre-mRNA is altered during aging and in response to growth factors.
    J Biol Chem. 1991 Aug 5;266(22):14654-62 PMID: 1713586
  40. Transforming growth factor beta 1 is present at sites of extracellular matrix gene expression in human pulmonary fibrosis.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6642-6 PMID: 1862087
  41. Polarized regulation of fibronectin secretion and alternative splicing by transforming growth factor.
    J Biol Chem. 1991 Aug 25;266(24):15598-601 PMID: 1874718
  42. Mouse macrophage clones immortalized by retroviruses are functionally heterogeneous.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7543-7 PMID: 1715569
  43. Alternative splicing of fibronectin: three variants, three functions.
    Bioessays. 1991 Oct;13(10):527-33 PMID: 1755828
  44. Identification and characterization of alternatively spliced fibronectin mRNAs expressed in early Xenopus embryos.
    Dev Biol. 1992 Feb;149(2):357-69 PMID: 1730390
  45. The alternatively spliced V region contributes to the differential incorporation of plasma and cellular fibronectins into fibrin clots.
    J Cell Biol. 1992 Nov;119(4):923-33 PMID: 1358897
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
0002-9440
Published
1993-03-00
Pages
793-801
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC1886786
Subset
IM
Grants
NCI NIH HHS · CA28471 · United States
NIGMS NIH HHS · GM36812 · United States
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