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PMID: 8514850 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-alpha-dependent mechanism in murine macrophages.

The Journal of clinical investigation ·Vol. 91 ·No. 6 ·1993-06-00 ·Pages 2368-77

Noble PW, Lake FR, Henson PM, Riches DW

Abstract

Macrophages participate in inflammatory and repair processes in part through the selective release of cytokines that contribute to tissue remodeling. Extracellular matrix components generated at inflammatory sites may influence tissue remodeling by effects on leukocyte adherence and local cytokine production. In murine bone marrow-derived macrophages, we found that soluble hyaluronic acid stimulated IL-1 beta, TNF alpha, and insulin-like growth factor-1 (IGF-1) mRNA transcript expression as well as IGF-1 protein synthesis. Monoclonal antibodies to the hyaluronic acid receptor CD44 blocked the effects of hyaluronic acid on IL-1 beta, TNF alpha, and IGF-1 expression. TNF alpha and IL-1 beta mRNA expression preceded IGF-1 protein synthesis, and TNF alpha, but not IL-1 beta, was found to directly stimulate IGF-1. Furthermore, IGF-1 induction was dependent on endogenous TNF alpha production since IGF-1 protein synthesis was inhibited in the presence of anti-TNF alpha antiserum. In addition, IL-1 beta was found to exert a regulatory role on IGF-1 production by enhancing the TNF alpha effect. IL-1 beta and TNF alpha mRNA transcript expression as well as IGF-1 protein synthesis were also stimulated by chrysotile asbestos. Anti-CD44 antibodies had no effect whereas anti-TNF alpha antiserum blocked asbestos-stimulated IGF-1 production. These results indicate that hyaluronate activation of CD44 induces cytokine expression and macrophage-derived IGF-1 production is dependent on TNF alpha expression.

MeSH Terms
Animals Asbestos/pharmacology Extracellular Matrix Female Fibrosis/etiology Gene Expression Regulation Growth Substances/biosynthesis Hyaluronic Acid/pharmacology Inflammation/etiology Insulin-Like Growth Factor I/biosynthesis Interleukin-1/biosynthesis Macrophages/drug effects Mice Mice, Inbred C3H RNA, Messenger/biosynthesis Receptors, Lymphocyte Homing/metabolism Tumor Necrosis Factor-alpha/biosynthesis
Chemicals
Growth Substances Interleukin-1 RNA, Messenger Receptors, Lymphocyte Homing Tumor Necrosis Factor-alpha Asbestos Insulin-Like Growth Factor I Hyaluronic Acid
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Noble P W
Department of Pediatrics, National Jewish Center for Immunology and Respiratory Medicine, Denver, Colorado 80206.
Lake F R
Henson P M
Riches D W
References (62)
62 references, click to expand
  1. Dual control of cell growth by somatomedins and platelet-derived growth factor.
    Proc Natl Acad Sci U S A. 1979 Mar;76(3):1279-83 PMID: 312500
  2. Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression.
    J Cell Biol. 1989 Aug;109(2):877-89 PMID: 2547805
  3. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  4. The glycosaminoglycans of open wounds.
    J Surg Res. 1980 Nov;29(5):422-9 PMID: 7421186
  5. Inhibition of phagocytosis by high molecular weight hyaluronate.
    Immunology. 1980 Jul;40(3):435-46 PMID: 7429537
  6. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201-5 PMID: 6159641
  7. Murine cell surface glycoproteins. Characterization of a major component of 80,000 daltons as a polymorphic differentiation antigen of mesenchymal cells.
    J Biol Chem. 1981 Jul 10;256(13):7023-7 PMID: 6787057
  8. Studies on glycosaminoglycans of regenerating rabbit ear cartilage.
    Dev Biol. 1981 Aug;86(1):198-205 PMID: 6793423
  9. Production of fibronectin by the human alveolar macrophage: mechanism for the recruitment of fibroblasts to sites of tissue injury in interstitial lung diseases.
    Proc Natl Acad Sci U S A. 1981 Nov;78(11):7147-51 PMID: 6947279
  10. Human alveolar macrophage growth factor for fibroblasts. Regulation and partial characterization.
    J Clin Invest. 1982 Oct;70(4):806-22 PMID: 7119116
  11. Growth factors in wound healing. Single and synergistic effects on partial thickness porcine skin wounds.
    J Clin Invest. 1989 Aug;84(2):640-6 PMID: 2788174
  12. Tumor necrosis factor/cachectin plays a key role in bleomycin-induced pneumopathy and fibrosis.
    J Exp Med. 1989 Sep 1;170(3):655-63 PMID: 2475571
  13. Hyaluronan (hyaluronic acid) in bronchoalveolar lavage fluid during the development of bleomycin-induced alveolitis in the rat.
    Am Rev Respir Dis. 1989 Oct;140(4):1028-32 PMID: 2478053
  14. Secretory products of phagocytes.
    Curr Opin Immunol. 1988 Sep-Oct;1(1):47-55 PMID: 3077299
  15. The cDNA sequence of mouse Pgp-1 and homology to human CD44 cell surface antigen and proteoglycan core/link proteins.
    J Biol Chem. 1990 Jan 5;265(1):341-7 PMID: 2403559
  16. Antibodies against the CD44 p80, lymphocyte homing receptor molecule augment human peripheral blood T cell activation.
    J Immunol. 1990 Jan 1;144(1):7-15 PMID: 1967267
  17. Warner-Lambert/Parke-Davis Award lecture. Cellular and molecular mechanisms that direct leukocyte traffic.
    Am J Pathol. 1990 Jan;136(1):3-11 PMID: 2404417
  18. CD44--a molecule involved in leukocyte adherence and T-cell activation.
    Immunol Today. 1989 Dec;10(12):423-8 PMID: 2695102
  19. Monoclonal antibodies to Pgp-1/CD44 block lympho-hemopoiesis in long-term bone marrow cultures.
    J Exp Med. 1990 Feb 1;171(2):477-88 PMID: 2406365
  20. Proteinases and extracellular matrix remodeling.
    Curr Opin Cell Biol. 1989 Oct;1(5):974-82 PMID: 2697298
  21. Requirement of tumour necrosis factor for development of silica-induced pulmonary fibrosis.
    Nature. 1990 Mar 15;344(6263):245-7 PMID: 2156165
  22. Binding of hyaluronic acid to lymphoid cell lines is inhibited by monoclonal antibodies against Pgp-1.
    Exp Cell Res. 1990 Apr;187(2):224-33 PMID: 2180732
  23. Hyaluronate can function as a cell adhesion molecule and CD44 participates in hyaluronate recognition.
    J Exp Med. 1990 Jul 1;172(1):69-75 PMID: 2193100
  24. Insulin-like growth factors and their binding proteins.
    Physiol Rev. 1990 Jul;70(3):591-614 PMID: 1694588
  25. CD44 is the principal cell surface receptor for hyaluronate.
    Cell. 1990 Jun 29;61(7):1303-13 PMID: 1694723
  26. Regulation of human monocyte/macrophage function by extracellular matrix. Adherence of monocytes to collagen matrices enhances phagocytosis of opsonized bacteria by activation of complement receptors and enhancement of Fc receptor function.
    J Clin Invest. 1990 Sep;86(3):703-14 PMID: 2168442
  27. LFA-3, CD44, and CD45: physiologic triggers of human monocyte TNF and IL-1 release.
    Science. 1990 Sep 14;249(4974):1295-7 PMID: 1697984
  28. IL-5 induces a Pgp-1 (CD44) bright B cell subpopulation that is highly enriched in proliferative and Ig secretory activity and binds to hyaluronate.
    J Immunol. 1990 Dec 1;145(11):3618-27 PMID: 2246506
  29. Insulin-like growth factor-1 (IGF-1) mRNA expression in bone marrow derived macrophages is stimulated by chrysotile asbestos and bleomycin. A potential marker for a reparative macrophage phenotype.
    Chest. 1991 Mar;99(3 Suppl):79S-80S PMID: 1705203
  30. Cytokines in context.
    J Cell Biol. 1991 Jun;113(5):981-6 PMID: 2040651
  31. Secretion of insulinlike growth factor I and insulinlike growth factor-binding proteins by murine bone marrow stromal cells.
    J Clin Invest. 1991 Aug;88(2):470-5 PMID: 1713920
  32. The two different receptors for tumor necrosis factor mediate distinct cellular responses.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9292-6 PMID: 1718003
  33. Measurement of an adhesion molecule as an indicator of inflammatory disease activity. Up-regulation of the receptor for hyaluronate (CD44) in rheumatoid arthritis.
    Arthritis Rheum. 1991 Nov;34(11):1434-43 PMID: 1719988
  34. Variations in the cytoskeletal interaction and posttranslational modification of the CD44 homing receptor in macrophages.
    J Cell Biol. 1991 Dec;115(5):1283-92 PMID: 1955476
  35. Expression of interferon-beta during the triggering phase of macrophage cytocidal activation. Evidence for an autocrine/paracrine role in the regulation of this state.
    J Biol Chem. 1991 Dec 25;266(36):24785-92 PMID: 1761573
  36. Murine cell surface glycoproteins. Purification of the polymorphic Pgp-1 antigen and analysis of its expression on macrophages and other myeloid cells.
    J Biol Chem. 1983 Jan 25;258(2):1014-21 PMID: 6822490
  37. Characterization and identification of the hyaluronate binding site from membranes of SV-3T3 cells.
    J Biol Chem. 1985 Jul 5;260(13):8128-33 PMID: 2989277
  38. Fibroblast growth enhancing activity of tumor necrosis factor and its relationship to other polypeptide growth factors.
    J Exp Med. 1986 Mar 1;163(3):632-43 PMID: 3512757
  39. Hyaluronic acid is an endogenous inducer of interleukin-1 production by human monocytes and rabbit macrophages.
    Biochem Biophys Res Commun. 1986 Oct 30;140(2):715-22 PMID: 3490850
  40. Tumor necrosis factor and interleukin 1: cytokines with multiple overlapping biological activities.
    Lab Invest. 1987 Mar;56(3):234-48 PMID: 3029503
  41. The hyaluronate receptor is associated with actin filaments.
    J Cell Biol. 1987 Sep;105(3):1395-404 PMID: 2443509
  42. Tumor necrosis factor alpha inhibits collagen gene transcription and collagen synthesis in cultured human fibroblasts.
    J Biol Chem. 1988 Apr 25;263(12):5841-5 PMID: 3258601
  43. Wound macrophages express TGF-alpha and other growth factors in vivo: analysis by mRNA phenotyping.
    Science. 1988 Aug 5;241(4866):708-12 PMID: 3041594
  44. Requirements for hyaluronic acid binding by CD44: a role for the cytoplasmic domain and activation by antibody.
    J Exp Med. 1992 Jan 1;175(1):257-66 PMID: 1730918
  45. Stimulation of human monocytes via CD45, CD44, and LFA-3 triggers macrophage-colony-stimulating factor production. Synergism with lipopolysaccharide and IL-1 beta.
    J Immunol. 1992 Feb 15;148(4):1113-8 PMID: 1371132
  46. Tumour necrosis factor alpha restores granulomas and induces parasite egg-laying in schistosome-infected SCID mice.
    Nature. 1992 Apr 16;356(6370):604-7 PMID: 1560843
  47. Tumor necrosis factor alpha is an autocrine growth regulator during macrophage differentiation.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4754-8 PMID: 1374912
  48. Shedding of the CD44 adhesion molecule from leukocytes induced by anti-CD44 monoclonal antibody simulating the effect of a natural receptor ligand.
    J Immunol. 1992 Aug 1;149(3):747-53 PMID: 1634766
  49. Receptor-specific induction of insulin-like growth factor I in human monocytes by advanced glycosylation end product-modified proteins.
    J Clin Invest. 1992 Aug;90(2):439-46 PMID: 1322940
  50. CD44 can be activated to function as an hyaluronic acid receptor in normal murine T cells.
    Eur J Immunol. 1992 Oct;22(10):2719-23 PMID: 1382996
  51. Molecular isoforms of murine CD44 and evidence that the membrane proximal domain is not critical for hyaluronate recognition.
    J Cell Biol. 1992 Dec;119(6):1711-9 PMID: 1469058
  52. Participation of hyaluronic acid in the macrophage disappearance reaction.
    Immunol Commun. 1980;9(4):357-70 PMID: 7409854
  53. Aggregation of macrophages and fibroblasts is inhibited by a monoclonal antibody to the hyaluronate receptor.
    Exp Cell Res. 1988 Oct;178(2):224-32 PMID: 2458949
  54. Alveolar macrophages release an insulin-like growth factor I-type molecule.
    J Clin Invest. 1988 Nov;82(5):1685-93 PMID: 3183063
  55. Distribution of hyaluronate and hyaluronate receptors in the adult lung.
    J Cell Sci. 1988 May;90 ( Pt 1):145-56 PMID: 2461953
  56. Stimulation of glycosaminoglycan synthesis in cultured human dermal fibroblasts by interleukin 1. Induction of hyaluronic acid synthesis by natural and recombinant interleukin 1s and synthetic interleukin 1 beta peptide 163-171.
    J Clin Invest. 1989 Feb;83(2):629-36 PMID: 2783590
  57. Human monocyte inflammatory mediator gene expression is selectively regulated by adherence substrates.
    J Immunol. 1989 Mar 15;142(6):1970-6 PMID: 2784145
  58. Accumulation of hyaluronic acid in the alveolar interstitial tissue in bleomycin-induced alveolitis.
    Am Rev Respir Dis. 1989 Mar;139(3):759-62 PMID: 2466429
  59. Hyaluronan and type III procollagen peptide concentrations in bronchoalveolar lavage fluid in idiopathic pulmonary fibrosis.
    Thorax. 1989 Feb;44(2):126-31 PMID: 2928996
  60. Asbestos fibers and silica particles stimulate rat alveolar macrophages to release tumor necrosis factor. Autoregulatory role of leukotriene B4.
    Am Rev Respir Dis. 1989 May;139(5):1257-64 PMID: 2540688
  61. Cultured human fibroblasts secrete insulin-like growth factor IA prohormone.
    J Clin Endocrinol Metab. 1989 Jul;69(1):25-30 PMID: 2732297
  62. Binding of hyaluronate to the surface of cultured cells.
    J Cell Biol. 1979 Aug;82(2):475-84 PMID: 479311
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
DOI
10.1172/JCI116469
Published
1993-06-00
Pages
2368-77
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC443294
Subset
IM
Grants
NHLBI NIH HHS · HL-27353 · United States
External Links
PubMed source DOI: 10.1172/JCI116469 PMC Full Text View journal details
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