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PMID: 1401082 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Cytokine regulation of human lung fibroblast hyaluronan (hyaluronic acid) production. Evidence for cytokine-regulated hyaluronan (hyaluronic acid) degradation and human lung fibroblast-derived hyaluronidase.

The Journal of clinical investigation ·Vol. 90 ·No. 4 ·1992-10-00 ·Pages 1492-503

Sampson PM, Rochester CL, Freundlich B, Elias JA

Abstract

We characterized the mechanisms by which recombinant (r) tumor necrosis factor (TNF), IFN-gamma, and IL-1, alone and in combination, regulate human lung fibroblast hyaluronic acid (HA) production. Each cytokine stimulated fibroblast HA production. The combination of rTNF and rIFN-gamma resulted in a synergistic increase in the production of high molecular weight HA. This was due to a synergistic increase in hyaluronate synthetase activity and a simultaneous decrease in HA degradation. In contrast, when rTNF and rIL-1 were combined, an additive increase in low molecular weight HA was noted. This was due to a synergistic increase in hyaluronate synthetase activity and a simultaneous increase in HA degradation. Human lung fibroblasts contained a hyaluronidase that, at pH 3.7, depolymerized high molecular weight HA to 10-40 kD end products of digestion. However, hyaluronidase activity did not correlate with fibroblast HA degradation. Instead, HA degradation correlated with fibroblast-HA binding, which was increased by rIL-1 plus rTNF and decreased by rIFN-gamma plus rTNF. Recombinant IL-1 and rTNF weakly stimulated and rIL-1 and rTNF in combination further augmented the levels of CD44 mRNA in lung fibroblasts. In contrast, rIFN-gamma did not significantly alter the levels of CD44 mRNA in unstimulated or rTNF stimulated cells. These studies demonstrate that rIL-1, rTNF, and rIFN-gamma have complex effects on biosynthesis and degradation which alter the quantity and molecular weight of the HA produced by lung fibroblasts. They also show that fibroblast HA degradation is mediated by a previously unrecognized lysosomal-type hyaluronidase whose function may be regulated by altering fibroblast-HA binding. Lastly, they suggest that the CD44 HA receptor may be involved in this process.

MeSH Terms
Adult Cells, Cultured Fibroblasts/enzymology Glucuronosyltransferase/analysis Glycosaminoglycans/metabolism Glycosyltransferases Humans Hyaluronan Synthases Hyaluronic Acid/metabolism Hyaluronoglucosaminidase/analysis Interferon-gamma/pharmacology Interleukin-1/pharmacology Lung/enzymology Membrane Proteins RNA, Messenger/analysis Receptors, Lymphocyte Homing/genetics Recombinant Proteins/pharmacology Transferases Tumor Necrosis Factor-alpha/pharmacology Xenopus Proteins
Chemicals
Glycosaminoglycans Interleukin-1 Membrane Proteins RNA, Messenger Receptors, Lymphocyte Homing Recombinant Proteins Tumor Necrosis Factor-alpha Xenopus Proteins Interferon-gamma Hyaluronic Acid Transferases Glycosyltransferases Glucuronosyltransferase HAS1 protein, Xenopus Hyaluronan Synthases Hyaluronoglucosaminidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sampson P M
Section of Pulmonary and Critical Care Medicine, Yale University School of Medicine, New Haven, Connecticut 06510.
Rochester C L
Freundlich B
Elias J A
References (53)
53 references, click to expand
  1. Human serum and synovial fluid hyaluronidase--bovine testicular hyaluronidase is not a valid substitute in drug evaluation studies.
    Biochem Pharmacol. 1976 Jul 1;25(13):1507-11 PMID: 8044
  2. Chick embryo fibroblasts produce two forms of hyaluronidase.
    J Cell Biol. 1980 May;85(2):248-57 PMID: 7372707
  3. Hyaluronic acid in the pulmonary secretions of patients with alveolar proteinosis.
    Inflammation. 1978 Jun;3(2):149-58 PMID: 738782
  4. Hyaluronidase activity of rabbit skin wound granulation tissue fibroblasts.
    J Dent Res. 1987 Jul;66(7):1283-7 PMID: 3305634
  5. Size-dependent hyaluronate degradation by cultured cells.
    J Cell Physiol. 1987 Nov;133(2):267-76 PMID: 3680390
  6. The lung parenchyma--a dynamic matrix. J. Burns Amberson lecture.
    Am Rev Respir Dis. 1985 Dec;132(6):1324-34 PMID: 3907445
  7. Hyaluronic acid production in vitro by synovial lining cells from normal and rheumatoid joints.
    Ann Rheum Dis. 1985 Oct;44(10):647-57 PMID: 4051585
  8. Connective tissue in scleroderma. A biochemical study on the correlation of fractionated glycosaminoglycans and collagen in human skin.
    Acta Derm Venereol. 1971;51(6):401-6 PMID: 4109419
  9. Novel hyaluronidase from streptomyces.
    Biochim Biophys Acta. 1970 Mar 18;198(3):607-9 PMID: 5436162
  10. Hyaluronate degradation in 3T3 and simian virus-transformed 3T3 cells.
    J Biol Chem. 1982 May 25;257(10):5821-6 PMID: 6279615
  11. Cytokines and other mediators in rheumatoid arthritis.
    Springer Semin Immunopathol. 1984;7(4):387-413 PMID: 6395411
  12. Interactions between human tumor cells and fibroblasts stimulate hyaluronate synthesis.
    Proc Natl Acad Sci U S A. 1984 Nov;81(21):6767-71 PMID: 6593727
  13. Characterization of dermatan sulfate in mucopolysaccharidosis VI. Evidence for the absence of hyaluronidase-like enzymes in human skin fibroblasts.
    Biochim Biophys Acta. 1980 Jun 5;630(1):10-4 PMID: 6770909
  14. Hyaluronic acid. An indicator of pathological conditions of human lungs?
    Inflammation. 1980 Mar;4(1):107-12 PMID: 7390611
  15. Characterization of macrophage agglutinating factor as a hyaluronic acid-protein complex.
    J Reticuloendothel Soc. 1979 Mar;25(3):269-82 PMID: 35610
  16. Physiological function of connective tissue polysaccharides.
    Physiol Rev. 1978 Jan;58(1):255-315 PMID: 414242
  17. Cell-free synthesis of hyaluronic acid in Marfan syndrome.
    J Biol Chem. 1979 Dec 10;254(23):12199-203 PMID: 500705
  18. Hyaluronidase activity during open wound healing in rabbits: a preliminary report.
    J Surg Res. 1978 Sep;25(3):256-9 PMID: 703304
  19. Absence of hyaluronidase in cultured human skin fibroblasts.
    Biochem Biophys Res Commun. 1975 Nov 3;67(1):376-82 PMID: 1201029
  20. Early changes in lung tissue hyaluronan (hyaluronic acid) and hyaluronidase in bleomycin-induced alveolitis in hamsters.
    Am Rev Respir Dis. 1991 Feb;143(2):284-8 PMID: 1703735
  21. Molecular cloning of CD44R1 and CD44R2, two novel isoforms of the human CD44 lymphocyte "homing" receptor expressed by hemopoietic cells.
    J Exp Med. 1991 Jul 1;174(1):1-5 PMID: 2056274
  22. TGF-beta enhances the production of hyaluronan in human lung but not in skin fibroblasts.
    Exp Cell Res. 1990 Jan;186(1):192-5 PMID: 2298235
  23. The localization of hyaluronan in normal and rejected human kidneys.
    Transplantation. 1990 Aug;50(2):240-3 PMID: 2382292
  24. Angiogenesis induced by degradation products of hyaluronic acid.
    Science. 1985 Jun 14;228(4705):1324-6 PMID: 2408340
  25. Cytokines in synovial fluid: II. The presence of tumour necrosis factor and interferon.
    Clin Exp Immunol. 1988 Jul;73(1):88-92 PMID: 2458872
  26. The role of a cell-associated hyaluronan-binding protein in fibroblast behaviour.
    Ciba Found Symp. 1989;143:121-33; discussion 133-7, 281-5 PMID: 2478343
  27. Changes in hyaluronan concentration in tissues and body fluids in disease states.
    Ciba Found Symp. 1989;143:233-40; discussion 240-7, 281-5 PMID: 2680345
  28. Mechanism of action of the migration stimulating factor produced by fetal and cancer patient fibroblasts: effect on hyaluronic and synthesis.
    In Vitro Cell Dev Biol. 1989 Aug;25(8):737-46 PMID: 2768134
  29. Accumulation of hyaluronan (hyaluronic acid) in the lung in adult respiratory distress syndrome.
    Am Rev Respir Dis. 1989 Mar;139(3):682-7 PMID: 2923370
  30. Increased hyaluronate synthesis is required for fibroblast detachment and mitosis.
    Biochem J. 1986 Oct 15;239(2):445-50 PMID: 3101667
  31. Hyaluronate and type III procollagen peptide concentrations in bronchoalveolar lavage fluid as markers of disease activity in farmer's lung.
    Br Med J (Clin Res Ed). 1987 Oct 3;295(6602):803-6 PMID: 3119050
  32. 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
  33. CD44 is the principal cell surface receptor for hyaluronate.
    Cell. 1990 Jun 29;61(7):1303-13 PMID: 1694723
  34. Extracellular depolymerization of hyaluronic acid in cultured human skin fibroblasts.
    Biochem Biophys Res Commun. 1990 Oct 15;172(1):70-6 PMID: 2222483
  35. IL-1 and tumor necrosis factor synergistically stimulate fibroblast IL-6 production and stabilize IL-6 messenger RNA.
    J Immunol. 1990 Jul 1;145(1):161-6 PMID: 2358670
  36. Regulation of human lung fibroblast glycosaminoglycan production by recombinant interferons, tumor necrosis factor, and lymphotoxin.
    J Clin Invest. 1988 Feb;81(2):325-33 PMID: 2448341
  37. A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins.
    Cell. 1989 Mar 24;56(6):1063-72 PMID: 2466576
  38. Circulating hyaluronate in rheumatoid arthritis: relationship to inflammatory activity and the effect of corticosteroid therapy.
    Ann Rheum Dis. 1985 Feb;44(2):83-8 PMID: 2579613
  39. 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
  40. The catabolic fate of hyaluronic acid.
    Connect Tissue Res. 1986;15(1-2):33-41 PMID: 2944700
  41. Raised serum hyaluronate levels in scleroderma: an effect of growth factor induced activation of connective tissue cells?
    Ann Rheum Dis. 1985 Sep;44(9):614-20 PMID: 3876080
  42. Gamma interferon is spontaneously released by alveolar macrophages and lung T lymphocytes in patients with pulmonary sarcoidosis.
    J Clin Invest. 1985 May;75(5):1488-95 PMID: 3923038
  43. Hyaluronate in bronchoalveolar lavage fluid: a new marker in sarcoidosis reflecting pulmonary disease.
    Br Med J (Clin Res Ed). 1985 Jun 15;290(6484):1778-81 PMID: 3924250
  44. [Detection and estimation of hyaluronic acid in the pleural fluid of mesothelioma].
    Clin Chim Acta. 1971 Jul;33(2):443-54 PMID: 4107522
  45. Glycosaminoglycans. A biochemical and clinical review.
    J Invest Dermatol. 1974 Dec;63(6):433-49 PMID: 4139221
  46. Connective tissue activation. 3. Observations on the mechanism of action of connective tissue activating peptide.
    J Lab Clin Med. 1972 Feb;79(2):285-301 PMID: 5009715
  47. Hyaluronidase activity of alveolar macrophages.
    J Histochem Cytochem. 1968 Nov;16(11):688-92 PMID: 5723776
  48. Sulfated glycosaminoglycans inhibit hyaluronic acid synthesizing activity in mouse cumuli oophori.
    Exp Cell Res. 1984 Feb;150(2):459-65 PMID: 6319167
  49. Increased biosynthesis of glycosaminoglycans by scleroderma fibroblasts in culture.
    Arthritis Rheum. 1984 Sep;27(9):1040-5 PMID: 6477654
  50. Hyaluronidase activity in embryonic chick heart muscle and cushion tissue and cells.
    Dev Biol. 1984 Dec;106(2):351-9 PMID: 6500178
  51. Release of interleukin-1 by alveolar macrophages of patients with active pulmonary sarcoidosis.
    Am Rev Respir Dis. 1984 Apr;129(4):569-72 PMID: 6608889
  52. Isolation and characterization of hyaluronidase from cultures of chick embryo skin- and muscle-derived fibroblasts.
    J Biol Chem. 1980 Feb 10;255(3):1036-42 PMID: 7356648
  53. Hyaluronic acid in the pulmonary secretions of patients with asthma.
    Biochem J. 1978 Aug 1;173(2):565-8 PMID: 697736
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1992-10-00
Pages
1492-503
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC443196
Subset
IM
Grants
NHLBI NIH HHS · HL-08805 · United States
NHLBI NIH HHS · HL-36708 · United States
NHLBI NIH HHS · HL-41216 · United States
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