Home LiteratureArticle Details
PMID: 15790861 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

The role of hyaluronan synthase 3 in ventilator-induced lung injury.

American journal of respiratory and critical care medicine ·Vol. 172 ·No. 1 ·2005-07-01 ·Pages 92-8

Bai KJ, Spicer AP, Mascarenhas MM, Yu L, Ochoa CD, Garg HG, Quinn DA

Abstract

We recently found that low-molecular-weight hyaluronan was induced by cyclic stretch in lung fibroblasts and accumulated in lungs from animals with ventilator-induced lung injury. The low-molecular-weight hyaluronan produced by stretch increased interleukin-8 production in epithelial cells, and was accompanied by an upregulation of hyaluronan synthase-3 mRNA. We hypothesized that low-molecular-weight hyaluronan induced by high VT was dependent on hyaluronan synthase 3, and was associated with ventilator-induced lung injury. Effects of high VT ventilation in C57BL/6 wild-type and hyaluronan synthase-3 knockout mice were compared. Significantly increased neutrophil infiltration, macrophage inflammatory protein-2 production, and lung microvascular leak were found in wild-type animals ventilated with high VT. These reactions were significantly reduced in hyaluronan synthase-3 knockout mice, except the capillary leak. Wild-type mice ventilated with high VT were found to have increased low-molecular-weight hyaluronan in lung tissues and concomitant increased expression of hyaluronan synthase-3 mRNA, neither of which was found in hyaluronan synthase-3 knockout mice. We conclude that high VT induced low-molecular-weight hyaluronan production is dependent on de novo synthesis through hyaluronan synthase 3, and plays a role in the inflammatory response of ventilator-induced lung injury.

MeSH Terms
Algorithms Animals Chemokine CXCL2 Disease Models, Animal Female Glucuronosyltransferase/biosynthesis,genetics Hyaluronan Synthases Interleukin-8/metabolism Lung/enzymology Lung Diseases/enzymology,etiology Lung Injury Male Mice Mice, Inbred C57BL Mice, Knockout Monokines/metabolism Respiration, Artificial/adverse effects Tidal Volume
Chemicals
Chemokine CXCL2 Interleukin-8 Monokines Glucuronosyltransferase Has3 protein, mouse Hyaluronan Synthases
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Bai Kuan-Jen
Pulmonary and Critical Care Unit, Massachusetts General Hospital, 55 Fruit Street, Bulfinch-148, Boston, MA 02114, USA.
Spicer Andrew P
Mascarenhas Marcella M
Yu Lunyin
Ochoa Cristhiaan D
Garg Hari G
Quinn Deborah A
References (41)
41 references, click to expand
  1. Ventilation-induced chemokine and cytokine release is associated with activation of nuclear factor-kappaB and is blocked by steroids.
    Am J Respir Crit Care Med. 2001 Mar;163(3 Pt 1):711-6 PMID: 11254529
  2. Production of inflammatory cytokines in ventilator-induced lung injury: a reappraisal.
    Am J Respir Crit Care Med. 2001 Apr;163(5):1176-80 PMID: 11316656
  3. Changes in proteoglycans and lung tissue mechanics during excessive mechanical ventilation in rats.
    Am J Physiol Lung Cell Mol Physiol. 2001 Nov;281(5):L1078-87 PMID: 11597898
  4. Signaling properties of hyaluronan receptors.
    J Biol Chem. 2002 Feb 15;277(7):4589-92 PMID: 11717317
  5. Role of MAP kinase activation in interleukin-8 production by human BEAS-2B bronchial epithelial cells submitted to cyclic stretch.
    Am J Respir Cell Mol Biol. 2002 Jul;27(1):107-14 PMID: 12091253
  6. Interactions of lung stretch, hyperoxia, and MIP-2 production in ventilator-induced lung injury.
    J Appl Physiol (1985). 2002 Aug;93(2):517-25 PMID: 12133859
  7. Ventilation-induced activation of the mitogen-activated protein kinase pathway.
    Eur Respir J. 2002 Oct;20(4):946-56 PMID: 12412688
  8. Critical role for CXCR2 and CXCR2 ligands during the pathogenesis of ventilator-induced lung injury.
    J Clin Invest. 2002 Dec;110(11):1703-16 PMID: 12464676
  9. Hyaluronan in respiratory injury and repair.
    Am J Respir Crit Care Med. 2003 May 1;167(9):1169-75 PMID: 12714341
  10. Stretch-induced IL-8 depends on c-Jun NH2-terminal and nuclear factor-kappaB-inducing kinases.
    Am J Physiol Lung Cell Mol Physiol. 2003 Aug;285(2):L464-75 PMID: 12716652
  11. High tidal volume upregulates intrapulmonary cytokines in an in vivo mouse model of ventilator-induced lung injury.
    J Appl Physiol (1985). 2003 Oct;95(4):1385-93 PMID: 12807894
  12. Cyclic tensile stretch loaded on bovine chondrocytes causes depolymerization of hyaluronan: involvement of reactive oxygen species.
    Arthritis Rheum. 2003 Nov;48(11):3151-8 PMID: 14613277
  13. Low molecular weight hyaluronan from stretched lung enhances interleukin-8 expression.
    Am J Respir Cell Mol Biol. 2004 Jan;30(1):51-60 PMID: 12738686
  14. Ventilation-induced neutrophil infiltration depends on c-Jun N-terminal kinase.
    Am J Respir Crit Care Med. 2004 Feb 15;169(4):518-24 PMID: 14644930
  15. Subcellular localization of hyaluronate synthetase in oligodendroglioma cells.
    J Biol Chem. 1984 Apr 25;259(8):5017-23 PMID: 6425282
  16. 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
  17. Increased hyaluronic acid production in lung--a possible important factor in interstitial and alveolar edema during general anesthesia and in adult respiratory distress syndrome.
    Resuscitation. 1989 Jun;17(3):223-31 PMID: 2548268
  18. Lung accumulation of hyaluronan parallels pulmonary edema in experimental alveolitis.
    Am J Physiol. 1989 Dec;257(6 Pt 1):L379-84 PMID: 2481983
  19. The prognostic value of extracellular matrix component concentrations in serum during treatment of adult respiratory distress syndrome with extracorporeal CO2 removal.
    Eur J Clin Chem Clin Biochem. 1991 Dec;29(12):805-12 PMID: 1797106
  20. Hyaluronic acid-induced lymphocyte signal transduction and HA receptor (GP85/CD44)-cytoskeleton interaction.
    J Immunol. 1993 Dec 15;151(12):6634-44 PMID: 7505012
  21. Hyaluronan fragments activate an NF-kappa B/I-kappa B alpha autoregulatory loop in murine macrophages.
    J Exp Med. 1996 May 1;183(5):2373-8 PMID: 8642348
  22. Mechanical strain induces constitutive and regulated secretion of glycosaminoglycans and proteoglycans in fetal lung cells.
    J Cell Sci. 1996 Jun;109 ( Pt 6):1605-13 PMID: 8799847
  23. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44.
    J Clin Invest. 1996 Nov 15;98(10):2403-13 PMID: 8941660
  24. Injurious ventilatory strategies increase cytokines and c-fos m-RNA expression in an isolated rat lung model.
    J Clin Invest. 1997 Mar 1;99(5):944-52 PMID: 9062352
  25. Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor kappaB-dependent mechanism.
    J Biol Chem. 1997 Mar 21;272(12):8013-8 PMID: 9065473
  26. High vascular and airway pressures increase interstitial protein mRNA expression in isolated rat lungs.
    J Appl Physiol (1985). 1997 Nov;83(5):1697-705 PMID: 9375341
  27. Ventilator-induced lung injury: lessons from experimental studies.
    Am J Respir Crit Care Med. 1998 Jan;157(1):294-323 PMID: 9445314
  28. Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family.
    J Biol Chem. 1998 Jan 23;273(4):1923-32 PMID: 9442026
  29. Hyaluronan fragments synergize with interferon-gamma to induce the C-X-C chemokines mig and interferon-inducible protein-10 in mouse macrophages.
    J Biol Chem. 1998 Dec 25;273(52):35088-94 PMID: 9857043
  30. Differential regulation of extracellular matrix molecules by mechanical strain of fetal lung cells.
    Am J Physiol. 1999 May;276(5 Pt 1):L728-35 PMID: 10330028
  31. High molecular weight hyaluronic acid inhibits advanced glycation endproduct-induced NF-kappaB activation and cytokine expression.
    FEBS Lett. 1999 Jun 25;453(3):283-7 PMID: 10405161
  32. Mechanical strain-induced posttranscriptional regulation of fibronectin production in fetal lung cells.
    Am J Physiol. 1999 Jul;277(1 Pt 1):L142-9 PMID: 10409241
  33. Lung injury caused by mechanical ventilation.
    Chest. 1999 Jul;116(1 Suppl):9S-15S PMID: 10424561
  34. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties.
    J Biol Chem. 1999 Aug 27;274(35):25085-92 PMID: 10455188
  35. International consensus conferences in intensive care medicine: Ventilator-associated Lung Injury in ARDS. This official conference report was cosponsored by the American Thoracic Society, The European Society of Intensive Care Medicine, and The Societé de Réanimation de Langue Française, and was approved by the ATS Board of Directors, July 1999.
    Am J Respir Crit Care Med. 1999 Dec;160(6):2118-24 PMID: 10588637
  36. Mechanical strain increases type I collagen expression in pulmonary fibroblasts in vitro.
    J Appl Physiol (1985). 2000 Jan;88(1):203-9 PMID: 10642382
  37. Ras, protein kinase C zeta, and I kappa B kinases 1 and 2 are downstream effectors of CD44 during the activation of NF-kappa B by hyaluronic acid fragments in T-24 carcinoma cells.
    J Immunol. 2000 Feb 15;164(4):2053-63 PMID: 10657658
  38. Ventilation with lower tidal volumes as compared with traditional tidal volumes for acute lung injury and the acute respiratory distress syndrome.
    N Engl J Med. 2000 May 4;342(18):1301-8 PMID: 10793162
  39. Disruption of hyaluronan synthase-2 abrogates normal cardiac morphogenesis and hyaluronan-mediated transformation of epithelium to mesenchyme.
    J Clin Invest. 2000 Aug;106(3):349-60 PMID: 10930438
  40. Hyaluronan: a multifunctional, megaDalton, stealth molecule.
    Curr Opin Cell Biol. 2000 Oct;12(5):581-6 PMID: 10978893
  41. Aquaporin channels may modulate ventilator-induced lung injury.
    Respir Physiol. 2001 Jan;124(2):159-66 PMID: 11164207
Article Info
Journal
American journal of respiratory and critical care medicine
Abbr.
Am J Respir Crit Care Med
ISSN
1073-449X
Published
2005-07-01
Epub
2005-00-24
Pages
92-8
Language
English
Region
United States
NLM ID
9421642
PMCID
PMC2718450
Subset
IM
Grants
NHLBI NIH HHS · 2T32 HL 07874 · United States
NHLBI NIH HHS · HL 03920 · 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