Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1990 Mar;85(3):668–673. doi: 10.1172/JCI114490

Accumulation of hyaluronan (hyaluronic acid) in myocardial interstitial tissue parallels development of transplantation edema in heart allografts in rats.

R Hällgren 1, B Gerdin 1, A Tengblad 1, G Tufveson 1
PMCID: PMC296481  PMID: 2312720

Abstract

By using biotin-labeled proteoglycan core protein, hyaluronan (hyaluronic acid; HA) was visualized in rat heart grafts at different times (2, 4, and 6 d) after transplantation. In normal, nontransplanted hearts HA was present in the adventitia of arteries and veins and in the myocardial interstitial tissue. An increased accumulation of HA was evident in the edematous interstitial tissue, infiltrated with lymphocytes, on day 4 after allogeneic transplantation, and was even more pronounced by day 6. No apparent increase in HA was seen in syngeneic grafts. Biochemical assay of HA in heart tissue demonstrated that the myocardial content of HA had increased 60% by day 2 after transplantation in allogeneic as well as syngeneic grafts, indicating that surgical trauma may induce some HA accumulation in heart grafts. The extractable amount of HA declined during the following days in the syngeneic grafts, but increased progressively during the development of rejection in the allogeneic grafts, and increased on average three times by day 6. The relative water content also increased progressively during rejection of allogeneic grafts and correlated with the HA accumulation. The interstitial accumulation of HA, a glycosaminoglycan with unique water-binding qualities, is presumably implicated in the development of interstitial edema during rejection of heart grafts.

Full text

PDF
668

Images in this article

670Image
on p.670
670Image
on p.670
671Image
on p.671
671Image
on p.671
671Image
on p.671
671Image
on p.671

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ahlgren T., Jarstrand C. Hyaluronic acid enhances phagocytosis of human monocytes in vitro. J Clin Immunol. 1984 May;4(3):246–249. doi: 10.1007/BF00914973. [DOI] [PubMed] [Google Scholar]
  2. Balazs E. A., Laurent T. C., Jeanloz R. W. Nomenclature of hyaluronic acid. Biochem J. 1986 May 1;235(3):903–903. doi: 10.1042/bj2350903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bjermer L., Engström-Laurent A., Lundgren R., Rosenhall L., Hällgren R. 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):803–806. doi: 10.1136/bmj.295.6602.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Comper W. D., Laurent T. C. Physiological function of connective tissue polysaccharides. Physiol Rev. 1978 Jan;58(1):255–315. doi: 10.1152/physrev.1978.58.1.255. [DOI] [PubMed] [Google Scholar]
  5. Engström-Laurent A., Feltelius N., Hällgren R., Wasteson A. Raised serum hyaluronate levels in scleroderma: an effect of growth factor induced activation of connective tissue cells? Ann Rheum Dis. 1985 Sep;44(9):614–620. doi: 10.1136/ard.44.9.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Eriksson S., Fraser J. R., Laurent T. C., Pertoft H., Smedsrød B. Endothelial cells are a site of uptake and degradation of hyaluronic acid in the liver. Exp Cell Res. 1983 Mar;144(1):223–228. doi: 10.1016/0014-4827(83)90458-5. [DOI] [PubMed] [Google Scholar]
  7. Forrester J. V., Balazs E. A. Inhibition of phagocytosis by high molecular weight hyaluronate. Immunology. 1980 Jul;40(3):435–446. [PMC free article] [PubMed] [Google Scholar]
  8. Hamerman D., Wood D. D. Interleukin 1 enhances synovial cell hyaluronate synthesis. Proc Soc Exp Biol Med. 1984 Oct;177(1):205–210. doi: 10.3181/00379727-177-1-rc1. [DOI] [PubMed] [Google Scholar]
  9. Hascall V. C. Interaction of cartilage proteoglycans with hyaluronic acid. J Supramol Struct. 1977;7(1):101–120. doi: 10.1002/jss.400070110. [DOI] [PubMed] [Google Scholar]
  10. Heron I. A technique for accessory cervical heart transplantation in rabbits and rats. Acta Pathol Microbiol Scand A. 1971;79(4):366–372. doi: 10.1111/j.1699-0463.1971.tb01833.x. [DOI] [PubMed] [Google Scholar]
  11. Håkansson L., Hällgren R., Venge P. Regulation of granulocyte function by hyaluronic acid. In vitro and in vivo effects on phagocytosis, locomotion, and metabolism. J Clin Invest. 1980 Aug;66(2):298–305. doi: 10.1172/JCI109857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Jacobsson J., Wahlberg J., Frödin L., Odlind B., Tufveson G. Organ flush out solutions and cold storage preservation solutions: effect on organ cooling and post ischemic erythrocyte trapping in kidney grafts. An experimental study in the rat. Scand J Urol Nephrol. 1989;23(3):219–222. doi: 10.3109/00365598909180845. [DOI] [PubMed] [Google Scholar]
  13. Johnson R. L., Ziff M. Lymphokine stimulation of collagen accumulation. J Clin Invest. 1976 Jul;58(1):240–252. doi: 10.1172/JCI108455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Le Douarin N. M. Cell migrations in embryos. Cell. 1984 Sep;38(2):353–360. doi: 10.1016/0092-8674(84)90490-2. [DOI] [PubMed] [Google Scholar]
  15. MARTINS DE OLIVEIRA J., LEVY M. N. Effects of hyaluronidase upon the water content of ischemic myocardium. Am Heart J. 1960 Jul;60:106–109. doi: 10.1016/0002-8703(60)90064-8. [DOI] [PubMed] [Google Scholar]
  16. Maclean D., Fishbein M. C., Maroko P. R., Braunwald E. Hyaluronidase-induced reductions in myocardial infarct size. Science. 1976 Oct 8;194(4261):199–200. doi: 10.1126/science.959848. [DOI] [PubMed] [Google Scholar]
  17. Maroko P. R., Libby P., Bloor C. M., Sobel B. E., Braunwald E. Reduction by hyaluronidase of myocardial necrosis following coronary artery occlusion. Circulation. 1972 Sep;46(3):430–437. doi: 10.1161/01.cir.46.3.430. [DOI] [PubMed] [Google Scholar]
  18. Mason R. M. Recent advances in the biochemistry of hyaluronic acid in cartilage. Prog Clin Biol Res. 1981;54:87–112. [PubMed] [Google Scholar]
  19. Nettelbladt O., Bergh J., Schenholm M., Tengblad A., Hällgren R. Accumulation of hyaluronic acid in the alveolar interstitial tissue in bleomycin-induced alveolitis. Am Rev Respir Dis. 1989 Mar;139(3):759–762. doi: 10.1164/ajrccm/139.3.759. [DOI] [PubMed] [Google Scholar]
  20. Olausson M., Mjörnstedt L., Lindholm L., Brynger H. Non-suture organ grafting to the neck vessels in rats. Acta Chir Scand. 1984;150(6):463–467. [PubMed] [Google Scholar]
  21. Ripellino J. A., Klinger M. M., Margolis R. U., Margolis R. K. The hyaluronic acid binding region as a specific probe for the localization of hyaluronic acid in tissue sections. Application to chick embryo and rat brain. J Histochem Cytochem. 1985 Oct;33(10):1060–1066. doi: 10.1177/33.10.4045184. [DOI] [PubMed] [Google Scholar]
  22. Shannon B. T., Love S. H., Myrvik Q. N. Participation of hyaluronic acid in the macrophage disappearance reaction. Immunol Commun. 1980;9(4):357–370. doi: 10.3109/08820138009052982. [DOI] [PubMed] [Google Scholar]
  23. Stern C. D. Mini-review: hyaluronidases in early embryonic development. Cell Biol Int Rep. 1984 Sep;8(9):703–717. doi: 10.1016/0309-1651(84)90108-5. [DOI] [PubMed] [Google Scholar]
  24. Sunnergren K. P., Rovetto M. J. Hyaluronidase reversal of increased coronary vascular resistance in ischemic rat hearts. Am J Physiol. 1983 Aug;245(2):H183–H188. doi: 10.1152/ajpheart.1983.245.2.H183. [DOI] [PubMed] [Google Scholar]
  25. Tengblad A. Affinity chromatography on immobilized hyaluronate and its application to the isolation of hyaluronate binding properties from cartilage. Biochim Biophys Acta. 1979 Jun 19;578(2):281–289. doi: 10.1016/0005-2795(79)90158-2. [DOI] [PubMed] [Google Scholar]
  26. Tengblad A. Quantitative analysis of hyaluronate in nanogram amounts. Biochem J. 1980 Jan 1;185(1):101–105. doi: 10.1042/bj1850101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tucker R. P., Erickson C. A. Morphology and behavior of quail neural crest cells in artificial three-dimensional extracellular matrices. Dev Biol. 1984 Aug;104(2):390–405. doi: 10.1016/0012-1606(84)90094-0. [DOI] [PubMed] [Google Scholar]
  28. Wahl S. M., Wahl L. M., McCarthy J. B. Lymphocyte-mediated activation of fibroblast proliferation and collagen production. J Immunol. 1978 Sep;121(3):942–946. [PubMed] [Google Scholar]
  29. Yaron M., Yaron I., Wiletzki C., Zor U. Interrelationship between stimulation of prostaglandin E and hyaluronate production by poly (I) . poly (C) and interferon in synovial fibroblast culture. Arthritis Rheum. 1978 Jul-Aug;21(6):694–698. doi: 10.1002/art.1780210614. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Clinical Investigation are provided here courtesy of American Society for Clinical Investigation

RESOURCES