Skip to main content
PMC home page
The Journal of Clinical Investigation logoLink to The Journal of Clinical Investigation
. 1994 Apr;93(4):1543–1553. doi: 10.1172/JCI117133

Modulation by beta-aminopropionitrile of vessel luminal narrowing and structural abnormalities in arterial wall collagen in a rabbit model of conventional balloon angioplasty versus laser balloon angioplasty.

J R Spears 1, H Zhan 1, S Khurana 1, R L Karvonen 1, K M Reiser 1
PMCID: PMC294173  PMID: 8163657

Abstract

This study was designed to assess the potential relationship between the late loss of angiographic luminal diameter and biochemical abnormalities of arterial wall collagen in rabbits subjected to angioplasty, and to test the hypothesis that beta-aminopropionitrile (beta APN), an inhibitor of lysyl oxidase, would inhibit such changes when administered orally for 1 mo after angioplasty. Endovascular injury was induced in rabbit iliac arteries by ipsilateral balloon angioplasty (BA) and by contralateral balloon angioplasty accompanied by exposure to continuous wave neodymium: yttrium aluminum garnet laser radiation (LBA). Computer measurement of angiographic luminal diameter demonstrated significant vessel narrowing at 1 and 6 mo after both procedures. By quantitative histology, the majority of the 1-mo loss in angiographic diameter could not be attributed to neointimal thickening. Analysis of collagen cross-linking by HPLC in collagen obtained from the LBA-injured segments of the arteries 1 mo after angioplasty revealed a significant increase, relative to values from uninjured arteries (P < 0.05), in the difunctional cross-link dihydroxylysinonorleucine (DHLNL). 6 mo after angioplasty, the content of hydroxypyridinium, the trifunctional maturational product of DHLNL, was significantly elevated in both BA- and LBA-treated arteries compared with values from uninjured arteries (P < 0.05). In animals administered beta APN, luminal narrowing at 1 mo, compared with controls, was attenuated (P < 0.01) and DHLNL content was decreased (P < 0.05) in arteries subjected to LBA, but not in arteries subjected to BA. The results suggest that lathyrogenic agents may be efficacious in favorably modulating LBA-induced alterations in vessel diameter and mural connective tissue.

Full text

PDF
1548

Images in this article

1547Image
on p.1547
1548Image
on p.1548
1548Image
on p.1548
1548Image
on p.1548
1549Image
on p.1549

Selected References

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

  1. Austin G. E., Ratliff N. B., Hollman J., Tabei S., Phillips D. F. Intimal proliferation of smooth muscle cells as an explanation for recurrent coronary artery stenosis after percutaneous transluminal coronary angioplasty. J Am Coll Cardiol. 1985 Aug;6(2):369–375. doi: 10.1016/s0735-1097(85)80174-1. [DOI] [PubMed] [Google Scholar]
  2. Bass L. S., Moazami N., Pocsidio J., Oz M. C., LoGerfo P., Treat M. R. Changes in type I collagen following laser welding. Lasers Surg Med. 1992;12(5):500–505. doi: 10.1002/lsm.1900120508. [DOI] [PubMed] [Google Scholar]
  3. Buckingham B., Reiser K. M. Relationship between the content of lysyl oxidase-dependent cross-links in skin collagen, nonenzymatic glycosylation, and long-term complications in type I diabetes mellitus. J Clin Invest. 1990 Oct;86(4):1046–1054. doi: 10.1172/JCI114807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Capdeville M., Coutard M., Osborne-Pellegrin M. J. Spontaneous rupture of the internal elastic lamina in the rat: the manifestation of a genetically determined factor which may be linked to vascular fragility. Blood Vessels. 1989;26(4):197–212. doi: 10.1159/000158768. [DOI] [PubMed] [Google Scholar]
  5. Cheong W. F., Spears J. R., Welch A. J. Laser balloon angioplasty. Crit Rev Biomed Eng. 1991;19(2-3):113–146. [PubMed] [Google Scholar]
  6. Clowes A. W., Reidy M. A., Clowes M. M. Mechanisms of stenosis after arterial injury. Lab Invest. 1983 Aug;49(2):208–215. [PubMed] [Google Scholar]
  7. Crawford D. W., Back L. H., Cole M. A. In vivo oxygen transport in the normal rabbit femoral arterial wall. J Clin Invest. 1980 Jun;65(6):1498–1508. doi: 10.1172/JCI109815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Essed C. E., Van den Brand M., Becker A. E. Transluminal coronary angioplasty and early restenosis. Fibrocellular occlusion after wall laceration. Br Heart J. 1983 Apr;49(4):393–396. doi: 10.1136/hrt.49.4.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eyre D. R., Koob T. J., Van Ness K. P. Quantitation of hydroxypyridinium crosslinks in collagen by high-performance liquid chromatography. Anal Biochem. 1984 Mar;137(2):380–388. doi: 10.1016/0003-2697(84)90101-5. [DOI] [PubMed] [Google Scholar]
  10. Eyre D. R., Paz M. A., Gallop P. M. Cross-linking in collagen and elastin. Annu Rev Biochem. 1984;53:717–748. doi: 10.1146/annurev.bi.53.070184.003441. [DOI] [PubMed] [Google Scholar]
  11. Fleisher J. H., Speer D., Brendel K., Chvapil M. Effect of pargyline on the metabolism of beta-aminopropionitrile (BAPN) by rabbits. Toxicol Appl Pharmacol. 1979 Jan;47(1):61–69. doi: 10.1016/0041-008x(79)90072-3. [DOI] [PubMed] [Google Scholar]
  12. Greenberg D. B., Reiser K. M., Last J. A. Correlation of biochemical and morphologic manifestations of acute pulmonary fibrosis in rats administered paraquat. Chest. 1978 Oct;74(4):421–425. doi: 10.1378/chest.74.4.421. [DOI] [PubMed] [Google Scholar]
  13. HURLEY J. V., STOREY E., HAM K. N. The effects of amino-acetonitrile and cortisone on the healing of turpentine-induced abscesses in the rat. Br J Exp Pathol. 1958 Apr;39(2):119–127. [PMC free article] [PubMed] [Google Scholar]
  14. Harker L. A. Role of platelets and thrombosis in mechanisms of acute occlusion and restenosis after angioplasty. Am J Cardiol. 1987 Jul 31;60(3):20B–28B. doi: 10.1016/0002-9149(87)90479-6. [DOI] [PubMed] [Google Scholar]
  15. Haschek W. M., Reiser K. M., Klein-Szanto A. J., Kehrer J. P., Smith L. H., Last J. A., Witschi H. P. Potentiation of butylated hydroxytoluene-induced acute lung damage by oxygen. Cell kinetics and collagen metabolism. Am Rev Respir Dis. 1983 Jan;127(1):28–34. doi: 10.1164/arrd.1983.127.1.28. [DOI] [PubMed] [Google Scholar]
  16. Jenkins R. D., Sinclair I. N., Leonard B. M., Sandor T., Schoen F. J., Spears J. R. Laser balloon angioplasty versus balloon angioplasty in normal rabbit iliac arteries. Lasers Surg Med. 1989;9(3):237–247. doi: 10.1002/lsm.1900090306. [DOI] [PubMed] [Google Scholar]
  17. Last J. A., Armstrong L. G., Reiser K. M. Biosynthesis of collagen crosslinks. Int J Biochem. 1990;22(6):559–564. doi: 10.1016/0020-711x(90)90031-w. [DOI] [PubMed] [Google Scholar]
  18. Last J. A., Reiser K. M. Biosynthesis of collagen crosslinks. III. In vivo labeling and stability of lung collagen in rats with bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol. 1989 Aug;1(2):111–117. doi: 10.1165/ajrcmb/1.2.111. [DOI] [PubMed] [Google Scholar]
  19. Last J. A., Summers P., Reiser K. M. Biosynthesis of collagen crosslinks. II. In vivo labelling and stability of lung collagen in rats. Biochim Biophys Acta. 1989 Feb 24;990(2):182–189. doi: 10.1016/s0304-4165(89)80032-7. [DOI] [PubMed] [Google Scholar]
  20. Lata A., Gowri C., Dhar S. C., Gibeault J. D., Chvapil M. Effect of topically applied beta-aminopropionitrile on granuloma tissue biochemistry. Proc Soc Exp Biol Med. 1988 Apr;187(4):442–447. doi: 10.3181/00379727-187-42686. [DOI] [PubMed] [Google Scholar]
  21. Moorhead L. C. Effects of beta-aminopropionitrile after posterior penetrating injury in the rabbit. Am J Ophthalmol. 1983 Jan;95(1):97–109. doi: 10.1016/0002-9394(83)90337-9. [DOI] [PubMed] [Google Scholar]
  22. Moorhead L. C., Smith J., Stewart R., Kimbrough R. Effects of beta-aminopropionitrile after glaucoma filtration surgery: pilot human trial. Ann Ophthalmol. 1987 Jun;19(6):223–225. [PubMed] [Google Scholar]
  23. Nelson J. M., Diegelmann R. F., Cohen I. K. Effect of beta-aminopropionitrile and ascorbate on fibroblast migration. Proc Soc Exp Biol Med. 1988 Jul;188(3):346–352. doi: 10.3181/00379727-188-42745. [DOI] [PubMed] [Google Scholar]
  24. Nobuyoshi M., Kimura T., Nosaka H., Mioka S., Ueno K., Yokoi H., Hamasaki N., Horiuchi H., Ohishi H. Restenosis after successful percutaneous transluminal coronary angioplasty: serial angiographic follow-up of 229 patients. J Am Coll Cardiol. 1988 Sep;12(3):616–623. doi: 10.1016/s0735-1097(88)80046-9. [DOI] [PubMed] [Google Scholar]
  25. Nobuyoshi M., Kimura T., Ohishi H., Horiuchi H., Nosaka H., Hamasaki N., Yokoi H., Kim K. Restenosis after percutaneous transluminal coronary angioplasty: pathologic observations in 20 patients. J Am Coll Cardiol. 1991 Feb;17(2):433–439. doi: 10.1016/s0735-1097(10)80111-1. [DOI] [PubMed] [Google Scholar]
  26. Peacock E. E., Jr Control of wound healing and scar formation in surgical patients. Arch Surg. 1981 Oct;116(10):1325–1329. doi: 10.1001/archsurg.1981.01380220069011. [DOI] [PubMed] [Google Scholar]
  27. Pickering J. G., Weir L., Rosenfield K., Stetz J., Jekanowski J., Isner J. M. Smooth muscle cell outgrowth from human atherosclerotic plaque: implications for the assessment of lesion biology. J Am Coll Cardiol. 1992 Nov 15;20(6):1430–1439. doi: 10.1016/0735-1097(92)90259-p. [DOI] [PubMed] [Google Scholar]
  28. Reiser K. M., Last J. A. Collagen crosslinking in lungs of rats with experimental silicosis. Coll Relat Res. 1986 Oct;6(4):313–323. doi: 10.1016/s0174-173x(86)80002-4. [DOI] [PubMed] [Google Scholar]
  29. Reiser K. M., Last J. A. Collagen crosslinking in lungs of rats with experimental silicosis. Coll Relat Res. 1986 Oct;6(4):313–323. doi: 10.1016/s0174-173x(86)80002-4. [DOI] [PubMed] [Google Scholar]
  30. Reiser K., McCormick R. J., Rucker R. B. Enzymatic and nonenzymatic cross-linking of collagen and elastin. FASEB J. 1992 Apr;6(7):2439–2449. doi: 10.1096/fasebj.6.7.1348714. [DOI] [PubMed] [Google Scholar]
  31. Riley D. J., Kerr J. S., Berg R. A., Ianni B. D., Pietra G. G., Edelman N. H., Prockop D. J. beta-Aminopropionitrile prevents bleomycin-induced pulmonary fibrosis in the hamster. Am Rev Respir Dis. 1982 Jan;125(1):67–73. doi: 10.1164/arrd.1982.125.1.67. [DOI] [PubMed] [Google Scholar]
  32. Ross R. The pathogenesis of atherosclerosis--an update. N Engl J Med. 1986 Feb 20;314(8):488–500. doi: 10.1056/NEJM198602203140806. [DOI] [PubMed] [Google Scholar]
  33. Sandor T., Spears J. R. Statistical considerations on the precision of assessing blood vessel diameter in cine coronary angiography. Comput Biomed Res. 1985 Dec;18(6):531–543. doi: 10.1016/0010-4809(85)90028-x. [DOI] [PubMed] [Google Scholar]
  34. Schwartz R. S., Huber K. C., Murphy J. G., Edwards W. D., Camrud A. R., Vlietstra R. E., Holmes D. R. Restenosis and the proportional neointimal response to coronary artery injury: results in a porcine model. J Am Coll Cardiol. 1992 Feb;19(2):267–274. doi: 10.1016/0735-1097(92)90476-4. [DOI] [PubMed] [Google Scholar]
  35. Schwartz R. S., Murphy J. G., Edwards W. D., Camrud A. R., Vliestra R. E., Holmes D. R. Restenosis after balloon angioplasty. A practical proliferative model in porcine coronary arteries. Circulation. 1990 Dec;82(6):2190–2200. doi: 10.1161/01.cir.82.6.2190. [DOI] [PubMed] [Google Scholar]
  36. Spears J. R., Kundu S. K., McMath L. P. Laser balloon angioplasty: potential for reduction of the thrombogenicity of the injured arterial wall and for local application of bioprotective materials. J Am Coll Cardiol. 1991 May;17(6 Suppl B):179B–188B. doi: 10.1016/0735-1097(91)90956-a. [DOI] [PubMed] [Google Scholar]
  37. Spears J. R., Sandor T., Als A. V., Malagold M., Markis J. E., Grossman W., Serur J. R., Paulin S. Computerized image analysis for quantitative measurement of vessel diameter from cineangiograms. Circulation. 1983 Aug;68(2):453–461. doi: 10.1161/01.cir.68.2.453. [DOI] [PubMed] [Google Scholar]
  38. Strauss B. H., Umans V. A., van Suylen R. J., de Feyter P. J., Marco J., Robertson G. C., Renkin J., Heyndrickx G., Vuzevski V. D., Bosman F. T. Directional atherectomy for treatment of restenosis within coronary stents: clinical, angiographic and histologic results. J Am Coll Cardiol. 1992 Dec;20(7):1465–1473. doi: 10.1016/0735-1097(92)90438-s. [DOI] [PubMed] [Google Scholar]
  39. Tang S. S., Trackman P. C., Kagan H. M. Reaction of aortic lysyl oxidase with beta-aminopropionitrile. J Biol Chem. 1983 Apr 10;258(7):4331–4338. [PubMed] [Google Scholar]
  40. WOESSNER J. F., Jr The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid. Arch Biochem Biophys. 1961 May;93:440–447. doi: 10.1016/0003-9861(61)90291-0. [DOI] [PubMed] [Google Scholar]
  41. Waller B. F., Pinkerton C. A. "Cutters, scoopers, shavers and scrapers": the importance of atherectomy devices and clinical relevance of tissue removed. J Am Coll Cardiol. 1990 Feb;15(2):426–428. doi: 10.1016/s0735-1097(10)80072-5. [DOI] [PubMed] [Google Scholar]

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

RESOURCES