Apoptosis of cardiac myocytes during cardiac allograft rejection: Relation to induction of nitric oxide synthase

Circulation

Volumn 94, Issue 7, 1996, Pages 1665-1673

  Szabolcs, Matthias ^a   Michler, Robert E ^a   Yang, Xiaochun ^a   Aji, Walif ^a   Roy, Dilip ^a   Athan, Eleni ^a   Sciacca, Robert R ^a   Minanov, Oktavjian P ^a   Cannon, Paul J ^a,b  

^a New York Presbyterian Columbia University Medical Center   (United States)

^b Columbia University ^*  (United States)

Author keywords

apoptosis; cells; rejection; transplantation

Indexed keywords

NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; GRAFT REJECTION; HEART MUSCLE CELL; HEART TRANSPLANTATION; HISTOPATHOLOGY; MACROPHAGE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT;

EID: 0029778443     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.94.7.1665     Document Type: Article

References (52)

1. Tilney NJ, Kopiec-Woglinski JW, Heideche CD, Lear PA, Strom TB. Mechanisms of rejection and prolongation of vascularized organ allografts. Immunol Rev. 1984;77:185-216.
2. Barry WH. Mechanisms of immune-mediated myocyte injury. Circulation. 1994;89:2421-2432.
3. Hall BM. Cells mediating allograft rejection. Transplantation. 1991; 51:1141-1151.
4. Cohen JJ, Duke RC, Fadok VA, Sellins KS. Apoptosis and programmed cell death in immunity. Annu Rev Immunol. 1992;10: 267-293.
5. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science. 1995;267:1456-1462.
6. Marboe CC, Buffaloe A, Fenoglio JJ Jr. Immunologic aspects of rejection. Prog Cardiovasc Dis. 1990;32:419-432.
7. Iwanaga T, Hoshi O, Han H, Takahashi-Iwanaya H, Uchiyama Y, Fujita T. Lamina propria macrophages involved in cell death (apoptosis) of enterocytes in the small intestine of rats. Arch Histol Cytol. 1994;57:267-276.
8. Maino G, Joris I. Apoptosis, oricosis, and necrosis: an overview of cell death. Am J Pathol. 1995;146:3-15.
9. Steller H. Mechanisms and genes of cellular suicide. Science. 1995; 267:1445-1449.
10. Arends MJ, Wyllie AH. Apoptosis: mechanisms and roles in pathology. Int Rev Exp Pathol 1991;32:223-254.
11. Pietsch MC, Polzar B, Stephan H, Cromptom T, MacDonald HR, Mannherz HG, Tschopp J. Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO J. 1993;12:371-377.
12. Abrams JM, White K, Fessler LI, Steller H. Programmed cell death during Drosophila embryogenesis. Development. 1993;117:29-43.
13. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biologic phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239-257.
14. Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature. 1980;284: 555-556.
15. English HF, Kyprianou N, Isaacs JT. Relationship between DNA fragmentation and apoptosis in the programmed cell death in the rat prostate following castration. Prostate. 1989;15:233-250.
16. Yamada T, Ohyama H. Radiation-induced interphase death of rat thymocytes is internally programmed (apoptosis). Int J Radiat Biol. 1988;53:65-75.
17. James TN. Normal and abnormal consequences of apoptosis in the human heart: from postnatal morphogenesis to paroxysmal arrhythmias. Circulation. 1994;90:556-573.
18. Tanaka M, Ito H, Adachi S, Akimoto H, Nishikawa T, Kasajima T, Marumo F, Hiroe M. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ Res. 1994;75:426-433.
19. Bing OH. Hypothesis: apoptosis may be a mechanism for the transition to heart failure with chronic pressure overload. J Mol Cell Cardiol. 1994;26:943-948.
20. Gottlieb RA, Berleson KO, Kloner RA, Bablor BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest. 1994;94:1621-1628.
21. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest. 1995;95:2266-2274.
22. Isner JM, Kearny M, Bortman S, Passen JP. Apoptosis in human atherosclerosis and restenosis. Circulation. 1995;91:2703-2711.
23. Yang X, Chowdhury N, Cai B, Brett J, Marboe C, Sciacca RR, Michler RE, Cannon PJ. Induction of myocardial nitric oxide synthase by cardiac allograft rejection. J Clin Invest. 1994;94:714-721.
24. Pinsky DJ, Cai B, Yang X, Rodriguez C, Sciacca RR, Cannon PJ. The lethal effects of cytokine-induced nitric oxide in cardiac myocytes are blocked by nitric oxide synthase antagonism or transforming growth factor β. J Clin Invest. 1995;95:677-685.
25. Albina JE, Cui S, Mateo RB, Reichner JS. Nitric oxide mediated apoptosis in murine peritoneal macrophages. J Immunol. 1993;150: 5080-5085.
26. Cui S, Reichner JS, Mateo RB, Albina JE. Activated murine macrophages induce apoptosis in tumor cells through nitric oxide-dependent or independent mechanisms. Cancer Res. 1994;54:2462-2467.
27. Shimaoka M, Iida T, Ohara A, Tanaka N, Mashimo T, Honda T, Yoshiya I. NOC, a nitric-oxide-releasing compound, induced dose dependent apoptosis in macrophages. Biochem Biophys Res Commun. 1995;209:519-526.
28. Messmer UK, Lapetina EG, Brune B. Nitric oxide-induced apoptosis in Raw 264.7 macrophages is antagonized by protein kinase C- and protein kinase A-activating compounds. Mol Pharmacol. 1995;47: 757-765.
29. Ono K, Lindsay ES. Improved technique of heart transplantation in rats. J Thorac Cardiovasc Surg. 1969;7:225-229.
30. Riedy MC, Timm EA Jr, Stewart CC. Quantitative RT-PCR for measuring gene expression. Biotechniques. 1995;18:70-76.
31. Billingham ME, Cary NRB, Hamond ME, Kemnitz J, Marboe C, McAllister HA, Snovar DC, Winters GL, Zerbe A. A working formulation for the standardization of nomenclature in the diagnosis of heart and lung rejection: Heart Rejection Study Group. J Heart Lung Transplant. 1990;9:587-593.
32. Gold R, Schmied M, Giegerich G, Breitschopf H, Hartung HP, Toyka KV, Lassmann H. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation techniques. Lab Invest. 1994;71:219-225.
33. Gorczyca W, Gong J, Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl and nick translation assays. Cancer Res. 1993;53: 1945-1954.
34. Gavrieli Y, Sherman Y, Ben-Sasson SA. Identification of programmed cell death in situ via specific labeling of DNA fragmentation. J Cell Biol 1992;119:493-501.
35. Miller SA, Dykes DD, Polesky HF. A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res. 1988;16:1215.
36. Rosl F. A simple and rapid method for the detection of apoptosis in human cells. Nucleic Acids Res. 1992;20:5243.
37. Tilly JL, Hsueh AJW. Microscale autoradiographic method for the qualitative and quantitative analysis of apoptotic fragmentation. J Cell Physiol 1993;154:519-526.
38. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric acid and Superoxide. Proc Natl Acad Sci U S A. 1990;87:1620-1624.
39. Beckman JS, Ye YZ, Anderson PC, Chen J, Accavitti MA, Tarpey MM, White CR. Extensive nitration of protein tyrosines in human atherosclerosis detected by immunohistochemistry. Biol Chem Hoppe Seyler. 1994;375:81-88.
40. Lancaster JR Jr, Langrehr JM, Bergonia HA, Murase N, Simmons RL, Huffman RA. EPR detection of heme and nonheme iron-containing protein nitrosylation by nitric oxide during rejection of rat heart allograft. J Biol Chem. 1992;267:10994-10998.
41. Cotter TG, Kennon SV, Glynn JG, Martin SJ. Cell death via apoptosis and its relationship to growth, development and differentiation of both tumor and normal cells. Anticancer Res. 1990;10:1153-1160.
42. Kajstura J, Minsukhani M, Cheng W, Reiss K, Krajewski S, Reed JC, Quaini F, Sonnenblick EH, Anversa P. Programmed cell death and the expression of the protooncogene Bcl-2 in myocytes during postnatal maturation of the heart. Exp Cell Res. 1995;219:110-121.
43. Cheng W, Li B, Kajstura J, Wolin MS, Sonnenblick EH, Hintze TH, Olivetti G, Anversa P. Stretch-induced programmed myocyte cell death. J Clin Invest. 1995;96:2247-2259.
44. Askew DS, Ashmun RA, Simmons BC, Cleveland JL. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene. 1991;6: 1915-1922.
45. Symonds H, Krall L, Remington L, Saenz-Rubles M, Lowe S, Jacks T, Van Dyke T. P53-dependent apoptosis suppresses tumor cell growth and progression in vivo. Cell. 1994;78:703-711.
46. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 1993;75:241-251.
47. Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol. 1994;124:1-6.
48. Tamir S, de Rojas-Walker T, Caulfield J, Wishnok JS, Tannenbaum SR. DNA damage by nitric oxide (NO) and peroxynitrite (ONOO). Proceedings of the First International Conference on the Biochemistry and Molecular Biology of Nitric Oxide; July 16-21, 1994; University of California at Los Angeles. 1994;B30:81.
49. Pinsky DJ, Yang X, Aji W, Sciacca RR, Cannon PJ. Nitric oxide induces apoptosis of adult rat cardiac myocytes. Circulation. 1995; 92(suppl I):I-565. Abstract.
50. Delang CA, Green MH, Lowe JE, Green IC. Endogenous nitric oxide induced by interleukin 1-beta in rat islets of Langerhans and HIT-T15 cells causes significant DNA damage as measured by the 'comet' assay. FEBS Lett. 1993;333:391-395.
51. Brady AJB, Poole-Wilson PA, Harding SE, Warren JB. Nitric oxide production within cardiac myocytes reduces their contractility in endotoxemia. Am J Physiol. 1992;263:H1963-H1966.
52. De Belder AJ, Radomski MW, Why HSF, Richardson PJ, Bucknell CG, Salas E, Martin JF, Moncada S. Nitric oxide synthase activities in human myocardium. Lancet. 1993;341:84-85.