Interleukin-1β induces cardiac myocyte growth but inhibits cardiac fibroblast proliferation in culture

Journal of Clinical Investigation

Volumn 95, Issue 6, 1995, Pages 2555-2564

  Palmer, James N ^a   Hartogensis, Wendy E ^a   Patten, Monica ^a   Fortuin, F David ^a   Long, Carlin S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Division of Cardiology 111 C8   (United States)

Author keywords

cardiac fibroblast; cardiac myocyte; hypertrophy; interleukin 1

Indexed keywords

DNA; INTERLEUKIN 1BETA; MESSENGER RNA;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL GROWTH; CELL INTERACTION; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DNA SYNTHESIS; FIBROBLAST; HEART MUSCLE CELL; HYPERTROPHY; IMMUNOFLUORESCENCE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0028990133     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI117956     Document Type: Article

References (77)

1. Ognibene, F., S. Rosenberg, M. Lotze, J. Skibber, M. Parker, J. Shelmer, and J. Parrillo. 1988. Interleukin-2 administration causes reversible hemodynamic changes and left ventricular dysfunction similar to those seen in septic shock. Chest. 94:750-754.
2. Lange, L., and G. Schreiner. 1992. Immune cytokines and cardiac disease. Trends Cardiovasc. Med. 2:145-151.
3. Wu, C. J., M. Lovett, L. J. Wong, F. Moeller, M. Kitamura, T. J. Goralski, M. E. Billingham, V. A. Starnes, and C. Clayberger. 1992. Cytokine gene expression in rejecting cardiac allografts. Transplantation (Baltimore). 54:326-332.
4. Zhao, X. M., W. H. Frist, T. K. Yeoh, and G. G. Miller. 1993. Expression of cytokine genes in human cardiac allografts: correlation of IL-6 and transforming growth factor-beta (TGF-beta) with histological rejection. Clin. Exp. Immunol. 93:448-451.
5. Finkel, M., C. Oddis, T. Jacob, S. Watkins, B. Hattler, and R. Simmons. 1992. Negative inotropic effects of cytokines on the heart mediated by nitric oxide. Science (Wash. DC). 257:387-389.
6. Hosenpud, J., S. Campbell, and D. Mendelson. 1989. Interleukin-1 -induced myocardial depression in an isolated beating heart preparation. J. Heart Transplant. 8:460-464.
7. Roberts, A. B., Y. Vodovotz, N. S. Roche, M. B. Sporn, and C. F. Nathan. 1992. Role of nitric oxide in antagonistic effects of transforming growth factor-beta and interleukin-1 beta on the beating rate of cultured cardiac myocytes. Mol. Endocrinol. 6:1921-1930.
8. Roberts, A. B., N. S. Roche, T. S. Winokur, J. K. Burmester, and M. B. Sporn. 1992. Role of transforming growth factor-beta in maintenance of function of cultured neonatal cardiac myocytes. Automne action and reversal of damaging effects of interleukin-1. J. Clin. Invest. 90:2056-2062.
9. Balligand, J.-L., D. Ungureanu, R. A. Kelly, L. Kobzik, D. Pimental, T. Michel, and T. W. Smith. 1993. Abnormal contractile function due to induction of nitric oxide synthesis in rat cardiac myocytes follows exposure to activated macrophage-conditioned medium. J. Clin. Invest. 91:2314-2319.
10. Li, Y. H., and G. J. Rozanski. 1993. Effects of human recombinant interleukin-1 on electrical properties of guinea pig ventricular cells. Cardiovasc. Res. 27:525-530.
11. Balligand, J.-L., D. Ungureanu-Longrois, W. W. Simmons, D. Pimental, T. A. Malinski, M. Kapturczak, Z. Taha, C. J. Lowenstein, A. J. Davidoff, R. A. Kelly, et al. 1994. Cytokine-inducible nitric oxide synthase (iNOS) expression in cardiac myocytes. J. Biol. Chem. 269:27580-27588.
12. Weiner, H. L., and J. L. Swain. 1989. Acidic fibroblast growth factor mRNA is expressed by cardiac myocytes in culture and the protein is localized to the extracellular matrix. Proc. Natl. Acad. Sci. USA. 86:2683-2687.
13. Kardami, E., and R. R. Fandrich. 1989. Basic fibroblast growth factor in atria and ventricles of the vertebrate heart. J. Cell Biol. 109:1865-1875.
14. Eghbali, M. 1989. Cellular origin and distribution of transforming growth factor-beta in the normal rat myocardium. Cell Tissue Res. 256:553-558.
15. Long, C. S., C. J. Henrich, and P. C. Simpson. 1991. A growth factor for cardiac myocytes is produced by cardiac nonmyocytes. Cell Regul. 2:1081-1095.
16. Long, C. S. 1992. TGFβ isoform expression and effect in neonatal rat cardiac myocytes and non-myocytes in culture. Circulation. 86:1-837 (Abstr.).
17. Long, C. S., J. N. Palmer, W. Hartogensis, N. Honbo, T. Miguel, C. Grunfeld, and J. S. Karliner. 1993. Hypoxia stimulates interleukin-1 RNA expression by cardiac non-myocytes in culture. Clin. Res. 41:145a. (Abstr.)
18. Weber, K. T., P. Anversa, P. W. Armstrong, C. G. Brilla, J. C. Burnett, J. M. Cruickshank, R. B. Devereux, T. D. Giles, N. Korsgaard, C. V. Leier, et al. 1992. Remodeling and repair of the cardiovascular system. J. Am. Coll. Cardiol. 20:3-16.
19. Frelin, C. 1980. Serum growth factors for rat cardiac non-muscle cells in culture. J. Mol. Cell. Cardiol. 12:1329-1340.
20. Kardami, E. 1990. Stimulation and inhibition of cardiac myocyte proliferation in vitro. Mol. Cell. Biochem. 92:129-135.
21. Schorb, W., G. W. Booz, D. E. Dostal, K. M. Conrad, K. C. Chang, and K. M. Baker. 1993. Angiotensin II is mitogenic in neonatal rat cardiac fibroblasts. Circ. Res. 72:1245-1254.
22. Colotta, F. F., M. Muzio, R. Bertini, N. Polentarutti, M. Sironi, J. G. Giri, S. K. Dower, J. E. Sims, and A. Mantovani. 1993. Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4. Science (Wash. DC). 261:472-475.
23. Sims, J. E., M. A. Gayle, J. L. Slack, M. R. Alderson, T. A. Bird, J. G. Giri, F. F. R. Colotta, A. Mantovanni, K. Shanebeck, K. H. Grabstein, and S. K. Dower. 1993. Interleukin-1 signaling occurs exclusively via the type 1 receptor. Proc. Natl. Acad. Sci. USA. 90:6155-6159.
24. Joshi-Barve, S. S., V. V. Rangnekar, S. F. Sells, and V. M. Rengnekar. 1993. Interleukin-1-inducible expression of gro-β via NF-kB activation is dependent upon tyrosine kinase signaling. J. Biol. Chem. 268:18018-18029.
25. Corbett, J. A., M. A. Sweetland, J. R. Lancaster, and M. L. McDaniel. 1993. A 1 hour pulse with IL-1β induces the formation of nitric oxide and inhibits insulin secretion by rat islets of Langerhans: evidence for a tyrosine kinase signaling mechanism. FASEB (Fed. Am. Soc. Exp. Biol.) J. 7:369-374.
26. Corbett, J. A., G. Kwon, T. P. Misko, C. P. Rodi, and M. L. McDaniel. 1994. Tyrosine kinase involvement in IL-1β-induced expression of iNOS by β-cells purified from islets of Langerhans. Am. J. Physiol. 267:C48-C54.
27. Simpson, P., A. McGrath, and S. Savion. 1982. Myocyte hypertrophy in neonatal rat heart cultures and its regulation by serum and by catecholamines. Circ. Res. 51:787-801.
28. Parker, T. G., and M. D. Schneider. 1990. Peptide growth factors can provoke "fetal" contractile protein gene expression in rat cardiac myocytes. J. Clin. Invest. 85:507-514.
29. 1D mRNAs are present in cardiac myocytes, but not in cardiac fibroblasts. Circ. Res. 75:796-802.
30. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
31. Simpson, P. 1985. Stimulation of hypertrophy of cultured neonatal rat heart cells through an α1-adrenergic receptor and induction of beating through an α1- and β1-adrenergic receptor interaction: evidence for independent regulation of growth and beating. Circ. Res. 56:884-894.
32. Lompre, A. M., B. Nadal-Ginard, and V. Mahdavi. 1984. Expression of the cardiac ventricular α- and β-myosin heavy chain genes is developmentally and hormonally regulated. J. Biol. Chem. 259:6437-6446.
33. 1D. Biochem. Biophys. Res. Commun. 200:1177-1184.
34. Boraschi, D., G. Volpini, L. Villa, L. Nencioni, G. Scapigliati, D. Nucci, G. Antoni, G. Matteucci, F. Cioli, and A. Tagliabue. 1989. A monoclonal antibody to the IL-1β peptide 163-171 blocks adjuvanticity but not pyrogenicity of IL-1β in vivo. J. Immunol. 143:131-134.
35. Long, C. S., W. E. Hartogensis, and P. C. Simpson. 1993. β-adrenergic stimulation of cardiac non-myocytes augments the growth-promoting activity of non-myocyte conditioned medium. J. Mol. Cell. Cardiol. 25:915-925.
36. Rangnekar, V. V., S. Waheed, T. J. Davies, F. G. Toback, and V. M. Rangnekar. 1991. Antimitogenic and mitogenic actions of interleukin-1 in diverse cell types are associated with induction of gro gene expression. J. Biol. Chem. 266:2415-2422.
37. Chomczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
38. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl, editors. 1987. Current Protocols in Molecular Biology. Greene Publishing Associates and Wiley-Interscience, New York. 4.9.1-4.9.14.
39. Anisowicz, A., L. Bardwell, and R. Sager. 1987. Constitutive overexpression of a growth-regulated gene in Chinese hamster and human cells. Proc. Natl. Acad. Sci. USA. 84:7188-7192.
40. Church, G. M., and W. Gilbert. 1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA. 81:1991-1995.
41. Snedecor, G. W., and W. G. Cochran. 1967. Statistical Methods. 6th ed. The Iowa State University Press, Ames, Iowa. 593 pp.
42. Simpson, P. C. 1990. Regulation of hypertrophy and gene transcription in cultured heart muscle cells. In Molecular Biology of the Cardiovascular System, UCLA Symposia on Molecular and Cellular Biology. New Series, R. Roberts and M. D. Schneider, editors. Alan R. Liss, Inc., New York. 125-133.
43. Arend, W. P., H. G. Welgus, R. C. Thompson, and S. P. Eisenberg. 1990. Biological properties of recombinant human monocyte-derived interleukin 1 receptor antagonist. J. Clin. Invest. 85:1694-1697.
44. Raines, E. W., S. K. Dower, and R. Ross. 1989. Interleukin-1 mitogenic activity for fibroblasts and smooth muscle cells is due to PDGF-AA. Science (Wash. DC). 243:393-395.
45. Libby, P., S. J. C. Warner, and G. B. Friedman. 1988. Interleukin 1: a mitogen for human vascular smooth muscle cells that induces the release of growth-inhibitory prostanoids. J. Clin. Invest. 81:487-498.
46. Xie, J.-F., J. Stroumza, and D. T. Graves. 1994. IL-1 down-regulates platelet-derived growth factor-a receptor gene expression at the transcriptional level in human osteoblastic cells. J. Immunol. 153:378-383.
47. Katsuura, G., P. E. Gottschall, R. R. Dall, and A. Arimura. 1989. Interleukin-1 beta increases prostaglandin E2 in rat astrocyte cultures: modulatory effect of neuropeptides. Endocrinology. 124:3125-3127.
48. Coyne, D. W., and A. R. Morrison. 1990. Effect of the tyrosine kinase inhibitor, genistein, on interleukin-1 stimulated PGE2 production in mesangial cells. Biochem. Biophys. Res. Commun. 173:718-724.
49. Marczin, N., A. Papapetropoulos, and J. D. Catravas. 1993. Tyrosine kinase inhibitors suppress IL-1β induced NO synthesis in aortic smooth muscle cells. Am. J. Plnsiol. 265:H1014-H1017.
50. Martin, M., G. F. Bol, A. Eriksson, K. Resch, and F. R. Brigelius. 1994. Interleukin-1-induced activation of a protein kinase co-precipitating with the type I interleukin-1 receptor in T cells. Eur. J. Immunol. 24:1566-1571.
51. 2+ channel currents in hippocampal neurons through protein kinase C. Eur. J. Pharmacol. 266:1-10.
52. Tsujino, M., Y. Hirata, T. Imai, K. Kanno, S. Eguchi, H. Ho, and F. Marumo. 1994. Induction of nitric oxide synthase gene by interleukin-1β in cultured rat cardiocytes. Circulation. 90:375-383.
53. Allo, S. N., L. L. Carl, and H. E. Morgan. 1992. Acceleration and growth of cultured cardiomyocytes and translocation of protein kinase C. Am. J. Physiol. 263:C319-C325.
54. Enright, W. J., and P. Booth. 1993. Specificity of inhibitors of tyrosine kinases. Focus (Idaho). 13:79-83.
55. Laiho, M., J. A. DeCaprio, J. W. Ludlow, D. M. Livingston, and J. Massague. 1990. Growth inhibition by TGFβ linked to suppression of retinoblastoma protein phosphorylation. Cell. 62:175-185.
56. Moses, H. L. 1992. TGF-beta regulation of epithelial cell proliferation. Mol. Reprod Dev. 32:179-184.
57. Libby, P., D. J. Wyler, M. W. Janicka, and C. A. Dinarello. 1985. Differential effects of human interleukin-1 on growth of human fibroblasts and vascular smooth muscle cells. Arteriosclerosis. 5:186-191.
58. Cozzolino, F., M. Torcia, D. Aldinucci, M. Ziehe, F. Almerigogna, D. Bani, and D. M. Stern. 1990. Interleukin 1 is an automne regulator of human endothelial cell growth. Proc. Natl. Acad. Sci. USA. 87:6487-6491.
59. Koga, H., J. Mukawa, K. Miyagi, Y. Higa, S. Nakasone, S. Mekaru, and M. Ingram. 1993. Human recombinant interleukin-1β-mediated growth inhibition of cultured malignant glioma cells. Neurol. Med. Chir. 33:1-6.
60. Han, R., P. Ray, K. Baughman, and A. Feldman. 1991. Detection of interleukin and interleukin-receptor mRNA in human heart by polymerase chain reaction. Biochem. Biophys. Res. Commun. 181:520-523.
61. Dallman, M. J., C. P. Larsen, and P. J. Morris. 1991. Cytokine gene transcription in vascularized organ grafts: analysis using semiquantitative polymerase chain reaction. J. Exp. Med. 174:493-496.
62. Lane, J. R., D. A. Neumann, A. Lafond-Walker, A. Herskowitz, and N. R. Rose. 1993. Role of IL-1 and tumor necrosis factor in Coxsackie virus-induced autoimmune myocarditis. J. Immunol. 151:1682-1690.
63. Hancock, W., P. L. Mottram, L. J. Purcell, W. R. Han, G. A. Pietersz, and I. F. McKenzie. 1993. Prolonged survival of mouse cardiac allografts after CD4 or CD8 monoclonal antibody therapy is associated with selective intragraft cytokine protein expression: interleukin (IL)-4 and IL-10 but not IL-2 or interferon-gamma. Transplant Proc. 25:2937-2938.
64. Hosenpud, J., S. Campbell, and G. Pan. 1990. Indirect inhibition of myocyte RNA and protein synthesis by interleukin-1. J. Mol. Cell. Cardiol. 22:213-225.
65. Giulian, D., J. Woodward, D. G. Young, J. F. Krebs, and L. B. Lachman. 1988. Interleukin-1 injected into mammalian brain stimulates astrogliosis and neovascularization. J. Neurosci. 8:2485-2490.
66. BenEzra, D., I. Hemo, and G. Maftzir. 1990. In vivo angiogenic activity of interleukins. Arch. Ophtalmol. 108:573-576.
67. Motro, B., A. Itin, L. Sachs, and E. Keshet. 1990. Pattern of interleukin 6 gene expression in vivo suggests a role for this cytokine in angiogenesis. Proc. Natl. Acad. Sci. USA. 87:3092-3096.
68. Gay, C. G., and J. A. Winkles. 1991. Interleukin 1 regulates heparin-binding growth factor 2 gene expression in vascular smooth muscle cells. Proc. Natl. Acad. Sci. USA. 88:296-300.
69. Libby, P., G. B. Friedman, and R. N. Salomon. 1989. Cytokines as modulators of cell proliferation in fibrotic diseases. Am. Rev. Respir. Dis. 140:1114-1117.
70. Sager, R., S. Haskill, A. Anisowicz, D. Trask, and M. C. Pike. 1991. gro: a novel chemotactic cytokine. In Chemotactic Cytokines. J. Westwick, editor. Plenum Press, New York. 73-77.
71. Barry, W. H. 1994. Mechanisms of immune-mediated myocyte injury. Circulation. 89:2421-2432.
72. Balligand, J.-L., R. A. Kelly, P. A. Marsden, T. W. Smith, and T. Michel. 1993. Control of cardiac muscle cell function by an endogenous nitric oxide signaling system. Proc. Natl. Acad. Sci. USA. 90:347-351.
73. Finkel, M. S., R. A. Hoffman, L. Shen, C. V. Oddis, R. L. Simmons, and B. G. Hattler. 1993. Interleukin-6 (IL-6) as a mediator of stunned myocardium. Am. J. Cardiol. 71:1231-1232.
74. i and cell contraction in cultured chick ventricular myocytes. Circ. Res. 75:285-295.
75. Eddy, L., D. Goeddel, and G. Wong. 1992. Tumor necrosis factor-α pretreatment is protective in a rat model of myocardial ischemia-reperfusion injury. Biochem. Biophys. Res. Commun. 184:1056-1059.
76. Brown, J., C. White, L. Terada, M. Grosso, P. Shanley, D. Mulvin, A. Banerjee, G. Whitman, A. Harken, and J. Repine. 1990. Interleukin 1 prelreatment decreases ischemia/reperfusion injury. Proc. Natl. Acad. Sci. USA. 87:5026-5030.
77. Trinkle, L. A., D. Beasley, and R. S. Moreland. 1992. Interleukin-1β alters actin expression and inhibits contraction of rat thoracic aorta. Am J. Physiol. 262:C828-C833.