150-kD oxygen-regulated protein is expressed in human atherosclerotic plaques and allows mononuclear phagocytes to withstand cellular stress on exposure to hypoxia and modified low density lipoprotein

Journal of Clinical Investigation

Volumn 98, Issue 8, 1996, Pages 1930-1941

  Tsukamoto, Yoshitane ^a   Kuwabara, Keisuke ^a   Hirota, Seiichi ^a   Ikeda, Jun ^b   Stern, David ^c   Yanagi, Hideki ^b   Matsumoto, Masayasu ^a   Ogawa, Satoshi ^a   Kitamura, Yukihiko ^a  

^a OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^b HSP Research Institute   (Japan)

^c Columbia University ^*  (United States)

Author keywords

atherosclerosis; macrophage; smooth muscle cell; stress response

Indexed keywords

AUTOANTIBODY; LOW DENSITY LIPOPROTEIN; OXYGEN; PROTEIN;

ARTICLE; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL WALL; CELL HYPOXIA; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MONONUCLEAR CELL; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN ISOLATION; SMOOTH MUSCLE FIBER; STRESS;

EID: 0029961386     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI118994     Document Type: Article

References (42)

1. Wilson, R.E., and R.M. Sutherland. 1989. Enhanced synthesis of specific proteins, RNA, and DNA caused by hypoxia and reoxygenation. Int. J. Radiat. Oncol. Biol. Phys. 16:957-961.
2. Maeda, Y., M. Matsumoto, T. Ohtsuki, K. Kuwabara, S. Ogawa, O. Hori, D.Y. Shui, T. Kinoshita, T. Kamada, and D.M. Stern. 1994. Hypoxia-reoxygenation mediated induction of Interleukin-6 in cultured rat astrocytes and expression in ischemic gerbil brain: a paracrine mechanism enhancing neuron survival. J. Exp. Med. 180:2297-2308.
3. Hori, O., M. Matsumoto, K. Kuwabara, Y. Maeda, H. Ueda, T. Ohtsuki, T. Kinoshita, S. Ogawa, D.M. Stern, and T. Kamada. 1996. Exposure of astrocytes to hypoxia/reoxygenation enhances expression of glucose-regulated protein 78 facilitating astrocyte release of the neuroprotective cytokine Interleukin 6. J. Neurochem. 66:973-979.
4. Kitagawa, K., M. Matsumoto, M. Tagaya, K. Kuwabara, R. Hata, N. Handa, R. Fukunaga, K. Kimura, and T. Kamada. 1991. Hyperthermia-induced neuronal protection against ischemic injury in gerbils. J. Cereb. Blood Flow Metab. 11:449-452.
5. Kuwabara, K., M. Matsumoto, J. Ikeda, O. Hori, S. Ogawa, Y. Maeda, K. Kitagawa, N. Imuta, K. Kinoshita, D.M. Stern, et al. 1996. Purification and characterization of a novel stress protein, the 150 kDa oxygen-regulated protein (ORP150), from cultured rat astrocytes and its expression in ischemic mouse brain. J. Biol. Chem. 271:5025-5032.
6. Koga, S., S. Ogawa, K. Kuwabara, J. Brett, L.A. Leavy, J. Ryan, Y. Koga, J. Plocinski, W. Benjamin, D.K. Burns, and D.M. Stern. 1992. Synthesis and release of Interleukin 1 by reoxygenated human mononuclear phagocyte. J. Clin. Invest. 90:1007-1015.
7. Ogawa, S., H. Gerlach, C. Esposito, A.P. Macaulay, J. Brett, and D.M. Stern. 1990. Hypoxia modulates the barrier and coagulant function of cultured bovine endothelium. J. Clin. Invest. 85:1090-1098.
8. Hori, O., M. Matsumoto, Y. Maeda, H. Ueda, T. Ohtsuki, D.M. Stern, T. Kinoshita, S. Ogawa, and T. Kamada. 1994. Metabolic and biosynthetic alterations in cultured astrocytes exposed to hypoxia/reoxygenation. J. Neurochem. 62:1489-1495.
9. Basu, S.K., J.L. Goldstein, R.G.W. Anderson, and M.S. Brown. 1976. Degradation of cationized low density lipoprotein and regulation of cholesterol metabolism in homozygous familial hypercholesterolemia fibroblasts. Proc. Natl. Acad. Sci. USA. 73:3178-3182.
10. Endemann, G., L.W. Stanton, K.S. Madden, C.M. Bryant, R.T. White, and A.A. Protter. 1993. CD36 is a receptor for oxidized low density lipoprotein. J. Biol. Chem. 268:11811-11816.
11. Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (Lond.). 277:680-685.
12. Fong, L.G., S. Parthasarathy, J.L. Witzum, and D. Steinberg. 1987. Nonenzymatic oxidative cleavage of peptide bonds in apoprotein B-100. J Lipid Res. 28:1466-1477.
13. Steinbrecher, U.P., S. Parthasarathy, D.S. Leake, J.L. Witzum, and D. Steinberg. 1984. Modification of low density lipoprotein by endothelial cells involves lipid peroxidation and degeneration of low density lipoprotein phospholipids. Proc. Natl. Acad. Sci. USA. 81:3883-3887.
14. Tam, J.P. 1989. Synthetic peptide vaccine design: synthesis and properties of a high-density multiple antigenic peptide system. Proc. Natl. Acad. Sci. USA. 86:9084-9088.
15. Cooper, H.M., and Y. Paterson. 1991. Production of antibodies. In Current Protocol in Immunology. J.E. Coligen, A.M. Kruisbeek, D.H. Margulies, E.M. Shevach, and W. Strober, editors. John Wylie & Sons, Inc., New York. 2.4.1-2.4.7.
16. Towbin, H., T. Strachelin, and J. Gordon. 1979. Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets; procedures and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
17. Lowry, O., N.J. Rosenbrough, L.A. Farr, and R.J. Randall. 1951. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193:265-275.
18. Shiratori, Y., K.A. Okwu, and I. Tabas. 1994. Free cholesterol loading of macrophages stimulates phosphatidylcholine biosynthesis and up-regulation of CTP: phosphocholine cytidylyltransferase. J. Biol. Chem. 269:11337-11348.
19. Chirgwin, J.M., A.E. Przybyla, R.J. MacDonald, and W.J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 18:5294-5299.
20. Stary, H.C., A.B. Chandler, R.E. Dinsmore, V. Fuster, S. Glasgov, W. Insull, M.E. Rosenfeld, C.J. Schwartz, W.D. Wagner, and R.W. Wissler. 1995. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis - a report from the committee of vascular lesions of council on atherosclerosis, American Heart Association. Arterioscler. Thromb. Vasc. Biol. 15:1512-1531.
21. Skalli, O., P. Ropraz, A. Trzeciak, G. Benzonana, D. Gillessen, and G. Gabbiani. 1986. A monoclonal antibody against α-smooth muscle actin: a new probe for smooth muscle differentiation. J. Cell. Biol. 103:2787-2796.
22. Sanger, A., S. Nicklen, and A. Coulson. 1977. DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
23. Hirota, S., M. Imakita, K. Kohri, A. Ito, E. Morii, S. Adachi, H.M. Kim, Y. Kitamura, C. Yutani, and S. Nomura. 1993. Expression of osteopontin messenger RNA by macrophages in atherosclerotic plaques. Am. J. Pathol. 143: 1003-1008.
24. Falini, B., L. Flenghi, S. Pileri, M. Gambacorta, B. Bigerna, H. Durkop, F. Eitelbach, J Thiele, R. Pacini, A. Cavaliere, et al. 1993. PG-M1: a new monoclonal antibody directed against a fixative-resistant epitope on the macrophage-restricted form of CD68 molecule. Am. J. Pathol. 142:1359-1372.
25. Matsuo, N., S. Ogawa, Y. Imai, T. Takagi, M. Tohyama, D.M. Stern, and A. Wanaka. 1995. Cloning of a novel RNA binding polypeptide (RA301) induced by hypoxia/reoxygenation. J. Biol. Chem. 270:28216-28222.
26. Kuwabara, K., D.J. Pinsky, A.M. Schmidt, C. Benedict, J. Brett, S. Ogawa, M.J. Broekman, A.J. Marcus, R.R. Sciacca, and M. Michalak. 1995. Calreticulin, an antithrombotic agent which binds to vitamin K-dependent coagulation factors, stimulates endothelial nitric oxide production, and limits thrombosis in canine coronary arteries. J. Biol. Chem. 270:8179-8187.
27. Barker, S.G., A. Talbert, S. Cottam, P.A. Baskerville, and J.F. Martin. 1993. Arterial intimai hyperplasia after occlusion of the adventitial vasa vasorum in the pig. Arterioscler. Thromb. 13:70-77.
28. Martin, J.F., R.F. Booth, and S. Moncada. 1991. Arterial wall hypoxia following thrombosis of the vasa vasorum is an initial lesion in atherosclerosis. Eur. J. Clin. Invest. 21:355-359.
29. Heistad, D.D., M.L. Marcus, G.E. Larsen, and M.L. Armstrong. 1982. Role of vasa vasorum in nourishment of the aortic wall. Am. J. Physiol. 240: 781-787.
30. Nakata, Y., and S. Shionoya. 1966. Vascular lesions due to obstruction of the vasa vasorum. Nature (Lond.). 212:1258-1259.
31. Crawford, D.W., and D.H. Blankenhorn. 1991. Arterial wall oxygenation, oxyradicals, and atherosclerosis. Atherosclerosis. 89:97-108.
32. Santilli, S.M., V.D. Fiegel, and D.R. Knighton. 1992. Changes in the aortic wall oxygen tensions of hypertensive rabbits. Hypertension and aortic wall oxygen. Hypertension (Dallas). 19:33-39.
33. Santilli, S.M., V.D. Fiegel, and D.R. Knighton. 1993. Alloxan diabetes alters the rabbit transarterial wall oxygen gradient. J Vasc Surg. 18:227-233.
34. Heacock, C.S., and R.M. Sutherland. 1986. Induction characteristics of oxygen regulated protein. Int. J. Radiat. Oncol. Biol. Phys. 12:1287-1290.
35. Pelham, R.B.H. 1986. Speculation on the functions on the major heat shock and glucose-regulated proteins. Cell. 46:959-961.
36. Libby, P., and S.K. Clinton. 1993. The role of macrophage in atherogenesis. Curr. Opin. Lipidol. 4:355-363.
37. Ross, R. 1993. The pathogenesis of atherosclerosis: a perspective for 1990s. Nature (Lond.). 362:801-809.
38. Lee, A.S. 1992. Mammalian stress response: induction of the glucose regulated protein family. Curr. Opin. Cell Biol. 4:267-273.
39. Knighton, D.R., T.K. Hunt, H. Scheuenstuhl, B. Halliday, Z. Werb, and M. Banda. 1983. Oxygen tension regulates the expression of angiogenesis factor by macrophages. Science (Wash. DC). 221:1283-1285.
40. Kuwabara, K., S. Ogawa, M. Matsumoto, S. Koga, M. Clauss, D.J. Pinsky, P. Lyn, J. Leavy, L. Witte, J. Joseph-Silverstein, et al. 1995. Hypoxia-mediated induction of acidic/basic fibroblast growth factor and platelet-derived growth factor in mononuclear phagocytes stimulates growth of hypoxic endothelial cells. Proc. Natl. Acad. Sci. USA. 92:4606-4610.
41. Falk, E. 1992. Why do plaques rupture? Circulation. 86(suppl. III): 30-42.
42. Xu, Q., J. Willeit, M. Marosi, R. Kleindienst, F. Oberhollenzer, S. Kiechl, T. Stulnig, G. Luef, and G. Wick. 1993. Association of serum antibodies to heat-shock protein 65 with carotid atherosclerosis. Lancet (N. Am. Ed.). 341: 255-259.