Distribution of heme oxygenase isoforms in rat liver. Topographic basis for carbon monoxide-mediated microvascular relaxation

Journal of Clinical Investigation

Volumn 101, Issue 3, 1998, Pages 604-612

  Goda, Nobuhito ^a   Suzuki, Kensuke ^d   Naito, Makoto ^b   Takeoka, Shinji ^c   Tsuchida, Eishun ^c   Ishimura, Yuzuru ^a   Tamatani, Takuya ^d   Suematsu, Makoto ^a  

^a KEIO UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c WASEDA UNIVERSITY   (Japan)

^d JT Inc   (Japan)

Author keywords

Heme oxygenase 1; Heme oxygenase 2; Hemoglobin; Hepatic stellate cells; Kupffer cells

Indexed keywords

HEME OXYGENASE;

ANIMAL TISSUE; ARTICLE; ENZYME INHIBITION; ENZYME SUBSTRATE; IMMUNOHISTOCHEMISTRY; KUPFFER CELL; LIVER METABOLISM; LIVER PARENCHYMA; LIVER PERFUSION; LIVER SINUSOID; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; STELLATE CELL; TISSUE DISTRIBUTION; VASCULAR RESISTANCE;

EID: 0032005790     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1324     Document Type: Article

References (46)

1. Shibahara, S., R. Müller, H. Taguchi, and T. Yoshida. 1985. Cloning and expression of cDNA of rat heme oxygenase. Proc. Natl. Acad. Sci. USA 82: 7865-7869.
2. Maines, M.D. 1988. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2:2557-2568.
3. Ewing, J.F., and M.D. Maines. 1991. Rapid induction of heme oxygenase 1 mRNA and protein by hyperthermia in rat brain: heme oxygenase 2 is not a heat shock protein. Proc. Natl. Acad. Sci. USA. 88:5364-5368.
4. Rizzardini, M., M. Terao, F. Falciani, and L. Cantoni. 1993. Cytokine induction of haem oxygenase mRNA in mouse liver. Biochem. J. 290:343-347.
5. Maines, M.D., and A. Kappas. 1977. Metals as regulators of heme metabolism: physiological and toxicological implications. Science. 198:1215-1221.
6. Kurata, S., M. Matsumoto, Y. Tsuji, and H. Nakajima. 1996. Lipopolysaccharide activates transcription of the heme oxygenase gene in mouse M1 cells through oxidative activation of nuclear factor κB. Eur. J. Biochem. 239:566-571.
7. Tacchini, L., L. Schiaffonati, C. Pappalardo, C. Gatti, and A. Bernelli-Zazzera. 1993. Expression of HSP 70, immediate-early response and heme oxygenase genes in ischemia-reperfused rat liver. Lab. Invest. 68:465-471.
8. Cruse, I., and M.D. Maines. 1988. Evidence suggesting that the two forms of heme oxygenase are products of different genes. J. Biol. Chem. 263:3348-3353.
9. Suematsu, M., S. Kashiwagi, T. Sano, N. Goda, Y. Shinoda, and Y. Ishimura. 1994. Carbon monoxide as an endogenous modulator of hepatic vascular perfusion. Biochem. Biophys. Res. Commun. 205:1333-1337.
10. Suematsu, M., N. Goda, T. Sano, S. Kashiwagi, Y. Shinoda, and Y. Ishimura. 1995. Carbon monoxide: an endogenous modulator of sinusoidal tone in the perfused rat liver. J. Clin. Invest. 96:2431-2437.
11. Sano, T., M. Shiomi, M. Wakabayashi, Y. Shinoda, N. Goda, T. Yamaguchi, Y. Nimura, Y. Ishimura, and M. Suematsu. 1997. Endogenous carbon monoxide suppression stimulates bile acid-dependent biliary transport in perfused rat liver. Am. J. Physiol. 272(35):G1268-G1275.
12. Stocker, R., A.N. Glazer, and B.N. Ames. 1987. Antioxidant activity of albumin-bound bilirubin. Proc. Natl. Acad. Sci. USA. 84:5918-5922.
13. Yamaguchi, T., F. Horio, T. Hashizume, M. Tanaka, S. Ikeda, A. Kakinuma, and H. Nakajima, 1995. Bilirubin is oxidized in rats treated with endotoxin and acts as a physiological antioxidant synergistically with ascorbic acid in vivo. Biochem. Biophys. Res. Commun. 214:11-19.
14. Oshio, C., and M.J. Phillips. 1981. Contractility of bile canaliculi: implications of liver function. Science. 212:1041-1042.
15. Rotenberg, M.O., and M.D. Maines. 1990. Isolation, characterization and expression in Escherichia coli of a cDNA encoding rat heme oxygenase-2. J. Biol. Chem. 265:7501-7506.
16. Ohashi, H., K. Maruyama, Y. Liu, and A. Yoshimura. 1994. Ligand-induced activation of chimeric receptors between the erythropoietin receptor and receptor tyrosine kinases. Proc. Natl. Acad. Sci. USA. 91:158-162.
17. Suda, T., T. Takahashi, P. Golstein, and S. Nagata. 1993. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell. 75:1169-1178.
18. Yoshida, T., and G. Kikuchi. 1978. Reaction of the microsomal heme oxygenase with cobaltic protoporphyrin IX, an extremely poor substrate. J. Biol. Chem. 253:8479-8482.
19. McKinney, M.M., and A. Parkinson. 1987. A simple, nonchromatographic procedure to purify immunoglobulins from serum and ascites fluid. J. Immunol. Methods. 96:271-278.
20. Yamamoto, T., M. Naito, H. Moriyama, H. Umezu, H. Matsuo, H. Kiwada, and M. Arakawa. 1996. Repopulation of murine Kupffer cells after intravenous administration of liposome-encapsulated dichloromethylene diphosphonate. Am. J. Pathol. 149:1271-1286.
21. Yamaguchi, T., Y. Wakabayashi, M. Tanaka, T. Sano, H. Ishikawa, H. Nakajima, M. Suematsu, and Y. Ishimura. 1996. Taurocholate induces directional transport of bilirubin into bile in the perfused rat liver. Am. J. Physiol. 270:G102H-G1032.
22. Falkenberg, F.W., H. Weichert, M. Krane, I. Bartels, M. Palme, H.O. Nagels, and H. Fiebig. 1995. In vitro production of monoclonal antibodies in high concentration in a new and easy to handle modular minifermentor. J. Immunol. Methods. 179(1):13-29.
23. Sakai, H., S. Takeoka, H. Yokohama, Y. Seino, H. Nishide, and Y. Tsuehida. 1993. Purification of concentrated hemoglobin using organic solvent and heat treatment. Prot. Expr. Pur. 4:563-569.
24. Sakai, H., K. Hamada, S. Takeoka, H. Nishide, and E. Tsuehida. 1996. Physical properties of hemoglobin vesicles as red cell substitutes. Biotechnol. Prog. 12:119-125.
25. Rudolph, A.S., H. Spielberg, B.J. Spargo, and N. Kossovsky. 1995. Histopathologic study following administration of liposome-encapsulated hemoglobin in the normovolemic rats. J. Biomed. Mater. Res. 29:189-196.
26. Naito, M., and E. Wisse. 1978. Filtration effect of endothelial fenestrations on chylomicron transport in neonatal rat liver sinusoids. Cell Tissue Res. 190:371-382.
27. Wisse, E., R.B. DeZanger, K. Charels, P. van der Smissen, and R.S. McCuskey. 1985. The liver sieve: considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Heputology. 5:683-692.
28. Stock, R.J., E.V. Cilento, and R.S. McCuskey. 1989. A quantitative study of fluorescein isothiocyanate-dextran transport in the microcirculation of the isolated perfused rat liver. Hepatology. 9:75-82.
29. Iigou, Y., M. Suematsu, T. Higashida, J. Oheda, K. Matsumoto, Y. Wakabayashi, Y. Ishimura, M. Miyasaka, and T. Takashi. 1997. In vivo constitutive expression of ICAM-1 in rat microvascular systems analyzed by laser confocal microscopy. Am. J. Physiol. 273:H138-H147.
30. Suematsu, M., M. Oda, H. Suzuki, H. Kaneko, N. Watanabe, T. Furusho, S. Masushige. and M. Tsuchiya. 1993. Intravital and electron microscopic observation of Ito cells in rat hepatic microcirculation. Microvasc. Res. 46:28-42.
31. Ewing, J.F., and M.D. Maines. 1995. Distribution of constitutive (HO-2) and heat-inducible (HO-1) heme oxygenase isozymes in rat testes: HO-2 displays stage-specific expression in germ cells. Endocrinology. 136:2294-2302.
32. Knook, D.E., and A.M. De Leeuw. 1982. Connective tissue of the normal and fibrotic human liver. Thieme, Stuttgart. 67-71 pp.
33. Wake, K. 1980. Perisinusoidal stellate cells (fat-storing cells, interstitial cells, lipocytes), their related structure in and around the liver sinusoids, and vitamin A-storing cells in extrahepatic organs. Int. Rev. Cytol. 66:303-353.
34. Kashiwagi, S., M. Suematsu, Y. Wakabayashi, N. Kawada, M. Tachibana, A. Koizumi, M. Inoue, Y. Ishimura, and A. Kaneko. 1997. Electrophysiological characterization of cultured hepatic stellate cells in rats. Am. J. Physiol. 272 (35):G742-G750.
35. Nishida, J., R.S. McCuskey, D. McDonnell, and E.S. Fox. 1994. Protective role of NO in hepatic microcirculatory dysfunction during endotoxemia. Am. J. Physiol. 267:G1135-G1141.
36. R.F. Eich, T. Li, D.D. Lomon, D.H. Doherty, S.R. Curry, J.F. Aitken, A.J. Mathews, K.A. Johnson, R.D. Smith, G.N. Phillips, and J.S. Olson. 1996. Mechanism of NO-induced oxidation of myoglobin and hemoglobin. Biochemistry. 35:6976-6983.
37. Ignarro, L.J., B. Barrot, and K.S. Wood. 1984. Regulation of soluble guanylate cyclase activity by porphyrins and metalloporphyrins. J. Biol. Chem. 259:6201-6207.
38. Wolff, D.J., R.A. Naddelman, A. Lubeskie, and D.A. Saks. 1996. Inhibition of nitric oxide synthase isoforms by porphyrins. Arch. Biochem. Biophys. 333:27-34.
39. Linden, D.J., K. Narasimhan, and D. Gurfel. 1993. Protoporphyrins modulate voltage-gated Ca current in AtT-20 pituitary cells. J. Neurophysiol. 70:2673-2677.
40. Gulati, A., and A.C. Sharma. 1994. Prazosin blocks the pressor but not the regional circulatory effects of diaspirin crosslinked hemoglobin. Life Sci. 55: 121-130.
41. Bissell, D.M., L. Hammaker, and R. Schmid. 1972. Hemoglobin and erythrocyte catabolism in rat liver: the separate roles of parenchymal and sinusoidal cells. Blood. 40:812-822.
42. Kutty, R.K., R.F. Daniel, D.E. Ryan, W. Levin, and M.D. Maines. 1988. Rat liver cytochrome P-450b, P-420b, and P-420c are degraded to biliverdin by heme oxygenase. Arch. Biochem. Biophys. 260:638-644.
43. Choi, A.M.K., and J. Alam. 1996. Heme oxygenase-1: function, regulation, and implication of a novel stress-inducible protein in oxidant-induced lung injury. Am. J. Respir. Cell Mol. Biol. 15:9-19.
44. Camhi, S.L., J. Alam, L. Otterbein, S.L. Sylvester, and A.M.K. Choi. 1995. Induction of heme oxygenase-1 gene expression by lipopolysaccharide is mediated by AP-1 activation. Am. J. Respir. Cell Mol. Biol. 13:387-398.
45. Roelofsen, H., C.N. Van Der Veere, R. Ottenhoff, B. Schoemaker, P.L.M. Jansen, and R.P.J. Oude Elferink. 1994. Decreased bilirubin transport in the perfused liver of endotoxemic rats. Gastroenterology. 107:1075-1084.
46. Roelofsen, H., B. Schoemaker, R. Ottenhoff, P.L.M. Jansen, and R.P.J. Oude Elferink. 1995. Impaired hepatocanalicular organ anion transport in endotoxemic rats. Am. J. Physiol. 269:G427-G434.