Immunohistochemical localization of hepatic nitric oxide synthase in normal and transgenic sickle cell mice: the effect of hypoxia.

Nitric oxide (NO) generated from L-arginine and molecular oxygen by nitric oxide synthase (NOS) has been shown to influence hepatocellular function and pathology in response to ischemia and certain hepatotoxins. In the present study, we examined the liver of a transgenic line of sickle cell mice for hepatocellular injury and localization of two isoforms of NOS, the endothelial constitutively expressed isoform (EcNOS) and the inducible isoform (iNOS) by immunohistochemistry. Diffuse expression of EcNOS was observed in hepatocytes of control and sickle cell animals maintained under room air conditions. In contrast, iNOS was observed only in the sickle cell mice, well-localized to hepatocytes surrounding the central veins of the lobules. When normal mice were exposed to hypoxic conditions for 4 to 5 days, iNOS immunostaining appeared de novo in a patchy distribution throughout the liver lobules. In the sickle cell mice, hypoxia appeared to increase the subjective intensity of pericentral staining of iNOS. Liver histology was normal in the sickle cell mice maintained under room air conditions, but showed multifocal areas of necrosis when sickling was exacerbated by chronic hypoxic conditions. However, a pericentral zone of preserved architecture was present, corresponding to the region of iNOS staining. We postulate that pericentral induction of iNOS under ambient conditions occurs in transgenic sickle cell mice in response to particularly intense hypoxic conditions near the central veins of the liver. Increases in NO synthesis may occur in this region, which would serve to protect these cells from ischemic damage either directly or by maintaining blood flow. These findings could be relevant to liver pathophysiology in patients with sickle cell disease.

[1]  R. Nagel,et al.  Renal nitric oxide synthases in transgenic sickle cell mice. , 1996, Kidney international.

[2]  M. Lerch,et al.  The role of nitric oxide in hemodynamic and metabolic alterations induced by prostaglandin F2α in the perfused rat liver , 1995 .

[3]  E. Connolly,et al.  Hypoxia and modification of the endothelium: implications for regulation of vascular homeostatic properties. , 1995, Seminars in cell biology.

[4]  J. Hofrichter,et al.  A second generation transgenic mouse model expressing both hemoglobin S (HbS) and HbS-Antilles results in increased phenotypic severity. , 1995, Blood.

[5]  C. Foster,et al.  Chronic intrahepatic cholestasis in sickle cell disease requiring exchange transfusion. , 1995, Gut.

[6]  H. Ischiropoulos,et al.  Endotoxin-stimulated nitric oxide production increases injury and reduces rat liver chemiluminescence during reperfusion. , 1995, Gastroenterology.

[7]  T. Billiar The delicate balance of nitric oxide and superoxide in liver pathology. , 1995, Gastroenterology.

[8]  J. Polak,et al.  Immunochemical localization of inducible nitric oxide synthase in endotoxin-treated rats. , 1994, Laboratory investigation; a journal of technical methods and pathology.

[9]  C. Nathan,et al.  The high‐output nitric oxide pathway: role and regulation , 1994, Journal of leukocyte biology.

[10]  R. Schrier,et al.  Nitric oxide: a mediator in rat tubular hypoxia/reoxygenation injury. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[11]  H. Miki,et al.  Prostaglandin E1 abrogates early reductive stress and zone-specific paradoxical oxidative injury in hypoperfused rat liver. , 1994, The Journal of clinical investigation.

[12]  T. Hoang,et al.  Sickle cell disease of transgenic SAD mice. , 1994, Blood.

[13]  Joseph Loscalzo,et al.  A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds , 1993, Nature.

[14]  E. Lapetina,et al.  Hepatocytes and macrophages express an identical cytokine inducible nitric oxide synthase gene. , 1993, Biochemical and biophysical research communications.

[15]  C. Lowenstein,et al.  Cytokines, endotoxin, and glucocorticoids regulate the expression of inducible nitric oxide synthase in hepatocytes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Nagel,et al.  High expression of human beta S- and alpha-globins in transgenic mice: hemoglobin composition and hematological consequences. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[17]  R. Nagel,et al.  High expression of human beta S- and alpha-globins in transgenic mice: erythrocyte abnormalities, organ damage, and the effect of hypoxia. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Pinsky,et al.  Hypoxia-mediated induction of endothelial cell interleukin-1 alpha. An autocrine mechanism promoting expression of leukocyte adhesion molecules on the vessel surface. , 1992, The Journal of clinical investigation.

[19]  T. Billiar,et al.  Nitric oxide synthesis serves to reduce hepatic damage during acute murine endotoxemia , 1992, Critical care medicine.

[20]  J. Crawford,et al.  Hypoxic liver injury and the ameliorating effects of fructose: the "glucose paradox" revisited. , 1992, The American journal of physiology.

[21]  A. Nussler,et al.  Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin , 1992, The Journal of experimental medicine.

[22]  S. Moncada,et al.  Protective and pathological roles of nitric oxide in endotoxin shock. , 1992, Cardiovascular research.

[23]  R. Johns,et al.  Characterization of endothelium-derived relaxing factor/nitric oxide synthase from bovine cerebellum and mechanism of modulation by high and low oxygen tensions. , 1991, The Journal of pharmacology and experimental therapeutics.

[24]  E. Rubin,et al.  Hypoxia-induced in vivo sickling of transgenic mouse red cells. , 1991, The Journal of clinical investigation.

[25]  R. L. Simmons,et al.  Modulation of Nitrogen Oxide Synthesis In Vivo: NG‐Monomethyl‐L‐Arginine Inhibits Endotoxin‐Induced Nitrate/Nitrate Biosynthesis While Promoting Hepatic Damage , 1990, Journal of leukocyte biology.

[26]  T. Schubert Hepatobiliary system in sickle cell disease. , 1986, Gastroenterology.

[27]  M. Omata,et al.  Liver Involvement in Sickle Cell Disease , 1985, Medicine.

[28]  J. Lemasters,et al.  Cell surface changes and enzyme release during hypoxia and reoxygenation in the isolated, perfused rat liver , 1983, The Journal of cell biology.

[29]  S. Ballas,et al.  Clinical, hematological, and biochemical features of Hb SC disease , 1982, American journal of hematology.

[30]  J. Lemasters,et al.  Centrilobular injury following hypoxia in isolated, perfused rat liver. , 1981, Science.

[31]  G. Hutchins,et al.  The liver in sickle cell disease. A clinicopathologic study of 70 patients. , 1980, The American journal of medicine.

[32]  W. Lautt Method for measuring hepatic uptake of oxygen or other blood-borne substances in situ. , 1976, Journal of applied physiology.

[33]  I. W. Mclean,et al.  PERIODATE-LYSINE-PARAFORMALDEHYDE FIXATIVE A NEW FIXATIVE FOR IMMUNOELECTRON MICROSCOPY , 1974, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.