ANP-induced decrease of iron regulatory protein activity is independent of HO-1 induction

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 287, Issue 3 50-3, 2004, Pages

  Kiemer, Alexandra K ^a,b,d   Förnges, Anke C ^a,b   Pantopoulos, Kostas ^c   Bilzer, Manfred ^b   Andriopoulos, Bill ^c   Gerwig, Tobias ^a,b   Kenngott, Silke ^b   Gerbes, Alexander L ^b   Vollmar, Angelika M ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^c MCGILL UNIVERSITY   (Canada)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

cGMP; Heat shock proteins; Hepatoprotection; Hormonal preconditioning; Ischemia reperfusion injury

Indexed keywords

8 BROMO CYCLIC GMP; ATRIAL NATRIURETIC FACTOR; FERRITIN; HEME OXYGENASE 1; IRON REGULATORY FACTOR; PROTEIN KINASE C ALPHA; PROTEIN KINASE C EPSILON; PROTOPORPHYRIN TIN; UNIVERSITY OF WISCONSIN SOLUTION;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INDUCTION; ENZYME LOCALIZATION; LIVER ISCHEMIA; LIVER PROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REPERFUSION INJURY; WESTERN BLOTTING;

ANIMALS; ATRIAL NATRIURETIC FACTOR; BLOTTING, WESTERN; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FERRITINS; HEME OXYGENASE (DECYCLIZING); HEME OXYGENASE-1; HEPATOCYTES; IRON-REGULATORY PROTEINS; ISOENZYMES; LIVER; PERFUSION; PHOSPHORYLATION; PRECIPITIN TESTS; PROTEIN KINASE C; RATS; REPERFUSION INJURY; RNA, MESSENGER; TETRADECANOYLPHORBOL ACETATE;

EID: 4143069099     PISSN: 01931857     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpgi.00514.2003     Document Type: Article

References (57)

1. Arosio P and Levi S. Ferritin, iron homeostasis, and oxidative damage. Free Radic Biol Med 33: 457-463, 2002.
2. Bauer M and Bauer I. Heme oxygenase-1: redox regulation and role in the hepatic response to oxidative stress. Antioxid Redox Signal 4: 749-758, 2002.
3. Berenshtein E, Vaisman B, Goldberg-Langerman C, Kitrossky N, Konijn AM, and Chevion M. Roles of ferritin and iron in ischemic preconditioning of the heart. Mol Cell Biochem 234-235: 283-292, 2002.
4. Beuers U, Bilzer M, Chittattu A, Kullak-Ublick GA, Keppler D, Paumgartner G, and Dombrowski F. Tauroursodeoxycholic acid inserts the apical conjugate export pump, Mrp2, into canalicular membranes and stimulates organic anion secretion by protein kinase C-dependent mechanisms in cholestatic rat liver. Hepatology 33: 1206-1216, 2001.
5. Beuers U, Denk GU, Soroka CJ, Wimmer R, Rust C, Paumgartner G, and Boyer JL. Taurolithocholic acid exerts cholestatic effects via phosphatidylinositol 3-kinase-dependent mechanisms in perfused rat livers and rat hepatocyte couplets. J Biol Chem 278: 17810-17818, 2003.
6. Beuers U, Probst I, Soroka C, Boyer JL, Kullak-Ublick GA, and Paumgartner G. Modulation of protein kinase C by taurolithocholic acid in isolated rat hepatocytes. Hepatology 29: 477-482, 1999.
7. Bilzer M, Jaeschke H, Vollmar AM, Paumgartner G, and Gerbes AL. Prevention of Kupffer cell-induced oxidant injury in rat liver by atrial natriuretic peptide. Am J Physiol Gastrointest Liver Physiol 276: G1137-G1144, 1999.
8. Bilzer M, Witthaut R, Paumgartner G, and Gerbes AL. Prevention of ischemia/reperfusion injury in the rat liver by atrial natriuretic peptide. Gasfroenterology 106: 143-151, 1994.
9. Cairo G, Recalcati S, Pietrangelo A, and Minotti G. The iron regulatory proteins: targets and modulators of free radical reactions and oxidative damage, Free Radic Biol Med 32: 1237-1243, 2002.
10. Carini R, De Cesaris MG, Splendore R, Domenicotti C, Nitti MP, Pronzato MA, and Albano E. Mechanisms of hepatocyte protection against hypoxic injury by atrial natriuretic peptide. Hepatology 37: 277-285, 2003.
11. Ferreira C, Bucchini D, Martin ME, Levi S, Arosio P, Grandchamp B, and Beaumont C. Early embryonic lethality of H ferritin gene deletion in mice. J Biol Chem 275: 3021-3024, 2000.
12. Garrick MD, Nunez MT, Olivares M, and Harris ED. Parallels and contrasts between iron and copper metabolism. Biometals 16: 1-8, 2003.
13. Gerbes AL, Vollmar AM, Kiemer AK, and Bilzer M. The guanylate cyclase-coupled natriuretic peptide receptor: a new target for prevention of cold ischemia-reperfusion damage of the rat liver. Hepatology 28: 1309-1317, 1998.
14. Gerwig T, Meissner H, Bilzer M, Kiemer AK, Arnholdt H, Vollmar AM, and Gerbes AL. Atrial natriuretic peptide preconditioning protects against hepatic preservation injury by attenuating necrotic and apoptotic cell death. J Hepatol 39: 341-348, 2003.
15. Gray NK, Quick S, Goossen B, Constable A, Hirling H, Kuhn LC, and Hentze MW. Recombinant iron-regulatory factor functions as an iron-responsive element-binding protein, a translational represser and an aconitase. A functional assay for translational repression and direct demonstration of the iron switch. Eur J Biochem 218: 657-667, 1993.
16. Gugenheim J. Atrial natriuretic peptide (ANP) preconditioning: what is the relevance of the antiapoptotic effects? J Hepatol 39: 428-430, 2003.
17. Halliwell B and Gutteridge JMC. Protection against oxidants in biological systems: the Superoxide theory of oxygen toxicity. In: Free Radic Biol Med Oxford: Clarendon, 1989, p. 86-179.
18. Hanson ES, Foot LM, and Leibold EA. Hypoxia post-translationally activates iron-regulatory protein 2. J Biol Chem 274: 5047-5052, 1999.
19. Hanson ES and Leibold EA. Regulation of iron regulatory protein 1 during hypoxia and hypoxia/reoxygenation. J Biol Chem 273: 7588-7593, 1998.
20. Hentze MW and Kuhn LC. Molecular control of vertebrate iron metabolism: mRNA-based regulatory circuits operated by iron, nitric oxide, and oxidative stress. Proc Natl Acad Sci USA 93: 8175-8182, 1996.
21. Immenschuh S and Ramadori G. Gene regulation of heme oxygenase-1 as a therapeutic target. Biochem Pharmacol 60: 1121-1128, 2000.
22. Jaeschke H. Molecular mechanisms of hepatic ischemia-reperfusion injury and preconditioning. Am J Physiol Gastrointest Liver Physiol 284: G15-G26, 2003.
23. Jaeschke H, Bautista AP, Spolarics Z, and Spitzer JJ. Superoxide generation by Kupffer cells and priming of neutrophils during reperfusion after hepatic ischemia. Free Radic Res Commun 15: 277-284, 1991.
24. Jaeschke H and Farhood A. Neutrophil and Kupffer cell-induced oxidant stress and ischemia-reperfusion injury in rat liver. Am J Physiol Gastrointest Liver Physiol 260: G355-G362, 1991.
25. Jaeschke H and Smith CW. Mechanisms of neutrophil-induced parenchymal cell injury. J Leukoc Biol 61: 647-653, 1997.
26. Kiemer AK, Gerbes AL, Bilzer M, and Vollmar AM. The atrial natriuretic peptide and cGMP-novel activators of the heat shock response in rat livers. Hepatology 35: 88-94, 2002.
27. Kiemer AK, Gerwig T, Gerbes AL, Meissner H, Bilzer M, and Vollmar AM. Kupffer cell-specific induction of heme oxygenase 1 (hsp32) by the atrial natriuretic peptide - role of cGMP. J Hepatol 38: 490-498, 2003.
28. Kumar R, Cartledge WA, Lincoln TM, and Pandey KN. Expression of guanylyl cyclase-A/atrial natriuretic peptide receptor blocks the activation of protein kinase C in vascular smooth muscle cells. Role of cGMP and cGMP-dependent protein kinase. Hypertension 29: 414-421, 1997.
29. Kumar R, von Geldern TW, Calle RA, and Pandey KN. Stimulation of atrial natriuretic peptide receptor/guanylyl cyclase - a signaling pathway antagonizes the activation of protein kinase C-α in maurine Leydig cells. Biochim Biophys Acta 1356: 221-228, 1997.
30. Kuriyama-Matsumura K, Sato H, Suzuki M, and Bannai S. Effects of hyperoxia and iron on iron regulatory protein-1 activity and the ferritin synthesis in mouse peritoneal macrophages. Biochim Biophys Acta 1544: 370-377, 2001.
31. LaPointe MC and Sitkins JR. Phorbol ester stimulates the synthesis and secretion of brain natriuretic peptide from neonatal rat ventricular cardiocytes: a comparison with the regulation of atrial natriuretic factor. Mol Endocrinol 7: 1284-1296, 1993.
32. Leibold EA and Munro HN. Cytoplasmic protein binds in vitro to a highly conserved sequence in the 5′ untranslated region of ferritin heavy- and light-subunit mRNAs. Proc Natl Acad Sci USA 85: 2171-2175, 1988.
33. Lowry OH, Rosebrough NJ, Farr AL, and Randall RJ. Protein measurement with the Polin phenol reagent. J Biol Chem 193: 265-271, 1951.
34. Okawa H, Horimoto H, Mieno S, Nomura Y, Yoshida M, and Shinjiro S. Preischemic infusion of α-human atrial natriuretic peptide elicits myoprotective effects against ischemia reperfusion in isolated rat hearts. Mol Cell Biochem 248: 171-177, 2003.
35. Pandey KN. Atrial natriuretic factor inhibits autophosphorylation of protein kinase C and A 240-kDa protein in plasma membranes of bovine adrenal glomerulosa cells: involvement of cGMP-dependent and independent signal transduction mechanisms. Mol Cell Biochem 141: 103-111, 1994.
36. Pandey KN. Atrial natriuretic factor inhibits the phosphorylation of protein kinase C in plasma membrane preparations of cultured Leydig tumor cells. J Androl 15: 100-109, 1994.
37. Pandey KN, Inagami T, Girard PR, Kuo JF, and Misono KS. New signal transduction mechanisms of atrial natriuretic factor: inhibition of phosphorylation of protein kinase C and A 240-kDa protein in adrenal cortical plasma membrane by cGMP-dependent and -independent mechanisms. Biochem Biophys Res Commun 148: 589-595, 1987.
38. Pantopoulos K and Hentze MW. Nitric oxide signaling to iron-regulatory protein: direct control of ferritin mRNA translation and transferrin receptor mRNA stability in transfected fibroblasts. Proc Natl Acad Sci USA 92: 1267-1271, 1995.
39. 2 formation. FASEB J 14: 1953-1964, 2000.
40. Rogers JT, Andriotakis JL, Lacroix L, Durmowicz GP, Kasschau KD, and Bridges KR. Translational enhancement of H-ferritin mRNA by interleukin-1β acts through 5′ leader sequences distinct from the iron responsive element. Nucleic Acids Res 22: 2678-2686, 1994.
41. Sauro MD and Fitzpatrick DF. Atrial natriuretic peptides inhibit protein kinase C activation in rat aortic smooth muscle. Pept Res 3: 138-141, 1990.
42. Schalinske KL and Eisenstein RS. Phosphorylation and activation of both iron regulatory proteins 1 and 2 in HL-60 cells. J Biol Chem 271: 7168-7176, 1996.
43. Schiaffonati L, Cairo G, and Bernelli-Zazzera A. RNA synthesis by nuclei and nucleoli from ischemic liver cells. J Cell Physiol 97: 487-496, 1978.
44. Schneider BD and Leibold EA. Effects of iron regulatory protein regulation on iron homeostasis during hypoxia. Blood 102: 3404-3411, 2003.
45. Suematsu M and Ishimura Y. The heme oxygenase-carbon monoxide system: a regulator of hepatobiliary function. Hepatology 31: 3-6, 2000.
46. Tacchini L, Recalcati S, Bernelli-Zazzera A, and Cairo G. Induction of ferritin synthesis in ischemic-reperfused rat liver: analysis of the molecular mechanisms. Gastroenterology 113: 946-953, 1997.
47. Theil EC. Ferritin: at the crossroads of iron and oxygen metabolism. J Nutr 133: 1549S-1553S, 2003.
48. Thomson AM, Rogers JT, and Leedman PJ. Iron-regulatory proteins, iron-responsive elements and ferritin mRNA translation, Int J Biochem Cell Biol 31: 1139-1152, 1999.
49. Thomson AM, Rogers JT, and Leedman PJ. Thyrotropin-releasing hormone and epidermal growth factor regulate iron-regulatory protein binding in pituitary cells via protein kinase C-dependent and -independent signaling pathways. J Biol Chem 275: 31609-31615, 2000.
50. Toth I, Yuan L, Rogers JT, Boyce H, and Bridges KR. Hypoxia alters iron-regulatory protein-1 binding capacity and modulates cellular iron homeostasis in human hepatoma and erythroleukemia cells. J Biol Chem 274: 4467-4473, 1999.
51. Tremblay J, Desjardins R, Hum D, Gutkowska J, and Hamet P. Biochemistry and physiology of the natriuretic peptide receptor guanylyl cyclases. Mol Cell Biochem 230: 31-47, 2002.
52. Vile GF, Basu-Modak S, Waltner C, and Tyrrell RM. Heme oxygenase 1 mediates an adaptive response to oxidative stress in human skin fibroblasts. Proc Natl Acad Sci USA 91: 2607-2610, 1994.
53. Vile GF and Tyrrell RM. Oxidative stress resulting from ultraviolet A irradiation of human skin fibroblasts leads to a heme oxygenase-dependent increase in ferritin. J Biol Chem 268: 14678-14681, 1993.
54. Wang J and Pantopoulos K. Conditional derepression of ferritin synthesis in cells expressing a constitutive IRP1 mutant. Mol Cell Biol 22: 4638-4651, 2002.
55. White K and Munro HN. Induction of ferritin subunit synthesis by iron is regulated at both the transcriptional and translational levels. J Biol Chem 263: 8938-8942, 1988.
56. Wyllie S, Seu P, Gao FQ, and Goss JA. Deregulation of iron homeostasis and cold-preservation injury to rat liver stored in University of Wisconsin solution. Liver Transpl 9: 401-410, 2003.
57. Yeh KY, Yeh M, and Glass J. Expression of intestinal brush-border membrane hydrolases and ferritin after segmental ischemia-reperfusion in rats. Am J Physiol Gastrointest Liver Physiol 275: G572-G583, 1998.