Induction of haem oxygenase-1 causes cortical non-haem iron increase in experimental pneumococcal meningitis: Evidence that concomitant ferritin up-regulation prevents iron-induced oxidative damage

Journal of Neurochemistry

Volumn 100, Issue 2, 2007, Pages 532-544

  Ren, Hao ^a   Leib, Stephen L ^a   Ferriero, Donna M ^b   Täuber, Martin G ^a   Christen, Stephan ^a,c  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Institute for Infectious Diseases   (Switzerland)

Author keywords

Bacterial meningitis; Bilirubin; Brain injury; Hydroxyl radical; Inflammation; Iron

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; BILIRUBIN; BRAIN ENZYME; DNA; FERRITIN; HEME; HEME OXYGENASE 1; HEME OXYGENASE 2; HEME OXYGENASE INHIBITOR; IRON; RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL MENINGITIS; BRAIN CORTEX; BRAIN LEVEL; CAPILLARY ENDOTHELIUM; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HOMEOSTASIS; MICROGLIA; NERVE CELL; NONHUMAN; OXIDATION; PERIKARYON; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; STAINING; UPREGULATION;

ANIMALS; ANIMALS, NEWBORN; APOFERRITINS; CEREBRAL CORTEX; DEOXYRIBONUCLEASES; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, VIRAL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCOPROTEINS; HEME OXYGENASE-1; HYDROGEN PEROXIDE; IN SITU NICK-END LABELING; IRON; LECTINS; MENINGITIS, PNEUMOCOCCAL; METALLOPORPHYRINS; PROTOPORPHYRINS; RATS; RATS, WISTAR; RIBONUCLEASES; UP-REGULATION;

ANIMALIA; BACTERIA (MICROORGANISMS);

EID: 33845730329     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04230.x     Document Type: Article

References (52)

1. Auer M., Pfister L. A., Leppert D., Täuber M. G. and Leib S. L. (2000) Effects of clinically used antioxidants in experimental pneumococcal meningitis. J. Infect. Dis. 182, 347-350.
2. Balla G., Jacob H. S., Balla J., Rosenberg M., Nath K., Apple F., Eaton J. W. and Vercellotti G. M. (1992) Ferritin: a cytoprotective antioxidant strategem of endothelium. J. Biol. Chem. 267, 18 148-18 153.
3. Bergeron M., Ferriero D. M., Vreman H. J., Stevenson D. K. and Sharp F. R. (1997) Hypoxia-ischemia, but not hypoxia alone, induces the expression of heme oxygenase-1 (HSP32) in newborn rat brain. J. Cereb. Blood Flow Metab. 17, 647-658.
4. Bergeron M., Gidday J. M., Yu A. Y., Semenza G. L., Ferriero D. M. and Sharp F. R. (2000) Role of hypoxia-inducible factor-1 in hypoxia-induced ischemic tolerance in neonatal rat brain. Ann. Neurol. 48, 285-296.
5. Böttcher T., Ren H., Goiny M. et al. (2004) Clindamycin is neuroprotective in experimental Streptococcus pneumoniae meningitis compared with ceftriaxone. J. Neurochem. 91, 1450-1460.
6. Carraway M. S., Ghio A. J., Taylor J. L. and Piantadosi C. A. (1998) Induction of ferritin and heme oxygenase-1 by endotoxin in the lung. Am. J. Physiol. 275, L583-L592.
7. Cheepsunthorn P., Palmer C. and Connor J. R. (1998) Cellular distribution of ferritin subunits in postnatal rat brain. J. Comp. Neurol. 400, 73-86.
8. Chen K., Gunter K. and Maines M. D. (2000) Neurons overexpressing heme oxygenase-1 resist oxidative stress-mediated cell death. J. Neurochem. 75, 304-313.
9. Connor J. R., Menzies S. L., Burdo J. R. and Boyer P. J. (2001) Iron and iron management proteins in neurobiology. Pediatr. Neurol. 25, 118-129.
10. Cui J., Holmes E. H. and Liu P. K. (1999) Oxidative damage to the c-fos gene and reduction of its transcription after focal cerebral ischemia. J. Neurochem. 73, 1164-1174.
11. Dore S., Takahashi M., Ferris C. D., Zakhary R., Hester L. D., Guastella D. and Snyder S. H. (1999) Bilirubin, formed by activation of heme oxygenase-2, protects neurons against oxidative stress injury. Proc. Natl Acad. Sci. USA 96, 2445-2450.
12. Eisenstein R. S., Garcia-Mayol D., Pettingell W. and Munro H. N. (1991) Regulation of ferritin and heme oxygenase synthesis in rat fibroblasts by different forms of iron. Proc. Natl Acad. Sci. USA 88, 688-692.
13. Everse J. and Hsia N. (1997) The toxicities of native and modified hemoglobins. Free Radic. Biol. Med. 22, 1075-1099.
14. Ewing J. F. and Maines M. D. (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.
15. Ferris C. D., Jaffrey S. R., Sawa A. et al. (1999) Haem oxygenase-1 prevents cell death by regulating cellular iron. Nat. Cell Biol. 1, 152-157.
16. Fukuda K., Richmon J. D., Sato M., Sharp F. R., Panter S. S. and Noble L. J. (1996) Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury. Brain Res. 736, 68-75.
17. Gianinazzi C., Grandgirard D., Imboden H., Egger L., Meli D. N., Bifrare Y. D., Joss P. C., Täuber M. G., Borner C. and Leib S. L. (2003) Caspase-3 mediates hippocampal apoptosis in pneumococcal meningitis. Acta Neuropathol. (Berl.) 105, 499-507.
18. Halliwell B. (1992) Reactive oxygen species and the central nervous system. J. Neurochem. 59, 1609-1623.
19. Henle E. S., Luo Y., Gassmann W. and Linn S. (1996) Oxidative damage to DNA constituents by iron-mediated fenton reactions. The deoxyguanosine family. J. Biol. Chem. 271, 21 177-21 186.
20. Higgins T. (1981) Novel chromogen for serum iron determinations. Clin. Chem. 27, 1619-1620.
21. Hintze K. J. and Theil E. C. (2005) DNA and mRNA elements with complementary responses to hemin, antioxidant inducers, and iron control ferritin-L expression. Proc. Natl Acad. Sci. USA 102, 15 048-15 052.
22. Honda K., Smith M. A., Zhu X. et al. (2005) Ribosomal RNA in Alzheimer disease is oxidized by bound redox-active iron. J. Biol. Chem. 280, 20 978-20 986.
23. Huang E., Ong W. Y., Go M. L. and Garey L. J. (2005) Heme oxygenase-1 activity after excitotoxic injury: immunohistochemical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainate treatment. J. Neurosci. Res. 80, 268-278.
24. ILARCLS (1996) Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington, D.C.
25. Kakhlon O. and Cabantchik Z. I. (2002) The labile iron pool: characterization, measurement, and participation in cellular processes (1). Free Radic. Biol. Med. 33, 1037-1046.
26. Keep R. F., Xi G., Hua Y. and Hoff J. T. (2005) The deleterious or beneficial effects of different agents in intracerebral hemorrhage: think big, think small, or is hematoma size important? Stroke 36, 1594-1596.
27. Kim C. K. and Rivier C. L. (2000) Nitric oxide and carbon monoxide have a stimulatory role in the hypothalamic-pituitary-adrenal response to physico-emotional stressors in rats. Endocrinology 141, 2244-2253.
28. Kitamura Y., Ishida Y., Takata K. et al. (2003) Hyperbilirubinemia protects against focal ischemia in rats. J. Neurosci. Res. 71, 544-550.
29. Leib S. L., Clements J. M., Lindberg R. L., Heimgartner C., Loeffler J. M., Pfister L. A., Täuber M. G. and Leppert D. (2001) Inhibition of matrix metalloproteinases and tumour necrosis factor alpha converting enzyme as adjuvant therapy in pneumococcal meningitis. Brain 124, 1734-1742.
30. Maines M. D. (1997) The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37, 517-554.
31. Mancuso C. (2004) Heme oxygenase and its products in the nervous system. Antioxid. Redox Signal. 6, 878-887.
32. Miller L. L., Miller S. C., Torti S. V., Tsuji Y. and Torti F. M. (1991) Iron-independent induction of ferritin H chain by tumor necrosis factor. Proc. Natl Acad. Sci. USA 88, 4946-4950.
33. Moos T. and Morgan E. H. (1998) Evidence for low molecular weight, non-transferrin-bound iron in rat brain and cerebrospinal fluid. J. Neurosci. Res. 54, 486-494.
34. Morita T. and Kourembanas S. (1995) Endothelial cell expression of vasoconstrictors and growth factors is regulated by smooth muscle cell-derived carbon monoxide. J. Clin. Invest. 96, 2676-2682.
35. Nguyen-Legros J., Bizot J., Bolesse M. and Pulicani J. P. (1980) 'Diaminobenzidine black' as a new histochemical demonstration of exogenous iron. Histochemistry 66, 239-244.
36. Nilsson U. A., Bassen M., Savman K. and Kjellmer I. (2002) A simple and rapid method for the determination of 'free' iron in biological fluids. Free Radic. Res. 36, 677-684.
37. Nunomura A., Perry G., Pappolla M. A., Wade R., Hirai K., Chiba S. and Smith M. A. (1999) RNA oxidation is a prominent feature of vulnerable neurons in Alzheimer's disease. J. Neurosci. 19, 1959-1964.
38. Ogihara T., Hirano K., Ogihara H. et al. (2003) Non-protein-bound transition metals and hydroxyl radical generation in cerebrospinal fluid of newborn infants with hypoxic ischemic encephalopathy. Pediatr. Res. 53, 594-599.
39. Otterbein L. E., Soares M. P., Yamashita K. and Bach F. H. (2003) Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 24, 449-455.
40. Panahian N., Yoshiura M. and Maines M. D. (1999) Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J. Neurochem. 72, 1187-1203.
41. Park E. M., Shigenaga M. K., Degan P., Korn T. S., Kitzler J. W., Wehr C. M., Kolachana P. and Ames B. N. (1992) Assay of excised oxidative DNA lesions: isolation of 8-oxoguanine and its nucleoside derivatives from biological fluids with a monoclonal antibody column. Proc. Natl Acad. Sci. USA 89, 3375-3379.
42. Pennell N. A., Hurley S. D. and Streit W. J. (1994) Lectin staining of sheep microglia. Histochemistry 102, 483-486.
43. Pfister L. A., Tureen J. H., Shaw S., Christen S., Ferriero D. M., Täuber M. G. and Leib S. L. (2000) Endothelin inhibition improves cerebral blood flow and is neuroprotective in pneumococcal meningitis. Ann. Neurol. 47, 329-335.
44. Ratan R. R., Siddiq A., Aminova L., Lange P. S., Langley B., Ayoub I., Gensert J. and Chavez J. (2004) Translation of ischemic preconditioning to the patient: prolyl hydroxylase inhibition and hypoxia inducible factor-1 as novel targets for stroke therapy. Stroke 35, 2687-2689.
45. Ryter S. W., Alam J. and Choi A. M. (2006) Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol. Rev. 86, 583-650.
46. Schaper M., Gergely S., Lykkesfeldt J., Zbären J., Leib S. L., Täuber M. G. and Christen S. (2002) Cerebral vasculature is the major target of oxidative protein alterations in bacterial meningitis. J. Neuropathol. Exp. Neurol. 61, 605-613.
47. Stocker R., Yamamoto Y., McDonagh A. F., Glazer A. N. and Ames B. N. (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235, 1043-1046.
48. Thompson K., Menzies S., Muckenthaler M., Torti F. M., Wood T., Torti S. V., Hentze M. W., Beard J. and Connor J. (2003) Mouse brains deficient in H-ferritin have normal iron concentration but a protein profile of iron deficiency and increased evidence of oxidative stress. J. Neurosci. Res. 71, 46-63.
49. Torti F. M. and Torti S. V. (2002) Regulation of ferritin genes and protein. Blood 99, 3505-3516.
50. Vreman H. J., Cipkala D. A. and Stevenson D. K. (1996) Characterization of porphyrin heme oxygenase inhibitors. Can. J. Physiol. Pharmacol. 74, 278-285.
51. Wang X. S., Ong W. Y. and Connor J. R. (2002) Increase in ferric and ferrous iron in the rat hippocampus with time after kainate-induced excitotoxic injury. Exp. Brain Res. 143, 137-148.
52. Yu S. W., Wang H., Dawson T. M. and Dawson V. L. (2003) Poly (ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol. Dis. 14, 303-317.