Glial HO-1 expression, iron deposition and oxidative stress in neurodegenerative diseases
Abstract
The mechanisms responsible for the pathological deposition of brain iron in Parkinson's disease, Alzheimer's disease and other human neurodegenerative disorders remain poorly understood. In rat primary astrocyte cultures, we demonstrated that dopamine, cysteamine, H(2)O(2) and menadione rapidly induce heme oxygenase-1 (HO-1) expression (mRNA and protein) followed by sequestration of non-transferrin-derived (55)Fe by the mitochondrial compartment. The effects of dopamine on HO-1 expression were inhibited by ascorbate implicating a free radical mechanism of action. Dopamine-induced mitochondrial iron trapping was abrogated by administration of the heme oxygenase inhibitors, tin mesoporphyrin (SnMP) or dexamethasone (DEX) indicating that HO-1 upregulation is necessary for subsequent mitochondrial iron deposition in these cells. Overexpression of the human HO-1 gene in cultured rat astroglia by transient transfection also stimulated mitochondrial (55)Fe deposition, an effect that was again preventible by SnMP or DEX administration. We hypothesize that free ferrous iron and carbon monoxide generated by HO-1-mediated heme degradation promote mitochondrial membrane injury and the deposition of redox-active iron within this organelle. We have shown that the percentages of GFAP-positive astrocytes that co-express HO-1 in Parkinson-affected substantia nigra and Alzheimer-diseased hippocampus are significantly increased relative to age-matched controls. Stress-induced up-regulation of HO-1 in astroglia may be responsible for the abnormal patterns of brain iron deposition and mitochondrial insufficiency documented in various human neurodegenerative disorders.
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Iron-mediated generation of ROS and injury to mitochondria are likely mechanisms of NBIA.
“Although iron-mediated generation of ROS and injury to mitochondria are likely mechanisms [196, 204]”
From “Pumping iron”—how macrophages handle iron at the systemic, microenvironmental, and cellular levels (2017) · cites this paper as [204]
Cites
Turiel, E. (2007) · doi:10.1002/9780470147658.chpsy0313 · Cited by 2,143 · see citing works
Transition metals, ferritin, glutathione, and ascorbic acid in parkinsonian brains
Riederer, P., Sofic, E., Rausch, W., Schmidt, B., Reynolds, G. P., Jellinger, K., & Youdim, M. B. H. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb09150.x · Cited by 1,383 · see citing works
Tenhunen, R., Marver, H. S., & Schmid, R. (1969) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)63477-5 · Cited by 1,357 · see citing works
Keyse, S. M., & Tyrrell, R. M. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.1.99 · Cited by 1,271 · see citing works
Regulating the fate of mRNA: the control of cellular iron metabolism
Klausner, R. D., Rouault, T. A., & Harford, J. B. (1993) · Cell · doi:10.1016/0092-8674(93)90046-s · Cited by 1,210 · see citing works
Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives
Mattson, M. P. (1997) · Physiological Reviews · doi:10.1152/physrev.1997.77.4.1081 · Cited by 1,006 · see citing works
Doré, S., Takahashi, M., Ferris, C. D., Hester, L. D., Guastella, D. B., & Snyder, S. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.2445 · Cited by 699 · see citing works
Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells.
Applegate, L. A., Lüscher, P., & Tyrrell, R. M. (1991) · PubMed · Cited by 636 · see citing works
(1994) · Toxicology and Industrial Health · doi:10.1177/074823379401000603 · Cited by 501 · see citing works
A histochemical study of iron, transferrin, and ferritin in Alzheimer's diseased brains
Connor, J. R., Menzies, S. L., Martin, S. M. S., & Mufson, E. J. (1992) · Journal of Neuroscience Research · doi:10.1002/jnr.490310111 · Cited by 468 · see citing works
Brain iron and ferritin in Parkinson’s and Alzheimer’s diseases
Jellinger, K., Paulus, W., Grundke-Iqbal, I., Riederer, P., & Youdim, M. B. H. (1990) · Journal of Neural Transmission - Parkinson's Disease and Dementia Section · doi:10.1007/bf02252926 · Cited by 445 · see citing works
Oxidative damage in neurodegenerative disease
Jenner, P. G. (1994) · The Lancet · doi:10.1016/s0140-6736(94)92347-7 · Cited by 419 · see citing works
Dyrks, T., Weidemann, A., Multhaup, G., Salbaum, J. M., Lemaire, H.-G., Kang, J., Müller‐Hill, B., Masters, C. L., & Beyreuther, K. T. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb02900.x · Cited by 394 · see citing works
Expression of heme oxygenase‐1 in the senescent and alzheimer‐diseased brain
Schipper, H. M., Cissé, S., & Stopa, E. G. (1995) · Annals of Neurology · doi:10.1002/ana.410370609 · Cited by 353 · see citing works
Self-citationRegulation of ferritin and transferrin receptor mRNAs.
Theil, E. C. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)34036-0 · Cited by 334 · see citing works
Mitochondrial oxidative stress after carbon monoxide hypoxia in the rat brain.
Zhang, J., & Piantadosi, C. A. (1992) · Journal of Clinical Investigation · doi:10.1172/jci115980 · Cited by 320 · see citing works
The possible role of iron in the etiopathology of parkinson's disease
Youdim, M. B. H., Ben‐Shachar, D., & Riederer, P. F. (1993) · Movement Disorders · doi:10.1002/mds.870080102 · Cited by 301 · see citing works
Neural Heme Oxygenase-1 Expression in Idiopathic Parkinson's Disease
Schipper, H. M., Liberman, A., & Stopa, E. G. (1998) · Experimental Neurology · doi:10.1006/exnr.1997.6752 · Cited by 300 · see citing works
Self-citationKontos, H. A., Wei, E. P., Ellis, E. F., Jenkins, L. W., Povlishock, J. T., Rowe, G. T., & Hess, M. L. (1985) · Circulation Research · doi:10.1161/01.res.57.1.142 · Cited by 291 · see citing works
Activation of heat-shock genes in eukaryotes
Pelham, H. R. B. (1985) · Trends in Genetics · doi:10.1016/0168-9525(85)90012-5 · Cited by 265 · see citing works
Ewing, J. F., & Maines, M. D. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.12.5364 · Cited by 264 · see citing works
Maines, M. D., & Kappas, A. (1974) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.71.11.4293 · Cited by 264 · see citing works
Keyse, S. M., & Tyrrell, R. M. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)47869-6 · Cited by 221 · see citing works
Ewing, J. F., Haber, S. N., & Maines, M. D. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb09373.x · Cited by 196 · see citing works
Zemlan, F. P., Thienhaus, O. J., & Bosmann, H. B. (1989) · Brain Research · doi:10.1016/0006-8993(89)91550-3 · Cited by 195 · see citing works
Astrocytes, brain aging, and neurodegeneration
Schipper, H. M. (1996) · Neurobiology of Aging · doi:10.1016/0197-4580(96)00014-0 · Cited by 138 · see citing works
Self-citationKalaria, R. N., Sromek, S. M., Grahovac, I., & Harik, S. I. (1992) · Brain Research · doi:10.1016/0006-8993(92)91193-i · Cited by 88 · see citing works
Schipper, H. M., Bernier, L., Mehindate, K., & Frankel, D. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0721802.x · Cited by 85 · see citing works
Self-citationHeme oxygenase is a heat shock protein and PEST protein in rat astroglial cells
Dwyer, B. E., Nishimura, R. N., de Vellis, J., & Yoshida, T. (1992) · Glia · doi:10.1002/glia.440050407 · Cited by 84 · see citing works
Iron histochemistry of the substantia nigra in Parkinson's disease.
Morris, C. M., & Edwardson, J. A. (1994) · PubMed · Cited by 70 · see citing works
Gelman, B. B. (1995) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-199507000-00001 · Cited by 62 · see citing works
Non-haem iron histochemistry of the normal and Alzheimer's disease hippocampus.
Morris, C. M., Kerwin, J. M., & Ja, E. (1994) · PubMed · Cited by 61 · see citing works
Schipper, H., Kotake, Y., & Janzen, E. (1991) · The Journal of Neuroscience · doi:10.1523/jneurosci.11-07-02170.1991 · Cited by 58 · see citing works
Self-citationDistribution and number of transferrin receptors in Parkinson's disease and in MPTP-treated mice
Mash, D. C., Pablo, J. P., Buck, B. E., Sanchez‐Ramos, J., & Weiner, W. J. (1991) · Experimental Neurology · doi:10.1016/0014-4886(91)90086-r · Cited by 56 · see citing works
Faucheux, B. A., Hirsch, É. C., Villares, J., Selimi, F., Prigent, A., Javoy-Agid, F., Hauw, J., & Agid, Y. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb03527.x · Cited by 54 · see citing works
Wang, X., Manganaro, F., & Schipper, H. M. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.64041868.x · Cited by 46 · see citing works
Self-citationManganaro, F., Chopra, V. S., Mydlarski, M. B., Bernatchez, G., & Schipper, H. M. (1995) · Free Radical Biology and Medicine · doi:10.1016/0891-5849(95)02008-x · Cited by 46 · see citing works
Self-citationMitochondria and Free Radicals in Neurodegenerative Diseases
Swerdlow, R. H. (1998) · The American Journal of Human Genetics · doi:10.1086/302091 · Cited by 43 · see citing works
Iron-mediated bioactivation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) in glial cultures
Di Monte, D. A., Schipper, H. M., Hetts, S., & Langston, J. W. (1995) · Glia · doi:10.1002/glia.440150213 · Cited by 43 · see citing works
Evidence for a peroxidatic oxidation of norepinephrine, a catecholamine, by lactoperoxidase
Metodiewa, D., Reszka, K. J., & Dunford, H. B. (1989) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(89)80128-7 · Cited by 42 · see citing works
Chopra, V. S., Chalifour, L. E., & Schipper, H. M. (1995) · Molecular Brain Research · doi:10.1016/0169-328x(95)00049-x · Cited by 38 · see citing works
Self-citationWhat Process Causes Nigral Cell Death in Parkinson’s Disease?
Jenner, P. G. (1992) · Neurologic Clinics · doi:10.1016/s0733-8619(18)30217-2 · Cited by 36 · see citing works
Iron‐Mediated Oxidation of 3,4‐Dihydroxyphenylalanine to an Excitotoxin
Newcomer, T. A., Rosenberg, P. A., & Aizenman, E. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.64041742.x · Cited by 26 · see citing works
Estrogen iof glial heat shock proteins: Implications for hypothalamic aging
Mydlarski, M. B., Liberman, A., & Schipper, H. M. (1995) · Neurobiology of Aging · doi:10.1016/0197-4580(95)02018-7 · Cited by 26 · see citing works
Self-citationPeterson, T. C., Peterson, M. R., & Williams, C. N. (1989) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(89)90248-2 · Cited by 14 · see citing works
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Pharmacological and Clinical Aspects of Heme Oxygenase
Abraham, N. G., & Kappas, A. (2008) · Pharmacological Reviews · doi:10.1124/pr.107.07104 · Cited by 1,115 · see citing works
The MPTP model of Parkinson's disease
Smeyne, R. J., & Jackson-Lewis, V. R. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.09.017 · Cited by 377 · see citing works
Brain iron pathways and their relevance to Parkinson's disease
Berg, D., Gerlach, M., Youdim, M. B. H., Double, K. L., Zecca, L., Riederer, P., & Becker, G. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00608.x · Cited by 362 · see citing works
Heme oxygenase-1 and neurodegeneration: expanding frontiers of engagement
Schipper, H. M., Song, W., Zukor, H., Hascalovici, J. R., & Zeligman, D. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06160.x · Cited by 298 · see citing works
Self-citationHeme oxygenase-1: role in brain aging and neurodegeneration
Schipper, H. M. (2000) · Experimental Gerontology · doi:10.1016/s0531-5565(00)00148-0 · Cited by 269 · see citing works
Self-citationKajimura, M., Fukuda, R., Bateman, R. M., Yamamoto, T., & Suematsu, M. (2009) · Antioxidants and Redox Signaling · doi:10.1089/ars.2009.2657 · Cited by 265 · see citing works
Schrag, M., Mueller, C., Oyoyo, U. E., Smith, M. A., & Kirsch, W. M. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.05.001 · Cited by 266 · see citing works
Heme Oxygenase-1: Redox Regulation of a Stress Protein in Lung and Cell Culture Models
Ryter, S. W., & Choi, A. M. K. (2004) · Antioxidants and Redox Signaling · doi:10.1089/ars.2005.7.80 · Cited by 244 · see citing works
Brain iron metabolism: Neurobiology and neurochemistry
Ke, Y., & Qian, Z. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.07.009 · Cited by 236 · see citing works
Heme oxygenase expression in human central nervous system disorders
Schipper, H. M. (2004) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2004.09.015 · Cited by 237 · see citing works
Self-citationZecca, L., Casella, L., Albertini, A., Bellei, C., Zucca, F. A., Engelen, M., Żądło, A. C., Szewczyk, G. M., Zaręba, M., & Sarna, T. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05541.x · Cited by 233 · see citing works
The sinister face of heme oxygenase-1 in brain aging and disease
Schipper, H. M., Song, W., Tavitian, A., & Cressatti, M. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.06.008 · Cited by 202 · see citing works
Self-citation“Pumping iron”—how macrophages handle iron at the systemic, microenvironmental, and cellular levels
Nairz, M., Theurl, I., Swirski, F. K., & Weiss, G. (2017) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-017-1944-8 · Cited by 178 · see citing works
Iron Metabolism in Oligodendrocytes and Astrocytes, Implications for Myelination and Remyelination
Cheli, V. T., Correale, J. D., Paez, P. M., & Pasquini, J. M. (2020) · ASN NEURO · doi:10.1177/1759091420962681 · Cited by 182 · see citing works
Brain iron deposition and the free radical-mitochondrial theory of ageing
Schipper, H. M. (2004) · Ageing Research Reviews · doi:10.1016/j.arr.2004.02.001 · Cited by 177 · see citing works
Self-citationNitti, M., Piras, S., Brondolo, L., Marinari, U. M., Pronzato, M. A., & Furfaro, A. L. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082260 · Cited by 161 · see citing works
Bansal, S., Biswas, G., & Avadhani, N. G. (2013) · Redox Biology · doi:10.1016/j.redox.2013.07.004 · Cited by 152 · see citing works
Blood and plasma-based proteomic biomarker research in Alzheimer's disease
Lista, S., Faltraco, F., Prvulovic, D., & Hampel, H. J. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.06.007 · Cited by 131 · see citing works
Mehindate, K., Sahlas, D. J., Frankel, D., Mawal, Y., Liberman, A., Corcos, J., Dion, S., & Schipper, H. M. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00354.x · Cited by 129 · see citing works
Self-citationOver‐expression of heme oxygenase‐1 promotes oxidative mitochondrial damage in rat astroglia
Song, W., Su, H., Song, S., Paudel, H. K., & Schipper, H. M. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20509 · Cited by 120 · see citing works
Self-citationHeme Oxygenase‐1: Transducer of Pathological Brain Iron Sequestration under Oxidative Stress
Schipper, H. M. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1306.007 · Cited by 117 · see citing works
Self-citationZukor, H., Song, W., Liberman, A., Mui, J., Vali, H., Fillebeen, C., Pantopoulos, K., Wu, T., Guerquin‐Kern, J., & Schipper, H. M. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06007.x · Cited by 105 · see citing works
Self-citationAberrant profiles of native and oxidized glycoproteins in Alzheimer plasma
Yu, H., Chertkow, H. M., Bergman, H., & Schipper, H. M. (2003) · PROTEOMICS · doi:10.1002/pmic.200300475 · Cited by 95 · see citing works
Self-citationGenetic contributions to Parkinson's disease
Huang, Y. M., Cheung, L., Rowe, D. B., & Halliday, G. M. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.04.007 · Cited by 91 · see citing works
Iron Exposure and the Cellular Mechanisms Linked to Neuron Degeneration in Adult Mice
Li, L.-B., Chai, R., Zhang, S., Xu, S., Zhang, Y., Li, H., Fan, Y., & Guo, C. (2019) · Cells · doi:10.3390/cells8020198 · Cited by 83 · see citing works
Hui, Y., Wang, D., Li, W., Zhang, L., Jin, J., Ma, N., Zhou, L., Nakajima, O., Zhao, W., & Gao, X. (2011) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-102061 · Cited by 71 · see citing works
Heme Regulation in Traumatic Brain Injury: Relevance to the Adult and Developing Brain
Chang, E. F., Claus, C. P., Vreman, H. J., Wong, R. J., & Noble‐Haeusslein, L. J. (2005) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600147 · Cited by 72 · see citing works
Song, W., Zukor, H., Lin, S.-H., Hascalovici, J., Liberman, A., Tavitian, A., Mui, J., Vali, H., Tong, X., Bhardwaj, S. K., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.6469-11.2012 · Cited by 69 · see citing works
Self-citationBeneficial and Detrimental Roles of Heme Oxygenase-1 in the Neurovascular System
Choi, Y. K., & Kim, Y. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137041 · Cited by 63 · see citing works
The Role of KLF4 in Alzheimer’s Disease
Cheng, Z., Zou, X., Jin, Y., Gao, S., Lv, J., Li, B., & Cui, R. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00325 · Cited by 63 · see citing works
Chung, M. J., Lee, S., Park, Y. I., Lee, J., & Kwon, K. H. (2016) · Life Sciences · doi:10.1016/j.lfs.2016.02.035 · Cited by 62 · see citing works
Biological Functions of the Elements
Lindh, U. (2012) · Springer eBooks · doi:10.1007/978-94-007-4375-5_7 · Cited by 60 · see citing works
A Heme Oxygenase-1 Transducer Model of Degenerative and Developmental Brain Disorders
Schipper, H. M., & Song, W. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms16035400 · Cited by 57 · see citing works
Self-citationHeme oxygenase-1 in Alzheimer disease: a tribute to Moussa Youdim
Schipper, H. M. (2010) · Journal of Neural Transmission · doi:10.1007/s00702-010-0436-1 · Cited by 55 · see citing works
Self-citationCharacterization of α1-antitrypsin as a heme oxygenase-1 suppressor in Alzheimer plasma
Maes, O. C., Kravitz, S., Mawal, Y. R., Su, H., Liberman, A., Mehindate, K., Berlin, D., Sahlas, D. J., Chertkow, H. M., & Bergman, H. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2006.06.009 · Cited by 54 · see citing works
Stress protein expression in the Alzheimer-diseased choroid plexus
Anthony, S. G., Schipper, H. M., Tavares, R., Hovanesian, V., Cortez, S. C., Stopa, E. G., & Johanson, C. E. (2003) · Journal of Alzheimer s Disease · doi:10.3233/jad-2003-5301 · Cited by 52 · see citing works
Self-citationSong, W., Zukor, H., Lin, S., Liberman, A., Tavitian, A., Mui, J., Vali, H., Fillebeen, C., Pantopoulos, K., Wu, T., et al. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07914.x · Cited by 52 · see citing works
Self-citationWang, D., Hui, Y., Peng, Y., Tang, L., Jin, J., He, R., Li, Y., Zhang, S., Li, L., Zhou, Y. L., et al. (2014) · Journal of Alzheimer s Disease · doi:10.3233/jad-140567 · Cited by 50 · see citing works
Lin, H.-Y., Yeh, W.-L., Huang, B.-R., Lin, C., Lai, C., Lin, H., & Lu, D.-Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050138 · Cited by 49 · see citing works
Regenerative effects of heme oxygenase metabolites on neuroinflammatory diseases
Lee, H., & Choi, Y. K. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms20010078 · Cited by 47 · see citing works
The Neuroprotective and Neurodegeneration Effects of Heme Oxygenase-1 in Alzheimer’s Disease
Si, Z., & Wang, X. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200720 · Cited by 46 · see citing works
Detrimental Roles of Hypoxia-Inducible Factor-1α in Severe Hypoxic Brain Diseases
Choi, Y. K. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084465 · Cited by 43 · see citing works
Sebghatollahi, Z., Yogesh, R., Mahato, N., Kumar, V., Mohanta, Y. K., Baek, K.-H., & Mishra, A. K. (2025) · Antioxidants · doi:10.3390/antiox14040457 · Cited by 41 · see citing works
Park, C., Cho, I., Kim, D., Jo, E., Choi, S., Oh, S. B., Park, K., Kim, J. S., & Lee, S. J. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.11.057 · Cited by 40 · see citing works
The Role of Vitamin D in Alzheimer’s Disease
Lương, K. V. Q., & Nguyễn, L. (2013) · American Journal of Alzheimer s Disease & Other Dementias® · doi:10.1177/1533317512473196 · Cited by 36 · see citing works
Role of iron in the pathogenesis of cysteamine-induced duodenal ulceration in rats
Khomenko, T., Szabó, S., Deng, X., Ishikawa, H., Anderson, G. J., & McLaren, G. D. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90257.2008 · Cited by 35 · see citing works
Ansari, N., Khodagholi, F., & Amini, M. (2011) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2011.02.028 · Cited by 35 · see citing works
Tamás, A., Lubics, A., Lengvári, I., & Reglődi, D. (2006) · Endocrine · doi:10.1385/endo:29:2:275 · Cited by 31 · see citing works
6-Hydroxydopamine promotes iron traffic in primary cultured astrocytes
Zhang, H., Wang, N., Song, N., Xu, H., Shi, L.-M., Jiang, H. F., & Xie, J. (2013) · BioMetals · doi:10.1007/s10534-013-9647-x · Cited by 29 · see citing works
Increased Plasma Heme Oxygenase-1 Levels in Patients With Early-Stage Parkinson’s Disease
Sun, W., Zheng, J., Ma, J., Wang, Z., Shi, X., Li, M., Huang, S., Hu, S., Zhao, Z., & Li, D. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.621508 · Cited by 28 · see citing works
Vakilzadeh, G., Khodagholi, F., Ghadiri, T., Darvishi, M., Ghaemi, A., Noorbakhsh, F., Gorji, A., & Sharifzadeh, M. S. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8857-8 · Cited by 29 · see citing works
RetractedRosa, P., Zerbinati, C., Crestini, A., Canudas, A.-M., Ragona, G., Confaloni, A., Iuliano, L., & Calogero, A. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00363 · Cited by 24 · see citing works
Carbon Monoxide Ameliorates 6-Hydroxydopamine-Induced Cell Death in C6 Glioma Cells
Moon, H., Jang, J., Jang, T. C., & Park, G. H. (2018) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2018.009 · Cited by 20 · see citing works
Zhao, B., Fei, J., Chen, Y., Ying, Y., Ma, L., Song, X., Wang, L., Chen, E., & Mao, E. (2014) · PLoS ONE · doi:10.1371/journal.pone.0099134 · Cited by 19 · see citing works
Ma, Z., Zhou, Y., & Xie, J. (2012) · Neurotoxicity Research · doi:10.1007/s12640-012-9309-8 · Cited by 18 · see citing works
Tavitian, A., Cressatti, M., Song, W., Turk, A. Z., Galindez, C., Smart, A., Liberman, A., & Schipper, H. M. (2019) · Antioxidants and Redox Signaling · doi:10.1089/ars.2019.7937 · Cited by 14 · see citing works
Self-citationNeuroprotective and neurorestorative strategies for neuronal injury
Beal, M. F., Palomo, T., Kostrzewa, R. M., & Archer, T. (2000) · Neurotoxicity Research · doi:10.1007/bf03033786 · Cited by 14 · see citing works
Borten, O., Liberman, A., Tuchweber, B., Chevalier, S., Ferland, G., & Schipper, H. M. (2004) · Biogerontology · doi:10.1023/b:bgen.0000025071.78517.3a · Cited by 14 · see citing works
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Jin, X., Chen, L., Yang, Y., Tan, R., & Jiang, C. (2025) · Antioxidants & Redox Signaling · doi:10.1089/ars.2024.0586 · Cited by 11 · see citing works
Papel de la hemooxigenasa-1 en las enfermedades neurodegenerativas
Orozco‐Ibarra, M., Chirino, Y. I., & Pedraza‐Chaverrí, J. (2006) · Revista de Neurología · doi:10.33588/rn.4309.2005487 · Cited by 10 · see citing works
Schipper, H. M., Small, L., Wang, X., & Brawer, J. R. (2002) · Developmental Neuroscience · doi:10.1159/000065692 · Cited by 9 · see citing works
Self-citationNeurochemical phenotype of cytoglobin-expressing neurons in the rat hippocampus
Hundahl, C. A., Fahrenkrug, J., & Hannibal, J. (2014) · Biomedical Reports · doi:10.3892/br.2014.299 · Cited by 6 · see citing works
Warenits, A.-M., Hatami, J., Müllebner, A., Ettl, F., Teubenbacher, U., Magnet, I. A. M., Bauder, B., Janata, A., Miller, I., Moldzio, R., et al. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.00513 · Cited by 6 · see citing works
Dysregulation of a Heme Oxygenase–Synuclein Axis in Parkinson Disease
Cressatti, M., & Schipper, H. M. (2022) · NeuroSci · doi:10.3390/neurosci3020020 · Cited by 6 · see citing works
Self-citationFrom Man to Mouse: The MPTP Model of Parkinson Disease
Jackson-Lewis, V. R., & Smeyne, R. J. (2005) · Elsevier eBooks · doi:10.1016/b978-012088382-0/50012-8 · Cited by 5 · see citing works
Jackson-Lewis, V., Lester, D. B., Kozina, E. A., Przedborski, S., & Smeyne, R. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-405195-9.00017-2 · Cited by 5 · see citing works
Heme Oxygenase-1 and Alzheimer Disease
Mawal, Y. R., Berlin, D., Kravitz, S., & Schipper, H. M. (2002) · Springer eBooks · doi:10.1007/978-1-4615-0741-3_12 · Cited by 4 · see citing works
Self-citationKim, C.-H., Kim, H., Nah, S., & Choi, Y. K. (2023) · Journal of Ginseng Research · doi:10.1016/j.jgr.2023.04.001 · Cited by 2 · see citing works
Glial heme oxygenase-1 in CNSinjury and disease
Schipper, H. M. (2003) · Advances in molecular and cell biology · doi:10.1016/s1569-2558(03)31038-0 · Cited by 1 · see citing works
Self-citationBrain Iron Deposition in Aging and Disease: Role of HO-1
Schipper, H. M. (2009) · Humana Press eBooks · doi:10.1007/978-1-59745-462-9_7 · Cited by 1 · see citing works
Self-citationHEME OXYGENASE-l AND ALZHEIMER DISEASE
Mawal, Y. R., Berlin, D., Kravitz, S., Schipper, H. M., Mortimer, S., & Davis, B. J. (2002) · Cited by 1 · see citing works
Self-citationThe Role of Cytochrome P450 Holoenzyme Metabolism in the Origin of Neuropathologies
Štambuk, S. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27156971
- Authors
- Schipper, H. M.
- Affiliations
- Lady Davis Institute for Medical Research (CA)
- Corresponding author
- Schipper, Hyman M.
- ORCID
- Schipper, Hyman M.
- Venue
- Neurotoxicity Research
- Published
- 1999-03
- Volume
- 1
- Issue
- 1
- Pages
- 57-70
- ISSN
- 1029-8428 (ISSN-L)
- 1476-3524
- OpenAlex
- W2005548012
- Cited by
- 72
- References
- 45
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 1 · 2016: 1 · 2015: 1 · 2014: 5 · 2013: 3 · 2012: 6
- FWCI
- 0.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neurotoxicity Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council Canada
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Life Sciences › Neuroscience › Neurology › Neurological diseases and metabolism
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Keywords
- heme oxygenase-1, brain iron accumulation, astrocytes, Parkinson's disease, Alzheimer's disease, oxidative stress, mitochondrial iron, dopamine, carbon monoxide, ferrous iron, heme oxygenase inhibitors, tin mesoporphyrin, dexamethasone, substantia nigra, hippocampus, neurodegenerative diseases
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