Hypoxia inducible factor-1α mediates iron uptake which induces inflammatory response in amoeboid microglial cells in developing periventricular white matter through MAP kinase pathway

Neuropharmacology

Volumn 77, Issue , 2014, Pages 428-440

  Rathnasamy, Gurugirijha ^a   Ling, Eng Ang ^a   Kaur, Charanjit ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cytokines; Deferoxamine; HIF 1 ; Hypoxia; Iron; KC7F2; MAPKs; Microglia

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ANTIINFLAMMATORY AGENT; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DEFEROXAMINE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1BETA; IRON; KC 7F2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 2; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INFLAMMATION; IRON TRANSPORT; MICROGLIA; NEWBORN; NONHUMAN; PERIVENTRICULAR WHITE MATTER; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WHITE MATTER;

CYTOKINES; DEFEROXAMINE; HIF-1Α; HYPOXIA; IRON; KC7F2; MAPKS; MICROGLIA;

ANIMALS; ANOXIA; CATION TRANSPORT PROTEINS; DEFEROXAMINE; DISULFIDES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERLEUKIN-1BETA; IRON; MAP KINASE SIGNALING SYSTEM; MICROGLIA; NERVE FIBERS, MYELINATED; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, TRANSFERRIN; SULFONAMIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84887935684     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.10.024     Document Type: Article

References (75)

1. L.M. Adcock, Y. Yamashita, J. GoddardFinegold, and C.V. Smith Cerebral hypoxia-ischemia increases microsomal iron in newborn piglets Metab. Brain Dis. 11 1996 359 367 (Pubitemid 27004860)
2. A. Alvarez-Diaz, E. Hilario, F.G. de Cerio, A. Valls-i-Soler, and F.J. Alvarez-Diaz Hypoxic-ischemic injury in the immature brain-key vascular and cellular players Neonatology 92 2007 227 235 (Pubitemid 350125279)
3. O. Baud, J.L. Daire, Y. Dalmaz, R.H. Fontaine, R.C. Krueger, G. Sebag, P. Evrard, P. Gressens, and C. Verney Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia Brain Pathol. 14 2004 1 10 (Pubitemid 38200584)
4. J. Beard Iron deficiency alters brain development and functioning J. Nutr. 133 2003 1468S 1472S (Pubitemid 36548728)
5. L. Bianchi, L. Tacchini, and G. Cairo HIF-1-mediated activation of transferrin receptor gene transcription by iron chelation Nucleic Acids Res. 27 1999 4223 4227 (Pubitemid 29500256)
6. T.G. Boulton, S.H. Nye, D.J. Robbins, N.Y. Ip, E. Radziejewska, S.D. Morgenbesser, R.A. DePinho, N. Panayotatos, M.H. Cobb, and G.D. Yancopoulos ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF Cell 65 1991 663 675
7. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
8. C. Casals-Casas, E. Alvarez, M. Serra, C. de la Torre, C. Farrera, E. Sanchez-Tillo, C. Caelles, J. Lloberas, and A. Celada CREB and AP-1 activation regulates MKP-1 induction by LPS or M-CSF and their kinetics correlate with macrophage activation versus proliferation Eur. J. Immunol. 39 2009 1902 1913
9. L. Chang, and M. Karin Mammalian MAP kinase signalling cascades Nature 410 2001 37 40 (Pubitemid 32225829)
10. Y.C. Chang, and C.C. Huang Perinatal brain injury and regulation of transcription Curr. Opin. Neurol. 19 2006 141 147
11. C. Chen, Q. Hu, J. Yan, X. Yang, X. Shi, J. Lei, L. Chen, H. Huang, J. Han, J.H. Zhang, and C. Zhou Early inhibition of HIF-1alpha with small interfering RNA reduces ischemic-reperfused brain injury in rats Neurobiol. Dis. 33 2009 509 517
12. P. Chen, J. Li, J. Barnes, G.C. Kokkonen, J.C. Lee, and Y. Liu Restraint of proinflammatory cytokine biosynthesis by mitogen-activated protein kinase phosphatase-1 in lipopolysaccharide-stimulated macrophages J. Immunol. 169 2002 6408 6416 (Pubitemid 36903490)
13. Y.S. Choi, H.Y. Cho, K.R. Hoyt, J.R. Naegele, and K. Obrietan IGF-1 receptor-mediated ERK/MAPK signaling couples status epilepticus to progenitor cell proliferation in the subgranular layer of the dentate gyrus Glia 56 2008 791 800
14. C. Colton, S. Wilt, D. Gilbert, O. Chernyshev, J. Snell, and M. Dubois-Dalcq Species differences in the generation of reactive oxygen species by microglia Mol. Chem. Neuropathol. 28 1996 15 20 (Pubitemid 26275046)
15. Y. Deng, J. Lu, V. Sivakumar, E.A. Ling, and C. Kaur Amoeboid microglia in the periventricular white matter induce oligodendrocyte damage through expression of proinflammatory cytokines via MAP kinase signaling pathway in hypoxic neonatal rats Brain Pathol. 18 2008 387 400 (Pubitemid 351782848)
16. X. Fan, C.J. Heijnen, M.A. van der Kooij, F. Groenendaal, and F. van Bel The role and regulation of hypoxia-inducible factor-1alpha expression in brain development and neonatal hypoxic-ischemic brain injury Brain Res. Rev. 62 2009 99 108
17. P.L. Follett, W. Deng, W. Dai, D.M. Talos, L.J. Massillon, P.A. Rosenberg, J.J. Volpe, and F.E. Jensen Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate J. Neurosci. 24 2004 4412 4420 (Pubitemid 38608152)
18. D. Giulian, and T.J. Baker Characterization of ameboid microglia isolated from developing mammalian brain J. Neurosci. 6 1986 2163 2178 (Pubitemid 16043659)
19. B.Y. Huang, and M. Castillo Hypoxic-ischemic brain injury: imaging findings from birth to adulthood Radiographics 28 2008 417 439 quiz 617
20. L.E. Huang, Z. Arany, D.M. Livingston, and H.F. Bunn Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit J. Biol. Chem. 271 1996 32253 32259 (Pubitemid 26422262)
21. X. Huang, J. Dai, C. Huang, Q. Zhang, O. Bhanot, and E. Pelle Deferoxamine synergistically enhances iron-mediated AP-1 activation: a showcase of the interplay between extracellular-signal-regulated kinase and tyrosine phosphatase Free Radic. Res. 41 2007 1135 1142 (Pubitemid 47470851)
22. Y. Huo, P. Rangarajan, E.A. Ling, and S.T. Dheen Dexamethasone inhibits the Nox-dependent ROS production via suppression of MKP-1-dependent MAPK pathways in activated microglia BMC Neurosci. 12 2011 49
23. 2 homeostasis by hypoxia-inducible factor 1 alpha Genes Dev. 12 1998 149 162 (Pubitemid 28060446)
24. M.V. Johnston Hypoxic and ischemic disorders of infants and children. Lecture for 38th Meeting of Japanese Society of Child Neurology, Tokyo, Japan, July 1996 Brain Dev. 19 1997 235 239 (Pubitemid 27236846)
25. P.J. Kallio, I. Pongratz, K. Gradin, J. McGuire, and L. Poellinger Activation of hypoxia-inducible factor 1alpha: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor Proc. Natl. Acad. Sci. U. S. A. 94 1997 5667 5672 (Pubitemid 27241827)
26. C. Kaur, and E.A. Ling Increased expression of transferrin receptors and iron in amoeboid microglial cells in postnatal rats following an exposure to hypoxia Neurosci. Lett. 262 1999 183 186 (Pubitemid 29136800)
27. C. Kaur, V. Sivakumar, L.S. Ang, and A. Sundaresan Hypoxic damage to the periventricular white matter in neonatal brain: role of vascular endothelial growth factor, nitric oxide and excitotoxicity J. Neurochem. 98 2006 1200 1216 (Pubitemid 44127795)
28. Q. Ke, and M. Costa Hypoxia-inducible factor-1 (HIF-1) Mol. Pharmacol. 70 2006 1469 1480
29. Y.S. Kim, S.S. Kim, J.J. Cho, D.H. Choi, O. Hwang, D.H. Shin, H.S. Chun, M.F. Beal, and T.H. Joh Matrix metalloproteinase-3: a novel signaling proteinase from apoptotic neuronal cells that activates microglia J. Neurosci. 25 2005 3701 3711
30. M. Koistinaho, and J. Koistinaho Role of p38 and p44/42 mitogen-activated protein kinases in microglia Glia 40 2002 175 183 (Pubitemid 35337375)
31. M. Lasa, S.M. Abraham, C. Boucheron, J. Saklatvala, and A.R. Clark Dexamethasone causes sustained expression of mitogen-activated protein kinase (MAPK) phosphatase 1 and phosphatase-mediated inhibition of MAPK p38 Mol. Cell Biol. 22 2002 7802 7811 (Pubitemid 35217291)
32. Y.B. Lee, J.W. Schrader, and S.U. Kim p38 map kinase regulates TNF-alpha production in human astrocytes and microglia by multiple mechanisms Cytokine 12 2000 874 880 (Pubitemid 30479468)
33. Z. Li, Z. Lai, K. Ya, D. Fang, Y.W. Ho, Y. Lei, and Q.Z. Ming Correlation between the expression of divalent metal transporter 1 and the content of hypoxia-inducible factor-1 in hypoxic HepG2 cells J. Cell Mol. Med. 12 2008 569 579 (Pubitemid 351555136)
34. J.R. Lokensgard, S. Hu, W. Sheng, M. vanOijen, D. Cox, M.C. Cheeran, and P.K. Peterson Robust expression of TNF-alpha, IL-1beta, RANTES, and IP-10 by human microglial cells during nonproductive infection with herpes simplex virus J. Neurovirol. 7 2001 208 219 (Pubitemid 32685255)
35. B. Lozoff, and M.K. Georgieff Iron deficiency and brain development Semin. Pediatr. Neurol. 13 2006 158 165 (Pubitemid 44712046)
36. D.Y. Lu, Y.Y. Tsao, Y.M. Leung, and K.P. Su Docosahexaenoic acid suppresses neuroinflammatory responses and induces heme oxygenase-1 expression in BV-2 microglia: implications of antidepressant effects for omega-3 fatty acids Neuropsychopharmacology 35 2010 2238 2248
37. T.C. Lu, Z. Wang, X. Feng, P. Chuang, W. Fang, Y. Chen, S. Neves, A. Maayan, H. Xiong, Y. Liu, R. Iyengar, P.E. Klotman, and J.C. He Retinoic acid utilizes CREB and USF1 in a transcriptional feed-forward loop in order to stimulate MKP1 expression in human immunodeficiency virus-infected podocytes Mol. Cell Biol. 28 2008 5785 5794
38. Y.S. Maeng, J.K. Min, J.H. Kim, A. Yamagishi, N. Mochizuki, J.Y. Kwon, Y.W. Park, Y.M. Kim, and Y.G. Kwon ERK is an anti-inflammatory signal that suppresses expression of NF-kappaB-dependent inflammatory genes by inhibiting IKK activity in endothelial cells Cell Signal. 18 2006 994 1005
39. L. Mardini, J. Gasiorek, A. Derjuga, L. Carriere, M. Schranzhofer, B.H. Paw, P. Ponka, and V. Blank Antagonistic roles of the ERK and p38 MAPK signalling pathways in globin expression, haem biosynthesis and iron uptake Biochem. J. 432 2010 145 151
40. D.S. Markovic, K. Vinnakota, S. Chirasani, M. Synowitz, H. Raguet, K. Stock, M. Sliwa, S. Lehmann, R. Kalin, N. van Rooijen, K. Holmbeck, F.L. Heppner, J. Kiwit, V. Matyash, S. Lehnardt, B. Kaminska, R. Glass, and H. Kettenmann Gliomas induce and exploit microglial MT1-MMP expression for tumor expansion Proc. Natl. Acad. Sci. U. S. A. 106 2009 12530 12535
41. C.J. Marshall Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation Cell 80 1995 179 185
42. X.Y. Miao, X.B. Liu, Q. Yue, N. Qiu, W.D. Huang, J.J. Wang, Y.G. Xu, Y.L. Zhang, J. Yang, and X.L. Chen Deferoxamine suppresses microglia activation and protects against secondary neural injury after intracerebral hemorrhage in rats Nan Fang Yi Ke Da Xue Xue Bao (J. South. Med. Univ.) 32 2012 970 975
43. M. Murugan, V. Sivakumar, J. Lu, E.A. Ling, and C. Kaur Expression of N-methyl D-aspartate receptor subunits in amoeboid microglia mediates production of nitric oxide via NF-kappaB signaling pathway and oligodendrocyte cell death in hypoxic postnatal rats Glia 59 2011 521 539
44. T. Narita, S. Yin, C.F. Gelin, C.S. Moreno, M. Yepes, K.C. Nicolaou, and E.G. Van Meir Identification of a novel small molecule HIF-1alpha translation inhibitor Clin. Cancer Res. 15 2009 6128 6136
45. C. Ndong, R.P. Landry, J.A. DeLeo, and E.A. Romero-Sandoval Mitogen activated protein kinase phosphatase-1 prevents the development of tactile sensitivity in a rodent model of neuropathic pain Mol. Pain 8 2012 34
46. J.K. Ness, M.J. Romanko, R.P. Rothstein, T.L. Wood, and S.W. Levison Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors Dev. Neurosci. 23 2001 203 208 (Pubitemid 34701673)
47. C. Palmer, S.L. Menzies, R.L. Roberts, G. Pavlick, and J.R. Connor Changes in iron histochemistry after hypoxic-ischemic brain injury in the neonatal rat J. Neurosci. Res. 56 1999 60 71 (Pubitemid 29190617)
48. C. Peeters-Scholte, K. Braun, J. Koster, N. Kops, K. Blomgren, G. Buonocore, S. van Buul-Offers, H. Hagberg, K. Nicolay, F. van Bel, and F. Groenendaal Effects of allopurinol and deferoxamine on reperfusion injury of the brain in newborn piglets after neonatal hypoxia-ischemia Pediatr. Res. 54 2003 516 522 (Pubitemid 37159122)
49. Z.M. Qian, X.M. Wu, M. Fan, L. Yang, F. Du, W.H. Yung, and Y. Ke Divalent metal transporter 1 is a hypoxia-inducible gene J. Cell Physiol. 226 2011 1596 1603
50. W.S. Qu, D.S. Tian, Z.B. Guo, J. Fang, Q. Zhang, Z.Y. Yu, M.J. Xie, H.Q. Zhang, J.G. Lu, and W. Wang Inhibition of EGFR/MAPK signaling reduces microglial inflammatory response and the associated secondary damage in rats after spinal cord injury J. Neuroinflam. 9 2012 178
51. G. Rathnasamy, E.A. Ling, and C. Kaur Iron and iron regulatory proteins in amoeboid microglial cells are linked to oligodendrocyte death in hypoxic neonatal rat periventricular white matter through production of proinflammatory cytokines and reactive oxygen/nitrogen species J. Neurosci. 31 2011 17982 17995
52. P. Rezaie, and A. Dean Periventricular leukomalacia, inflammation and white matter lesions within the developing nervous system Neuropathology 22 2002 106 132 (Pubitemid 35252702)
53. J. Saura, J.M. Tusell, and J. Serratosa High-yield isolation of murine microglia by mild trypsinization Glia 44 2003 183 189 (Pubitemid 37484470)
54. R.J. Scott, and L. Hegyi Cell death in perinatal hypoxic-ischaemic brain injury Neuropathol. Appl. Neurobiol. 23 1997 307 314 (Pubitemid 27352841)
55. R.A. Segal, and M.E. Greenberg Intracellular signaling pathways activated by neurotrophic factors Annu. Rev. Neurosci. 19 1996 463 489 (Pubitemid 26080836)
56. M. Selim Deferoxamine mesylate: a new hope for intracerebral hemorrhage: from bench to clinical trials Stroke 40 2009 S90 S91
57. G.L. Semenza Hypoxia-inducible factor 1: master regulator of O2 homeostasis Curr. Opin. Genet. Dev. 8 1998 588 594 (Pubitemid 28477364)
58. V. Sgambato, C. Pages, M. Rogard, M.J. Besson, and J. Caboche Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation J. Neurosci. 18 1998 8814 8825 (Pubitemid 28491747)
59. R.A. Sheldon, J. Chuai, and D.M. Ferriero A rat model for hypoxic-ischemic brain damage in very premature infants Biol. Neonate 69 1996 327 341 (Pubitemid 26170648)
60. R.A. Sheldon, D. Osredkar, C.L. Lee, X. Jiang, D. Mu, and D.M. Ferriero HIF-1 alpha-deficient mice have increased brain injury after neonatal hypoxia-ischemia Dev. Neurosci. 31 2009 452 458
61. R.P. Skoff, D.A. Bessert, J.D. Barks, D. Song, M. Cerghet, and F.S. Silverstein Hypoxic-ischemic injury results in acute disruption of myelin gene expression and death of oligodendroglial precursors in neonatal mice Int. J. Dev. Neurosci. 19 2001 197 208 (Pubitemid 32194655)
62. F.A. Sorond, M.L. Shaffer, A.L. Kung, and L.A. Lipsitz Desferroxamine infusion increases cerebral blood flow: a potential association with hypoxia-inducible factor-1 Clin. Sci. 116 2009 771 779
63. L. Tacchini, L. Bianchi, A. Bernelli-Zazzera, and G. Cairo Transferrin receptor induction by hypoxia. HIF-1-mediated transcriptional activation and cell-specific post-transcriptional regulation J. Biol. Chem. 274 1999 24142 24146
64. S. Takashima, K. Iida, and K. Deguchi Periventricular leukomalacia, glial development and myelination Early Hum. Dev. 43 1995 177 184 (Pubitemid 26010442)
65. G. Vangeison, D. Carr, H.J. Federoff, and D.A. Rempe The good, the bad, and the cell type-specific roles of hypoxia inducible factor-1 alpha in neurons and astrocytes J. Neurosci. 28 2008 1988 1993 (Pubitemid 351302661)
66. J.J. Volpe Cerebral white matter injury of the premature infant - more common than you think Pediatrics 112 2003 176 180 (Pubitemid 36792944)
67. G.L. Wang, B.H. Jiang, and G.L. Semenza Effect of altered redox states on expression and DNA-binding activity of hypoxia-inducible factor 1 Biochem. Biophys. Res. Commun. 212 1995 550 556
68. M.S. Woo, P.G. Jang, J.S. Park, W.K. Kim, T.H. Joh, and H.S. Kim Selective modulation of lipopolysaccharide-stimulated cytokine expression and mitogen-activated protein kinase pathways by dibutyryl-cAMP in BV2 microglial cells Brain Research. Mol. Brain Res. 113 2003 86 96 (Pubitemid 36579070)
69. H. Wu, T. Wu, X. Xu, and J. Wang Iron toxicity in mice with collagenase-induced intracerebral hemorrhage J. Cereb. Blood Flow Metab. 31 2011 1243 1250
70. L. Yao, E.M. Kan, J. Lu, A. Hao, S.T. Dheen, C. Kaur, and E.A. Ling Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia J. Neuroinflam. 10 2013 23
71. J. Zhang, T.N. Bui, J. Xiang, and A. Lin Cyclic AMP inhibits p38 activation via CREB-induced dynein light chain Mol. Cell Biol. 26 2006 1223 1234 (Pubitemid 43202551)
72. X. Zhang, M. Haaf, B. Todorich, E. Grosstephan, H. Schieremberg, N. Surguladze, and J.R. Connor Cytokine toxicity to oligodendrocyte precursors is mediated by iron Glia 52 2005 199 208 (Pubitemid 43078509)
73. X. Zhang, N. Surguladze, B. Slagle-Webb, A. Cozzi, and J.R. Connor Cellular iron status influences the functional relationship between microglia and oligodendrocytes Glia 54 2006 795 804 (Pubitemid 44671985)
74. J.Y. Zhou, Y. Liu, and G.S. Wu The role of mitogen-activated protein kinase phosphatase-1 in oxidative damage-induced cell death Cancer Res. 66 2006 4888 4894
75. Y. Zhou, E.A. Ling, and S.T. Dheen Dexamethasone suppresses monocyte chemoattractant protein-1 production via mitogen activated protein kinase phosphatase-1 dependent inhibition of Jun N-terminal kinase and p38 mitogen-activated protein kinase in activated rat microglia J. Neurochem. 102 2007 667 678 (Pubitemid 47057277)