Evaluation of hypoxia inducible factor expression in inflammatory and neurodegenerative brain models

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 7, 2013, Pages 1377-1388

  De Lemos, Maria Luisa ^a   De La Torre, Aurelio Vazquez ^a   Petrov, Dimitry ^a   Brox, Susana ^a   Folch, Jaume ^b   Pallàs, Mercè ^a   Lazarowski, Alberto ^c   Beas Zarate, Carlos ^d   Auladell, Carme ^a   Camins, Antoni ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^c University of Buenos Aires   (Argentina)

^d INSTITUTO MEXICANO DEL SEGURO SOCIAL   (Mexico)

Author keywords

Alzheimer's; Apoptosis; APP PS1; c Jun; HIF 1

Indexed keywords

ENZYME INHIBITOR; HYPOXIA INDUCIBLE FACTOR; INTERLEUKIN 1BETA; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN C JUN; PROTEIN KINASE B; SP 600126; UNCLASSIFIED DRUG; GAMMA INTERFERON; HIF1A PROTEIN, MOUSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENCEPHALITIS; GLIA CELL; IN VITRO STUDY; MOUSE; NERVE DEGENERATION; NONHUMAN; PROTEIN EXPRESSION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRAIN; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; GENETICS; GLIA; INFLAMMATION; METABOLISM; PATHOLOGY; RAT; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; BRAIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-1BETA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; NEUROGLIA; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84877094845     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.04.011     Document Type: Article

References (64)

1. H. Akiyama, S. Barger, S. Barnum, B. Bradt, J. Bauer, and G.M. Cole Inflammation and Alzheimer's disease Neurobiology of Aging 21 2000 383 421 (Pubitemid 30349107)
2. J.E. Albina, B. Mastrofrancesco, J.A. Vessella, C.A. Louis, W.L. Henry Jr., and J.S. Reichner HIF-1 expression in healing wounds: HIF-1alpha induction in primary inflammatory cells by TNF-alpha American Journal of Physiology. Cell Physiology 281 2001 C1971 C1977
3. L.R. Aminova, A. Siddiq, and R.R. Ratan Antioxidants, HIF prolyl hydroxylase inhibitors or short interfering RNAs to BNIP3 or PUMA, can prevent prodeath effects of the transcriptional activator, HIF-1alpha, in a mouse hippocampal neuronal line Antioxidants and Redox Signalling 10 2008 1989 1998
4. J.H. Bae, B.C. Jang, S.I. Suh, E. Ha, H.H. Baik, and S.S. Kim Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3K/Akt pathways in BV2 microglial cells Neuroscience Letters 398 2006 151 154
5. S. Barouk, T. Hintz, P. Li, A.M. Duffy, N.J. MacLusky, and H.E. Scharfman 17β-estradiol increases astrocytic vascular endothelial growth factor (VEGF) in adult female rat hippocampus Endocrinology 152 2011 1745 1751
6. A.M. Bodles, and S.W. Barger Secreted beta-amyloid precursor protein activates microglia via JNK and p38-MAPK Neurobiology of Aging 26 2005 9 16 (Pubitemid 39600586)
7. S. Brault, F. Gobeil Jr., A. Fortier, J.C. Honoré, J.S. Joyal, and P.S. Sapieha Lysophosphatidic acid induces endothelial cell death by modulating the redox environment American Journal of Physiology Regulatory Integrative and Comparative Physiology 292 2007 R1174 R1183
8. C. Brigati, B. Banelli, A. di Vinci, I. Casciano, G. Allemanni, and A. Forlani Inflammation, HIF-1, and the epigenetics that follows Mediators of Inflammation 2010 2010 263914
9. L. Caltana, A. Merelli, A. Lazarowski, and A. Brusco Neuronal and glial alterations due to focal cortical hypoxia induced by direct cobalt chloride (CoCl2) brain injection Neurotoxicity Research 15 2009 348 358
10. H. Chen, T. Xiong, Y. Qu, F. Zhao, D. Ferriero, and D. Mu mTOR activates hypoxia-inducible factor-1α and inhibits neuronal apoptosis in the developing ratbrain during the early phase after hypoxia-ischemia Neuroscience Letters 507 2012 118 123
11. J.R. Cirrito, R. Deane, A.M. Fagan, M.L. Spinner, M. Parsadanian, and M.B. Finn P-glycoprotein deficiency at the blood-brain barrier increases amyloid-beta deposition in an Alzheimer disease mouse model Journal of Clinical Investigation 115 2005 3285 3290 (Pubitemid 41567593)
12. S.C. Correia, and P.I. Moreira Hypoxia-inducible factor 1: a new hope to counteract neurodegeneration? Journal of Neurochemistry 112 2010 1 12
13. M. Demaria, S. Misale, C. Giorgi, V. Miano, A. Camporeale, and J. Campisi STAT3 can serve as a hit in the process of malignant transformation of primary cells Cell Death and Differentiation 19 2012 1390 1397
14. F. Du, X.M. Wu, Q. Gong, X. He, and Y. Ke Hyperthermia conditioned astrocyte-cultured medium protects neurons from ischemic injury by the up-regulation of HIF-1 alpha and the increased anti-apoptotic ability European Journal of Pharmacology 666 2011 19 25
15. F. Du, L. Zhu, Z.M. Qian, X.M. Wu, W.H. Yung, and Y. Ke Hyperthermic preconditioning protects astrocytes from ischemia/reperfusion injury by up-regulation of HIF-1 alpha expression and binding activity Biochimica et Biophysica Acta 1802 2010 1048 1053
16. D. Games, D. Adams, R. Alessandrini, R. Barbour, P. Berthelette, and C. Blackwell Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein Nature 373 1995 523 527
17. S.K. Harten, M. Ashcroft, and P.H. Maxwell Prolyl hydroxylase domain inhibitors: a route to HIF activation and neuroprotection Antioxidants & Redox Signaling 12 2010 459 480
18. R. Helton, J. Cui, J.R. Scheel, J.A. Ellison, C. Ames, and C. Gibson Brain-specific knock-out of hypoxia-inducible factor-1alpha reduces rather than increases hypoxic-ischemic damage Journal of Neuroscience 25 2005 4099 4107 (Pubitemid 40563385)
19. K. Hsiao, P. Chapman, S. Nilsen, C. Eckman, Y. Harigaya, and S. Younkin Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice Science 274 1996 99 102 (Pubitemid 26332733)
20. M.A. Hossain, C.M. Bouton, J. Pevsner, and J. Laterra Induction of vascular endothelial growth factor in human astrocytes by lead. Involvement of a protein kinase C/activator protein-1 complex-dependent and hypoxia-inducible factor 1-independent signaling pathway Journal of Biological Chemistry 275 2000 27874 27882
21. H.Z. Imtiyaz, and M.C. Simon Hypoxia-inducible factors as essential regulators of inflammation Current Topics in Microbiology and Immunology 345 2010 105 120
22. J.K. Jeong, J.S. Seo, M.H. Moon, Y.J. Lee, J.W. Seol, and S.Y. Park Hypoxia-inducible factor-1 alpha regulates prion protein expression to protect against neuron cell damage Neurobiology of Aging 33 2012 1006 e1-10
23. Q. Ji, L. Yang, J. Zhou, R. Lin, J. Zhang, and Q. Lin Protective effects of paeoniflorin against cobalt chloride-induced apoptosis of endothelial cells via HIF-1α pathway Toxicology in Vitro 26 2012 455 461
24. H. Jiang, Y. Huang, H. Xu, Y. Sun, N. Han, and Q.F. Li Hypoxia inducible factor-1α is involved in the neurodegeneration induced by isoflurane in the brainof neonatal rats Journal of Neurochemistry 120 2012 453 460
25. T. Kawasaki, T. Kitao, K. Nakagawa, H. Fujisaki, Y. Takegawa, and K. Koda Nitric oxide-induced apoptosis in cultured rat astrocytes: protection by edaravone, a radical scavenger Glia 55 2007 1325 1333 (Pubitemid 47328936)
26. S.C. Keswani, M. Bosch-Marcé, N. Reed, A. Fischer, G.L. Semenza, and A. Höke Nitric oxide prevents axonal degeneration by inducing HIF-1-dependent expression of erythropoietin Proceedings of the National Academy of Sciences of the United States of America A108 2011 4986-4690
27. H. Kimura, and H. Esumi Reciprocal regulation between nitric oxide and vascular endothelial growth factor in angiogenesis Acta Biochimica Polonica 50 1 2003 49 59 (Pubitemid 37034227)
28. H.P. Kuo, D.F. Lee, W. Xia, Y. Wei, and M.C. Hung TNFalpha induces HIF-1alpha expression through activation of IKKbeta Biochemical and Biophysical Research Communications 389 2009 640 644
29. L. Kupershmidt, O. Weinreb, T. Amit, S. Mandel, O. Bar-Am, and M.B. Youdim Novel molecular targets of the neuroprotective/neurorescue multimodal iron chelating drug M30 in the mouse brain Neuroscience 189 2011 345 358
30. B. López-Hernández, I. Posadas, P. Podlesniy, M.A. Abad, R. Trullas, and V. Ceña HIF-1α is neuroprotective during the early phases of mild hypoxia in rat cortical neurons Experimental Neurology 233 2012 543 554
31. A. Merelli, L. Caltana, P. Girimonti, A.J. Ramos, A. Lazarowski, and A. Brusco Recovery of motor spontaneous activity after intranasal delivery of human recombinant erythropoietin in a focal brain hypoxia model induced by CoCl2 in rats Neurotoxicity Research 20 2011 182 192
32. L. Nardinocchi, R. Puca, A. Sacchi, and G. D'Orazi Inhibition of HIF-1alpha activity by homeodomain-interacting protein kinase-2 correlates with sensitization of chemoresistant cells to undergo apoptosis Molecular Cancer 8 January 2009 1
33. K. Naruishi, F. Nishimura, H. Yamada-Naruishi, K. Omori, M. Yamaguchi, and S. Takashiba C-jun N-terminal kinase (JNK) inhibitor, SP600125, blocks interleukin (IL)-6-induced vascular endothelial growth factor (VEGF) production: cyclosporine A partially mimics this inhibitory effect Transplantation 76 2003 1380 1382 (Pubitemid 37430727)
34. O.O. Ogunshola, and X. Antoniou Contribution of hypoxia to Alzheimer's disease: is HIF-1alpha a mediator of neurodegeneration? Cellular and Molecular Life Sciences 66 2009 3555 3563
35. S. Pawate, and N.R. Bhat C-Jun N-terminal kinase (JNK) regulation of iNOS expression in glial cells: predominant role of JNK1 isoform Antioxidants and Redox Signalling 8 2006 903 909 (Pubitemid 44036507)
36. A. Pocivavsek, M.P. Burns, and G.W. Rebeck Low-density lipoprotein receptors regulate microglial inflammation through c-Jun N-terminal kinase Glia 57 2009 444 453
37. F.L. Powell, B.C. Kim, S.R. Johnson, and Z. Fu Oxygen sensing in the brain - invited article Advances in Experimental Medicine and Biology 648 2009 369 376
38. L. Ruan, Z. Kang, G. Pei, and Y. Le Amyloid deposition and inflammation in APPswe/PS1dE9 mouse model of Alzheimer's disease Current Alzheimer Research 6 2009 531 540
39. K.B. Sandau, J. Zhou, T. Kietzmann, and B. Brüne Regulation of the hypoxia-inducible factor 1alpha by the inflammatory mediators nitric oxide and tumor necrosis factor-alpha in contrast to desferroxamine and phenylarsine oxide Journal of Biological Chemistry 276 2001 39805 39811
40. J.E. Shay, and M. Celeste Simon Hypoxia-inducible factors: crosstalk between inflammation and metabolism Seminars in Cell and Developmental Biology 23 2012 389 394
41. A. Sendoel, I. Kohler, C. Fellmann, S.W. Lowe, and M.O. Hengartner HIF-1 antagonizes p53-mediated apoptosis through a secreted neuronal tyrosinase Nature 465 2010 577 583
42. H. Shi Hypoxia inducible factor 1 as a therapeutic target in ischemic stroke Current Medicinal Chemistry 16 2009 4593 4600
43. A.P. Sinke, A.R. Jayakumar, K.S. Panickar, M. Moriyama, P.V. Reddy, and M.D. Norenberg NFkappaB in the mechanism of ammonia-induced astrocyte swelling in culture Journal of Neurochemistry 106 2008 2302 2311
44. Z.C. Song, W. Zhou, R. Shu, and J. Ni Hypoxia induces apoptosis and autophagic cell death in human periodontal ligament cells through HIF-1α pathway Cell Proliferation 45 2012 239 248
45. C. Sturchler-Pierrat, D. Abramowski, M. Duke, K.H. Wiederhold, C. Mistl, and S. Rothacher Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology Proceedings of the National Academy of Sciences of the United States of America 94 1997 13287 13292 (Pubitemid 27518514)
46. 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-1alpha in neurons and astrocytes Journal of Neuroscience 28 2008 1988 1993 (Pubitemid 351302661)
47. A.V. de la Torre, F. Junyent, J. Folch, C. Pelegrí, J. Vilaplana, and C. Auladell GSK3β inhibition is involved in the neuroprotective effects of cyclin-dependent kinase inhibitors in neurons Pharmacological Research 65 2012 66 73
48. H. Wang, C. Cheng, Y. Qin, S. Niu, S. Gao, and X. Li Role of mitogen-activated protein kinase cascades in inducible nitric oxide synthase expression by lipopolysaccharide in a rat Schwann cell line Neurochemical Research 34 2009 430 437
49. A. Weidemann, T.U. Krohne, E. Aguilar, T. Kurihara, N. Takeda, and M.I. Dorrell Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina Glia 58 2010 1177 1185
50. O. Weinreb, T. Amit, S. Mandel, and M.B. Youdim Novel therapeutic approach for neurodegenerative pathologies: multitarget iron-chelating drugs regulating hypoxia-inducible factor 1 signal transduction pathway Neurodegenerative Diseases 10 2009 112 115
51. R. Wuestefeld, J. Chen, K. Meller, B. Brand-Saberi, and C. Theiss Impact of vegf on astrocytes: analysis of gap junctional intercellular communication, proliferation, and motility Glia 60 2012 936 947
52. A. Xanthi, S. Alessandra, P. Cristina, C. Alessio, M. Gautier, and B. Tiziana JNK contributes to Hif-1 regulation in hypoxic neurons Molecules 30 2009 114 127
53. L. Xie, R.S. Johnson, and R.S. Freeman Inhibition of NGF deprivation-induced death by low oxygen involves suppression of BIMEL and activation of HIF-1 Journal of Cell Biology 168 2005 911 920 (Pubitemid 40397005)
54. Z.H. Yang, K. Sun, Z.H. Yan, W.H. Suo, G.H. Fu, and Y. Lu Panaxynol protects cortical neurons from ischemia-like injury by up-regulation of HIF-1alpha expression and inhibition of apoptotic cascade Chemico-Biological Interactions 183 2010 165 171
55. K. Yoo, J.W. Choi, M.S. Choi, M.K. Ryu, G.H. Park, and M.J. Jeon Mitogen-activated protein kinases (MAPKs) mediate SIN-1/glucose deprivation-induced death in rat primary astrocytes Archives of Pharmacal Research 28 2005 942 947
56. Y. Yoshioka, N. Takeda, A. Yamamuro, A. Kasai, and S. Maeda Nitric oxide inhibits lipopolysaccharide-induced inducible nitric oxide synthase expression and its own production through the cGMP signaling pathway in murine microglia BV-2 cells Journal of Pharmacological Sciences 113 2010 153 160
57. B. Yu, Z.H. Miao, Y. Jiang, M.H. Li, N. Yang, and T. Li c-Jun protects hypoxia-inducible factor-1alpha from degradation via its oxygen-dependent degradation domain in a nontranscriptional manner Cancer Research 69 2009 7704 7712
58. C.H. Yu, C.T. Moon, J.H. Sur, Y.I. Chun, W.H. Choi, and J.Y. Yhee Serial expression of hypoxia inducible factor-1α and neuronal apoptosis in hippocampus of rats with chronic ischemic brain Journal of Korean Neurosurgical Society 50 2011 481 485
59. P. Zhang, B.S. Miller, S.A. Rosenzweig, and N.R. Bhat Activation of C-jun N-terminal kinase/stress-activated protein kinase in primary glial cultures Journal of Neuroscience Research 46 1996 114 121 (Pubitemid 26330585)
60. Q. Zhang, Z. Qian, L. Pan, H. Li, and H. Zhu Hypoxia-inducible factor 1 mediates the anti-apoptosis of berberine in neurons during hypoxia/ischemia Acta Physiologica Hungarica 99 2012 311 323
61. Y. Zhang, C. Li, X. Sun, X. Kuang, and X. Ruan High glucose decreases expression and activity of p-glycoprotein in cultured human retinal pigment epithelium possibly through iNOS induction PLoS ONE 7 2 2012 e31631
62. Z. Zhang, J. Yan, Y. Chang, S. ShiDu Yan, and H. Shi Hypoxia inducible factor-1 as a target for neurodegenerative diseases Current Medicinal Chemistry 18 2011 4335 4343
63. D. Zhang, J. Li, M. Zhang, G. Gao, Z. Zuo, and Y. Yu The requirement of c-Jun N-terminal kinase 2 in regulation of hypoxia-inducing factor-1α mRNA stability Journal of Biological Chemistry 287 2012 34361 34371
64. Z. Zhu, S. Zhong, and Z. Shen Targeting the inflammatory pathways to enhance chemotherapy of cancer Cancer Biology and Therapy 12 2011 95 105