Fractalkine activates NRF2/NFE2L2 and heme oxygenase 1 to restrain tauopathy-induced microgliosis

Brain

Volumn 137, Issue 1, 2014, Pages 78-91

  Lastres Becker, Isabel ^a   Innamorato, Nadia G ^a   Jaworski, Tomasz ^b,e   Rábano, Alberto ^c   Kügler, Sebastian ^d   Van Leuven, Fred ^b   Cuadrado, Antonio ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^e NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

adeno associated virus; Alzheimer's disease; neuroimmunology; oxidative stress

Indexed keywords

FRACTALKINE; GLYCOGEN SYNTHASE KINASE 3BETA; HEME OXYGENASE 1; PARVOVIRUS VECTOR; TAU PROTEIN; TRANSCRIPTION FACTOR NRF2;

AGED; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTOSIS; CONTROLLED STUDY; ENZYME ACTIVATION; GENE TARGETING; GLIOSIS; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROGLIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TAUOPATHY; UPREGULATION; VERY ELDERLY;

ADENO-ASSOCIATED VIRUS; ALZHEIMER'S DISEASE; NEUROIMMUNOLOGY; OXIDATIVE STRESS;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANIMALS; BLOTTING, WESTERN; BRAIN; CELL NUCLEUS; CHEMOKINE CX3CL1; CYTOSOL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLIOSIS; HEME OXYGENASE-1; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; LENTIVIRUS; MALE; MICE; NF-E2-RELATED FACTOR 2; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TAUOPATHIES;

EID: 84892773204     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt323     Document Type: Article

References (63)

1. Aw Yeang HX, Hamdam JM, Al-Huseini LM, Sethu S, Djouhri L, Walsh J, et al. Loss of transcription factor nuclear factor-erythroid 2 (NF-E2) p45-related factor-2 (Nrf2) leads to dysregulation of immune functions, redox homeostasis, and intracellular signaling in dendritic cells. J Biol Chem 2012; 287: 10556-64.
2. Bell RD, Winkler EA, Singh I, Sagare AP, Deane R, Wu Z, et al. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature 2012; 485: 512-6.
3. Bhaskar K, Konerth M, Kokiko-Cochran ON, Cardona A, Ransohoff RM, Lamb BT. Regulation of tau pathology by the microglial fractalkine receptor. Neuron 2010; 68: 19-31.
4. Boche D, Perry VH, Nicoll JA. Review: activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol 2013; 39: 3-18.
5. Bouchard M, Suchowersky O. Tauopathies: one disease or many? Can J Neurol Sci 2011; 38: 547-56.
6. Brigelius-Flohe R, Flohe L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 2011; 15: 2335-81.
7. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ. Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci 2000; 20: RC87.
8. Chora AA, Fontoura P, Cunha A, Pais TF, Cardoso S, Ho PP, et al. Heme oxygenase-1 and carbon monoxide suppress autoimmune neuroinflammation. J Clin Invest 2007; 117: 438-47.
9. Clark AK, Yip PK, Malcangio M. The liberation of fractalkine in the dorsal horn requires microglial cathepsin S. J Neurosci 2009; 29: 6945-54.
10. Cuadrado A, Rojo AI. Heme oxygenase-1 as a therapeutic target in neurodegenerative diseases and brain infections. Curr Pharm Des 2008; 14: 429-42.
11. Dash PK, Zhao J, Orsi SA, Zhang M, Moore AN. Sulforaphane improves cognitive function administered following traumatic brain injury. Neurosci Lett 2009; 460: 103-7.
12. Desforges NM, Hebron ML, Algarzae NK, Lonskaya I, Moussa CE. Fractalkine mediates communication between pathogenic proteins and microglia: implications of anti-inflammatory treatments in different stages of neurodegenerative diseases. Int J Alzheimers Dis 2012; 2012: 345472.
13. Forman MS, Lal D, Zhang B, Dabir DV, Swanson E, Lee VM, et al. Transgenic mouse model of tau pathology in astrocytes leading to nervous system degeneration. J Neurosci 2005; 25: 3539-50.
14. Fuhrmann M, Bittner T, Jung CK, Burgold S, Page RM, Mitteregger G, et al. Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer's disease. Nat Neurosci 2010; 13: 411-3.
15. Galimberti D, Scarpini E. Inflammation and oxidative damage in Alzheimer's disease: friend or foe? Front Biosci 2011; 3: 252-66.
16. Gozzelino R, Jeney V, Soares MP. Mechanisms of cell protection by heme oxygenase-1. Annu Rev Pharmacol Toxicol 2010; 50: 323-54.
17. Harrison JK, Jiang Y, Chen S, Xia Y, Maciejewski D, McNamara RK, et al. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc Natl Acad Sci USA 1998; 95: 10896-901.
18. Hatori K, Nagai A, Heisel R, Ryu JK, Kim SU. Fractalkine and fractalkine receptors in human neurons and glial cells. J Neurosci Res 2002; 69: 418-26.
19. Hochreiter-Hufford A, Ravichandran KS. Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol 2013; 5: a008748.
20. Hurst LA, Bunning RA, Sharrack B, Woodroofe MN. siRNA knockdown of ADAM-10, but not ADAM-17, significantly reduces fractalkine shedding following pro-inflammatory cytokine treatment in a human adult brain endothelial cell line. Neurosci Lett 2012; 521: 52-6.
21. Imai T, Hieshima K, Haskell C, Baba M, Nagira M, Nishimura M, et al. Identification and molecular characterization of fractalkine receptor CX3CR1, which mediates both leukocyte migration and adhesion. Cell 1997; 91: 521-30.
22. Imaizumi T, Yoshida H, Satoh K. Regulation of CX3CL1/fractalkine expression in endothelial cells. J Atheroscler Thromb 2004; 11: 15-21.
23. Innamorato NG, Lastres-Becker I, Cuadrado A. Role of microglial redox balance in modulation of neuroinflammation. Curr Opin Neurol 2009; 22: 308-14.
24. Innamorato NG, Rojo AI, Garcia-Yague AJ, Yamamoto M, de Ceballos ML, Cuadrado A. The transcription factor Nrf2 is a therapeutic target against brain inflammation. J Immunol 2008; 181: 680-9.
25. Itoh K, Chiba T, Takahashi S, Ishii T, Igarashi K, Katoh Y, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun 1997; 236: 313-22.
26. Jaworski T, Dewachter I, Lechat B, Croes S, Termont A, Demedts D, et al. AAV-tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice. PLoS One 2009; 4: e7280.
27. Jaworski T, Lechat B, Demedts D, Gielis L, Devijver H, Borghgraef P, et al. Dendritic degeneration, neurovascular defects, and inflammation precede neuronal loss in a mouse model for tau-mediated neurodegeneration. Am J Pathol 2011; 179: 2001-15.
28. Jazwa A, Cuadrado A. Targeting heme oxygenase-1 for neuroprotection and neuroinflammation in neurodegenerative diseases. Curr Drug Targets 2010; 11: 1517-31.
29. Jazwa A, Rojo AI, Innamorato NG, Hesse M, Fernandez-Ruiz J, Cuadrado A. Pharmacological targeting of the transcription factor Nrf2 at the basal ganglia provides disease modifying therapy for experimental parkinsonism. Antioxid Redox Signal 2011; 14: 2347-60.
30. Jimenez S, Torres M, Vizuete M, Sanchez-Varo R, Sanchez-Mejias E, Trujillo-Estrada L, et al. Age-dependent accumulation of soluble amyloid beta (Abeta) oligomers reverses the neuroprotective effect of soluble amyloid precursor protein-alpha (sAPP(alpha)) by modulating phosphatidylinositol 3-kinase (PI3K)/Akt-GSK-3beta pathway in Alzheimer mouse model. J Biol Chem 2011; 286: 18414-25.
31. Joshi G, Johnson JA. The Nrf2-ARE pathway: a valuable therapeutic target for the treatment of neurodegenerative diseases. Recent Pat CNS Drug Discov 2012; 7: 218-29.
32. Jung S, Aliberti J, Graemmel P, Sunshine MJ, Kreutzberg GW, Sher A, et al. Analysis of fractalkine receptor CX(3)CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Mol Cell Biol 2000; 20: 4106-14.
33. Kanninen K, Heikkinen R, Malm T, Rolova T, Kuhmonen S, Leinonen H, et al. Intrahippocampal injection of a lentiviral vector expressing Nrf2 improves spatial learning in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2009; 106: 16505-10.
34. Kanninen K, Malm TM, Jyrkkanen HK, Goldsteins G, Keksa-Goldsteine V, Tanila H, et al. Nuclear factor erythroid 2-related factor 2 protects against beta amyloid. Mol Cell Neurosci 2008; 39: 302-13.
35. Khandelwal PJ, Dumanis SB, Herman AM, Rebeck GW, Moussa CE. Wild type and P301L mutant Tau promote neuro-inflammation and alpha-Synuclein accumulation in lentiviral gene delivery models. Mol Cell Neurosci 2012; 49: 44-53.
36. Kim TS, Lim HK, Lee JY, Kim DJ, Park S, Lee C, et al. Changes in the levels of plasma soluble fractalkine in patients with mild cognitive impairment and Alzheimer's disease. Neurosci Lett 2008; 436: 196-200.
37. Koudinov A, Kezlya E, Koudinova N, Berezov T. Amyloid-beta, tau protein, and oxidative changes as a physiological compensatory mechanism to maintain CNS plasticity under Alzheimer's disease and other neurodegenerative conditions. J Alzheimers Dis 2009; 18: 381-400.
38. Lastres-Becker I, Ulusoy A, Innamorato NG, Sahin G, Rabano A, Kirik D, et al. Alpha-Synuclein expression and Nrf2 deficiency cooperate to aggravate protein aggregation, neuronal death and inflammation in early-stage Parkinson's disease. Hum Mol Genet 2012; 21: 3173-92.
39. Lee DC, Rizer J, Hunt JB, Selenica ML, Gordon MN, Morgan D. Review: experimental manipulations of microglia in mouse models of Alzheimer's pathology: activation reduces amyloid but hastens tau pathology. Neuropathol Appl Neurobiol 2013; 39: 69-85.
40. Lee S, Varvel NH, Konerth ME, Xu G, Cardona AE, Ransohoff RM, et al. CX3CR1 deficiency alters microglial activation and reduces beta-amyloid deposition in two Alzheimer's disease mouse models. Am J Pathol 2010; 177: 2549-62.
41. Morganti JM, Nash KR, Grimmig BA, Ranjit S, Small B, Bickford PC, et al. The soluble isoform of CX3CL1 is necessary for neuroprotection in a mouse model of Parkinson's disease. J Neurosci 2012; 32: 14592-601.
42. Nash KR, Lee DC, Hunt JB Jr, Morganti JM, Selenica ML, Moran P, et al. Fractalkine overexpression suppresses tau pathology in a mouse model of tauopathy. Neurobiol Aging 2013; 34: 1540-8.
43. Noda M, Doi Y, Liang J, Kawanokuchi J, Sonobe Y, Takeuchi H, et al. Fractalkine attenuates excito-neurotoxicity via microglial clearance of damaged neurons and antioxidant enzyme heme oxygenase-1 expression. J Biol Chem 2011; 286: 2308-19.
44. Rada P, Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A. SCF/{beta}-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 2011; 31: 1121-33.
45. Rada P, Rojo AI, Evrard-Todeschi N, Innamorato NG, Cotte A, Jaworski T, et al. Structural and functional characterization of Nrf2 degradation by the glycogen synthase kinase 3/beta-TrCP axis. Mol Cell Biol 2012; 32: 3486-99.
46. Rangasamy T, Cho CY, Thimmulappa RK, Zhen L, Srisuma SS, Kensler TW, et al. Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice. J Clin Invest 2004; 114: 1248-59.
47. Rangasamy T, Guo J, Mitzner WA, Roman J, Singh A, Fryer AD, et al. Disruption of Nrf2 enhances susceptibility to severe airway inflammation and asthma in mice. J Exp Med 2005; 202: 47-59.
48. Ransohoff RM, Liu L, Cardona AE. Chemokines and chemokine receptors: multipurpose players in neuroinflammation. Int Rev Neurobiol 2007; 82: 187-204.
49. Rezai-Zadeh K, Gate D, Gowing G, Town T. How to get from here to there: macrophage recruitment in Alzheimer's disease. Curr Alzheimer Res 2011; 8: 156-63.
50. Rojo AI, Innamorato NG, Martin-Moreno AM, De Ceballos ML, Yamamoto M, Cuadrado A. Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 2010; 58: 588-98.
51. Rojo AI, Salinas M, Martin D, Perona R, Cuadrado A. Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-kappaB. J Neurosci 2004; 24: 7324-34.
52. Sengillo JD, Winkler EA, Walker CT, Sullivan JS, Johnson M, Zlokovic BV. Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer's disease. Brain Pathol 2013; 23: 303-10.
53. Shenvi SV, Smith E, Hagen TM. Identification of age-specific Nrf2 binding to a novel antioxidant response element locus in the Gclc promoter: a compensatory means for the loss of glutathione synthetic capacity in the aging rat liver? Aging Cell 2012; 11: 297-304.
54. Shi M, Bradner J, Hancock AM, Chung KA, Quinn JF, Peskind ER, et al. Cerebrospinal fluid biomarkers for Parkinson disease diagnosis and progression. Ann Neurol 2011; 69: 570-80.
55. Suh JH, Shenvi SV, Dixon BM, Liu H, Jaiswal AK, Liu RM, et al. Decline in transcriptional activity of Nrf2 causes age-related loss of glutathione synthesis, which is reversible with lipoic acid. Proc Natl Acad Sci USA 2004; 101: 3381-6.
56. Thimmulappa RK, Lee H, Rangasamy T, Reddy SP, Yamamoto M, Kensler TW, et al. Nrf2 is a critical regulator of the innate immune response and survival during experimental sepsis. J Clin Invest 2006; 116: 984-95.
57. Tomobe K, Shinozuka T, Kuroiwa M, Nomura Y. Age-related changes of Nrf2 and phosphorylated GSK-3beta in a mouse model of accelerated aging (SAMP8). Arch Gerontol Geriatr 2012; 54: e1-7.
58. Tong KI, Kobayashi A, Katsuoka F, Yamamoto M. Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol Chem 2006; 387: 1311-20.
59. Villeneuve NF, Lau A, Zhang DD. Regulation of the Nrf2-Keap1 antioxidant response by the ubiquitin proteasome system: an insight into cullin-ring ubiquitin ligases. Antioxid Redox Signal 2010; 13: 1699-712.
60. Wakabayashi N, Slocum SL, Skoko JJ, Shin S, Kensler TW. When NRF2 talks, who's listening? Antioxid Redox Signal 2010; 13: 1649-63.
61. Yoshida H, Imaizumi T, Fujimoto K, Matsuo N, Kimura K, Cui X, et al. Synergistic stimulation, by tumor necrosis factor-alpha and interferongamma, of fractalkine expression in human astrocytes. Neurosci Lett 2001; 303: 132-6.
62. Zhao J, Moore AN, Redell JB, Dash PK. Enhancing expression of Nrf2-driven genes protects the blood brain barrier after brain injury. J Neurosci 2007; 27: 10240-8.
63. Zlokovic BV. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat Rev Neurosci 2011; 12: 723-38.