Astrocyte NMDA receptors' activity sustains neuronal survival through a Cdk5-Nrf2 pathway

Cell Death and Differentiation

Volumn 22, Issue 11, 2015, Pages 1877-1889

  Jimenez Blasco, D ^a,b   Santofimia Castano P ^c   Gonzalez, A ^c   Almeida, A ^a,b   Bolanos J P ^a,b  

^a UNIVERSITY OF SALAMANCA   (Spain)

^b HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^c UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLIN DEPENDENT KINASE 5; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PHOSPHOLIPASE C; PROTEIN KINASE C DELTA; PROTEIN P35; TRANSCRIPTION FACTOR NRF2; HYDROGEN PEROXIDE; LIPID; LIPOFECTAMINE;

ANIMAL CELL; ARTICLE; ASTROCYTE; CALCIUM TRANSPORT; CELL COMMUNICATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; EXTRACELLULAR CALCIUM; FETUS; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL CULTURE; DRUG EFFECTS; FLOW CYTOMETRY; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOPRECIPITATION; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 5; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; HYDROGEN PEROXIDE; IMMUNOPRECIPITATION; LIPIDS; MEMBRANE POTENTIAL, MITOCHONDRIAL; NEURONS; NF-E2-RELATED FACTOR 2; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SIGNAL TRANSDUCTION;

EID: 84943197836     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2015.49     Document Type: Article

References (55)

1. Bossy-Wetzel E, Schwarzenbacher R, Lipton SA. Molecular pathways to neurodegeneration. Nat Med 2004; 10: S2-S9.
2. Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 2010; 11: 682-696.
3. Vaughn AE, Deshmukh M. Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat Cell Biol 2008; 10: 1477-1483.
4. Herrero-Mendez A, Almeida A, Fernandez E, Maestre C, Moncada S, Bolanos JP. The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol 2009; 11: 747-752.
5. Papadia S, Soriano FX, Leveille F, Martel MA, Dakin KA, Hansen HH et al. Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat Neurosci 2008; 11: 476-487.
6. Maestre C, Delgado-Esteban M, Gomez-Sanchez JC, Bolanos JP, Almeida A. Cdk5 phosphorylates Cdh1 and modulates cyclin B1 stability in excitotoxicity. Embo J 2008; 27: 2736-2745.
7. Rodriguez-Rodriguez P, Fernandez E, Almeida A, Bolanos JP. Excitotoxic stimulus stabilizes PFKFB3 causing pentose-phosphate pathway to glycolysis switch and neurodegeneration. Cell Death Differ 2012; 19: 1582-1589.
8. Rothstein JD, Dykes-Hoberg M, Pardo CA, Bristol LA, Jin L, Kunci RW et al. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 1996; 16: 675-686.
9. Pellerin L, Magistretti PJ. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc Natl Acad Sci USA 1994; 91: 10625-10629.
10. Bouzier-Sore AK, Voisin P, Canioni P, Magistretti PJ, Pellerin L. Lactate is a preferential oxidative energy substrate over glucose for neurons in culture. J Cereb Blood Flow Metab 2003; 23: 1298-1306.
11. Allaman I, Belanger M, Magistretti PJ. Astrocyte-neuron metabolic relationships: for better and for worse. Trends Neurosci 2011; 34: 76-87.
12. Dringen R, Pfeiffer B, Hamprecht B. Synthesis of the antioxidant glutathione in neurons: supply by astrocytes of CysGly as precursor for neuronal glutathione. J Neurosci 1999; 19: 562-569.
13. Hayes JD, McMahon M. NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci 2009; 34: 176-188.
14. Habas A, Hahn J, Wang X, Margeta M. Neuronal activity regulates astrocytic Nrf2 signaling. Proc Natl Acad Sci USA 2013; 110: 18291-18296.
15. Deighton RF, Markus NM, Al-Mubarak B, Bell KF, Papadia S, Meakin PJ et al. Nrf2 target genes can be controlled by neuronal activity in the absence of Nrf2 and astrocytes. Proc Natl Acad Sci USA 2014; 111: E1818-E1820.
16. Habas A, Hahn J, Wang X, Margeta M. Reply to Deighton et al.: neuronal activity regulates distinct antioxidant pathways in neurons and astrocytes. Proc Natl Acad Sci USA 2014; 111: E1821-E1822.
17. Haskew-Layton RE, Payappilly JB, Smirnova NA, Ma TC, Chan KK, Murphy TH et al. Controlled enzymatic production of astrocytic hydrogen peroxide protects neurons from oxidative stress via an Nrf2-independent pathway. Proc Natl Acad Sci USA 2010; 107: 17385-17390.
18. Bell KF, Al-Mubarak B, Fowler JH, Baxter PS, Gupta K, Tsujita T et al. Mild oxidative stress activates Nrf2 in astrocytes, which contributes to neuroprotective ischemic preconditioning. Proc Natl Acad Sci USA 2011; 108: E1-E2 author reply E3-4.
19. Verkhratsky A, Kirchhoff F. NMDA Receptors in glia. Neuroscientist 2007; 13: 28-37.
20. Zhou C, Wee S, Rhee E, Naumann M, Dubiel W, Wiolf DA. Fission yeast COP9/signalosome suppresses cullin activity through recruitment of the deubiquitylating enzyme Ubp12p. Mol Cell 2003; 11: 927-938.
21. Lo SC, Hannink M. CAND1-mediated substrate adaptor recycling is required for efficient repression of Nrf2 by Keap1. Mol Cell Biol 2006; 26: 1235-1244.
22. Seifert G, Steinhaüser C. Ionotropic glutamate receptors in astrocytes. Prog Brain Res 2001; 132: 287-299.
23. Conti F, DeBiasi S, Minelli A, Melone M. Expression of NR1 and NR2A/B subunits of the NMDA receptor in cortical astrocytes. Glia 1996; 17: 254-258.
24. Schipke C, Ohlemeyer C, Matyash M, Nolte C, Kettenmann H, Kirchhoff F. Astrocytes of the mouse neocortex express functional N-methyl-D-aspartate receptors. Faseb J 2001; 15: 1270-1272.
25. Lee M, Ting K, Adams S, Brew B, Chung R, Guillemin G. Characterisation of the expression of NMDA receptors in human astrocytes. PLos One 2010; 5: e14123.
26. Wroge CM, Hogins J, Eisenman L, Mennerick S. Synaptic NMDA receptors mediate hypoxic excitotoxic death. J Neurosci 2012; 32: 6732-6742.
27. Palygin O, Lalo U, Pankratov Y. Distinct pharmacological and functional properties of NMDA receptors in mouse cortical astrocytes. Br J Pharmacol 2011; 163: 1755-1766.
28. Kusakawa G, Saito T, Onuki R, Ishiguro K, Kishimoto T, Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J Biol Chem 2000; 275: 17166-17172.
29. Hisanaga S, Endo R. Regulation and role of cyclin-dependent kinase activity in neuronal survival and death. J Neurochem 2010; 115: 1309-1321.
30. Zhao CT, Li K, Li JT, Zheng W, Liang XJ, Geng AQ et al. PKCdelta regulates cortical radial migration by stabilizing the Cdk5 activator p35. Proc Natl Acad Sci USA 2009; 106: 21353-21358.
31. Agarwal ML, Larkin HE, Zaidi SI, Mukhtar H, Oleinick NL. Phospholipase activation triggers apoptosis in photosensitized mouse lymphoma cells. Cancer Res 1993; 53: 5897-5902.
32. Susarla BT, Robinson MB. Rottlerin, an inhibitor of protein kinase Cdelta (PKCdelta), inhibits astrocytic glutamate transport activity and reduces GLAST immunoreactivity by a mechanism that appears to be PKCdelta-independent. J Neurochem 2003; 86: 635-645.
33. Dringen R, Kranich O, Hamprecht B. The g-glutamyltranspeptidase inhibitor acivicin preserves glutathione released by astroglial cells in culture. Neurochem Res 1997; 22: 727-733.
34. Fernandez-Fernandez S, Almeida A, Bolanos JP. Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem J 2012; 443: 3-11.
35. Kikkawa U, Matsuzaki H, Yamamoto T. Protein kinase C delta (PKC delta): activation mechanisms and functions. J Biochem 2002; 132: 831-839.
36. Young KW, Garro MA, Challiss RA, Nahorski SR. NMDA-receptor regulation of muscarinicreceptor stimulated inositol 1,4,5-trisphosphate production and protein kinase C activation in single cerebellar granule neurons. J Neurochem 2004; 89: 1537-1546.
37. Bloom DA, Jaiswal AK. Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response elementmediated NAD(P)H:quinone oxidoreductase-1 gene expression. J Biol Chem 2003; 278: 44675-44682.
38. Araque A, Carmignoto G, Haydon PG, Oliet SH, Robitaille R, Volterra A. Gliotransmitters travel in time and space. Neuron 2014; 81: 728-739.
39. Pellerin L, Pellegri G, Bittar PG, Charnay Y, Bouras C, Martin JL et al. Evidence supporting the existence of an activity-dependent astrocyte-neuron lactate shuttle. Dev Neurosci 1998; 20: 291-299.
40. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R et al. Activitydependent regulation of energy metabolism by astrocytes: an update. Glia 2007; 55: 1251-1262.
41. Yang J, Ruchti E, Petit JM, Jourdain P, Grenningloh G, Allaman I et al. Lactate promotes plasticity gene expression by potentiating NMDA signaling in neurons. Proc Natl Acad Sci USA 2014; 111: 12228-12233.
42. DeNicola GM, Karreth FA, Humpton TJ, Gopinathan A, Wei C, Frese K et al. Oncogeneinduced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature 2011; 475: 106-109.
43. Jaramillo MC, Zhang DD. The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev 2013; 27: 2179-2191.
44. Liang Q, Li L, Zhang J, Lei Y, Wang L, Liu DX et al. CDK5 is essential for TGF-beta1-induced epithelial-mesenchymal transition and breast cancer progression. Sci Rep 2013; 3: 2932.
45. Almeida A, Moncada S, Bolanõs JP. Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway. Nat Cell Biol 2004; 6: 45-51.
46. Zheng YL, Li BS, Kanungo J, Kesavapany S, Amin N, Grant P et al. Cdk5 Modulation of mitogen-activated protein kinase signaling regulates neuronal survival. Mol Biol Cell 2007; 18: 404-413.
47. Ohtsuka T, Ryu H, Minamishima YA, Macip S, Sagara J, Nakayama KI et al. ASC is a Bax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway. Nat Cell Biol 2004; 6: 121-128.
48. Almeida A, Bolanõs JP. A transient inhibition of mitochondrial ATP synthesis by nitric oxide synthase activation triggered apoptosis in primary cortical neurons. J Neurochem 2001; 77: 676-690.
49. Dos-Anjos S, Martínez-Villayandre B, Montori S, Regueiro-Purrinõs M, Gonzalo-Orden J, Fernández-López A. Transient global ischemia in rat brain promotes different NMDA receptor regulation depending on the brain structure studied. Neurochem Int 2009; 54: 180-185.
50. Salazar M, Pariente JA, Salido GM, Gonzalez A. Ebselen increases cytosolic free Ca2+ concentration, stimulates glutamate release and increases GFAP content in rat hippocampal astrocytes. Toxicology 2008; 244: 280-291.
51. Grynkiewicz G, Poenie M, Tsien RY. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 1985; 260: 3440-3450.
52. Tietze F. Enzyme method for quantitative determination of nanogram amounts of total and oxidized glutathione: application to mammalian blood and other tissues. Anal Biochem 1969; 27: 502-522.
53. Foo LC. Purification of rat and mouse astrocytes by immunopanning. Cold Spring Harb Protoc 2013; 2013: 421-432.
54. Wang J, Liu S, Fu Y,Wang JH, Lu Y. Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat Neurosci 2003; 6: 1039-1047.
55. Lowry OH, Rosebrough NJ, Lewis-Farr A, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275.