AMP-activated protein kinase (AMPK)-induced preconditioning in primary cortical neurons involves activation of MCL-1

Journal of Neurochemistry

Volumn 124, Issue 5, 2013, Pages 721-734

  Anilkumar, Ujval ^a   Weisová, Petronela ^a,b   Düssmann, Heiko ^a   Concannon, Caoimhín G ^a   König, Hans Georg ^a   Prehn, Jochen H M ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b UNIVERSITY OF VIENNA   (Austria)

Author keywords

BCL 2 family; bioenergetics; Ca2+ homeostasis; excitotoxicity; glutamate; mitochondria

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; CALCIUM; GLUCOSE TRANSPORTER 3; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; PROTEIN BCL 2; PROTEIN MCL 1;

ANIMAL CELL; ARTICLE; BIOENERGY; BRAIN CELL; BRAIN ISCHEMIA; CALCIUM CELL LEVEL; CELL PROTECTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; GENE OVEREXPRESSION; GENE SILENCING; ISCHEMIC PRECONDITIONING; MOLECULAR MECHANICS; MOUSE; NERVE CELL EXCITABILITY; NEUROPROTECTION; NONHUMAN; OXIDATIVE PHOSPHORYLATION UNCOUPLING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY;

ADAPTATION, PHYSIOLOGICAL; AMINOIMIDAZOLE CARBOXAMIDE; ANIMALS; BLOTTING, WESTERN; CEREBRAL CORTEX; FLOW CYTOMETRY; HYPOGLYCEMIC AGENTS; MICE; MICROSCOPY, CONFOCAL; N-METHYLASPARTATE; NEURONS; PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; RIBONUCLEOTIDES; STRESS, PHYSIOLOGICAL;

EID: 84874117510     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12108     Document Type: Article

References (63)

1. Akgul C., Moulding D. A., White M. R., and, Edwards S. W., (2000) In vivo localisation and stability of human Mcl-1 using green fluorescent protein (GFP) fusion proteins. FEBS Lett. 478, 72-76. (Pubitemid 30462261)
2. Ankarcrona M., Dypbukt J. M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S. A., and, Nicotera P., (1995) Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
3. Arbour N., Vanderluit J. L., le Grand J. N., et al,. (2008) Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J. Neurosci. 28, 6068-6078.
4. Bergeron R., Ren J. M., Cadman K. S., Moore I. K., Perret P., Pypaert M., Young L. H., Semenkovich C. F., and, Shulman G. I., (2001) Chronic activation of AMP kinase results in NRF-1 activation and mitochondrial biogenesis. Am. J. Physiol. Endocrinol. Metab. 281, E1340-E1346.
5. Bickler P. E., Fahlman C. S., and, Gray J. J., (2010) Hypoxic preconditioning failure in aging hippocampal neurons: impaired gene expression and rescue with intracellular calcium chelation. J. Neurosci. Res. 88, 3520-3529.
6. Budd S. L., and, Nicholls D. G., (1998) Mitochondria in the life and death of neurons. Essays Biochem. 33, 43-52. (Pubitemid 128471909)
7. Castilho R. F., Hansson O., Ward M. W., Budd S. L., and, Nicholls D. G., (1998) Mitochondrial control of acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 18, 10277-10286. (Pubitemid 29016547)
8. Chen J., Graham S. H., Zhu R. L., and, Simon R. P., (1996) Stress proteins and tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metab. 16, 566-577. (Pubitemid 26227065)
9. Cheng E. H., Wei M. C., Weiler S., Flavell R. A., Mak T. W., Lindsten T., and, Korsmeyer S. J., (2001) BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell 8, 705-711. (Pubitemid 32946946)
10. Choi D. W., (1987) Ionic dependence of glutamate neurotoxicity. J. Neurosci. 7, 369-379. (Pubitemid 17017466)
11. Choi D. W., and, Rothman S. M., (1990) The role of glutamate neurotoxicity in hypoxic-ischemic neuronal death. Annu. Rev. Neurosci. 13, 171-182. (Pubitemid 20100647)
12. Concannon C. G., Tuffy L. P., Weisova P., Bonner H. P., Davila D., Bonner C., Devocelle M. C., Strasser A., Ward M. W., and, Prehn J. H., (2010) AMP kinase-mediated activation of the BH3-only protein Bim couples energy depletion to stress-induced apoptosis. J. Cell Biol. 189, 83-94.
13. Culmsee C., Monnig J., Kemp B. E., and, Mattson M. P., (2001) AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation. J. Mol. Neurosci. 17, 45-58. (Pubitemid 32928285)
14. Dasgupta B., and, Milbrandt J., (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc. Natl Acad. Sci. USA 104, 7217-7222. (Pubitemid 47186035)
15. Davila D., Connolly N. M., Bonner H., Weisova P., Dussmann H., Concannon C. G., Huber H. J., and, Prehn J. H., (2012) Two-step activation of FOXO3 by AMPK generates a coherent feed-forward loop determining excitotoxic cell fate. Cell Death Differ. 19, 1677-1688.
16. Delgado-Esteban M., Almeida A., and, Bolanos J. P., (2000) D-Glucose prevents glutathione oxidation and mitochondrial damage after glutamate receptor stimulation in rat cortical primary neurons. J. Neurochem. 75, 1618-1624.
17. Dietz G. P., Dietz B., and, Bahr M., (2007) Bcl-xL protects cerebellar granule neurons against the late phase, but not against the early phase of glutamate-induced cell death. Brain Res. 1164, 136-141. (Pubitemid 47198227)
18. D'Orsi B., Bonner H., Tuffy L. P., Dussmann H., Woods I., Courtney M. J., Ward M. W., and, Prehn J. H., (2012) Calpains are downstream effectors of bax-dependent excitotoxic apoptosis. J. Neurosci. 32, 1847-1858.
19. Garnier P., Ying W., and, Swanson R. A., (2003) Ischemic preconditioning by caspase cleavage of poly(ADP-ribose) polymerase-1. J. Neurosci. 23, 7967-7973. (Pubitemid 37082448)
20. Germain M., Nguyen A. P., le Grand J. N., Arbour N., Vanderluit J. L., Park D. S., Opferman J. T., and, Slack R. S., (2011) MCL-1 is a stress sensor that regulates autophagy in a developmentally regulated manner. EMBO J. 30, 395-407.
21. Gidday J. M., Shah A. R., Maceren R. G., Wang Q., Pelligrino D. A., Holtzman D. M., and, Park T. S., (1999) Nitric oxide mediates cerebral ischemic tolerance in a neonatal rat model of hypoxic preconditioning. J. Cereb. Blood Flow Metab. 19, 331-340. (Pubitemid 30026923)
22. Goetze B., Grunewald B., Baldassa S., and, Kiebler M., (2004) Chemically controlled formation of a DNA/calcium phosphate coprecipitate: application for transfection of mature hippocampal neurons. J. Neurobiol. 60, 517-525. (Pubitemid 39108891)
23. Grabb M. C., and, Choi D. W., (1999) Ischemic tolerance in murine cortical cell culture: critical role for NMDA receptors. J. Neurosci. 19, 1657-1662. (Pubitemid 29094184)
24. Hawley S. A., Davison M., Woods A., Davies S. P., Beri R. K., Carling D., and, Hardie D. G., (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271, 27879-27887. (Pubitemid 26367365)
25. Kefas B. A., Cai Y., Ling Z., Heimberg H., Hue L., Pipeleers D., and, van de Casteele M., (2003) AMP-activated protein kinase can induce apoptosis of insulin-producing MIN6 cells through stimulation of c-Jun-N-terminal kinase. J. Mol. Endocrinol. 30, 151-161. (Pubitemid 36592509)
26. Kiedrowski L., and, Costa E., (1995) Glutamate-induced destabilization of intracellular calcium concentration homeostasis in cultured cerebellar granule cells: role of mitochondria in calcium buffering. Mol. Pharmacol. 47, 140-147.
27. Kilbride S. M., and, Prehn J. H., (2012) Central roles of apoptotic proteins in mitochondrial function. Oncogene doi: 10.1038/onc.2012.348.
28. Kimura N., Tokunaga C., Dalal S., Richardson C., Yoshino K., Hara K., Kemp B. E., Witters L. A., Mimura O., and, Yonezawa K., (2003) A possible linkage between AMP-activated protein kinase (AMPK) and mammalian target of rapamycin (mTOR) signalling pathway. Genes Cells 8, 65-79. (Pubitemid 36511694)
29. Kitagawa K., Matsumoto M., Tagaya M., et al,. (1990) 'Ischemic tolerance' phenomenon found in the brain. Brain Res. 528, 21-24. (Pubitemid 20292932)
30. Lankiewicz S., Marc Luetjens C., Truc Bui N., Krohn A. J., Poppe M., Cole G. M., Saido T. C., and, Prehn J. H., (2000) Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death. J. Biol. Chem. 275, 17064-17071. (Pubitemid 30398949)
31. Liu L., Cash T. P., Jones R. G., Keith B., Thompson C. B., and, Simon M. C., (2006) Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 21, 521-531. (Pubitemid 43228007)
32. Liu C., Liang B., Wang Q., Wu J., and, Zou M. H., (2010) Activation of AMP-activated protein kinase alpha1 alleviates endothelial cell apoptosis by increasing the expression of anti-apoptotic proteins Bcl-2 and survivin. J. Biol. Chem. 285, 15346-15355.
33. Malone C. D., Hasan S. M., Roome R. B., Xiong J., Furlong M., Opferman J. T., and, Vanderluit J. L., (2012) Mcl-1 regulates the survival of adult neural precursor cells. Mol. Cell. Neurosci. 49, 439-447.
34. McLaughlin B., Hartnett K. A., Erhardt J. A., Legos J. J., White R. F., Barone F. C., and, Aizenman E., (2003) Caspase 3 activation is essential for neuroprotection in preconditioning. Proc. Natl Acad. Sci. USA 100, 715-720. (Pubitemid 36126118)
35. Meisse D., van de Casteele M., Beauloye C., Hainault I., Kefas B. A., Rider M. H., Foufelle F., and, Hue L., (2002) Sustained activation of AMP-activated protein kinase induces c-Jun N-terminal kinase activation and apoptosis in liver cells. FEBS Lett. 526, 38-42. (Pubitemid 35245688)
36. Meller R., Minami M., Cameron J. A., Impey S., Chen D., Lan J. Q., Henshall D. C., and, Simon R. P., (2005) CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J. Cereb. Blood Flow Metab. 25, 234-246. (Pubitemid 40171205)
37. Navon H., Bromberg Y., Sperling O., and, Shani E., (2012) Neuroprotection by NMDA preconditioning against glutamate cytotoxicity is mediated through activation of ERK 1/2, inactivation of JNK, and by prevention of glutamate-induced CREB inactivation. J. Mol. Neurosci. 46, 100-108.
38. Nijhawan D., Fang M., Traer E., Zhong Q., Gao W., Du F., and, Wang X., (2003) Elimination of Mcl-1 is required for the initiation of apoptosis following ultraviolet irradiation. Genes Dev. 17, 1475-1486. (Pubitemid 36734705)
39. Ojuka E. O., (2004) Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle. Proc. Nutr. Soc. 63, 275-278. (Pubitemid 38787478)
40. Perciavalle R. M., Stewart D. P., Koss B., et al,. (2012) Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat. Cell Biol. 14, 575-583.
41. Rinkenberger J. L., Horning S., Klocke B., Roth K., and, Korsmeyer S. J., (2000) Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 14, 23-27. (Pubitemid 30051575)
42. Sabina R. L., Patterson D., and, Holmes E. W., (1985) 5-Amino-4-imidazolecarboxamide riboside (Z-riboside) metabolism in eukaryotic cells. J. Biol. Chem. 260, 6107-6114. (Pubitemid 15071307)
43. Smith A. J., Tauskela J. S., Stone T. W., and, Smith R. A., (2009) Preconditioning with 4-aminopyridine protects cerebellar granule neurons against excitotoxicity. Brain Res. 1294, 165-175.
44. Stein S. C., Woods A., Jones N. A., Davison M. D., and, Carling D., (2000) The regulation of AMP-activated protein kinase by phosphorylation. Biochem. J. 345 (Pt 3), 437-443. (Pubitemid 30099070)
45. Sullivan J. E., Brocklehurst K. J., Marley A. E., Carey F., Carling D., and, Beri R. K., (1994) Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett. 353, 33-36. (Pubitemid 24312538)
46. Turnley A. M., Stapleton D., Mann R. J., Witters L. A., Kemp B. E., and, Bartlett P. F., (1999) Cellular distribution and developmental expression of AMP-activated protein kinase isoforms in mouse central nervous system. J. Neurochem. 72, 1707-1716. (Pubitemid 29140848)
47. Viana R., Aguado C., Esteban I., Moreno D., Viollet B., Knecht E., and, Sanz P., (2008) Role of AMP-activated protein kinase in autophagy and proteasome function. Biochem. Biophys. Res. Commun. 369, 964-968.
48. Wang H., Yu S. W., Koh D. W., Lew J., Coombs C., Bowers W., Federoff H. J., Poirier G. G., Dawson T. M., and, Dawson V. L., (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J. Neurosci. 24, 10963-10973. (Pubitemid 39602407)
49. Ward M. W., Rego A. C., Frenguelli B. G., and, Nicholls D. G., (2000) Mitochondrial membrane potential and glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurosci. 20, 7208-7219.
50. Ward M. W., Huber H. J., Weisova P., Dussmann H., Nicholls D. G., and, Prehn J. H., (2007) Mitochondrial and plasma membrane potential of cultured cerebellar neurons during glutamate-induced necrosis, apoptosis, and tolerance. J. Neurosci. 27, 8238-8249. (Pubitemid 47219629)
51. Wei M. C., Zong W. X., Cheng E. H., Lindsten T., Panoutsakopoulou V., Ross A. J., Roth K. A., Macgregor G. R., Thompson C. B., and, Korsmeyer S. J., (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730. (Pubitemid 32385543)
52. Weisova P., Concannon C. G., Devocelle M., Prehn J. H., and, Ward M. W., (2009) Regulation of glucose transporter 3 surface expression by the AMP-activated protein kinase mediates tolerance to glutamate excitation in neurons. J. Neurosci. 29, 2997-3008.
53. Weisova P., Anilkumar U., Ryan C., Concannon C. G., Prehn J. H., and, Ward M. W., (2012) 'Mild mitochondrial uncoupling' induced protection against neuronal excitotoxicity requires AMPK activity. Biochim. Biophys. Acta 1817, 744-753.
54. White R. J., and, Reynolds I. J., (1995) Mitochondria and Na+/Ca2+ exchange buffer glutamate-induced calcium loads in cultured cortical neurons. J. Neurosci. 15, 1318-1328.
55. Wiegand F., Liao W., Busch C., et al. (1999) Respiratory chain inhibition induces tolerance to focal cerebral ischemia. J. Cereb. Blood Flow Metab. 19, 1229-1237. (Pubitemid 30176451)
56. Yang T., Kozopas K. M., and, Craig R. W., (1995) The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J. Cell Biol. 128, 1173-1184.
57. Youle R. J., and, Strasser A., (2008) The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9, 47-59.
58. Yu L., and, Yang S. J., (2010) AMP-activated protein kinase mediates activity-dependent regulation of peroxisome proliferator-activated receptor gamma coactivator-1alpha and nuclear respiratory factor 1 expression in rat visual cortical neurons. Neuroscience 169, 23-38.
59. Yu S. W., Wang H., Poitras M. F., Coombs C., Bowers W. J., Federoff H. J., Poirier G. G., Dawson T. M., and, Dawson V. L., (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297, 259-263. (Pubitemid 34761289)
60. Yun H., Lee M., Kim S. S., and, Ha J., (2005) Glucose deprivation increases mRNA stability of vascular endothelial growth factor through activation of AMP-activated protein kinase in DU145 prostate carcinoma. J. Biol. Chem. 280, 9963-9972. (Pubitemid 40395845)
61. Zhang H. X., Du G. H., and, Zhang J. T., (2003) Ischemic pre-conditioning preserves brain mitochondrial functions during the middle cerebral artery occlusion in rat. Neurol. Res. 25, 471-476.
62. Zong W. X., Lindsten T., Ross A. J., Macgregor G. R., and, Thompson C. B., (2001) BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15, 1481-1486. (Pubitemid 32552527)
63. Zong H., Ren J. M., Young L. H., Pypaert M., Mu J., Birnbaum M. J., and, Shulman G. I., (2002) AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc. Natl Acad. Sci. USA 99, 15983-15987. (Pubitemid 35462735)