Preconditioning stimuli induce autophagy via Sphingosine kinase 2 in mouse cortical neurons

Journal of Biological Chemistry

Volumn 289, Issue 30, 2014, Pages 20845-20857

  Sheng, Rui ^a,b   Zhang, Tong Tong ^a   Felice, Valeria D ^c   Qin, Tao ^b   Qin, Zheng Hong ^a   Smith, Charles D ^d   Sapp, Ellen ^e   Difiglia, Marian ^e   Waeber, Christian ^b,c,d  

^a SOOCHOW UNIVERSITY   (China)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d UNIVERSITY COLLEGE CORK   (Ireland)

^e APOGEE BIOTECHNOLOGY CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALS; NEURONS; SPHINGOSINES;

CORTICAL NEURONS; CULTURED NEURONS; IMMUNOSTAINING; OXYGEN GLUCOSE DEPRIVATION; SPHINGOSINE 1 PHOSPHATES; SPHINGOSINE KINASE 2; UP-REGULATION; WESTERN BLOTS;

ANESTHETICS;

2-MORPHOLIN-4-YL-6-THIANTHREN-1-YL-PYRAN-4-ONE; 3-(4-CHLOROPHENYL)-ADAMANTANE-1-CARBOXYLIC ACID (PYRIDIN-4-YLMETHYL)AMIDE; ADAMANTANE; APOPTOSIS REGULATORY PROTEIN; BECN1 PROTEIN, MOUSE; ENZYME INHIBITOR; GTF2H1 PROTEIN, MOUSE; INHALATION ANESTHETIC AGENT; ISOFLURANE; LACTOSYLCERAMIDE; LACTOTRIAOSYLCERAMIDE; MORPHOLINE DERIVATIVE; PHOSPHOTRANSFERASE; PROTEIN BCL 2; PYRIDINE DERIVATIVE; PYRONE DERIVATIVE; SPHINGOSINE KINASE; TRANSCRIPTION FACTOR;

ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; AUTOPHAGY; BRAIN CORTEX; CELL CULTURE; CYTOLOGY; GENETICS; ISCHEMIC PRECONDITIONING; KNOCKOUT MOUSE; METABOLISM; MOUSE; NERVE CELL;

ADAMANTANE; ANESTHETICS, INHALATION; ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELLS, CULTURED; CEREBRAL CORTEX; ENZYME INHIBITORS; ISCHEMIC PRECONDITIONING; ISOFLURANE; LACTOSYLCERAMIDES; MICE; MICE, KNOCKOUT; MORPHOLINES; NEURONS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTO-ONCOGENE PROTEINS C-BCL-2; PYRIDINES; PYRONES; TRANSCRIPTION FACTORS;

EID: 84905392495     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578120     Document Type: Article

References (55)

1. Dirnagl, U., Becker, K., and Meisel, A. (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol. 8, 398-412
2. Gidday, J. M. (2006) Cerebral preconditioning and ischaemic tolerance. Nat. Rev. Neurosci. 7, 437-448
3. Harada, J., Foley, M., Moskowitz, M. A., and Waeber, C. (2004) Sphingosine-1-phosphate induces proliferation and morphological changes of neural progenitor cells. J. Neurochem. 88, 1026-1039
4. Jin, Z. Q., Goetzl, E. J., and Karliner, J. S. (2004) Sphingosine kinase activation mediates ischemic preconditioning in murine heart. Circulation 110, 1980-1989
5. Vessey, D. A., Li, L., Kelley, M., and Karliner, J. S. (2008) Combined sphingosine, S1P and ischemic postconditioning rescue the heart after protracted ischemia. Biochem. Biophys. Res. Commun. 375, 425-429
6. Vessey, D. A., Li, L., Jin, Z. Q., Kelley, M., Honbo, N., Zhang, J., and Karliner, J. S. (2011) A sphingosine kinase form 2 knockout sensitizes mouse myocardium to ischemia/reoxygenation injury and diminishes responsiveness to ischemic preconditioning. Oxid. Med. Cell. Longev. 2011, 961059
7. Jin, Z. Q., Karliner, J. S., and Vessey, D. A. (2008) Ischaemic postconditioning protects isolated mouse hearts against ischaemia/reperfusion injury via sphingosine kinase isoform-1 activation. Cardiovasc. Res. 79, 134-140
8. Kim, M., Kim, N., D'Agati, V. D., Emala, C. W., Sr., and Lee, H. T. (2007) Isoflurane mediates protection from renal ischemia-reperfusion injury via sphingosine kinase and sphingosine-1-phosphate-dependent pathways. Am. J. Physiol. Renal Physiol. 293, F1827-F1835
9. Yung, L. M., Wei, Y., Qin, T., Wang, Y., Smith, C. D., and Waeber, C. (2012) Sphingosine kinase 2 mediates cerebral preconditioning and protects the mouse brain against ischemic injury. Stroke 43, 199-204
10. Klionsky, D. J., and Emr, S. D. (2000) Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721
11. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., and Tanaka, K. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884
12. Gottlieb, R. A., and Mentzer, R. M. (2010) Autophagy during cardiac stress: joys and frustrations of autophagy. Annu. Rev. Physiol. 72, 45-59
13. Huang, C., Yitzhaki, S., Perry, C. N., Liu, W., Giricz, Z., Mentzer, R. M., Jr., and Gottlieb, R. A. (2010) Autophagy induced by ischemic preconditioning is essential for cardioprotection. J. Cardiovasc. Transl. Res. 3, 365-373
14. Sheng, R., Zhang, L. S., Han, R., Liu, X. Q., Gao, B., and Qin, Z. H. (2010) Autophagy activation is associated with neuroprotection in a rat model of focal cerebral ischemic preconditioning. Autophagy 6, 482-494
15. Sheng, R., Liu, X. Q., Zhang, L. S., Gao, B., Han, R., Wu, Y. Q., Zhang, X. Y., and Qin, Z. H. (2012) Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 8, 310-325
16. Xia, M. Q., Bacskai, B. J., Knowles, R. B., Qin, S. X., and Hyman, B. T. (2000) Expression of the chemokine receptor CXCR3 on neurons and the elevated expression of its ligand IP-10 in reactive astrocytes: in vitro ERK1/2 activation and role in Alzheimer's disease. J. Neuroimmunol. 108, 227-235
17. Wick, A., Wick, W., Waltenberger, J., Weller, M., Dichgans, J., and Schulz, J. B. (2002) Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J. Neurosci. 22, 6401-6407
18. Zheng, S., and Zuo, Z. (2003) Isoflurane preconditioning reduces Purkinje cell death in an in vitro model of rat cerebellar ischemia. Neuroscience 118, 99-106
19. McMurtrey, R. J., and Zuo, Z. (2010) Isoflurane preconditioning and postconditioning in rat hippocampal neurons. Brain Res. 1358, 184-190
20. Zhao, P., and Zuo, Z. (2004) Isoflurane preconditioning induces neuroprotection that is inducible nitric oxide synthase-dependent in neonatal rats. Anesthesiology 101, 695-703
21. Shimada, K., Motoi, Y., Ishiguro, K., Kambe, T., Matsumoto, S. E., Itaya, M., Kunichika, M., Mori, H., Shinohara, A., Chiba, M., Mizuno, Y., Ueno, T., and Hattori, N. (2012) Long-term oral lithium treatment attenuates motor disturbance in tauopathy model mice: implications of autophagy promotion. Neurobiol. Dis. 46, 101-108
22. Seglen, P. O., and Gordon, P. B. (1982) 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 79, 1889-1892
23. Farkas, T., Daugaard, M., and Jäättelä, M. (2011) Identification of small molecule inhibitors of phosphatidylinositol 3-kinase and autophagy. J. Biol. Chem. 286, 38904-38912
24. French, K. J., Upson, J. J., Keller, S. N., Zhuang, Y., Yun, J. K., and Smith, C. D. (2006) Antitumor activity of sphingosine kinase inhibitors. J. Pharmacol. Exp. Ther. 318, 596-603
25. French, K. J., Zhuang, Y., Maines, L. W., Gao, P., Wang, W., Beljanski, V., Upson, J. J., Green, C. L., Keller, S. N., and Smith, C. D. (2010) Pharmacology and antitumor activity of ABC294640, a selective inhibitor of sphingosine kinase-2. J. Pharmacol. Exp. Ther. 333, 129-139
26. Wei, Y., Yemisci, M., Kim, H. H., Yung, L. M., Shin, H. K., Hwang, S. K., Guo, S., Qin, T., Alsharif, N., Brinkmann, V., Liao, J. K., Lo, E. H., and Waeber, C. (2011) Fingolimod provides long-term protection in rodent models of cerebral ischemia. Ann. Neurol. 69, 119-129
27. Tönges, L., Lingor, P., Egle, R., Dietz, G. P., Fahr, A., and Bähr, M. (2006) Stearylated octaarginine and artificial virus-like particles for transfection of siRNA into primary rat neurons. RNA 12, 1431-1438
28. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
29. Chakrabarti, L., Eng, J., Ivanov, N., Garden, G. A., and La Spada, A. R. (2009) Autophagy activation and enhanced mitophagy characterize the Purkinje cells of pcd mice prior to neuronal death. Mol. Brain 2, 24
30. Sato, K., Tsuchihara, K., Fujii, S., Sugiyama, M., Goya, T., Atomi, Y., Ueno, T., Ochiai, A., and Esumi, H. (2007) Autophagy is activated in colorectal cancer cells and contributes to the tolerance to nutrient deprivation. Cancer Res. 67, 9677-9684
31. Beljanski, V., Knaak, C., and Smith, C. D. (2010) A novel sphingosine kinase inhibitor induces autophagy in tumor cells. J. Pharmacol. Exp. Ther. 333, 454-464
32. Allende, M. L., Sasaki, T., Kawai, H., Olivera, A., Mi, Y., van Echten-Deckert, G., Hajdu, R., Rosenbach, M., Keohane, C. A., Mandala, S., Spiegel, S., and Proia, R. L. (2004) Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J. Biol. Chem. 279, 52487-52492
33. Mizugishi, K., Yamashita, T., Olivera, A., Miller, G. F., Spiegel, S., and Proia, R. L. (2005) Essential role for sphingosine kinases in neural and vascular development. Mol. Cell. Biol. 25, 11113-11121
34. Liu, H., Toman, R. E., Goparaju, S. K., Maceyka, M., Nava, V. E., Sankala, H., Payne, S. G., Bektas, M., Ishii, I., Chun, J., Milstien, S., and Spiegel, S. (2003) Sphingosine kinase type 2 is a putative BH3-only protein that induces apoptosis. J. Biol. Chem. 278, 40330-40336
35. Bellot, G., Garcia-Medina, R., Gounon, P., Chiche, J., Roux, D., Pouysségur, J., and Mazure, N. M. (2009) Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 29, 2570-2581
36. Blondeau, N., Lai, Y., Tyndall, S., Popolo, M., Topalkara, K., Pru, J. K., Zhang, L., Kim, H., Liao, J. K., Ding, K., and Waeber, C. (2007) Distribution of sphingosine kinase activity and mRNA in rodent brain. J. Neurochem. 103, 509-517
37. Wacker, B. K., Park, T. S., and Gidday, J. M. (2009) Hypoxic preconditioninginduced cerebral ischemic tolerance: role of microvascular sphingosine kinase 2. Stroke 40, 3342-3348
38. Wacker, B. K., Freie, A. B., Perfater, J. L., and Gidday, J. M. (2012) Junctional protein regulation by sphingosine kinase 2 contributes to bloodbrain barrier protection in hypoxic preconditioning-induced cerebral ischemic tolerance. J. Cereb. Blood Flow Metab. 32, 1014-1023
39. Wacker, B. K., Perfater, J. L., and Gidday, J. M. (2012) Hypoxic preconditioning induces stroke tolerance in mice via a cascading HIF, sphingosine kinase, and CCL2 signaling pathway. J. Neurochem. 123, 954-962
40. Pattingre, S., Bauvy, C., Levade, T., Levine, B., and Codogno, P. (2009) Ceramide-induced autophagy: to junk or to protect cells? Autophagy 5, 558-560
41. Sentelle, R. D., Senkal, C. E., Jiang, W., Ponnusamy, S., Gencer, S., Selvam, S. P., Ramshesh, V. K., Peterson, Y. K., Lemasters, J. J., Szulc, Z. M., Bielawski, J., and Ogretmen, B. (2012) Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy. Nat. Chem. Biol. 8, 831-838
42. Chang, C. L., Ho, M. C., Lee, P. H., Hsu, C. Y., Huang, W. P., and Lee, H. (2009) S1P (5) is required for sphingosine 1-phosphate-induced autophagy in human prostate cancer PC-3 cells. Am. J. Physiol. Cell Physiol. 297, C451-C458
43. Zhang, N., Qi, Y., Wadham, C., Wang, L., Warren, A., Di, W., and Xia, P. (2010) FTY720 induces necrotic cell death and autophagy in ovarian cancer cells: a protective role of autophagy. Autophagy 6, 1157-1167
44. Taniguchi, M., Kitatani, K., Kondo, T., Hashimoto-Nishimura, M., Asano, S., Hayashi, A., Mitsutake, S., Igarashi, Y., Umehara, H., Takeya, H., Kigawa, J., and Okazaki, T. (2012) Regulation of autophagy and its associated cell death by "sphingolipid rheostat": reciprocal role of ceramide and sphingosine 1-phosphate in the mammalian target of rapamycin pathway. J. Biol. Chem. 287, 39898-39910
45. Payne, S. G., Milstien, S., and Spiegel, S. (2002) Sphingosine-1- phosphate: dual messenger functions. FEBS Lett. 531, 54-57
46. Liu, J., Zhang, C., Tao, W., and Liu, M. (2013) Systematic review and meta-analysis of the efficacy of sphingosine-1-phosphate (S1P) receptor agonist FTY720 (fingolimod) in animal models of stroke. Int. J. Neurosci. 123, 163-169
47. Di Menna, L., Molinaro, G., Di Nuzzo, L., Riozzi, B., Zappulla, C., Pozzilli, C., Turrini, R., Caraci, F., Copani, A., Battaglia, G., Nicoletti, F., and Bruno, V. (2013) Fingolimod protects cultured cortical neurons against excitotoxic death. Pharmacol. Res. 67, 1-9
48. Loveridge, C., Tonelli, F., Leclercq, T., Lim, K. G., Long, J. S., Berdyshev, E., Tate, R. J., Natarajan, V., Pitson, S. M., Pyne, N. J., and Pyne, S. (2010) The sphingosine kinase 1 inhibitor 2-(p-hydroxyanilino)-4-(p- chlorophenyl) thiazole induces proteasomal degradation of sphingosine kinase 1 in mammalian cells. J. Biol. Chem. 285, 38841-38852
49. Tonelli, F., Lim, K. G., Loveridge, C., Long, J., Pitson, S. M., Tigyi, G., Bittman, R., Pyne, S., and Pyne, N. J. (2010) FTY720 and (S)-FTY720 vinylphosphonate inhibit sphingosine kinase 1 and promote its proteasomal degradation in human pulmonary artery smooth muscle, breast cancer and androgen-independent prostate cancer cells. Cell. Signal. 22, 1536-1542
50. Samy, E. T., Meyer, C. A., Caplazi, P., Langrish, C. L., Lora, J. M., Bluethmann, H., and Peng, S. L. (2007) Cutting edge: Modulation of intestinal autoimmunity and IL-2 signaling by sphingosine kinase 2 independent of sphingosine 1-phosphate. J. Immunol. 179, 5644-5648
51. Maiuri, M. C., Criollo, A., Tasdemir, E., Vicencio, J. M., Tajeddine, N., Hickman, J. A., Geneste, O., and Kroemer, G. (2007) BH3-only proteins and BH3 mimetics induce autophagy by competitively disrupting the interaction between Beclin 1 and Bcl-2/Bcl-X (L). Autophagy 3, 374-376
52. Zhang, H., Bosch-Marce, M., Shimoda, L. A., Tan, Y. S., Baek, J. H., Wesley, J. B., Gonzalez, F. J., and Semenza, G. L. (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 283, 10892-10903
53. Schnitzer, S. E., Weigert, A., Zhou, J., and Brüne, B. (2009) Hypoxia enhances sphingosine kinase 2 activity and provokes sphingosine-1- phosphatemediated chemoresistance in A549 lung cancer cells. Mol. Cancer Res. 7, 393-401
54. Papandreou, I., Krishna, C., Kaper, F., Cai, D., Giaccia, A. J., and Denko, N. C. (2005) Anoxia is necessary for tumor cell toxicity caused by a lowoxygen environment. Cancer Res. 65, 3171-3178
55. Drews, J. (2000) Drug discovery: a historical perspective. Science 287, 1960-1964