Global SUMOylation is a molecular mechanism underlying hypothermia-induced ischemic tolerance

Frontiers in Cellular Neuroscience

Volumn 8, Issue DEC, 2014, Pages

  Lee, Yang Ja ^a   Mou, Yongshan ^a   Klimanis, Dace ^a   Bernstock, Joshua D ^a   Hallenbeck, John M ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Hypothermia; Neuroprotection; PMCAO; SUMOylation; Ubc9

Indexed keywords

POTASSIUM DIHYDROGEN PHOSPHATE;

ARTICLE; CRYSTAL STRUCTURE; DOPING; FOURIER TRANSFORM INFRARED PHOTOACOUSTIC SPECTROSCOPY; MECHANICS; MELTING POINT; MICROSCOPY; MORPHOLOGY; NONLINEAR SYSTEM; SPECTRAL SENSITIVITY; ULTRAVIOLET SPECTROPHOTOMETRY; X RAY DIFFRACTION; YAG LASER;

EID: 84930674216     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00416     Document Type: Article

References (45)

1. Abdullah, J. M., and Husin, A. (2011). Intravascular hypothermia for acute hemorrhagic stroke: a pilot study. Acta Neurochir. Suppl. 111, 421-424. doi: 10.1007/978-3-7091-0693-8_72
2. Arsenijevic, D., de Bilbao, F., Plamondon, J., Paradis, E., Vallet, P., Richard, D., et al. (2006). Increased infarct size and lack of hyperphagic response after focal cerebral ischemia in peroxisome proliferator-activated receptor beta-deficient mice. J. Cereb. Blood Flow Metab. 26, 433-445. doi: 10.1038/sj.jcbfm.9600200
3. Broussalis, E., Killer, M., McCoy, M., Harrer, A., Trinka, E., and Kraus, J. (2012a). Current therapies in ischemic stroke. Part A. Recent developments in acute stroke treatment and in stroke prevention. Drug Discov. Today 17, 296-309. doi: 10.1016/j.drudis.2011.11.005
4. Broussalis, E., Trinka, E., Killer, M., Harrer, A., McCoy, M., and Kraus, J. (2012b). Current therapies in ischemic stroke. Part B. Future candidates in stroke therapy and experimental studies. Drug Discov. Today 17, 671-684. doi: 10.1016/j.drudis.2012.02.011
5. Choi, K. E., Hall, C. L., Sun, J. M., Wei, L., Mohamad, O., Dix, T. A., et al. (2012). A novel stroke therapy of pharmacologically induced hypothermia after focal cerebral ischemia in mice. FASEB J. 26, 2799-2810. doi: 10.1096/fj.11-201822
6. Cimarosti, H., Ashikaga, E., Jaafari, N., Dearden, L., Rubin, P., Wilkinson, K. A., et al. (2012). Enhanced SUMOylation and SENP-1 protein levels following oxygen and glucose deprivation in neurones. J. Cereb. Blood Flow Metab. 32, 17-22. doi: 10.1038/jcbfm.2011.146
7. Cimarosti, H., Lindberg, C., Bomholt, S. F., Rønn, L. C., and Henley, J. M. (2008). Increased protein SUMOylation following focal cerebral ischemia. Neuropharmacology 54, 280-289. doi: 10.1016/j.neuropharm.2007.09.010
8. Datwyler, A. L., Lättig-Tünnemann, G., Yang, W., Paschen, W., Lee, S. L., Dirnagl, U., et al. (2011). SUMO2/3 conjugation is an endogenous neuroprotective mechanism. J. Cereb. Blood Flow Metab. 31, 2152-2159. doi: 10.1038/jcbfm.2011.112
9. Dirnagl, U., Iadecola, C., and Moskowitz, M. A. (1999). Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391-397. doi: 10.1016/s0166-2236(99)01401-0
10. Evdokimov, E., Sharma, P., Lockett, S. J., Lualdi, M., and Kuehn, M. R. (2008). Loss of SUMO1 in mice affects RanGAP1 localization and formation of PML nuclear bodies, but is not lethal as it can be compensated by SUMO2 or SUMO3. J. Cell Sci. 121, 4106-4113. doi: 10.1242/jcs.038570
11. González-Ibarra, F. P., Varon, J., and López-Meza, E. G. (2011). Therapeutic hypothermia: critical review of the molecular mechanisms of action. Front. Neurol. 2:4. doi: 10.3389/fneur.2011.00004
12. Hallenbeck, J. M. (2002). The many faces of tumor necrosis factor in stroke. Nat. Med. 8, 1363-1368. doi: 10.1038/nm1202-1363
13. Hallenbeck, J. M., and Frerichs, K. U. (1993). Stroke therapy. It may be time for an integrated approach. Arch. Neurol. 50, 768-770. doi: 10.1001/archneur.1993.00540070080020
14. Hay, R. T. (2005). SUMO: a history of modification. Mol. Cell 18, 1-12. doi: 10.1016/j.molcel.2005.03.012
15. Hayashi, T., Seki, M., Maeda, D., Wang, W., Kawabe, Y., Seki, T., et al. (2002). Ubc9 is essential for viability of higher eukaryotic cells. Exp. Cell Res. 280, 212-221. doi: 10.1006/excr.2002.5634
16. Iadecola, C., and Anrather, J. (2011). Stroke research at a crossroad: asking the brain for directions. Nat. Neurosci.14, 1363-1368. doi: 10.1038/nn.2953
17. Katz, L. M., Young, A., Frank, J. E., Wang, Y., and Park, K. (2004). Neurotensin-induced hypothermia improves neurologic outcome after hypoxic-ischemia. Crit. Care Med. 32, 806-810. doi: 10.1097/01.ccm.0000114998.00860.fd
18. Kollmar, R., Juettler, E., Huttner, H. B., Dörfler, A., Staykov, D., Kallmuenzer, B., et al. (2012). Cooling in intracerebral hemorrhage (CINCH) trial: protocol of a randomized German-Austrian clinical trial. Int. J. Stroke 7, 168-172. doi: 10.1111/j.1747-4949.2011.00707.x
19. Krieger, D. W., and Yenari, M. A. (2004). Therapeutic hypothermia for acute ischemic stroke: what do laboratory studies teach us? Stroke 35, 1482-1489. doi: 10.1161/01.str.0000126118.44249.5c
20. Leach, M. J., Swan, J. H., Eisenthal, D., Dopson, M., and Nobbs, M. (1993). BW619C89, a glutamate release inhibitor, protects against focal cerebral ischemic damage. Stroke 24, 1063-1067. doi: 10.1161/01.str.24.7.1063
21. Lee, Y. J., Castri, P., Bembry, J., Maric, D., Auh, S., and Hallenbeck, J. M. (2009). SUMOylation participates in induction of ischemic tolerance. J. Neurochem. 109, 257-267. doi: 10.1111/j.1471-4159.2009.05957.x
22. Lee, Y. J., Miyake, S., Wakita, H., McMullen, D. C., Azuma, Y., Auh, S., et al. (2007). Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. J. Cereb. Blood Flow Metab. 27, 950-962. doi: 10.1038/sj.jcbfm.9600395
23. Lee, Y. J., Mou, Y., Maric, D., Klimanis, D., Auh, S., and Hallenbeck, J. M. (2011). Elevated global SUMOylation in Ubc9 transgenic mice protects their brains against focal cerebral ischemic damage. PLoS One 6:e25852. doi: 10.1371/journal.pone.0025852
24. Loftus, L. T., Gala, R., Yang, T., Jessick, V. J., Ashley, M. D., Ordonez, A. N., et al. (2009). Sumo-2/3-ylation following in vitro modeled ischemia is reduced in delayed ischemic tolerance. Brain Res. 1272, 71-80. doi: 10.1016/j.brainres.2009.03.034
25. Macleod, M. R., Petersson, J., Norrving, B., Hacke, W., Dirnagl, U., Wagner, M., et al. (2010). Hypothermia for stroke: call to action 2010. Int. J. Stroke 5, 489-492. doi: 10.1111/j.1747-4949.2010.00520.x
26. Mergenthaler, P., Dirnagl, U., and Meisel, A. (2004). Pathophysiology of stroke: lessons from animal models. Metab. Brain Dis. 19, 151-167. doi: 10.1023/b:mebr.0000043966.46964.e6
27. Mou, Y., Wilgenburg, B. J., Lee, Y. J., and Hallenbeck, J. M. (2013). A method for hypothermia-induction and maintenance allows precise body and brain temperature control in mice. J. Neurosci. Methods 213, 1-5. doi: 10.1016/j.jneumeth.2012.11.006
28. Müller, S., Hoege, C., Pyrowolakis, G., and Jentsch, S. (2001). SUMO, ubiquitin's mysterious cousin. Nat. Rev. Mol. Cell Biol. 2, 202-210. doi: 10.1038/35056591
29. Nacerddine, K., Lehembre, F., Bhaumik, M., Artus, J., Cohen-Tannoudji, M., Babinet, C., et al. (2005). The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. Dev. Cell 9, 769-779. doi: 10.1016/j.devcel.2005.10.007
30. Nagel, S., Papadakis, M., Hoyte, L., and Buchan, A. M. (2008). Therapeutic hypothermia in experimental models of focal and global cerebral ischemia and intracerebral hemorrhage. Expert Rev. Neurother. 8, 1255-1268. doi: 10.1586/14737175.8.8.1255
31. Nishio, S., Yunoki, M., Chen, Z. F., Anzivino, M. J., and Lee, K. S. (2000). Ischemic tolerance in the rat neocortex following hypothermic preconditioning. J. Neurosurg. 93, 845-851. doi: 10.3171/jns.2000.93.5.0845
32. O'Collins, V. E., Donnan, G. A., Macleod, M. R., and Howells, D. W. (2009). Scope of preclinical testing versus quality control within experiments. Stroke 40:e497. doi: 10.1161/STROKEAHA.109.550335
33. O'Collins, V. E., Macleod, M. R., Donnan, G. A., Horky, L. L., van der Worp, B. H., and Howells, D. W. (2006). 1,026 experimental treatments in acute stroke. Ann. Neurol. 59, 467-477. doi: 10.1002/ana.20741
34. Roger, V. L., Go, A. S., Lloyd-Jones, D. M., Benjamin, E. J., Berry, J. D., Borden, W. B., et al. (2012). Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125, e2-e220. doi: 10.1161/CIR.0b013e31823ac046
35. Tatham, M. H., Jaffray, E., Vaughan, O. A., Desterro, J. M., Botting, C. H., Naismith, J. H., et al. (2001). Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9. J. Biol. Chem. 276, 35368-35374. doi: 10.1074/jbc.m104214200
36. Tempé, D., Piechaczyk, M., and Bossis, G. (2008). SUMO under stress. Biochem. Soc. Trans. 36, 874-878. doi: 10.1042/BST0360874
37. van der Worp, H. B., Macleod, M. R., Kollmar, R., and European Stroke Research Network for Hypothermia (EuroHYP). (2010). Therapeutic hypothermia for acute ischemic stroke: ready to start large randomized trials? J. Cereb. Blood Flow Metab. 30, 1079-1093. doi: 10.1038/jcbfm.2010.44
38. Wang, L., Ma, Q., Yang, W., Mackensen, G. B., and Paschen, W. (2012). Moderate hypothermia induces marked increase in levels and nuclear accumulation of SUMO2/3-conjugated proteins in neurons. J. Neurochem. 123, 349-359. doi: 10.1111/j.1471-4159.2012.07916.x
39. Yang, W., Ma, Q., Mackensen, G. B., and Paschen, W. (2009). Deep hypothermia markedly activates the small ubiquitin-like modifier conjugation pathway; implications for the fate of cells exposed to transient deep hypothermic cardiopulmonary bypass. J. Cereb. Blood Flow Metab. 29, 886-890. doi: 10.1038/jcbfm.2009.16
40. Yang, W., Sheng, H., Homi, H. M., Warner, D. S., and Paschen, W. (2008). Cerebral ischemia/stroke and small ubiquitin-like modifier (SUMO) conjugation-a new target for therapeutic intervention? J. Neurochem. 106, 989-999. doi: 10.1111/j.1471-4159.2008.05404.x
41. Yenari, M. A., and Han, H. S. (2012). Neuroprotective mechanisms of hypothermia in brain ischaemia. Nat. Rev. Neurosci. 13, 267-278. doi: 10.1038/nrn3174
42. Yenari, M., Kitagawa, K., Lyden, P., and Perez-Pinzon, M. (2008). Metabolic downregulation: a key to successful neuroprotection? Stroke 39, 2910-2917. doi: 10.1161/STROKEAHA.108.514471
43. Yunoki, M., Nishio, S., Ukita, N., Anzivino, M. J., and Lee, K. S. (2002). Characteristics of hypothermic preconditioning influencing the induction of delayed ischemic tolerance. J. Neurosurg. 97, 650-657. doi: 10.3171/jns.2002.97.3.0650
44. Yunoki, M., Nishio, S., Ukita, N., Anzivino, M. J., and Lee, K. S. (2003). Hypothermic preconditioning induces rapid tolerance to focal ischemic injury in the rat. Exp. Neurol. 181, 291-300. doi: 10.1016/s0014-4886(03)00056-6
45. Zhang, F. P., Mikkonen, L., Toppari, J., Palvimo, J. J., Thesleff, I., and Jänne, O. A. (2008). Sumo-1 function is dispensable in normal mouse development. Mol. Cell. Biol. 28, 5381-5390. doi: 10.1128/MCB.00651-08