Sphingosine kinase 2-deficiency mediated changes in spinal pain processing

Frontiers in Molecular Neuroscience

Volumn 8, Issue AUGUST, 2015, Pages

  Canlas, Jastrow ^a   Holt, Phillip ^a   Carroll, Alexander ^a   Rix, Shane ^a   Ryan, Paul ^a   Davies, Lorena ^b   Matusica, Dusan ^a   Pitson, Stuart M ^b   Jessup, Claire F ^a   Gibbins, Ian L ^a   Haberberger, Rainer V ^a  

^a FLINDERS UNIVERSITY   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

CFA; Dorsal horn; Formalin; Knock out mouse; RT PCR; Sphingosine 1 phosphate

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLIAL FIBRILLARY ACIDIC PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; PURINERGIC P2X4 RECEPTOR; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE KINASE 2;

ANIMAL EXPERIMENT; ARTICLE; FLUORESCENCE MICROSCOPY; FORMALIN TEST; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MALE; MECHANICAL HYPERALGESIA; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; RADIOIMMUNOPRECIPITATION; REVERSE TRANSCRIPTION; SIGNAL TRANSDUCTION; SPINAL PAIN; WESTERN BLOTTING;

EID: 84940995740     PISSN: 16625099     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnmol.2015.00029     Document Type: Article

References (47)

1. Allende, M. L., Sasaki, T., Kawai, H., Olivera, A., Mi, Y., van Echten-Deckert, G., et al. (2004). Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720.J. Biol. Chem. 279, 52487-52492. doi: 10.1074/jbc.m406512200
2. Beroukas, D., Pitson, S. M., Matusica, D., Gibbins, I. L., Kress, M., and Haberberger, R. V. (2015). Sphingosine kinase 1 in murine dorsal root ganglia. AIMS Mol. Sci. 1, 22-33. doi: 10.3934/molsci.2015.1.22
3. Boettger, M. K., Uceyler, N., Zelenka, M., Schmitt, A., Reif, A., Chen, Y., et al. (2007). Differences in inflammatory pain in nNOS-, iNOS- and eNOS-deficient mice. Eur. J. Pain 11, 810-818. doi: 10.1016/j.ejpain.2006.12.008
4. Bryan, L., Kordula, T., Spiegel, S., and Milstien, S. (2008). Regulation and functions of sphingosine kinases in the brain. Biochim. Biophys. Acta 1781, 459-466. doi: 10.1016/j.bbalip.2008.04.008
5. Camprubí-Robles, M., Mair, N., Andratsch, M., Benetti, C., Beroukas, D., Rukwied, R., et al. (2013). Sphingosine-1-phosphate-induced nociceptor excitation and ongoing pain behavior in mice and humans is largely mediated by S1P3 receptor. J. Neurosci.33, 2582-2592. doi: 10.1523/JNEUROSCI.4479-12.2013
6. Carr, F. B., Géranton, S. M., and Hunt, S. P. (2014). Descending controls modulate inflammatory joint pain and regulate CXC chemokine and iNOS expression in the dorsal horn. Mol. Pain 10:39. doi: 10.1186/1744-8069-10-39
7. Chang, Y. W., and Waxman, S. G. (2010). Minocycline attenuates mechanical allodynia and central sensitization following peripheral second-degree burn injury. J. Pain 11, 1146-1154. doi: 10.1016/j.jpain.2010.02.010
8. Choi, H. S., Roh, D. H., Yoon, S. Y., Moon, J. Y., Choi, S. R., Kwon, S. G., et al. (2015). Microglial interleukin-1beta in the ipsilateral dorsal horn inhibits the development of mirror-image, contralateral mechanical allodynia via astrocyte activation in a rat model of inflammatory pain. Pain 156, 1046-1059. doi: 10.1097/j.pain.0000000000000148
9. Coste, O., Brenneis, C., Linke, B., Pierre, S., Maeurer, C., Becker, W., et al. (2008a). Sphingosine 1-phosphate modulates spinal nociceptive processing. J. Biol. Chem. 283, 32442-32451. doi: 10.1074/jbc.m806410200
10. Coste, O., Pierre, S., Marian, C., Brenneis, C., Angioni, C., Schmidt, H., et al. (2008b). Antinociceptive activity of the S1P-receptor agonist FTY720. J. Cell. Mol. Med. 12, 995-1004. doi: 10.1111/j.1582-4934.2008.00160.x
11. da Costa, D. S., Meotti, F. C., Andrade, E. L., Leal, P. C., Motta, E. M., and Calixto, J. B. (2010). The involvement of the transient receptor potential A1 (TRPA1) in the maintenance of mechanical and cold hyperalgesia in persistent inflammation. Pain148, 431-437. doi: 10.1016/j.pain.2009.12.002
12. Finley, A., Chen, Z., Esposito, E., Cuzzocrea, S., Sabbadini, R., and Salvemini, D. (2013). Sphingosine 1-phosphate mediates hyperalgesia via a neutrophil-dependent mechanism. PLoS One 8:e55255. doi: 10.1371/journal.pone.0055255
13. Fischer, M., Carli, G., Raboisson, P., and Reeh, P. (2014). The interphase of the formalin test. Pain 155, 511-521. doi: 10.1016/j.pain.2013.11.015
14. Gao, Y. J., Xu, Z. Z., Liu, Y. C., Wen, Y. R., Decosterd, I., and Ji, R. R. (2010). The c-Jun N-terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition. Pain148, 309-319. doi: 10.1016/j.pain.2009.11.017
15. Hunskaar, S., and Hole, K. (1987). The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain 30, 103-114. doi: 10.1016/0304-3959(87)90088-1
16. Janes, K., Little, J. W., Li, C., Bryant, L., Chen, C., Chen, Z., et al. (2014). The development and maintenance of paclitaxel-induced neuropathic pain require activation of the sphingosine 1-phosphate receptor subtype 1. J. Biol. Chem. 289, 21082-21097. doi: 10.1074/jbc.m114.569574
17. Kharel, Y., Raje, M., Gao, M., Gellett, A. M., Tomsig, J. L., Lynch, K. R., et al. (2012). Sphingosine kinase type 2 inhibition elevates circulating sphingosine 1-phosphate.Biochem. J. 447, 149-157. doi: 10.1042/BJ20120609
18. Latremoliere, A., and Woolf, C. J. (2009). Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J. Pain 10, 895-926. doi: 10.1016/j.jpain.2009.06.012
19. Leclercq, T. M., Moretti, P. A., and Pitson, S. M. (2011). Guanine nucleotides regulate sphingosine kinase 1 activation by eukaryotic elongation factor 1A and provide a mechanism for eEF1A-associated oncogenesis. Oncogene 30, 372-378. doi: 10.1038/onc.2010.420
20. Liang, J., Nagahashi, M., Kim, E. Y., Harikumar, K. B., Yamada, A., Huang, W. C., et al. (2013). Sphingosine-1-phosphate links persistent STAT3 activation, chronic intestinal inflammation and development of colitis-associated cancer. Cancer Cell 23, 107-120. doi: 10.1016/j.ccr.2012.11.013
21. Lin, T., Li, K., Zhang, F. Y., Zhang, Z. K., Light, A. R., and Fu, K. Y. (2007). Dissociation of spinal microglia morphological activation and peripheral inflammation in inflammatory pain models. J. Neuroimmunol. 192, 40-48. doi: 10.1016/j.jneuroim.2007.09.003
22. Linke, B., Schreiber, Y., Zhang, D. D., Pierre, S., Coste, O., Henke, M., et al. (2012). Analysis of sphingolipid and prostaglandin synthesis during zymosan-induced inflammation. Prostaglandins Other Lipid Mediat. 99, 15-23. doi: 10.1016/j.prostaglandins.2012.06.002
23. Liu, X., Zhang, Q. H., and Yi, G. H. (2012). Regulation of metabolism and transport of sphingosine-1-phosphate in mammalian cells. Mol. Cell. Biochem. 363, 21-33. doi: 10.1007/s11010-011-1154-1
24. Mair, N., Benetti, C., Andratsch, M., Leitner, M. G., Constantin, C. E., Camprubí-Robles, M., et al. (2011). Genetic evidence for involvement of neuronally expressed S1P(1) receptor in nociceptor sensitization and inflammatory pain. PLoS One6:e17268. doi: 10.1371/journal.pone.0017268
25. Milligan, E. D., Twining, C., Chacur, M., Biedenkapp, J., O'connor, K., Poole, S., et al. (2003). Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J. Neurosci. 23, 1026-1040.
26. 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. doi: 10.1128/mcb.25.24.11113-11121.2005
27. Murphy, S. M., Pilowsky, P. M., and Llewellyn-Smith, I. J. (1998). Pre-embedding staining for GAD67 versus postembedding staining for GABA as markers for central GABAergic terminals. J. Histochem. Cytochem. 46, 1261-1268. doi: 10.1177/002215549804601106
28. Muscoli, C., Doyle, T., Dagostino, C., Bryant, L., Chen, Z., Watkins, L. R., et al. (2010). Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J. Neurosci. 30, 15400-15408. doi: 10.1523/JNEUROSCI.2391-10.2010
29. Orr Gandy, K. A., and Obeid, L. M. (2013). Targeting the sphingosine kinase/sphingosine 1-phosphate pathway in disease: review of sphingosine kinase inhibitors. Biochim. Biophys. Acta 1831, 157-166. doi: 10.1016/j.bbalip.2012.07.002
30. Pitman, M. R., and Pitson, S. M. (2010). Inhibitors of the sphingosine kinase pathway as potential therapeutics. Curr. Cancer Drug Targets. 10, 354-367. doi: 10.2174/156800910791208599
31. Pitman, M. R., Pham, D. H., and Pitson, S. M. (2012). Isoform-selective assays for sphingosine kinase activity. Methods Mol. Biol. 874, 21-31. doi: 10.1007/978-1-61779-800-9_2
32. Pitson, S. M. (2011). Regulation of sphingosine kinase and sphingolipid signaling.Trends Biochem. Sci. 36, 97-107. doi: 10.1016/j.tibs.2010.08.001
33. Salvemini, D., Doyle, T., Kress, M., and Nicol, G. (2013). Therapeutic targeting of the ceramide-to-sphingosine 1-phosphate pathway in pain. Trends Pharmacol. Sci. 34, 110-118. doi: 10.1016/j.tips.2012.12.001
34. Schreiber, K. L., Beitz, A. J., and Wilcox, G. L. (2008). Activation of spinal microglia in a murine model of peripheral inflammation-induced, long-lasting contralateral allodynia. Neurosci. Lett. 440, 63-67. doi: 10.1016/j.neulet.2008.05.044
35. Shields, S. D., Cavanaugh, D. J., Lee, H., Anderson, D. J., and Basbaum, A. I. (2010). Pain behavior in the formalin test persists after ablation of the great majority of C-fiber nociceptors. Pain 151, 422-429. doi: 10.1016/j.pain.2010.08.001
36. Simon, P. (2003). Q-Gene: processing quantitative real-time RT-PCR data.Bioinformatics 19, 1439-1440. doi: 10.1093/bioinformatics/btg157
37. Sim-Selley, L. J., Goforth, P. B., Mba, M. U., Macdonald, T. L., Lynch, K. R., Milstien, S., et al. (2009). Sphingosine-1-phosphate receptors mediate neuromodulatory functions in the CNS. J. Neurochem. 110, 1191-1202. doi: 10.1111/j.1471-4159.2009.06202.x
38. Siow, D., and Wattenberg, B. (2011). The compartmentalization and translocation of the sphingosine kinases: mechanisms and functions in cell signaling and sphingolipid metabolism. Crit. Rev. Biochem. Mol. Biol. 46, 365-375. doi: 10.3109/10409238.2011.580097
39. Strub, G. M., Paillard, M., Liang, J., Gomez, L., Allegood, J. C., Hait, N. C., et al. (2011). Sphingosine-1-phosphate produced by sphingosine kinase 2 in mitochondria interacts with prohibitin 2 to regulate complex IV assembly and respiration. FASEB J. 25, 600-612. doi: 10.1096/fj.10-167502
40. Sun, Y. H., Dong, Y. L., Wang, Y. T., Zhao, G. L., Lu, G. J., Yang, J., et al. (2013). Synergistic analgesia of duloxetine and celecoxib in the mouse formalin test: a combination analysis. PLoS One 8:e76603. doi: 10.1371/journal.pone.0076603
41. Sung, C. S., Cherng, C. H., Wen, Z. H., Chang, W. K., Huang, S. Y., Lin, S. L., et al. (2012). Minocycline and fluorocitrate suppress spinal nociceptive signaling in intrathecal IL-1beta-induced thermal hyperalgesic rats. Glia 60, 2004-2017. doi: 10.1002/glia.22415
42. Trang, T., Beggs, S., and Salter, M. W. (2012). ATP receptors gate microglia signaling in neuropathic pain. Exp Neurol 234, 354-361. doi: 10.1016/j.expneurol.2011.11.012
43. Tsuda, M., Shigemoto-Mogami, Y., Koizumi, S., Mizokoshi, A., Kohsaka, S., Salter, M. W., et al. (2003). P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424, 778-783. doi: 10.1038/nature01786
44. Ulmann, L., Hatcher, J. P., Hughes, J. P., Chaumont, S., Green, P. J., Conquet, F., et al. (2008). Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci. 28, 11263-11268. doi: 10.1523/jneurosci.2308-08.2008
45. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., et al. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3:RESEARCH0034. doi: 10.1186/gb-2002-3-7-research0034
46. Yaksh, T. L., Ozaki, G., Mccumber, D., Rathbun, M., Svensson, C., Malkmus, S., et al. (2001). An automated flinch detecting system for use in the formalin nociceptive bioassay. J. Appl. Physiol.(1985) 90, 2386-2402.
47. Zhang, D. D., Linke, B., Suo, J., Zivkovic, A., Schreiber, Y., Ferreirós, N., et al. (2015). Antinociceptive effects of FTY720 during trauma-induced neuropathic pain are mediated by pinal S1P receptors. Biol. Chem. 396, 783-794. doi: 10.1515/hsz-2014-0276