Sphingosine 1-phosphate receptor 2 (S1P2) attenuates reactive oxygen species formation and inhibits cell death: Implications for otoprotective therapy

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Herr, Deron R ^a,b   Reolo, Marie J Y ^a   Peh, Yee Xin ^a   Wang, Wei ^a   Lee, Chang Wook ^c   Rivera, Rich ^c   Paterson, Ian C ^d   Chun, Jerold ^c  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF MALAYA   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

AGONISTS; ANIMAL; CELL DEATH; CELL SURVIVAL; COCHLEA; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DEATH; CELL SURVIVAL; COCHLEA; MICE; MICE, KNOCKOUT; REACTIVE OXYGEN SPECIES; RECEPTORS, LYSOSPHINGOLIPID; SIGNAL TRANSDUCTION;

EID: 84964311238     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24541     Document Type: Article

References (52)

1. Oishi, N. & Schacht, J. Emerging treatments for noise-induced hearing loss. Expert Opin Emerg Drugs 16, 235-245, doi: 10.1517/14728214.2011.552427 (2011).
2. Bedard, K. & Krause, K. H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87, 245-313, doi: 10.1152/physrev.00044.2005 (2007).
3. Banfi, B. et al. NOX3, a superoxide-generating NADPH oxidase of the inner ear. J. Biol. Chem. 279, 46065-46072 (2004).
4. Kihara, Y., Maceyka, M., Spiegel, S. & Chun, J. Lysophospholipid receptor nomenclature review: IUPHAR Review 8. Br. J. Pharmacol. 171, 3575-3594, doi: 10.1111/bph.12678 (2014).
5. Pyne, N. J. & Pyne, S. Sphingosine 1-phosphate and cancer. Nat Rev Cancer 10, 489-503, doi: 10.1038/nrc2875 (2010).
6. Choi, J. W. & Chun, J. Lysophospholipids and their receptors in the central nervous system. Biochim. Biophys. Acta 1831, 20-32, doi: 10.1016/j.bbalip.2012.07.015 (2013).
7. Takuwa, N. et al. S1P3-mediated cardiac fibrosis in sphingosine kinase 1 transgenic mice involves reactive oxygen species. Cardiovasc. Res. 85, 484-493, doi: 10.1093/cvr/cvp312 (2010).
8. Keller, M. et al. Sphingosine kinase functionally links elevated transmural pressure and increased reactive oxygen species formation in resistance arteries. FASEB J. 20, 702-704, doi: 10.1096/fj.05-4075fje (2006).
9. Catarzi, S. et al. Sphingosine 1-phosphate stimulation of NADPH oxidase activity: relationship with platelet-derived growth factor receptor and c-Src kinase. Biochim. Biophys. Acta 1770, 872-883, doi: 10.1016/j.bbagen.2007.01.008 (2007).
10. Golan, K. et al. S1P promotes murine progenitor cell egress and mobilization via S1P1-mediated ROS signaling and SDF-1 release. Blood 119, 2478-2488, doi: 10.1182/blood-2011-06-358614 (2012).
11. Liu, Y. et al. Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J. Clin. Invest. 106, 951-961 (2000).
12. Matloubian, M. et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427, 355-360 (2004).
13. Herr, D. R. et al. Sphingosine 1-phosphate receptors are essential mediators of eyelid closure during embryonic development. J. Biol. Chem. 288, 29882-29889, doi: 10.1074/jbc.M113.510099 (2013).
14. Green, J. A. et al. The sphingosine 1-phosphate receptor S1P(2) maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat Immunol 12, 672-680, doi: 10.1038/ni.2047 (2011).
15. Jenne, C. N. et al. T-bet-dependent S1P5 expression in NK cells promotes egress from lymph nodes and bone marrow. J. Exp. Med. 206, 2469-2481, doi: 10.1084/jem.20090525 (2009).
16. Chun, J. & Hartung, H. P. Mechanism of action of oral fingolimod (FTY720) in multiple sclerosis. Clin. neuropharmacol. 33, 91-101, doi: 10.1097/WNF.0b013e3181cbf825 (2010).
17. Chun, J. & Brinkmann, V. A mechanistically novel, first oral therapy for multiple sclerosis: the development of fingolimod (FTY720, Gilenya). Discov. med. 12, 213-228 (2011).
18. Choi, J. W. et al. FTY720 (fingolimod) efficacy in an animal model of multiple sclerosis requires astrocyte sphingosine 1-phosphate receptor 1 (S1P1) modulation. Proc. Natl. Acad. Sci. USA 108, 751-756, doi: 10.1073/pnas.1014154108 (2011).
19. Herr, D. R. et al. Sphingosine 1-phosphate (S1P) signaling is required for maintenance of hair cells mainly via activation of S1P2. J. Neurosci. 27, 1474-1478, doi: 10.1523/JNEUROSCI.4245-06.2007 (2007).
20. Kono, M. et al. Deafness and stria vascularis defects in S1P2 receptor-null mice. J. Biol. Chem. 282, 10690-10696 (2007).
21. MacLennan, A. J. et al. The S1P2 sphingosine 1-phosphate receptor is essential for auditory and vestibular function. Hear Res 220, 38-48, doi: 10.1016/j.heares.2006.06.016 (2006).
22. Chen, J. et al. Spinster homolog 2 (spns2) deficiency causes early onset progressive hearing loss. PLoS genetics 10, e1004688, doi: 10.1371/journal.pgen.1004688 (2014).
23. Mutoh, T., Rivera, R. & Chun, J. Insights into the pharmacological relevance of lysophospholipid receptors. Br. J. Pharmacol. 165, 829-844, doi: 10.1111/j.1476-5381.2011.01622.x (2012).
24. Kim, J. S., Diebold, B. A., Babior, B. M., Knaus, U. G. & Bokoch, G. M. Regulation of Nox1 activity via protein kinase A-mediated phosphorylation of NoxA1 and 14-3-3 binding. J. Biol. Chem. 282, 34787-34800, doi: 10.1074/jbc.M704754200 (2007).
25. Kim, J. S. & Bokoch, G. M. Anthrax edema toxin inhibits Nox1-mediated formation of reactive oxygen species by colon epithelial cells. J Innate Immun 1, 145-152, doi: 10.1159/000151481 (2009).
26. Windh, R. T. et al. Differential coupling of the sphingosine 1-phosphate receptors Edg-1, Edg-3, and H218/Edg-5 to the G(i), G(q), and G(12) families of heterotrimeric G proteins. J. Biol. Chem. 274, 27351-27358 (1999).
27. Satsu, H. et al. A sphingosine 1-phosphate receptor 2 selective allosteric agonist. Bioorg. med. chem. 21, 5373-5382, doi: 10.1016/j. bmc.2013.06.012 (2013).
28. Inoue, A. et al. TGFalpha shedding assay: an accurate and versatile method for detecting GPCR activation. Nat. methods 9, 1021-1029, doi: 10.1038/nmeth.2172 (2012).
29. Osada, M., Yatomi, Y., Ohmori, T., Ikeda, H. & Ozaki, Y. Enhancement of sphingosine 1-phosphate-induced migration of vascular endothelial cells and smooth muscle cells by an EDG-5 antagonist. Biochem. Biophys. Res. Commun. 299, 483-487 (2002).
30. Benda, P., Lightbody, J., Sato, G., Levine, L. & Sweet, W. Differentiated rat glial cell strain in tissue culture. Science 161, 370-371 (1968).
31. Aruoma, O. I., Halliwell, B., Hoey, B. M. & Butler, J. The antioxidant action of N-acetylcysteine: its reaction with hydrogen peroxide, hydroxyl radical, superoxide, and hypochlorous acid. Free radic. biol. med. 6, 593-597 (1989).
32. Bedard, K. & Krause, K. H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiological reviews 87, 245-313, doi: 10.1152/physrev.00044.2005 (2007).
33. Burridge, K. & Wennerberg, K. Rho and Rac take center stage. Cell 116, 167-179 (2004).
34. Harijith, A. et al. Sphingosine kinase 1 deficiency confers protection against hyperoxia-induced bronchopulmonary dysplasia in a murine model: role of S1P signaling and Nox proteins. Am. J. Pathol. 183, 1169-1182, doi: 10.1016/j.ajpath.2013.06.018 (2013).
35. Tolle, M. et al. HDL-associated lysosphingolipids inhibit NAD(P)H oxidase-dependent monocyte chemoattractant protein-1 production. Arterioscler Thromb Vasc Biol 28, 1542-1548, doi: 10.1161/ATVBAHA.107.161042 (2008).
36. Galvani, S. et al. HDL-bound sphingosine 1-phosphate acts as a biased agonist for the endothelial cell receptor S1P1 to limit vascular inflammation. Sci. signal. 8, ra79, doi: 10.1126/scisignal.aaa2581 (2015).
37. Santos-Cortez, R. L. et al. Autosomal-Recessive Hearing Impairment due to Rare Missense Variants within S1PR2. Am. J. Hum. Genet., doi: 10.1016/j.ajhg.2015.12.004 (2016).
38. McKeage, M. J. Comparative adverse effect profiles of platinum drugs. Drug saf. 13, 228-244 (1995).
39. Rybak, L. P., Whitworth, C. A., Mukherjea, D. & Ramkumar, V. Mechanisms of cisplatin-induced ototoxicity and prevention. Hear Res 226, 157-167 (2007).
40. Brock, P. R. et al. Platinum-induced ototoxicity in children: a consensus review on mechanisms, predisposition, and protection, including a new International Society of Pediatric Oncology Boston ototoxicity scale. J. clin. oncol. 30, 2408-2417, doi: 10.1200/JCO.2011.39.1110 (2012).
41. Riga, M. G. et al. Transtympanic injections of N-acetylcysteine for the prevention of cisplatin-induced ototoxicity: a feasible method with promising efficacy. Am. j. clin. oncol. 36, 1-6, doi: 10.1097/COC.0b013e31822e006d (2013).
42. Nishimura, B., Tabuchi, K., Nakamagoe, M. & Hara, A. The influences of sphingolipid metabolites on gentamicin-induced hair cell loss of the rat cochlea. Neurosci. Lett. 485, 1-5, doi: 10.1016/j.neulet.2010.08.014 (2010).
43. Nakayama, M. et al. The influence of sphingosine-1-phosphate receptor antagonists on gentamicin-induced hair cell loss of the rat cochlea. Neurosci. Lett. 561, 91-95, doi: 10.1016/j.neulet.2013.12.063 (2014).
44. Tani, K., Tabuchi, K. & Hara, A. Hair Cell Loss Induced by Sphingosine and a Sphingosine Kinase Inhibitor in the Rat Cochlea. Neurotox. res., doi: 10.1007/s12640-015-9563-7 (2015).
45. Romero-Guevara, R., Cencetti, F., Donati, C. & Bruni, P. Sphingosine 1-phosphate signaling pathway in inner ear biology. New therapeutic strategies for hearing loss? Front. aging neurosci. 7, 60, doi: 10.3389/fnagi.2015.00060 (2015).
46. Scherer, E. Q. et al. Sphingosine-1-phosphate modulates spiral modiolar artery tone: A potential role in vascular-based inner ear pathologies? Cardiovasc. Res. 70, 79-87 (2006).
47. Ishii, I. et al. Marked perinatal lethality and cellular signaling deficits in mice null for the two sphingosine 1-phosphate (S1P) receptors, S1P(2)/LP(B2)/EDG-5 and S1P(3)/LP(B3)/EDG-3. J. Biol. Chem. 277, 25152-25159. Epub 22002 May 25152. (2002).
48. Serrander, L. et al. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem. J. 406, 105-114, doi: 10.1042/BJ20061903 (2007).
49. Bartosz, G. Use of spectroscopic probes for detection of reactive oxygen species. Clin. Chim. Acta 368, 53-76, doi: 10.1016/j. cca.2005.12.039 (2006).
50. Harris, G. L., Creason, M. B., Brulte, G. B. & Herr, D. R. In Vitro and In Vivo Antagonism of a G Protein-Coupled Receptor (S1P3) with a Novel Blocking Monoclonal Antibody. PLoS One 7, e35129, doi: 10.1371/journal.pone.0035129 (2012).
51. Herr, K. J., Herr, D. R., Lee, C. W., Noguchi, K. & Chun, J. Stereotyped fetal brain disorganization is induced by hypoxia and requires lysophosphatidic acid receptor 1 (LPA1) signaling. Proc. Natl. Acad. Sci. USA 108, 15444-15449, doi: 10.1073/pnas.1106129108 (2011).
52. Dubin, A. E., Herr, D. R. & Chun, J. Diversity of lysophosphatidic acid receptor-mediated intracellular calcium signaling in early cortical neurogenesis. J. Neurosci. 30, 7300-7309, doi: 10.1523/JNEUROSCI.6151-09.2010 (2010).