Genetic evidence for involvement of neuronally expressed s1P1 receptor in nociceptor sensitization and inflammatory pain

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Mair, Norbert ^a   Benetti, Camilla ^a   Andratsch, Manfred ^a   Leitner, Michael G ^a   Constantin, Cristina E ^a   Camprubí Robles, Maria ^a   Quarta, Serena ^a   Biasio, Wolfgang ^a   Kuner, Rohini ^b   Gibbins, Ian L ^c   Kress, Michaela ^a   Haberberger, Rainer V ^c  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c FLINDERS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

5 (4 PHENYL 5 TRIFLUOROMETHYL 2 THIENYL) 3 (3 TRIFLUOROMETHYLPHENYL) 1,2,4 OXADIAZOLE; CAPSAICIN; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; VANILLOID RECEPTOR 1; DRUG DERIVATIVE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTACT SENSITIZATION; CONTROLLED STUDY; GENETIC ANALYSIS; HEAT SENSITIVITY; HYPERALGESIA; HYPERSENSITIVITY; INFLAMMATION; MALE; MOUSE; NOCICEPTION; NOCICEPTIVE RECEPTOR; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; THERMAL STIMULATION; ANIMAL; C57BL MOUSE; GENETICS; HEAT; INNERVATION; METABOLISM; MOUSE MUTANT; PAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; SENSORY RECEPTOR; SKIN;

MUS;

ANIMALS; HOT TEMPERATURE; HYPERALGESIA; INFLAMMATION; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NOCICEPTORS; PAIN; RECEPTORS, LYSOSPHINGOLIPID; SENSORY RECEPTOR CELLS; SIGNAL TRANSDUCTION; SKIN; SPHINGOSINE;

EID: 79951922162     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017268     Document Type: Article

References (63)

1. Hannun YA, Obeid LM, (2008) Principles of bioactive lipid signalling: lessons from sphingolipids. Nat Rev Mol Cell Biol 9: 139-150.
2. Kitano M, Hla T, Sekiguchi M, Kawahito Y, Yoshimura R, et al. (2006) Sphingosine 1-phosphate/sphingosine 1-phosphate receptor 1 signaling in rheumatoid synovium: regulation of synovial proliferation and inflammatory gene expression. Arthritis Rheum 54: 742-753.
3. Park KA, Vasko MR, (2005) Lipid mediators of sensitivity in sensory neurons. Trends Pharmacol Sci 26: 571-577.
4. Rivera J, Proia RL, Olivera A, (2008) The alliance of sphingosine-1-phosphate and its receptors in immunity. Nat Rev Immunol 8: 753-763.
5. Alvarez SE, Milstien S, Spiegel S, (2007) Autocrine and paracrine roles of sphingosine-1-phosphate. Trends Endocrinol Metab 18: 300-307.
6. Mitra P, Oskeritzian CA, Payne SG, Beaven MA, Milstien S, et al. (2006) Role of ABCC1 in export of sphingosine-1-phosphate from mast cells. Proc Natl Acad Sci U S A 103: 16394-16399.
7. Takabe K, Paugh SW, Milstien S, Spiegel S, (2008) "Inside-out" signaling of sphingosine-1-phosphate: therapeutic targets. Pharmacol Rev 60: 181-195.
8. Spiegel S, Milstien S, (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat Rev Mol Cell Biol 4: 397-407.
9. van Echten-Deckert G, Herget T, (2006) Sphingolipid metabolism in neural cells. Biochim Biophys Acta 1758: 1978-1994.
10. Alemany R, van Koppen CJ, Danneberg K, Ter BM, Meyer Zu HD, (2007) Regulation and functional roles of sphingosine kinases. Naunyn Schmiedebergs Arch Pharmacol 374: 413-428.
11. Maceyka M, Payne SG, Milstien S, Spiegel S, (2002) Sphingosine kinase, sphingosine-1-phosphate, and apoptosis. Biochim Biophys Acta 1585: 193-201.
12. Taha TA, Hannun YA, Obeid LM, (2006) Sphingosine kinase: biochemical and cellular regulation and role in disease. J Biochem Mol Biol 39: 113-131.
13. Bandhuvula P, Saba JD, (2007) Sphingosine-1-phosphate lyase in immunity and cancer: silencing the siren. Trends Mol Med 13: 210-217.
14. Le SH, Milstien S, Spiegel S, (2004) Generation and metabolism of bioactive sphingosine-1-phosphate. J Cell Biochem 92: 882-899.
15. Pyne S, Pyne NJ, (2000) Sphingosine 1-phosphate signalling in mammalian cells. Biochem J 349: 385-402.
16. Mizugishi K, Yamashita T, Olivera A, Miller GF, Spiegel S, et al. (2005) Essential role for sphingosine kinases in neural and vascular development. Mol Cell Biol 25: 11113-11121.
17. Zhang YH, Vasko MR, Nicol GD, (2006) Intracellular sphingosine 1-phosphate mediates the increased excitability produced by nerve growth factor in rat sensory neurons. J Physiol 575: 101-113.
18. Murata N, Sato K, Kon J, Tomura H, Yanagita M, et al. (2000) Interaction of sphingosine 1-phosphate with plasma components, including lipoproteins, regulates the lipid receptor-mediated actions. Biochem J 352 (Pt 3): 809-815.
19. Ohkawa R, Nakamura K, Okubo S, Hosogaya S, Ozaki Y, et al. (2008) Plasma sphingosine-1-phosphate measurement in healthy subjects: close correlation with red blood cell parameters. Ann Clin Biochem 45: 356-363.
20. Schmidt H, Schmidt R, Geisslinger G, (2006) LC-MS/MS-analysis of sphingosine-1-phosphate and related compounds in plasma samples. Prostaglandins Other Lipid Mediat 81: 162-170.
21. Lai WQ, Irwan AW, Goh HH, Howe HS, Yu DT, et al. (2008) Anti-inflammatory effects of sphingosine kinase modulation in inflammatory arthritis. J Immunol 181: 8010-8017.
22. Hammad SM, Crellin HG, Wu BX, Melton J, Anelli V, et al. (2008) Dual and distinct roles for sphingosine kinase 1 and sphingosine 1 phosphate in the response to inflammatory stimuli in RAW macrophages. Prostaglandins Other Lipid Mediat 85: 107-114.
23. Bourgoin SG, Zhao C, (2010) Autotaxin and lysophospholipids in rheumatoid arthritis. Curr Opin Investig Drugs 11: 515-526.
24. Hagen KB, Kvien TK, Bjorndal A, (1997) Musculoskeletal pain and quality of life in patients with noninflammatory joint pain compared to rheumatoid arthritis: a population survey. J Rheumatol 24: 1703-1709.
25. Saravanan V, Hamilton J, (2002) Advances in the treatment of rheumatoid arthritis: old versus new therapies. Expert Opin Pharmacother 3: 845-856.
26. Smolen JS, Aletaha D, Koeller M, Weisman MH, Emery P, (2007) New therapies for treatment of rheumatoid arthritis. Lancet 370: 1861-1874.
27. Tsunemi S, Iwasaki T, Kitano S, Imado T, Miyazawa K, et al. (2010) Effects of the novel immunosuppressant FTY720 in a murine rheumatoid arthritis model. Clin Immunol 136: 197-204.
28. Graler MH, (2010) Targeting sphingosine 1-phosphate (S1P) levels and S1P receptor functions for therapeutic immune interventions. Cell Physiol Biochem 26: 79-86.
29. Ishii M, Egen JG, Klauschen F, Meier-Schellersheim M, Saeki Y, et al. (2009) Sphingosine-1-phosphate mobilizes osteoclast precursors and regulates bone homeostasis. Nature 458: 524-528.
30. Hargreaves K, Dubner R, Brown F, Flores C, Joris J, (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88.
31. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, et al. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824.
32. Coste O, Brenneis C, Linke B, Pierre S, Maeurer C, et al. (2008) Sphingosine 1-phosphate modulates spinal nociceptive processing. J Biol Chem 283: 32442-32451.
33. Meng H, Lee VM, (2009) Differential expression of sphingosine-1-phosphate receptors 1-5 in the developing nervous system. Dev Dyn 238: 487-500.
34. Siehler S, Manning DR, (2002) Pathways of transduction engaged by sphingosine 1-phosphate through G protein-coupled receptors. Biochim Biophys Acta 1582: 94-99.
35. Zhang YH, Fehrenbacher JC, Vasko MR, Nicol GD, (2006) Sphingosine-1-phosphate via activation of a G-protein-coupled receptor(s) enhances the excitability of rat sensory neurons. J Neurophysiol 96: 1042-1052.
36. Scholz J, Woolf CJ, (2007) The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10: 1361-1368.
37. Rivera R, Chun J, (2008) Biological effects of lysophospholipids. Rev Physiol Biochem Pharmacol 160: 25-46.
38. Goldstein ME, House SB, Gainer H, (1991) NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J Neurosci Res 30: 92-104.
39. Hunt SP, Mantyh PW, (2001) The molecular dynamics of pain control. Nat Rev Neurosci 2: 83-91.
40. Jo E, Sanna MG, Gonzalez-Cabrera PJ, Thangada S, Tigyi G, Osborne DA, et al. (2005) S1P1-selective in vivo-active agonists from high-throughput screening: off-the-shelf chemical probes of receptor interactions, signaling, and fate. Chem Biol 12: 703-715.
41. Liu Y, Wada R, Yamashita T, Mi Y, Deng CX, et al. (2000) Edg-1, the G protein-coupled receptor for sphingosine-1-phosphate, is essential for vascular maturation. J Clin Invest 106: 951-961.
42. Allende ML, Yamashita T, Proia RL, (2003) G-protein-coupled receptor S1P1 acts within endothelial cells to regulate vascular maturation. Blood 102: 3665-3667.
43. Agarwal N, Offermanns S, Kuner R, (2004) Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 38: 122-129.
44. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, et al. (2007) Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10: 870-879.
45. Andratsch M, Mair N, Constantin CE, Scherbakov N, Benetti C, et al. (2009) A key role for gp130 expressed on peripheral sensory nerves in pathological pain. J Neurosci 29: 13473-13483.
46. Deng Q, Clemas JA, Chrebet G, Fischer P, Hale JJ, et al. (2007) Identification of Leu276 of the S1P1 receptor and Phe263 of the S1P3 receptor in interaction with receptor specific agonists by molecular modeling, site-directed mutagenesis, and affinity studies. Mol Pharmacol 71: 724-735.
47. Lindfors PH, Voikar V, Rossi J, Airaksinen MS, (2006) Deficient nonpeptidergic epidermis innervation and reduced inflammatory pain in glial cell line-derived neurotrophic factor family receptor alpha2 knock-out mice. J Neurosci 26: 1953-1960.
48. Breese NM, George AC, Pauers LE, Stucky CL, (2005) Peripheral inflammation selectively increases TRPV1 function in IB4-positive sensory neurons from adult mouse. Pain 115: 37-49.
49. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, et al. (2009) Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci U S A 106: 9075-9080.
50. Zwick M, Davis BM, Woodbury CJ, Burkett JN, Koerber HR, et al. (2002) Glial cell line-derived neurotrophic factor is a survival factor for isolectin B4-positive, but not vanilloid receptor 1-positive, neurons in the mouse. J Neurosci 22: 4057-4065.
51. Dirajlal S, Pauers LE, Stucky CL, (2003) Differential response properties of IB(4)-positive and-negative unmyelinated sensory neurons to protons and capsaicin. J Neurophysiol 89: 513-524.
52. Braz JM, Basbaum AI, (2010) Differential ATF3 expression in dorsal root ganglion neurons reveals the profile of primary afferents engaged by diverse noxious chemical stimuli. Pain 150: 290-301.
53. Coste O, Pierre S, Marian C, Brenneis C, Angioni C, et al. (2008) Antinociceptive activity of the S1P-receptor agonist FTY720. J Cell Mol Med 12: 995-1004.
54. Pernia-Andrade AJ, Kato A, Witschi R, Nyilas R, Katona I, et al. (2009) Spinal endocannabinoids and CB1 receptors mediate C-fiber-induced heterosynaptic pain sensitization. Science 325: 760-764.
55. Koltzenburg M, Stucky CL, Lewin GR, (1997) Receptive properties of mouse sensory neurons innervating hairy skin. J Neurophysiol 78: 1841-1850.
56. Kress M, Koltzenburg M, Reeh PW, Handwerker HO, (1992) Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68: 581-595.
57. Forster C, Handwerker HO, (1990) Automatic classification and analysis of microneurographic spike data using a PC/AT. J Neurosci Methods 31: 109-118.
58. Obreja O, Rathee PK, Lips KS, Distler C, Kress M, (2002) IL-1 beta potentiates heat-activated currents in rat sensory neurons: involvement of IL-1RI, tyrosine kinase, and protein kinase C. FASEB J 16: 1497-1503.
59. Obreja O, Biasio W, Andratsch M, Lips KS, Rathee PK, et al. (2005) Fast modulation of heat-activated ionic current by proinflammatory interleukin 6 in rat sensory neurons. Brain 128: 1634-1641.
60. Dittert I, Vlachova V, Knotkova H, Vitaskova Z, Vyklicky L, et al. (1998) A technique for fast application of heated solutions of different composition to cultured neurones. J Neurosci Methods 82: 195-201.
61. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
62. Vandesompele J, De PK, Pattyn F, Poppe B, Van RN, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
63. Linhart O, Obreja O, Kress M, (2003) The inflammatory mediators serotonin, prostaglandin E2 and bradykinin evoke calcium influx in rat sensory neurons. Neuroscience 118: 69-74.