Enhanced sphingosine-1-phosphate receptor 2 expression underlies female CNS autoimmunity susceptibility

Journal of Clinical Investigation

Volumn 124, Issue 6, 2014, Pages 2571-2584

  Cruz Orengo, Lillian ^a   Daniels, Brian P ^a   Dorsey, Denise ^a   Basak, Sarah Alison ^a   Grajales Reyes, José G ^a   McCandless, Erin E ^a   Piccio, Laura ^a   Schmidt, Robert E ^a   Cross, Anne H ^a   Crosby, Seth D ^a   Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2,6 DICHLORO 4 PYRIDINYL) 1 (1,3 DIMETHYL 4 ISOPROPYL 1H PYRAZOLO[3,4 B]PYRIDIN 6 YL)SEMICARBAZIDE; CAVEOLIN; CLAUDIN 5; ESTRADIOL; PROTEIN CDC42; RHO FACTOR; RHO KINASE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR 2; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN;

ACTIVE IMMUNIZATION; ADULT; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; AUTOIMMUNITY; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CONTROLLED STUDY; DISEASE COURSE; DISEASE PREDISPOSITION; DISEASE SEVERITY; ENDOCYTOSIS; FEMALE; GENE EXPRESSION; IMMUNOREACTIVITY; LYMPHOCYTIC INFILTRATION; MALE; MICROARRAY ANALYSIS; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEX DIFFERENCE; SEXUAL MATURITY; SIGNAL TRANSDUCTION; SPINAL CORD; UPREGULATION; WHITE MATTER;

ANIMALS; AUTOIMMUNITY; BLOOD-BRAIN BARRIER; CASE-CONTROL STUDIES; CENTRAL NERVOUS SYSTEM; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; GENE EXPRESSION PROFILING; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MULTIPLE SCLEROSIS; RECEPTORS, LYSOSPHINGOLIPID; SEX CHARACTERISTICS; SPECIES SPECIFICITY;

EID: 84901343151     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI73408     Document Type: Article

References (90)

1. Compston A, Coles A. Multiple sclerosis. Lancet. 2008;372(9648):1502- 1517.
2. Handel AE, Jarvis L, McLaughlin R, Fries A, Ebers GC, Ramagopalan SV. The epidemiology of multiple sclerosis in Scotland: inferences from hospital admissions. PLoS One. 2011;6(1):e14606.
3. Orton SM, et al. Sex ratio of multiple sclerosis in Canada: a longitudinal study. Lancet Neurol. 2006;5(11):932-936.
4. Smith-Bouvier DL, et al. A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med. 2008;205(5):1099-1108.
5. Spence RD, Voskuhl RR. Neuroprotective effects of estrogens and androgens in CNS inflammation and neurodegeneration. Front Neuroendocrinol. 2012;33(1):105-115.
6. Murphy HS, et al. Tissue-specific effect of estradiol on endothelial cell-dependent lymphocyte recruitment. Microvasc Res. 2004;68(3):273-285.
7. Dang J, Mitkari B, Kipp M, Beyer C. Gonadal steroids prevent cell damage and stimulate behavioral recovery after transient middle cerebral artery occlusion in male and female rats. Brain Behav Immun. 2011;25(4):715-726.
8. Burek M, Arias-Loza PA, Roewer N, Forster CY. Claudin-5 as a novel estrogen target in vascular endothelium. Arterioscler Thromb Vasc Biol. 2010;30(2):298-304.
9. Chi OZ, Barsoum S, Wen Y, Liu X, Weiss HR. 17β-estradiol prevents blood-brain barrier disruption induced by VEGF. Horm Metab Res. 2004;36(5):272-276.
10. Mochizuki N. Vascular integrity mediated by vascular endothelial cadherin and regulated by sphingosine 1-phosphate and angiopoietin-1. Circ J. 2009;73(12):2183-2191.
11. Green KJ, Getsios S, Troyanovsky S, Godsel LM. Intercellular junction assembly, dynamics, and homeostasis. Cold Spring Harb Perspect Biol. 2010;2(2):a000125.
12. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol. 2010;72:463-493.
13. Song L, Ge S, Pachter JS. Caveolin-1 regulates expression of junction-associated proteins in brain microvascular endothelial cells. Blood. 2007;109(4):1515-1523.
14. Lampugnani MG, et al. CCM1 regulates vascular-lumen organization by inducing endothelial polarity. J Cell Sci. 2010;123(pt 7):1073-1080.
15. Minagar A, et al. Serum from patients with multiple sclerosis downregulates occludin and VE-cadherin expression in cultured endothelial cells. Mult Scler. 2003;9(3):235-238.
16. Shen W, et al. Tyrosine phosphorylation of VE-cadherin and claudin-5 is associated with TGF-β1-induced permeability of centrally derived vascular endothelium. Eur J Cell Biol. 2011;90(4):323-332.
17. Bode C, et al. Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J Cell Biochem. 2010;109(6):1232-1243.
18. Callihan P, Hooks SB. Sphingosine-1-phosphate signaling in neural progenitors. Methods Mol Biol. 2012;874:193-200.
19. Hla T, Brinkmann V. Sphingosine 1-phosphate (S1P): Physiology and the effects of S1P receptor modulation. Neurology. 2011;76(S1P):S3-S8.
20. Garcia JG, et al. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest. 2001;108(5):689-701.
21. Lee MJ, et al. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell. 1999;99(3):301-312.
22. Sanchez T, et al. Phosphorylation and action of the immunomodulator FTY720 inhibits vascular endothelial cell growth factor-induced vascular permeability. J Biol Chem. 2003;278(47):47281-47290.
23. Lee MJ, et al. Akt-mediated phosphorylation of the G protein-coupled receptor EDG-1 is required for endothelial cell chemotaxis. Mol Cell. 2001;8(3):693-704.
24. Cohen JA, Chun J. Mechanisms of fingolimod's efficacy and adverse effects in multiple sclerosis. Ann Neurol. 2011;69(5):759-777.
25. Kageyama Y, et al. Antagonism of sphingosine 1-phosphate receptor 2 causes a selective reduction of portal vein pressure in bile duct-ligated rodents. Hepatology. 2012;56(4):1427-1438.
26. Skoura A, et al. Sphingosine-1-phosphate receptor-2 function in myeloid cells regulates vascular inflammation and atherosclerosis. Arterioscler Thromb Vasc Biol. 2011;31(1):81-85.
27. Zhang G, et al. Critical role of sphingosine-1-phosphate receptor 2 (S1PR2) in acute vascular inflammation. Blood. 2013;122(3):443-455.
28. Skoura A, Sanchez T, Claffey K, Mandala SM, Proia RL, Hla T. Essential role of sphingosine 1-phosphate receptor 2 in pathological angiogenesis of the mouse retina. J Clin Invest. 2007;117(9):2506-2516.
29. Sanchez T, Skoura A, Wu MT, Casserly B, Harrington EO, Hla T. Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arterioscler Thromb Vasc Biol. 2007;27(6):1312-1318.
30. Cruz-Orengo L, et al. CXCR7 influences leukocyte entry into the CNS parenchyma by controlling abluminal CXCL12 abundance during autoimmunity. J Exp Med. 2011;208(2):327-339.
31. McCandless EE, et al. Pathological expression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am J Pathol. 2008;172(3):799-808.
32. McCandless EE, Wang Q, Woerner BM, Harper JM, Klein RS. CXCL12 limits inflammation by localizing mononuclear infiltrates to the perivascular space during experimental autoimmune encephalomyelitis. J Immunol. 2006;177(11):8053-8064.
33. Papenfuss TL, et al. Sex differences in experimental autoimmune encephalomyelitis in multiple murine strains. J Neuroimmunol. 2004;150(1-2):59-69.
34. Kingo K, et al. Association analysis of IL20RA and IL20RB genes in psoriasis. Genes Immun. 2008;9(5):445-451.
35. Kingo K, et al. Association analysis of genes of the IL19 cluster and their receptors in vitiligo patients. Dermatology. 2010;221(3):261-266.
36. Reimann E, et al. The mRNA expression profile of cytokines connected to the regulation of melanocyte functioning in vitiligo skin biopsy samples and peripheral blood mononuclear cells. Hum Immunol. 2012;73(4):393-398.
37. Wahl C, et al. IL-20 receptor 2 signaling down-regulates antigen-specific T cell responses. J Immunol. 2009;182(2):802-810.
38. Ikeda H, et al. Sphingosine 1-phosphate enhances portal pressure in isolated perfused liver via S1P2 with Rho activation. Biochem Biophys Res Commun. 2004;320(3):754-759.
39. Inoki I, et al. Negative regulation of endothelial morphogenesis and angiogenesis by S1P2 receptor. Biochem Biophys Res Commun. 2006;346(1):293-300.
40. Spach KM, et al. Cutting edge: the Y chromosome controls the age-dependent experimental allergic encephalomyelitis sexual dimorphism in SJL/J mice. J Immunol. 2009;182(4):1789-1793.
41. Subramanian S, Matejuk A, Zamora A, Vandenbark AA, Offner H. Oral feeding with ethinyl estradiol suppresses and treats experimental autoimmune encephalomyelitis in SJL mice and inhibits the recruitment of inflammatory cells into the central nervous system. J Immunol. 2003;170(3):1548-1555.
42. Elloso MM, Phiel K, Henderson RA, Harris HA, Adelman SJ. Suppression of experimental autoimmune encephalomyelitis using estrogen receptorselective ligands. J Endocrinol. 2005;185(2):243-252.
43. Fillmore PD, Blankenhorn EP, Zachary JF, Teuscher C. Adult gonadal hormones selectively regulate sexually dimorphic quantitative traits observed in experimental allergic encephalomyelitis. Am J Pathol. 2004;164(1):167-175.
44. Smith-Bouvier DL, et al. A role for sex chromosome complement in the female bias in autoimmune disease. J Exp Med. 2008;205(5):1099-1108.
45. Wu WF, Tan XJ, Dai YB, Krishnan V, Warner M, Gustafsson JA. Targeting estrogen receptor beta in microglia and T cells to treat experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A. 2013;110(9):3543-3548.
46. Loh KC, et al. Sphingosine-1-phosphate enhances satellite cell activation in dystrophic muscles through a S1PR2/STAT3 signaling pathway. PLoS One. 2012;7(5):e37218.
47. Daniels BP, et al. Immortalized human cerebral microvascular endothelial cells maintain the properties of primary cells in an in vitro model of immune migration across the blood brain barrier. J Neurosci Methods. 2013;212(1):173-179.
48. McCandless EE, Zhang B, Diamond MS, Klein RS. CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proc Natl Acad Sci U S A. 2008;105(32):11270-11275.
49. El-Etr M, Ghoumari A, Sitruk-Ware R, Schumacher M. Hormonal influences in multiple sclerosis: new therapeutic benefits for steroids. Maturitas. 2011;68(1):47-51.
50. Amur S, Parekh A, Mummaneni P. Sex differences and genomics in autoimmune diseases. J Autoimmun. 2012;38(2-3):J254-J265.
51. Badawi AH, Siahaan TJ. Immune modulating peptides for the treatment and suppression of multiple sclerosis. Clin Immunol. 2012;144(2):127-138.
52. Gasperini C, Ruggieri S. Development of oral agent in the treatment of multiple sclerosis: how the first available oral therapy, fingolimod will change therapeutic paradigm approach. Drug Des Devel Ther. 2012;6:175-186.
53. Ferenczy MW, et al. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clin Microbiol Rev. 2012;25(3):471-506.
54. Ghosh S. Biologic therapies: lessons from multiple sclerosis. Dig Dis. 2012;30(4):383-386.
55. Green JA, et al. The sphingosine 1-phosphate receptor S1P (2) maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat Immunol. 2011;12(7):672-680.
56. Cohen JA, Chun J. Mechanisms of fingolimod's efficacy and adverse effects in multiple sclerosis. Ann Neurol. 2011;69(5):759-777.
57. Schwarz A, Korporal M, Hosch W, Max R, Wildemann B. Critical vasospasm during fingolimod (FTY720) treatment in a patient with multiple sclerosis. Neurology. 2010;74(24):2022-2024.
58. Jeffery DR, Markowitz CE, Reder AT, Weinstock-Guttman B, Tobias K. Fingolimod for the treatment of relapsing multiple sclerosis. Expert Rev Neurother. 2011;11(2):165-183.
59. Tolle M, et al. Immunomodulator FTY720 induces eNOS-dependent arterial vasodilatation via the lysophospholipid receptor S1P3. Circ Res. 2005;96(8):913-920.
60. Cohen D. NICE rules out NHS prescription of fingolimod for multiple sclerosis. BMJ. 2011;343:d5117.
61. Doggrell SA. Oral fingolimod for relapsing-remitting multiple sclerosis Evaluation of: Kappos L, Radue E-M, O'Connor P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med. 2010;362:387-401;
62. and Cohen JA, Barkhof F, Comi G, et al. Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med. 2010;362:402-15.
63. Expert Opin Pharmacother. 2010;11(10):1777-1781.
64. Portaccio E. Evidence-based assessment of potential use of fingolimod in treatment of relapsing multiple sclerosis. Core Evid. 2011;6:13-21.
65. Camerer E, et al. Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. J Clin Invest. 2009;119(7):1871-1879.
66. Singleton PA, Dudek SM, Chiang ET, Garcia JG. Regulation of sphingosine 1-phosphate-induced endothelial cytoskeletal rearrangement and barrier enhancement by S1P1 receptor, PI3 kinase, Tiam1/Rac1, anda-actinin. FASEB J. 2005;19(12):1646-1656.
67. Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci. 2001;114(pt 7):1343-1355.
68. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature. 2002;420(6916):629-635.
69. Wilkinson S, Paterson HF, Marshall CJ. Cdc42-M-RCK and Rho-ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat Cell Biol. 2005;7(3):255-261.
70. Shen L, Turner JR Actin depolymerization disrupts tight junctions via caveolae-mediated endocytosis. Mol Biol Cell. 2005;16(9):3919-3936.
71. Lu Z, Ghosh S, Wang Z, Hunter T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of p-catenin, and enhanced tumor cell invasion. Cancer Cell. 2003;4(6):499-515.
72. Minagar A, et al. Interferon (IFN)-beta 1a and IFN-beta 1b block IFN-y-induced disintegration of endothelial junction integrity and barrier. Endothelium. 2003;10(6):299-307.
73. Park SW, Kim M, Brown KM, D'Agati VD, Lee HT Inhibition of sphingosine 1-phosphate receptor 2 protects against renal ischemia-reperfusion injury. J Am Soc Nephrol. 2012;23(2):266-280.
74. Sanchez T, Skoura A, Wu MT, Casserly B, Harrington EO, Hla T. Induction of vascular permeability by the sphingosine-1-phosphate receptor-2 (S1P2R) and its downstream effectors ROCK and PTEN. Arterioscler Thromb Vasc Biol. 2007;27(6):1312-1318.
75. Armulik A, et al. Pericytes regulate the blood-brain barrier. Nature. 2010;468(7323):557-561.
76. Bell RD, et al. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron. 2010;68(3):409-427.
77. Bell RD, et al. Apolipoprotein E controls cerebrovascular integrity via cyclophilin A. Nature. 2012;485(7399):512-516.
78. Daneman R, Zhou L, Kebede AA, Barres BA. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature. 2010;468(7323):562- 566.
79. Japtok L, Schaper K, Baumer W, Radeke HH, Jeong SK, Kleuser B. Sphingosine 1-phosphate modulates antigen capture by murine Langerhans cells via the S1P2 receptor subtype. PLoS One. 2012;7(11):e49427.
80. McQuiston T, Luberto C, Del Poeta M. Role of sphingosine-1-phosphate (S1P) and S1P receptor 2 in the phagocytosis of Cryptococcus neoformans by alveolar macrophages. Microbiology. 2011;157(pt 5):1416-1427.
81. Green JA, Cyster JG. S1PR2 links germinal center confinement and growth regulation. Immunol Rev. 2012;247(1):36-51.
82. Green JA, et al. The sphingosine 1-phosphate receptor S1P maintains the homeostasis of germinal center B cells and promotes niche confinement. Nat Immunol. 2011;12(7):672-680.
83. Oskeritzian CA, et al. Essential roles of sphingosine-1-phosphate receptor 2 in human mast cell activation, anaphylaxis, and pulmonary edema. J Exp Med. 2010;207(3):465-474.
84. Trifilieff A, Fozard JR. Sphingosine-1-phosphate-induced airway hyper-reactivity in rodents is mediated by the sphingosine-1-phosphate type 3 receptor. J Pharmacol Exp Ther. 2012;342(2):399-406.
85. Secor VH, Secor WE, Gutekunst CA, Brown MA. Mast cells are essential for early onset and severe disease in a murine model of multiple sclerosis. J Exp Med. 2000;191(5):813-822.
86. McCandless EE, Budde M, Lees JR, Dorsey D, Lyng E, Klein RS. IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis. J Immunol. 2009;183(1):613-620.
87. Kono M, et al. Deafness and stria vascularis defects in S1P2 receptor-null mice. J Biol Chem. 2007;282(14):10690-10696.
88. + T-cell recruitment and control of West Nile virus encephalitis. J Virol. 2005;79(17):11457-11466.
89. Edsbagge J, Johansson JK, Esni F, Luo Y, Radice GL, Semb H. Vascular function and sphingosine-1-phosphate regulate development of the dorsal pancreatic mesenchyme. Development. 2005;132(5):1085-1092.
90. Weksler BB, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005;19(13):1872-1874. Stroke