Bitopic Sphingosine 1-Phosphate Receptor 3 (S1P3) Antagonist Rescue from complete heart block: Pharmacological and genetic evidence for direct s1p3 regulation of mouse cardiac conduction

Molecular Pharmacology

Volumn 89, Issue 1, 2016, Pages 176-186

  Germana Sanna, M ^a   Vincent, Kevin P ^b   Repetto, Emanuela ^a   Nguyen, Nhan ^a   Brown, Steven J ^c   Abgaryan, Lusine ^c   Riley, Sean W ^c   Leaf, Nora B ^a   Cahalan, Stuart M ^b   Kiosses, William B ^f   Kohno, Yasushi ^d   Brown, Joan Heller ^f   McCulloch, Andrew D ^e   Rosen, Hugh ^a   Gonzalez Cabrera, Pedro J ^a  

^a San Diego   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c Scripps Research Institute Molecular Screening Center ^*  (United States)

^d KYORIN PHARMACEUTICAL CO LTD   (Japan)

^e Departments of Bioengineering   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOTONIC AGENT; EDG3 PROTEIN, MOUSE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; GENETICS; HEART BLOCK; HEART RATE; KNOCKOUT MOUSE; MALE; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CARDIOTONIC AGENTS; HEART BLOCK; HEART RATE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, LYSOSPHINGOLIPID;

EID: 84958180166     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.115.100222     Document Type: Article

References (44)

1. Bandhuvula P, Tam YY, Oskouian B, and Saba JD (2005) The immune modulator FTY720 inhibits sphingosine-1-phosphate lyase activity. J Biol Chem 280: 33697-33700.
2. Baruscotti M, Bucchi A, Viscomi C, Mandelli G, Consalez G, Gnecchi-Rusconi T, Montano N, Casali KR, Micheloni S, and Barbuti A et al. (2011) Deep bradycardia and heart block caused by inducible cardiac-specific knockout of the pacemaker channel gene Hcn4. Proc Natl Acad Sci USA 108:1705-1710.
3. Boukens BJ, Rivaud MR, Rentschler S, and Coronel R (2014) Misinterpretation of the mouse ECG: 'musing the waves of Mus musculus'. J Physiol 592:4613-4626.
4. Bunemann M, Brandts B, zu Heringdorf DM, van Koppen CJ, Jakobs KH, and Pott L (1995) Activation of muscarinic K1 current in guinea-pig atrial myocytes by sphingosine-1-phosphate. J Physiol 489:701-777
5. Cahalan SM, Gonzalez-Cabrera PJ, Sarkisyan G, Nguyen N, Schaeffer MT, Huang L, Yeager A, Clemons B, Scott F, and Rosen H (2011) Actions of a picomolar shortacting S1P agonist in S1P-eGFP knock-in mice. Nat Chem Biol 7:254-256.
6. Chu DK, Jordan MC, Kim JK, Couto MA, and Roos KP (2006) Comparing isoflurane with tribromoethanol anesthesia for echocardiographic phenotyping of transgenic mice. J Am Assoc Lab Anim Sci 45:8-13.
7. Cohen JA, Barkhof F, Comi G, Hartung HP, Khatri BO, Montalban X, Pelletier J, Capra R, Gallo P, and Izquierdo G et al.; TRANSFORMS Study Group (2010) Oral fingolimod or intramuscular interferon for relapsing multiple sclerosis. N Engl J Med 362:402-415.
8. Egom EE, Kruzliak P, Rotrekl V, and Lei M (2015) The effect of the sphingosine-1-phosphate analogue FTY720 on atrioventricular nodal tissue. J Cell Mol Med 19: 1729-1734.
9. Espinosa PS and Berger JR (2011) Delayed fingolimod-Associated asystole. Mult Scler 17:1387-1389.
10. Forrest M, Sun SY, Hajdu R, Bergstrom J, Card D, Doherty G, Hale J, Keohane C, Meyers C, and Milligan J et al. (2004) Immune cell regulation and cardiovascular effects of sphingosine 1-phosphate receptor agonists in rodents are mediated via distinct receptor subtypes. J Pharmacol Exp Ther 309:758-768.
11. Fryer RM, Muthukumarana A, Harrison PC, Nodop Mazurek S, Chen RR, Harrington KE, Dinallo RM, Horan JC, Patnaude L, and Modis LK et al. (2012) The clinically-Tested S1P receptor agonists, FTY720 and BAF312, demonstrate subtype-specific bradycardia (S1P) and hypertension (S1P) in rat. PLoS One 7: e52985.
12. Gonzalez-Cabrera PJ, Cahalan SM, Nguyen N, Sarkisyan G, Leaf NB, Cameron MD, Kago T, and Rosen H (2012) S1P(1) receptor modulation with cyclical recovery from lymphopenia ameliorates mouse model of multiple sclerosis. Mol Pharmacol 81: 166-174.
13. Gonzalez-Cabrera PJ, Jo E, Sanna MG, Brown S, Leaf N, Marsolais D, Schaeffer MT, Chapman J, Cameron M, and Guerrero M et al. (2008) Full pharmacological efficacy of a novel S1P1 agonist that does not require S1P-like headgroup interactions. Mol Pharmacol 74:1308-1318.
14. Guo J, MacDonell KL, and Giles WR (1999) Effects of sphingosine 1-phosphate on pacemaker activity in rabbit sino-Atrial node cells. Pflugers Arch 438:642-648.
15. Hanson MA, Roth CB, Jo E, Griffith MT, Scott FL, Reinhart G, Desale H, Clemons B, Cahalan SM, and Schuerer SC et al. (2012) Crystal structure of a lipid G proteincoupled receptor. Science 335:851-855.
16. Harzheim D, Pfeiffer KH, Fabritz L, Kremmer E, Buch T, Waisman A, Kirchhof P, Kaupp UB, and Seifert R (2008) Cardiac pacemaker function of HCN4 channels in mice is confined to embryonic development and requires cyclic AMP. EMBO J 27: 692-703.
17. Ishii I, Friedman B, Ye X, Kawamura S, McGiffert C, Contos JJ, Kingsbury MA, Zhang G, Brown JH, and Chun J (2001) Selective loss of sphingosine 1-phosphate signaling with no obvious phenotypic abnormality in mice lacking its G proteincoupled receptor, LP(B3)/EDG-3. J Biol Chem 276:33697-33704.
18. Jo E, Bhhatarai B, Repetto E, Guerrero M, Riley S, Brown SJ, Kohno Y, Roberts E, Schörer SC, and Rosen H (2012) Novel selective allosteric and bitopic ligands for the S1P(3) receptor. ACS Chem Biol 7:1975-1983.
19. Kappos L, Radue EW, O'Connor P, Polman C, Hohlfeld R, Calabresi P, Selmaj K, Agoropoulou C, Leyk M, and Zhang-Auberson L et al.; FREEDOMS Study Group (2010) A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 362:387-401.
20. Kovarik JM, Slade A, Riviere GJ, Neddermann D, Maton S, Hunt TL, and Schmouder RL (2008) The ability of atropine to prevent and reverse the negative chronotropic effect of fingolimod in healthy subjects. Br J Clin Pharmacol 66:199-206.
21. Kuratomi S, Ohmori Y, Ito M, Shimazaki K, Muramatsu S, Mizukami H, Uosaki H, Yamashita JK, Arai Y, and Kuwahara K et al. (2009) The cardiac pacemakerspecific channel Hcn4 is a direct transcriptional target of MEF2. Cardiovasc Res 83:682-687.
22. Legangneux E, Gardin A, and Johns D (2013) Dose titration of BAF312 attenuates the initial heart rate reducing effect in healthy subjects. Br J Clin Pharmacol 75: 831-841.
23. Liao R, Podesser BK, and Lim CC (2012) The continuing evolution of the Langendorff and ejecting murine heart: new advances in cardiac phenotyping. Am J Physiol Heart Circ Physiol 303:H156-H167.
24. Mazurais D, Robert P, Gout B, Berrebi-Bertrand I, Laville MP, and Calmels T (2002) Cell type-specific localization of human cardiac S1P receptors. J Histochem Cytochem 50:661-670.
25. Mendelson K, Evans T, and Hla T (2014) Sphingosine 1-phosphate signalling. Development 141:5-9.
26. Meng H and Lee VM (2009) Differential expression of sphingosine-1-phosphate receptors 1-5 in the developing nervous system. Dev Dyn 238:487-500.
27. Murakami A, Takasugi H, Ohnuma S, Koide Y, Sakurai A, Takeda S, Hasegawa T, Sasamori J, Konno T, and Hayashi K et al. (2010) Sphingosine 1-phosphate (S1P) regulates vascular contraction via S1P3 receptor: investigation based on a new S1P3 receptor antagonist. Mol Pharmacol 77:704-713.
28. Parrill AL, Wang D, Bautista DL, Van Brocklyn JR, Lorincz Z, Fischer DJ, Baker DL, Liliom K, Spiegel S, and Tigyi G (2000) Identification of Edg1 receptor residues that recognize sphingosine 1-phosphate. J Biol Chem275:39379-39384.
29. Qin X, Yue Z, Sun B, Yang W, Xie J, Ni E, Feng Y, Mahmood R, Zhang Y, and Yue L (2013) Sphingosine and FTY720 are potent inhibitors of the transient receptor potential melastatin 7 (TRPM7) channels. Br J Pharmacol 168:1294-1312.
30. Rosen H, Stevens RC, Hanson M, Roberts E, and Oldstone MBA (2013) Sphingosine-1-phosphate and its receptors: structure, signaling, and influence. Annu Rev Biochem 82:637-662.
31. Roth DM, Swaney JS, Dalton ND, Gilpin EA, and Ross J, Jr (2002) Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol 282:H2134-H2140.
32. Salomone S, Potts EM, Tyndall S, Ip PC, Chun J, Brinkmann V, and Waeber C (2008) Analysis of sphingosine 1-phosphate receptors involved in constriction of isolated cerebral arteries with receptor null mice and pharmacological tools. Br J Pharmacol 153:140-147.
33. Salomone S, Yoshimura S, Reuter U, Foley M, Thomas SS, Moskowitz MA, and Waeber C (2003) S1P3 receptors mediate the potent constriction of cerebral arteries by sphingosine-1-phosphate. Eur J Pharmacol 469:125-134.
34. Sanna MG, Liao J, Jo E, Alfonso C, Ahn MY, Peterson MS, Webb B, Lefebvre S, Chun J, and Gray N et al. (2004) Sphingosine 1-phosphate (S1P) receptor subtypes S1P1 and S1P3, respectively, regulate lymphocyte recirculation and heart rate. J Biol Chem 279:13839-13848.
35. Sanna MG, Wang SK, Gonzalez-Cabrera PJ, Don A, Marsolais D, Matheu MP, Wei SH, Parker I, Jo E, and Cheng WC et al. (2006) Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo. Nat Chem Biol 2:434-441.
36. Schmouder R, Serra D, Wang Y, Kovarik JM, DiMarco J, Hunt TL, and Bastien MC (2006) FTY720: placebo-controlled study of the effect on cardiac rate and rhythm in healthy subjects. J Clin Pharmacol 46:895-904.
37. Schörer SC, Brown SJ, Gonzalez-Cabrera PJ, Schaeffer MT, Chapman J, Jo E, Chase P, Spicer T, Hodder P and Rosen H (2008) Ligand-binding pocket shape differences between sphingosine 1-phosphate (S1P) receptors S1P1 and S1P3 determine efficiency of chemical probe identification by ultrahigh-Throughput screening. ACS Chem Biol 3:486-498.
38. Trifilieff A and Fozard JR (2012). Sphingosine-1-phosphate-induced airway hyperreactivity in rodents is mediated by the sphingosine-1-phosphate type 3 receptor. J Pharmacol Exp Ther 342:399-406.
39. Vanoli E, Pentimalli F and Botto G (2014) Vagomimetic effects of fingolimod: physiology and clinical implications. CNS Neurosci Ther 20:496-502.
40. Vargas WS and Perumal JS (2013) Fingolimod and cardiac risk: latest findings and clinical implications. Ther Adv Drug Saf 4:119-124.
41. Yagi Y, Nakamura Y, Kitahara K, Harada T, Kato K, Ninomiya T, Cao X, Ohara H, Izumi-Nakaseko H, and Suzuki K et al. (2014) Analysis of onset mechanisms of a sphingosine 1-phosphate receptor modulator fingolimod-induced atrioventricular conduction block and QT-interval prolongation. Toxicol Appl Pharmacol 281: 39-47.
42. Yamamoto M, Dobrzynski H, Tellez J, Niwa R, Billeter R, Honjo H, Kodama I, and Boyett MR (2006) Extended atrial conduction system characterised by the expression of the HCN4 channel and connexin45. Cardiovasc Res 72:271-281.
43. Yang AH, Ishii I, and Chun J (2002) In vivo roles of lysophospholipid receptors revealed by gene targeting studies in mice. Biochim Biophys Acta 1582:197-203.
44. Yasushi K, Fujii K, Taru M, and Miyoshi K (2011) inventors, Kyorin Pharmaceutical Co., Ltd, assignee. DIPHENYL SULFIDE DERIVATIVES AND MEDICINES CONTAINING SAMEAS ACTIVE INGREDIENT. PatentWO/2011/004604. 2011 Jan 13.