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Substitution of the DRY arginine with histidine in the human vasopressin receptor results in a loss-of-function phenotype associated with diabetes insipidus. The analogous R150H substitution of the DRY motif in zebrafish sphingosine-1 phosphate receptor 2 (S1p2) produces a mutation, miles apart m93 (milm93), that not only disrupts signaling but also impairs heart field migration. We hypothesized that constitutive S1p2 desensitization is the underlying cause of this strong zebrafish developmental defect. We observed in cell assays that the wild-type S1p2 receptor is at the cell surface whereas in distinct contrast the S1p2 R150H receptor is found in intracellular vesicles, blocking G protein but not arrestin signaling activity. Surface S1p2 R150H expression could be restored by inhibition of G protein-coupled receptor kinase 2 (GRK2). Moreover, we observed that \u03b2-arrestin 2 and GRK2 colocalize with S1p2 in developing zebrafish embryos and depletion of GRK2 in the S1p2 R150H miles apart zebrafish partially rescued cardia bifida. The ability of reduced GRK2 activity to reverse a developmental phenotype associated with constitutive desensitization supports efforts to genetically or pharmacologically target this kinase in diseases involving biased GPCR signaling.<\/jats:p>","DOI":"10.1021\/bi501061h","type":"journal-article","created":{"date-parts":[[2015,1,2]],"date-time":"2015-01-02T08:52:59Z","timestamp":1420188779000},"page":"765-775","source":"Crossref","is-referenced-by-count":15,"title":["Phenotypic Regulation of the Sphingosine 1-Phosphate\nReceptor Miles Apart by G Protein-Coupled Receptor Kinase 2"],"prefix":"10.1021","volume":"54","author":[{"given":"Martina","family":"Burczyk","sequence":"first","affiliation":[{"name":"Ulm University , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin D.","family":"Burkhalter","sequence":"additional","affiliation":[{"name":"Leibniz Institute for Age Research , , ,","place":["Jena, Germany, 07745"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tamara","family":"Bla\u0308tte","sequence":"additional","affiliation":[{"name":"Ulm University , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabrina","family":"Matysik","sequence":"additional","affiliation":[{"name":"Ulm University , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc G.","family":"Caron","sequence":"additional","affiliation":[{"name":"Duke University , , , ,","place":["Durham, North Carolina, United States, 27710"]},{"name":"Duke University , , , ,","place":["Durham, North Carolina, United States, 27710"]},{"name":"Duke University , , , ,","place":["Durham, North Carolina, United States, 27710"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lawrence S.","family":"Barak","sequence":"additional","affiliation":[{"name":"Duke University , , , ,","place":["Durham, North Carolina, United States, 27710"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melanie","family":"Philipp","sequence":"additional","affiliation":[{"name":"Ulm University , , ,","place":["Ulm, Germany, 89081"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2015,1,2]]},"reference":[{"key":"2026090301475545700_cit1","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.molmed.2010.11.004","article-title":"Therapeutic potential of \u03b2-arrestin-\nand G protein-biased agonists","volume":"17","author":"Whalen","year":"2011","journal-title":"Trends Mol. Med."},{"key":"2026090301475545700_cit2","doi-asserted-by":"crossref","first-page":"153","DOI":"10.3109\/10799893.2013.769004","article-title":"Emergent biological\nproperties of arrestin pathway-selective\nbiased agonism","volume":"33","author":"Appleton","year":"2013","journal-title":"J. Recept. Signal Transduction\nRes."},{"key":"2026090301475545700_cit3","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1038\/nrd3954","article-title":"Signalling\nbias in new drug discovery: Detection, quantification\nand therapeutic impact","volume":"12","author":"Kenakin","year":"2013","journal-title":"Nat. Rev. Drug Discovery"},{"key":"2026090301475545700_cit4","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1016\/j.ceb.2013.10.008","article-title":"Recent\ndevelopments in biased agonism","volume":"27","author":"Wisler","year":"2014","journal-title":"Curr. Opin.\nCell Biol."},{"key":"2026090301475545700_cit5","doi-asserted-by":"crossref","first-page":"1312","DOI":"10.1172\/JCI36806","article-title":"\u03b2-Arrestin1\nmediates nicotinic\nacid-induced flushing, but not its antilipolytic effect, in mice","volume":"119","author":"Walters","year":"2009","journal-title":"J. Clin. Invest."},{"key":"2026090301475545700_cit6","doi-asserted-by":"crossref","first-page":"1ra1","DOI":"10.1126\/scitranslmed.3000071","article-title":"A \u03b2-arrestin-biased agonist\nof the parathyroid hormone receptor (PTH1R) promotes bone formation\nindependent of G protein activation","volume":"1","author":"Gesty-Palmer","year":"2009","journal-title":"Sci. Transl.\nMed."},{"key":"2026090301475545700_cit7","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1073\/pnas.98.1.93","article-title":"Constitutive arrestin-mediated\ndesensitization of a human vasopressin receptor mutant associated\nwith nephrogenic diabetes insipidus","volume":"98","author":"Barak","year":"2001","journal-title":"Proc. Natl.\nAcad. Sci. U.S.A."},{"key":"2026090301475545700_cit8","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1242\/dev.123.1.285","article-title":"Mutations affecting the formation\nand function of the cardiovascular system in the zebrafish embryo","volume":"123","author":"Stainier","year":"1996","journal-title":"Development"},{"key":"2026090301475545700_cit9","doi-asserted-by":"crossref","first-page":"192","DOI":"10.1038\/35018092","article-title":"A sphingosine-1-phosphate\nreceptor regulates cell migration during vertebrate heart development","volume":"406","author":"Kupperman","year":"2000","journal-title":"Nature"},{"key":"2026090301475545700_cit10","doi-asserted-by":"crossref","first-page":"2379","DOI":"10.1242\/dev.02857","article-title":"Endocardium is necessary\nfor cardiomyocyte movement during heart tube assembly","volume":"134","author":"Holtzman","year":"2007","journal-title":"Development"},{"key":"2026090301475545700_cit11","doi-asserted-by":"crossref","first-page":"524","DOI":"10.1126\/science.1167449","article-title":"The sphingolipid transporter spns2 functions in migration\nof zebrafish myocardial precursors","volume":"323","author":"Kawahara","year":"2009","journal-title":"Science"},{"key":"2026090301475545700_cit12","doi-asserted-by":"crossref","first-page":"1882","DOI":"10.1016\/j.cub.2008.10.061","article-title":"The spinster homolog,\ntwo of hearts, is required for sphingosine 1-phosphate signaling in\nzebrafish","volume":"18","author":"Osborne","year":"2008","journal-title":"Curr. 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Immunol."},{"issue":"Suppl. 1","key":"2026090301475545700_cit15","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1159\/000052312","article-title":"Structure-function relationships\nof the \u03b11b-adrenergic\nreceptor","volume":"36","author":"Scheer","year":"1999","journal-title":"Eur. Urol."},{"key":"2026090301475545700_cit16","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1016\/S0026-895X(24)12198-0","article-title":"Mutagenesis\nand modelling of the \u03b1(1b)-adrenergic receptor highlight the\nrole of the helix 3\/helix 6 interface in receptor activation","volume":"61","author":"Greasley","year":"2002","journal-title":"Mol. Pharmacol."},{"key":"2026090301475545700_cit17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1124\/mol.105.014183","article-title":"A GPCR\nthat is not \u201cDRY\u201d","volume":"68","author":"Flanagan","year":"2005","journal-title":"Mol. Pharmacol."},{"key":"2026090301475545700_cit18","doi-asserted-by":"crossref","first-page":"880","DOI":"10.1124\/mol.104.001487","article-title":"Mutational\nanalysis of the highly\nconserved ERY motif of the thromboxane A2 receptor: Alternative role\nin G protein-coupled receptor signaling","volume":"66","author":"Capra","year":"2004","journal-title":"Mol.\nPharmacol."},{"key":"2026090301475545700_cit19","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1089\/15406580360545152","article-title":"Constitutive\ndesensitization: A new\nparadigm for G protein-coupled receptor regulation","volume":"1","author":"Barak","year":"2003","journal-title":"Assay Drug Dev. Technol."},{"key":"2026090301475545700_cit20","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1111\/jth.12539","article-title":"A novel mutation in the P2Y12 receptor\nand a function-reducing polymorphism in protease-activated receptor\n1 in a patient with chronic bleeding","volume":"12","author":"Patel","year":"2014","journal-title":"J. Thromb.\nHaemostasis"},{"key":"2026090301475545700_cit21","doi-asserted-by":"crossref","first-page":"11981","DOI":"10.1021\/bi020275m","article-title":"Apparent\nloss-of-function mutant GPCRs revealed as constitutively desensitized\nreceptors","volume":"41","author":"Wilbanks","year":"2002","journal-title":"Biochemistry"},{"key":"2026090301475545700_cit22","doi-asserted-by":"crossref","first-page":"e11839","DOI":"10.1371\/journal.pone.0011839","article-title":"An evolutionarily\nconserved arginine is essential for Tre1 G protein-coupled receptor\nfunction during germ cell migration in Drosophila melanogaster","volume":"5","author":"Kamps","year":"2010","journal-title":"PLoS One"},{"key":"2026090301475545700_cit23","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.pharmthera.2011.08.001","article-title":"G protein-coupled\nreceptor kinases: More than just kinases and not only for GPCRs","volume":"133","author":"Gurevich","year":"2012","journal-title":"Pharmacol. 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