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succinate receptor

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Target id: 166

Nomenclature: succinate receptor

Family: Succinate receptor

Gene and Protein Information Click here for help
class A G protein-coupled receptor
Species TM AA Chromosomal Location Gene Symbol Gene Name Reference
Human 7 334 3q25.1 SUCNR1 succinate receptor 1 27
Mouse 7 317 3 D Sucnr1 succinate receptor 1
Rat 7 317 2q31 Sucnr1 succinate receptor 1
Gene and Protein Information Comments
In humans, there is the possibility of two open-reading frames (ORFs) for SUCNR1, one giving a protein of 330 amino acids (aa) and the other one 334-aa. Wittenberger et al. [27] noted that the 330-aa protein was more likely to be expressed given the Kozak sequence surrounding the second ATG. Some databases report SUCNR1 as being 334-aa long.
Previous and Unofficial Names Click here for help
succinate receptor 1 | GPR91 | P2Y purinoceptor 1 | SUCNR1 | G protein-coupled receptor 91
Database Links Click here for help
Specialist databases
GPCRdb sucr1_human (Hs), sucr1_mouse (Mm), sucr1_rat (Rn)
Other databases
Alphafold
ChEMBL Target
Ensembl Gene
Entrez Gene
Human Protein Atlas
KEGG Gene
OMIM
Pharos
RefSeq Nucleotide
RefSeq Protein
UniProtKB
Wikipedia
Selected 3D Structures Click here for help
Image of receptor 3D structure from RCSB PDB
Description:  Crystal structure of a humanized (K18E, K269N) rat succinate receptor SUCNR1 (GPR91) in complex with a nanobody and antagonist NF-56-EJ40.
PDB Id:  6RNK
Ligand:  NF-56-EJ40
Resolution:  1.94Å
Species:  Rat
References:  9
Natural/Endogenous Ligands Click here for help
succinic acid

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Agonists
Key to terms and symbols View all chemical structures Click column headers to sort
Ligand Sp. Action Value Parameter Reference
compound 31 [PMID: 29968758] Small molecule or natural product Hs Partial agonist 7.6 pEC50 18
pEC50 7.6 (EC50 2.3x10-8 M) [18]
Description: IP3 accumulation, Emax=61%
cis-epoxysuccinic acid Small molecule or natural product Ligand has a PDB structure Hs Full agonist 5.6 – 5.8 pEC50 6,25
pEC50 5.8 (EC50 1.7x10-6 M) [25]
Description: IP3 accumulation, Emax=93%
pEC50 5.6 (EC50 2.7x10-6 M) [6]
Description: cAMP inhibition, Emax=100%
compound 130 [PMID: 29157600] Small molecule or natural product Hs Partial agonist 5.7 pEC50 25
pEC50 5.7 (EC50 2.25x10-6 M) [25]
Description: IP3 accumulation, Emax=75%
cis-1,2-cyclopropanedicarboxylic acid Small molecule or natural product Hs Full agonist 4.3 pEC50 6
pEC50 4.3 (EC50 4.9x10-5 M) [6]
(S)-chlorosuccinic acid Small molecule or natural product Hs Full agonist 4.1 pEC50 6
pEC50 4.1 (EC50 7.2x10-5 M) [6]
maleic acid Small molecule or natural product Ligand has a PDB structure Hs Agonist 3.9 – 4.2 pEC50 6-7,11
pEC50 3.9 – 4.2 [6-7,11]
succinic acid Small molecule or natural product Ligand is endogenous in the given species Ligand has a PDB structure Hs Full agonist 3.1 – 4.7 pEC50 11,22
pEC50 3.1 – 4.7 (EC50 9.1x10-5 – 2x10-5 M) [11,22]
methylmalonic acid Small molecule or natural product Ligand has a PDB structure Hs Full agonist 3.5 – 3.8 pEC50 6,11
pEC50 3.8 (EC50 1.69x10-4 M) [6]
pEC50 3.5 (EC50 2.84x10-4 M) [11]
Agonist Comments
Using molecular docking calculations, it is predicted that SUCNR1 may interact with gamma-hydroxybutyrate [16].
Antagonists
Key to terms and symbols View all chemical structures Click column headers to sort
Ligand Sp. Action Value Parameter Reference
NF-56-EJ40 Small molecule or natural product Ligand has a PDB structure Immunopharmacology Ligand Hs Antagonist 7.5 pKd 9
pKd 7.5 (Kd 3.3x10-8 M) [9]
Description: Dissociation constant for [3H]-labelled NF-56-EJ40 binding to human SUCNR1 determined in a radioligand binding assay.
NF-56-EJ40 Small molecule or natural product Ligand has a PDB structure Immunopharmacology Ligand Hs Antagonist 7.8 pKi 9
pKi 7.8 (Ki 1.74x10-8 M) [9]
compound 5g [PMID: 21571530] Small molecule or natural product Hs Antagonist 7.5 pIC50 3
pIC50 7.5 (IC50 3.5x10-8 M) [3]
compound 5g [PMID: 21571530] Small molecule or natural product Rn Antagonist 6.9 pIC50 3
pIC50 6.9 (IC50 1.35x10-7 M) [3]
compound 7e [PMID: 21571530] Small molecule or natural product Hs Antagonist 6.7 pIC50 3
pIC50 6.7 (IC50 1.8x10-7 M) [3]
View species-specific antagonist tables
Antagonist Comments
There are several synthetic antagonists against SUCNR1 discovered from a systematic structure-activity relationship study [3]. Among these antagonists, N-[{3-(3-trifluoromethyl-4-fluorophenyl)isoxazol-5-yl}methyl]-4-([1,8]naphthyridin-2-yl)butyramide (5g) and 2-{4-[5-(3-Chloro-4-trifluoromethoxyphenyl)-[1,3,4]oxadiazol-2-yl]butyl}-[1,8]naphthyridine (7e) are identified to have high pharmaceutical and clinical importance. 5g demonstrated satisfactory oral bioavailability in rats (%F: 26), very good plasma concentration (Cmax: 37uM, AUC0-24h: 69uM at 30mg/kg p.o. dose) and low plasma clearance. Similarly, 7e demonstrates low plasma clearance (2.0mL/min/kg), excellent bioavailability (%F: 87) and drug exposure (Cmax: 72uM, AUC0-24h: 471uMh, t1/2: 3.4h) upon oral admistration (30mg/kg p.o.) in rats.
Immunopharmacology Comments
Succinate acts an an alarmin that triggers the initiation and propagation of danger signals resulting from tissue injury or inflammatory stimuli. It acts through the succinate receptor, SUCNR1. SUCNR1-expressing macrophages release succinate that acts in an autocrine and paracrine feed-forward loop that elevates SUCNR1 expression and leads to enhanced IL-1β production [14]. This mechanism appears to be involved in promoting allergic and autoimmune diseases [20] such as rheumatoid arthritis (RA) (note that succinate levels are elevated in synovial fluids from RA patients), and could potentially be targeted by succinate receptor antagonists for clinical application.
Immuno Process Associations
Immuno Process:  Inflammation
Immuno Process:  Immune regulation
Immuno Process:  Cytokine production & signalling
Immuno Process:  Cellular signalling
Primary Transduction Mechanisms Click here for help
Transducer Effector/Response
Gi/Go family Adenylyl cyclase inhibition
Phospholipase C stimulation
Other - See Comments
Comments:  The Succinate receptor can recruit arrestins [7] and is internalized upon stimulation [7,11]. The precise mechanism for internalization has not been elucidated.
References:  7,11,23
Secondary Transduction Mechanisms Click here for help
Transducer Effector/Response
Gq/G11 family Phospholipase C stimulation
Comments:  Several authors were unable to confirm the activation of the Gq/G11 in transfected HEK293 cells [7,23]. It has been suggested that the Phospholipase C-β activation by Succinate receptor was mediated by Gβγ [23].
References:  11
Tissue Distribution Click here for help
Immature monocyte-derived DCs (MoDCs), macrophages, T cells, B cells
Species:  Human
Technique:  RT-PCR
References:  19
Megakaryocytes, platelets, monocytes
Species:  Human
Technique:  RT-PCR
References:  15
Present in platelets, T cells, B cells and monocytes. Absent in granulocytes.
Species:  Human
Technique:  Western blot
References:  15
Kidney
Species:  Human
Technique:  Northen blot
References:  27
Platelets
Species:  Human
Technique:  RT-PCR, western blot and confocal immunofluorescene microscopy
References:  1
CD34+ haematopoietic stem cells, megakaryocytes, erythroid progenitor cultures, bone marrow-derived stromal cell cultures.
Species:  Human
Technique:  RT-PCR and immunoblot
References:  10
Cortical region of mouse kidney, including proximal tubules, distal tubules, juxtaglomerular apparatus
Species:  Mouse
Technique:  in situ hybridisation
References:  11
Kidney, liver, spleen
Species:  Mouse
Technique:  RT-PCR
References:  10-11
Kidney, liver
Species:  Mouse
Technique:  Northen blot
References:  27
Isolated adipocytes, white adipose tissues, kidney, liver, gall bladder, vena cava, skin, spleen, thyroid
Species:  Mouse
Technique:  RT-PCR
References:  17
Kidney and glomerular endothelial cells. No transcripts of SUCNR1 were detected in vascular smooth muscle cell and juxtaglomerular cell.
Species:  Mouse
Technique:  RT-PCR
References:  24
Apical membrane of retinal pigment epithelium
Species:  Mouse
Technique:  in situ hybridisation
References:  8
Apical membrane of macula densa cells
Species:  Rat
Technique:  Immunohistochemistry
References:  26
Cell bodies of retinal ganglion cell layer and cells of the inner nuclear layer and outer retina
Species:  Rat
Technique:  Immunohistochemistry
References:  8
Vascular endothelial cells in the afferent arteriole and glomerulus. No expression of SUCR1 was detected in juxtaglomerular cell.
Species:  Rat
Technique:  Immunohistochemistry
References:  24,26
Ventricular cardiomyocytes
Species:  Rat
Technique:  RT-PCR, western blot and confocal microscopy
References:  1
Quiescent hepatic stellate cells. The transcipts of SUCNR1 were not detected in hepatocytes, cholangiocytes, Kuppffer cells, sinusoidal endothelial cells and portal fibroblasts
Species:  Rat
Technique:  RT-PCR and confocal immunofluorescence
References:  5
Tissue Distribution Comments
No transcripts of SUCNR1 were detected in the brain when examined by Northern blot analysis [4]. SUCNR1 is functionally expressed by immature dendritic cells after differentiation from monocytes and was rapidly downregulated after dendritic cell maturation [19]. SUCNR1 expression is enriched in both early and late-stage haematopoietic progenitor cells [10].
Expression Datasets Click here for help

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Log average relative transcript abundance in mouse tissues measured by qPCR from Regard, J.B., Sato, I.T., and Coughlin, S.R. (2008). Anatomical profiling of G protein-coupled receptor expression. Cell, 135(3): 561-71. [PMID:18984166] [Raw data: website]

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Physiological Functions Click here for help
Mediates hypertensive effect of succinate through the release of renin from the kidney and activation of the renin-angiotensin system.
Species:  Mouse
Tissue:  Kidney
References:  11-12
Mediates extracellular succinate-induced inhibition of lipolysis in white adipose tissue.
Species:  Mouse
Tissue:  White adipose tissue
References:  17
Mediates succinate-induced platelet aggregation of human platelets by decreasing cAMP levels and activating P13K [B]/Akt pathway, leading to P-selectin and glycoprotein IIb-IIIa activation.
Species:  Human
Tissue:  Platelets
References:  13
Mediates succinate-modulated Ca2+ transient in cardiomyocytes.
Species:  Rat
Tissue:  Cardiomyocytes
References:  1
Mediates the immunomodulatory effect of succinate, such as enhancing the secretion of proinflammatory cytokines by dendritic cells, inducing chemotaxis of dendritic cells, potentiating T cell activation and enhancing the homing of dendritic cells to draining lymph nodes.
Species:  Mouse
Tissue:  Dendritic cells
References:  19
Mediates the proliferation of TF-1 cell in response to succinate through Gi pathway activation of Erk1/2. Protect TF-1 cells from apoptosis induced by serum deprivation.
Species:  Human
Tissue:  Human erythroleukemic cell line
References:  11
Stimulate blood cell development in vivo under conditions of myelosuppression.
Species:  Mouse
Tissue:  Erythrocytes, platelets, neutrophils, lymphocytes
References:  11
Involved in the activation of MAPKs, COX-2 and the release of prostaglandin E2in macula densa cells, leading to renin release and renal angiotensin system activation.
Species:  Mouse
Tissue:  Macula densa
References:  26
Involved in retinal angiogenesis by regulating various angiogenic factors including vascular endothelial growth factor (VEGF) and angiopoietins.
Species:  Rat
Tissue:  Retina ganglion cells
References:  21
Mediates the succinate-induced expression of VEGF in iron-overloaded retinal pigment epithelium cells.
Species:  Mouse
Tissue:  Retical pigment epithelium
References:  8
Physiological Functions Comments
SUCNR1 signaling may have a role in activating hepatic stellate cells to restore damaged tissue in the ischemic liver [2].
Physiological Consequences of Altering Gene Expression Click here for help
Hypertension can not be induced by succinate in mice with SUCNR1 knockout.
Species:  Mouse
Tissue:  Kidney
Technique:  Gene knockouts
References:  11
The effect of succinate on Ca2+ transient in cardiomycytes is abolished in mice with SUCNR1 knockdown.
Species:  Rat
Tissue:  Cardiomyocytes
Technique:  RNA interference
References:  1
High glucose level-induced renin release is abolished in GPR91-/- mice.
Species:  Mouse
Tissue:  Kidney
Technique:  Breeding of GPR+/- mice
References:  24
Impaired migration of dendritic cells, diminished succinate-mediated immune responses, decreased T cell proliferation, weaker allograft rejection. SUCNR mice have impaired dendritic cell migration and diminished succinate-mediated immune responses such as chemotaxis of immature monocytes-driven dendritic cells and production of inflammotory cytokines. SUCNR-/- lymph node cells show lower ex vivo T cell proliferation. In addition, SUCNR-/- skin grafts show weaker allograft rejection responses than wild-type grafts.
Species:  Mouse
Tissue:  Embryonic stem cells
Technique:  Gene knockouts
References:  19
TF-1 cells with SUCNR1 knockdown do not proliferate in response to succinate.
Species:  Human
Tissue:  Human erythroleukemic cell line
Technique:  RNA interference
References:  10
Less tuft formation, extra-retinal neovascularization and blood vessel tortuosity. Rats with SUCNR1 knockdown are protected from retinal neovascularization in ischemic proliferative retinopathy.
Species:  Rat
Tissue:  Retina
Technique:  RNA interference
References:  21
Phenotypes, Alleles and Disease Models Click here for help Mouse data from MGI

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Allele Composition & genetic background Accession Phenotype Id Phenotype Reference
Sucnr1tm1Dgen Sucnr1tm1Dgen/Sucnr1tm1Dgen
B6.129P2-Sucnr1
MGI:1934135  MP:0002376 abnormal dendritic cell physiology PMID: 18820681 
Sucnr1tm1Dgen Sucnr1tm1Dgen/Sucnr1tm1Dgen
B6.129P2-Sucnr1
MGI:1934135  MP:0008686 abnormal interleukin-2 secretion PMID: 18820681 
Sucnr1tm1Lex Sucnr1tm1Lex/Sucnr1tm1Lex
involves: 129S/SvEvBrd
MGI:1934135  MP:0002136 abnormal kidney physiology PMID: 18535668 
Sucnr1tm1Dgen Sucnr1tm1Dgen/Sucnr1tm1Dgen
B6.129P2-Sucnr1
MGI:1934135  MP:0005362 abnormal Langerhans cell physiology PMID: 18820681 
Sucnr1tm1Dgen Sucnr1tm1Dgen/Sucnr1tm1Dgen
B6.129P2-Sucnr1
MGI:1934135  MP:0001828 abnormal T cell activation PMID: 18820681 
Sucnr1tm1Lex Sucnr1tm1Lex/Sucnr1tm1Lex
involves: 129S/SvEvBrd
MGI:1934135  MP:0003353 decreased circulating renin level PMID: 18535668 
Sucnr1tm1Dgen Sucnr1tm1Dgen/Sucnr1tm1Dgen
B6.129P2-Sucnr1
MGI:1934135  MP:0005095 decreased T cell proliferation PMID: 18820681 
Sucnr1tm1Dgen Sucnr1tm1Dgen/Sucnr1tm1Dgen
B6.129P2-Sucnr1
MGI:1934135  MP:0004751 increased length of allograft survival PMID: 18820681 
Gene Expression and Pathophysiology Comments
The signalling of SUCNR1 is involved in various pathologies, such as renal hypertension, diabetic nephropathy, retinal angiogenesis, diabetic retinopathy and aggregation of platelets [2-3]. SUCNR1 signalling may also contribue to the formation of fibrosis [2].
General Comments
Succinate is as an intermediary of the citric acid cycle. It exerts biological effects via activation of the membrane-bound succinate receptor, SUCNR1 [2]. SUCRN1 is a novel potential drug target to prevent renal complications of diabetes [24]. The expression of SUCNR1 in retinal pigment epithelium cells is iron-dependent [8].

References

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1. Aguiar CJ, Andrade VL, Gomes ER, Alves MN, Ladeira MS, Pinheiro AC, Gomes DA, Almeida AP, Goes AM, Resende RR et al.. (2010) Succinate modulates Ca(2+) transient and cardiomyocyte viability through PKA-dependent pathway. Cell Calcium, 47 (1): 37-46. [PMID:20018372]

2. Ariza AC, Deen PM, Robben JH. (2012) The succinate receptor as a novel therapeutic target for oxidative and metabolic stress-related conditions. Front Endocrinol (Lausanne), 3: 22. [PMID:22649411]

3. Bhuniya D, Umrani D, Dave B, Salunke D, Kukreja G, Gundu J, Naykodi M, Shaikh NS, Shitole P, Kurhade S et al.. (2011) Discovery of a potent and selective small molecule hGPR91 antagonist. Bioorg Med Chem Lett, 21 (12): 3596-602. [PMID:21571530]

4. Cantagrel V, Lossi AM, Boulanger S, Depetris D, Mattei MG, Gecz J, Schwartz CE, Van Maldergem L, Villard L. (2004) Disruption of a new X linked gene highly expressed in brain in a family with two mentally retarded males. J Med Genet, 41 (10): 736-42. [PMID:15466006]

5. Correa PR, Kruglov EA, Thompson M, Leite MF, Dranoff JA, Nathanson MH. (2007) Succinate is a paracrine signal for liver damage. J Hepatol, 47 (2): 262-9. [PMID:17451837]

6. Geubelle P, Gilissen J, Dilly S, Poma L, Dupuis N, Laschet C, Abboud D, Inoue A, Jouret F, Pirotte B et al.. (2017) Identification and pharmacological characterization of succinate receptor agonists. Br J Pharmacol, 174 (9): 796-808. [PMID:28160606]

7. Gilissen J, Geubelle P, Dupuis N, Laschet C, Pirotte B, Hanson J. (2015) Forskolin-free cAMP assay for Gi-coupled receptors. Biochem Pharmacol, 98 (3): 381-91. [PMID:26386312]

8. Gnana-Prakasam JP, Ananth S, Prasad PD, Zhang M, Atherton SS, Martin PM, Smith SB, Ganapathy V. (2011) Expression and iron-dependent regulation of succinate receptor GPR91 in retinal pigment epithelium. Invest Ophthalmol Vis Sci, 52 (6): 3751-8. [PMID:21357408]

9. Haffke M, Fehlmann D, Rummel G, Boivineau J, Duckely M, Gommermann N, Cotesta S, Sirockin F, Freuler F, Littlewood-Evans A et al.. (2019) Structural basis of species-selective antagonist binding to the succinate receptor. Nature, 574 (7779): 581-585. DOI: 10.1038/s41586-019-1663-8 [PMID:31645725]

10. Hakak Y, Lehmann-Bruinsma K, Phillips S, Le T, Liaw C, Connolly DT, Behan DP. (2009) The role of the GPR91 ligand succinate in hematopoiesis. J Leukoc Biol, 85 (5): 837-43. [PMID:19204147]

11. He W, Miao FJ, Lin DC, Schwandner RT, Wang Z, Gao J, Chen JL, Tian H, Ling L. (2004) Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors. Nature, 429 (6988): 188-93. [PMID:15141213]

12. Hebert SC. (2004) Physiology: orphan detectors of metabolism. Nature, 429 (6988): 143-5. [PMID:15141197]

13. Högberg C, Gidlöf O, Tan C, Svensson S, Nilsson-Öhman J, Erlinge D, Olde B. (2011) Succinate independently stimulates full platelet activation via cAMP and phosphoinositide 3-kinase-β signaling. J Thromb Haemost, 9 (2): 361-72. [PMID:21143371]

14. Littlewood-Evans A, Sarret S, Apfel V, Loesle P, Dawson J, Zhang J, Muller A, Tigani B, Kneuer R, Patel S et al.. (2016) GPR91 senses extracellular succinate released from inflammatory macrophages and exacerbates rheumatoid arthritis. J Exp Med, 213 (9): 1655-62. [PMID:27481132]

15. Macaulay IC, Tijssen MR, Thijssen-Timmer DC, Gusnanto A, Steward M, Burns P, Langford CF, Ellis PD, Dudbridge F, Zwaginga JJ, Watkins NA, van der Schoot CE, Ouwehand WH. (2007) Comparative gene expression profiling of in vitro differentiated megakaryocytes and erythroblasts identifies novel activatory and inhibitory platelet membrane proteins. Blood, 109 (8): 3260-9. [PMID:17192395]

16. Molnár T, Héja L, Emri Z, Simon A, Nyitrai G, Pál I, Kardos J. (2011) Activation of astroglial calcium signaling by endogenous metabolites succinate and gamma-hydroxybutyrate in the nucleus accumbens. Front Neuroenergetics, 3: 7. [PMID:22180742]

17. Regard JB, Sato IT, Coughlin SR. (2008) Anatomical profiling of G protein-coupled receptor expression. Cell, 135 (3): 561-71. [PMID:18984166]

18. Rexen Ulven E, Trauelsen M, Brvar M, Lückmann M, Bielefeldt LØ, Jensen LKI, Schwartz TW, Frimurer TM. (2018) Structure-Activity Investigations and Optimisations of Non-metabolite Agonists for the Succinate Receptor 1. Sci Rep, 8 (1): 10010. [PMID:29968758]

19. Rubic T, Lametschwandtner G, Jost S, Hinteregger S, Kund J, Carballido-Perrig N, Schwärzler C, Junt T, Voshol H, Meingassner JG et al.. (2008) Triggering the succinate receptor GPR91 on dendritic cells enhances immunity. Nat Immunol, 9 (11): 1261-9. [PMID:18820681]

20. Rubić-Schneider T, Carballido-Perrig N, Regairaz C, Raad L, Jost S, Rauld C, Christen B, Wieczorek G, Kreutzer R, Dawson J et al.. (2017) GPR91 deficiency exacerbates allergic contact dermatitis while reducing arthritic disease in mice. Allergy, 72 (3): 444-452. [PMID:27527650]

21. Sapieha P, Sirinyan M, Hamel D, Zaniolo K, Joyal JS, Cho JH, Honoré JC, Kermorvant-Duchemin E, Varma DR, Tremblay S et al.. (2008) The succinate receptor GPR91 in neurons has a major role in retinal angiogenesis. Nat Med, 14 (10): 1067-76. [PMID:18836459]

22. Southern C, Cook JM, Neetoo-Isseljee Z, Taylor DL, Kettleborough CA, Merritt A, Bassoni DL, Raab WJ, Quinn E, Wehrman TS et al.. (2013) Screening β-Arrestin Recruitment for the Identification of Natural Ligands for Orphan G-Protein-Coupled Receptors. J Biomol Screen, 18 (5): 599-609. [PMID:23396314]

23. Sundström L, Greasley PJ, Engberg S, Wallander M, Ryberg E. (2013) Succinate receptor GPR91, a Gα(i) coupled receptor that increases intracellular calcium concentrations through PLCβ. FEBS Lett, 587 (15): 2399-404. [PMID:23770096]

24. Toma I, Kang JJ, Sipos A, Vargas S, Bansal E, Hanner F, Meer E, Peti-Peterdi J. (2008) Succinate receptor GPR91 provides a direct link between high glucose levels and renin release in murine and rabbit kidney. J Clin Invest, 118 (7): 2526-34. [PMID:18535668]

25. Trauelsen M, Rexen Ulven E, Hjorth SA, Brvar M, Monaco C, Frimurer TM, Schwartz TW. (2017) Receptor structure-based discovery of non-metabolite agonists for the succinate receptor GPR91. Mol Metab, 6 (12): 1585-1596. [PMID:29157600]

26. Vargas SL, Toma I, Kang JJ, Meer EJ, Peti-Peterdi J. (2009) Activation of the succinate receptor GPR91 in macula densa cells causes renin release. J Am Soc Nephrol, 20 (5): 1002-11. [PMID:19389848]

27. Wittenberger T, Schaller HC, Hellebrand S. (2001) An expressed sequence tag (EST) data mining strategy succeeding in the discovery of new G-protein coupled receptors. J Mol Biol, 307 (3): 799-813. [PMID:11273702]

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