Login Register Cart 0
Generic placeholder image

Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Apelin Receptor Dimerization and Oligomerization

Author(s): Mahboobeh Yeganeh-Hajahmadi, Yasmin Moosavi-Saeed and Farzaneh Rostamzadeh*

Volume 17, 2024

Published on: 06 October, 2023

Article ID: e180823219999 Pages: 11

DOI: 10.2174/1874467217666230818113538

open_access

Abstract

Apelin and its receptor are expressed in many tissues and play an important role in maintaining the homeostasis of the cardiovascular system and body fluids. Also, the association of this system with many diseases, such as diabetes, hypertension, obesity, cancer, diabetic retinopathy, etc., has been determined. This system is considered a therapeutic goal in many mentioned diseases. G protein-coupled receptors (GPCRs) have the ability to form oligomers and dimers with themselves and other receptors. The formation of these oligomers is associated with a change in the signaling pathways of the receptors. Research on the oligo and dimers of these receptors can revolutionize the principles of pharmacology. The apelin receptor (APJ) is also a GPCR and has been shown to have the ability to form dimers and oligomers. This article discusses the dimerization and oligomerization of this receptor with its own receptor and other receptors, as well as the signaling pathways.

Keywords: Apelin receptor, APJ, Dimerization, Oligomerization, Signaling pathway, Homodimerization. Article

[1]
Bai, M. Dimerization of G-protein-coupled receptors: Roles in signal transduction. Cell. Signal., 2004, 16(2), 175-186.
[http://dx.doi.org/10.1016/S0898-6568(03)00128-1] [PMID: 14636888]
[2]
Milligan, G.; Ward, R.J.; Marsango, S. GPCR homo-oligomerization. Curr. Opin. Cell Biol., 2019, 57, 40-47.
[http://dx.doi.org/10.1016/j.ceb.2018.10.007] [PMID: 30453145]
[3]
Liu, J.; Tang, H.; Xu, C.; Zhou, S.; Zhu, X.; Li, Y.; Prézeau, L.; Xu, T.; Pin, J.P.; Rondard, P.; Ji, W.; Liu, J. Biased signaling due to oligomerization of the G protein-coupled platelet-activating factor receptor. Nat. Commun., 2022, 13(1), 6365.
[http://dx.doi.org/10.1038/s41467-022-34056-4] [PMID: 36289206]
[4]
Reiter, E.; Lefkowitz, R.J. GRKs and β-arrestins: Roles in receptor silencing, trafficking and signaling. Trends Endocrinol. Metab., 2006, 17(4), 159-165.
[http://dx.doi.org/10.1016/j.tem.2006.03.008] [PMID: 16595179]
[5]
O’Hayre, M.; Eichel, K.; Avino, S.; Zhao, X.; Steffen, D.J.; Feng, X.; Kawakami, K.; Aoki, J.; Messer, K.; Sunahara, R.; Inoue, A.; von Zastrow, M.; Gutkind, J.S. Genetic evidence that β-arrestins are dispensable for the initiation of β 2 -adrenergic receptor signaling to ERK. Sci. Signal., 2017, 10(484), eaal3395.
[http://dx.doi.org/10.1126/scisignal.aal3395] [PMID: 28634209]
[6]
Luttrell, L.M.; Wang, J.; Plouffe, B.; Smith, J.S.; Yamani, L.; Kaur, S.; Jean-Charles, P.Y.; Gauthier, C.; Lee, M.H.; Pani, B.; Kim, J.; Ahn, S.; Rajagopal, S.; Reiter, E.; Bouvier, M.; Shenoy, S.K.; Laporte, S.A.; Rockman, H.A.; Lefkowitz, R.J. Manifold roles of β-arrestins in GPCR signaling elucidated with siRNA and CRISPR/Cas9. Sci. Signal., 2018, 11(549), eaat7650.
[http://dx.doi.org/10.1126/scisignal.aat7650] [PMID: 30254056]
[7]
Rozenfeld, R.; Devi, L.A. Exploring a role for heteromerization in GPCR signalling specificity. Biochem. J., 2011, 433(1), 11-18.
[http://dx.doi.org/10.1042/BJ20100458] [PMID: 21158738]
[8]
Pérez de la Mora, M.; Borroto-Escuela, D.O.; Crespo-Ramírez, M.; Rejón-Orantes, J.C.; Palacios-Lagunas, D.A.; Martínez-Mata, M.K.; Sánchez-Luna, D.; Tesoro-Cruz, E.; Fuxe, K. Dysfunctional heteroreceptor complexes as novel targets for the treatment of major depressive and anxiety disorders. Cells, 2022, 11(11), 1826.
[http://dx.doi.org/10.3390/cells11111826] [PMID: 35681521]
[9]
Farran, B. An update on the physiological and therapeutic relevance of GPCR oligomers. Pharmacol. Res., 2017, 117, 303-327.
[http://dx.doi.org/10.1016/j.phrs.2017.01.008] [PMID: 28087443]
[10]
Ferré, S.; Franco, R. Oligomerization of G-protein-coupled receptors: A reality. Curr. Opin. Pharmacol., 2010, 10(1), 1-5.
[http://dx.doi.org/10.1016/j.coph.2009.11.002] [PMID: 20015687]
[11]
Galvez, T.; Duthey, B.; Kniazeff, J.; Blahos, J.; Rovelli, G.; Bettler, B.; Prézeau, L.; Pin, J-P. Allosteric interactions between GB1 andGB2 subunits are required for optimalGABAB receptor function. EMBO J., 2001, 20(9), 2152-2159.
[http://dx.doi.org/10.1093/emboj/20.9.2152] [PMID: 11331581]
[12]
Palmer, R.K. The pharmacology and signaling of bitter, sweet, and umami taste sensing. Mol. Interv., 2007, 7(2), 87-98.
[http://dx.doi.org/10.1124/mi.7.2.9] [PMID: 17468389]
[13]
Prinster, S.C.; Hague, C.; Hall, R.A. Heterodimerization of g protein-coupled receptors: Specificity and functional significance. Pharmacol. Rev., 2005, 57(3), 289-298.
[http://dx.doi.org/10.1124/pr.57.3.1] [PMID: 16109836]
[14]
Jordan, B.A.; Devi, L.A. G-protein-coupled receptor heterodimerization modulates receptor function. Nature, 1999, 399(6737), 697-700.
[http://dx.doi.org/10.1038/21441] [PMID: 10385123]
[15]
Ward, R.J.; Pediani, J.D.; Godin, A.G.; Milligan, G. Regulation of oligomeric organization of the serotonin 5-hydroxytryptamine 2C (5-HT2C) receptor observed by spatial intensity distribution analysis. J. Biol. Chem., 2015, 290(20), 12844-12857.
[http://dx.doi.org/10.1074/jbc.M115.644724] [PMID: 25825490]
[16]
AbdAlla, S.; Lother, H.; el Massiery, A.; Quitterer, U. Increased AT1 receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat. Med., 2001, 7(9), 1003-1009.
[http://dx.doi.org/10.1038/nm0901-1003] [PMID: 11533702]
[17]
Tatemoto, K.; Hosoya, M.; Habata, Y.; Fujii, R.; Kakegawa, T.; Zou, M.X.; Kawamata, Y.; Fukusumi, S.; Hinuma, S.; Kitada, C.; Kurokawa, T.; Onda, H.; Fujino, M. Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem. Biophys. Res. Commun., 1998, 251(2), 471-476.
[http://dx.doi.org/10.1006/bbrc.1998.9489] [PMID: 9792798]
[18]
O’Carroll, A.M.; Lolait, S.J.; Harris, L.E.; Pope, G.R. The apelin receptor APJ: Journey from an orphan to a multifaceted regulator of homeostasis. J. Endocrinol., 2013, 219(1), R13-R35.
[http://dx.doi.org/10.1530/JOE-13-0227] [PMID: 23943882]
[19]
O’Dowd, B.F.; Heiber, M.; Chan, A.; Heng, H.H.Q.; Tsui, L.C.; Kennedy, J.L.; Shi, X.; Petronis, A.; George, S.R.; Nguyen, T. A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11. Gene, 1993, 136(1-2), 355-360.
[http://dx.doi.org/10.1016/0378-1119(93)90495-O] [PMID: 8294032]
[20]
Lee, D.K.; Cheng, R.; Nguyen, T.; Fan, T.; Kariyawasam, A.P.; Liu, Y.; Osmond, D.H.; George, S.R.; O’Dowd, B.F. Characterization of apelin, the ligand for the APJ receptor. J. Neurochem., 2000, 74(1), 34-41.
[http://dx.doi.org/10.1046/j.1471-4159.2000.0740034.x] [PMID: 10617103]
[21]
Yang, P.; Maguire, J.J.; Davenport, A.P. Apelin, Elabela/Toddler, and biased agonists as novel therapeutic agents in the cardiovascular system. Trends Pharmacol. Sci., 2015, 36(9), 560-567.
[http://dx.doi.org/10.1016/j.tips.2015.06.002] [PMID: 26143239]
[22]
Medhurst, A.D.; Jennings, C.A.; Robbins, M.J.; Davis, R.P.; Ellis, C.; Winborn, K.Y.; Lawrie, K.W.M.; Hervieu, G.; Riley, G.; Bolaky, J.E.; Herrity, N.C.; Murdock, P.; Darker, J.G. Pharmacological and immunohistochemical characterization of the APJ receptor and its endogenous ligand apelin. J. Neurochem., 2003, 84(5), 1162-1172.
[http://dx.doi.org/10.1046/j.1471-4159.2003.01587.x] [PMID: 12603839]
[23]
Pope, G.R.; Roberts, E.M.; Lolait, S.J.; O’Carroll, A.M. Central and peripheral apelin receptor distribution in the mouse: Species differences with rat. Peptides, 2012, 33(1), 139-148.
[http://dx.doi.org/10.1016/j.peptides.2011.12.005] [PMID: 22197493]
[24]
Kleinz, M.J.; Skepper, J.N.; Davenport, A.P. Immunocytochemical localisation of the apelin receptor, APJ, to human cardiomyocytes, vascular smooth muscle and endothelial cells. Regul. Pept., 2005, 126(3), 233-240.
[http://dx.doi.org/10.1016/j.regpep.2004.10.019] [PMID: 15664671]
[25]
Folino, A.; Montarolo, P.G.; Samaja, M.; Rastaldo, R. Effects of apelin on the cardiovascular system. Heart Fail. Rev., 2015, 20(4), 505-518.
[http://dx.doi.org/10.1007/s10741-015-9475-x] [PMID: 25652330]
[26]
Chaves-Almagro, C.; Castan-Laurell, I.; Dray, C.; Knauf, C.; Valet, P.; Masri, B. Apelin receptors: From signaling to antidiabetic strategy. Eur. J. Pharmacol., 2015, 763(Pt B), 149-159.
[http://dx.doi.org/10.1016/j.ejphar.2015.05.017] [PMID: 26007641]
[27]
Hu, G.; Wang, Z.; Zhang, R.; Sun, W.; Chen, X. The role of apelin/apelin receptor in energy metabolism and water homeostasis: A Comprehensive narrative review. Front. Physiol., 2021, 12, 632886.
[http://dx.doi.org/10.3389/fphys.2021.632886] [PMID: 33679444]
[28]
Bai, B.; Yan, X.; Cheng, B.; Wang, X.; Ding, L.; Liu, H.; Chen, J. Lateral intracerebroventricular injection of Apelin-13 inhibits apoptosis after cerebral ischemia/reperfusion injury. Neural Regen. Res., 2015, 10(5), 766-771.
[http://dx.doi.org/10.4103/1673-5374.157243] [PMID: 26109951]
[29]
Yang, Y.; Lv, S.Y.; Lyu, S.K.; Wu, D.; Chen, Q. The protective effect of apelin on ischemia/reperfusion injury. Peptides, 2015, 63, 43-46.
[http://dx.doi.org/10.1016/j.peptides.2014.11.001] [PMID: 25447414]
[30]
Chng, S.C.; Ho, L.; Tian, J.; Reversade, B. ELABELA: A hormone essential for heart development signals via the apelin receptor. Dev. Cell, 2013, 27(6), 672-680.
[http://dx.doi.org/10.1016/j.devcel.2013.11.002] [PMID: 24316148]
[31]
Read, C.; Nyimanu, D.; Williams, T. L.; Huggins, D. J.; Sulentic, P.; Macrae, R. G. C.; Yang, P.; Glen, R. C.; Maguire, J. J.; Davenport, A. P. International union of basic and clinical pharmacology. CVII. Structure and pharmacology of the apelin receptor with a recommendation that elabela/toddler is a second endogenous peptide ligand. Pharmacol. Rev., 2019, 71(4), 467-502.
[http://dx.doi.org/10.1124/pr.119.017533]
[32]
Pauli, A.; Norris, M. L.; Valen, E.; Chew, G.-L.; Gagnon, J. A.; Zimmerman, S.; Mitchell, A.; Ma, J.; Dubrulle, J.; Reyon, D.; Tsai, S. Q.; Joung, J. K.; Saghatelian, A.; Schier, A. F. Toddler: An embryonic signal that promotes cell movement via apelin receptors. Science , 2014, 343(6172), 1248636.
[http://dx.doi.org/10.1126/science.1248636]
[33]
Scimia, M.C.; Hurtado, C.; Ray, S.; Metzler, S.; Wei, K.; Wang, J.; Woods, C.E.; Purcell, N.H.; Catalucci, D.; Akasaka, T.; Bueno, O.F.; Vlasuk, G.P.; Kaliman, P.; Bodmer, R.; Smith, L.H.; Ashley, E.; Mercola, M.; Brown, J.H.; Ruiz-Lozano, P. APJ acts as a dual receptor in cardiac hypertrophy. Nature, 2012, 488(7411), 394-398.
[http://dx.doi.org/10.1038/nature11263] [PMID: 22810587]
[34]
Wilde, C.; Mitgau, J.; Suchý, T.; Schöneberg, T.; Liebscher, I. Translating the force-mechano-sensing GPCRs. Am. J. Physiol. Cell Physiol., 2022, 322(6), C1047-C1060.
[http://dx.doi.org/10.1152/ajpcell.00465.2021] [PMID: 35417266]
[35]
Chun, H.J.; Ali, Z.A.; Kojima, Y.; Kundu, R.K.; Sheikh, A.Y.; Agrawal, R.; Zheng, L.; Leeper, N.J.; Pearl, N.E.; Patterson, A.J.; Anderson, J.P.; Tsao, P.S.; Lenardo, M.J.; Ashley, E.A.; Quertermous, T. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J. Clin. Invest., 2008, 118(10), 3343-3354.
[http://dx.doi.org/10.1172/JCI34871] [PMID: 18769630]
[36]
Li, Y.; Chen, J.; Bai, B.; Du, H.; Liu, Y.; Liu, H. Heterodimerization of human apelin and kappa opioid receptors: Roles in signal transduction. Cell. Signal., 2012, 24(5), 991-1001.
[http://dx.doi.org/10.1016/j.cellsig.2011.12.012] [PMID: 22200678]
[37]
Bai, B.; Liu, L.; Zhang, N.; Wang, C.; Jiang, Y.; Chen, J. Heterodimerization of human apelin and bradykinin 1 receptors: Novel signal transduction characteristics. Cell. Signal., 2014, 26(7), 1549-1559.
[http://dx.doi.org/10.1016/j.cellsig.2014.03.022] [PMID: 24686079]
[38]
Bai, B.; Cai, X.; Jiang, Y.; Karteris, E.; Chen, J. Heterodimerization of apelin receptor and neurotensin receptor 1 induces phosphorylation of ERK 1/2 and cell proliferation via Gαq‐mediated mechanism. J. Cell. Mol. Med., 2014, 18(10), 2071-2081.
[http://dx.doi.org/10.1111/jcmm.12404] [PMID: 25164432]
[39]
Wang, D.; Wang, Y.; Shan, M.; Chen, J.; Wang, H.; Sun, B.; Jin, C.; Li, X.; Yin, Y.; Song, C.; Xiao, C.; Li, J.; Wang, T.; Cai, X. Apelin receptor homodimer inhibits apoptosis in vascular dementia. Exp. Cell Res., 2021, 407(1), 112739.
[http://dx.doi.org/10.1016/j.yexcr.2021.112739] [PMID: 34343559]
[40]
Cai, X.; Bai, B.; Zhang, R.; Wang, C.; Chen, J. Apelin receptor homodimer-oligomers revealed by single-molecule imaging and novel G protein-dependent signaling. Sci. Rep., 2017, 7(1), 40335.
[http://dx.doi.org/10.1038/srep40335] [PMID: 28091541]
[41]
St-Gelais, F.; Jomphe, C.; Trudeau, L-É. The role of neurotensin in central nervous system pathophysiology: What is the evidence? J. Psychiatry Neurosci., 2006, 31(4), 229-245.
[PMID: 16862241]
[42]
Vincent, J.P.; Mazella, J.; Kitabgi, P. Neurotensin and neurotensin receptors. Trends Pharmacol. Sci., 1999, 20(7), 302-309.
[http://dx.doi.org/10.1016/S0165-6147(99)01357-7] [PMID: 10390649]
[43]
Liu, H.; Tian, Y.; Ji, B.; Lu, H.; Xin, Q.; Jiang, Y.; Ding, L.; Zhang, J.; Chen, J.; Bai, B. Heterodimerization of the kappa opioid receptor and neurotensin receptor 1 contributes to a novel β-arrestin-2–biased pathway. Biochim. Biophys. Acta Mol. Cell Res., 2016, 1863(11), 2719-2738.
[http://dx.doi.org/10.1016/j.bbamcr.2016.07.009] [PMID: 27523794]
[44]
Sakurai, T. The role of orexin in motivated behaviours. Nat. Rev. Neurosci., 2014, 15(11), 719-731.
[http://dx.doi.org/10.1038/nrn3837] [PMID: 25301357]
[45]
Chieffi, S.; Carotenuto, M.; Monda, V.; Valenzano, A.; Villano, I.; Precenzano, F.; Tafuri, D.; Salerno, M.; Filippi, N.; Nuccio, F.; Ruberto, M.; De Luca, V.; Cipolloni, L.; Cibelli, G.; Mollica, M.P.; Iacono, D.; Nigro, E.; Monda, M.; Messina, G.; Messina, A. Orexin system: The key for a healthy life. Front. Physiol., 2017, 8, 357.
[http://dx.doi.org/10.3389/fphys.2017.00357] [PMID: 28620314]
[46]
Wan, L.; Xu, F.; Liu, C.; Ji, B.; Zhang, R.; Wang, P.; Wu, F.; Pan, Y.; Yang, C.; Wang, C.; Chen, J. Transmembrane peptide 4 and 5 of APJ are essential for its heterodimerization with OX1R. Biochem. Biophys. Res. Commun., 2020, 521(2), 408-413.
[http://dx.doi.org/10.1016/j.bbrc.2019.10.146] [PMID: 31668922]
[47]
Bai, B.; Chen, X.; Zhang, R.; Wang, X.; Jiang, Y.; Li, D.; Wang, Z.; Chen, J. Dual-agonist occupancy of orexin receptor 1 and cholecystokinin A receptor heterodimers decreases G-protein-dependent signaling and migration in the human colon cancer cell line HT-29. Biochim. Biophys. Acta Mol. Cell Res., 2017, 1864(7), 1153-1164.
[http://dx.doi.org/10.1016/j.bbamcr.2017.03.003] [PMID: 28288880]
[48]
Chen, J.; Zhang, R.; Chen, X.; Wang, C.; Cai, X.; Liu, H.; Jiang, Y.; Liu, C.; Bai, B. Heterodimerization of human orexin receptor 1 and kappa opioid receptor promotes protein kinase A/cAMP-response element binding protein signaling via a Gαs-mediated mechanism. Cell. Signal., 2015, 27(7), 1426-1438.
[http://dx.doi.org/10.1016/j.cellsig.2015.03.027] [PMID: 25866368]
[49]
Sun, X.; Iida, S.; Yoshikawa, A.; Senbonmatsu, R.; Imanaka, K.; Maruyama, K.; Nishimura, S.; Inagami, T.; Senbonmatsu, T. Non-activated APJ suppresses the angiotensin II type 1 receptor, whereas apelin-activated APJ acts conversely. Hypertens. Res., 2011, 34(6), 701-706.
[http://dx.doi.org/10.1038/hr.2011.19] [PMID: 21412239]
[50]
Chandrasekaran, B.; Dar, O.; McDonagh, T. The role of apelin in cardiovascular function and heart failure. Eur. J. Heart Fail., 2008, 10(8), 725-732.
[http://dx.doi.org/10.1016/j.ejheart.2008.06.002] [PMID: 18583184]
[51]
Ishida, J.; Hashimoto, T.; Hashimoto, Y.; Nishiwaki, S.; Iguchi, T.; Harada, S.; Sugaya, T.; Matsuzaki, H.; Yamamoto, R.; Shiota, N.; Okunishi, H.; Kihara, M.; Umemura, S.; Sugiyama, F.; Yagami, K.; Kasuya, Y.; Mochizuki, N.; Fukamizu, A. Regulatory roles for APJ, a seven-transmembrane receptor related to angiotensin-type 1 receptor in blood pressure in vivo. J. Biol. Chem., 2004, 279(25), 26274-26279.
[http://dx.doi.org/10.1074/jbc.M404149200] [PMID: 15087458]
[52]
Siddiquee, K.; Hampton, J.; McAnally, D.; May, L.T.; Smith, L.H. The apelin receptor inhibits the angiotensin II type 1 receptor via allosteric trans-inhibition. Br. J. Pharmacol., 2013, 168(5), 1104-1117.
[http://dx.doi.org/10.1111/j.1476-5381.2012.02192.x] [PMID: 22935142]
[53]
Hashimoto, T.; Kihara, M.; Imai, N.; Yoshida, S.; Shimoyamada, H.; Yasuzaki, H.; Ishida, J.; Toya, Y.; Kiuchi, Y.; Hirawa, N.; Tamura, K.; Yazawa, T.; Kitamura, H.; Fukamizu, A.; Umemura, S. Requirement of apelin-apelin receptor system for oxidative stress-linked atherosclerosis. Am. J. Pathol., 2007, 171(5), 1705-1712.
[http://dx.doi.org/10.2353/ajpath.2007.070471] [PMID: 17884970]
[54]
Liu, C.; Su, T.; Li, F.; Li, L.; Qin, X.; Pan, W.; Feng, F.; Chen, F.; Liao, D.; Chen, L. PI3K/Akt signaling transduction pathway is involved in rat vascular smooth muscle cell proliferation induced by apelin-13. Acta Biochim. Biophys. Sin., 2010, 42(6), 396-402.
[http://dx.doi.org/10.1093/abbs/gmq035] [PMID: 20539939]
[55]
Yeganeh-Hajahmadi, M.; Najafipour, H.; Farzaneh, F.; Esmaeili-Mahani, S.; Joukar, S. Effect of apelin on cardiac contractility in acute reno-vascular hypertension: The role of apelin receptor and kappa opioid receptor heterodimerization. Iran. J. Basic Med. Sci., 2018, 21(12), 1305-1315.
[PMID: 30627376]
[56]
Yeganeh-Hajahmadi, M.; Najafipour, H.; Rostamzadeh, F. The differential effects of low and high doses of apelin through opioid receptors on the blood pressure of rats with renovascular hypertension. Hypertens. Res., 2017, 40(8), 732-737.
[http://dx.doi.org/10.1038/hr.2017.28] [PMID: 28275232]
[57]
Barki-Harrington, L.; Luttrell, L.M.; Rockman, H.A. Dual inhibition of β-adrenergic and angiotensin II receptors by a single antagonist: A functional role for receptor-receptor interaction in vivo. Circulation, 2003, 108(13), 1611-1618.
[http://dx.doi.org/10.1161/01.CIR.0000092166.30360.78] [PMID: 12963634]
[58]
Kao, T.K.; Ou, Y.C.; Liao, S.L.; Chen, W.Y.; Wang, C.C.; Chen, S.Y.; Chiang, A.N.; Chen, C.J. Opioids modulate post-ischemic progression in a rat model of stroke. Neurochem. Int., 2008, 52(6), 1256-1265.
[http://dx.doi.org/10.1016/j.neuint.2008.01.007] [PMID: 18294735]
[59]
Chen, C.H.; Toung, T.J.K.; Hurn, P.D.; Koehler, R.C.; Bhardwaj, A. Ischemic neuroprotection with selective κ-opioid receptor agonist is gender specific. Stroke, 2005, 36(7), 1557-1561.
[http://dx.doi.org/10.1161/01.STR.0000169928.76321.3d] [PMID: 15933260]
[60]
Qi, W.; Smith, F.G. Kappa opioids modulate the arterial baroreflex control of heart rate in conscious young sheep. Can. J. Physiol. Pharmacol., 2007, 85(8), 811-817.
[http://dx.doi.org/10.1139/Y07-074] [PMID: 17901891]
[61]
Wang, C.; Bian, W.; Xia, C.; Zhang, T.; Guillemot, F.; Jing, N. Visualization of bHLH transcription factor interactions in living mammalian cell nuclei and developing chicken neural tube by FRET. Cell Res., 2006, 16(6), 585-598.
[http://dx.doi.org/10.1038/sj.cr.7310076] [PMID: 16775630]
[62]
Rostamzadeh, F.; Najafipour, H.; Yeganeh-Hajahmadi, M.; Esmaeili-mahani, S.; Joukar, S.; Iranpour, M. Heterodimerization of apelin and opioid receptors and cardiac inotropic and lusitropic effects of apelin in 2K1C hypertension: Role of pERK1/2 and PKC. Life Sci., 2017, 191, 24-33.
[http://dx.doi.org/10.1016/j.lfs.2017.09.044] [PMID: 28987634]
[63]
Xu, N.; Wang, H.; Fan, L.; Chen, Q. Supraspinal administration of apelin-13 induces antinociception via the opioid receptor in mice. Peptides, 2009, 30(6), 1153-1157.
[http://dx.doi.org/10.1016/j.peptides.2009.02.011] [PMID: 19463749]
[64]
Prado, G.N.; Taylor, L.; Zhou, X.; Ricupero, D.; Mierke, D.F.; Polgar, P. Mechanisms regulating the expression, self-maintenance, and signaling-function of the bradykinin B2 and B1 receptors. J. Cell. Physiol., 2002, 193(3), 275-286.
[http://dx.doi.org/10.1002/jcp.10175] [PMID: 12384980]
[65]
Howl, J.; Payne, S.J. Bradykinin receptors as a therapeutic target. Expert Opin. Ther. Targets, 2003, 7(2), 277-285.
[http://dx.doi.org/10.1517/14728222.7.2.277] [PMID: 12667103]
[66]
Ji, B.; Shang, L.; Wang, C.; Wan, L.; Cheng, B.; Chen, J. Roles for heterodimerization of APJ and B2R in promoting cell proliferation via ERK1/2-eNOS signaling pathway. Cell. Signal., 2020, 73, 109671.
[http://dx.doi.org/10.1016/j.cellsig.2020.109671] [PMID: 32407761]
[67]
Sierra, S.; Gupta, A.; Gomes, I.; Fowkes, M.; Ram, A.; Bobeck, E.N.; Devi, L.A. Targeting cannabinoid 1 and delta opioid receptor heteromers alleviates chemotherapy-induced neuropathic pain. ACS Pharmacol. Transl. Sci., 2019, 2(4), 219-229.
[http://dx.doi.org/10.1021/acsptsci.9b00008] [PMID: 31565698]
[68]
Fuxe, K.; Borroto-Escuela, D.O.; Tarakanov, A.O.; Romero-Fernandez, W.; Ferraro, L.; Tanganelli, S.; Perez-Alea, M.; Di Palma, M.; Agnati, L.F. Dopamine D2 heteroreceptor complexes and their receptor–receptor interactions in ventral striatum. Prog. Brain Res., 2014, 211, 113-139.
[http://dx.doi.org/10.1016/B978-0-444-63425-2.00005-2] [PMID: 24968778]
[69]
Toll, L.; Bruchas, M.R.; Calo’, G.; Cox, B.M.; Zaveri, N.T. Nociceptin/orphanin FQ receptor structure, signaling, ligands, functions, and interactions with opioid systems. Pharmacol. Rev., 2016, 68(2), 419-457.
[http://dx.doi.org/10.1124/pr.114.009209] [PMID: 26956246]
[70]
Badal, S.; Turfus, S.; Rajnarayanan, R.; Wilson-Clarke, C.; Sandiford, S.L. Analysis of natural product regulation of opioid receptors in the treatment of human disease. Pharmacol. Ther., 2018, 184, 51-80.
[http://dx.doi.org/10.1016/j.pharmthera.2017.10.021] [PMID: 29097308]
[71]
Lu, J.J.; Polgar, W.E.; Mann, A.; Dasgupta, P.; Schulz, S.; Zaveri, N.T. Differential in vitro pharmacological profiles of structurally diverse nociceptin receptor agonists in activating g protein and beta-arrestin signaling at the human nociceptin opioid receptor. Mol. Pharmacol., 2021, 100(1), 7-18.
[http://dx.doi.org/10.1124/molpharm.120.000076] [PMID: 33958480]
[72]
Mann, A.; Moulédous, L.; Froment, C.; O’Neill, P.R.; Dasgupta, P.; Günther, T.; Brunori, G.; Kieffer, B.L.; Toll, L.; Bruchas, M.R.; Zaveri, N.T.; Schulz, S. Agonist-selective NOP receptor phosphorylation correlates in vitro and in vivo and reveals differential post-activation signaling by chemically diverse agonists. Sci. Signal., 2019, 12(574), eaau8072.
[http://dx.doi.org/10.1126/scisignal.aau8072] [PMID: 30914485]
[73]
Wtorek, K.; Janecka, A. Potential of nociceptin/orphanin FQ peptide analogs for drug development. Chem. Biodivers., 2021, 18(1), e2000871.
[http://dx.doi.org/10.1002/cbdv.202000871] [PMID: 33351271]
[74]
Chen, J.; Wang, Z.; Zhang, R.; Yin, H.; Wang, P.; Wang, C.; Jiang, Y. Heterodimerization of apelin and opioid receptor-like 1 receptors mediates apelin-13-induced G protein biased signaling. Life Sci., 2023, 328, 121892.
[http://dx.doi.org/10.1016/j.lfs.2023.121892] [PMID: 37364634]
[75]
Wang, H.L.; Hsu, C.Y.; Huang, P.C.; Kuo, Y.L.; Li, A.H.; Yeh, T.H.; Tso, A.S.; Chen, Y.L. Heterodimerization of opioid receptor-like 1 and µ-opioid receptors impairs the potency of µ receptor agonist. J. Neurochem., 2005, 92(6), 1285-1294.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02921.x] [PMID: 15748148]
[76]
Evans, R.M.; You, H.; Hameed, S.; Altier, C.; Mezghrani, A.; Bourinet, E.; Zamponi, G.W. Heterodimerization of ORL1 and opioid receptors and its consequences for N-type calcium channel regulation. J. Biol. Chem., 2010, 285(2), 1032-1040.
[http://dx.doi.org/10.1074/jbc.M109.040634] [PMID: 19887453]
[77]
Griffiths, P.R.; Lolait, S.J.; Harris, L.E.; Paton, J.F.R.; O’Carroll, A.M. Vasopressin V1a receptors mediate the hypertensive effects of [Pyr 1 ]apelin-13 in the rat rostral ventrolateral medulla. J. Physiol., 2017, 595(11), 3303-3318.
[http://dx.doi.org/10.1113/JP274178] [PMID: 28255983]
[78]
Goazigo, A.R-L.; Morinville, A.; Burlet, A.; Llorens-Cortes, C.; Beaudet, A. Dehydration-induced cross-regulation of apelin and vasopressin immunoreactivity levels in magnocellular hypothalamic neurons. Endocrinology, 2004, 145(9), 4392-4400.
[http://dx.doi.org/10.1210/en.2004-0384] [PMID: 15166125]
[79]
Hus-Citharel, A.; Bodineau, L.; Frugière, A.; Joubert, F.; Bouby, N.; Llorens-Cortes, C. Apelin counteracts vasopressin-induced water reabsorption via cross talk between apelin and vasopressin receptor signaling pathways in the rat collecting duct. Endocrinology, 2014, 155(11), 4483-4493.
[http://dx.doi.org/10.1210/en.2014-1257] [PMID: 25157454]
[80]
Milligan, G. G protein-coupled receptor hetero-dimerization: Contribution to pharmacology and function. Br. J. Pharmacol., 2009, 158(1), 5-14.
[http://dx.doi.org/10.1111/j.1476-5381.2009.00169.x] [PMID: 19309353]
[81]
Nagano, K.; Kwon, C.; Ishida, J.; Hashimoto, T.; Kim, J.D.; Kishikawa, N.; Murao, M.; Kimura, K.; Kasuya, Y.; Kimura, S.; Chen, Y.C.; Tsuchimochi, H.; Shirai, M.; Pearson, J.T.; Fukamizu, A. Cooperative action of APJ and α1A-adrenergic receptor in vascular smooth muscle cells induces vasoconstriction. J. Biochem., 2019, 166(5), 383-392.
[http://dx.doi.org/10.1093/jb/mvz071] [PMID: 31504625]
[82]
Liu, F.; Wan, Q.; Pristupa, Z.B.; Yu, X.M.; Wang, Y.T.; Niznik, H.B. Direct protein–protein coupling enables cross-talk between dopamine D5 and γ-aminobutyric acid A receptors. Nature, 2000, 403(6767), 274-280.
[http://dx.doi.org/10.1038/35002014] [PMID: 10659839]
[83]
de la Mora, M.P.; Ferré, S.; Fuxe, K. GABA-dopamine receptor-receptor interactions in neostriatal membranes of the rat. Neurochem. Res., 1997, 22(8), 1051-1054.
[http://dx.doi.org/10.1023/A:1022439212836] [PMID: 9239761]
[84]
Wang, M.; Wong, A.H.; Liu, F. Interactions between NMDA and dopamine receptors: A potential therapeutic target. Brain Res., 2012, 1476, 154-163.
[http://dx.doi.org/10.1016/j.brainres.2012.03.029] [PMID: 22472597]
[85]
Lavine, N.; Ethier, N.; Oak, J.N.; Pei, L.; Liu, F.; Trieu, P.; Rebois, R.V.; Bouvier, M.; Hébert, T.E.; Van Tol, H.H.M. G protein-coupled receptors form stable complexes with inwardly rectifying potassium channels and adenylyl cyclase. J. Biol. Chem., 2002, 277(48), 46010-46019.
[http://dx.doi.org/10.1074/jbc.M205035200] [PMID: 12297500]
[86]
Lee, F.J.S.; Pei, L.; Moszczynska, A.; Vukusic, B.; Fletcher, P.J.; Liu, F. Dopamine transporter cell surface localization facilitated by a direct interaction with the dopamine D2 receptor. EMBO J., 2007, 26(8), 2127-2136.
[http://dx.doi.org/10.1038/sj.emboj.7601656] [PMID: 17380124]
[87]
Di Palma, M.; Sartini, S.; Lattanzi, D.; Cuppini, R.; Pita-Rodriguez, M.; Diaz-Carmenate, Y.; Narvaez, M.; Fuxe, K.; Borroto-Escuela, D.O.; Ambrogini, P. Evidence for the existence of A2AR-TrkB heteroreceptor complexes in the dorsal hippocampus of the rat brain: Potential implications of A2AR and TrkB interplay upon ageing. Mech. Ageing Dev., 2020, 190, 111289.
[http://dx.doi.org/10.1016/j.mad.2020.111289] [PMID: 32565059]
[88]
Borroto-Escuela, D.O.; Romero-Fernandez, W.; Pérez-Alea, M.; Narvaez, M.; Tarakanov, A.O.; Mudó, G.; Agnati, L.F.; Ciruela, F.; Belluardo, N.; Fuxe, K. The existence of FGFR1–5-HT1A receptor heterocomplexes in midbrain 5-ht neurons of the rat: Relevance for neuroplasticity. J. Neurosci., 2012, 32(18), 6295-6303.
[http://dx.doi.org/10.1523/JNEUROSCI.4203-11.2012]
[89]
Antushevich, H.; Wójcik, M. Review: Apelin in disease. Clin. Chim. Acta, 2018, 483, 241-248.
[http://dx.doi.org/10.1016/j.cca.2018.05.012] [PMID: 29750964]
[90]
Bulenger, S.; Marullo, S.; Bouvier, M. Emerging role of homo- and heterodimerization in G-protein-coupled receptor biosynthesis and maturation. Trends Pharmacol. Sci., 2005, 26(3), 131-137.
[http://dx.doi.org/10.1016/j.tips.2005.01.004] [PMID: 15749158]

Rights & Permissions Print Cite
Article Metrics
28
1
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy