Apelin Receptor Signaling During Mesoderm Development
- 549 Downloads
Abstract
The Apelin receptor (Aplnr) is a G-protein coupled receptor which has a wide body distribution and various physiological roles including homeostasis, angiogenesis, cardiovascular and neuroendocrine function. Apelin and Elabela are two peptide components of the Aplnr signaling and are cleaved to give different isoforms which are active in different tissues and organisms.
Aplnr signaling is related to several pathologies including obesity, heart disases and cancer in the adult body. However, the developmental role in mammalian embryogenesis is crucial for migration of early cardiac progenitors and cardiac function. Aplnr and peptide components have a role in proliferation, differentiation and movement of endodermal precursors. Although expression of Aplnr signaling is observed in endodermal lineages, the main function is the control of mesoderm cell movement and cardiac development. Mutant of the Aplnr signaling components results in the malformations, defects and lethality mainly due to the deformed heart function. This developmental role share similarity with the cardiovascular functions in the adult body.
Determination of Aplnr signaling and underlying mechanisms during mammalian development might enable understanding of regulatory molecular mechanisms which not only control embryonic development process but also control tissue function and disease pathology in the adult body.
Keywords
Apelin Apelin receptor Development Elabela MesodermAbbreviations
- ACTH
Adrenocorticotropic Hormone
- Aplnr
Apelin Receptor
- AVP
Arginine Vasopressin Hormone
- bFGF
Basic Fibroblast Growth Factor
- BMP-4
Bone Morphogenic Protein-4
- CD
Cluster of Differentiation
- CNS
Central Nervous System
- DNA
Deoxyribonucleic Acid
- Ela
Elabela
- EMT
Epithelial to Mesenchymal Transition
- eNOS
Endothelial Nitric Oxide Synthase
- FGF
Fibroblast Growth Factor
- FOXF-1
Forkhead Box F-1
- GATA-4
GATA Binding Protein-4
- HAND-1
Heart- and Neural Crest Derivatives-Expressed Protein-1
- hESCs
Human Embryonic Stem Cells
- HIV
Human Immunodeficiency Virus
- HUVEC
Human Umbilical Vein Endothelial Cells
- IFN
Interferon
- IL
Interleukin
- IRX-3
Iroquois-class Homeodomain Protein-3
- KO
Knock Out
- MEOX-1
Mesenchyme Homeobox-1
- mESCs
Mouse Embryonic Stem Cells
- mRNA
Messenger Ribonucleic Acid
- MYH-6
Myosin Heavy Chain-6
- Nkx-2.5
NK-2 Homeobox-5
- OXY
Oxytocin
- PAX-3
Paired Box-3
- PHA
Phytohemagglutinin
- PVN
Paraventricular Nucleus
- siRNA
Small Interfering Ribonucleic Acid
- SON
Supraoptic Nucleus
- TBX-5
T-box transcription factor-5
- TCF-15
Transcription Factor-15
- TDGF-1
Teratocarcinoma-Derived Growth Factor-1
- TGF-β
Transforming Growth Factor Beta
- VSMCs
Vascular Smooth Muscle Cells
Notes
Acknowledegement
This study was supported by TÜBİTAK 2232 International Fellowship for Outstanding Researchers Program (Project no: 118C186). Authors declare no conflict of interest.
References
- Ang S-LBRR (2002) Anterior-posterior patterning of the mouse body axis at gastrulation. In: Rossant JTPL (ed) Mouse development. Academic, pp 37–53. https://doi.org/10.1016/B978-012597951-1/50005-6
- Bakkum BW, Bachop WE (2013) Development of the spine and spinal cord. In: Clinical anatomy of the spine, spinal cord, and ANS. Elsevier Inc, pp 541–565. https://doi.org/10.1016/B978-0-323-07954-9.00012-8
- Bellairs R, Osmond M (2014) Establishment of the embryonic body. In: The atlas of chick development, 3rd edn. Elsevier, pp 29–43. https://doi.org/10.1016/b978-0-12-384951-9.00004-6
- Boucher J, Masri B, Daviaud D, Gesta S, Guigné C, Mazzucotelli A et al (2005) Apelin, a newly identified adipokine up-regulated by insulin and obesity. Endocrinology 146:1764–1771. https://doi.org/10.1210/en.2004-1427CrossRefGoogle Scholar
- Carlson BM (2015) Gastrulation and germ layer formation. In: Reference module in biomedical research. Elsevier. https://doi.org/10.1016/b978-0-12-801238-3.05432-5
- Chapman NA, Dupré DJ, Rainey JK (2014) The apelin receptor: physiology, pathology, cell signalling, and ligand modulation of a peptide-activated class A GPCR. Biochem Cell Biol 92:431–440. https://doi.org/10.1139/bcb-2014-0072CrossRefGoogle Scholar
- Charo DN, Ho M, Fajardo G, Kawana M, Kundu RK, Sheikh AY et al (2009) Endogenous regulation of cardiovascular function by apelin-APJ. Am J Physiol Heart Circ Physiol 297. https://doi.org/10.1152/ajpheart.00686.2009
- Cheng B, Chen J, Bai B, Xin Q (2012) Neuroprotection of apelin and its signaling pathway. Peptides 37:171–173. https://doi.org/10.1016/j.peptides.2012.07.012CrossRefGoogle Scholar
- Chng SC, Ho L, Tian J, Reversade B (2013) ELABELA: a hormone essential for heart development signals via the apelin receptor. Dev Cell 27:672–680. https://doi.org/10.1016/j.devcel.2013.11.002CrossRefGoogle Scholar
- Choe H, Farzan M, Konkel M, Martin K, Sun Y, Marcon L et al (1998) The orphan seven-transmembrane receptor Apj supports the entry of primary T-cell-line-tropic and Dualtropic human immunodeficiency virus type 1. J Virol 72:6113–6118. https://doi.org/10.1128/jvi.72.7.6113-6118.1998CrossRefGoogle Scholar
- Choe W, Albright A, Sulcove J, Jaffer S, Hesselgesser J, Lavi E et al (2000) Functional expression of the seven-transmembrane HIV-1 co-receptor APJ in neural cells. J Neurovirol 6:S61–S69CrossRefGoogle Scholar
- Clarke KJ, Whitaker KW, Reyes TM (2009) Diminished metabolic responses to centrally-administered apelin-13 in diet-induced obese rats fed a high-fat diet. J Neuroendocrinol 21:83–89. https://doi.org/10.1111/j.1365-2826.2008.01815.xCrossRefGoogle Scholar
- D’Aniello C, Lonardo E, Iaconis S, Guardiola O, Liguoro AM, Liguori GL et al (2009) G protein-coupled receptor APJ and its ligand apelin act downstream of cripto to specify embryonic stem cells toward the cardiac lineage through extracellular signal-regulated kinase/p70S6 kinase signaling pathway. Circ Res 105:231–238. https://doi.org/10.1161/CIRCRESAHA.109.201186CrossRefGoogle Scholar
- De Mota N, Lenkei Z, Llorens-Cortès C (2000) Cloning, pharmacological characterization and brain distribution of the rat apelin receptor. Neuroendocrinology 72:400–407. https://doi.org/10.1159/000054609CrossRefGoogle Scholar
- Deng C, Chen H, Yang N, Feng Y, Hsueh AJW (2015) Apela regulates fluid homeostasis by binding to the APJ receptor to activate Gi signaling. J Biol Chem 290:18261–18268. https://doi.org/10.1074/jbc.M115.648238CrossRefGoogle Scholar
- Deshwar AR, Chng SC, Ho L, Reversade B, Scott IC (2016) The Apelin receptor enhances Nodal/TGFβ signaling to ensure proper cardiac development. elife 5. https://doi.org/10.7554/eLife.13758
- Devic E, Paquereau L, Vernier P, Knibiehler B, Audigier Y (1996) Expression of a new G protein-coupled receptor X-msr is associated with an endothelial lineage in Xenopus laevis. Mech Dev 59:129–140. https://doi.org/10.1016/0925-4773(96)00585-0CrossRefGoogle Scholar
- Doğan A (2019) Apelin receptor (Aplnr) signaling promotes fibroblast migration. Tissue Cell 56:98–106. https://doi.org/10.1016/j.tice.2019.01.003CrossRefGoogle Scholar
- Dunn NR, Vincent SD, Oxburgh L, Robertson EJ, Bikoff EK (2004) Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo. Development 131:1717–1728. https://doi.org/10.1242/dev.01072CrossRefGoogle Scholar
- Eberlé D, Marousez L, Hanssens S, Knauf C, Breton C, Deruelle P et al (2019) Elabela and Apelin actions in healthy and pathological pregnancies. Cytokine Growth Factor Rev 46:45–53. https://doi.org/10.1016/j.cytogfr.2019.03.003CrossRefGoogle Scholar
- Edinger AL, Hoffman TL, Sharron M, Lee B, Yi Y, Choe W et al (1998) An orphan seven-transmembrane domain receptor expressed widely in the brain functions as a coreceptor for human immunodeficiency virus type 1 and simian immunodeficiency virus. J Virol 72:7934–7940. https://doi.org/10.1128/jvi.72.10.7934-7940.1998CrossRefGoogle Scholar
- Folino A, Montarolo PG, Samaja M, Rastaldo R (2015) Effects of apelin on the cardiovascular system. Heart Fail Rev 20:505–518. https://doi.org/10.1007/s10741-015-9475-xCrossRefGoogle Scholar
- Freyer L, Hsu CW, Nowotschin S, Pauli A, Ishida J, Kuba K et al (2017) Loss of Apela peptide in mice causes low penetrance embryonic lethality and defects in early mesodermal derivatives. Cell Rep 20:2116–2130. https://doi.org/10.1016/j.celrep.2017.08.014CrossRefGoogle Scholar
- Georgiadou D, Afink GB, van Dijk M (2019) The apelinergic-axis in human preeclamptic pregnancies: a systematic review. Pregnancy Hypertens 17:148–157. https://doi.org/10.1016/j.preghy.2019.06.002CrossRefGoogle Scholar
- Gheldof A, Berx G (2013) Cadherins and epithelial-to-mesenchymal transition. Prog Mol Biol Transl Sci 116:317–336. Elsevier B.V. https://doi.org/10.1016/B978-0-12-394311-8.00014-5CrossRefGoogle Scholar
- Gilbert SF (2000) Paraxial mesoderm: the somites and their derivatives. In: Developmental biology, 6th edn. Sinauer Associates, SunderlandGoogle Scholar
- Habata Y, Fujii R, Hosoya M, Fukusumi S, Kawamata Y, Hinuma S et al (1999) Apelin, the natural ligand of the orphan receptor APJ, is abundantly secreted in the colostrum. Biochim Biophys Acta, Mol Cell Res 1452:25–35. https://doi.org/10.1016/S0167-4889(99)00114-7CrossRefGoogle Scholar
- Hamada J, Kimura J, Ishida J, Kohda T, Morishita S, Ichihara S et al (2008) Evaluation of novel cyclic analogues of apelin. Int J Mol Med 22:547–552. https://doi.org/10.3892/ijmm_00000054CrossRefGoogle Scholar
- Han S, Englander EW, Gomez GA, Rastellini C, Quertermous T, Kundu RK et al (2015) Pancreatic islet APJ deletion reduces islet density and glucose tolerance in mice. Endocrinology 156:2451–2460. https://doi.org/10.1210/en.2014-1631CrossRefGoogle Scholar
- Hashimoto T, Kihara M, Ishida J, Imai N, Yoshida S, Toya Y et al (2006) Apelin stimulates myosin light chain phosphorylation in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 26:1267–1272. https://doi.org/10.1161/01.ATV.0000218841.39828.91CrossRefGoogle Scholar
- Hassan AS, Hou J, Wei W, Hoodless PA (2010) Expression of two novel transcripts in the mouse definitive endoderm. Gene Expr Patterns 10:127–134. https://doi.org/10.1016/j.gep.2010.02.001CrossRefGoogle Scholar
- Helker CS, Schuermann A, Pollmann C, Chng SC, Kiefer F, Reversade B et al (2015) The hormonal peptide Elabela guides angioblasts to the midline during vasculogenesis. elife. https://doi.org/10.7554/eLife.06726.001
- Ho L, Tan SYX, Wee S, Wu Y, Tan SJC, Ramakrishna NB et al (2015) ELABELA is an endogenous growth factor that sustains hESC self-renewal via the PI3K/AKT pathway. Cell Stem Cell 17:435–447. https://doi.org/10.1016/j.stem.2015.08.010CrossRefGoogle Scholar
- Ho L, Van Dijk M, Chye STJ, Messerschmidt DM, Chng SC, Ong S et al (2017) ELABELA deficiency promotes preeclampsia and cardiovascular malformations in mice. Science (80-) 357:707–713. https://doi.org/10.1126/science.aam6607CrossRefGoogle Scholar
- Hosoya M, Kawamata Y, Fukusumi S, Fujii R, Habata Y, Hinumat S et al (2000) Molecular and functional characteristics of APJ: tissue distribution of mRNA and interaction with the endogenous ligand apelin. J Biol Chem 275:21061–21067. https://doi.org/10.1074/jbc.M908417199CrossRefGoogle Scholar
- Inui M, Fukui A, Ito Y, Asashima M (2006) Xapelin and Xmsr are required for cardiovascular development in Xenopus laevis. Dev Biol 298:188–200. https://doi.org/10.1016/j.ydbio.2006.06.028CrossRefGoogle Scholar
- Ishida J, Hashimoto T, Hashimoto Y, Nishiwaki S, Iguchi T, Harad S, ... & Okunishi H (2004) Regulatory roles for APJ, a seven-transmembrane receptor related to angiotensin-type 1 receptor in blood pressure in vivo. J Biol Chem 279(25):26274–26279Google Scholar
- Iturrioz X, Llorens-Cortes C (2013) Apelin. In: Handbook of biologically active peptides. Elsevier Inc, pp 715–723. https://doi.org/10.1016/B978-0-12-385095-9.00096-8
- Kang Y, Kim J, Anderson JP, Wu J, Scott RG, Kundu RK et al (2013) Apelin-APJ signaling is a critical regulator of endothelial MEF2 activation in cardiovascular development. Circ Res 113:22–31. https://doi.org/10.1161/CIRCRESAHA.113.301324CrossRefGoogle Scholar
- Kapica M, Jankowska A, Antushevich H, Pietrzak P, Bierla JB, Dembinski A et al (2012) The effect of exogenous apelin on the secretion of pancreatic juice in anaesthetized rats. J Physiol Pharmacol 63:53–60Google Scholar
- Kasai A, Ishimaru Y, Kinjo T, Satooka T, Matsumoto N, Yoshioka Y et al (2010) Apelin is a crucial factor for hypoxia-induced retinal angiogenesis. Arterioscler Thromb Vasc Biol 30:2182–2187. https://doi.org/10.1161/ATVBAHA.110.209775CrossRefGoogle Scholar
- Kidoya H, Takakura NJB (2012) Review biology of the apelin-APJ axis in vascular formation. J Biochem 152:125–131. https://doi.org/10.1093/jb/mvs071CrossRefGoogle Scholar
- Kidoya H, Naito H, Muramatsu F, Yamakawa D, Jia W, Ikawa M et al (2015) APJ regulates parallel alignment of arteries and veins in the skin. Dev Cell 33:247–259. https://doi.org/10.1016/j.devcel.2015.02.024CrossRefGoogle Scholar
- Kleinz MJ, Skepper JN, Davenport AP (2005) Immunocytochemical localisation of the apelin receptor, APJ, to human cardiomyocytes, vascular smooth muscle and endothelial cells. Regul Pept 126:233–240. https://doi.org/10.1016/j.regpep.2004.10.019CrossRefGoogle Scholar
- Kovacic JC, Mercader N, Torres M, Boehm M, Fuster V (2012) Epithelial-to-mesenchymal and endothelial-to-mesenchymal transition. Circulation 125:1795–1808. https://doi.org/10.1161/CIRCULATIONAHA.111.040352CrossRefGoogle Scholar
- Ladeiras-Lopes R, Ferreira-Martins J, Leite-Moreira AF (2008) The Apelinergic system: the role played in human physiology and pathology and potential therapeutic applications. Arq Bras Cardiol 90:374–380. https://doi.org/10.1590/S0066-782X2008000500012CrossRefGoogle Scholar
- Lambrecht NWG, Yakubov I, Zer C, Sachs G (2006) Transcriptomes of purified gastric ECL and parietal cells: identification of a novel pathway regulating acid secretion. Physiol Genomics 25:153–165. https://doi.org/10.1152/physiolgenomics.00271.2005CrossRefGoogle Scholar
- Le Goazigo AR, Alvear-Perez R, Zizzari P, Epelbaum J, Bluet-Pajot MT, Llorens-Cortes C (2007) Cellular localization of apelin and its receptor in the anterior pituitary: evidence for a direct stimulatory action of apelin on ACTH release. Am J Physiol Endocrinol Metab 292. https://doi.org/10.1152/ajpendo.00521.2005
- Li F, Li L, Qin X, Pan W, Feng F, Chen F et al (2008) Apelin-induced vascular smooth muscle cell proliferation: the regulation of cyclin D1. Front Biosci 13:3786–3792. https://doi.org/10.2741/2967CrossRefGoogle Scholar
- Liu W, Yan J, Pan W, Tang M (2020) Apelin/Elabela-APJ: a novel therapeutic target in the cardiovascular system. Ann Transl Med 8:243–243. https://doi.org/10.21037/atm.2020.02.07CrossRefGoogle Scholar
- Luo X, Liu J, Zhou H, Chen L (2018) Apelin/APJ system: a critical regulator of vascular smooth muscle cell. J Cell Physiol 233:5180–5188. https://doi.org/10.1002/jcp.26339CrossRefGoogle Scholar
- Maguire JJ, Kleinz MJ, Pitkin SL, Davenport AP (2009) [Pyr1]apelin-13 identified as the predominant apelin isoform in the human heart: vasoactive mechanisms and inotropic action in disease. Hypertension 54:598–604. https://doi.org/10.1161/HYPERTENSIONAHA.109.134619CrossRefGoogle Scholar
- Maroto M, Bone RA, Kim Dale J (2012) Somitogenesis. Development 139:2453–2456. https://doi.org/10.1242/dev.069310CrossRefGoogle Scholar
- Masri B, Knibiehler B, Audigier Y, Lahlou H, Mazarguil H (2002) Apelin (65-77) activates extracellular signal-regulated kinases via a PTX-sensitive G protein. Biochem Biophys Res Commun 290:539–545. https://doi.org/10.1006/bbrc.2001.6230CrossRefGoogle Scholar
- Masri B, Morin N, Cornu M, Knibiehler B, Audigier Y (2004) Apelin (65-77) activates p70 S6 kinase and is mitogenic for umbilical endothelial cells. FASEB J 18:1909–1911. https://doi.org/10.1096/fj.04-1930fjeCrossRefGoogle Scholar
- Masri B, Knibiehler B, Audigier Y (2005) Apelin signalling: a promising pathway from cloning to pharmacology. Cell Signal 17:415–426. https://doi.org/10.1016/j.cellsig.2004.09.018CrossRefGoogle Scholar
- Matsumoto M, Hidaka K, Akiho H, Tada S, Okada M, Yamaguchi T (1996) Low stringency hybridization study of the dopamine D4 receptor revealed D4-like mRNA distribution of the orphan seven-transmembrane receptor, APJ, in human brain. Neurosci Lett 219:119–122. https://doi.org/10.1016/S0304-3940(96)13198-0CrossRefGoogle Scholar
- Medhurst AD, Jennings CA, Robbins MJ, Davis RP, Ellis C, Winborn KY et al (2003) Pharmacological and immunohistochemical characterization of the APJ receptor and its endogenous ligand apelin. J Neurochem 84:1162–1172. https://doi.org/10.1046/j.1471-4159.2003.01587.xCrossRefGoogle Scholar
- Mesmin C, Fenaille F, Becher F, Tabet JC, Ezan E (2011) Identification and characterization of apelin peptides in bovine colostrum and milk by liquid chromatography-mass spectrometry. J Proteome Res 10:5222–5231. https://doi.org/10.1021/pr200725xCrossRefGoogle Scholar
- Miura T, Luo Y, Khrebtukova I, Brandenberger R, Zhou D, Scott Thies R et al (2004) Monitoring early differentiation events in human embryonic stem cells by massively parallel signature sequencing and expressed sequence tag scan. Stem Cells Dev 13:694–715. https://doi.org/10.1089/scd.2004.13.694CrossRefGoogle Scholar
- Mughal A, O’Rourke ST (2018) Vascular effects of apelin: mechanisms and therapeutic potential. Pharmacol Ther 190:139–147. https://doi.org/10.1016/j.pharmthera.2018.05.013CrossRefGoogle Scholar
- Murza A, Sainsily X, Coquerel D, Côté J, Marx P, Besserer-Offroy É et al (2016) Discovery and structure-activity relationship of a bioactive fragment of ELABELA that modulates vascular and cardiac functions. J Med Chem 59:2962–2972. https://doi.org/10.1021/acs.jmedchem.5b01549CrossRefGoogle Scholar
- Nebigil CG, Désaubry L (2019) The role of GPCR signaling in cardiac epithelial to mesenchymal transformation (EMT). Trends Cardiovasc Med 29:200–204. https://doi.org/10.1016/j.tcm.2018.08.007CrossRefGoogle Scholar
- Norris ML, Pauli A, Gagnon JA, Lord ND, Rogers KW, Mosimann C et al (2017) Toddler signaling regulates mesodermal cell migration downstream of nodal signaling. elife 6. https://doi.org/10.7554/eLife.22626
- Novakov V, Sandhu GS, Dragomir-Daescu D, Klabusay M (2015) Apelinergic system in endothelial cells and its role in angiogenesis in myocardial ischemia. Vasc Pharmacol 76:1–10. https://doi.org/10.1016/j.vph.2015.08.005CrossRefGoogle Scholar
- O’Carroll AM, Lolait SJ, Harris LE, Pope GR (2013) The apelin receptor APJ: journey from an orphan to a multifaceted regulator of homeostasis. J Endocrinol 219. https://doi.org/10.1530/JOE-13-0227
- O’Donnell LA, Agrawal A, Sabnekar P, Dichter MA, Lynch DR, Kolson DL (2007) Apelin, an endogenous neuronal peptide, protects hippocampal neurons against excitotoxic injury. J Neurochem 102:1905–1917. https://doi.org/10.1111/j.1471-4159.2007.04645.xCrossRefGoogle Scholar
- O’Dowd BF, Heiber M, Chan A, Heng HHQ, Tsui LC, Kennedy JL et al (1993) A human gene that shows identity with the gene encoding the angiotensin receptor is located on chromosome 11. Gene 136:355–360. https://doi.org/10.1016/0378-1119(93)90495-OCrossRefGoogle Scholar
- Ohta S, Suzuki K, Tachibana K, Tanaka H, Yamada G (2007) Development 122:2977–2986. https://doi.org/10.1242/dev.01907CrossRefGoogle Scholar
- Pauli A, Norris ML, Valen E, Chew GL, Gagnon JA, Zimmerman S et al (2014a) Toddler: an embryonic signal that promotes cell movement via apelin receptors. Science (80-) 343:1248636–1248636. https://doi.org/10.1126/science.1248636CrossRefGoogle Scholar
- Pauli A, Norris ML, Valen E, Chew G-L, J a G, Zimmerman S et al (2014b) Toddler: an embryonic signal that promotes cell movement via Apelin receptors. Science 343:1248636. https://doi.org/10.1126/science.1248636CrossRefGoogle Scholar
- Perjés Á, Kilpiö T, Ulvila J, Magga J, Alakoski T, Szabó Z et al (2016) Characterization of apela, a novel endogenous ligand of apelin receptor, in the adult heart. Basic Res Cardiol 111:1–12. https://doi.org/10.1007/s00395-015-0521-6CrossRefGoogle Scholar
- Pitkin SL, Maguire JJ, Bonner TI, Davenport AP (2010) International Union of Basic and Clinical Pharmacology. LXXIV. Apelin receptor nomenclature, distribution, pharmacology, and function. Pharmacol Rev 62:331–342. https://doi.org/10.1124/pr.110.002949CrossRefGoogle Scholar
- Pope GR, Roberts EM, Lolait SJ, O’Carroll AM (2012) Central and peripheral apelin receptor distribution in the mouse: species differences with rat. Peptides 33:139–148. https://doi.org/10.1016/j.peptides.2011.12.005CrossRefGoogle Scholar
- Read C, Nyimanu D, Williams TL, Huggins DJ, Sulentic P, Macrae RGC et al (2019) 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 71:467–502. https://doi.org/10.1124/pr.119.017533CrossRefGoogle Scholar
- Reaux A, De Mota N, Skultetyova I, Lenkei Z, El Messari S, Gallatz K et al (2001) Physiological role of a novel neuropeptide, apelin, and its receptor in the rat brain. J Neurochem 77:1085–1096. https://doi.org/10.1046/j.1471-4159.2001.00320.xCrossRefGoogle Scholar
- Regard JB, Sato IT, Coughlin SR (2008) Anatomical profiling of G protein-coupled receptor expression. Cell 135:561–571. https://doi.org/10.1016/j.cell.2008.08.040CrossRefGoogle Scholar
- Rehman B, Muzio MR (2019) Embryology, week 2–3 [Updated 2019 Sep 27]. In: StatPearls [Internet]. StatPearls Publishing, Treasure Island, 2020 Jan-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK546679/
- Ringström C, Nitert MD, Bennet H, Fex M, Valet P, Rehfeld JF et al (2010) Apelin is a novel islet peptide. Regul Pept 162:44–51. https://doi.org/10.1016/j.regpep.2010.03.005CrossRefGoogle Scholar
- Roberts EM, Newson MJF, Pope GR, Landgraf R, Lolait SJ, O’Carroll AM (2009) Abnormal fluid homeostasis in apelin receptor knockout mice. J Endocrinol 202:453–462. https://doi.org/10.1677/JOE-09-0134CrossRefGoogle Scholar
- Roberts EM, Pope GR, Newson MJF, Landgraf R, Lolait SJ, O’Carroll AM (2010) Stimulus-specific neuroendocrine responses to osmotic challenges in apelin receptor knockout mice. J Neuroendocrinol 22:301–308. https://doi.org/10.1111/j.1365-2826.2010.01968.xCrossRefGoogle Scholar
- Różycka M, Kurowska P, Grzesiak M, Kotula-Balak M, Tworzydło W, Rame C et al (2018) Apelin and apelin receptor at different stages of corpus luteum development and effect of apelin on progesterone secretion and 3β-hydroxysteroid dehydrogenase (3β-HSD) in pigs. Anim Reprod Sci 192:251–260. https://doi.org/10.1016/j.anireprosci.2018.03.021CrossRefGoogle Scholar
- Saint-Geniez M, Masri B, Malecaze F, Knibiehler B, Audigier Y (2002) Expression of the murine msr/apj receptor and its ligand apelin is upregulated during formation of the retinal vessels. Mech Dev 110:183–186. https://doi.org/10.1016/S0925-4773(01)00558-5CrossRefGoogle Scholar
- Scott IC, Masri B, D’Amico LA, Jin SW, Jungblut B, Wehman AM et al (2007) The G protein-coupled receptor Agtrl1b regulates early development of myocardial progenitors. Dev Cell 12:403–413. https://doi.org/10.1016/j.devcel.2007.01.012CrossRefGoogle Scholar
- Sharma B, Ho L, Ford GH, Chen HI, Goldstone AB, Woo YJ et al (2017) Alternative progenitor cells compensate to rebuild the coronary vasculature in Elabela- and Apj-deficient hearts. Dev Cell 42:655–666.e3. https://doi.org/10.1016/j.devcel.2017.08.008CrossRefGoogle Scholar
- Shin K, Kenward C, Rainey JK (2018) Apelinergic system structure and function. Compr Physiol 8:407–450. https://doi.org/10.1002/cphy.c170028CrossRefGoogle Scholar
- Stricker S, Rauschenberger V, Schambony A (2017) ROR-family receptor tyrosine kinases. Curr Top Dev Biol 123:105–142. Academic. https://doi.org/10.1016/bs.ctdb.2016.09.003CrossRefGoogle Scholar
- Taheri S, Murphy K, Cohen M, Sujkovic E, Kennedy A, Dhillo W et al (2002) The effects of centrally administered apelin-13 on food intake, water intake and pituitary hormone release in rats. Biochem Biophys Res Commun 291:1208–1212. https://doi.org/10.1006/bbrc.2002.6575CrossRefGoogle Scholar
- Tam PPL, Parameswaran M, Kinder SJ, Weinberger RP (1997) The allocation of epiblast cells to the embryonic heart and other mesodermal lineages: the role of ingression and tissue movement during gastrulation. Development 124:1631–1642Google Scholar
- Tatemoto K, Hosoya M, Habata Y, Fujii R, Kakegawa T, Zou MX et al (1998) Isolation and characterization of a novel endogenous peptide ligand for the human APJ receptor. Biochem Biophys Res Commun 251:471–476. https://doi.org/10.1006/bbrc.1998.9489CrossRefGoogle Scholar
- Tatemoto K, Takayama K, Zou MX, Kumaki I, Zhang W, Kumano K et al (2001) The novel peptide apelin lowers blood pressure via a nitric oxide-dependent mechanism. Regul Pept 99:87–92. https://doi.org/10.1016/S0167-0115(01)00236-1CrossRefGoogle Scholar
- Tissue expression of APLNR – Summary – The Human Protein Atlas (n.d.). https://www.proteinatlas.org/ENSG00000134817-APLNR/tissue. Accessed 31 May 2020
- Uribesalgo I, Hoffmann D, Zhang Y, Kavirayani A, Lazovic J, Berta J et al (2019) Apelin inhibition prevents resistance and metastasis associated with anti-angiogenic therapy. EMBO Mol Med 11. https://doi.org/10.15252/emmm.201809266
- Vodyanik MA, Yu J, Zhang X, Tian S, Stewart R, Thomson JA et al (2010) A mesoderm-derived precursor for mesenchymal stem and endothelial cells. Cell Stem Cell 7:718–729. https://doi.org/10.1016/j.stem.2010.11.011CrossRefGoogle Scholar
- Wang Z, Huang J (2019) Apela promotes cardiomyocyte differentiation from transgenic human embryonic stem cell lines. Appl Biochem Biotechnol 189:396–410. https://doi.org/10.1007/s12010-019-03012-2CrossRefGoogle Scholar
- Wang G, Anini Y, Wei W, Qi X, O’Carroll AM, Mochizuki T et al (2004) Apelin, a new enteric peptide: localization in the gastrointestinal tract, ontogeny, and stimulation of gastric cell proliferation and of cholecystokinin secretion. Endocrinology 145:1342–1348. https://doi.org/10.1210/en.2003-1116CrossRefGoogle Scholar
- Wang INE, Wang X, Ge X, Anderson J, Ho M, Ashley E et al (2012) Apelin enhances directed cardiac differentiation of mouse and human embryonic stem cells. PLoS One 7:e38328. https://doi.org/10.1371/journal.pone.0038328CrossRefGoogle Scholar
- Wang Z, Yu D, Wang M, Wang Q, Kouznetsova J, Yang R et al (2015) Elabela-Apelin receptor signaling pathway is functional in mammalian systems. Sci Rep 5:8170. https://doi.org/10.1038/srep08170CrossRefGoogle Scholar
- Wang L, Zhang Y, Qu H, Xu F, Hu H, Zhang Q et al (2019) Reduced ELABELA expression attenuates trophoblast invasion through the PI3K/AKT/mTOR pathway in early onset preeclampsia. Placenta 87:38–45. https://doi.org/10.1016/j.placenta.2019.08.077CrossRefGoogle Scholar
- Wei L, Hou X, Tatemoto K (2005) Regulation of apelin mRNA expression by insulin and glucocorticoids in mouse 3T3-L1 adipocytes. Regul Pept 132:27–32. https://doi.org/10.1016/j.regpep.2005.08.003CrossRefGoogle Scholar
- Winzell MS, Magnusson C, Ahrén B (2005) The apj receptor is expressed in pancreatic islets and its ligand, apelin, inhibits insulin secretion in mice. Regul Pept 131:12–17. https://doi.org/10.1016/j.regpep.2005.05.004CrossRefGoogle Scholar
- Wu MY, Hill CS (2009) TGF-β superfamily signaling in embryonic development and homeostasis. Dev Cell 16:329–343. https://doi.org/10.1016/j.devcel.2009.02.012CrossRefGoogle Scholar
- Wu D, He L, Chen L (2014) Apelin/APJ system: a promising therapy target for hypertension. Mol Biol Rep 41:6691–6703. https://doi.org/10.1007/s11033-014-3552-4CrossRefGoogle Scholar
- Xi Y, Yu D, Yang R, Zhao Q, Wang J, Zhang H et al (2019) Recombinant Fc-Elabela fusion protein has extended plasma half-life andmitigates post-infarct heart dysfunction in rats. Int J Cardiol 292:180–187. https://doi.org/10.1016/j.ijcard.2019.04.089CrossRefGoogle Scholar
- Xie H, Yuan LQ, Luo XH, Huang J, Cui RR, Guo LJ et al (2007) Apelin suppresses apoptosis of human osteoblasts. Apoptosis 12:247–254. https://doi.org/10.1007/s10495-006-0489-7CrossRefGoogle Scholar
- Xu J, Chen L, Jiang Z, Li L (2018) Biological functions of Elabela, a novel endogenous ligand of APJ receptor. J Cell Physiol. https://doi.org/10.1002/jcp.26492
- Yang H, Bednarek MA, Spurlock SM, Paavola KJ, Ko B, To C et al (2017) Apelin-36 modulates blood glucose and body weight independently of canonical APJ receptor signaling * Hadas Galon-Tilleman ‡1. J Biol Chem 292:1925–1933. https://doi.org/10.1074/jbc.M116.748103CrossRefGoogle Scholar
- Yu QC, Hirst CE, Costa M, Ng ES, Schiesser JV, Gertow K et al (2012) Apelin promotes hematopoiesis from human embryonic stem cells. Blood 119:6243–6254. https://doi.org/10.1182/blood-2011-12-396093CrossRefGoogle Scholar
- Zeng XXI, Wilm TP, Sepich DS, Solnica-Krezel L (2007) Apelin and its receptor control heart field formation during zebrafish gastrulation. Dev Cell 12:391–402. https://doi.org/10.1016/j.devcel.2007.01.011CrossRefGoogle Scholar
- Zhen EY, Higgs RE, Gutierrez JA (2013) Pyroglutamyl apelin-13 identified as the major apelin isoform in human plasma. Anal Biochem 442:1–9. https://doi.org/10.1016/j.ab.2013.07.006CrossRefGoogle Scholar
- Zhong JC, Yu XY, Huang Y, Yung LM, Lau CW, Lin SG (2007) Apelin modulates aortic vascular tone via endothelial nitric oxide synthase phosphorylation pathway in diabetic mice. Cardiovasc Res 74:388–395. https://doi.org/10.1016/j.cardiores.2007.02.002CrossRefGoogle Scholar
- Zhou L, Sun H, Cheng R, Fan X, Lai S, Deng C (2019) ELABELA, as a potential diagnostic biomarker of preeclampsia, regulates abnormally shallow placentation via APJ. Am J Physiol Metab 316:E773–E781. https://doi.org/10.1152/ajpendo.00383.2018CrossRefGoogle Scholar
- Zou MX, Liu HY, Haraguchi Y, Soda Y, Tatemoto K, Hoshino H (2000) Apelin peptides block the entry of human immunodeficiency virus (HIV). FEBS Lett 473:15–18. https://doi.org/10.1016/S0014-5793(00)01487-3CrossRefGoogle Scholar