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2023, Number 1

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TIP Rev Esp Cienc Quim Biol 2023; 26 (1)

Coordinated activation of cell surface receptors: physiological repercussions

Lee-Rivera I, López E, López CAM
Full text How to cite this article

Language: Spanish
References: 108
Page: 1-17
PDF size: 608.87 Kb.


Key words:

GPCRs, Protease-activated receptors, transactivation, signal transduction.

ABSTRACT

For a long time, G-protein-coupled receptors (GPCRs) were considered monomeric and only occasionally interacted with other receptors, mainly members of their own family. This concept has recently changed, and there is ever-growing evidence that this is not the case, thus diversifying their function and ability to respond to the environment. The process by which a membrane receptor triggers signaling pathways from a second one in the absence of protein synthesis is referred to as “transactivation”. This brief review will focus on the intracellular mechanisms and physio-pathological implications of the transactivation process, emphasizing its participation in the regulation of protease-activated receptors (PARs). These were among the first GPCRs for which receptorreceptor interaction was described, thus amplifying their function in a wide variety of tissues and contexts. This new level of molecular interrelation among receptors represents a great opportunity for the development of new therapeutic protocols.


REFERENCES

  1. Alberelli, M. A., & de Candia, E. (2014). Functional role ofprotease activated receptors in vascular biology. In VascularPharmacology (Vol. 62, Issue 2, pp. 72–81). Elsevier Inc.https://doi.org/10.1016/j.vph.2014.06.001

  2. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts,K., & Walter, P. (2002). General Principles of CellCommunication. https://www.ncbi.nlm.nih.gov/books/NBK26813/

  3. Almonte, A. G., Hamill, C. E., Chhatwal, J. P., Wingo, T. S.,Barber, J. A., Lyuboslavsky, P. N., David Sweatt, J., Ressler,K. J., White, D. A., & Traynelis, S. F. (2007). Learningand memory deficits in mice lacking protease activatedreceptor-1. Neurobiology of Learning and Memory, 88(3),295–304. https://doi.org/10.1016/J.NLM.2007.04.004

  4. Almonte, A. G., Qadri, L. H., Sultan, F. A., Watson, J. A.,Mount, D. J., Rumbaugh, G., & Sweatt, J. D. (2013).Protease-activated receptor-1 modulates hippocampalmemory formation and synaptic plasticity. Journal ofNeurochemistry, 124(1), 109. https://doi.org/10.1111/JNC.12075

  5. Amadesi, S., Cottrell, G. S., Divino, L., Chapman, K., Grady,E. F., Bautista, F., Karanjia, R., Barajas-Lopez, C., Vanner,S., Vergnolle, N., & Bunnett, N. W. (2006). Proteaseactivatedreceptor 2 sensitizes TRPV1 by protein kinaseCε- and A-dependent mechanisms in rats and mice. Journalof Physiology, 575(2), 555–571. https://doi.org/10.1113/jphysiol.2006.111534

  6. Asokananthan, N., Graham, P. T., Fink, J., Knight, D. A., Bakker,A. J., McWilliam, A. S., Thompson, P. J., & Stewart, G. A.(2002). Activation of Protease-Activated Receptor (PAR)-1,PAR-2, and PAR-4 Stimulates IL-6, IL-8, and ProstaglandinE 2 Release from Human Respiratory Epithelial Cells. TheJournal of Immunology, 168(7), 3577–3585. https://doi.org/10.4049/jimmunol.168.7.3577

  7. Bai, M. (2004). Dimerization of G-protein-coupled receptors:roles in signal transduction. Cellular Signalling, 16(2),175–186. https://doi.org/10.1016/S0898-6568(03)00128-1

  8. Bang, E. J., Kim, D. H., & Chung, H. Y. (2021). Proteaseactivatedreceptor 2 induces ROS-mediated inflammationthrough Akt-mediated NF-κB and FoxO6 modulationduring skin photoaging. Redox Biology, 44. https://doi.org/10.1016/J.REDOX.2021.102022

  9. Bergmann, S., Junker, K., Henklein, P., Hollenberg, M. D.,Settmacher, U., & Kaufmann, R. (2006). PAR-type thrombinreceptors in renal carcinoma cells: PAR1-mediated EGFRactivation promotes cell migration. Oncology Reports,15(4), 889–893.

  10. Blackhart, B. D., Emilsson, K., Nguyen, D., Teng, W., Martelli,A. J., Nystedt, S., Sundelin, J., & Scarborough, R. M. (1996).Ligand cross-reactivity within the protease-activatedreceptor family. Journal of Biological Chemistry, 271(28),16466–16471. https://doi.org/10.1074/jbc.271.28.16466

  11. Burch, M. L., Ballinger, M. L., Yang, S. N. Y., Getachew, R.,Itman, C., Loveland, K., Osman, N., & Little, P. J. (2010a).Thrombin stimulation of proteoglycan synthesis in vascularsmooth muscle is mediated by protease-activated receptor-1transactivation of the transforming growth factor βtypeI receptor. Journal of Biological Chemistry, 285(35),26798–26805. https://doi.org/10.1074/jbc.M109.092767

  12. Burch, M. L., Ballinger, M. L., Yang, S. N. Y., Getachew, R.,Itman, C., Loveland, K., Osman, N., & Little, P. J. (2010b).Thrombin stimulation of proteoglycan synthesis in vascularsmooth muscle is mediated by protease-activated receptor-1transactivation of the transforming growth factor βtypeI receptor. Journal of Biological Chemistry, 285(35),26798–26805. https://doi.org/10.1074/jbc.M109.092767

  13. Burch, M. L., Osman, N., Getachew, R., Al-Aryahi, S., Poronnik,P., Zheng, W., Hill, M. A., & Little, P. J. (2012). G proteincoupled receptor transactivation: Extending the paradigm toinclude serine/threonine kinase receptors. In InternationalJournal of Biochemistry and Cell Biology (Vol. 44, Issue5, pp. 722–727). Elsevier Ltd. https://doi.org/10.1016/j.biocel.2012.01.018

  14. Burke, K. J., & Bender, K. J. (2019). Modulation of IonChannels in the Axon: Mechanisms and Function. Frontiersin Cellular Neuroscience, 13. https://doi.org/10.3389/FNCEL.2019.00221

  15. Burnier, L., & Mosnier, L. O. (2013). Novel mechanisms foractivated protein C cytoprotective activities involvingnoncanonical activation of protease-activated receptor3. Blood, 122(5), 807–816. https://doi.org/10.1182/blood-2013-03-488957

  16. Caruso, R., Pallone, F., Fina, D., Gioia, V., Peluso, I., Caprioli,F., Stolfi, C., Perfetti, A., Spagnoli, L. G., Palmieri, G.,MacDonald, T. T., & Monteleone, G. (2006). Proteaseactivatedreceptor-2 activation in gastric cancer cellspromotes epidermal growth factor receptor trans-activationand proliferation. American Journal of Pathology, 169(1),268–278. https://doi.org/10.2353/ajpath.2006.050841

  17. Cattaneo, F., Castaldo, M., Parisi, M., Faraonio, R., Esposito,G., & Ammendola, R. (2018). Formyl peptide receptor1 modulates endothelial cell functions by NADPHoxidase-dependent VEGFR2 transactivation. OxidativeMedicine and Cellular Longevity, 2018. https://doi.org/10.1155/2018/2609847

  18. Cattaneo, F., Guerra, G., Parisi, M., De Marinis, M., Tafuri,D., Cinelli, M., & Ammendola, R. (2014). Cell-surfacereceptors transactivation mediated by G protein-coupledreceptors. In International Journal of Molecular Sciences(Vol. 15, Issue 11, pp. 19700–19728). MDPI AG. https://doi.org/10.3390/ijms151119700

  19. Cattaneo, F., Iaccio, A., Guerra, G., Montagnani, S., &Ammendola, R. (2011). NADPH-oxidase-dependentreactive oxygen species mediate EGFR transactivation byFPRL1 in WKYMVm-stimulated human lung cancer cells.Free Radical Biology and Medicine, 51(6), 1126–1136.https://doi.org/10.1016/j.freeradbiomed.2011.05.040

  20. Chandrasekharan, U. M., Waitkus, M., Kinney, C. M., Walters-Stewart, A., & Dicorleto, P. E. (2010). Synergistic inductionof mitogen-activated protein kinase phosphatase-1 bythrombin and epidermal growth factor requires vascularendothelial growth factor receptor-2. Arteriosclerosis,Thrombosis, and Vascular Biology, 30(10), 1983–1989.https://doi.org/10.1161/ATVBAHA.110.212399

  21. Chang, J. Z.-C., Hsieh, Y.-P., Lin, W.-H., Chen, H.-M., & Kuo,M. Y.-P. (2017). Activation of transforming growth factor-β1by thrombin via integrins αvβ1, αvβ3, and αvβ5 in buccalfibroblasts: Suppression by epigallocatechin-3-gallate.Head & Neck, 39(7), 1436–1445. https://doi.org/10.1002/HED.24791

  22. Chaplin, R., Thach, L., Hollenberg, M. D., Cao, Y., Little, P. J.,& Kamato, D. (2017). Insights into cellular signalling byG protein coupled receptor transactivation of cell surfaceprotein kinase receptors. Journal of Cell Communicationand Signaling, 11(2), 117–125. https://doi.org/10.1007/S12079-017-0375-9

  23. Chen, J., Ishii, M., Wang, L., Ishii, K., & Coughlin, S. R.(1994). Thrombin receptor activation. Confirmation of theintramolecular tethered liganding hypothesis and discoveryof an alternative intermolecular liganding mode. Journalof Biological Chemistry, 269(23), 16041–16045. https://doi.org/10.1016/s0021-9258(17)33970-4

  24. Chung, H., Ramachandran, R., Hollenberg, M. D., & Muruve,D. (2013). Proteinase-activated receptor-2 transactivation ofepidermal growth factor receptor and transforming growthfactor-β receptor signaling pathways contributes to renalfibrosis. The Journal of Biological Chemistry, 288(52),37319–37331. https://doi.org/10.1074/JBC.M113.492793

  25. Covic, L., Gresser, A. L., & Kuliopulos, A. (2000). Biphasickinetics of activation and signaling for PAR1 and PAR4thrombin receptors in platelets. Biochemistry, 39(18).https://doi.org/10.1021/bi9927078

  26. Darmoul, D., Gratio, V., Devaud, H., & Laburthe, M. (2004).Protease-activated receptor 2 in colon cancer: TrypsininducedMAPK phosphorylation and cell proliferationare mediated by epidermal growth factor receptortransactivation. Journal of Biological Chemistry, 279(20),20927–20934. https://doi.org/10.1074/jbc.M401430200

  27. Daub, H., Weiss, F. U., Wallasch, C., & Ullrich, A. (1996).Role of transactivation of the EGF receptor in signalling byG-protein-coupled receptors. Nature, 379(6565), 557–560.https://doi.org/10.1038/379557a0

  28. de La Fuente, M., Noble, D. N., Verma, S., & Nieman, M.T. (2012). Mapping human Protease-activated Receptor4 (PAR4) homodimer interface to transmembrane helix4. Journal of Biological Chemistry, 287(13). https://doi.org/10.1074/jbc.M112.341438

  29. Derynck, R., Akhurst, R. J., & Balmain, A. (2001). TGF-βsignaling in tumor suppression and cancer progression.In Nature Genetics (Vol. 29, Issue 2, pp. 117–129). NatGenet. https://doi.org/10.1038/ng1001-117

  30. Dominguez, Z. (2006). Los prostanoides, una revoluciónautacoide. Anales Venezolanos de Nutrición, 19(2),74–82. http://ve.scielo.org/scielo.php?script=sci_arttext&pid=S0798-07522006000200004&lng=es&nrm=iso&tlng=es

  31. Dorsam, R. T., Tuluc, M., & Kunapuli, S. P. (2004). Role ofprotease-activated and ADP receptor subtypes in thrombingeneration on human platelets. Journal of Thrombosis andHaemostasis, 2(5), 804–812. https://doi.org/10.1111/j.1538-7836.2004.00692.x

  32. El-Daly, M., Saifeddine, M., Mihara, K., Ramachandran, R.,Triggle, C. R., & Hollenberg, M. D. (2014). Proteinaseactivatedreceptors 1 and 2 and the regulation of porcinecoronary artery contractility: A role for distinct tyrosinekinase pathways. British Journal of Pharmacology, 171(9),2413–2425. https://doi.org/10.1111/bph.12593

  33. Feistritzer, C., Lenta, R., & Riewald, M. (2005). Proteaseactivatedreceptors-1 and -2 can mediate endothelialbarrier protection: Role in factor Xa signaling. Journal ofThrombosis and Haemostasis, 3(12), 2798–2805. https://doi.org/10.1111/j.1538-7836.2005.01610.x

  34. Fitzpatrick, F. (2005). Cyclooxygenase Enzymes: Regulationand Function. Current Pharmaceutical Design, 10(6),577–588. https://doi.org/10.2174/1381612043453144

  35. Fujimoto, D., Hirono, Y., Goi, T., Katayama, K., Matsukawa,S., & Yamaguchi, A. (2010). The activation of Proteinase-Activated Receptor-1 (PAR1) mediates gastric cancer cellproliferation and invasion. BMC Cancer, 10(443). https://doi.org/10.1186/1471-2407-10-443

  36. Gan, J., Greenwood, S. M., Cobb, S. R., & Bushell, T. J.(2011). Indirect modulation of neuronal excitability andsynaptic transmission in the hippocampus by activationof proteinase-activated receptor-2. British Journal ofPharmacology, 163(5), 984–994. https://doi.org/10.1111/j.1476-5381.2011.01293.x

  37. Gieseler, F., Ungefroren, H., Settmacher, U., Hollenberg, M.D., & Kaufmann, R. (2013). Proteinase-activated receptors(PARs) - Focus on receptor-receptor- interactions andtheir physiological and pathophysiological impact. In CellCommunication and Signaling (Vol. 11, Issue 1). https://doi.org/10.1186/1478-811X-11-86

  38. Guo, H., Liu, D., Gelbard, H., Cheng, T., Insalaco, R., Fernández,J. A., Griffin, J. H., & Zlokovic, B. v. (2004). ActivatedProtein C Prevents Neuronal Apoptosis via ProteaseActivated Receptors 1 and 3. Neuron, 41(4), 563–572.https://doi.org/10.1016/S0896-6273(04)00019-4

  39. Han, K. S., Mannaioni, G., Hamill, C. E., Lee, J., Junge, C. E.,Lee, C. J., & Traynelis, S. F. (2011). Activation of proteaseactivated receptor 1 increases the excitability of the dentategranule neurons of hippocampus. Molecular Brain, 4(1).https://doi.org/10.1186/1756-6606-4-32

  40. Han, X., & Nieman, M. T. (2020). The domino effect triggeredby the tethered ligand of the protease activated receptors.Thrombosis Research, 196, 87–98. https://doi.org/10.1016/j.thromres.2020.08.004

  41. Hardie, R. C., & Minke, B. (1992). The trp gene is essential fora light-activated Ca2+ channel in Drosophila photoreceptors.Neuron, 8(4), 643–651. https://doi.org/https://doi.org/10.1016/0896-6273(92)90086-S

  42. Hawkins, B. J., Solt, L. A., Chowdhury, I., Kazi, A. S., Abid,M. R., Aird, W. C., May, M. J., Foskett, J. K., & Madesh,M. (2007). G Protein-Coupled Receptor Ca2+-LinkedMitochondrial Reactive Oxygen Species Are Essentialfor Endothelial/Leukocyte Adherence. Molecular andCellular Biology, 27(21), 7582. https://doi.org/10.1128/MCB.00493-07

  43. Henry, P. J. (2006). The protease-activated receptor2 (PAR2)-prostaglandin E2-prostanoid EP receptor axis: A potentialbronchoprotective unit in the respiratory tract? In EuropeanJournal of Pharmacology (Vol. 533, Issues 1–3, pp.156–170). Eur J Pharmacol. https://doi.org/10.1016/j.ejphar.2005.12.051

  44. Holinstat, M., Boutaud, O., Apopa, P. L., Vesci, J., Bala, M.,Oates, J. A., & Hamm, H. E. (2011). Protease-ActivatedReceptor Signaling in Platelets Activates CytosolicPhospholipase A2α Differently for Cyclooxygenase-1 and12-Lipoxygenase Catalysis. Arteriosclerosis, Thrombosis,and Vascular Biology, 31(2), 435. https://doi.org/10.1161/ATVBAHA.110.219527

  45. Holinstat, M., Voss, B., Bilodeau, M. L., McLaughlin, J. N.,Cleator, J., & Hamm, H. E. (2006). PAR4, but not PAR1,signals human platelet aggregation via Ca2+ mobilizationand synergistic P2Y12 receptor activation. Journal ofBiological Chemistry, 281(36), 26665–26674. https://doi.org/10.1074/jbc.M602174200

  46. Hollmann, M., O’Shea-Greenfield, A., Rogers, S. W., &Heinemann, S. (1989). Cloning by functional expressionof a member of the glutamate receptor family. Nature,342(6250), 643–648. https://doi.org/10.1038/342643a0

  47. Hubbard, S. R. (1999). Structural analysis of receptor tyrosinekinases. Progress in Biophysics and Molecular Biology,71(3–4), 343–358. https://doi.org/10.1016/S0079-6107(98)00047-9

  48. Jarry, A., Dorso, L., Gratio, V., Forgue-Lafitte, M. E., Laburthe,M., Laboisse, C. L., & Darmoul, D. (2007). PAR-2 activationincreases human intestinal mucin secretion throughEGFR transactivation. Biochemical and BiophysicalResearch Communications, 364(3), 689–694. https://doi.org/10.1016/j.bbrc.2007.10.073

  49. Jenkins, R. G., Su, X., Su, G., Scotton, C. J., Camerer, E.,Laurent, G. J., Davis, G. E., Chambers, R. C., Matthay,M. A., & Sheppard, D. (2006). Ligation of proteaseactivatedreceptor 1 enhances α vβ6 integrin-dependentTGF-β activation and promotes acute lung injury. Journalof Clinical Investigation, 116(6), 1606–1614. https://doi.org/10.1172/JCI27183

  50. Junge, C., Hubbard, K., Zhang, Z., Olson, J., Hepler, J., Brat,D., & Traynelis, S. (2004). Protease-activated receptor-1in human brain: localization and functional expressionin astrocytes. Experimental Neurology, 188(1), 94–103.https://doi.org/10.1016/J.EXPNEUROL.2004.02.018

  51. Kamato, D., Bhaskarala, V. V., Mantri, N., Oh, T. G., Ling, D.,Janke, R., Zheng, W., Little, P. J., & Osman, N. (2017). RNAsequencing to determine the contribution of kinase receptortransactivation to G protein coupled receptor signalling invascular smooth muscle cells. PLoS ONE, 12(7). https://doi.org/10.1371/JOURNAL.PONE.0180842

  52. Kamato, D., Do, B. H., Osman, N., Ross, B. P., Mohamed,R., Xu, S., & Little, P. J. (2020). Smad linker regionphosphorylation is a signalling pathway in its own rightand not only a modulator of canonical TGF-β signalling.Cellular and Molecular Life Sciences, 77(2), 243–251.https://doi.org/10.1007/S00018-019-03266-3

  53. Kamato, D., Ta, H., Afroz, R., Xu, S., Osman, N., & Little, P.J. (2019). Mechanisms of PAR-1 mediated kinase receptortransactivation: Smad linker region phosphorylation.Journal of Cell Communication and Signaling, 13(4), 539.https://doi.org/10.1007/S12079-019-00527-5

  54. Kaneider, N. C., Leger, A. J., Agarwal, A., Nguyen, N., Perides,G., Derian, C., Covic, L., & Kuliopulos, A. (2007a). “Rolereversal” for the receptor PAR1 in sepsis-induced vasculardamage. Nat Immunol, 8(12), 1303–1312. https://doi.org/10.1038/ni1525

  55. Kaneider, N. C., Leger, A. J., Agarwal, A., Nguyen, N., Perides,G., Derian, C., Covic, L., & Kuliopulos, A. (2007b). “Rolereversal” for the receptor PAR1 in sepsis-induced vasculardamage. Nature Immunology, 8(12), 1303–1312. https://doi.org/10.1038/ni1525

  56. Kataoka, H., Hamilton, J. R., McKemy, D. D., Camerer, E.,Zheng, Y. W., Cheng, A., Griffin, C., & Coughlin, S. R.(2003). Protease-activated receptors 1 and 4 mediatethrombin signaling in endothelial cells. Blood, 102(9).https://doi.org/10.1182/blood-2003-04-1130

  57. Kaufmann, R., Hascher, A., Mubbach, F., Henklein, P.,Katenkamp, K., Westermann, M., & Settmacher, U.(2012). Proteinase-activated receptor 2 (PAR2) incholangiocarcinoma (CCA) cells: Effects on signaling andcellular level. Histochemistry and Cell Biology, 138(6),913–924. https://doi.org/10.1007/s00418-012-1006-4

  58. Kaufmann, R., Oettel, C., Horn, A., Halbhuber, K. J., Eitner,A., Krieg, R., Katenkamp, K., Henklein, P., Westermann,M., Böhmer, F. D., Ramachandran, R., Saifeddine, M.,Hollenberg, M. D., & Settmacher, U. (2009). Met receptortyrosine kinase transactivation is involved in proteinaseactivatedreceptor-2-mediated hepatocellular carcinomacell invasion. Carcinogenesis, 30(9), 1487–1496. https://doi.org/10.1093/carcin/bgp153

  59. Kawabata, A., Kubo, S., Ishiki, T., Kawao, N., Sekiguchi, F.,Kuroda, R., Hollenberg, M. D., Kanke, T., & Saito, N. (2004).Proteinase-Activated Receptor-2-Mediated Relaxation inMouse Tracheal and Bronchial Smooth Muscle: SignalTransduction Mechanisms and Distinct Agonist Sensitivity.Journal of Pharmacology and Experimental Therapeutics,311(1), 402–410. https://doi.org/10.1124/JPET.104.068387

  60. Kawabata, A., Matsunami, M., & Sekiguchi, F. (2008).Gastrointestinal roles for proteinase-activated receptorsin health and disease. British Journal of Pharmacology,153(SUPPL. 1). https://doi.org/10.1038/sj.bjp.0707491

  61. Kawao, N., Nagataki, M., Nagasawa, K., Kubo, S., Cushing,K., Wada, T., Sekiguchi, F., Ichida, S., Hollenberg, M.D., MacNaughton, W. K., Nishikawa, H., & Kawabata,A. (2005a). Signal transduction for proteinase-activatedreceptor-2-triggered prostaglandin E2 formation inhuman lung epithelial cells. Journal of Pharmacology andExperimental Therapeutics, 315(2), 576–589. https://doi.org/10.1124/jpet.105.089490

  62. Kawao, N., Nagataki, M., Nagasawa, K., Kubo, S., Cushing,K., Wada, T., Sekiguchi, F., Ichida, S., Hollenberg, M.D., MacNaughton, W. K., Nishikawa, H., & Kawabata,A. (2005b). Signal transduction for proteinase-activatedreceptor-2-triggered prostaglandin E2 formation inhuman lung epithelial cells. Journal of Pharmacology andExperimental Therapeutics, 315(2), 576–589. https://doi.org/10.1124/jpet.105.089490

  63. Komarova, Y. A., Mehta, D., & Malik, A. B. (2007). Dualregulation of endothelial junctional permeability.In Science’s STKE: signal transduction knowledgeenvironment (Vol. 2007, Issue 412). Sci STKE. https://doi.org/10.1126/stke.4122007re8

  64. Lee, C. J., Mannaioni, G., Yuan, H., Woo, D. H., Gingrich,M. B., & Traynelis, S. F. (2007). Astrocytic control ofsynaptic NMDA receptors. Journal of Physiology, 581(3),1057–1081. https://doi.org/10.1113/jphysiol.2007.130377

  65. Lee-Rivera, I., López, E., & López-Colomé, A. M. (2022).Diversification of PAR signaling through receptor crosstalk.Cellular & Molecular Biology Letters, 27(1), 77. https://doi.org/10.1186/S11658-022-00382-0

  66. Lei, H., & Kazlauskas, A. (2014). A Reactive Oxygen Species-Mediated, Self-Perpetuating Loop Persistently ActivatesPlatelet-Derived Growth Factor Receptor α. Molecular andCellular Biology, 34(1), 110–122. https://doi.org/10.1128/mcb.00839-1366. Lin, H., Liu, A. P., Smith, T. H., & Trejo, J. A. (2013). Cofactoringand dimerization of proteinase-activated receptors. InPharmacological Reviews (Vol. 65, Issue 4, pp. 1198–1213).American Society for Pharmacology and ExperimentalTherapeutics. https://doi.org/10.1124/pr.111.004747

  67. Lin, H., & Trejo, J. (2013). Transactivation of the PAR1-PAR2heterodimer by thrombin elicits β-arrestin-mediatedendosomal signaling. Journal of Biological Chemistry,288(16), 11203–11215. https://doi.org/10.1074/jbc.M112.439950

  68. Little, P. J., Burch, M. L., Al-aryahi, S., & Zheng, W. (2011). Theparadigm of G protein receptor transactivation: A mechanisticdefinition and novel example. In TheScientificWorldJournal(Vol. 11, pp. 709–714). ScientificWorldJournal. https://doi.org/10.1100/tsw.2011.75

  69. Lohman, R. J., Jones, N. C., O’Brien, T. J., & Cocks, T. M.(2009). A regulatory role for protease-activated receptor-2in motivational learning in rats. Neurobiology of Learningand Memory, 92(3), 301–309. https://doi.org/10.1016/J.NLM.2009.03.010

  70. Luo, W., Wang, Y., & Reiser, G. (2007). Protease-activatedreceptors in the brain: receptor expression, activation,and functions in neurodegeneration and neuroprotection.Brain Research Reviews, 56(2), 331–345. https://doi.org/10.1016/J.BRAINRESREV.2007.08.002

  71. Madhusudhan, T., Wang, H., Straub, B. K., Gröne, E., Zhou,Q., Shahzad, K., Müller-Krebs, S., Schwenger, V., Gerlitz,B., Grinnell, B. W., Griffin, J. H., Reiser, J., Gröne, H.J., Esmon, C. T., Nawroth, P. P., & Isermann, B. (2012).Cytoprotective signaling by activated protein C requiresprotease-activated receptor-3 in podocytes. Blood, 119(3),874–883. https://doi.org/10.1182/blood-2011-07-365973

  72. Maeda, Y., Sekiguchi, F., Yamanaka, R., Sugimoto, R.,Yamasoba, D., Tomita, S., Nishikawa, H., & Kawabata,A. (2015). Mechanisms for proteinase-activated receptor1-triggered prostaglandin E2 generation in mouseosteoblastic MC3T3-E1 cells. Biological Chemistry, 396(2),153–162. https://doi.org/10.1515/HSZ-2014-0148

  73. Maggio, N., Itsekson, Z., Dominissini, D., Blatt, I., Amariglio,N., Rechavi, G., Tanne, D., & Chapman, J. (2013). Thrombinregulation of synaptic plasticity: Implications for physiologyand pathology. Experimental Neurology, 247, 595–604.https://doi.org/10.1016/J.EXPNEUROL.2013.02.011

  74. Maggio, N., Shavit, E., Chapman, J., & Segal, M. (2008).Thrombin Induces Long-Term Potentiation of Reactivityto Afferent Stimulation and Facilitates Epileptic Seizuresin Rat Hippocampal Slices: Toward Understanding theFunctional Consequences of Cerebrovascular Insults.Journal of Neuroscience, 28(3), 732–736. https://doi.org/10.1523/JNEUROSCI.3665-07.2008

  75. McHowat, J., Creer, M., & Rickard, A. (2001). Stimulationof protease activated receptors on RT4 cells mediatesarachidonic acid release via Ca2+ independent phospholipaseA2. The Journal of Urology, 165(6 Pt 1), 2063–2067. https://doi.org/10.1097/00005392-200106000-00071

  76. McLaughlin, J. N., Patterson, M. M., & Malik, A. B. (2007).Protease-activated receptor-3 (PAR3) regulates PAR1signaling by receptor dimerization. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 104(13), 5662–5667. https://doi.org/10.1073/pnas.0700763104

  77. Moriyuki, K., Sekiguchi, F., Matsubara, K., Nishikawa, H.,& Kawabata, A. (2009). Proteinase-activated receptor-2-triggered prostaglandin E2 release, but not cyclooxygenase-2upregulation, requires activation of the phosphatidylinositol3-kinase / akt / nuclear factor-κB pathway in human alveolarepithelial cells. Journal of Pharmacological Sciences,111(3), 269–275. https://doi.org/10.1254/jphs.09155FP

  78. Mußbach, F., Henklein, P., Westermann, M., Settmacher,U., Böhmer, F. D., & Kaufmann, R. (2015). Proteinaseactivatedreceptor 1- and 4-promoted migration of Hep3Bhepatocellular carcinoma cells depends on ROS formationand RTK transactivation. Journal of Cancer Researchand Clinical Oncology, 141(5), 813–825. https://doi.org/10.1007/S00432-014-1863-4

  79. Nakanishi-Matsui, M., Zheng, Y. W., Sulciner, D. J., Welss,E. J., Ludeman, M. J., & Coughlin, S. R. (2000). PAR3is a cofactor for PAR4 activation by thrombin. Nature,404(6778), 609–613. https://doi.org/10.1038/35007085

  80. Ossovskaya, V. S., & Bunnett, N. W. (2004). Protease-ActivatedReceptors: Contribution to Physiology and Disease. InPhysiological Reviews (Vol. 84, Issue 2, pp. 579–621).Physiol Rev. https://doi.org/10.1152/physrev.00028.2003

  81. Pagano, J., Giona, F., Beretta, S., Verpelli, C., & Sala, C. (2021).N-methyl-d-aspartate receptor function in neuronal andsynaptic development and signaling. Current Opinionin Pharmacology, 56, 93–101. https://doi.org/10.1016/J.COPH.2020.12.006

  82. Peach, C. J., Edgington-Mitchell, L. E., Bunnett, N. W., &Schmidt, B. L. (2022). Protease-Activated Receptors inHealth and Disease. Physiological Reviews. https://doi.org/10.1152/PHYSREV.00044.2021

  83. Peng, S., Grace, M., Gondin, A., Retamal, J., Dill, L., Darby, W.,Bunnett, N., Abogadie, F., Carbone, S., Tigani, T., Davis, T.,Poole, D., NA, Veldhuis, N., & P, McIntyre, P. (2020). Thetransient receptor potential vanilloid 4 (TRPV4) ion channelmediates protease activated receptor 1 (PAR1)-inducedvascular hyperpermeability. Laboratory Investigation;a Journal of Technical Methods and Pathology, 100(8),1057–1067. https://doi.org/10.1038/S41374-020-0430-7

  84. Poole, D. P., Amadesi, S., Veldhuis, N. A., Abogadie, F. C.,Lieu, T., Darby, W., Liedtke, W., Lew, M. J., McIntyre, P.,& Bunnett, N. W. (2013). Protease-activated Receptor 2(PAR2) Protein and Transient Receptor Potential Vanilloid4 (TRPV4) Protein Coupling Is Required for SustainedInflammatory Signaling. The Journal of BiologicalChemistry, 288(8), 5790. https://doi.org/10.1074/JBC.M112.438184

  85. Price, R., Ferrari, E., Gardoni, F., Mercuri, N. B., & Ledonne,A. (2020). Protease-activated receptor 1 (PAR1) inhibitssynaptic NMDARs in mouse nigral dopaminergic neurons.Pharmacological Research, 160, 105185. https://doi.org/10.1016/J.PHRS.2020.105185

  86. Principe, D. R., Diaz, A. M., Torres, C., Mangan, R. J., DeCant,B., McKinney, R., Tsao, M.-S., Lowy, A., Munshi, H. G.,Jung, B., & Grippo, P. J. (2017). TGFβ engages MEK/ERKto differentially regulate benign and malignant pancreas cellfunction. Oncogene, 36(30), 4336. https://doi.org/10.1038/ONC.2016.500

  87. Ruf, W. (2003). PAR1 signaling: More good than harm? InNature Medicine (Vol. 9, Issue 3, pp. 258–260). Nat Med.https://doi.org/10.1038/nm0303-258

  88. Sabri, A., Guo, J., Elouardighi, H., Darrow, A. L., Andrade-Gordon, P., & Steinberg, S. F. (2003). Mechanisms ofprotease-activated receptor-4 actions in cardiomyocytes:Role of Src tyrosine kinase. Journal of Biological Chemistry,278(13), 11714–11720. https://doi.org/10.1074/jbc.M213091200

  89. Sekiguchi, F., Saito, S., Takaoka, K., Hayashi, H., Nagataki, M.,Nagasawa, K., Nishikawa, H., Matsui, H., & Kawabata,A. (2007). Mechanisms for prostaglandin E2 formationcaused by proteinase-activated receptor-1 activation in ratgastric mucosal epithelial cells. Biochemical Pharmacology,73(1), 103–114. https://doi.org/10.1016/J.BCP.2006.09.016

  90. Sevigny, L. M., Zhang, P., Bohm, A., Lazarides, K., Perides,G., Covic, L., & Kuliopulos, A. (2011). Interdictingprotease-activated receptor-2-driven inflammationwith cell-penetrating pepducins. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 108(20), 8491–8496. https://doi.org/10.1073/pnas.1017091108

  91. Shankar, H., Garcia, A., Prabhakar, J., Kim, S., & Kunapuli,S. P. (2006). P2Y12 receptor-mediated potentiation ofthrombin-induced thromboxane A2 generation in plateletsoccurs through regulation of Erk1/2 activation. Journal ofThrombosis and Haemostasis, 4(3), 638–647. https://doi.org/10.1111/j.1538-7836.2006.01789.x

  92. Shapiro, M. J., Weiss, E. J., Faruqi, T. R., & Coughlin, S. R.(2000). Protease-activated receptors 1 and 4 are shut offwith distinct kinetics after activation by thrombin. Journalof Biological Chemistry, 275(33). https://doi.org/10.1074/jbc.M004589200

  93. Shavit-Stein, E., Artan-Furman, A., Feingold, E., Shimon, M.ben, Itzekson-Hayosh, Z., Chapman, J., Vlachos, A., &Maggio, N. (2017). Protease Activated Receptor 2 (PAR2)Induces Long-Term Depression in the Hippocampus throughTransient Receptor Potential Vanilloid 4 (TRPV4). Frontiersin Molecular Neuroscience, 10. https://doi.org/10.3389/FNMOL.2017.00042

  94. Shavit-Stein, E., Itsekson-Hayosh, Z., Aronovich, A., Reisner,Y., Bushi, D., Pick, C. G., Tanne, D., Chapman, J., Vlachos,A., & Maggio, N. (2015). Thrombin induces ischemic LTP(iLTP): implications for synaptic plasticity in the acutephase of ischemic stroke. Scientific Reports, 5. https://doi.org/10.1038/SREP07912

  95. Shi, X., Gangadharan, B., Brass, L. F., Ruf, W., & Mueller, B.M. (2004). Protease-activated receptors (PAR1 and PAR2)contribute to tumor cell motility and metastasis. MolecularCancer Research, 2(7).

  96. Stone, L. S., & Molliver, D. C. (2009). In search of analgesia:emerging roles of GPCRs in pain. Molecular Interventions,9(5), 234–251. https://doi.org/10.1124/MI.9.5.7

  97. Sweeney, A. M., Fleming, K. E., McCauley, J. P., Rodriguez,M. F., Martin, E. T., Sousa, A. A., Leapman, R. D., &Scimemi, A. (2017). PAR1 activation induces rapid changesin glutamate uptake and astrocyte morphology. ScientificReports 2017 7:1, 7(1), 1–20. https://doi.org/10.1038/srep43606

  98. Tiruppathi, C., Minshall, R., Paria, B., Vogel, S., & Malik, A.(2002). Role of Ca2+ signaling in the regulation of endothelialpermeability. Vascular Pharmacology, 39(4–5), 173–185.https://doi.org/10.1016/S1537-1891(03)00007-7

  99. Trusevych, E., & MacNaughton, W. (2015). Proteases andtheir receptors as mediators of inflammation-associatedcolon cancer. Current Pharmaceutical Design, 21(21),2983–2992. https://doi.org/10.2174/1381612821666150514104800

  100. van der Merwe, J. Q., Hollenberg, M. D., & MacNaughton, W.K. (2008). EGF receptor transactivation and MAP kinasemediate proteinase-activated receptor-2-induced chloridesecretion in intestinal epithelial cells. American Journal ofPhysiology - Gastrointestinal and Liver Physiology, 294(2).https://doi.org/10.1152/ajpgi.00303.2007

  101. Van Der Merwe, J. Q., Hollenberg, M. D., & MacNaughton,W. K. (2008). EGF receptor transactivation and MAPkinase mediate proteinase-activated receptor-2-inducedchloride secretion in intestinal epithelial cells. AmericanJournal of Physiology - Gastrointestinal and LiverPhysiology, 294(2), G441–G451. https://doi.org/10.1152/ajpgi.00303.2007

  102. Vance, K. M., Rogers, R. C., & Hermann, G. E. (2015).PAR1-Activated Astrocytes in the Nucleus of the SolitaryTract Stimulate Adjacent Neurons via NMDA Receptors.The Journal of Neuroscience, 35(2), 776. https://doi.org/10.1523/JNEUROSCI.3105-14.2015

  103. Veldhuis, N. A., Poole, D. P., Grace, M., McIntyre, P., &Bunnett, N. W. (2015). The g protein–coupled receptor–transient receptor potential channel axis: Molecular insightsfor targeting disorders of sensation and inflammation.Pharmacological Reviews, 67(1), 36–73. https://doi.org/10.1124/PR.114.009555

  104. Vellani, V., Kinsey, A. M., Prandini, M., Hechtfischer, S. C.,Reeh, P., Magherini, P. C., Giacomoni, C., & McNaughton,P. A. (2010). Protease activated receptors 1 and 4 sensitizeTRPV1 in nociceptive neurones. Molecular Pain, 6, 61.https://doi.org/10.1186/1744-8069-6-61

  105. Wang, W., Qiao, Y., & Li, Z. (2018). New Insights intoModes of GPCR Activation. Trends in PharmacologicalSciences, 39(4), 367–386. https://doi.org/10.1016/J.TIPS.2018.01.001

  106. Wu, L. J., Sweet, T. B., & Clapham, D. E. (2010). InternationalUnion of Basic and Clinical Pharmacology. LXXVI. Currentprogress in the Mammalian TRP ion channel family. InPharmacological Reviews (Vol. 62, Issue 3, pp. 381–404).Pharmacol Rev. https://doi.org/10.1124/pr.110.002725

  107. Zhao, P., Lieu, T., Barlow, N., Metcalf, M., Veldhuis, N. A.,Jensen, D. D., Kocan, M., Sostegni, S., Haerteis, S.,Baraznenok, V., Henderson, I., Lindström, E., Guerrero-Alba, R., Valdez-Morales, E. E., Liedtke, W., McIntyre, P.,Vanner, S. J., Korbmacher, C., & Bunnett, N. W. (2014).Cathepsin S Causes Inflammatory Pain via Biased Agonismof PAR2 and TRPV4. The Journal of Biological Chemistry,289(39), 27215. https://doi.org/10.1074/JBC.M114.599712

  108. Zhao, P., Lieu, T., Barlow, N., Sostegni, S., Haerteis, S.,Korbmacher, C., Liedtke, W., Jimenez-Vargas, N. N.,Vanner, S. J., & Bunnett, N. W. (2015). NeutrophilElastase Activates Protease-activated Receptor-2 (PAR2)and Transient Receptor Potential Vanilloid 4 (TRPV4) toCause Inflammation and Pain. The Journal of BiologicalChemistry, 290(22), 13875. https://doi.org/10.1074/JBC.M115.642736




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