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Published in: Inflammation Research 3/2020

01-03-2020 | Original Research Paper

Tachykinin-1 receptor antagonism suppresses substance-P- and compound 48/80-induced mast cell activation from rat mast cells expressing functional mas-related GPCR B3

Authors: Muhammad N. A. Sahid, Shuang Liu, Masaki Mogi, Kazutaka Maeyama

Published in: Inflammation Research | Issue 3/2020

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Abstract

Objective

Mice and rats are important animal models for mast cell (MC) study. However, rat Mas-related-GPCR-B3 receptor (MRGPRB3) has been less studied than its mouse counterpart. Therefore, we aimed to characterize rat MRGPRB3.

Methods

Mrgprb3 mRNA expression was assessed in peritoneal cells (RPCs) and peritoneal MCs (RPMCs) of wild-type rats, RPCs of MC-deficient rats, and RBL-2H3 cells by reverse-transcriptase polymerase chain reaction (RT-PCR). RPMCs, MRGPRX2-transfected and non-transfected RBL-2H3 cells were activated by 15–30 min incubation with DNP-BSA, substance-P (SP), or compound-48/80. L732138 or CP96344 was used as a tachykinin/neurokinin-1-receptor antagonist. Histamine release from MCs was measured by HPLC fluorometry.

Results

Mrgprb3 mRNA expression was found in all cells, with the highest level in wild-type RPCs. All cells responded to DNP-BSA, but only MRGPRX2-transfected-RBL-2H3 cells and RPMCs responded to all activators. L732138 (0.1–10 μM) and CP96344 (1–100 μM) suppressed SP (10 μM)-induced RPMC activation. L732138 inhibition was dose independent, whereas CP96344 inhibition occurred in a dose-dependent manner. Additionally, only CP96344 suppressed SP (100 μM)- and compound-48/80 (10 μg/mL)-induced RPMC activation.

Conclusions

RPMCs expressing functional MRGPRB3 response upon MRGPRX2 ligands to regulated MC-mediated activities. It`s provide novel insights for future pseudo-allergic studies in rodents.
Appendix
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Literature
1.
go back to reference Tatemoto K, Nozaki Y, Tsuda R, Konno S, Tomura K, Furuno M, Ogasawara H, Edamura K, Takagi H, Iwamura H, Noguchi M, Naito T. Immunoglobulin E-independent activation of mast cell is mediated by Mrg receptors. Biochem Biophys Res Commun. 2006;349:1322–8.CrossRef Tatemoto K, Nozaki Y, Tsuda R, Konno S, Tomura K, Furuno M, Ogasawara H, Edamura K, Takagi H, Iwamura H, Noguchi M, Naito T. Immunoglobulin E-independent activation of mast cell is mediated by Mrg receptors. Biochem Biophys Res Commun. 2006;349:1322–8.CrossRef
2.
go back to reference Mousli M, Bueb JL, Bronner C, Rouot B, Landry Y. G Protein activation: a receptor-independent mode of action for cationic amphiphilic neuropeptides and venom peptides. Trends Pharmacol Sci. 1990;11(9):358–62.CrossRef Mousli M, Bueb JL, Bronner C, Rouot B, Landry Y. G Protein activation: a receptor-independent mode of action for cationic amphiphilic neuropeptides and venom peptides. Trends Pharmacol Sci. 1990;11(9):358–62.CrossRef
3.
go back to reference Chahdi A, Fraundorfer PF, Beaven MA. Compound 48/80 activates mast cell phospholipase D via heterotrimeric GTP-binding proteins. J Pharmacol Exp Ther. 2000;292(1):122–30.PubMed Chahdi A, Fraundorfer PF, Beaven MA. Compound 48/80 activates mast cell phospholipase D via heterotrimeric GTP-binding proteins. J Pharmacol Exp Ther. 2000;292(1):122–30.PubMed
4.
go back to reference Palomaki VA, Laitinen JT. The basic secretagogue compound 48/80 activates G proteins indirectly via stimulation of phospholipase d-lysophosphatidic acid receptor axis and 5-HT1A receptors in rat brain sections. Br J Pharmacol. 2006;147(6):596–606.CrossRef Palomaki VA, Laitinen JT. The basic secretagogue compound 48/80 activates G proteins indirectly via stimulation of phospholipase d-lysophosphatidic acid receptor axis and 5-HT1A receptors in rat brain sections. Br J Pharmacol. 2006;147(6):596–606.CrossRef
5.
go back to reference Thurmond RL, Gelfand EW, Dunford PJ. The role of histamine H1 and H4 receptors in allergic inflammation: the search for new antihistamines. Nat Rev Drug Disc. 2008;7(1):41–53.CrossRef Thurmond RL, Gelfand EW, Dunford PJ. The role of histamine H1 and H4 receptors in allergic inflammation: the search for new antihistamines. Nat Rev Drug Disc. 2008;7(1):41–53.CrossRef
6.
go back to reference Ohsawa Y, Hirasawa N. The role of histamine H1 and H4 receptors in atopic dermatitis: from basic research to clinical study. Allergol Int. 2014;63:533–42.CrossRef Ohsawa Y, Hirasawa N. The role of histamine H1 and H4 receptors in atopic dermatitis: from basic research to clinical study. Allergol Int. 2014;63:533–42.CrossRef
7.
go back to reference Azimi E, Reddy VB, Shade K-TC, Anthony RM, Talbot S, Pereira PJS, Lerner EA. Dual action of neurokinin-1 antagonists on Mas-related GPCRs. JCI Insight. 2016;1(16):e89362. Azimi E, Reddy VB, Shade K-TC, Anthony RM, Talbot S, Pereira PJS, Lerner EA. Dual action of neurokinin-1 antagonists on Mas-related GPCRs. JCI Insight. 2016;1(16):e89362.
8.
go back to reference Dong X, Han S-K, Zylka MJ, Simon MI, Anderson DJ. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell. 2001;106:619–32.CrossRef Dong X, Han S-K, Zylka MJ, Simon MI, Anderson DJ. A diverse family of GPCRs expressed in specific subsets of nociceptive sensory neurons. Cell. 2001;106:619–32.CrossRef
9.
go back to reference Liu Q, Tang Z, Surdenikova L, Kim S, Patel KN, Kim A, Ru F, Guan Y, Weng H-J, Geng Y, Undem BJ, Kollarik M, Chen Z-F, Anderson DJ, Dong X. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. 2009;139:1353–65.CrossRef Liu Q, Tang Z, Surdenikova L, Kim S, Patel KN, Kim A, Ru F, Guan Y, Weng H-J, Geng Y, Undem BJ, Kollarik M, Chen Z-F, Anderson DJ, Dong X. Sensory neuron-specific GPCR Mrgprs are itch receptors mediating chloroquine-induced pruritus. Cell. 2009;139:1353–65.CrossRef
10.
go back to reference Robas N, Mead E, Fidock M. MrgX2 is a high potency cortistatin receptor expressed in dorsal root ganglion. J Biol Chem. 2003;278(45):44400–4.CrossRef Robas N, Mead E, Fidock M. MrgX2 is a high potency cortistatin receptor expressed in dorsal root ganglion. J Biol Chem. 2003;278(45):44400–4.CrossRef
11.
go back to reference Kamohara M, Matsuo A, Takasaki J, Kohda M, Matsumoto M, Matsumoto S, Soga T, Hiyama H, Kobori M, Katou M. Identification of MrgX2 as a human G-protein-coupled receptor for proadrenomedullin N-terminal peptides. Biochem Biophys Res Commun. 2005;330:1146–52.CrossRef Kamohara M, Matsuo A, Takasaki J, Kohda M, Matsumoto M, Matsumoto S, Soga T, Hiyama H, Kobori M, Katou M. Identification of MrgX2 as a human G-protein-coupled receptor for proadrenomedullin N-terminal peptides. Biochem Biophys Res Commun. 2005;330:1146–52.CrossRef
12.
go back to reference Nothacker H-P, Wang Z, Zeng H, Mahata SK, O’Connor DT, Civelli O. Proadrenomedullin N-terminal peptide and cortistatin activation of MrgX2 receptor is based on a common structural motif. Eur J Pharmacol. 2005;519:191–3.CrossRef Nothacker H-P, Wang Z, Zeng H, Mahata SK, O’Connor DT, Civelli O. Proadrenomedullin N-terminal peptide and cortistatin activation of MrgX2 receptor is based on a common structural motif. Eur J Pharmacol. 2005;519:191–3.CrossRef
13.
go back to reference McNeil BD, Pundir P, Meeker S, Han L, Undem BJ, Kulka M, Dong X. Identification of a mast-cell-specific receptor crucial for pseudo-allergic drug reactions. Nature. 2015;519(7542):237–41.CrossRef McNeil BD, Pundir P, Meeker S, Han L, Undem BJ, Kulka M, Dong X. Identification of a mast-cell-specific receptor crucial for pseudo-allergic drug reactions. Nature. 2015;519(7542):237–41.CrossRef
14.
go back to reference Zhang T, Che D, Liu R, Han S, Wang N, Zhang Y, Pundir P, Cao J, Lv Y, Yang L, Wang J, Ding M, Dong X, He L. Typical antimicrobials induced mast cell degranulation and anaphylactoid reactions via MrgprX2 and its murine homologue Mrgprb2. Eur J Immunol. 2017;47(11):1949–58.CrossRef Zhang T, Che D, Liu R, Han S, Wang N, Zhang Y, Pundir P, Cao J, Lv Y, Yang L, Wang J, Ding M, Dong X, He L. Typical antimicrobials induced mast cell degranulation and anaphylactoid reactions via MrgprX2 and its murine homologue Mrgprb2. Eur J Immunol. 2017;47(11):1949–58.CrossRef
15.
go back to reference Pennefather JN, Lecci A, Candenas ML, Patak E, Pinto FM, Maggi CA. Tachykinins and tachykinin receptors: a growing family. Life Sci. 2004;74:1445–633.CrossRef Pennefather JN, Lecci A, Candenas ML, Patak E, Pinto FM, Maggi CA. Tachykinins and tachykinin receptors: a growing family. Life Sci. 2004;74:1445–633.CrossRef
16.
go back to reference Fridmanis D, Roga A, Klovins J. ACTH receptor (MC2R) specificity: what do we know about underlying molecular mechanisms? Front Endocrinol. 2017;8:13.CrossRef Fridmanis D, Roga A, Klovins J. ACTH receptor (MC2R) specificity: what do we know about underlying molecular mechanisms? Front Endocrinol. 2017;8:13.CrossRef
17.
go back to reference Tusnady GE, Simon I. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol. 1998;283:489–506.CrossRef Tusnady GE, Simon I. Principles governing amino acid composition of integral membrane proteins: application to topology prediction. J Mol Biol. 1998;283:489–506.CrossRef
18.
go back to reference Tusnady GE, Simon I. The HMMTOP transmembrane topology prediction server. Bioinformatics. 2001;17:849–50.CrossRef Tusnady GE, Simon I. The HMMTOP transmembrane topology prediction server. Bioinformatics. 2001;17:849–50.CrossRef
19.
go back to reference Omasits U, Ahrens CH, Muller S, Wollscheid B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics. 2014;30(6):884–6.CrossRef Omasits U, Ahrens CH, Muller S, Wollscheid B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics. 2014;30(6):884–6.CrossRef
20.
go back to reference Skrabanek L, Campagne F, Weinstein H. Building protein diagrams on the web with the residue-based diagram editor RbDe. Nucleic Acids Res. 2003;31:3856–8.CrossRef Skrabanek L, Campagne F, Weinstein H. Building protein diagrams on the web with the residue-based diagram editor RbDe. Nucleic Acids Res. 2003;31:3856–8.CrossRef
21.
go back to reference Kiyoi T, Liu S, Sahid MNA, Shudou M, Ogasawara M, Mogi M, Maeyama K. Morphological and functional analysis of beige (Chediak–Higashi syndrome) mouse mat cells with giant granules. Int Immunopharmacol. 2019;69:202–12.CrossRef Kiyoi T, Liu S, Sahid MNA, Shudou M, Ogasawara M, Mogi M, Maeyama K. Morphological and functional analysis of beige (Chediak–Higashi syndrome) mouse mat cells with giant granules. Int Immunopharmacol. 2019;69:202–12.CrossRef
22.
go back to reference Yamatodani A, Fukuda H, Iwaeda T, Watanabe T, Wada H. HPLC determination of plasma and brain histamine without previous purification of biological samples: cation exchange chromatography coupled with post-column derivatization fluorometry. J Chromatogr. 1985;344:115–23.CrossRef Yamatodani A, Fukuda H, Iwaeda T, Watanabe T, Wada H. HPLC determination of plasma and brain histamine without previous purification of biological samples: cation exchange chromatography coupled with post-column derivatization fluorometry. J Chromatogr. 1985;344:115–23.CrossRef
23.
go back to reference Aun MV, Bonamichi-Santos R, Arantes-Costa FM, Kalil J, Giavina-Bianchi P. Animal models of asthma: utility and limitations. J Asthma Allergy. 2017;10:293–301.CrossRef Aun MV, Bonamichi-Santos R, Arantes-Costa FM, Kalil J, Giavina-Bianchi P. Animal models of asthma: utility and limitations. J Asthma Allergy. 2017;10:293–301.CrossRef
24.
go back to reference Reber LL, Marichal T, Galli SJ. New models for analyzing mast cell function in vivo. Trends Immunol. 2012;33(12):613–25.CrossRef Reber LL, Marichal T, Galli SJ. New models for analyzing mast cell function in vivo. Trends Immunol. 2012;33(12):613–25.CrossRef
25.
go back to reference Lei Y, Gregory JA, Nilsson GP, Adner M. Insights into mast cell functions in asthma using mouse models. Pulm Pharmacol Ther. 2013;26(5):532–9.CrossRef Lei Y, Gregory JA, Nilsson GP, Adner M. Insights into mast cell functions in asthma using mouse models. Pulm Pharmacol Ther. 2013;26(5):532–9.CrossRef
26.
go back to reference Kucharewicz I, Bodzenta-Lukaszyk A, Buczko W. Experimental asthma in rats. Pharmacol Rep. 2008;60(6):783–8.PubMed Kucharewicz I, Bodzenta-Lukaszyk A, Buczko W. Experimental asthma in rats. Pharmacol Rep. 2008;60(6):783–8.PubMed
27.
go back to reference Oka T, Kalesnikoff J, Starkl P, Tsai M, Galli SJ. Evidence questioning cromolyn’s effectiveness and selectivity as a “mast cell stabilizer” in mice. Lab Invest. 2012;92(10):1472–82.CrossRef Oka T, Kalesnikoff J, Starkl P, Tsai M, Galli SJ. Evidence questioning cromolyn’s effectiveness and selectivity as a “mast cell stabilizer” in mice. Lab Invest. 2012;92(10):1472–82.CrossRef
28.
go back to reference Arizono N, Kasugai T, Yamada M, Okada M, Morimoto M, Tei H, Newlands GF, Miller HR, Kitamura Y. Infection of Nippostrongylus brasiliensis induces development of mucosal-type but not connective tissue-type mast cells in genetically mast cell-deficient Ws/Ws rats. Blood. 1993;81(10):2572–8.CrossRef Arizono N, Kasugai T, Yamada M, Okada M, Morimoto M, Tei H, Newlands GF, Miller HR, Kitamura Y. Infection of Nippostrongylus brasiliensis induces development of mucosal-type but not connective tissue-type mast cells in genetically mast cell-deficient Ws/Ws rats. Blood. 1993;81(10):2572–8.CrossRef
29.
go back to reference Barsumian EL, Isersky C, Petrino MG, Siraganian RP. IgE-induced histamine release from rat basophilic leukemia cell lines: isolation of releasing and non-releasing clones. Eur J Immunol. 1981;11:317–23.CrossRef Barsumian EL, Isersky C, Petrino MG, Siraganian RP. IgE-induced histamine release from rat basophilic leukemia cell lines: isolation of releasing and non-releasing clones. Eur J Immunol. 1981;11:317–23.CrossRef
30.
go back to reference Passante E, Frankish N. The RBL-2H3 cell line: its provenance and suitability as a model for the mast cell. Inflamm Res. 2009;58:737–45.CrossRef Passante E, Frankish N. The RBL-2H3 cell line: its provenance and suitability as a model for the mast cell. Inflamm Res. 2009;58:737–45.CrossRef
31.
go back to reference Lai J-P, Lai S, Tuluc F, Tansky MF, Kilpatrick LE, Leeman SE, Douglas SD. Differences in the length of the carboxyl terminus mediate functional properties of neurokinin-1 receptor. Proc Natl Acad Sci USA. 2008;105(34):12605–10.CrossRef Lai J-P, Lai S, Tuluc F, Tansky MF, Kilpatrick LE, Leeman SE, Douglas SD. Differences in the length of the carboxyl terminus mediate functional properties of neurokinin-1 receptor. Proc Natl Acad Sci USA. 2008;105(34):12605–10.CrossRef
32.
go back to reference Snider RM, Longo KP, Drozda SE, Lowe JA III, Leeman SE. Effect of CP-96345, a nonpeptide substance P receptor antagonist, on salivation in rats. Proc Natl Acad Sci USA. 1991;88:10042–4.CrossRef Snider RM, Longo KP, Drozda SE, Lowe JA III, Leeman SE. Effect of CP-96345, a nonpeptide substance P receptor antagonist, on salivation in rats. Proc Natl Acad Sci USA. 1991;88:10042–4.CrossRef
33.
go back to reference Griesbacher T, Donnerer J, Legat FJ, Lembeck F. CP-96345, a non-peptide antagonist of substance P: II. Actions on substance P-induced hypotension and bronchoconstriction, and on depressor reflexes in mammals. Naunyn-Schmiedeberg’s Arch Pharmacol. 1992;346:323–7. Griesbacher T, Donnerer J, Legat FJ, Lembeck F. CP-96345, a non-peptide antagonist of substance P: II. Actions on substance P-induced hypotension and bronchoconstriction, and on depressor reflexes in mammals. Naunyn-Schmiedeberg’s Arch Pharmacol. 1992;346:323–7.
34.
go back to reference Yashpal K, Radhakrishnan V, Coderres TJ, Henry JL. CP-96345, but not its stereoisomer, CP-96344, blocks the nociceptive responses to intrathecally administered substance P and to noxious thermal and chemical stimuli in the rat. Neuroscience. 1993;52(4):1039–47.CrossRef Yashpal K, Radhakrishnan V, Coderres TJ, Henry JL. CP-96345, but not its stereoisomer, CP-96344, blocks the nociceptive responses to intrathecally administered substance P and to noxious thermal and chemical stimuli in the rat. Neuroscience. 1993;52(4):1039–47.CrossRef
35.
go back to reference Jacob S, Deyo DJ, Cox RA, Jacob RK, Herndon DN, Traber DL, Hawkins HK. Substance P antagonist CP-96345 blocks lung vascular leakage and inflammation more effectively than its stereoisomer CP-96344 in a mouse model of smoke inhalation and burn injury. Toxical Mech Meth. 2010;20(4):197–203.CrossRef Jacob S, Deyo DJ, Cox RA, Jacob RK, Herndon DN, Traber DL, Hawkins HK. Substance P antagonist CP-96345 blocks lung vascular leakage and inflammation more effectively than its stereoisomer CP-96344 in a mouse model of smoke inhalation and burn injury. Toxical Mech Meth. 2010;20(4):197–203.CrossRef
36.
go back to reference Leffler A, Ahlstedt I, Engberg S, Svensson A, Billger M, Oberg L, Bjursell MK, Lindstrom E, von Mentzer B. Characterization of species-related differences in the pharmacology of tachykinin NK receptors 1, 2 and 3. Biochem Pharmacol. 2009;77(9):1522–30.CrossRef Leffler A, Ahlstedt I, Engberg S, Svensson A, Billger M, Oberg L, Bjursell MK, Lindstrom E, von Mentzer B. Characterization of species-related differences in the pharmacology of tachykinin NK receptors 1, 2 and 3. Biochem Pharmacol. 2009;77(9):1522–30.CrossRef
37.
go back to reference Calcieri MA, Macleod AM, Underwood D, Shiao LL, Ber E, Sadowski S, Yu H, Merchant KJ, Swain CJ, Strader CD, Fong TM. Characterization of the interaction of N-acyl-l-tryptophan benzyl ester neurokinin antagonists with the human neurokinin-1 receptor. J Biol Chem. 1994;269(9):6587–91. Calcieri MA, Macleod AM, Underwood D, Shiao LL, Ber E, Sadowski S, Yu H, Merchant KJ, Swain CJ, Strader CD, Fong TM. Characterization of the interaction of N-acyl-l-tryptophan benzyl ester neurokinin antagonists with the human neurokinin-1 receptor. J Biol Chem. 1994;269(9):6587–91.
Metadata
Title
Tachykinin-1 receptor antagonism suppresses substance-P- and compound 48/80-induced mast cell activation from rat mast cells expressing functional mas-related GPCR B3
Authors
Muhammad N. A. Sahid
Shuang Liu
Masaki Mogi
Kazutaka Maeyama
Publication date
01-03-2020
Publisher
Springer International Publishing
Published in
Inflammation Research / Issue 3/2020
Print ISSN: 1023-3830
Electronic ISSN: 1420-908X
DOI
https://doi.org/10.1007/s00011-020-01319-z

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