Current Protein & Peptide Science

Author(s): Muhammad N.A. Sahid*

DOI: 10.2174/1389203723666220620164024

Non-Nitrogen-Containing Bisphosphonates Prevent Pyrophosphorylation of Exocytosis Proteins

Page: [505 - 509] Pages: 5

  • * (Excluding Mailing and Handling)

Abstract

Background: Clodronate, a non-nitrogen-containing bisphosphonate (non-NBP), is intracellularly converted into non-hydrolyzable ATP analogs. Clodronate and its analogs impair normal cell functions, including the exocytosis process. However, how this occurs in mast cells is still not well characterized.

Objective: To summarize the possible mechanisms of clodronate-mediated exocytosis inhibition in mast cells.

Results: Non-NBPs display several possible mechanisms of exocytosis inhibition in various cell types, including vesicular nucleotide transporter (VNUT) and purinergic receptor inhibition. Inhibition of purinergic receptors has been shown in mast cells, but VNUT inhibition remains to be confirmed. Inhibition of protein prenylation by non-NBPs has also been shown; however, direct evidence of non-NBPs in prenylated exocytosis proteins is still contradictory. Finally, non-NBPs may inhibit mast cell exocytosis via impairment of protein pyrophosphorylation. This mechanism is less studied, and direct evidence of the involvement of pyrophosphorylated proteins in exocytosis is still lacking.

Conclusion: Non-NBPs may affect mast cell exocytosis by interacting with purinergic receptors or VNUT or by preventing post-translational modifications of exocytosis protein(s), i.e., prenylation and pyrophosphorylation. The latter needs further investigation to provide direct evidence of a role for non- NBPs.

Keywords: Non-nitrogen-containing, bisphosphonates, pyrophosphorylation, post-translational modifications, exocytosis, pyrophosphate, clodronate.

Graphical Abstract

[1]
Rogers, M.J.; Crockett, J.C.; Coxon, F.P.; Mönkkönen, J. Biochemical and molecular mechanisms of action of bisphosphonates. Bone, 2011, 49(1), 34-41.
[http://dx.doi.org/10.1016/j.bone.2010.11.008] [PMID: 21111853]
[2]
Russell, R.G.G. Bisphosphonates: The first 40 years. Bone, 2011, 49(1), 2-19.
[http://dx.doi.org/10.1016/j.bone.2011.04.022] [PMID: 21555003]
[3]
Sahid, M.N.A.; Liu, S.; Kiyoi, T.; Maeyama, K.; Mogi, M. Inhibition of histamine release from RBL-2H3 cells by zoledronate did not affect rab27a/doc2a interaction. Biol. Pharm. Bull., 2021, 44(12), 1902-1906.
[http://dx.doi.org/10.1248/bpb.b21-00717] [PMID: 34853276]
[4]
Sahid, M.N.A.; Liu, S.; Kiyoi, T.; Maeyama, K. Inhibition of the mevalonate pathway by simvastatin interferes with mast cell degranula-tion by disrupting the interaction between Rab27a and double C2 alpha proteins. Eur. J. Pharmacol., 2017, 814, 255-263.
[http://dx.doi.org/10.1016/j.ejphar.2017.08.026] [PMID: 28864210]
[5]
Liu, S.; Sahid, M.N.A.; Takemasa, E.; Maeyama, K.; Mogi, M. Zoledronate modulates intracellular vesicle trafficking in mast cells via disturbing the interaction of myosinVa/Rab3a and sytaxin4/VAMP7. Biochem. Pharmacol., 2018, 151, 18-25.
[http://dx.doi.org/10.1016/j.bcp.2018.02.013] [PMID: 29454616]
[6]
Beutier, H.; Gillis, C.M.; Iannascoli, B.; Godon, O.; England, P.; Sibilano, R.; Reber, L.L.; Galli, S.J.; Cragg, M.S.; Van Rooijen, N.; Man-cardi, D.A.; Bruhns, P.; Jönsson, F. IgG subclasses determine pathways of anaphylaxis in mice. J. Allergy Clin. Immunol., 2017, 139(1), 269-280.e7.
[http://dx.doi.org/10.1016/j.jaci.2016.03.028] [PMID: 27246523]
[7]
Iwasaki, N.; Matsushita, K.; Fukuoka, A.; Nakahira, M.; Matsumoto, M.; Akasaki, S.; Yasuda, K.; Shimizu, T.; Yoshimoto, T. Allergen endotoxins induce T-cell-dependent and non-IgE-mediated nasal hypersensitivity in mice. J. Allergy Clin. Immunol., 2017, 139(1), 258-268.e10.
[http://dx.doi.org/10.1016/j.jaci.2016.03.023] [PMID: 27287257]
[8]
Van Rooijen, N.; Sanders, A. Liposome mediated depletion of macrophages: Mechanism of action, preparation of liposomes and applica-tions. J. Immunol. Methods, 1994, 174(1-2), 83-93.
[http://dx.doi.org/10.1016/0022-1759(94)90012-4] [PMID: 8083541]
[9]
Kato, Y.; Hiasa, M.; Ichikawa, R.; Hasuzawa, N.; Kadowaki, A.; Iwatsuki, K.; Shima, K.; Endo, Y.; Kitahara, Y.; Inoue, T.; Nomura, M.; Omote, H.; Moriyama, Y.; Miyaji, T. Identification of a vesicular ATP release inhibitor for the treatment of neuropathic and inflammatory pain. Proc. Natl. Acad. Sci. USA, 2017, 114(31), E6297-E6305.
[http://dx.doi.org/10.1073/pnas.1704847114] [PMID: 28720702]
[10]
Estévez-Herrera, J.; Domínguez, N.; Pardo, M.R.; González-Santana, A.; Westhead, E.W.; Borges, R.; Machado, J.D. ATP: The crucial component of secretory vesicles. Proc. Natl. Acad. Sci. USA, 2016, 113(28), E4098-E4106.
[http://dx.doi.org/10.1073/pnas.1600690113] [PMID: 27342860]
[11]
Hasuzawa, N.; Moriyama, S.; Moriyama, Y.; Nomura, M. Physiopathological roles of vesicular nucleotide transporter (VNUT), an essen-tial component for vesicular ATP release. Biochim. Biophys. Acta Biomembr., 2020, 1862(12), 183408.
[http://dx.doi.org/10.1016/j.bbamem.2020.183408] [PMID: 32652056]
[12]
Mihara, H.; Uchida, K.; Koizumi, S.; Moriyama, Y. Involvement of VNUT-exocytosis in transient receptor potential vanilloid 4-dependent ATP release from gastrointestinal epithelium. PLoS One, 2018, 13(10), e0206276.
[http://dx.doi.org/10.1371/journal.pone.0206276] [PMID: 30365528]
[13]
Schulman, E.S.; Glaum, M.C.; Post, T.; Wang, Y.; Raible, D.G.; Mohanty, J.; Butterfield, J.H.; Pelleg, A. ATP modulates anti-IgE-induced release of histamine from human lung mast cells. Am. J. Respir. Cell Mol. Biol., 1999, 20(3), 530-537.
[http://dx.doi.org/10.1165/ajrcmb.20.3.3387] [PMID: 10030852]
[14]
Pettersson, H.; Zarnegar, B.; Westin, A.; Persson, V.; Peuckert, C.; Jonsson, J.; Hallgren, J.; Kullander, K. SLC10A4 regulates IgE-mediated mast cell degranulation in vitro and mast cell-mediated reactions in vivo. Sci. Rep., 2017, 7(1), 1085.
[http://dx.doi.org/10.1038/s41598-017-01121-8] [PMID: 28439090]
[15]
Yoshida, K.; Ito, M.; Matsuoka, I. Divergent regulatory roles of extracellular ATP in the degranulation response of mouse bone marrow-derived mast cells. Int. Immunopharmacol., 2017, 43, 99-107.
[http://dx.doi.org/10.1016/j.intimp.2016.12.014] [PMID: 27988461]
[16]
Yoshida, K.; Ito, M-A.; Sato, N.; Obayashi, K.; Yamamoto, K.; Koizumi, S.; Tanaka, S.; Furuta, K.; Matsuoka, I. Extracellular ATP aug-ments antigen-induced murine mast cell degranulation and allergic responses via P2X4 receptor activation. J. Immunol., 2020, 204(12), 3077-3085.
[http://dx.doi.org/10.4049/jimmunol.1900954] [PMID: 32358018]
[17]
Malwal, S.R.; O’Dowd, B.; Feng, X.; Turhanen, P.; Shin, C.; Yao, J.; Kim, B.K.; Baig, N.; Zhou, T.; Bansal, S.; Khade, R.L.; Zhang, Y.; Oldfield, E. Bisphosphonate-generated ATP-analogs inhibit cell signaling pathways. J. Am. Chem. Soc., 2018, 140(24), 7568-7578.
[http://dx.doi.org/10.1021/jacs.8b02363] [PMID: 29787268]
[18]
Thastrup, O.; Cullen, P.J.; Drøbak, B.K.; Hanley, M.R.; Dawson, A.P. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc. Natl. Acad. Sci. USA, 1990, 87(7), 2466-2470.
[http://dx.doi.org/10.1073/pnas.87.7.2466] [PMID: 2138778]
[19]
Morgan, A.J.; Jacob, R. Ionomycin enhances Ca2+ influx by stimulating store-regulated cation entry and not by a direct action at the plas-ma membrane. Biochem. J., 1994, 300(Pt 3), 665-672.
[http://dx.doi.org/10.1042/bj3000665] [PMID: 8010948]
[20]
Xu, H.; Bin, N-R.; Sugita, S. Diverse exocytic pathways for mast cell mediators. Biochem. Soc. Trans., 2018, 46(2), 235-247.
[http://dx.doi.org/10.1042/BST20170450] [PMID: 29472369]
[21]
Hanson, D.A.; Ziegler, S.F. Regulation of ionomycin-mediated granule release from rat basophil leukemia cells. Mol. Immunol., 2002, 38(16-18), 1329-1335.
[http://dx.doi.org/10.1016/S0161-5890(02)00083-4] [PMID: 12217403]
[22]
Filtz, T.M.; Vogel, W.K.; Leid, M. Regulation of transcription factor activity by interconnected post-translational modifications. Trends Pharmacol. Sci., 2014, 35(2), 76-85.
[http://dx.doi.org/10.1016/j.tips.2013.11.005] [PMID: 24388790]
[23]
van beek, E.; Löwik, C.; van der Pluijm, G.; Papapoulos, S. The role of geranylgeranylation in bone resorption and its suppression by bisphosphonates in fetal bone explants in vitro: A clue to the mechanism of action of nitrogen-containing bisphosphonates. J. Bone Miner. Res., 1999, 14(5), 722-729.
[http://dx.doi.org/10.1359/jbmr.1999.14.5.722] [PMID: 10320520]
[24]
Pabst, A.M.; Krüger, M.; Ziebart, T.; Jacobs, C.; Sagheb, K.; Walter, C. The influence of geranylgeraniol on human oral keratinocytes after bisphosphonate treatment: An in vitro study. J. Craniomaxillofac. Surg., 2015, 43(5), 688-695.
[http://dx.doi.org/10.1016/j.jcms.2015.03.014] [PMID: 25913629]
[25]
Pabst, A.M.; Krüger, M.; Sagheb, K.; Ziebart, T.; Jacobs, C.; Blatt, S.; Goetze, E.; Walter, C. The influence of geranylgeraniol on mi-crovessel sprouting after bisphosphonate substitution in an in vitro 3D-angiogenesis assay. Clin. Oral Investig., 2017, 21(3), 771-778.
[http://dx.doi.org/10.1007/s00784-016-1842-z] [PMID: 27170294]
[26]
Park, S.J.; Lee, S.; Park, S.E.; Kim, S. Inositol pyrophosphates as multifaceted metabolites in the regulation of mammalian signaling net-works. Anim. Cells Syst., 2018, 22(1), 1-6.
[http://dx.doi.org/10.1080/19768354.2017.1408684]
[27]
Ganguli, S.; Shah, A.; Hamid, A.; Singh, A.; Palakurti, R.; Bhandari, R. A high energy phosphate jump - From pyrophospho-inositol to pyrophospho-serine. Adv. Biol. Regul., 2020, 75, 100662.
[http://dx.doi.org/10.1016/j.jbior.2019.100662] [PMID: 31668836]
[28]
Azevedo, C.; Burton, A.; Ruiz-Mateos, E.; Marsh, M.; Saiardi, A. Inositol pyrophosphate mediated pyrophosphorylation of AP3B1 regu-lates HIV-1 Gag release. Proc. Natl. Acad. Sci. USA, 2009, 106(50), 21161-21166.
[http://dx.doi.org/10.1073/pnas.0909176106] [PMID: 19934039]
[29]
Munoz, I.; Danelli, L.; Claver, J.; Goudin, N.; Kurowska, M.; Madera-Salcedo, I.K.; Huang, J.D.; Fischer, A.; González-Espinosa, C.; de Saint Basile, G.; Blank, U.; Ménasché, G. Kinesin-1 controls mast cell degranulation and anaphylaxis through PI3K-dependent recruitment to the granular Slp3/Rab27b complex. J. Cell Biol., 2016, 215(2), 203-216.
[http://dx.doi.org/10.1083/jcb.201605073] [PMID: 27810912]
[30]
Mizuno, N.; Toba, S.; Edamatsu, M.; Watai-Nishii, J.; Hirokawa, N.; Toyoshima, Y.Y.; Kikkawa, M. Dynein and kinesin share an over-lapping microtubule-binding site. EMBO J., 2004, 23(13), 2459-2467.
[http://dx.doi.org/10.1038/sj.emboj.7600240] [PMID: 15175652]
[31]
Chanduri, M.; Rai, A.; Malla, A.B.; Wu, M.; Fiedler, D.; Mallik, R.; Bhandari, R. Inositol hexakisphosphate kinase 1 (IP6K1) activity is required for cytoplasmic dynein-driven transport. Biochem. J., 2016, 473(19), 3031-3047.
[http://dx.doi.org/10.1042/BCJ20160610] [PMID: 27474409]
[32]
Efergan, A.; Azouz, N.P.; Klein, O.; Noguchi, K.; Rothenberg, M.E.; Fukuda, M.; Sagi-Eisenberg, R. Rab12 regulates retrograde transport of mast cell secretory granules by interacting with the RILP-Dynein complex. J. Immunol., 2016, 196(3), 1091-1101.
[http://dx.doi.org/10.4049/jimmunol.1500731] [PMID: 26740112]
[33]
Saiardi, A. Protein pyrophosphorylation: Moving forward. Biochem. J., 2016, 473(21), 3765-3768.
[http://dx.doi.org/10.1042/BCJ20160710C] [PMID: 27789744]
[34]
Shah, A.; Ganguli, S.; Sen, J.; Bhandari, R. Inositol pyrophosphates: Energetic, omnipresent and versatile signalling molecules. J. Indian Inst. Sci., 2017, 97(1), 23-40.
[http://dx.doi.org/10.1007/s41745-016-0011-3] [PMID: 32214696]