Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Systematic Review Article

A Systematic Review of the Anti-inflammatory Effects of Gallium Compounds

Author(s): Victor de Albuquerque Wanderley Sales*, Taysa Renata Ribeiro Timóteo, Natália Millena da Silva, Camila Gomes de Melo, Aline Silva Ferreira, Marcos Victor Gregório de Oliveira, Emerson de Oliveira Silva, Larissa Morgana dos Santos Mendes, Larissa Araújo Rolim and Pedro José Rolim Neto

Volume 28 , Issue 10 , 2021

Published on: 25 May, 2020

Page: [2062 - 2076] Pages: 15

DOI: 10.2174/0929867327666200525160556

Price: $65

Abstract

Background: Inflammation is an essential response provided by the immune system, ensuring the survival during microbial infection, tissue injury and other noxious conditions. However, prolonged inflammatory processes are often associated with severe side effects on health.

Objective: This systematic review aimed to provide the evidence in the literature of the preclinical and human anti-inflammatory activity of gallium compounds from 2000 to 2019 focused on elucidating the mechanisms involved in the inflammatory process.

Methods: Seven bibliographical databases were consulted (PubMed, Medline, ScienceDirect, Scopus, Springer, Web of Science, and EBSCOhost). The selection of appropriate publications and writing of this systematic review were based on the guidelines mentioned in the PRISMA statement. Moreover, the assessment of the methodological quality of the selected studies was also performed.

Results: From a total of 3018 studies, 16 studies were included in this paper based on our eligibility criteria, which showed promising and consistent results.

Conclusion: Further research concerning specific inflammatory conditions is required.

Keywords: Gallium composts, inflammation, pro-inflammatory mediators, regeneration, medicinal chemistry, inorganic compounds.

[1]
Bernstein, L.R. Mechanisms of therapeutic activity for gallium. Pharmacol. Rev., 1998, 50(4), 665-682.
[PMID: 9860806]
[2]
Chitambar, C.R. The therapeutic potential of iron-targeting gallium compounds in human disease: from basic research to clinical application. Pharmacol. Res., 2017, 115, 56-64.
[http://dx.doi.org/10.1016/j.phrs.2016.11.009] [PMID: 27856328]
[3]
Chitambar, C.R. Gallium-containing anticancer compounds. Future Med. Chem., 2012, 4(10), 1257-1272.
[http://dx.doi.org/10.4155/fmc.12.69] [PMID: 22800370]
[4]
Bernstein, L.R.; Tanner, T.; Godfrey, C.; Noll, B. Chemistry and pharmacokinetics of gallium maltolate, a compound with high oral gallium bioavailability. Met. Based Drugs, 2000, 7(1), 33-47.
[http://dx.doi.org/10.1155/MBD.2000.33] [PMID: 18475921]
[5]
Whitacre, C.; Apseloff, G.; Cox, K.; Matkovic, V.; Jewell, S.; Gerber, N. Suppression of experimental autoimmune encephalomyelitis by gallium nitrate. J. Neuroimmunol., 1992, 39(1-2), 175-181.
[http://dx.doi.org/10.1016/0165-5728(92)90186-O] [PMID: 1377710]
[6]
Huang, E.H.; Gabler, D.M.; Krecic, M.E.; Gerber, N.; Ferguson, R.M.; Orosz, C.G. Differential effects of gallium nitrate on T lymphocyte and endothelial cell activation. Transplantation, 1994, 58(11), 1216-1222.
[PMID: 7992366]
[7]
Kovar, J.; Seligman, P.; Gelfand, E.W. Differential growth-inhibitory effects of gallium on B-lymphocyte lines in high versus low iron concentrations. Cancer Res., 1990, 50(18), 5727-5730.
[PMID: 2393846]
[8]
Drobyski, W.R.; Ul-Haq, R.; Majewski, D.; Chitambar, C.R. Modulation of in vitro and in vivo T-cell responses by transferrin-gallium and gallium nitrate. Blood, 1996, 88(8), 3056-3064.
[http://dx.doi.org/10.1182/blood.V88.8.3056.bloodjournal8883056] [PMID: 8874204]
[9]
Matkovic, V.; Balboa, A.; Clinchot, D.; Whitacre, C.; Zwilling, B.; Brown, D. Gallium prevents adjuvant arthritis in rats and interferes with macrophage/T-cell function in the immune response. Curr. Ther. Res. Clin. Exp., 1991, 50(2), 255-267.
[10]
Apseloff, G.; Hackshaw, K.V.; Whitacre, C.; Weisbrode, S.E.; Gerber, N. Gallium nitrate suppresses lupus in MRL/lpr mice. Naunyn Schmiedebergs Arch. Pharmacol., 1997, 356(4), 517-525.
[http://dx.doi.org/10.1007/PL00005085] [PMID: 9349640]
[11]
Orosz, C.G.; Wakely, E.; Bergese, S.D.; VanBuskirk, A.M.; Ferguson, R.M.; Mullet, D.; Apseloff, G.; Gerber, N. Prevention of murine cardiac allograft rejection with gallium nitrate. Comparison with anti-CD4 monoclonal antibody. Transplantation, 1996, 61(5), 783-791.
[http://dx.doi.org/10.1097/00007890-199603150-00019] [PMID: 8607184]
[12]
Lobanoff, M.C.; Kozhich, A.T.; Mullet, D.I.; Gerber, N.; Gery, I.; Chan, C.C.; Whitcup, S.M. Effect of gallium nitrate on experimental autoimmune uveitis. Exp. Eye Res., 1997, 65(6), 797-801.
[http://dx.doi.org/10.1006/exer.1997.0395] [PMID: 9441703]
[13]
Matkovic, V.; Apseloff, G.; Shepard, D.R.; Gerber, N. Use of gallium to treat Paget’s disease of bone: a pilot study. Lancet, 1990, 335(8681), 72-75.
[http://dx.doi.org/10.1016/0140-6736(90)90540-L] [PMID: 1967419]
[14]
Makkonen, N.; Hirvonen, M.-R.; Savolainen, K.; Lapinjoki, S.; Mönkkönen, J. The effect of free gallium and gallium in liposomes on cytokine and nitric oxide secretion from macrophage-like cells in vitro. Inflamm. Res., 1995, 44(12), 523-528.
[http://dx.doi.org/10.1007/BF01757356] [PMID: 8788232]
[15]
Mullet, D.; Bian, X.; Cox, G.W.; Zaveri, N.; Gerber, N.; Fertel, R.H. Gallium nitrate inhibits nitric acid production by activated ANA-1 macrophages. FASEB J., 1995, 9, A944.
[16]
Chitambar, C.R. Medical applications and toxicities of gallium compounds. Int. J. Environ. Res. Public Health, 2010, 7(5), 2337-2361.
[http://dx.doi.org/10.3390/ijerph7052337] [PMID: 20623028]
[17]
Wessling-Resnick, M. Iron homeostasis and the inflammatory response. Annu. Rev. Nutr., 2010, 30, 105-122.
[http://dx.doi.org/10.1146/annurev.nutr.012809.104804] [PMID: 20420524]
[18]
Moher, D.; Liberati, A.; Tetzlaff, J.; Altman, D.G. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann. Intern. Med., 2009, 151(4), 264-269.
[http://dx.doi.org/10.7326/0003-4819-151-4-200908180-00135] [PMID: 19622511]
[19]
Schneider, K.; Schwarz, M.; Burkholder, I.; Kopp-Schneider, A.; Edler, L.; Kinsner-Ovaskainen, A.; Hartung, T.; Hoffmann, S. “ToxRTool”, a new tool to assess the reliability of toxicological data. Toxicol. Lett., 2009, 189(2), 138-144.
[http://dx.doi.org/10.1016/j.toxlet.2009.05.013] [PMID: 19477248]
[20]
Murad, M.H.; Sultan, S.; Haffar, S.; Bazerbachi, F. Methodological quality and synthesis of case series and case reports. BMJ Evid. Based Med., 2018, 23(2), 60-63.
[http://dx.doi.org/10.1136/bmjebm-2017-110853] [PMID: 29420178]
[21]
Akira, S.; Uematsu, S.; Takeuchi, O. Pathogen recognition and innate immunity. Cell, 2006, 124(4), 783-801.
[http://dx.doi.org/10.1016/j.cell.2006.02.015] [PMID: 16497588]
[22]
Fujiwara, N.; Kobayashi, K. Macrophages in inflammation. Curr. Drug Targets Inflamm. Allergy, 2005, 4(3), 281-286.
[http://dx.doi.org/10.2174/1568010054022024] [PMID: 16101534]
[23]
Bibi, H.; Vinokur, V.; Waisman, D.; Elenberg, Y.; Landesberg, A.; Faingersh, A.; Yadid, M.; Brod, V.; Pesin, J.; Berenshtein, E.; Eliashar, R.; Chevion, M. Zn/Ga-DFO iron-chelating complex attenuates the inflammatory process in a mouse model of asthma. Redox Biol., 2014, 2(1), 814-819.
[http://dx.doi.org/10.1016/j.redox.2014.06.009] [PMID: 25009783]
[24]
Sahiner, U.M.; Birben, E.; Erzurum, S.; Sackesen, C.; Kalayci, O. Oxidative stress in asthma. World Allergy Organ. J., 2011, 4(10), 151-158.
[http://dx.doi.org/10.1097/WOX.0b013e318232389e] [PMID: 23268432]
[25]
Dong, J.; Fang, D.; Zhang, L.; Shan, Q.; Huang, Y. Gallium-doped titania nanotubes elicit anti-bacterial efficacy in vivo against Escherichia coli and Staphylococcus aureus biofilm. Materialia., 2019, 5, 100209.
[http://dx.doi.org/10.1016/j.mtla.2019.100209]
[26]
Epstein, H.; Berger, V.; Levi, I.; Eisenberg, G.; Koroukhov, N.; Gao, J.; Golomb, G. Nanosuspensions of alendronate with gallium or gadolinium attenuate neointimal hyperplasia in rats. J. Control. Release, 2007, 117(3), 322-332.
[http://dx.doi.org/10.1016/j.jconrel.2006.10.030] [PMID: 17234295]
[27]
House, S.D.; Guidon, P.T. Jr.; Perdrizet, G.A.; Rewinski, M.; Kyriakos, R.; Bockman, R.S.; Mistry, T.; Gallagher, R.A.; Hightower, L.E. Effects of heat shock, stannous chloride, and gallium nitrate on the rat inflammatory response. Cell Stress Chaperones, 2001, 6(2), 164-171.
[http://dx.doi.org/10.1379/1466-1268(2001)006<0164: EOHSSC>2.0.CO;2] [PMID: 11599578]
[28]
Thompson, M.G.; Truong-Le, V.; Alamneh, Y.A.; Black, C.C.; Anderl, J.; Honnold, C.L.; Pavlicek, R.L.; Abu-Taleb, R.; Wise, M.C.; Hall, E.R.; Wagar, E.J.; Patzer, E.; Zurawski, D.V. Evaluation of gallium citrate formulations against a multidrug-resistant strain of Klebsiella pneumoniae in a murine wound model of infection. Antimicrob. Agents Chemother., 2015, 59(10), 6484-6493.
[http://dx.doi.org/10.1128/AAC.00882-15] [PMID: 26239978]
[29]
Verri, W.A. Jr.; Cunha, T.M.; Poole, S.; Ferreira, S.H.; Cunha, F.Q. Cytokine inhibitors and pain control. Rev. Bras. Reumatol., 2007, 47(5), 341-353.
[http://dx.doi.org/10.1590/S0482-50042007000500009]
[30]
Moss, J.W.; Ramji, D.P. Cytokines: roles in atherosclerosis disease progression and potential therapeutic targets. Future Med. Chem., 2016, 8(11), 1317-1330.
[http://dx.doi.org/10.4155/fmc-2016-0072] [PMID: 27357616]
[31]
Choi, J.H.; Lee, J.H.; Roh, K.H.; Seo, S.K.; Choi, I.W.; Park, S.G.; Lim, J.G.; Lee, W.J.; Kim, M.H.; Cho, K.R.; Kim, Y.J. Gallium nitrate ameliorates type II collagen-induced arthritis in mice. Int. Immunopharmacol., 2014, 20(1), 269-275.
[http://dx.doi.org/10.1016/j.intimp.2014.03.005] [PMID: 24656780]
[32]
Wang, J.; He, M.; Wang, G.; Fu, Q. Organic gallium treatment improves osteoporotic fracture healing through affecting the OPG/RANKL ratio and expression of serum inflammatory cytokines in ovariectomized rats. Biol. Trace Elem. Res., 2018, 183(2), 270-279.
[http://dx.doi.org/10.1007/s12011-017-1123-y] [PMID: 28836172]
[33]
Joosten, L.A.B.; Crişan, T.O.; Azam, T.; Cleophas, M.C.; Koenders, M.I.; van de Veerdonk, F.L.; Netea, M.G.; Kim, S.; Dinarello, C.A. Alpha-1-anti-trypsin-Fc fusion protein ameliorates gouty arthritis by reducing release and extracellular processing of IL-1β and by the induction of endogenous IL-1Ra. Ann. Rheum. Dis., 2016, 75(6), 1219-1227.
[http://dx.doi.org/10.1136/annrheumdis-2014-206966] [PMID: 26174021]
[34]
Panagakos, F.S.; Kumar, E.; Venescar, C.; Guidon, P. The effect of gallium nitrate on synoviocyte MMP activity. Biochimie, 2000, 82(2), 147-151.
[http://dx.doi.org/10.1016/S0300-9084(00)00384-9] [PMID: 10727770]
[35]
Choi, S.R.; Britigan, B.E.; Narayanasamy, P. Treatment of virulent Mycobacterium tuberculosis and HIV coinfected macrophages with gallium nanoparticles inhibits pathogen growth and modulates macrophage cytokine production. MSphere, 2019, 4(4), 1-11.
[http://dx.doi.org/10.1128/mSphere.00443-19] [PMID: 31341073]
[36]
Bickerstaff, A.A.; Wang, J.J.; Pelletier, R.P.; Orosz, C.G. The graft helps to define the character of the alloimmune response. Transpl. Immunol., 2002, 9(2-4), 137-141.
[http://dx.doi.org/10.1016/S0966-3274(02)00036-9] [PMID: 12180821]
[37]
Wu, X.; Wang, T.W.; Lessmann, G.M.; Saleh, J.; Liu, X.; Chitambar, C.R.; Hwang, S.T. Gallium maltolate inhibits human cutaneous T-cell lymphoma tumor development in mice. J. Invest. Dermatol., 2015, 135(3), 877-884.
[http://dx.doi.org/10.1038/jid.2014.476] [PMID: 25371972]
[38]
English, W.R.; Puente, X.S.; Freije, J.M.; Knauper, V.; Amour, A.; Merryweather, A.; Lopez-Otin, C.; Murphy, G. Membrane type 4 matrix metalloproteinase (MMP17) has tumor necrosis factor-alpha convertase activity but does not activate pro-MMP2. J. Biol. Chem., 2000, 275(19), 14046-14055.
[http://dx.doi.org/10.1074/jbc.275.19.14046] [PMID: 10799478]
[39]
Mohan, M.J.; Seaton, T.; Mitchell, J.; Howe, A.; Blackburn, K.; Burkhart, W.; Moyer, M.; Patel, I.; Waitt, G.M.; Becherer, J.D.; Moss, M.L.; Milla, M.E. The tumor necrosis factor-alpha converting enzyme (TACE): a unique metalloproteinase with highly defined substrate selectivity. Biochemistry, 2002, 41(30), 9462-9469.
[http://dx.doi.org/10.1021/bi0260132] [PMID: 12135369]
[40]
Navarro, V.P.; Nelson Filho, P.; Silva, L.A.B.; Freitas, A.C. The participation of matrix metalloproteinases in the physiopathological processes of the oral cavity. Rev. Odontol., 2006, 35(4), 233-238.
[41]
Manicone, A.M.; McGuire, J.K. Matrix metalloproteinases as modulators of inflammation. Semin. Cell Dev. Biol., 2008, 19(1), 34-41.
[http://dx.doi.org/10.1016/j.semcdb.2007.07.003] [PMID: 17707664]
[42]
Johansson, N.; Ahonen, M.; Kähäri, V.M. Matrix metalloproteinases in tumor invasion. Cell. Mol. Life Sci., 2000, 57(1), 5-15.
[http://dx.doi.org/10.1007/s000180050495] [PMID: 10949577]
[43]
Sahdev, R.; Ansari, T.I.; Higham, S.M.; Valappil, S.P. Potential use of gallium-doped phosphate-based glass material for periodontitis treatment. J. Biomater. Appl., 2015, 30(1), 85-92.
[http://dx.doi.org/10.1177/0885328215571952] [PMID: 25681404]
[44]
Xue, M.; McKelvey, K.; Shen, K.; Minhas, N.; March, L.; Park, S.Y.; Jackson, C.J. Endogenous MMP-9 and not MMP-2 promotes rheumatoid synovial fibroblast survival, inflammation and cartilage degradation. Rheumatology (Oxford), 2014, 53(12), 2270-2279.
[http://dx.doi.org/10.1093/rheumatology/keu254] [PMID: 24982240]
[45]
Silva, D.C.; Cerchiaro, G.; Honório, K.M. Pathophysiologic relationships between oxidative stress and atherosclerosis. Quim. Nova, 2011, 34(2), 300-305.
[http://dx.doi.org/10.1590/S0100-40422011000200024]
[46]
Vellosa, J.C.R.; Parabocz, G.C.; Manente, F.A.; Ribas, J.T.; Lima, L.W. Alterações metabólicas e inflamatórias em condições de estresse oxidativo. Rev. Cienc. Farm. Basica Apl., 2013, 34(3), 305-312.
[47]
Banin, E.; Morad, Y.; Berenshtein, E.; Obolensky, A.; Yahalom, C.; Goldich, J.; Adibelli, F.M.; Zuniga, G.; DeAnda, M.; Pe’er, J.; Chevion, M. Injury induced by chemical warfare agents: characterization and treatment of ocular tissues exposed to nitrogen mustard. Invest. Ophthalmol. Vis. Sci., 2003, 44(7), 2966-2972.
[http://dx.doi.org/10.1167/iovs.02-1164] [PMID: 12824239]
[48]
Ricciotti, E.; FitzGerald, G.A. Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol., 2011, 31(5), 986-1000.
[http://dx.doi.org/10.1161/ATVBAHA.110.207449] [PMID: 21508345]
[49]
Campos, A.C.L.; Borges-Branco, A.; Groth, A.K. Cicatrização de feridas. Arq. Bras. Cir. Dig., 2007, 20(1), 51-58.
[http://dx.doi.org/10.1590/S0102-67202007000100010]
[50]
Pinho-Ribeiro, F.A.; Verri, W.A. Jr.; Chiu, I.M. Nociceptor sensory neuron-immune interactions in pain and inflammation. Trends Immunol., 2017, 38(1), 5-19.
[http://dx.doi.org/10.1016/j.it.2016.10.001] [PMID: 27793571]
[51]
Lorenz, M.D.; Coates, J.R.; Kent, M. Pain. Handbook of Veterinary Neurology; Elsevier, 2011, Vol. 5, pp. 413-431.
[http://dx.doi.org/10.1016/B978-1-4377-0651-2.10014-1]
[52]
Waljee, A.K.; Rogers, M.A.M.; Lin, P.; Singal, A.G.; Stein, J.D.; Marks, R.M.; Ayanian, J.Z.; Nallamothu, B.K. Short term use of oral corticosteroids and related harms among adults in the United States: population based cohort study. BMJ, 2017, 357, j1415.
[http://dx.doi.org/10.1136/bmj.j1415] [PMID: 28404617]
[53]
Bernstein, L.R.; van der Hoeven, J.J.M.; Boer, R.O. Hepatocellular carcinoma detection by gallium scan and subsequent treatment by gallium maltolate: rationale and case study. Anticancer. Agents Med. Chem., 2011, 11(6), 585-590.
[http://dx.doi.org/10.2174/187152011796011046] [PMID: 21554205]
[54]
Bernstein, L.R. Successful treatment of refractory postherpetic neuralgia with topical gallium maltolate: case report. Pain Med., 2012, 13(7), 915-918.
[http://dx.doi.org/10.1111/j.1526-4637.2012.01404.x] [PMID: 22680305]
[55]
Eby, G. Elimination of arthritis pain and inflammation for over 2 years with a single 90 min, topical 14% gallium nitrate treatment: case reports and review of actions of gallium III. Med. Hypotheses, 2005, 65(6), 1136-1141.
[http://dx.doi.org/10.1016/j.mehy.2005.06.021] [PMID: 16122880]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy