Antimony(III) induces fibroblast-like phenotype, profibrotic factors and reactive oxygen species in mouse renal cells
Nicole Roldán A , Danitza Pizarro A , Marcelo Verdugo A , Nicolas Salinas-Parra A , Waldo Quiroz A , Cristian Reyes-Martinez A , Stefanny Figueroa A , Carolina Quiroz A and Alexis A. Gonzalez A BA Instituto de Química, Pontificia Universidad Católica de Valparaíso, Avenida Universidad N° 330, Curauma 56-032-2274964, Valparaíso, Chile.
B Corresponding author. Email: alexis.gonzalez@pucv.cl
Environmental Chemistry 17(2) 182-190 https://doi.org/10.1071/EN19156
Submitted: 27 May 2019 Accepted: 31 July 2019 Published: 9 September 2019
Environmental context. Antimony is a metalloid occurring at overall low concentrations in the Earth’s crust. Owing to anthropogenic activities, however, antimony can be found at elevated and detrimental levels in some environments. We report eco-toxicological effects of antimony in biological models, results from which can help predict antimony’s ecological and environmental impact.
Abstract. The aim of this work was to evaluate the effect of SbIII on cell integrity, expression of profibrotic factors and reactive oxygen species (ROS) in mouse cortical collecting duct cells (M-1 cell line). M-1 cells were incubated with SbIII for 24 h. Cell morphology and RNA expression level (connecting tissue growth factor, CTGF), α-SMOOTH MUSCLE ACTIN (α-SMA) and collagen I were analysed. The total Sb content according to each cell compartment was determined and ROS production was measured. Eighty percent of the total Sb was detected in the extracellular medium. A significant increase in ROS production and CTGF protein expression were observed at 100 μg L−1 SbIII. M-1 cells showed a non-classic epithelial cell shape at 100 μg L−1 and a reduction in the collecting duct-specific marker aquaporin-2. At 100 μg L−1, the number of collagen I-positive cells increased. At 300 μg L−1, a gross cell nuclear rupture was observed. These results demonstrate that an SbIII concentration of 100 μg L−1 is able to promote the induction of CTGF and collagen I along with the induction of ROS, which suggests a cytotoxicity of SbIII in M-1 kidney collecting duct cells.
Additional keywords: collagen I, collecting duct, CTGF, cytotoxicity, kidney, α-SMA, Sb2O3.
References
Berman J (2003). Current treatment approaches to leishmaniasis. Current Opinion in Infectious Diseases 16, 397–401.| Current treatment approaches to leishmaniasisCrossref | GoogleScholarGoogle Scholar | 14501991PubMed |
Brochu C, Wang J, Roy G, Messier N, Wang XY, Saravia NG, Ouellette M (2003). Antimony uptake systems in the protozoan parasite Leishmania and accumulation differences in antimony-resistant parasites. Antimicrobial Agents and Chemotherapy 47, 3073–3079.
| Antimony uptake systems in the protozoan parasite Leishmania and accumulation differences in antimony-resistant parasitesCrossref | GoogleScholarGoogle Scholar | 14506011PubMed |
Casas JM, Crisóstomo G, Cifuentes L (2004). Antimony solubility and speciation in aqueous sulphuric acid solutions at 298 K. Canadian Journal of Chemical Engineering 82, 175–183.
| Antimony solubility and speciation in aqueous sulphuric acid solutions at 298 KCrossref | GoogleScholarGoogle Scholar |
Chulay JD, Fleckenstein L, Smith DH (1988). Pharmacokinetics of antimony during treatment of visceral leishmaniasis with sodium stibogluconate or meglumine antimoniate. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 69–72.
| Pharmacokinetics of antimony during treatment of visceral leishmaniasis with sodium stibogluconate or meglumine antimoniateCrossref | GoogleScholarGoogle Scholar | 2845611PubMed |
Cuevas CA, Gonzalez AA, Inestrosa NC, Vio CP, Prieto MC (2015). Angiotensin II increases fibronectin and collagen I through the β-catenin-dependent signaling in mouse collecting duct cells. American Journal of Physiology. Renal Physiology 308, F358–F365.
| Angiotensin II increases fibronectin and collagen I through the β-catenin-dependent signaling in mouse collecting duct cellsCrossref | GoogleScholarGoogle Scholar | 25411386PubMed |
de la Calle-Guntiñas MB, Madrid Y, Cámara C (1992). Stability study of total antimony, Sb(III) and Sb(V) at the trace level. Fresenius’ Journal of Analytical Chemistry 344, 27–29.
| Stability study of total antimony, Sb(III) and Sb(V) at the trace levelCrossref | GoogleScholarGoogle Scholar |
Fenton RA, Praetorius J (2011). Molecular physiology of the medullary collecting duct. Comprehensive Physiology 1, 1031–1056.
| Molecular physiology of the medullary collecting ductCrossref | GoogleScholarGoogle Scholar | 23737211PubMed |
Ferreira WA, Islam A, Andrade APS, Fernandes FR, Frézard F, Demicheli C (2014). Mixed antimony(V) complexes with different sugars to modulate the oral bioavailability of pentavalent antimonial drugs. Molecules 19, 5478–5489.
| Mixed antimony(V) complexes with different sugars to modulate the oral bioavailability of pentavalent antimonial drugsCrossref | GoogleScholarGoogle Scholar | 24786687PubMed |
Filella M, Belzile N, Chen YW (2002). Antimony in the environment: A review focused on natural waters II. Relevant solution chemistry. Earth-Science Reviews 59, 265–285.
| Antimony in the environment: A review focused on natural waters II. Relevant solution chemistryCrossref | GoogleScholarGoogle Scholar |
Frézard F, Demicheli C, Ribeiro RR (2009). Pentavalent antimonials: New perspectives for old drugs. Molecules 14, 2317–2336.
| Pentavalent antimonials: New perspectives for old drugsCrossref | GoogleScholarGoogle Scholar | 19633606PubMed |
Friedrich K, Vieira FA, Porrozzi R, Marchevsky RS, Miekeley N, Grimaldi G, Paumgartten FJR (2012). Disposition of antimony in rhesus monkeys infected with Leishmania braziliensis and treated with meglumine antimoniate. Journal of Toxicology and Environmental Health. Part A. 75, 63–75.
| Disposition of antimony in rhesus monkeys infected with Leishmania braziliensis and treated with meglumine antimoniateCrossref | GoogleScholarGoogle Scholar | 22129235PubMed |
Furuta N, Iijima A, Kambe A, Sakai K, Sato K (2005). Concentrations, enrichment and predominant sources of Sb and other trace elements in size classified airborne particulate matter collected in Tokyo from 1995 to 2004. Journal of Environmental Monitoring 7, 1155–1161.
| Concentrations, enrichment and predominant sources of Sb and other trace elements in size classified airborne particulate matter collected in Tokyo from 1995 to 2004Crossref | GoogleScholarGoogle Scholar | 16307066PubMed |
Gebel TW, Suchenwirth RHR, Bolten C, Dunkelberg HH (1998). Human biomonitoring of arsenic and antimony in case of an elevated geogenic exposure. Environmental Health Perspectives 106, 33–39.
| Human biomonitoring of arsenic and antimony in case of an elevated geogenic exposureCrossref | GoogleScholarGoogle Scholar | 9417766PubMed |
Gómez DR, Fernanda Giné M, Claudia Sánchez Bellato A, Smichowski P (2005). Antimony: a traffic-related element in the atmosphere of Buenos Aires, Argentina. Journal of Environmental Monitoring 7, 1162–1168.
| Antimony: a traffic-related element in the atmosphere of Buenos Aires, ArgentinaCrossref | GoogleScholarGoogle Scholar | 16307067PubMed |
Gonzalez AA, Liu L, Lara LS, Bourgeois CRT, Ibaceta-Gonzalez C, Salinas-Parra N, Gogulamudi VR, Seth DM, Prieto MC (2015). PKCα-dependent augmentation of cAMP and CREB phosphorylation mediates the angiotensin II stimulation of renin in the collecting duct. American Journal of Physiology. Renal Physiology 309, F880–F888.
| PKCα-dependent augmentation of cAMP and CREB phosphorylation mediates the angiotensin II stimulation of renin in the collecting ductCrossref | GoogleScholarGoogle Scholar | 26268270PubMed |
Gonzalez AA, Cifuentes-Araneda F, Ibaceta-Gonzalez C, Gonzalez-Vergara A, Zamora L, Henriquez R, Rosales CB, Gabriel Navar L, Prieto MC (2016). Vasopressin/V2 receptor stimulates renin synthesis in the collecting duct. American Journal of Physiology. Renal Physiology 310, F284–F293.
| Vasopressin/V2 receptor stimulates renin synthesis in the collecting ductCrossref | GoogleScholarGoogle Scholar | 26608789PubMed |
Gonzalez AA, Salinas-Parra N, Leach D, Navar LG, Prieto MC (2017). PGE2 upregulates renin through E-prostanoid receptor 1 via PKC/cAMP/CREB pathway in M-1 cells. American Journal of Physiology. Renal Physiology 313, F1038–F1049.
| PGE2 upregulates renin through E-prostanoid receptor 1 via PKC/cAMP/CREB pathway in M-1 cellsCrossref | GoogleScholarGoogle Scholar | 28701311PubMed |
Hansen C, Hansen EW, Hansen HR, Gammelgaard B, Stürup S (2011). Reduction of Sb(V) in a human macrophage cell line measured by HPLC-ICP-MS. Biological Trace Element Research 144, 234–243.
| Reduction of Sb(V) in a human macrophage cell line measured by HPLC-ICP-MSCrossref | GoogleScholarGoogle Scholar | 21618006PubMed |
Iwano M, Plieth D, Danoff TM (2002). Evidence that Fibroblasts Derive from Epithelium During Tissue Fibrosis. The Journal of Clinical Investigation 110, 341–350.
| Evidence that Fibroblasts Derive from Epithelium During Tissue FibrosisCrossref | GoogleScholarGoogle Scholar | 12163453PubMed |
Kalluri R, Zeisberg M (2006). Fibroblasts in cancer. Nature Reviews. Cancer 6, 392–401.
| Fibroblasts in cancerCrossref | GoogleScholarGoogle Scholar | 16572188PubMed |
Kokko JP (1987). Role of the collecting duct in urinary concentration. Kidney International 31, 606–610.
| Role of the collecting duct in urinary concentrationCrossref | GoogleScholarGoogle Scholar | 3550230PubMed |
Lecureur V, Lagadic-Gossmann D, Fardel O (2002). Potassium antimonyl tartrate induces reactive oxygen species-related apoptosis in human myeloid leukemic HL60 cells. International Journal of Oncology 20, 1071–1076.
| Potassium antimonyl tartrate induces reactive oxygen species-related apoptosis in human myeloid leukemic HL60 cellsCrossref | GoogleScholarGoogle Scholar | 11956606PubMed |
Lee JM, Dedhar S, Kalluri R, Thompson EW (2006). The epithelial-mesenchymal transition: New insights in signaling, development, and disease. The Journal of Cell Biology 172, 973–981.
| The epithelial-mesenchymal transition: New insights in signaling, development, and diseaseCrossref | GoogleScholarGoogle Scholar | 16567498PubMed |
Lipson KE, Wong C, Teng Y, Spong S (2012). CTGF is a central mediator of tissue remodeling and fibrosis and its inhibition can reverse the process of fibrosis. Fibrogenesis & Tissue Repair 5, S24
| CTGF is a central mediator of tissue remodeling and fibrosis and its inhibition can reverse the process of fibrosisCrossref | GoogleScholarGoogle Scholar |
López S, Aguilar L, Mercado L, Bravo M, Quiroz W (2015). Sb(V) reactivity with human blood components: redox effects. PLoS One 10, e0114796
| Sb(V) reactivity with human blood components: redox effectsCrossref | GoogleScholarGoogle Scholar | 26618512PubMed |
Maciaszczyk-Dziubinska E, Wawrzycka D, Wysocki R (2012). Arsenic and antimony transporters in eukaryotes. International Journal of Molecular Sciences 13, 3527–3548.
| Arsenic and antimony transporters in eukaryotesCrossref | GoogleScholarGoogle Scholar | 22489166PubMed |
Mann KK, Davison K, Colombo M, Colosimo AL, Diaz Z, Padovani AMS, Guo Q, Scrivens PJ, Gao W, Mader S, Miller WH (2006). Antimony trioxide-induced apoptosis is dependent on SEK1/JNK signaling. Toxicology Letters 160, 158–170.
| Antimony trioxide-induced apoptosis is dependent on SEK1/JNK signalingCrossref | GoogleScholarGoogle Scholar | 16112521PubMed |
Meran S, Steadman R (2011). Fibroblasts and myofibroblasts in renal fibrosis. International Journal of Experimental Pathology 92, 158–167.
| Fibroblasts and myofibroblasts in renal fibrosisCrossref | GoogleScholarGoogle Scholar | 21355940PubMed |
Miekeley N, Mortari SR, Schubach AO (2002). Monitoring of total antimony and its species by ICP-MS and on-line ion chromatography in biological samples from patients treated for leishmaniasis. Analytical and Bioanalytical Chemistry 372, 495–502.
| Monitoring of total antimony and its species by ICP-MS and on-line ion chromatography in biological samples from patients treated for leishmaniasisCrossref | GoogleScholarGoogle Scholar | 11939540PubMed |
Murciego AM, Sánchez AG, González MAR, Gil EP, Gordillo CT, Fernández JC, Triguero TB (2007). Antimony distribution and mobility in topsoils and plants (Cytisus striatus, Cistus ladanifer and Dittrichia viscosa) from polluted Sb-mining areas in Extremadura (Spain). Environmental Pollution 145, 15–21.
| Antimony distribution and mobility in topsoils and plants (Cytisus striatus, Cistus ladanifer and Dittrichia viscosa) from polluted Sb-mining areas in Extremadura (Spain)Crossref | GoogleScholarGoogle Scholar | 16730108PubMed |
Ng YY, Huang TP, Yang WC, Chen ZP, Yang AH, Mu W, Nikolic-Paterson DJ, Atkins RC, Lan HY (1998). Tubular epithelial-myofibroblast transdifferentiation in progressive tubulointerstitial fibrosis in 5/6 nephrectomized rats. Kidney International 54, 864–876.
| Tubular epithelial-myofibroblast transdifferentiation in progressive tubulointerstitial fibrosis in 5/6 nephrectomized ratsCrossref | GoogleScholarGoogle Scholar | 9734611PubMed |
Okkenhaug G, Grasshorn Gebhardt KA, Amstaetter K, Lassen Bue H, Herzel H, Mariussen E, Rossebø Almås Å, Cornelissen G, Breedveld GD, Rasmussen G, Mulder J (2016). Antimony (Sb) and lead (Pb) in contaminated shooting range soils: Sb and Pb mobility and immobilization by iron based sorbents, a field study. Journal of Hazardous Materials 307, 336–343.
| Antimony (Sb) and lead (Pb) in contaminated shooting range soils: Sb and Pb mobility and immobilization by iron based sorbents, a field studyCrossref | GoogleScholarGoogle Scholar | 26799225PubMed |
Olliaro PL, Bryceson ADM (1993). Practical progress and new drugs for changing patterns of leishmaniasis. Parasitology Today 9, 323–328.
| Practical progress and new drugs for changing patterns of leishmaniasisCrossref | GoogleScholarGoogle Scholar | 15463794PubMed |
Quiroz W, De Gregori I, Basilio P, Bravo M, Pinto M, Lobos MG (2009). Heavy weight vehicle traffic and its relationship with antimony content in human blood. Journal of Environmental Monitoring 11, 1051–1055.
| Heavy weight vehicle traffic and its relationship with antimony content in human bloodCrossref | GoogleScholarGoogle Scholar | 19436864PubMed |
Quiroz W, Arias H, Bravo M, Pinto M, Lobos MG, Cortés M (2011). Development of analytical method for determination of Sb(V), Sb(III) and TMSb(V) in occupationally exposed human urine samples by HPLC-HG-AFS. Microchemical Journal 97, 78–84.
| Development of analytical method for determination of Sb(V), Sb(III) and TMSb(V) in occupationally exposed human urine samples by HPLC-HG-AFSCrossref | GoogleScholarGoogle Scholar |
Quiroz W, Aguilar L, Barría M, Veneciano J, Martínez D, Bravo M, Lobos MG, Mercado L (2013a). Sb(V) and Sb(III) distribution in human erythrocytes: Speciation methodology and the influence of temperature, time and anticoagulants. Talanta 115, 902–910.
| Sb(V) and Sb(III) distribution in human erythrocytes: Speciation methodology and the influence of temperature, time and anticoagulantsCrossref | GoogleScholarGoogle Scholar | 24054681PubMed |
Quiroz W, Cortés M, Astudillo F, Bravo M, Cereceda F, Vidal V, Lobos MG (2013b). Antimony speciation in road dust and urban particulate matter in Valparaiso, Chile: Analytical and environmental considerations. Microchemical Journal 110, 266–272.
| Antimony speciation in road dust and urban particulate matter in Valparaiso, Chile: Analytical and environmental considerationsCrossref | GoogleScholarGoogle Scholar |
Rashedy AH, Solimany AA, Ismail AK, Wahdan MH, Saban KA (2013). Histopathological and functional effects of antimony on the renal cortex of growing albino rat. International Journal of Clinical and Experimental Pathology 6, 1467–1480.
Roldán N, Salinas-Parra N, Gonzalez AA, Cifuentes-Araneda F, Arias H, Bravo M, Quiroz W (2016). Implementation of an analytical method for the determination of inorganic arsenic species in occupationally exposed human urine samples and its toxic effects on epithelial cells of renal collecting tubule. Journal of the Chilean Chemical Society 61, 3214–3218.
| Implementation of an analytical method for the determination of inorganic arsenic species in occupationally exposed human urine samples and its toxic effects on epithelial cells of renal collecting tubuleCrossref | GoogleScholarGoogle Scholar |
Roldán N, Pizarro D, Frezard F, Bravo M, Verdugo M, Suzuki N, Ogra Y, Quiroz W (2019). Analytical methodology for the simultaneous determination of NMG-Sb(V), iSb(V), and iSb(III) species by anion exchange liquid chromatography in Glucantime® and its biological application in Wistar rat urine. Journal of Analytical Atomic Spectrometry 34, 203–213.
| Analytical methodology for the simultaneous determination of NMG-Sb(V), iSb(V), and iSb(III) species by anion exchange liquid chromatography in Glucantime® and its biological application in Wistar rat urineCrossref | GoogleScholarGoogle Scholar |
Saggerson ED, Carpenter CA, Veiga JA (1983). Stimulation Of Renal Gluconeogenesis By Exogenous Adenine Nucleotides. Biochimica et Biophysica Acta 755, 119–126.
| Stimulation Of Renal Gluconeogenesis By Exogenous Adenine NucleotidesCrossref | GoogleScholarGoogle Scholar | 6297608PubMed |
Salerno M, Petroutsa M, Garnier-Suillerot A (2002). The MRP1-mediated effluxes of arsenic and antimony do not require arsenic-glutathione and antimony-glutathione complex formation. Journal of Bioenergetics and Biomembranes 34, 135–145.
| The MRP1-mediated effluxes of arsenic and antimony do not require arsenic-glutathione and antimony-glutathione complex formationCrossref | GoogleScholarGoogle Scholar | 12018890PubMed |
Salinas-Parra N, Reyes-Martínez C, Prieto MC, Gonzalez AA (2017). Prostaglandin E2 Induces Prorenin-Dependent Activation of (Pro)renin Receptor and Upregulation of Cyclooxygenase-2 in Collecting Duct Cells. The American Journal of the Medical Sciences 354, 310–318.
| Prostaglandin E2 Induces Prorenin-Dependent Activation of (Pro)renin Receptor and Upregulation of Cyclooxygenase-2 in Collecting Duct CellsCrossref | GoogleScholarGoogle Scholar | 28918839PubMed |
Sánchez-López E, Díez RR, Vita JR, Mateos SR, Díez RRR, García ER, Barria CL, Mezzano S, Selgas R, Egido J, Ortiz A, Ruiz-Ortega M (2009). El factor de crecimiento de tejido conectivo (CTGF): factor clave en el inicio y la progresión del daño renal. Órgano Oficial de la Sociedad Española de Nefrología 29, 382–391.
Schafer FQ, Buettner GR (2001). Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radical Biology & Medicine 30, 1191–1212.
| Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione coupleCrossref | GoogleScholarGoogle Scholar |
Séby F, Gleyzes C, Grosso O, Plau B, Donard OFX (2012). Speciation of antimony in injectable drugs used for leishmaniasis treatment (Glucantime®) by HPLC-ICP-MS and DPP. Analytical and Bioanalytical Chemistry 404, 2939–2948.
| Speciation of antimony in injectable drugs used for leishmaniasis treatment (Glucantime®) by HPLC-ICP-MS and DPPCrossref | GoogleScholarGoogle Scholar | 23052871PubMed |
Smichowski P, Gómez D, Frazzoli C, Caroli S (2007). Traffic-Related Elements in Airborne Particulate Matter. Applied Spectroscopy Reviews 43, 23–49.
| Traffic-Related Elements in Airborne Particulate MatterCrossref | GoogleScholarGoogle Scholar |
Stoos BA, Náray-Fejes-Tóth A, Carretero OA, Ito S, Fejes-Tóth G (1991). Characterization of a mouse cortical collecting duct cell line. Kidney International 39, 1168–1175.
| Characterization of a mouse cortical collecting duct cell lineCrossref | GoogleScholarGoogle Scholar | 1654478PubMed |
Sun H, Yan SC, Cheng WS (2000). Interaction of antimony tartrate with the tripeptide glutathione implication for its mode of action. European Journal of Biochemistry 267, 5450–5457.
| Interaction of antimony tartrate with the tripeptide glutathione implication for its mode of actionCrossref | GoogleScholarGoogle Scholar | 10951203PubMed |
Sundar S, Chakravarty J (2010). Antimony toxicity. International Journal of Environmental Research and Public Health 7, 4267–4277.
| Antimony toxicityCrossref | GoogleScholarGoogle Scholar | 21318007PubMed |
Takahashi S, Sato H, Kubota Y, Utsumi H, Bedford JS, Okayasu R (2002). Inhibition of DNA-double strand break repair by antimony compounds. Toxicology 180, 249–256.
| Inhibition of DNA-double strand break repair by antimony compoundsCrossref | GoogleScholarGoogle Scholar | 12393294PubMed |
Tirmenstein MA, Plews C, Walker M, Woolery HW, Toraason M (1995). Antimony-Induced Oxidative Stress and Toxicity un Cultured Cardiac Myocytes. Toxicology and Applied Pharmacology 130, 41–47.
| Antimony-Induced Oxidative Stress and Toxicity un Cultured Cardiac MyocytesCrossref | GoogleScholarGoogle Scholar | 7839369PubMed |
Verdugo M, Ogra Y, Quiroz W (2016). Mechanisms underlying the toxic effects of antimony species in human embryonic kidney cells (HEK-293) and their comparison with arsenic species. The Journal of Toxicological Sciences 41, 783–792.
| Mechanisms underlying the toxic effects of antimony species in human embryonic kidney cells (HEK-293) and their comparison with arsenic speciesCrossref | GoogleScholarGoogle Scholar | 27853107PubMed |
Verdugo M, Encinar JR, Costa-Fernández JM, Menendez-Miranda M, Bouzas-Ramos D, Bravo M, Quiroz W (2017). Study of conformational changes and protein aggregation of bovine serum albumin in presence of Sb(III) and Sb(V). PLoS One 12, e0170869
| Study of conformational changes and protein aggregation of bovine serum albumin in presence of Sb(III) and Sb(V)Crossref | GoogleScholarGoogle Scholar | 28151990PubMed |
Zaghloul IY, Radwan MA, Al Jaser MH, Al Issa R (2010). Clinical efficacy and pharmacokinetics of antimony in cutaneous leishmaniasis patients treated with sodium stibogluconate. Journal of Clinical Pharmacology 50, 1230–1237.
| Clinical efficacy and pharmacokinetics of antimony in cutaneous leishmaniasis patients treated with sodium stibogluconateCrossref | GoogleScholarGoogle Scholar | 20663995PubMed |