Thiopurine S‑methyltransferase- and indolethylamine N‑methyltransferase-mediated formation of methylated tellurium compounds from tellurite.
INMT
LC-ICP-MS
Methylation
TPMT
Tellurium
Journal
Archives of toxicology
ISSN: 1432-0738
Titre abrégé: Arch Toxicol
Pays: Germany
ID NLM: 0417615
Informations de publication
Date de publication:
17 Oct 2024
17 Oct 2024
Historique:
received:
30
08
2024
accepted:
09
10
2024
medline:
17
10
2024
pubmed:
17
10
2024
entrez:
17
10
2024
Statut:
aheadofprint
Résumé
Tellurium (Te) is a metalloid widely used in various industries. However, its toxicological impact on humans is poorly understood. In this study, we investigated the role of two methyltransferases, thiopurine S‑methyltransferase (TPMT) and indolethylamine N‑methyltransferase (INMT), in the methylation of tellurite, an inorganic Te oxyanion. The products of the reaction of Te compounds catalyzed by recombinant human TPMT and/or INMT were analyzed by liquid chromatography hyphenated to inductively coupled plasma mass spectrometry (LC-ICP-MS) and gas chromatography mass spectrometry (GC-MS). We found that TPMT catalyzes the methylation of non-methylated Te and methanetellurol to generate dimethyltelluride. On the other hand, INMT catalyzes the methylation of methanetellurol and dimethyltelluride to produce trimethyltelluronium ion, a metabolite excreted into animal urine. We conclude that TPMT and INMT are cooperatively responsible for the detoxification of Te oxyanions through methylation to form trimethyltelluronium ions.
Identifiants
pubmed: 39417876
doi: 10.1007/s00204-024-03890-4
pii: 10.1007/s00204-024-03890-4
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Japan Society for the Promotion of Science
ID : 19K07079
Organisme : Japan Society for the Promotion of Science
ID : 22K15260
Organisme : Japan Society for the Promotion of Science
ID : 24H00749
Organisme : Japan Society for the Promotion of Science
ID : 24K21304
Informations de copyright
© 2024. The Author(s).
Références
Anan Y, Yoshida M, Hasegawa S et al (2013) Speciation and identification of tellurium-containing metabolites in garlic. Allium Sativum Metallomics 5(9):1215–1224. https://doi.org/10.1039/c3mt00108c
doi: 10.1039/c3mt00108c
Baesman SM, Bullen TD, Dewald J et al (2007) Formation of tellurium nanocrystals during anaerobic growth of bacteria that use Te oxyanions as respiratory electron acceptors. Appl Environ Microbiol 73(7):2135–2143. https://doi.org/10.1128/aem.02558-06
doi: 10.1128/aem.02558-06
pmcid: 1855670
Borsetti F, Borghese R, Francia F, Randi MR, Fedi S, Zannoni D (2003) Reduction of potassium tellurite to elemental tellurium and its effect on the plasma membrane redox components of the facultative phototroph Rhodobacter capsulatus. Protoplasma 221(1–2):153–161. https://doi.org/10.1007/s00709-002-0058-z
doi: 10.1007/s00709-002-0058-z
Byard JL (1969) Trimethyl selenide. A urinary metabolite of selenite. Arch Biochem Biophys 130:556–560. https://doi.org/10.1016/0003-9861(69)90070-8
doi: 10.1016/0003-9861(69)90070-8
Cournoyer B, Watanabe S, Vivian A (1998) A tellurite-resistance genetic determinant from phytopathogenic pseudomonads encodes a thiopurine methyltransferase: evidence of a widely-conserved family of methyltransferases1The international collaboration (IC) accession number of the DNA sequence is L49178.1. Biochim Biophys—Acta Gene Struct Expr 1397(2):161–168. https://doi.org/10.1016/S0167-4781(98)00020-7
doi: 10.1016/S0167-4781(98)00020-7
Cowgill UM (1988) The tellurium content of vegetation. Biol Trace Elem Res 17:43–67. https://doi.org/10.1007/bf02795446
doi: 10.1007/bf02795446
Crecelius EA (1977) Changes in the chemical speciation of arsenic following ingestion by man. Environ Health Perspect 19:147–150. https://doi.org/10.1289/ehp.7719147
doi: 10.1289/ehp.7719147
pmcid: 1637415
Di Tomaso G, Fedi S, Carnevali M, Manegatti M, Taddei C, Zannoni D (2002) The membrane-bound respiratory chain of Pseudomonas pseudoalcaligenes KF707 cells grown in the presence or absence of potassium tellurite. Microbiology 148(Pt 6):1699–1708. https://doi.org/10.1099/00221287-148-6-1699
doi: 10.1099/00221287-148-6-1699
Filonov D, Tice R, Luo R et al (2018) Initial assessment of variability of responses to toxicants in donor-specific endothelial colony forming cells. Front Public Health 6:369. https://doi.org/10.3389/fpubh.2018.00369
doi: 10.3389/fpubh.2018.00369
pmcid: 6308159
Fukumoto Y, Yamada H, Matsuhashi K et al (2020) Production of a urinary selenium metabolite, trimethylselenonium, by thiopurine S-methyltransferase and indolethylamine N-methyltransferase. Chem Res Toxicol 33(9):2467–2474. https://doi.org/10.1021/acs.chemrestox.0c00254
doi: 10.1021/acs.chemrestox.0c00254
Fukumoto Y, Kyono R, Shibukawa Y, Tanaka Y-k, Suzuki N, Ogra Y (2024) Differential molecular mechanisms of substrate recognition by selenium methyltransferases, INMT and TPMT, in selenium detoxification and excretion. J Biol Chem 300(2):105599. https://doi.org/10.1016/j.jbc.2023.105599
doi: 10.1016/j.jbc.2023.105599
Lin S, Shi Q, Nix FB et al (2002) A novel S-adenosyl-L-methionine: Arsenic(III) methyltransferase from rat liver cytosol. J Biol Chem 277(13):10795–10803. https://doi.org/10.1074/jbc.M110246200
doi: 10.1074/jbc.M110246200
Lohren H, Blagojevic L, Fitkau R et al (2015) Toxicity of organic and inorganic mercury species in differentiated human neurons and human astrocytes. J Trace Elem Med Biol 32:200–208. https://doi.org/10.1016/j.jtemb.2015.06.008
doi: 10.1016/j.jtemb.2015.06.008
Matos Reyes MN, Cervera ML, de la Guardia M (2009) Determination of total Sb, Se, Te, and Bi and evaluation of their inorganic species in garlic by hydride-generation–atomic-fluorescence spectrometry. Anal Bioanal Chem 394(6):1557–1562. https://doi.org/10.1007/s00216-009-2713-0
doi: 10.1007/s00216-009-2713-0
Medina-Cruz D, Tien-Street W, Vernet-Crua A et al (2020) Tellurium, the forgotten element: A review of the properties, processes, and biomedical applications of the bulk and nanoscale metalloid. In: Li B, Moriarty TF, Webster T, Xing M (eds) Racing for the surface: antimicrobial and interface tissue engineering. Springer International Publishing, Cham, pp 723–783
doi: 10.1007/978-3-030-34471-9_26
Ogra Y, Kobayashi R, Ishiwata K, Suzuki KT (2007) Identification of urinary tellurium metabolite in rats administered sodium tellurite. J Anal at Spectrom 22(2):153–157. https://doi.org/10.1039/B613835G
doi: 10.1039/B613835G
Ogra Y, Kobayashi R, Ishiwata K, Suzuki KT (2008) Comparison of distribution and metabolism between tellurium and selenium in rats. J Inorg Biochem 102(7):1507–1513. https://doi.org/10.1016/j.jinorgbio.2008.01.012
doi: 10.1016/j.jinorgbio.2008.01.012
Ogra Y, Okubo E, Takahira M (2010) Distinct uptake of tellurate from selenate in a selenium accumulator, Indian mustard (Brassica juncea). Metallomics 2(5):328–333. https://doi.org/10.1039/C000088D
doi: 10.1039/C000088D
Ogra Y, Awaya Y, Anan Y (2015) Comparison of accumulation of four metalloids in Allium sativum. Bull Environ Contam Toxicol 94(5):604–608. https://doi.org/10.1007/s00128-015-1508-6
doi: 10.1007/s00128-015-1508-6
Ranjard L, Prigent-Combaret C, Nazaret S, Cournoyer B (2002) Methylation of inorganic and organic selenium by the bacterial thiopurine methyltransferase. J Bacteriol 184(11):3146–3149
doi: 10.1128/JB.184.11.3146-3149.2002
pmcid: 135077
Ranjard L, Nazaret S, Cournoyer B (2003) Freshwater bacteria can methylate sselenium through the thiopurine methyltransferase pathway. Appl Environ Microbiol 69(7):3784–3790. https://doi.org/10.1128/AEM.69.7.3784-3790.2003
doi: 10.1128/AEM.69.7.3784-3790.2003
pmcid: 165148
Takada S, Tanaka Y-k, Kumagai K, Kobayashi K, Hokura A, Ogra Y (2022) Formation of biogenic tellurium nanorods in unicellular green alga Chlamydomonas reinhardtii. Metallomics. https://doi.org/10.1093/mtomcs/mfac089
doi: 10.1093/mtomcs/mfac089
Takada S, Yamagishi Y, Tanaka Y-k et al (2024) Identification of tellurium metabolite in broccoli using complementary analyses of inorganic and organic mass spectrometry. Chem Res Toxicol 37(7):1210–1217. https://doi.org/10.1021/acs.chemrestox.4c00148
doi: 10.1021/acs.chemrestox.4c00148
Tam GKH, Charbonneau SM, Bryce F, Pomroy C, Sandi E (1979) Metabolism of inorganic arsenic (
doi: 10.1016/0041-008X(79)90157-1
Tanaka Y-k, Takada S, Kumagai K, Kobayashi K, Hokura A, Ogra Y (2020) Elucidation of tellurium biogenic nanoparticles in garlic, Allium sativum, by inductively coupled plasma-mass spectrometry. J Trace Elem Med Biol 62:126628. https://doi.org/10.1016/j.jtemb.2020.126628
doi: 10.1016/j.jtemb.2020.126628
Tanaka Y-k, Yanagi H, Shiokawa A et al (2024) Role of sulfane sulfur species in elemental tellurium nanorod formation in mammalian cells. Red Biochem Chem 8:100029. https://doi.org/10.1016/j.rbc.2024.100029
doi: 10.1016/j.rbc.2024.100029
Torres B, Tyler JS, Satyshur KA, Ruoho AE (2019) Human indole(ethyl)amine-N-methyltransferase (hINMT) catalyzed methylation of tryptamine, dimethylsulfide and dimethylselenide is enhanced under reducing conditions—a comparison between 254C and 254F, two common hINMT variants. PLoS ONE 14(7):e0219664. https://doi.org/10.1371/journal.pone.0219664
doi: 10.1371/journal.pone.0219664
pmcid: 6634407
Urbančič D, Kotar A, Šmid A et al (1863) (2019) Methylation of selenocysteine catalysed by thiopurine S-methyltransferase. Biochim Biophys Acta—General Subjects 1:182–190. https://doi.org/10.1016/j.bbagen.2018.10.002
doi: 10.1016/j.bbagen.2018.10.002
Weinshilboum RM, Otterness DM, Szumlanski CL (1999) Methylation Pharmacogenetics: catechol O-methyltransferase, thiopurine methyltransferase, and histamine N-methyltransferase. Ann Rev Pharmacol Toxicol 39:19–52. https://doi.org/10.1146/annurev.pharmtox.39.1.19
doi: 10.1146/annurev.pharmtox.39.1.19
Yurkov V, Jappe J, Vermeglio A (1996) Tellurite resistance and reduction by obligately aerobic photosynthetic bacteria. Appl Environ Microbiol 62(11):4195–4198
doi: 10.1128/aem.62.11.4195-4198.1996
pmcid: 1388984