Hydroxylamine-induced oxidation of ferrous nitrobindins.

Ferrous Arabidopsis thaliana nitrobindin Ferrous Homo sapiens nitrobindin Ferrous Mycobacterium tuberculosis nitrobindin Hydroxylamine-induced oxidation Kinetics

Journal

Journal of biological inorganic chemistry : JBIC : a publication of the Society of Biological Inorganic Chemistry
ISSN: 1432-1327
Titre abrégé: J Biol Inorg Chem
Pays: Germany
ID NLM: 9616326

Informations de publication

Date de publication:
08 2022
Historique:
received: 20 12 2021
accepted: 21 04 2022
pubmed: 12 5 2022
medline: 26 8 2022
entrez: 11 5 2022
Statut: ppublish

Résumé

Hemoglobin and myoglobin are generally taken as molecular models of all-α-helical heme-proteins. On the other hand, nitrophorins and nitrobindins (Nb), which are arranged in 8 and 10 β-strands, respectively, represent the molecular models of all-β-barrel heme-proteins. Here, kinetics of the hydroxylamine- (HA-) mediated oxidation of ferrous Mycobacterium tuberculosis, Arabidopsis thaliana, and Homo sapiens nitrobindins (Mt-Nb(II), At-Nb(II), and Hs-Nb(II), respectively), at pH 7.0 and 20.0 °C, are reported. Of note, HA displays antibacterial properties and is a good candidate for the treatment and/or prevention of reactive nitrogen species- (RNS-) linked aging-related pathologies, such as macular degeneration. Under anaerobic conditions, mixing the Mt-Nb(II), At-Nb(II), and Hs-Nb(II) solutions with the HA solutions brings about absorbance spectral changes reflecting the formation of the ferric derivative (i.e., Mt-Nb(III), At-Nb(III), and Hs-Nb(III), respectively). Values of the second order rate constant for the HA-mediated oxidation of Mt-Nb(II), At-Nb(II), and Hs-Nb(II) are 1.1 × 10

Identifiants

pubmed: 35543759
doi: 10.1007/s00775-022-01940-9
pii: 10.1007/s00775-022-01940-9
doi:

Substances chimiques

Ferric Compounds 0
Hydroxylamines 0
Myoglobin 0
Hydroxylamine 2FP81O2L9Z
Heme 42VZT0U6YR
Iron E1UOL152H7

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

443-453

Informations de copyright

© 2022. The Author(s), under exclusive licence to Society for Biological Inorganic Chemistry (SBIC).

Références

Bunn HF, Forget BG (1986) Hemoglobin: molecular, genetic and clinical aspects. WB Saunders Company, Philadelphia
Wittenberg JB, Wittenberg BA (2003) Myoglobin function reassessed. J Exp Biol 206:2011–2020. https://doi.org/10.1242/jeb.00243
doi: 10.1242/jeb.00243 pubmed: 12756283
Ascenzi P, Brunori M (2016) A molecule for all seasons: the heme. J Porphyrins Phthalocyanines 29:1–16. https://doi.org/10.1142/S1088424616300081
doi: 10.1142/S1088424616300081
Keppner A, Maric D, Correia M, Koay TW, Orlando I, Vinogradov SN, Hoogewijs D (2020) Lessons from the post-genomic era: globin diversity beyond oxygen binding and transport. Redox Biol 37:101687. https://doi.org/10.1016/j.redox.2020.101687
doi: 10.1016/j.redox.2020.101687 pubmed: 32863222 pmcid: 7475203
Bianchetti CM, Blouin GC, Bitto E, Olson JS, Phillips GN Jr (2010) The structure and NO binding properties of the nitrophorin-like heme-binding protein from Arabidopsis thaliana gene locus At1g79260.1. Proteins 78:917–931. https://doi.org/10.1002/prot.22617
doi: 10.1002/prot.22617 pubmed: 19938152 pmcid: 2811769
De Simone G, di Masi A, Vita GM, Polticelli F, Pesce A, Nardini M, Bolognesi M, Ciaccio C, Coletta M, Turilli ES, Fasano M, Tognaccini L, Smulevich G, Abbruzzetti S, Viappiani C, Bruno S, Ascenzi P (2020) Mycobacterial and human nitrobindins: structure and function. Antioxid Redox Signal 33:229–246. https://doi.org/10.1089/ars.2019.7874
doi: 10.1089/ars.2019.7874 pubmed: 32295384
De Simone G, di Masi A, Pesce A, Bolognesi M, Ciaccio C, Tognaccini L, Smulevich G, Abbruzzetti S, Viappiani C, Bruno S, Monaca SD, Pietraforte D, Fattibene P, Coletta M, Ascenzi P (2021) Mycobacterial and human ferrous nitrobindins: spectroscopic and reactivity properties. Int J Mol Sci 22:1674. https://doi.org/10.3390/ijms22041674
doi: 10.3390/ijms22041674 pubmed: 33562340 pmcid: 7915275
De Simone G, di Masi A, Polticelli F, Ascenzi P (2018) Human nitrobindin: the first example of an all-β-barrel ferric heme-protein that catalyzes peroxynitrite detoxification. FEBS Open Bio 8:2002–2010. https://doi.org/10.1002/2211-5463.12534
doi: 10.1002/2211-5463.12534 pubmed: 30524950 pmcid: 6275384
Ascenzi P, Visca P (2008) Scavenging of reactive nitrogen species by mycobacterial truncated hemoglobins. Methods Enzymol 436:317–337. https://doi.org/10.1016/S0076-6879(08)36018-2
doi: 10.1016/S0076-6879(08)36018-2 pubmed: 18237641
Awuh JA, Flo TH (2017) Molecular basis of mycobacterial survival in macrophages. Cell Mol Life Sci 74:1625–1648. https://doi.org/10.1007/s00018-016-2422-8
doi: 10.1007/s00018-016-2422-8 pubmed: 27866220
Albert DM, Raven ML (2016) Ocular tuberculosis. Microbiol Spectr 4:101128. https://doi.org/10.1128/microbiolspec.TNMI7-0001-2016
doi: 10.1128/microbiolspec.TNMI7-0001-2016
Rifkind JM, Ramasamy S, Manoharan PT, Nagababu E, Mohanty JG (2004) Redox reactions of hemoglobin. Antioxid Redox Signal 6:657–666. https://doi.org/10.1089/152308604773934422
doi: 10.1089/152308604773934422 pubmed: 15130293
Mansouri A, Lurie AA (1993) Concise review: methemoglobinemia. Am J Hematol 42:7–12. https://doi.org/10.1002/ajh.2830420104
doi: 10.1002/ajh.2830420104 pubmed: 8416301
Smith LJ, Kahraman A, Thornton JM (2010) Heme proteins—diversity in structural characteristics, function, and folding. Proteins 78:2349–2368. https://doi.org/10.1002/prot.22747
doi: 10.1002/prot.22747 pubmed: 20544970
Ascenzi P, di Masi A, Tundo GR, Pesce A, Visca P, Coletta M (2014) Nitrosylation mechanisms of Mycobacterium tuberculosis and Campylobacter jejuni truncated hemoglobins N, O, and P. PLoS ONE 9:e102811. https://doi.org/10.1371/journal.pone.0102811
doi: 10.1371/journal.pone.0102811 pubmed: 25051055 pmcid: 4106858
Elahian F, Sepehrizadeh Z, Moghimi B, Mirzaei SA (2014) Human cytochrome b
doi: 10.3109/07388551.2012.732031 pubmed: 23113554
Ascenzi P, De Simone G, Polticelli F, Gioia M, Coletta M (2018) Reductive nitrosylation of ferric human hemoglobin bound to human haptoglobin 1–1 and 2–2. J Biol Inorg Chem 23:437–445. https://doi.org/10.1007/s00775-018-1551-y
doi: 10.1007/s00775-018-1551-y pubmed: 29605886
De Simone G, di Masi A, Ciaccio C, Coletta M, Ascenzi P (2020) NO Scavenging through reductive nitrosylation of ferric Mycobacterium tuberculosis and Homo sapiens Nitrobindins. Int J Mol Sci 21(24):9395. https://doi.org/10.3390/ijms21249395
doi: 10.3390/ijms21249395 pmcid: 7763097
Herold S (1999) Kinetic and spectroscopic characterization of an intermediate peroxynitrite complex in the nitrogen monoxide induced oxidation of oxyhemoglobin. FEBS Lett 443:81–84. https://doi.org/10.1016/s0014-5793(98)01345-3
doi: 10.1016/s0014-5793(98)01345-3 pubmed: 9928957
Minning DM, Gow AJ, Bonaventura J, Braun R, Dewhirst M, Goldberg DE, Stamler JS (1999) Ascaris haemoglobin is a nitric oxide-activated “deoxygenase.” Nature 401:497–502. https://doi.org/10.1038/46822
doi: 10.1038/46822 pubmed: 10519555
Herold S, Exner M, Nauser T (2001) Kinetic and mechanistic studies of the NO
doi: 10.1021/bi002407m pubmed: 11258960
Herold S, Fago A, Weber RE, Dewilde S, Moens L (2004) Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress. J Biol Chem 279:22841–22847. https://doi.org/10.1074/jbc.M313732200
doi: 10.1074/jbc.M313732200 pubmed: 15020597
Møller JKS, Skibsted LH (2004) Mechanism of nitrosylmyoglobin autoxidation: temperature and oxygen pressure effects on the two consecutive reactions. Chem Eur J 10:2291–2300. https://doi.org/10.1002/chem.200305368
doi: 10.1002/chem.200305368 pubmed: 15112219
Herold S, Puppo A (2005) Oxyleghemoglobin scavenges nitrogen monoxide and peroxynitrite: a possible role in functioning nodules? J Biol Inorg Chem 10:935–945. https://doi.org/10.1007/s00775-005-0046-9
doi: 10.1007/s00775-005-0046-9 pubmed: 16267661
Herold S, Röck G (2005) Mechanistic studies of the oxygen-mediated oxidation of nitrosylhemoglobin. Biochemistry 44:6223–6231. https://doi.org/10.1021/bi0475929
doi: 10.1021/bi0475929 pubmed: 15835910
Fasano M, Antonini G, Ascenzi P (2006) O
doi: 10.1016/j.bbrc.2006.04.154 pubmed: 16696943
Ascenzi P, Bolognesi M, Visca P (2007)
doi: 10.1016/j.bbrc.2007.04.024 pubmed: 17451651
Koebke KJ, Pauly DJ, Lerner L, Liu X, Pacheco AA (2013) Does the oxidation of nitric oxide by oxymyoglobin share an intermediate with the metmyoglobin-catalyzed isomerization of peroxynitrite? Inorg Chem 52:7623–7632. https://doi.org/10.1021/ic400697a
doi: 10.1021/ic400697a pubmed: 23768169
De Simone G, di Masi A, Fattibene P, Ciaccio C, Platas-Iglesias C, Coletta M, Pesce A, Ascenzi P (2021) Oxygen-mediated oxidation of ferrous nitrosylated nitrobindins. J Inorg Biochem 224:111579. https://doi.org/10.1016/j.jinorgbio.2021.111579
doi: 10.1016/j.jinorgbio.2021.111579 pubmed: 34479003
Exner M, Herold S (2000) Kinetic and mechanistic studies of the peroxynitrite-mediated oxidation of oxymyoglobin and oxyhemoglobin. Chem Res Toxicol 13:287–293. https://doi.org/10.1021/tx990201k
doi: 10.1021/tx990201k pubmed: 10775329
Ascenzi P, Milani M, Visca P (2006) Peroxynitrite scavenging by ferrous truncated hemoglobin GlbO from Mycobacterium leprae. Biochem Biophys Res Commun 351:528–533. https://doi.org/10.1016/j.bbrc.2006.10.060
doi: 10.1016/j.bbrc.2006.10.060 pubmed: 17069757
Herold S, Boccini F (2006) NO
doi: 10.1021/ic060469g pubmed: 16903752
Ascenzi P, Petrella G, Coletta M (2007) Ferricyanide-mediated oxidation of ferrous nitrosylated sperm whale myoglobin involves the formation of the ferric nitrosylated intermediate. Biochem Biophys Res Commun 359:871–876. https://doi.org/10.1016/j.bbrc.2007.05.196
doi: 10.1016/j.bbrc.2007.05.196 pubmed: 17562327
Ascenzi P, Ciaccio C, Coletta M (2007) Peroxynitrite-mediated oxidation of ferrous carbonylated myoglobin is limited by carbon monoxide dissociation. Biochem Biophys Res Commun 363:931–936. https://doi.org/10.1016/j.bbrc.2007.09.053
doi: 10.1016/j.bbrc.2007.09.053 pubmed: 17910950
De Marinis E, Casella L, Ciaccio C, Coletta M, Visca P, Ascenzi P (2009) Catalytic peroxidation of nitrogen monoxide and peroxynitrite by globins. IUBMB Life 61:62–73. https://doi.org/10.1002/iub.149
doi: 10.1002/iub.149 pubmed: 19109828
Antonini E, Brunori M, Wyman J (1965) Studies on the oxidation-reduction potentials of heme proteins. IV. The kinetics of oxidation of hemoglobin and myoglobin by ferricyanide. Biochemistry 4:545–551. https://doi.org/10.1021/bi00879a026
doi: 10.1021/bi00879a026 pubmed: 14311627
Antonini E, Brunori M (1971) Hemoglobin and myoglobin in their reactions with ligands. North-Holland Publishing Co, Amsterdam
Bannister JV, Bannister WH, Ascenzi P, Focesi A, Brunori M (1976) Oxygen and carbon monoxide binding to myoglobin from the dolphin fish Coryphaena hippurus. FEBS Lett 65:361–364. https://doi.org/10.1016/0014-5793(76)80147-0
doi: 10.1016/0014-5793(76)80147-0 pubmed: 955070
Bazylinski DA, Arkowitz RA, Hollocher TC (1987) Decomposition of hydroxylamine by hemoglobin. Arch Biochem Biophys 259:520–526. https://doi.org/10.1016/0003-9861(87)90518-2
doi: 10.1016/0003-9861(87)90518-2 pubmed: 3426242
Sturms R, DiSpirito AA, Fulton DB, Hargrove MS (2011) Hydroxylamine reduction to ammonium by plant and cyanobacterial hemoglobins. Biochemistry 50:10829–10835. https://doi.org/10.1021/bi201425f
doi: 10.1021/bi201425f pubmed: 22080728
Athwal NS, Alagurajan J, Andreotti AH, Hargrove MS (2016) Role of reversible histidine coordination in hydroxylamine reduction by plant hemoglobins (phytoglobins). Biochemistry 55:5809–5817. https://doi.org/10.1021/acs.biochem.6b00775
doi: 10.1021/acs.biochem.6b00775 pubmed: 27661977
Ascenzi P, Ciaccio C, Gasperi T, Pesce A, Caporaso L, Coletta M (2017) Hydroxylamine-induced oxidation of ferrous carbonylated truncated hemoglobins from Mycobacterium tuberculosis and Campylobacter jejuni is limited by carbon monoxide dissociation. J Biol Inorg Chem 22:977–986. https://doi.org/10.1007/s00775-017-1476-x
doi: 10.1007/s00775-017-1476-x pubmed: 28646425
Ascenzi P, De Simone G, Ciaccio C, Santucci R, Coletta M (2018) Hydroxylamine-induced oxidation of ferrous CO-bound carboxymethylated-cytochrome c. J Porphyrins Phthalocyanines 22:1–10. https://doi.org/10.1142/S1088424618501055
doi: 10.1142/S1088424618501055
Miret-Casals L, Baelo A, Julián E, Astola J, Lobo-Ruiz A, Albericio F, Torrents E (2018) Hydroxylamine derivatives as a new paradigm in the search of antibacterial agents. ACS Omega 3:17057–17069. https://doi.org/10.1021/acsomega.8b01384
doi: 10.1021/acsomega.8b01384 pubmed: 31458325 pmcid: 6643834
Voloboueva LA, Killilea DW, Atamna H, Ames BN (2007) N-tert-butyl hydroxylamine, a mitochondrial antioxidant, protects human retinal pigment epithelial cells from iron overload: relevance to macular degeneration. FASEB J 21:4077–4086. https://doi.org/10.1096/fj.07-8396com
doi: 10.1096/fj.07-8396com pubmed: 17656467
Jarrett SG, Boulton ME (2012) Consequences of oxidative stress in age-related macular degeneration. Mol Aspects Med 33:399–417. https://doi.org/10.1016/j.mam.2012.03.009
doi: 10.1016/j.mam.2012.03.009 pubmed: 22510306 pmcid: 3392472
Zarling JA, Brunt VE, Vallerga AK, Li W, Tao A, Zarling DA, Minson CT (2015) Nitroxide pharmaceutical development for age-related degeneration and disease. Front Gen 6:325. https://doi.org/10.3389/fgene.2015.00325
doi: 10.3389/fgene.2015.00325
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71. https://doi.org/10.1006/niox.2000.0319
doi: 10.1006/niox.2000.0319 pubmed: 11178938
Afkhami A, Madrakian T, Maleki A (2005) Spectrophotometric determination of hydroxylamine and nitrite in mixture in water and biological samples after micelle-mediated extraction. Anal Biochem 347:162–164. https://doi.org/10.1016/j.ab.2005.09.018
doi: 10.1016/j.ab.2005.09.018 pubmed: 16243290
Fago A, Mathews AJ, Dewilde S, Moens L, Brittain T (2006) The reaction of neuroglobin with CO: evidence for two forms of the ferrous protein. J Inorg Biochem 100:1339–1343. https://doi.org/10.1016/j.jinorgbio.2006.03.009
doi: 10.1016/j.jinorgbio.2006.03.009 pubmed: 16684569
Ascenzi P, di Masi A, Leboffe L, Fiocchetti M, Nuzzo MT, Brunori M, Marino M (2016) Neuroglobin: from structure to function in health and disease. Mol Aspects Med 52:1–48. https://doi.org/10.1016/j.mam.2016.10.004
doi: 10.1016/j.mam.2016.10.004 pubmed: 27825818
Ouellet H, Juszczak L, Dantsker D, Samuni U, Ouellet YH, Savard PY, Wittenberg JB, Wittenberg BA, Friedman JM, Guertin M (2003) Reactions of Mycobacterium tuberculosis truncated hemoglobin O with ligands reveal a novel ligand-inclusive hydrogen bond network. Biochemistry 42:5764–5774. https://doi.org/10.1021/bi0270337
doi: 10.1021/bi0270337 pubmed: 12741834
Bianchetti CM, Bingman CA, Phillips GN Jr (2011) Structure of the C-terminal heme-binding domain of THAP domain containing protein 4 from Homo sapiens. Proteins 79:1337–1341. https://doi.org/10.1002/prot.22944
doi: 10.1002/prot.22944 pubmed: 21387410 pmcid: 3179982
Pesce A, Bolognesi M, Nardini M (2013) The diversity of 2/2 (truncated) globins. Adv Microb Physiol 63:49–78. https://doi.org/10.1016/B978-0-12-407693-8.00002-9
doi: 10.1016/B978-0-12-407693-8.00002-9 pubmed: 24054794
Bustamante JP, Radusky L, Boechi L, Estrin DA, ten Have A, Marti MA (2016) Evolutionary and functional relationships in the truncated hemoglobin family. PLoS Comput Biol 12:e1004701. https://doi.org/10.1371/journal.pcbi.1004701
doi: 10.1371/journal.pcbi.1004701 pubmed: 26788940 pmcid: 4720485
Weiland T, Kundu S, Trent J, Hoy J, Hargrove M (2004) Bis-histidyl hexacoordination in hemoglobins facilitates heme reduction kinetics. J Am Chem Soc 126:11930–11935. https://doi.org/10.1021/ja046990w
doi: 10.1021/ja046990w pubmed: 15382928
Milani M, Pesce A, Ouellet Y, Ascenzi P, Guertin M, Bolognesi M (2001) Mycobacterium tuberculosis hemoglobin N displays a protein tunnel suited for O
doi: 10.1093/emboj/20.15.3902 pubmed: 11483493 pmcid: 149180
Milani M, Savard PY, Ouellet H, Ascenzi P, Guertin M, Bolognesi M (2003) A TyrCD1/TrpG8 hydrogen bond network and a TyrB10TyrCD1 covalent link shape the heme distal site of Mycobacterium tuberculosis hemoglobin O. Proc Natl Acad Sci USA 100:5766–5771. https://doi.org/10.1073/pnas.1037676100
doi: 10.1073/pnas.1037676100 pubmed: 12719529 pmcid: 156275
Nardini M, Pesce A, Labarre M, Richard C, Bolli A, Ascenzi P, Guertin M, Bolognesi M (2006) Structural determinants in the group III truncated hemoglobin from Campylobacter jejuni. J Biol Chem 281:37803–37812. https://doi.org/10.1074/jbc.M607254200
doi: 10.1074/jbc.M607254200 pubmed: 17023416
Couture M, Yeh S, Wittenberg BA, Wittenberg JB, Ouellet Y, Rousseau DL, Guertin M (1999) A cooperative oxygen-binding hemoglobin from Mycobacterium tuberculosis. Proc Natl Acad Sci USA 96:11223–11228. https://doi.org/10.1073/pnas.96.20.11223
doi: 10.1073/pnas.96.20.11223 pubmed: 10500158 pmcid: 18015
Ascenzi P, Coletta A, Cao Y, Trezza V, Leboffe L, Fanali G, Fasano M, Pesce A, Ciaccio C, Marini S, Coletta M (2013) Isoniazid inhibits the heme-based reactivity of Mycobacterium tuberculosis truncated hemoglobin N. PLoS ONE 8:e69762. https://doi.org/10.1371/journal.pone.0069762
doi: 10.1371/journal.pone.0069762 pubmed: 23936350 pmcid: 3731299
Mukai M, Savard PY, Ouellet H, Guertin M, Yeh SR (2002) Unique ligand-protein interactions in a new truncated hemoglobin from Mycobacterium tuberculosis. Biochemistry 41:3897–3905. https://doi.org/10.1021/bi0156409
doi: 10.1021/bi0156409 pubmed: 11900532
Farrés J, Rechsteiner MP, Herold S, Frey AD, Kallio PT (2005) Ligand binding properties of bacterial hemoglobins and flavohemoglobins. Biochemistry 44:4125–4134. https://doi.org/10.1021/bi047389d
doi: 10.1021/bi047389d pubmed: 15751990
Hargrove MS (2000) A flash photolysis method to characterize hexacoordinate hemoglobin kinetics. Biophys J 79:2733–2738. https://doi.org/10.1016/S0006-3495(00)76512-X
doi: 10.1016/S0006-3495(00)76512-X pubmed: 11053146 pmcid: 1301154
Appleby CA (1969) Properties of leghaemoglobin in vivo, and its isolation as ferrous oxyleghaemoglobin. Biochim Biophys Acta 188:222–229. https://doi.org/10.1016/0005-2795(69)90069-5
doi: 10.1016/0005-2795(69)90069-5 pubmed: 5387819
Gibson QH, Wittenberg JB, Wittenberg BA, Bogusz D, Appleby CA (1989) The kinetics of ligand binding to plant hemoglobins: structural implications. J Biol Chem 264:100–107 (PMID: 2909508)
doi: 10.1016/S0021-9258(17)31228-0
Ioanitescu AI, Dewilde S, Kiger L, Marden MC, Moens L, Van Doorslaer S (2005) Characterization of nonsymbiotic tomato hemoglobin. Biophys J 89:2628–2639. https://doi.org/10.1529/biophysj.105.060582
doi: 10.1529/biophysj.105.060582 pubmed: 16040738 pmcid: 1366763
Hvitved AN, Trent JT 3rd, Premer SA, Hargrove MS (2001) Ligand binding and hexacoordination in Synechocystis hemoglobin. J Biol Chem 276:34714–34721. https://doi.org/10.1074/jbc.M105175200
doi: 10.1074/jbc.M105175200 pubmed: 11438545
Hoy JA, Smagghe BJ, Halder P, Hargrove MS (2007) Covalent heme attachment in Synechocystis hemoglobin is required to prevent ferrous heme dissociation. Protein Sci 16:250–260. https://doi.org/10.1110/ps.062572607
doi: 10.1110/ps.062572607 pubmed: 17242429 pmcid: 2203299

Auteurs

Giovanna De Simone (G)

Department of Sciences, Roma Tre University, 00146, Rome, Italy.

Grazia R Tundo (GR)

Department of Clinical Sciences and Translational Medicine, University of Roma "Tor Vergata", 00133, Rome, Italy.
IRCCS Fondazione Bietti, Rome, Italy.

Andrea Coletta (A)

WasteHero, Aarhus, Denmark.

Massimo Coletta (M)

IRCCS Fondazione Bietti, Rome, Italy. massimiliano.coletta@fondazionebietti.it.

Paolo Ascenzi (P)

Interdepartmental Laboratory for Electron Microscopy, Roma Tre University, Via della Vasca Navale 79, 00146, Rome, Italy. ascenzi@uniroma3.it.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH