{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T03:03:50Z","timestamp":1740107030324,"version":"3.37.3"},"reference-count":41,"publisher":"Springer Science and Business Media LLC","issue":"4-5","license":[{"start":{"date-parts":[[2022,7,8]],"date-time":"2022-07-08T00:00:00Z","timestamp":1657238400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,7,8]],"date-time":"2022-07-08T00:00:00Z","timestamp":1657238400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["J Biol Inorg Chem"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>An EPR spectrometer has been developed that can be tuned to many frequencies in the range of ca 0.1\u201315\u00a0GHz. Applicability has been tested on ferrimyoglobin fluoride (MbF) and ferrimyoglobin cyanide (MbCN). MbF has a high-spin (<jats:italic>S<\/jats:italic>\u2009=\u20095\/2) spectrum with <jats:sup>19<\/jats:sup>F superhyperfine splitting that is only resolved in X-band along the heme normal. Low-frequency EPR also resolves the splitting in the heme plane. Measurement of linewidth as a function of frequency provides the basis for an analysis of inhomogeneous broadening in terms of <jats:italic>g<\/jats:italic>-strain, zero-field distribution, unresolved superhyperfine splittings and dipolar interaction. Rhombicity in the <jats:italic>g<\/jats:italic> tensor is found to be absent. MbCN (<jats:italic>S<\/jats:italic>\u2009=\u20091\/2) has a highly anisotropic low spin (HALS) spectrum for which <jats:italic>g<\/jats:italic><jats:sub><jats:italic>x<\/jats:italic><\/jats:sub> cannot be determined unequivocally in X-band. Low-frequency EPR allows for measurement of the complete spectrum and determination of the <jats:italic>g<\/jats:italic>-tensor.<\/jats:p>\n                <jats:p><jats:bold>Graphical abstract<\/jats:bold><\/jats:p>","DOI":"10.1007\/s00775-022-01948-1","type":"journal-article","created":{"date-parts":[[2022,7,8]],"date-time":"2022-07-08T08:13:19Z","timestamp":1657267999000},"page":"497-507","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Low-frequency EPR of ferrimyoglobin fluoride and ferrimyoglobin cyanide: a case study on the applicability of broadband analysis to high-spin hemoproteins and to HALS hemoproteins"],"prefix":"10.1007","volume":"27","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-1609-6671","authenticated-orcid":false,"given":"Wilfred R.","family":"Hagen","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,7,8]]},"reference":[{"volume-title":"Advanced EPR; applications in biology and biochemistry","year":"1989","key":"1948_CR1","unstructured":"Hoff AJ (ed) (1989) Advanced EPR; applications in biology and biochemistry. Elsevier, Amsterdam"},{"volume-title":"EPR spectroscopy; fundamentals and methods","year":"2018","key":"1948_CR2","unstructured":"Goldfarb D, Stoll S (eds) (2018) EPR spectroscopy; fundamentals and methods. Wiley, Chichester"},{"key":"1948_CR3","doi-asserted-by":"publisher","first-page":"2308","DOI":"10.1016\/j.ccr.2006.03.016","volume":"250","author":"J Krzystek","year":"2006","unstructured":"Krzystek J, Ozarowski A, Telser J (2006) Multi-frequency, high-field EPR as a powerful tool to accurately determine zero-field splitting in high-spin transition metal coordination complexes. Coord Chem Rev 250:2308\u20132324","journal-title":"Coord Chem Rev"},{"key":"1948_CR4","doi-asserted-by":"publisher","first-page":"2534","DOI":"10.1039\/C6CS00565A","volume":"47","author":"MM Roessler","year":"2018","unstructured":"Roessler MM, Salvadori E (2018) Principles and applications of EPR spectroscopy in the chemical sciences. Chem Soc Rev 47:2534\u20132553","journal-title":"Chem Soc Rev"},{"key":"1948_CR5","doi-asserted-by":"publisher","first-page":"7482","DOI":"10.1016\/S0021-9258(18)35967-2","volume":"254","author":"W Froncisz","year":"1979","unstructured":"Froncisz W, Scholes CP, Hyde JS, Wei Y-H, King TE, Shaw RW, Beinert H (1979) Hyperfine structure resolved by 2 to 4 GHz EPR of cytochrome c oxidase. J Biol Chem 254:7482\u20137484","journal-title":"J Biol Chem"},{"key":"1948_CR6","first-page":"391","volume":"11","author":"JS Hyde","year":"1982","unstructured":"Hyde JS, Froncisz W (1982) The role of microwave frequency in EPR spectroscopy of copper complexes. Coord Chem Rev 11:391\u2013417","journal-title":"Coord Chem Rev"},{"key":"1948_CR7","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1016\/S0006-3495(93)81363-8","volume":"64","author":"WE Antoline","year":"1993","unstructured":"Antoline WE, Hanna PM, McMillan DR (1993) Low frequency EPR of Pseudomonas aeruginosa azurin; analysis of ligand superhyperfine structure from a type 1 copper site. Biophys J 64:267\u2013272","journal-title":"Biophys J"},{"key":"1948_CR8","doi-asserted-by":"publisher","first-page":"1814","DOI":"10.1021\/ja106550u","volume":"133","author":"JM Kowalski","year":"2011","unstructured":"Kowalski JM, Bennett B (2011) Spin Hamiltonian parameters for Cu(II)-prion peptide complexes from L-band electron paramagnetic resonance spectroscopy. J Am Chem Soc 133:1814\u20131823","journal-title":"J Am Chem Soc"},{"key":"1948_CR9","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0059874","volume":"8","author":"WR Hagen","year":"2013","unstructured":"Hagen WR (2013) Broadband transmission EPR spectroscopy. PLoS ONE 8:e59874","journal-title":"PLoS ONE"},{"key":"1948_CR10","doi-asserted-by":"publisher","first-page":"6986","DOI":"10.1021\/acs.jpca.9b03574","volume":"123","author":"WR Hagen","year":"2019","unstructured":"Hagen WR (2019) Broadband tunable electron paramagnetic resonance spectroscopy of dilute metal complexes. J Phys Chem A 123:6986\u20136995","journal-title":"J Phys Chem A"},{"key":"1948_CR11","doi-asserted-by":"publisher","first-page":"3208","DOI":"10.1021\/acs.jpca.1c01217","volume":"125","author":"WR Hagen","year":"2021","unstructured":"Hagen WR (2021) Very low-frequency broadband electron paramagnetic resonance spectroscopy of metalloproteins. J Phys Chem A 125:3208\u20133218","journal-title":"J Phys Chem A"},{"key":"1948_CR12","doi-asserted-by":"publisher","first-page":"2975","DOI":"10.1039\/a803058h","volume":"94","author":"PJM van Kan","year":"1998","unstructured":"van Kan PJM, van der Horst E, Reijerse EJ, van Bentum PJM, Hagen WR (1998) Multi-frequency EPR spectroscopy of myoglobin. Spectral effects for high-spin iron (III) ion at high magnetic fields. J Chem Soc, Faraday Trans 94:2975\u20132978","journal-title":"J Chem Soc, Faraday Trans"},{"key":"1948_CR13","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1007\/s00775-002-0429-0","volume":"8","author":"KK Andersson","year":"2003","unstructured":"Andersson KK, Smidt PP, Katterle B, Strand KR, Palmer AE, Lee S-K, Solomon EI, Gr\u00e4slund A, Barra A-L (2003) Examples of high-frequency EPR studies in bioinorganic chemistry. J Biol Inorg Chem 8:235\u2013247","journal-title":"J Biol Inorg Chem"},{"key":"1948_CR14","doi-asserted-by":"publisher","first-page":"2696","DOI":"10.1080\/00268976.2013.809806","volume":"111","author":"J Nehrkorn","year":"2013","unstructured":"Nehrkorn J, Martins BM, Holldack K, Stoll S, Dobbek H, Bittl R, Schnegg A (2013) Zero-field splittings in met Hb and met Mb with aquo and fluoro ligands: a FD-FT THz-EPR study. Mol Phys 111:2696\u20132707","journal-title":"Mol Phys"},{"key":"1948_CR15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/BFb0118872","volume":"2","author":"M Weissbluth","year":"1967","unstructured":"Weissbluth M (1967) The physics of haemoglobin. Struct Bond 2:1\u2013125","journal-title":"Struct Bond"},{"key":"1948_CR16","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1016\/S0898-8838(08)60064-1","volume":"38","author":"WR Hagen","year":"1992","unstructured":"Hagen WR (1992) EPR spectroscopy of iron-sulfur proteins. Adv Inorg Chem 38:165\u2013222","journal-title":"Adv Inorg Chem"},{"key":"1948_CR17","doi-asserted-by":"publisher","first-page":"4415","DOI":"10.1039\/b608163k","volume":"2006","author":"WR Hagen","year":"2006","unstructured":"Hagen WR (2006) EPR spectroscopy as a probe of metal centers in biological systems. Dalton Trans 2006:4415\u20134434","journal-title":"Dalton Trans"},{"key":"1948_CR18","volume-title":"Biomolecular EPR spectroscopy","author":"WR Hagen","year":"2009","unstructured":"Hagen WR (2009) Biomolecular EPR spectroscopy. CRC Press, Taylor & Francis Group, Boca Raton"},{"key":"1948_CR19","doi-asserted-by":"publisher","first-page":"4324","DOI":"10.1103\/PhysRevB.5.4324","volume":"5","author":"Th Von Waldkirch","year":"1972","unstructured":"Von Waldkirch Th, M\u00fcller KA, Berlinger W (1972) Analysis of the Fe3+-V0 center in the tetragonal phase of SrTiO3. Phys Rev B 5:4324\u20134334","journal-title":"Phys Rev B"},{"key":"1948_CR20","unstructured":"Kotani M, Morimoto H (1967) In: Ehrenberg A, Malmstr\u00f6m BG, V\u00e4nng\u00e5rd T (eds) Magnetic resonance in biological systems. Pergamon Press, Oxford"},{"key":"1948_CR21","doi-asserted-by":"publisher","first-page":"450","DOI":"10.1016\/0005-2795(72)90005-0","volume":"278","author":"EF Slade","year":"1972","unstructured":"Slade EF, Farrow RH (1972) Millimeter wave EPR studies of some high spin myoglobin derivatives. Biochim Biophys Acta 278:450\u2013458","journal-title":"Biochim Biophys Acta"},{"key":"1948_CR22","doi-asserted-by":"publisher","first-page":"6109","DOI":"10.1021\/ja00127a025","volume":"117","author":"Y-C Fann","year":"1995","unstructured":"Fann Y-C, Ong J-L, Nocek JM, Hoffman BM (1995) 19F and 1,2H ENDOR study of distal-pocket N(\u03b5)-H\u22c5\u22c5\u22c5F hydrogen bonding in fluorometmyoglobin. J Am Chem Soc 117:6109\u20136116","journal-title":"J Am Chem Soc"},{"key":"1948_CR23","unstructured":"Peisach J, Blumberg WE (1970) In: \u00c5keson \u00c5, Ehrenberg A (eds) Structure and function of oxidation-reduction enzymes. Pergamon Press, Oxford"},{"key":"1948_CR24","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/0926-6585(66)90050-1","volume":"126","author":"H Morimoto","year":"1966","unstructured":"Morimoto H, Kotani M (1966) Fluorine superhyperfine structure in EPR spectra of the single crystal of the myoglobin fluoride. Biochim Biophys Acta 126:176\u2013178","journal-title":"Biochim Biophys Acta"},{"key":"1948_CR25","doi-asserted-by":"publisher","first-page":"4174","DOI":"10.1016\/S0021-9258(18)62069-1","volume":"245","author":"T Yonetani","year":"1971","unstructured":"Yonetani T, Leigh JS (1971) Electromagnetic properties of hemoproteins: IV Single crystal electron paramagnetic resonance spectroscopy of hemoproteins at ambient temperature. J Biol Chem 245:4174\u20134177","journal-title":"J Biol Chem"},{"key":"1948_CR26","doi-asserted-by":"publisher","first-page":"1769","DOI":"10.5012\/bkcs.2002.23.12.1769","volume":"23","author":"H-I Lee","year":"2002","unstructured":"Lee H-I (2002) 14N Mims pulsed ENDOR of proximal histidine and heme of aquometmyoglobin and fluorometmyoglobin. Bull Korean Chem Soc 23:1769\u20131772","journal-title":"Bull Korean Chem Soc"},{"key":"1948_CR27","doi-asserted-by":"publisher","first-page":"1645","DOI":"10.1021\/ja00501a001","volume":"101","author":"CF Mulks","year":"1979","unstructured":"Mulks CF, Scholes CP, Dickinson LC, Lapidot A (1979) Electron nuclear double resonance from high- and low-spin ferric hemoglobins and myoglobins. J Am Chem Soc 101:1645\u20131654","journal-title":"J Am Chem Soc"},{"key":"1948_CR28","doi-asserted-by":"publisher","first-page":"2724","DOI":"10.1021\/ja00374a007","volume":"104","author":"CP Scholes","year":"1982","unstructured":"Scholes CP, Lapidot A, Mascarenhas R, Inubushi T, Isaacson RA, Feher G (1982) Electron nuclear double resonance (ENDOR) from heme and histidine nitrogens in single crystals of aquometmyoglobin. J Am Chem Soc 104:2724\u20132735","journal-title":"J Am Chem Soc"},{"key":"1948_CR29","first-page":"447","volume":"44","author":"WR Hagen","year":"1981","unstructured":"Hagen WR (1981) Dislocation strain broadening as a source of anisotropic linewidth and asymmetric lineshape in the electron paramagnetic resonance spectrum of metalloproteins and related systems. J Magn Reson 44:447\u2013469","journal-title":"J Magn Reson"},{"key":"1948_CR30","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1038\/180030a0","volume":"180","author":"JS Griffith","year":"1957","unstructured":"Griffith JS (1957) Theory of electron resonance in ferrihaemoglobin azide. Nature 180:30\u201331","journal-title":"Nature"},{"key":"1948_CR31","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1080\/00268977100101251","volume":"21","author":"JS Griffith","year":"1971","unstructured":"Griffith JS (1971) Theory of E.P.R. in low-spin ferric haemoproteins. Mol Phys 21:135\u2013139","journal-title":"Mol Phys"},{"key":"1948_CR32","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/0005-2795(77)90049-6","volume":"491","author":"CPS Taylor","year":"1977","unstructured":"Taylor CPS (1977) The EPR of low spin heme complexes. Relation of the t2g hole model to the directional properties of the g tensor, and a new method for calculating the ligand field parameters. Biochim Biophys Acta 491:137\u2013149","journal-title":"Biochim Biophys Acta"},{"key":"1948_CR33","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1016\/0003-9861(84)90495-8","volume":"233","author":"BB Muhoberac","year":"1984","unstructured":"Muhoberac BB (1984) Correlations among parameters that describe low-spin ferric heme complexes. Arch Biochem Biophys 233:682\u2013697","journal-title":"Arch Biochem Biophys"},{"key":"1948_CR34","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1016\/S0010-8545(99)00029-6","volume":"185\u2013186","author":"FA Walker","year":"1999","unstructured":"Walker FA (1999) Magnetic spectroscopy (EPR, ESEEM, M\u00f6ssbauer, MCD and NMR) studies of low-spin ferriheme centers and their corresponding proteins. Coord Chem Rev 185\u2013186:471\u2013534","journal-title":"Coord Chem Rev"},{"key":"1948_CR35","doi-asserted-by":"publisher","first-page":"1064","DOI":"10.1002\/bip.21267","volume":"91","author":"G Zoppellaro","year":"2009","unstructured":"Zoppellaro G, Bren KL, Ensign AA, Harbitz E, Kaur R, Hersleth H-P, Ryde U, Hederstedt L, Andersson KK (2009) Studies of ferric heme proteins with highly anisotropic\/highly axial low spin (S = 1\/2) electron paramagnetic resonance signals with bis-histidineand histidine-methionine axial iron coordination. Biopolymers 91:1064\u20131082","journal-title":"Biopolymers"},{"key":"1948_CR36","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/j.jinorgbio.2018.02.021","volume":"183","author":"MM Lockart","year":"2018","unstructured":"Lockart MM, Rodriguez CA, Atkins WM, Bowman MK (2018) CW EPR parameters reveal cytochrome P450 ligand binding modes. J Inorg Biochem 183:157\u2013164","journal-title":"J Inorg Biochem"},{"key":"1948_CR37","doi-asserted-by":"publisher","first-page":"1258","DOI":"10.1002\/cphc.200500693","volume":"7","author":"G Zoppellaro","year":"2006","unstructured":"Zoppellaro G, Teschner T, Harbitz E, Sch\u00fcnemann V, Karlsen S, Arciero DM, Ciurli S, Trautwein AX, Hooper AB, Andersson KK (2006) Low-temperature EPR and M\u00f6ssbauer spectroscopy of twh cytochromes with His-Met axial coordination exhibiting HALS signals. ChemPhysChem 7:1258\u20131267","journal-title":"ChemPhysChem"},{"key":"1948_CR38","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0022014","volume":"6","author":"E Harbitz","year":"2011","unstructured":"Harbitz E, Andersson KK (2011) Cytochrome c-554 from Methylosinus trichosporium OB3b; a protein that belongs to the cytochrome c2 family and exhibits a HALS-type EPR signal. PLoS ONE 6:e22014","journal-title":"PLoS ONE"},{"key":"1948_CR39","doi-asserted-by":"publisher","first-page":"334","DOI":"10.1016\/0005-2728(79)90050-1","volume":"546","author":"S de Vries","year":"1979","unstructured":"de Vries S, Albracht SPJ (1979) Intensity of highly anisotropic low-spin heme EPR signals. Biochim Biophys Acta 546:334\u2013340","journal-title":"Biochim Biophys Acta"},{"key":"1948_CR40","doi-asserted-by":"publisher","first-page":"1660","DOI":"10.1021\/ja00267a041","volume":"108","author":"CP Scholes","year":"1986","unstructured":"Scholes CP, Falkowski KM, Chen S, Bank J (1986) Electron nuclear double resonance (ENDOR) of bis(imidazole)-ligated low-spin ferric heme systems. J Am Chem Soc 108:1660\u20131671","journal-title":"J Am Chem Soc"},{"key":"1948_CR41","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.jmr.2013.03.004","volume":"231","author":"AV Astashkin","year":"2013","unstructured":"Astashkin AV, Walker FA (2013) Determination of the principal g-values of type I or highly anisotropic low spin (HALS) ferriheme centers in frozen solutions. J Magn Reson 231:15\u201321","journal-title":"J Magn Reson"}],"container-title":["JBIC Journal of Biological Inorganic Chemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00775-022-01948-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00775-022-01948-1\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00775-022-01948-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,23]],"date-time":"2022-08-23T08:17:31Z","timestamp":1661242651000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00775-022-01948-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,8]]},"references-count":41,"journal-issue":{"issue":"4-5","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["1948"],"URL":"https:\/\/doi.org\/10.1007\/s00775-022-01948-1","relation":{},"ISSN":["1432-1327"],"issn-type":[{"type":"electronic","value":"1432-1327"}],"subject":[],"published":{"date-parts":[[2022,7,8]]},"assertion":[{"value":"12 April 2022","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"4 June 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 July 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The author declares no conflict of interest.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of interest"}}]}}