Advertisement

Paramagnetomics

  • Przemysław M. PłonkaEmail author
Chapter

Abstract

EPR spectroscopy and imaging remain still a branch of physical sciences, while its application to biology and medicine is wide and valuable. The EPR-measureable species create in biological systems important and well-defined pool, unique on the background of metabolomes and metallomes. At the same time, they seem to be these constituents of the system, which make it deserving to be called “alive”. I propose to coin the phrase “the paramagnetome” to name this pool and to replace the common, descriptive name of “biologically and medically-oriented EPR/ESR spectroscopy” with “paramagnetomics”, per analogiam to other “-omes” and “-omics”. A short characteristic of these two newly defined terms is proposed, which makes the paramagnetomics closely related to other branches of the systems biology. Relations to the problems of genomics and the central problems of molecular genetics, genetic information, as well as biological evolution are also discussed. The position of EPR spectroscopy and a special role that it plays in defining and understanding the phenomenon of life seem to accomplish the long expected establishing the paramagnetomics and research on paramagnetomes as a branch of biology.

Keywords

Biophysics Definition of life EPR ESR Evolution Free radicals Functional genomics Genetic information Metabolome Metallome Paramagnetic centres Paramagnetome 

Notes

Acknowledgements

I would like to recall the memory of two excellent scientists from Kraków, who actually created the topic and the subject of this chapter: Professor Stanisław J. Łukiewicz (1927–2005) and Professor Aleksander Koj (1935–2016). Professor Łukiewicz established “The Kraków School of Biophysics”, but I particularly appreciate his monographic course entitled “The electron phenomena in living systems and the ways of their investigations” which I attended in 1985/1986 and which actually in detail outlined and designed paramagnetomics. Professor Koj, a famous Polish biochemist, and a Rector of the Jagiellonian University in Kraków, was a supporter of systemic approach in modern biology, fascinated by functional genomics—with the term itself and the genomic approach to biochemistry. He had always encouraged me to head crosswise the standard pathways of thinking in biology and to look for new qualities in the process of “making the science”. I would like to express my particular gratitude to all the students of mine (some of whom being now professors) who have always inspired me to do so and who invited me to their conference in 2017 [172]. In particular, I must acknowledge Dr. Sebastian Pintscher, who in 2010 carried out under my supervision the EPR measurements exhibited in Fig. 9.3 and let me publish the spectra under my name.

The Faculty of Biochemistry, Biophysics and Biotechnology of Jagiellonian University is a partner of the Leading National Research Centre (KNOW) supported by the Polish Ministry of Science and Higher Education. The paper was partially supported from this fund (PMP, grant KNOW 35p/10/2015).

Conflict of Interest I have no conflict of interest to disclose.

References

  1. 1.
    Kon H. Recommendations for EPR/ESR nomenclature and conventions for presenting experimental data in publications. Pure Appl Chem. 1989;61:2195–200.CrossRefGoogle Scholar
  2. 2.
    Prosser V. Postavení a úloha biofyziky v ostatních přírodních védách. [The position and role of biophysics in other natural sciences.]. In: Prosser V, collective, editors. Eksperimentální metody biofyziky [Experimental methods of biophysics]. Praha: Academia; 1989. p. 21–31. [In Czech].Google Scholar
  3. 3.
    Weiner J. Życie i ewolucja biosfery. Podręcznik ekologii ogólnej [Life and evolution of biosphere. A handbook on general ecology]. Warszawa: PWN; 1999. p. 53. [in Polish]Google Scholar
  4. 4.
    Bernal JD. The origin of life. Cleveland, Ohio: The World Publishing Company; 1967. Preface, p. xvGoogle Scholar
  5. 5.
    Mendel J/G, Wilczyński J, Tschermak E. Prace naukowe Jana/Grzegorza Mendla [The scientific works of John/Gregor Mendel], Spółdzielnia Wydawnicza Książka, Warszawa 1948. [in Polish, Translation of the 6 Edition and Forward by J. Wilczyński, Commentaries by E. Tschermak].Google Scholar
  6. 6.
    Beadle GW, Tatum EL. Genetic control of biochemical reactions in Neurospora. Proc Natl Acad Sci U S A. 1941;27:499–506.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Higgs PG, Attwood TK. Bioinformatyka i ewolucja molekularna [Bioinformatics and molecular evolution], Polish Scientific Editors PWN, Warszawa 2012. [in Polish, transl. by Murzyn K, Liguziński P and Kurdziel M, Murzyn K transl. editor, of 1 ed. Blackwell Sci Ltd, a Blackwell Publishing Company, 2005].Google Scholar
  8. 8.
    Flanagan SP. ‘Nude’, a new hairless gene with pleiotropic effects in the mouse. Genet Res Camb. 1966;8:295–309.PubMedCrossRefGoogle Scholar
  9. 9.
    Mecklenburg L, Nakamura M, Sundberg JP, Paus R. The nude mouse skin phenotype: The role of Foxn1 in hair follicle development and cycling. Exp Mol Pathol. 2001;71:171–8.PubMedCrossRefGoogle Scholar
  10. 10.
    Pantelouris EM. Absence of thymus in a mouse mutant. Nature. 1968;217:370–1.PubMedCrossRefGoogle Scholar
  11. 11.
    Jacob F, Perrin D, Sánchez C, Monod J. “L’opéron: groupe de gènes à expression coordonnée par un opérateur” [Operon: a group of genes with the expression coordinated by an operator]. C R Hebd Seances Acad Sci. 1960;250:1727–9. [in French]Google Scholar
  12. 12.
    Searls DB. The language of genes. Nature. 2002;420:211–7.PubMedCrossRefGoogle Scholar
  13. 13.
    Tarski A. Pojęcie prawdy w językach nauk dedukcyjnych [The notion of truth in languages of deductive/formal sciences]. Warszawa: Towarzystwo Naukowe Warszawskie; 1933. [in Polish]Google Scholar
  14. 14.
    Ji S. The Bhopalator–a molecular model of the living cell based on the concepts of conformons and dissipative structures. J Theor Biol. 1985;116:399–426.PubMedCrossRefGoogle Scholar
  15. 15.
    Kuska B. Beer, Bethesda, and Biology: How “Genomics” Came Into Being. J Natl Cancer Inst. 1998;90:93.Google Scholar
  16. 16.
    Piétu G, Mariage-Samson R, Fayein NA, Matingou C, Eveno E, Houlgatte R, Decraene C, Vandenbrouck Y, Tahi F, Devignes MD, Wirkner U, Ansorge W, Cox D, Nagase T, Nomura N, Auffray C. The Genexpress IMAGE knowledge base of the human brain transcriptome: a prototype integrated resource for functional and computational genomics. Genome Res. 1999;9:195–209.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    James P. Protein identification in the post-genome era: the rapid rise of proteomics. Q Rev Biophys. 1997;30:279–331.PubMedCrossRefGoogle Scholar
  18. 18.
    Winkler HL. Verbreitung und Ursache der Parthenogenesis im Pflanzen- und Tierreiche [Occurrence and cause of parthenogenesis in plants and animals]. Jena: Verlag Fischer; 1920. [in German]Google Scholar
  19. 19.
    Olivier SG. From DNA sequence to biological function. Nature. 1998;379:597–600.CrossRefGoogle Scholar
  20. 20.
    Hicks GG, Shi EG, Li XM, Li CH, Pawlak M, Ruley HE. Functional genomics in mice by tagged sequence mutagenesis. Nat Genet. 1997;16:338–44.PubMedCrossRefGoogle Scholar
  21. 21.
    Velculescu VE, Zhang L, Zhou W, Vogelstein J, Basrai MA, Bassett DE Jr, Hieter P, Vogelstein B, Kinzler KW. Characterization of the yeast transcriptome. Cell. 1997;88:243–51.PubMedCrossRefGoogle Scholar
  22. 22.
    Wasinger VC, Cordwell SJ, Cerpa-Poljak A, Yan JX, Gooley AA, Wilkins MR, Duncan MW, Harris R, Williams KL. Humphery-Smith I. Progress with gene-product mapping of Mycoplasma genitalium. Electrophoresis. 1995;16:1090–4.PubMedCrossRefGoogle Scholar
  23. 23.
    Olsen GJ, Lane DJ, Giovannoni SJ, Pace NR, Stahl DA. Microbial ecology and evolution: A ribosomal RNA approach. Annu Rev Microbiol. 1986;40:337–65.PubMedCrossRefGoogle Scholar
  24. 24.
    Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol. 1998;5:R245–9.PubMedCrossRefGoogle Scholar
  25. 25.
    Chen K, Pachter L. Bioinformatics for whole-genome shotgun sequencing of microbial communities. PLoS Comput Biol. 2005;1:106–12.PubMedCrossRefGoogle Scholar
  26. 26.
    Han X, Gross RW. Global analyses of cellular lipidomes directly from crude extracts of biological samples by ESI mass spectrometry: a bridge to lipidomics. J Lipid Res. 2003;44:1071–9.PubMedCrossRefGoogle Scholar
  27. 27.
    Hirabayashi J, Kasai K. Glycomics, coming of age! Trends Glycosci Glycotechnol. 2000;12:1–5.CrossRefGoogle Scholar
  28. 28.
    Feizi T. Progress in deciphering the information content of the ‘glycome’–a crescendo in the closing years of the millennium. Glycoconj J. 2000;17:553–65.Google Scholar
  29. 29.
    Williams RJP. Chemical selection of elements by cells. Coord Chem Rev. 2001;216–217:583–95.CrossRefGoogle Scholar
  30. 30.
    Szpunar J. Advances in analytical methodology for bioinorganic speciation analysis: metallomics, metalloproteomics and heteroatom-tagged proteomics and metabolomics. Analyst. 2005;130:442–65.PubMedCrossRefGoogle Scholar
  31. 31.
    Fiehn O, Kopka J, Dörmann P, Altmann T, Trethewey RN, Willmitzer L. Metabolite profiling for plant functional genomics. Nat Biotechnol. 2000;18:1157–61.CrossRefGoogle Scholar
  32. 32.
    Oliver SG, Winson MK, Kell DB, Baganz F. Systematic functional analysis of the yeast genome. Trends Biotechnol. 1998;16:373–8.PubMedCrossRefGoogle Scholar
  33. 33.
    Cesareni G, Ceol A, Gavrila C, Palazzi LM, Persico M, Schneider MV. Comparative interactomics. FEBS Lett. 2005;579:1828–33.PubMedCrossRefGoogle Scholar
  34. 34.
    Sanchez C, Lachaize C, Janody F, Bellon B, Röder L, Euzenat J, Rechenmann F, Jacq B. Grasping at molecular interactions and genetic networks in Drosophila melanogaster using FlyNets, an Internet database. Nucleic Acids Res. 1999;27:89–94.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Devlin DKJ. Goodbye, Descartes: the end of logic and the search for a new cosmology of the mind. Chichester: John Wiley & Sons, Inc; 1997.Google Scholar
  36. 36.
    Williams RJP. Signalling: basics and evolution. Acta Biochim Pol. 2004;51:281–98.PubMedGoogle Scholar
  37. 37.
    Jura J, Węgrzyn P, Jura J, Koj A. Regulatory mechanisms of gene expression: complexity with elements of deterministic chaos. Acta Biochim Pol. 2006;53:1–9.PubMedGoogle Scholar
  38. 38.
    Shannon CE. A mathematical theory of communication. Bell Syst Tech J. 1948;27:379–423.CrossRefGoogle Scholar
  39. 39.
    Mazur M. Jakościowa teoria informacji [Qualitative Information Theory]. Warszawa: Wydawnictwa Naukowo Techniczne; 1970. [in Polish]Google Scholar
  40. 40.
    Chmielecki A. Między mózgiem i świadomością: próba rozwiązania problemu psychofizycznego [Between the brain and the consciousness: an attempt to solve the psychophysical problem]. Warszawa: Wydawnictwo Instytutu Filozofii i Socjologii PAN; 2001. [in Polish]Google Scholar
  41. 41.
    Yadav SP. The Wholeness in Suffix -omics, -omes, and the Word Om. J Biomol Tech. 2007;18:277.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Commoner B. In defense of biology. The integrity of biology must be maintained if physics and chemistry are to be properly applied to the problems of life. Science. 1961;133:1745–8.PubMedCrossRefGoogle Scholar
  43. 43.
    Asimov I, Najarian HH, Commoner B. Modern Biology. Science. 1961;134:1020–4.PubMedCrossRefGoogle Scholar
  44. 44.
    Salikhov KM. Voevodsky Award 2001 to Prof L. A. Blumenfeld. EPR Newsletter. 2001;12(1):3.Google Scholar
  45. 45.
    Commoner B, Townsend J, Pake GW. Free radicals in biological materials. Nature. 1954;174:689–91.PubMedCrossRefGoogle Scholar
  46. 46.
    Blumenfeld LA. Problemy Fizyki Biologicznej [Problems of biological physics]. Warszawa: PWN;1978. [in Polish, transl. by Berens K and Wartoń A from Russian “Проблемы биологической физики”. Издательство “Наука”; Москва 1974. Available also in English: Blumenfeld LA, author, Haken H editor. Problems of biological physics. Springer-Verlag; Berlin-Heidelberg-New York 1981].Google Scholar
  47. 47.
    Pauli W, Über den Zusammenhang d. Abschlusses der Elektronenbahnen im Atom mit der Komplexstruktur der Spektren [On the connection between the completions of the electron orbitals in atoms with complex structure of their spectra]. Z Phys. 1925;31:765–85. [in German]CrossRefGoogle Scholar
  48. 48.
    Uhlenbeck GE, Goudsmit S. Spinning electrons and the structure of spectra. Nature. 1926;117:264–5.CrossRefGoogle Scholar
  49. 49.
    Michaelis L. Oxidation-reduction systems of biological significance. VI. The mechanism of the catalytic effect of iron on the oxidation of cysteine. J Biol Chem. 1929;84:777–87.Google Scholar
  50. 50.
    Lancaster JR Jr, Hibbs JB Jr. EPR demonstration of iron-nitrosyl complex formation by cytotoxic activated macrophages. Proc Natl Acad Sci U S A. 1990;87:1223–7.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Michaelis L. The formation of semiquinones as intermediary reduction products from pyocyanine and some other dyestuffs. J Biol Chem. 1931;92:211–32.Google Scholar
  52. 52.
    Michaelis L. Theory of the reversible two-step oxidation. J Biol Chem. 1932;96:703–15.Google Scholar
  53. 53.
    Michaelis L. Semiquinones, the intermediate steps of reversible organic oxidation-reduction. Chem Rev. 1935;16:243–86.CrossRefGoogle Scholar
  54. 54.
    Huber M. Introduction to magnetic resonance methods in photosynthesis. Photosynth Res. 2009;102:305–10.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Tikhonov AN. Induction events and short-term regulation of electron transport in chloroplasts: an overview. Photosynth Res. 2015;125:65–94.PubMedCrossRefGoogle Scholar
  56. 56.
    Świerczek M, Cieluch E, Sarewicz M, Borek A, Moser CC, Dutton PL, Osyczka A. An electronic bus bar lies in the core of cytochrome bc1. Science. 2010;329:451–3.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Sarewicz M, Dutka M, Pintscher S, Osyczka A. Triplet state of the semiquinone-rieske cluster as an intermediate of electronic bifurcation catalyzed by cytochrome bc1. Biochemistry. 2013;52:6388–95.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Kuleta P, Sarewicz M, Postila P, Róg T, Osyczka A. Identifying involvement of Lys251/Asp252 pair in electron transfer and associated proton transfer at the quinone reduction site of Rhodobacter capsulatus cytochrome bc1. Biochim Biophys Acta. 2016;1857:1661–8.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Pintscher S, Kuleta P, Cieluch E, Sarewicz M, Osyczka A. Tuning of hemes b equilibrium redox potential is not required for cross-membrane electron transfer. J Biol Chem. 2016;291:6872–81.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Sarewicz M, Bujnowicz Ł, Bhaduri S, Singh SK, Cramer WA, Osyczka A. Metastable radical state, nonreactive with oxygen, is inherent to catalysis by respiratory and photosynthetic cytochromes bc1/b6f. Proc Natl Acad Sci U S A. 2017;114:1323–8.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Asimov I, Dawson CR. On the reaction inactivation of tyrosinase during the aerobic oxidation of catechol. J Am Chem Soc. 1950;72:820–8.CrossRefGoogle Scholar
  62. 62.
    Ksenzhek O. Money: virtual energy. Economy through the prism of thermodynamics. Boca Raton, Florida: Universal-Publishers; 2007.Google Scholar
  63. 63.
    Slominski AT, Zmijewski MA, Plonka PM, Szaflarski JP, Paus R. How UV Light Touches the Brain and Endocrine System Through Skin, and Why. Endocrinology. 2018;159:1992–2007.PubMedCrossRefGoogle Scholar
  64. 64.
    Pulatova MK. Localization of paramagnetic centre in gamma irradiated protein. Biophysics (USSR). 1963;8:700–3.Google Scholar
  65. 65.
    Pulatova MK. On the problem of the localization of the paramagnetic center of proteins irradiated with gamma rays. Biofizika. 1963;8:632–4. [Article in Russian]PubMedGoogle Scholar
  66. 66.
    Atkins PW, Symons MCR. The structure of inorganic radicals. An application of electron spin resonance to the study of molecular structure. Amsterdam-London-New York: Elsevier Publishing Company; 1967. [Russian transl. by Germanv ED, Dyatkina ME editor. “Спектры ЭПР н строение неорганичецких радикалов”. Издателство “Мир“; Москва 1970, p. 56–65].Google Scholar
  67. 67.
    Berliner JL, Fujii H. Magnetic resonance imaging of biological specimens by electron paramagnetic resonance of nitroxide spin labels. Science. 1985;227:517–9.CrossRefGoogle Scholar
  68. 68.
    Plonka PM. Electron paramagnetic resonance as a unique tool for skin and hair research. Exp Dermatol. 2009;18:472–84.PubMedCrossRefGoogle Scholar
  69. 69.
    Schaumlöffel D. The position of metallomics within other omics fields. In: Michalke B, editor. Metallomics: analytical techniques and speciation methods. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA; 2016. p. 3–16.Google Scholar
  70. 70.
    Haraguchi H. Metallomics: the history in the last decade and a future outlook. Metallomics. 2017;9(8):1001–13.  https://doi.org/10.1039/C7MT00023E.CrossRefPubMedGoogle Scholar
  71. 71.
    Rachmilewitz EA, Peisach J, Blumberg WE. Studies on the stability of oxyhemoglobin A and its constituent chains and derivatives. J Biol Chem. 1971;246:3356–66.PubMedGoogle Scholar
  72. 72.
    Miki T, Kai A, Ikeya M. Electron spin resonance of bloodstains and its application to the estimation of time after bleeding. Forensic Sci Int. 1987;35:149–58.CrossRefGoogle Scholar
  73. 73.
    Svistunenko DA, Davies N, Brealey D, Singer M, Cooper CE. Mitochondrial dysfunction in patients with severe sepsis: An EPR interrogation of individual respiratory chain components. Biochim Biophys Acta. 2006;1757:262–72.PubMedCrossRefGoogle Scholar
  74. 74.
    Elas M, Bielanska J, Pustelny K, Plonka PM, Drelicharz L, Skorka T, Tyrankiewicz U, Wozniak M, Heinze-Paluchowska S, Walski M, Wojnar L, Fortin D, Ventura-Clapier R, Chlopicki S. Detection of mitochondrial dysfunction by EPR technique in mouse model of dilated cardiomyopathy. Free Radic Biol Med. 2008;45:321–8.PubMedCrossRefGoogle Scholar
  75. 75.
    Reed GH. Electron-paramagnetic-resonance studies of Mn(II) complexes with enzymes and substrates. Biochem Soc Trans. 1985;13:567–71.PubMedCrossRefGoogle Scholar
  76. 76.
    Wever R, Oudega B, Van Gelder BF. Generation of superoxide radicals during the autoxidation of mammalian oxyhemoglobin. Biochim Biophys Acta. 1973;302:475–8.CrossRefGoogle Scholar
  77. 77.
    Tsuruga M, Matsuoka A, Hachimori A, Sugawara Y, Shikama K. The molecular mechanism of autoxidation for human oxyhemoglobin. Tilting of the distal histidine causes nonequivalent oxidation in the β chain. J Biol Chem. 1998;273:8607–15.PubMedCrossRefGoogle Scholar
  78. 78.
    Lendzian F. Structure and interactions of amino acid radicals in class I ribonucleotide reductase studied by ENDOR and high-field EPR spectroscopy. Biochim Biophys Acta. 2005;1707:67–90.PubMedCrossRefGoogle Scholar
  79. 79.
    Kohno M. Applications of electron spin resonance spectrometry for reactive oxygen species and reactive nitrogen species research. J Clin Biochem Nutr. 2010;47:1–11.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Pucciariello C, Pierdomenico P. New insights into reactive oxygen species and nitric oxide signalling under low oxygen in plants. Plant Cell Environ. 2017;40:473–82.PubMedCrossRefGoogle Scholar
  81. 81.
    Palmer RMJ, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987;327:524–6.PubMedCrossRefGoogle Scholar
  82. 82.
    Ortiz de Montellano PR, Wilks A. Heme oxygenase structure and mechanism. Adv Inorg Chem. 2001;51:359–407.CrossRefGoogle Scholar
  83. 83.
    Hlavica P. N-oxidative transformation of free and N-substituted amine functions by cytochrome P450 as means of bioactivation and detoxication. Drug Metab Rev. 2002;34:451–77.PubMedCrossRefGoogle Scholar
  84. 84.
    Wilks A, Heinzl G. Heme oxygenation and the widening paradigm of heme degradation. Arch Biochem Biophys. 2014;544:87–95.PubMedCrossRefGoogle Scholar
  85. 85.
    Land EJ, Ramsden CA, Riley PA. Quinone chemistry and melanogenesis. Methods Enzymol. 2004;378:88–109.PubMedCrossRefGoogle Scholar
  86. 86.
    Pey AL, Martinez A, Charubala R, Maitland DJ, Teigen K, Calvo A, Pfleiderer W, Wood JM, Schallreuter KU. Specific interaction of the diastereomers 7(R)- and 7(S)-tetrahydrobiopterin with phenylalanine hydroxylase: implications for understanding primapterinuria and vitiligo. FASEB J. 2006;20:E1451–64.CrossRefGoogle Scholar
  87. 87.
    Daniel J, Kosman DJ. Multicopper oxidases: a workshop on copper coordination chemistry, electron transfer, and metallophysiology. J Biol Inorg Chem. 2010;15:15–28.CrossRefGoogle Scholar
  88. 88.
    Fenton HJH. Oxidation of tartaric acid in presence of iron. J Chem Soc Trans. 1894;65:899–910.CrossRefGoogle Scholar
  89. 89.
    Wang W, Zafiriou OC, Chan IY, Zepp RG, Blough NV. Production of hydrated electrons from photoionization of dissolved organic matter in natural waters. Environ Sci Technol. 2007;41:1601–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Nikitaki Z, Mavragani IV, Laskaratou DA, Gika V, Moskvin VP, Theofilatos K, Vougas K, Stewart RD, Georgakilas AG. Systemic mechanisms and effects of ionizing radiation: A new ‘old’ paradigm of how the bystanders and distant can become the players. Semin Cancer Biol. 2016;37-38:77–95.Google Scholar
  91. 91.
    Hawkins CL, Davies MJ. Detection and characterisation of radicals in biological materials using EPR methodology. Biochim Biophys Acta. 2014;1840:708–21.PubMedCrossRefGoogle Scholar
  92. 92.
    Davies MJ, Hawkins CL. EPR spin trapping of protein radicals. Free Radic Biol Med. 2004;36:1072–86.PubMedCrossRefGoogle Scholar
  93. 93.
    Chikira M, Ng CH, M P. Interaction of DNA with Simple and Mixed Ligand Copper(II) Complexes of 1,10-Phenanthrolines as Studied by DNA-Fiber EPR Spectroscopy. Int J Mol Sci. 2015;16:22754–80.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Haber F, Weiss J. Über die Katalyse des Hydroperoxydes. (On the catalyse of hydrogen peroxide). Naturwissenschaften. 1932;20:948–50. [in German].CrossRefGoogle Scholar
  95. 95.
    Blough NV, Zafiriou OC. Reaction of superoxide with nitric oxide to form peroxonitrite in alkaline aqueous solution. Inorg Chem. 1985;24:3502–4.CrossRefGoogle Scholar
  96. 96.
    Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A. 1990;87:1620–4.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Curie P. Lippmann M. Propriétés magnétiques des corps à diverses températures (note de P. Curie, prèsentée par M. Lippmann). [Magnetic properties of bodies in various temperatures]. Comptes Rendus Hebdomadaires de Séances de l’Académie des Sciences 116. Paris: Gauthier-Villars et Fils, Imprimeurs-Libraires des C. R., 1893: 136–139. [in French]Google Scholar
  98. 98.
    Langevin M P. La théorie cinétique du magnétisme et les magnétons [The kinetic theory of magnetism and the magnets]. Rapport présenté à la Conférence Solvay, Bruxelles, 30 oct.-3 nov. 1911, In: Langevin P. La physique depuis vingt ans. Paris: Douin, 1923: 171–188. [in French]Google Scholar
  99. 99.
    Gordy W, Ard WB, Shields H. Microwave spectroscopy of biological substances. I. Paramagnetic substances in X-irradiated amino acids and proteins. Proc Natl Acad Sci U S A. 1955;41:983–96.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Landar A, Giles N, Zmijewski J, Watanabe N, Oh J-Y, Darley-Usmar V. Modification of lipids by reactive oxygen and nitrogen species: the oxy-nitroxy-lipidome and its role in redox cell signaling. Future Lipidol. 2006;1(2):203–11.CrossRefGoogle Scholar
  101. 101.
    Buettner GR, Wagner BA, Rodgers VGJ. Quantitative redox biology: An approach to understand the role of reactive species in defining the cellular redox environment. Cell Biochem Biophys. 2013;67:477–83.PubMedCrossRefGoogle Scholar
  102. 102.
    Lohan SB, Müller R, Albrecht S, Mink K, Tscherch K, Ismaeel F, Lademann J, Rohn S, Meinke MC. Free radicals induced by sunlight in different spectral regions—in vivo versus ex vivo study. Exp Dermatol. 2016;25:380–5.PubMedCrossRefGoogle Scholar
  103. 103.
    Lennard-Jones JE. The electronic structure of some diatomic molecules. Trans Faraday Soc. 1929;25:668–86.CrossRefGoogle Scholar
  104. 104.
    Uehara H, Arimitsu S. Gas-phase electron paramagnetic resonance detection of nitric oxide and nitrogen dioxide in polluted air. Anal Chem. 1973;45:1897–9.PubMedCrossRefGoogle Scholar
  105. 105.
    Vanin AF, Mordvintsev PI, Kleshchov AL. Nitrogen oxide appearance in animal tissues in vivo. Studia Biophys. 1984;192:135–43.Google Scholar
  106. 106.
    Castle JG Jr, Beringer R. Microwave magnetic resonance absorption in nitrogen dioxide. Physiol Res. 1950;80:114–5.CrossRefGoogle Scholar
  107. 107.
    Lowe DJ. ENDOR and EPR of metalloproteins. Prog Biophys Mol Biol. 1992;5:1–22.CrossRefGoogle Scholar
  108. 108.
    Antholine W, Mailer C, Reichlin B, Swartz HM. Experimental considerations in biological ESR studies. 1. Identity and origin of the ‘tissue lipid signal’: A copper-dithiocarbamate complex. Phys Med Biol. 1976;21:840–6.PubMedCrossRefGoogle Scholar
  109. 109.
    Kakuda T, Tanaka H, Kimoto E, Morishige F. Electron paramagnetic resonance spectrum of human serum copper. Appl Spectrosc. 1980;34:276–80.CrossRefGoogle Scholar
  110. 110.
    Stegmann HB, Schuler P, Ruff H-J. Investigation of damage to forest by EPR spectroscopy in vivo. Photochem Photobiol. 1989;50:209–11.CrossRefGoogle Scholar
  111. 111.
    Rakoczy L, Płonka PM. Akumulacja manganu w plazmodiach śluzowca (Myxomycetes) Metatrichia vesparum. [Accumulation of manganese in the plasmodia of a true slime mould (Myxomycetes) Metatrichia vesparium]. Ochrona Środowiska i Zasobów Naturalnych, Instytut Ochrony Środowiska. Warszawa. 1999;18:299–308. [In Polish]Google Scholar
  112. 112.
    Ramos S, Moura JJG, Aureliano M. Recent advances into vanadyl, vanadate and decavanadate interactions with actins. Metallomics. 2012;4:16–22.PubMedCrossRefGoogle Scholar
  113. 113.
    Gutierrez P, Sarna T, Swartz HM. Experimental considerations in biological ESR studies. 11. Chromium-tissue complexes detected by electron spin resonance. Phys Med Biol. 1976;21:949–54.PubMedCrossRefGoogle Scholar
  114. 114.
    Liu KJ, Mader K, Shi X, Swartz HM. Reduction of carcinogenic chromium(VI) on the skin of living rats. Magn Reson Med. 1997;38:524–6.PubMedCrossRefGoogle Scholar
  115. 115.
    Blois MS, Zahlan AB, Maling JE. Electron spin resonance studies on melanin. Biophys J. 1964;4:471–90.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Meredith P, Sarna T. The physical and chemical properties of eumelanin. Pigment Cell Res. 2006;19:572–94.PubMedCrossRefGoogle Scholar
  117. 117.
    Fattibene P, Callens F. EPR dosimetry with tooth enamel: A review. Appl Radiat Isot. 2010;68:2033–116.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Hauska G, Schoedl T, Remigy H, Tsiots G. The reaction center of green sulfur bacteria. Biochim Biophys Acta. 2001;1507:260–77.PubMedCrossRefGoogle Scholar
  119. 119.
    Barry BA. Reaction dynamics and proton coupled electron transfer: Studies of tyrosine-based charge transfer in natural and biomimetic systems. Biochim Biophys Acta. 2015;1847:46–54.PubMedCrossRefGoogle Scholar
  120. 120.
    Slominski A, Tobin DJ, Shibahara S, Wortsman J. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev. 2004;84:1155–228.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Glass K, Ito S, Wilby PR, Sota T, Nakamura A, Bowers CR, Vinther J, Dutta S, Summons R, Briggs DEG, Wakamatsu K, Simon JD. Direct chemical evidence for eumelanin pigment from the Jurassic period. Proc Natl Acad Sci U S A. 2012;109:10218–23.PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Brozyna AA, Jozwicki W, Roszkowski K, Filipiak J, Slominski AT. Melanin content in melanoma metastases affects the outcome of radiotherapy. Oncotarget. 2016;7:17844–53.PubMedPubMedCentralGoogle Scholar
  123. 123.
    Wood JM, Jimbow K, Boissy RE, Slominski A, Plonka PM, Slawinski J, Wortsman J, Tosk J. What’s the use of generating melanin? Exp Dermatol. 1999;8:153–64.PubMedCrossRefGoogle Scholar
  124. 124.
    Riley PA. Materia melanica: further dark thoughts. Pigment Cell Res. 1992;5:101–6.PubMedCrossRefGoogle Scholar
  125. 125.
    Slominski A, Wortsman J, Plonka PM, Schallreuter KU, Paus R, Tobin DJ. Hair follicle pigmentation. J Invest Dermatol. 2005;124:13–21.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Singh SK, Kurfurst R, Nizard C, Schnebert S, Perrier E, Tobin DJ. Melanin transfer in human skin cells is mediated by filopodia–a model for homotypic and heterotypic lysosome-related organelle transfer. FASEB J. 2010;24:3756–69.PubMedCrossRefGoogle Scholar
  127. 127.
    Tobin DJ, Slominski A, Botchkarev V, Paus R. The fate of hair follicle melanocytes during the hair growth cycle. J Investig Dermatol Symp Proc. 1999;4:323–32.PubMedCrossRefGoogle Scholar
  128. 128.
    Lembo S, Di Caprio R, Micillo R, Balato A, Monfrecola G, Panzella L, Napolitano A. Light-independent pro-inflammatory and pro-oxidant effects of purified human hair melanins on keratinocyte cell cultures. Exp Dermatol. 2017;26:592–4.PubMedCrossRefGoogle Scholar
  129. 129.
    Płonka PM, Picardo M, Slominski AT. Does melanin matter in the dark? Exp Dermatol. 2017;26:595–7.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Menter JM, Willis I. Electron transfer and photoprotective properties of melanins in solution. Pigment Cell Res. 1997;10:214–7.PubMedCrossRefGoogle Scholar
  131. 131.
    Turick CE, Tisa LS, Caccavo F Jr. Melanin production and use as a soluble electron shuttle for Fe(iii) oxide reduction and as a terminal electron acceptor by Shewanella algae BrY. Appl Environ Microbiol. 2002;68:2436–44.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 132.
    Plonka PM, Grabacka M. Melanin synthesis in microorganisms–biotechnological and medical aspects. Acta Biochim Pol. 2006;53:429–43.PubMedGoogle Scholar
  133. 133.
    Perrette Y, Poulenard J, Protiere M, Fanget B, Lombard C, Miege C, Quiers M, Nafferchoux E, Pepin-Donat B. Determining soil sources by organic matter EPR fingerprints in two modern speleothems. Org Geochem. 2015;88:59–68.CrossRefGoogle Scholar
  134. 134.
    Sarna T, Lukiewicz S. Electron spin resonance on living cells. IV. Pathological changes in amphibian eggs and embryos. Folia Histochem Cytochem. 1972;10:265–78.Google Scholar
  135. 135.
    Plonka PM, Wisniewska M, Chlopicki S, Elas M, Rosen GM. X-band and S-band EPR detection of nitric oxide in murine endotoxaemia using spin trapping by ferro-di(N-(dithiocarboxy)sarcosine). Acta Biochim Pol. 2003;50:799–806.PubMedGoogle Scholar
  136. 136.
    Jakubowska M, Sniegocka M, Podgorska E, Michalczyk-Wetula D, Urbanska K, Susz A, Fiedor L, Pyka J, Plonka PM. Pulmonary metastases of the A549-derived lung adenocarcinoma tumors growing in nude mice. A multiple case study. Acta Biochim Pol. 2013;60:323–30.PubMedGoogle Scholar
  137. 137.
    Gruen R, Eggins S, Aubert M, Spooner N, Pike A, Mueller W. ESR and U-series analyses of faunal material from Cuddie Springs, NSW, Australia: implications for the timing of the extinction of the Australian megafauna. Quat Sci Rev. 2010;29:596–610.CrossRefGoogle Scholar
  138. 138.
    Vahidi N, Clarkson RB, Liu KJ, Norby SW, Wu M, Swartz HM. In-vivo and in-vitro EPR oximetry with fusinite - a new coal-derived, particulate EPR probe. Magn Reson Med. 1994;31:139–46.PubMedCrossRefGoogle Scholar
  139. 139.
    Ligeza A, Tikhonov AN, Subczynski WK. In situ measurements of oxygen production and consumption using paramagnetic fusinite particles injected into a bean leaf. Biochim Biophys Acta. 1997;1319:133–7.CrossRefGoogle Scholar
  140. 140.
    Płonka PM, Elas M. Application of the electron paramagnetic resonance spectroscopy to modern biotechnology. Curr Top Biophys. 2002;26(1):175–89.Google Scholar
  141. 141.
    Hagen WR. Metallomic EPR spectroscopy. Metallomics. 2009;1:384–91.PubMedCrossRefGoogle Scholar
  142. 142.
    Eaton SS, Eaton GR. The world as viewed by and with unpaired electrons. J Magn Reson. 2012;223:151–63.PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Namazi MR. Cytochrome-P450 enzymes and autoimmunity: expansion of the relationship and introduction of free radicals as the link. J Autoimmune Dis. 2009;6:4.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Ignarro LJ. Haem-dependent activation of guanylate cyclase and cyclic GMP formation by endogenous nitric oxide: a unique transduction mechanism for transcellular signaling. Pharmacol Toxicol. 1990;67:1–7.PubMedCrossRefGoogle Scholar
  145. 145.
    Ignarro LJ. Regulation of cytosolic guanylyl cyclase by porphyrins and metalloporphyrins. Adv Pharmacol. 1994;26:35–65.PubMedCrossRefGoogle Scholar
  146. 146.
    Denninger JW, Marletta MA. Guanylate cyclase and the NO/cGMP signaling pathway. Biochim Biophys Acta. 1999;1411:334–50.PubMedCrossRefGoogle Scholar
  147. 147.
    Gunn A, Derbyshire ER, Marletta MA, Britt RD. Conformationally distinct five-coordinate heme-NO complexes of soluble guanylate cyclase elucidated by multifrequency electron paramagnetic resonance (EPR). Biochemistry. 2012;51:8384–90.CrossRefGoogle Scholar
  148. 148.
    Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J. 2001;357:593–615.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    van Gastel M, Bubacco L, Groenen EJ, Vijgenboom E, Canters GW. EPR study of the dinuclear active copper site of tyrosinase from Streptomyces antibioticus. FEBS Lett. 2000;474:228–32.PubMedCrossRefGoogle Scholar
  150. 150.
    Segal HL, Boyer PD. The role of sulfhydryl groups in the activity of D-glyceraldehyde 3-phosphate dehydrogenase. J Biol Chem. 1953;204:265–81.PubMedGoogle Scholar
  151. 151.
    Dalziel K, McFerran NV, Wonacott AJ. Glyceraldehyde-3-phosphate dehydrogenase. Philos Trans R Soc Lond Ser B Biol Sci. 1981;293:105–18.CrossRefGoogle Scholar
  152. 152.
    Wu K, Li W, Yu L, Tong W, Feng Y, Ling S, Zhang L, Zheng X, Yang M, Tian C. Temperature-dependent ESR and computational studies on antiferromagnetic electron transfer in the yeast NADH dehydrogenase Ndi1. Phys Chem Chem Phys. 2017;19:4849–54.PubMedCrossRefGoogle Scholar
  153. 153.
    Migita CT, Salerno JC, Masters BS, Martasek P, McMillan K, Ikeda-Saito M. Substrate binding-induced changes in the EPR spectra of the ferrous nitric oxide complexes of neuronal nitric oxide synthase. Biochemistry. 1997;36:10987–92.PubMedCrossRefGoogle Scholar
  154. 154.
    Smith JM. Evolution and information. In: Koj A, Sztompka P, editors. Images of the World: Science, Humanities, Art. Kraków: The Jagiellonian University; 2001. p. 13–7.Google Scholar
  155. 155.
    Muh F, Zouni A. Light-induced water oxidation in photosystem II. Front Biosci (Landmark Ed). 2011;16:3072–132.CrossRefGoogle Scholar
  156. 156.
    Müh F, Glöckner C, Hellmich J, Zouni A. Light-induced quinone reduction in photosystem II. Biochim Biophys Acta. 2012;1817:44–65.PubMedCrossRefGoogle Scholar
  157. 157.
    Marciniak A, Ciesielski B. EPR dosimetry in nails—A review. Appl Spectrosc Rev. 2016;51:73–92.CrossRefGoogle Scholar
  158. 158.
    Hong H, Sun J, Cai W. Multimodality imaging of nitric oxide and nitric oxide synthases. Free Radic Biol Med. 2009;47:684–98.PubMedCrossRefGoogle Scholar
  159. 159.
    Spasojević I. Free radicals and antioxidants at a glance using EPR Spectroscopy. Crit Rev Clin Lab Sci. 2011;48:114–42.PubMedCrossRefGoogle Scholar
  160. 160.
    Plonka PM, Chlopicki S, Plonka BK, Jawien J, Gryglewski RJ. Endotoxaemia in rats: detection of nitrosyl-haemoglobin in blood and lung by EPR. Curr Top Biophys. 1999;23(1):47–53.Google Scholar
  161. 161.
    Szczygiel D, Pawlus J, Plonka PM, Elas M, Szczygiel M, Plonka BK, Łukiewicz SJ. Nitric oxide in the interaction between primary and secondary tumor of L5178Y lymphoma. Nitric Oxide. 2004;11:279–89.PubMedCrossRefGoogle Scholar
  162. 162.
    Subczynski WK, Widomska J, Feix JB. Physical properties of lipid bilayers from EPR spin labeling and their influence on chemical reactions in a membrane environment. Free Radic Biol Med. 2009;46:707–18.PubMedCrossRefGoogle Scholar
  163. 163.
    Elas M, Magwood JM, Butler B, Li C, Wardak R, DeVries R, Barth ED, Epel B, Rubinstein S, Pelizzari CA, Weichselbaum RR, Halpern HJ. EPR oxygen images predict tumor control by a 50% tumor control radiation dose. Cancer Res. 2013;73:5328–35.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 164.
    Krzykawska-Serda M, Miller RC, Elas M, Epel B, Barth ED, Maggio M, Halpern HJ. Correlation between hypoxia proteins and EPR-detected hypoxia in tumors. Adv Exp Med Biol. 2017;977:319–25.PubMedCrossRefGoogle Scholar
  165. 165.
    Godechal Q, Ghanem GE, Cook MG, Gallez B. Electron paramagnetic resonance spectrometry and imaging in melanomas: comparison between pigmented and nonpigmented human malignant melanomas. Mol Imaging. 2013;12:218–23.CrossRefGoogle Scholar
  166. 166.
    Danhier P, Gallez B. Electron paramagnetic resonance: a powerful tool to support magnetic resonance imaging research. Contrast Media Mol Imaging. 2015;10:266–81.PubMedCrossRefGoogle Scholar
  167. 167.
    Metabolism, Metabolomics, Imaging in Cancer. Cherukuri MK, Kalyanaraman B (Chairs). Session 6th, Wednesday, October 5th, 2016. Xth International Workshop on EPR in Biology and Medicine, Kraków, October 02–06, 2016. www.eprworkshop.info [Access: Aug 29th, 2017].
  168. 168.
    McCall KA, Huang C, Fierke CA. Function and mechanism of zinc metalloenzymes. J Nutr. 2000;130:1437S–46S.PubMedCrossRefGoogle Scholar
  169. 169.
    Pasenkiewicz-Gierula M, Murzyn K, Róg T, Czaplewski C. Molecular dynamics simulation studies of lipid bilayer systems. Acta Biochim Pol. 2000;47:601–11.PubMedGoogle Scholar
  170. 170.
    Symons MC. Electron movement through proteins and DNA. Free Radic Biol Med. 1997;22:1271–6.PubMedCrossRefGoogle Scholar
  171. 171.
    Szent-Györgyi A. Wstęp do biologii submolekularnej. Warszawa: PWN; 1961. [Polish, transl. by Stolarek J from English “Introduction to a submolecular biology”. New York: Academic Press; 1960].Google Scholar
  172. 172.
    VI International Conference of Biophysics Students. Biophysics Students’ Association ‘Nobel’ and Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Cracow, Poland, 19th-21st May 2017. Programme Book. http://www.nobel.wbbib.uj.edu.pl/ [Access: Aug 30th, 2017].
  173. 173.
    Benenson Y, Adar R, Paz-Elizur T, Livneh Z, Shapiro E. DNA molecule provides a computing machine with both data and fuel. Proc Natl Acad Sci U S A. 2003;100:2191–6.PubMedPubMedCentralCrossRefGoogle Scholar
  174. 174.
    Nickoloff JA. Paths from DNA damage and signaling to genome rearrangements via homologous recombination. Mutat Res. 2017;806:64–74.  https://doi.org/10.1016/j.mrfmmm.2017.07.008.CrossRefPubMedGoogle Scholar
  175. 175.
    Küppers B-A. Geneza informacji biologicznej. Filozoficzne problem powstania życia. [The genesis of biological information. On philosophical problems of the origin of life]. Warszawa: PWN; 1991. [in Polish, transl. by Ługowski W from German “Der Ursprung biologischer Information. Zur Naturphilosophie der Lebenentstehung”. B. Piper Verlag GmbH & Co. K.G. Munich 1986. Available also in English: Information and the origin of life. The MIT Press, Cambridge/Mass. 1990].Google Scholar
  176. 176.
    Ohno S. Evolution from primordial oligomeric repeats to modern coding sequences. J Mol Evol. 1987;25:325–9.PubMedCrossRefGoogle Scholar
  177. 177.
    Arodź T, Płonka PM. Effects of point mutations on protein structure are nonexponentially distributed. Proteins. 2012;80:1780–90.PubMedGoogle Scholar
  178. 178.
    Arodź T, Płonka PM. Sequence and structure space model of protein divergence driven by point mutations. J Theor Biol. 2013;330:1–8.PubMedCrossRefGoogle Scholar
  179. 179.
    Eigen M. Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971;58:465–523.PubMedCrossRefGoogle Scholar
  180. 180.
    Muller HJ. Artificial transmutation of the gene. Science. 1927;66:84–7.PubMedCrossRefGoogle Scholar
  181. 181.
    Howard BD, Tessman I. Identification of altered bases in mutated single-stranded DNA III. Mutagenesis by ultraviolet light. J Mol Biol. 1964;9:372–5.PubMedCrossRefGoogle Scholar
  182. 182.
    Tessman I, Poddart RK, Kumar S. Identification of the altered bases in mutated single-stranded DNA I. In vitro mutagenesis by hydroxylamine, ethyl methanesulfonate and nitrous acid. J Mol Biol. 1964;9:352–63.PubMedCrossRefGoogle Scholar
  183. 183.
    Cech TR. RNA chemistry. Ribozyme self-replication? Nature. 1989;339:507–8.PubMedCrossRefGoogle Scholar
  184. 184.
    Niziolek M, Korytowski W, Girotti AW. Chain-breaking antioxidant and cytoprotective action of nitric oxide on photodynamically stressed tumor cells. Photochem Photobiol. 2003;78:262–70.PubMedCrossRefGoogle Scholar
  185. 185.
    El-Agamey A, Lowe GM, McGarvey DJ, Mortensen A, Phillip DM, Truscott TG, Young AJ. Carotenoid radical chemistry and antioxidant/pro-oxidant properties. Arch Biochem Biophys. 2004;430:37–48.PubMedCrossRefGoogle Scholar
  186. 186.
    Schultz T, Samoylova E, Radloff W, Hertel IV, Sobolewski AL, Domcke W. Efficient deactivation of a model base pair via excited-state hydrogen transfer. Science. 2004;306:1765–8.PubMedCrossRefGoogle Scholar
  187. 187.
    Reichard P, Baldesten A, Rutberg L. Formation of deoxycytidine phosphates from cytidine phosphates in extracts from Escherichia coli. J Biol Chem. 1961;236:1150–7.PubMedGoogle Scholar
  188. 188.
    Jordan A, Reichard P. Ribonucleotide reductases. Annu Rev Biochem. 1998;67:71–98.PubMedCrossRefGoogle Scholar
  189. 189.
    Chang MC, Yee CS, Stubbe J, Nocera DG. Turning on ribonucleotide reductase by light-initiated amino acid radical generation. Proc Natl Acad Sci U S A. 2004;101:6882–7.PubMedPubMedCentralCrossRefGoogle Scholar
  190. 190.
    Nordlund P, Reichard P. Ribonucleotide reductases. Annu Rev Biochem. 2006;75:681–706.PubMedCrossRefGoogle Scholar
  191. 191.
    Berggren G, Duraffourg N, Sahlin M, Sjöberg BM. Semiquinone-induced maturation of Bacillus anthracis ribonucleotide reductase by a superoxide intermediate. J Biol Chem. 2014;289:31940–9.PubMedPubMedCentralCrossRefGoogle Scholar
  192. 192.
    Pulatova MK, Sharygin VL, Todorov IN. The activation of ribonucleotide reductase in animal organs as the cellular response against the treatment with DNA-damaging factors and the influence of radioprotectors on this effect. Biochim Biophys Acta. 1999;1453:321–9.PubMedCrossRefGoogle Scholar
  193. 193.
    Poole AM, Jeffares DC, Penny D. The path from the RNA world. J Mol Evol. 1998;46:1–17.PubMedCrossRefGoogle Scholar
  194. 194.
    Jeffares DC, Poole AM, Penny D. Relics from the RNA world. J Mol Evol. 1998;46:18–36.PubMedCrossRefGoogle Scholar
  195. 195.
    Zhao H, Dobrucki J, Rybak P, Traganos F, Halicka HD, Darzynkiewicz Z. Induction of DNA damage signaling by oxidative stress in relation to DNA replication as detected using “click chemistry”. Cytometry A. 2011;79:897–902.PubMedPubMedCentralCrossRefGoogle Scholar
  196. 196.
    Berniak K, Rybak P, Bernas T, Zarębski M, Biela E, Zhao H, Darzynkiewicz Z, Dobrucki JW. Relationship between DNA damage response, initiated by camptothecin or oxidative stress, and DNA replication, analyzed by quantitative 3D image analysis. Cytometry A. 2013;83:913–24.PubMedPubMedCentralGoogle Scholar
  197. 197.
    Joyce GF, Orgel LE. Prospects for understanding the origin of RNA world. In: Gesteland RF, Atkins JF, editors. The RNA world. New York, NJ: Cold Spring Harbour Laboratory Press; 1993. p. 1–25.Google Scholar
  198. 198.
    Plume A. “Omics”: ‘genomics’ offspring shed light on biodiversity. Res Trends. 2010;19:6–7.Google Scholar
  199. 199.
    Malinski T, Taha Z. Nitric oxide release from a single cell measured in situ by a porphyrinic-based microsensor. Nature. 1992;358:676–8.PubMedCrossRefGoogle Scholar
  200. 200.
    Soh N, Katayama Y, Maeda M. A fluorescent probe for monitoring nitric oxide production using a novel detection concept. Analyst. 2001;126:564–6.PubMedCrossRefGoogle Scholar
  201. 201.
    Mal A, Chatterjee IB. Mechanism of autoxidation of oxyhaemoglobin. J Biosci. 1991;16:55–70.CrossRefGoogle Scholar
  202. 202.
    Batthyány C, Bartesaghi S, Mastrogiovanni M, Lima A, Demicheli V, Radi R. Tyrosine-nitrated proteins: proteomic and bioanalytical aspects. Antioxid Redox Signal. 2017;26:313–28.PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    Mak PJ, Denisov IG. Spectroscopic studies of the cytochrome P450 reaction mechanisms. Biochim Biophys Acta. 2018;1866(1):178–204.  https://doi.org/10.1016/j.bbapap.2017.06.021.CrossRefGoogle Scholar
  204. 204.
    Di Giuseppe S, Placidi G, Sotgiu A. New experimental apparatus for multimodal resonance imaging: initial EPRI and NMRI experimental results. Phys Med Biol. 2001;46:1003–16.PubMedCrossRefGoogle Scholar
  205. 205.
    Beer S. Cybernetyka a zarządzanie [Cybernetics and management]. Warszawa: PWN; 1966, pp. 67–74. [in Polish, transl. by Ś. Sorokowski of the 1st Edition, The English London: University Press Ltd; 1959].Google Scholar
  206. 206.
    Pasenkiewicz-Gierula M, Sealy RC. Analysis of the ESR spectrum of synthetic dopa melanin. Biochim Biophys Acta. 1986;884:510–6.PubMedCrossRefGoogle Scholar
  207. 207.
    Subczynski WK, Kusumi A. Dynamics of raft molecules in the cell and artificial membranes: approaches by pulse EPR spin labeling and single molecule optical microscopy. Biochim Biophys Acta. 2003;1610:231–43.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Department of Biophysics, Faculty of Biochemistry, Biophysics and BiotechnologyJagiellonian UniversityKrakówPoland

Personalised recommendations