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Nanoscale detection and real-time monitoring of free radicals in a single living cell under the stimulation of targeting moieties using a nanodiamond quantum sensor

Kaiqi Wu ,
Qi Lu ,
Maabur Sow ,
Priyadharshini Balasubramanian ,
Fedor Jelezko ,
Tanja Weil ,
Yingke Wu
Volume 4, Issue 1 (2024)
DOI: 10.1080/26941112.2024.2336524
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Keywords

Nanodiamond; cell targeting peptides; in-cell free radicals detection; nitrogen-vacancy center; quantum sensor; T1 relaxometry

References

  • Pizzino G, Irrera N, Cucinotta M, et al. Oxidative stress: harms and benefits for human health. Oxidative Med Cell Longev. 2017;2017:1–13.  Web of Science ®Google Scholar
  • Lobo V, Patil A, Phatak A, et al. Free radicals, antioxidants and functional foods: impact on human health. Phcog Rev. 2010;4(8):118–126.  Google Scholar
  • Okada F. Inflammation and free radicals in tumor development and progression. Redox Rep. 2002;7(6):357–368.  PubMed Web of Science ®Google Scholar
  • Nathan C, Cunningham-Bussel A. Beyond oxidative stress: an immunologist’s guide to reactive oxygen species. Nat Rev Immunol. 2013;13(5):349–361.  PubMed Web of Science ®Google Scholar
  • Radi R. Oxygen radicals, nitric oxide, and peroxynitrite: redox pathways in molecular medicine. Proc Natl Acad Sci USA. 2018;115(23):5839–5848.  PubMed Web of Science ®Google Scholar
  • Knight JA. Review: free radicals, antioxidants, and the immune system. Ann Clin Lab Sci. 2000;30(2):145–158.  PubMed Web of Science ®Google Scholar
  • Andrés C, Pérez de la Lastra J, Juan C, et al. The role of reactive species on innate immunity. Vaccines. 2022;10(10):1735.  PubMed Web of Science ®Google Scholar
  • Gomes A, Fernandes E, Lima JL. Fluorescence probes used for detection of reactive oxygen species. J Biochem Biophys Methods. 2005;65(2–3):45–80.  PubMedGoogle Scholar
  • Damle VG, Wu K, Arouri DJ, et al. Detecting free radicals post viral infections. Free Radic Biol Med. 2022;191:8–23.  PubMed Web of Science ®Google Scholar
  • Kalyanaraman B, Darley-Usmar V, Davies KJ, et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med. 2012;52(1):1–6.  PubMed Web of Science ®Google Scholar
  • Wu Y, Weil T. Recent developments of nanodiamond quantum sensors for biological applications. Adv Sci. 2022;9(19):2200059.  Web of Science ®Google Scholar
  • Schirhagl R, Chang K, Loretz M, et al. Nitrogen-vacancy centers in diamond: nanoscale sensors for physics and biology. Annu Rev Phys Chem. 2014;65(1):83–105.  PubMed Web of Science ®Google Scholar
  • Steinert S, Ziem F, Hall LT, et al. Magnetic spin imaging under ambient conditions with sub-cellular resolution. Nat Commun. 2013;4(1):1607.  PubMed Web of Science ®Google Scholar
  • Vaijayanthimala V, Tzeng Y, Chang H, et al. The biocompatibility of fluorescent nanodiamonds and their mechanism of cellular uptake. Nanotechnology. 2009;20(42):425103.  PubMed Web of Science ®Google Scholar
  • Barton J, Gulka M, Tarabek J, et al. Nanoscale dynamic readout of a chemical redox process using radicals coupled with nitrogen-vacancy centers in nanodiamonds. ACS Nano. 2020;14(10):12938–12950.  PubMed Web of Science ®Google Scholar
  • Wu Y, Balasubramanian P, Wang Z, et al. Detection of few hydrogen peroxide molecules using self-reporting fluorescent nanodiamond quantum sensors. J Am Chem Soc. 2022;144(28):12642–12651.  PubMed Web of Science ®Google Scholar
  • Maze JR, Stanwix PL, Hodges JS, et al. Nanoscale magnetic sensing with an individual electronic spin in diamond. Nature. 2008;455(7213):644–647.  PubMed Web of Science ®Google Scholar
  • Ackermann K, Wort JL, Bode BE. Pulse dipolar EPR for determining nanomolar binding affinities. Chem Commun. 2022;58(63):8790–8793.  PubMed Web of Science ®Google Scholar
  • Sigaeva A, Shirzad H, Martinez FP, et al. Diamond-based nanoscale quantum relaxometry for sensing free radical production in cells. Small. 2022;18(44):2105750.  Web of Science ®Google Scholar
  • Sigaeva A, Norouzi N, Schirhagl R. Intracellular relaxometry, challenges, and future directions. ACS Cent Sci. 2022;8(11):1484–1489.  PubMed Web of Science ®Google Scholar
  • Nie L, Nusantara AC, Damle VG, et al. Quantum monitoring of cellular metabolic activities in single mitochondria. Sci Adv. 2021;7(21):eabf0573.  PubMed Web of Science ®Google Scholar
  • Wu K, Vedelaar TA, Damle VG, et al. Applying NV center-based quantum sensing to study intracellular free radical response upon viral infections. Redox Biol. 2022;52:102279.  PubMed Web of Science ®Google Scholar
  • Wu K, Nie L, Nusantara AC, et al. Diamond relaxometry as a tool to investigate the free radical dialogue between macrophages and bacteria. ACS Nano. 2023;17(2):1100–1111.  PubMed Web of Science ®Google Scholar
  • Lu Q, Vosberg B, Wang Z, et al. Unraveling eumelanin radical formation by nanodiamond optical relaxometry in a living cell. J. Am. Chem. Soc. 2024;146(11):7222–7232.  Google Scholar
  • Wu Y, Alam MNA, Balasubramanian P, et al. Nanodiamond theranostic for light-controlled intracellular heating and nanoscale temperature sensing. Nano Lett. 2021;21(9):3780–3788.  PubMed Web of Science ®Google Scholar
  • Wu Y, Alam MNA, Balasubramanian P, et al. Fluorescent nanodiamond–nanogels for nanoscale sensing and photodynamic applications. Adv Biomed Res. 2021;1(7):2000101.  Google Scholar
  • Theodoropoulou M, Stalla GK. Somatostatin receptors: from signaling to clinical practice. Front Neuro­endocrinol. 2013;34(3):228–252.  PubMed Web of Science ®Google Scholar
  • Zielonka J, Joseph J, Sikora A, et al. Mitochondria-targeted triphenylphosphonium-based compounds: syntheses, mechanisms of action, and therapeutic and diagnostic applications. Chem Rev. 2017;117(15):10043–10120.  PubMed Web of Science ®Google Scholar
  • Gump JM, Dowdy SF. TAT transduction: the molecular mechanism and therapeutic prospects. Trends Mol Med. 2007;13(10):443–448.  PubMed Web of Science ®Google Scholar
  • Jung HS, Cho KJ, Seol Y, et al. Polydopamine encapsulation of fluorescent nanodiamonds for biomedical applications. Adv Funct Mater. 2018;28(33):1801252.  PubMed Web of Science ®Google Scholar
  • Shamsi BH, Chatoo M, Xu X, et al. Versatile functions of somatostatin and somatostatin receptors in the gastrointestinal system. Front Endocrinol. 2021;12:652363.  PubMed Web of Science ®Google Scholar
  • Bousquet C, Puente E, Buscail L, et al. Antiproliferative effect of somatostatin and analogs. Chemotherapy. 2001;47(Suppl. 2):30–39.  PubMedGoogle Scholar
  • Zou Y, Xiao X, Li Y, et al. Somatostatin analogues inhibit cancer cell proliferation in an SSTR2-dependent manner via both cytostatic and cytotoxic pathways. Oncol Rep. 2009;21(2):379–386.  PubMed Web of Science ®Google Scholar
  • Sun L, Coy DH. Somatostatin receptor-targeted anti-cancer therapy. CDD. 2011;8(1):2–10.  PubMed Web of Science ®Google Scholar
  • Grötzinger C, Wiedenmann B. Somatostatin receptor targeting for tumor imaging and therapy. Ann N Y Acad Sci. 2004;1014(1):258–264.  PubMedGoogle Scholar
  • Arena S, Pattarozzi A, Corsaro A, et al. Somatostatin receptor subtype-dependent regulation of nitric oxide release: involvement of different intracellular pathways. Mol Endocrinol. 2005;19(1):255–267.  PubMedGoogle Scholar
  • Akaike T, Maeda H. Nitric oxide and virus infection. Immunology. 2000;101(3):300–308.  PubMed Web of Science ®Google Scholar
  • Hou C, Metcalfe NB, Salin K. Is mitochondrial reactive oxygen species production proportional to oxygen consumption? A theoretical consideration. Bioessays. 2021;43(4):e2000165.  PubMed Web of Science ®Google Scholar
  • Reily C, Mitchell T, Chacko BK, et al. Mitochondrially targeted compounds and their impact on cellular bioenergetics. Redox Biol. 2013;1(1):86–93.  PubMed Web of Science ®Google Scholar
  • Frankel AD, Pabo CO. Cellular uptake of the TAT protein from human immunodeficiency virus. Cell. 1988;55(6):1189–1193.  PubMed Web of Science ®Google Scholar
  • Green M, Loewenstein PM. Autonomous functional domains of chemically synthesized human immunodeficiency virus TAT trans-activator protein. Cell. 1988;55(6):1179–1188.  PubMed Web of Science ®Google Scholar
  • Kuroda Y, Kato-Kogoe N, Tasaki E, et al. Oligopeptides derived from autophosphorylation sites of EGF receptor suppress EGF-stimulated responses in human lung carcinoma a549 cells. Eur J Pharmacol. 2013;698(1–3):87–94.  PubMed Web of Science ®Google Scholar
  • Ruseska I, Zimmer A. Internalization mechanisms of cell-penetrating peptides. Beilstein J Nanotechnol. 2020;11:101–123.  PubMed Web of Science ®Google Scholar
  • Sarder P, Nehorai A. Deconvolution methods for 3-D fluorescence microscopy images. IEEE Signal Process Mag. 2006;23(3):32–45.  Web of Science ®Google Scholar
  • Dunn KW, Kamocka MM, McDonald JH. A practical guide to evaluating colocalization in biological microscopy. Am J Physiol-Cell Physiol. 2011;300(4):C723–C742.  PubMed Web of Science ®Google Scholar
  • Zhang Y, Sharmin R, Sigaeva A, et al. Not all cells are created equal – endosomal escape in fluorescent nanodiamonds in different cells. Nanoscale. 2021;13(31):13294–13300.  PubMed Web of Science ®Google Scholar
  • Stauffer W, Sheng H, Lim H. Ezcolocalization: an imagej plugin for visualizing and measuring colocalization in cells and organisms. Sci Rep. 2018;8(1):15764.  PubMedGoogle Scholar
  • Martens TF, Remaut K, Demeester J, et al. Intracellular delivery of nanomaterials: how to catch endosomal escape in the act. Nano Today. 2014;9(3):344–364.  Web of Science ®Google Scholar
  • Binder JM, Stark A, Tomek N, et al. Qudi: a modular python suite for experiment control and data processing. SoftwareX. 2017;6:85–90.  Web of Science ®Google Scholar
  • Yanagi T, Kaminaga K, Suzuki M, et al. All-optical wide-field selective imaging of fluorescent nanodiamonds in cells, in vivo and ex vivo. ACS Nano. 2021;15(8):12869–12879.  PubMed Web of Science ®Google Scholar
  • Bluvstein D, Zhang Z, Jayich ACB. Identifying and mitigating charge instabilities in shallow diamond nitrogen-vacancy centers. Phys Rev Lett. 2019;122(7):076101.  PubMed Web of Science ®Google Scholar
  • Barbosa I, Gutsche J, Widera A. Impact of charge conversion on NV-center relaxometry. Phys Rev B. 2023;108(7):075411.  Web of Science ®Google Scholar
  • Barnett P. Somatostatin and somatostatin receptor physiology. ENDO. 2003;20(3):255–264.  Google Scholar
  • Hofland LJ, Lamberts SW. The pathophysiological consequences of somatostatin receptor internalization and resistance. Endocr Rev. 2003;24(1):28–47.  PubMed Web of Science ®Google Scholar
  • Cakir M, Dworakowska D, Grossman A. Somatostatin receptor biology in neuroendocrine and pituitary tumours: part 1-molecular pathways. J Cellular Molecular Medi. 2010;14(11):2570–2584.  PubMed Web of Science ®Google Scholar
  • White RE, Schonbrunn A, Armstrong DL. Somatostatin stimulates Ca2+-activated K+ channels through protein dephosphorylation. Nature. 1991;351(6327):570–573.  PubMed Web of Science ®Google Scholar
  • Choi EJ, Jeon CH, Lee IK. Ferric ammonium citrate upregulates PD-L1 expression through generation of reactive oxygen species. J Immunol Res. 2022;2022:1–8.  Web of Science ®Google Scholar
  • Zorko M, Langel U. Cell-penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev. 2005;57(4):529–545.  PubMed Web of Science ®Google Scholar
  • de Guillebon T, Vindolet B, Roch JF, et al. Temperature dependence of the longitudinal spin relaxation time t1 of single nitrogen-vacancy centers in nanodiamonds. Phys Rev B. 2020;102(16):165427.  Web of Science ®Google Scholar
  • Fujisaku T, Tanabe R, Onoda S, et al. pH nanosensor using electronic spins in diamond. ACS Nano. 2019;13(10):11726–11732.  PubMed Web of Science ®Google Scholar
  • Shi FZ, Zhang Q, Wang PF, et al. Single-protein spin resonance spectroscopy under ambient conditions. Science. 2015;347(6226):1135–1138.  PubMed Web of Science ®Google Scholar
  • Shi FZ, Kong F, Zhao PJ, et al. Single-DNA electron spin resonance spectroscopy in aqueous solutions. Nat Methods. 2018;15(9):697–699.  PubMed Web of Science ®Google Scholar
  • Wood JDA, Tetienne JP, Broadway DA, et al. Microwave-free nuclear magnetic resonance at molecular scales. Nat Commun. 2017;8(1):15950.  PubMedGoogle Scholar
  • Qin Z, Wang Z, Kong F, et al. In situ electron paramagnetic resonance spectroscopy using single nanodiamond sensors. Nat Commun. 2023;14(1):6278.  PubMed Web of Science ®Google Scholar
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