A puromycin-dependent activity-based sensing probe for histochemical staining of hydrogen peroxide in cells and animal tissues

Kaede Hoshi, Marco S. Messina, Jun Ohata, Clive Yik-Sham Chung, Christopher J. Chang

Published: 2022-05-12 DOI: 10.1038/s41596-022-00694-7

Hydrogen Peroxide

Activity-Based Probe

Peroxymycin-1

Chemoselective Oxidation

Histochemical Staining

AI 解读

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Chromatin accessibility profiling by ATAC-seq

Deoxyfluorination of phenols for chemoselective18F-labeling of peptides

Author Correction: cfSNV: a software tool for the sensitive detection of somatic mutations from cell-free DNA

Human primordial germ cell-like cells specified from resetting precursors develop in human hindgut organoids

An inexpensive semi-automated sample processing pipeline for cell-free RNA extraction

Application of CHyMErA Cas9-Cas12a combinatorial genome-editing platform for genetic interaction mapping and gene fragment deletion screening

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Hydrogen peroxide (H2O2) is a key member of the reactive oxygen species family of transient small molecules that has broad contributions to oxidative stress and redox signaling. The development of selective and sensitive chemical probes can enable the stu
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ACKNOWLEDGMENTS

Baynes, J. W. Role of oxidative stress in development of complications in diabetes. Diabetes 40, 405–412 (1991).
Multhaup, G. et al. Reactive oxygen species and Alzheimer’s disease. Biochem. Pharmacol. 54, 533–539 (1997).
Stone, J. R. & Yang, S. Hydrogen peroxide: a signaling messenger. Antioxid. Redox Signal. 8, 243–270 (2006).
Rhee, S. G. H2O2, a necessary evil for cell signaling. Science 312, 1882–1883 (2006).
D’Autréaux, B. & Toledano, M. B. ROS as signaling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 8, 813–824 (2007).
Finkel, T., Serrano, M. & Blasco, M. A. The common biology of cancer and ageing. Nature 448, 767–774 (2007).
Winterbourn, C. C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 4, 278–286 (2008).
Dickinson, B. C. & Chang, C. J. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat. Chem. Biol. 7, 504–511 (2011).
Murphy, M. P. et al. Unraveling the biological roles of reactive oxygen species. Cell Metab. 13, 361–366 (2011).
Schieber, M. & Chandel, N. S. ROS function in redox signaling and oxidative stress. Curr. Biol. 24, R453–R462 (2014).
Reichmann, D., Voth, W. & Jakob, U. Maintaining a healthy proteome during oxidative stress. Mol. Cell 69, 203–213 (2018).
Sies, H. & Jones, D. P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 21, 363–383 (2020).
Inoguchi, T. et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C–dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 49, 1939–1945 (2000).
Park, L. et al. Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc. Natl Acad. Sci. USA. 105, 1347–1352 (2008).
Schmidt, K. N., Amstad, P., Cerutti, P. & Baeuerle, P. A. The roles of hydrogen peroxide and superoxide as messengers in the activation of transcription factor NF-κB. Chem. Biol. 2, 13–22 (1995).
Guyton, K. Z., Liu, Y., Gorospe, M., Xu, Q. & Holbrook, N. J. Activation of mitogen-activated protein kinase by H2O2: role in cell survival following oxidant injury. J. Biol. Chem. 271, 4138–4142 (1996).
Lee, S.-R., Kwon, K.-S., Kim, S.-R. & Rhee, S. G. Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273, 15366–15372 (1998).
Salmeen, A. et al. Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate. Nature 423, 769–773 (2003).
Avshalumov, M. V. & Rice, M. E. Activation of ATP-sensitive K+ (KATP) channels by H2O2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc. Natl Acad. Sci. USA. 100, 11729–11734 (2003).
Lambeth, J. D. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181–189 (2004).
Dinauer, M. C., Orkin, S. H., Brown, R., Jesaitis, A. J. & Parkos, C. A. The glycoprotein encoded by the X-linked chronic granulomatous disease locus is a component of the neutrophil cytochrome b complex. Nature 327, 717–720 (1987).
Volpp, B., Nauseef, W. & Clark, R. Two cytosolic neutrophil oxidase components absent in autosomal chronic granulomatous disease. Science 242, 1295–1297 (1988).
Clark, R. A. et al. Genetic variants of chronic granulomatous disease: prevalence of deficiencies of two cytosolic components of the NADPH oxidase system. N. Engl. J. Med. 321, 647–652 (1989).
Ohba, M., Shibanuma, M., Kuroki, T. & Nose, K. Production of hydrogen peroxide by transforming growth factor-beta 1 and its involvement in induction of egr-1 in mouse osteoblastic cells. J. Cell Biol. 126, 1079–1088 (1994).
Sundaresan, M., Yu, Z.-X., Ferrans, V. J., Irani, K. & Finkel, T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 270, 296–299 (1995).
Kimura, T., Okajima, F., Sho, K., Kobayashi, I. & Kondo, Y. Thyrotropin-induced hydrogen peroxide production in FRTL-5 thyroid cells is mediated not by adenosine 3′, 5′-monophosphate, but by Ca2+ signaling followed by phospholipase-A2 activation and potentiated by an adenosine derivative. Endocrinology 136, 116–123 (1995).
Bae, Y. S. et al. Epidermal growth factor (EGF)-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 272, 217–221 (1997).
Mukhin, Y. V. et al. 5-Hydroxytryptamine1A receptor/Giβγ stimulates mitogen-activated protein kinase via NAD(P)H oxidase and reactive oxygen species upstream of src in chinese hamster ovary fibroblasts. Biochem. J. 347, 61–67 (2000).
Dickinson, B. C., Peltier, J., Stone, D., Schaffer, D. V. & Chang, C. J. Nox2 redox signaling maintains essential cell populations in the brain. Nat. Chem. Biol. 7, 106–112 (2011).
Kamsler, A. & Segal, M. Hydrogen peroxide modulation of synaptic plasticity. J. Neurosci. 23, 269–276 (2003).
Tejada-Simon, M. V. et al. Synaptic localization of a functional NADPH oxidase in the mouse hippocampus. Mol. Cell. Neurosci. 29, 97–106 (2005).
Brennan, A. M. et al. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat. Neurosci. 12, 857–863 (2009).
De Pasquale, R., Beckhauser, T. F., Hernandes, M. S. & Giorgetti Britto, L. R. LTP and LTD in the visual cortex require the activation of NOX2. J. Neurosci. 34, 12778–12787 (2014).
Le Belle, J. E. et al. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 8, 59–71 (2011).
Xu, C., Luo, J., He, L., Montell, C. & Perrimon, N. Oxidative stress induces stem cell proliferation via TRPA1/RyR-mediated Ca2+ signaling in the Drosophila midgut. eLife 6, e22441 (2017).
O’Neill, J. S. & Reddy, A. B. Circadian clocks in human red blood cells. Nature 469, 498–503 (2011).
Wible, R. S. et al. NRF2 regulates core and stabilizing circadian clock loops, coupling redox and timekeeping in Mus musculus. eLife 7, e31656 (2018).
Pei, J.-F. et al. Diurnal oscillations of endogenous H2O2 sustained by p66Shc regulate circadian clocks. Nat. Cell Biol. 21, 1553–1564 (2019).
Niethammer, P., Grabher, C., Look, A. T. & Mitchison, T. J. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 459, 996–999 (2009).
Hervera, A. et al. Reactive oxygen species regulate axonal regeneration through the release of exosomal NADPH oxidase 2 complexes into injured axons. Nat. Cell Biol. 20, 307–319 (2018).
Lippert, A. R., Van de Bittner, G. C. & Chang, C. J. Boronate oxidation as a bioorthogonal reaction approach for studying the chemistry of hydrogen peroxide in living systems. Acc. Chem. Res. 44, 793–804 (2011).
Chan, J., Dodani, S. C. & Chang, C. J. Reaction-based small-molecule fluorescent probes for chemoselective bioimaging. Nat. Chem. 4, 973–984 (2012).
Brewer, T. F., Garcia, F. J., Onak, C. S., Carroll, K. S. & Chang, C. J. Chemical approaches to discovery and study of sources and targets of hydrogen peroxide redox signaling through NADPH oxidase proteins. Annu. Rev. Biochem. 84, 765–790 (2015).
Bruemmer, K. J., Crossley, S. W. M. & Chang, C. J. Activity-based sensing: a synthetic methods approach for selective molecular imaging and beyond. Angew. Chem. Int. Ed. 59, 13734–13762 (2019).
Chang, M. C. Y., Pralle, A., Isacoff, E. Y. & Chang, C. J. A selective, cell-permeable optical probe for hydrogen peroxide in living cells. J. Am. Chem. Soc. 126, 15392–15393 (2004).
Miller, E. W., Tulyathan, O., Isacoff, E. Y. & Chang, C. J. Molecular imaging of hydrogen peroxide produced for cell signaling. Nat. Chem. Biol. 3, 263–267 (2007).
Dickinson, B. C., Huynh, C. & Chang, C. J. A palette of fluorescent probes with varying emission colors for imaging hydrogen peroxide signaling in living cells. J. Am. Chem. Soc. 132, 5906–5915 (2010).
Srikun, D., Miller, E. W., Domaille, D. W. & Chang, C. J. An ICT-based approach to ratiometric fluorescence imaging of hydrogen peroxide produced in living cells. J. Am. Chem. Soc. 130, 4596–4597 (2008).
Albers, A. E., Okreglak, V. S. & Chang, C. J. A FRET-based approach to ratiometric fluorescence detection of hydrogen peroxide. J. Am. Chem. Soc. 128, 9640–9641 (2006).
Chung, C., Srikun, D., Lim, C. S., Chang, C. J. & Cho, B. R. A two-photon fluorescent probe for ratiometric imaging of hydrogen peroxide in live tissue. Chem. Commun. 47, 9618–9620 (2011).
Dickinson, B. C. & Chang, C. J. A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells. J. Am. Chem. Soc. 130, 9638–9639 (2008).
Dickinson, B. C., Tang, Y., Chang, Z. & Chang, C. J. A nuclear-localized fluorescent hydrogen peroxide probe for monitoring sirtuin-mediated oxidative stress responses in vivo. Chem. Biol. 18, 943–948 (2011).
Miller, E. W., Dickinson, B. C. & Chang, C. J. Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl Acad. Sci. USA. 107, 15681–15686 (2010).
Iwashita, H., Castillo, E., Messina, M. S., Swanson, R. A. & Chang, C. J. A tandem activity-based sensing and labeling strategy enables imaging of transcellular hydrogen peroxide signaling. Proc. Natl Acad. Sci. USA. 118, e2018513118 (2021).
Van de Bittner, G. C., Dubikovskaya, E. A., Bertozzi, C. R. & Chang, C. J. In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporter. Proc. Natl Acad. Sci. USA. 107, 21316–21321 (2010).
Van de Bittner, G. C., Bertozzi, C. R. & Chang, C. J. Strategy for dual-analyte luciferin imaging: in vivo bioluminescence detection of hydrogen peroxide and caspase activity in a murine model of acute Inflammation. J. Am. Chem. Soc. 135, 1783–1795 (2013).
Jin, L. et al. Glutamate dehydrogenase 1 signals through antioxidant glutathione peroxidase 1 to regulate redox homeostasis and tumor growth. Cancer Cell 27, 257–270 (2015).
Schoenfeld, J. D. et al. O2⋅− and H2O2–mediated disruption of Fe metabolism causes the differential susceptibility of NSCLC and GBM cancer cells to pharmacological ascorbate. Cancer Cell 31, 487–500 (2017).
Chung, C. Y.-S., Timblin, G. A., Saijo, K. & Chang, C. J. Versatile histochemical approach to detection of hydrogen peroxide in cells and tissues based on puromycin staining. J. Am. Chem. Soc. 140, 6109–6121 (2018).
Dhibi, M. et al. The intake of high fat diet with different trans fatty acid levels differentially induces oxidative stress and non alcoholic fatty liver disease (NAFLD) in rats. Nutr. Metab. 8, 65–77 (2011).
Bilan Dmitry, S. & Belousov Vsevolod, V. In vivo imaging of hydrogen peroxide with HyPer probes. Antioxid. Redox Signal. 29, 569–584 (2018).
Morgan, B. et al. Real-time monitoring of basal H2O2 levels with peroxiredoxin-based probes. Nat. Chem. Biol. 12, 437–443 (2016).
Srikun, D., Albers, A. E., Nam, C. I., Iavarone, A. T. & Chang, C. J. Organelle-targetable fluorescent probes for imaging hydrogen peroxide in living cells via SNAP-Tag protein labeling. J. Am. Chem. Soc. 132, 4455–4465 (2010).
Dickinson, B. C., Lin, V. S. & Chang, C. J. Preparation and use of MitoPY1 for imaging hydrogen peroxide in mitochondria of live cells. Nat. Protoc. 8, 1249–1259 (2013).
Szweda, P. A., Tsai, L. & Szweda, L. I. Immunochemical detection of a fluorophore derived from the lipid peroxidation product 4-hydroxy-2-nonenal and lysine. In Oxidants and Antioxidants: Ultrastructure and Molecular Biology Protocols (ed. Armstrong, D.) Vol. 196 277–290 (Humana Press, 2002).
Spangler, B. et al. A reactivity-based probe of the intracellular labile ferrous iron pool. Nat. Chem. Biol. 12, 680–685 (2016).
Schmidt, E. K., Clavarino, G., Ceppi, M. & Pierre, P. SUnSET, a nonradioactive method to monitor protein synthesis. Nat. Methods 6, 275–277 (2009).
Su, K.-H. et al. HSF1 critically attunes proteotoxic stress sensing by mTORC1 to combat stress and promote growth. Nat. Cell Biol. 18, 527–539 (2016).
tom Dieck, S. et al. Direct visualization of newly synthesized target proteins in situ. Nat. Methods 12, 411–414 (2015).
Deliu, L. P., Ghosh, A. & Grewal, S. S. Investigation of protein synthesis in Drosophila larvae using puromycin labelling. Biol. Open 6, 1229–1234 (2017).
Bielczyk-Maczyńska, E. et al. The ribosome biogenesis protein Nol9 is essential for definitive hematopoiesis and pancreas morphogenesis in zebrafish. PLoS Genet. 11, e1005677 (2015).

A puromycin-dependent activity-based sensing probe for histochemical staining of hydrogen peroxide in cells and animal tissues

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