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Nicotinamide adenine dinucleotide (NAD+) reduction enabled by an atomically precise Au-Ag alloy nanocluster

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Abstract

The redox property of the ultrasmall coinage nanoclusters (with several to tens of Au/Ag atoms) has elucidated the electron-transfer capacity of nanoclusters, and has been successfully utilized in a variety of redox conversions (such as from CO2 to CO). Nevertheless, their biological applications are mainly restricted by the scarcity of atomically precise, water-soluble metal nanoclusters, and the limited application (mainly on the decomposition of H2O2 in these days). Herein, mercaptosuccinic acid (MSA) protected ultrasmall alloy AuAg nanoclusters were prepared, and the main product was determined [Au3Ag5(MSA)3] by electrospray ionization mass spectrometry (ESI-MS). The clusters can not only mediate the decomposition of H2O2 to generate hydroxyl radicals, but is also able to mediate the reduction of nicotinamide adenine dinucleotide (NAD) to its reduced form of NADH. This is the first time that the atomically precise metal nanoclusters were used to mediate the coenzyme reduction. The preliminary mechanistic insights imply the reaction to be driven by the hydrogen bonding between the carboxylic groups (on the surface of MSA) and the amino N—H bonds (on NAD). In this context, the presence of the carboxylic groups, the sub-nanometer size regime (∼ 1 nm), and the synergistic effect of the Au-Ag clusters are pre-requisite to the NAD reduction.

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References

  1. Yang, J.; Jin, R. C. New advances in atomically precise silver nanoclusters. ACS Mater. Lett. 2019, 1, 482–489.

    CAS  Google Scholar 

  2. Kang, X.; Li, Y. W.; Zhu, M. Z.; Jin, R. C. Atomically precise alloy nanoclusters: Syntheses, structures, and properties. Chem. Soc. Rev. 2020, 49, 6443–6514.

    Google Scholar 

  3. Nasaruddin, R. R.; Chen, T. K.; Yan, N.; Xie, J. P. Roles of thiolate ligands in the synthesis, properties and catalytic application of gold nanoclusters. Coord. Chem. Rev. 2018, 368, 60–79.

    CAS  Google Scholar 

  4. Du, Y. X.; Sheng, H. T.; Astruc, D.; Zhu, M. Z. Atomically precise noble metal nanoclusters as efficient catalysts: A bridge between structure and properties. Chem. Rev. 2020, 120, 526–622.

    CAS  Google Scholar 

  5. Li, G.; Jin, R. C. Atomically precise gold nanoclusters as new model catalysts. Acc. Chem. Res. 2013, 46, 1749–1758.

    CAS  Google Scholar 

  6. Li, G.; Abroshan, H.; Chen, Y. X.; Jin, R. C.; Kim, H. J. Experimental and mechanistic understanding of aldehyde hydrogenation using Au25 nanoclusters with Lewis acids: Unique sites for catalytic reactions. J. Am. Chem. Soc. 2015, 137, 14295–304.

    CAS  Google Scholar 

  7. Zhuang, S. L.; Chen, D.; Liao, L. W.; Zhao, Y.; Xia, N.; Zhang, W. H.; Wang, C. M.; Yang, J.; Wu, Z. K. Hard-sphere random close-packed Au47Cd2(TBBT)31 nanoclusters with a Faradaic efficiency of up to 96% for electrocatalytic CO2 reduction to CO. Angew. Chem., Int. Ed. 2020, 59, 3073–3077.

    CAS  Google Scholar 

  8. Sun, Y. N.; Liu, X.; Xiao, K.; Zhu, Y.; Chen, M. Y. Active-site tailoring of gold cluster catalysts for electrochemical CO2 reduction. ACS Catal. 2021, 11, 11551–11560.

    CAS  Google Scholar 

  9. Yuan, S. F.; Guan, Z. J.; Wang, Q. M. Identification of the active species in bimetallic cluster catalyzed hydrogenation. J. Am. Chem. Soc. 2022, 144, 11405–11412.

    CAS  Google Scholar 

  10. Shivhare, A.; Ambrose, S. J.; Zhang, H. X.; Purves, R. W.; Scott, R. W. J. Stable and recyclable Au25 clusters for the reduction of 4-nitrophenol. Chem. Commun. 2013, 49, 276–278.

    CAS  Google Scholar 

  11. Chong, H. B.; Li, P.; Wang, S. X.; Fu, F. Y.; Xiang, J.; Zhu, M. Z.; Li, Y. D. Au25 clusters as electron-transfer catalysts induced the intramolecular cascade reaction of 2-nitrobenzonitrile. Sci. Rep. 2013, 3, 3214.

    Google Scholar 

  12. Li, X.; Takano, S.; Tsukuda, T. Ligand effects on the hydrogen evolution reaction catalyzed by Au13 and Pt@Au12: Alkynyl vs thiolate. J. Phys. Chem. C 2021, 125, 23226–23230.

    CAS  Google Scholar 

  13. Pollitt, S.; Truttmann, V.; Haunold, T.; Garcia, C.; Olszewski, W.; Llorca, J.; Barrabés, N.; Rupprechter, G. The dynamic structure of Au38(SR)24 nanoclusters supported on CeO2 upon pretreatment and CO oxidation. ACS Catal. 2020, 10, 6144–6148.

    CAS  Google Scholar 

  14. Sarkar, B.; Prajapati, P.; Tiwari, R.; Tiwari, R.; Ghosh, S.; Shubhra Acharyya, S.; Pendem, C.; Kumar Singha, R.; Sivakumar Konathala, L. N.; Kumar, J. et al. Room temperature selective oxidation of cyclohexane over Cu-nanoclusters supported on nanocrystalline Cr2O3. Green Chem. 2012, 14, 2600–2606.

    CAS  Google Scholar 

  15. Kaizuka, K.; Miyamura, H.; Kobayashi, S. Remarkable effect of bimetallic nanocluster catalysts for aerobic oxidation of alcohols: Combining metals changes the activities and the reaction pathways to aldehydes/carboxylic acids or esters. J. Am. Chem. Soc. 2010, 132, 15096–15098.

    CAS  Google Scholar 

  16. Shang, L.; Xu, J.; Nienhaus, G. U. Recent advances in synthesizing metal nanocluster-based nanocomposites for application in sensing, imaging and catalysis. Nano Today 2019, 28, 100767.

    Google Scholar 

  17. Peng, Y. W.; Gao, L.; Pidamaimaiti, G.; Zhao, D.; Zhang, L. M.; Yin, G. W.; Wang, F. Facile construction of highly luminescent and biocompatible gold nanoclusters by shell rigidification for two-photon pH-edited cytoplasmic and in vivo imaging. Nanoscale 2022, 14, 8342–8348.

    CAS  Google Scholar 

  18. Yu, M. X.; Zhou, C.; Liu, J. B.; Hankins, J. D.; Zheng, J. Luminescent gold nanoparticles with pH-dependent membrane adsorption. J. Am. Chem. Soc. 2011, 133, 11014–11017.

    CAS  Google Scholar 

  19. Yahia-Ammar, A.; Sierra, D.; Mérola, F.; Hildebrandt, N.; Guével, X. L. Self-assembled gold nanoclusters for bright fluorescence imaging and enhanced drug delivery. ACS Nano 2016, 10, 2591–2599.

    CAS  Google Scholar 

  20. Zhao, Y.; Zhuang, S. L.; Liao, L. W.; Wang, C. M.; Xia, N.; Gan, Z. B.; Gu, W. M.; Li, J.; Deng, H. T.; Wu, Z. K. A dual purpose strategy to endow gold nanoclusters with both catalysis activity and water solubility. J. Am. Chem. Soc. 2020, 142, 973–977.

    CAS  Google Scholar 

  21. Hu, L. Z.; Yuan, Y. L.; Zhang, L.; Zhao, J. M.; Majeed, S.; Xu, G. B. Copper nanoclusters as peroxidase mimetics and their applications to H2O2 and glucose detection. Anal. Chim. Acta 2013, 762, 83–86.

    CAS  Google Scholar 

  22. Zhang, C. X.; Gao, Y. C.; Li, H. W.; Wu, Y. Q. Gold-platinum bimetallic nanoclusters for oxidase-like catalysis. ACS Appl. Nano Mater. 2020, 3, 9318–9328.

    CAS  Google Scholar 

  23. Xu, J.; Sun, F. Y.; Li, Q.; Yuan, H. X.; Ma, F. Y.; Wen, D.; Shang, L. Ultrasmall gold nanoclusters-enabled fabrication of ultrafine gold aerogels as novel self-supported nanozymes. Small 2022, 18, 2200525.

    CAS  Google Scholar 

  24. Hong, C. Y.; Chen, L. L.; Wu, C. Y.; Yang, D.; Dai, J. Y.; Huang, Z. Y.; Cai, R.; Tan, W. H. Green synthesis of Au@WSe2 hybrid nanostructures with the enhanced peroxidase-like activity for sensitive colorimetric detection of glucose. Nano Res. 2022, 15, 1587–1592.

    CAS  Google Scholar 

  25. Hong, C. Y.; Zhang, X. X.; Wu, C. Y.; Chen, Q.; Yang, H. F.; Yang, D.; Huang, Z. Y.; Cai, R.; Tan, W. H. On-site colorimetric detection of cholesterol based on polypyrrole nanoparticles. ACS. Appl. Mater. Interfaces 2020, 12, 54426–54432.

    CAS  Google Scholar 

  26. Brust, M.; Walker, M.; Bethell, D.; Schiffrin, D. J.; Whyman, R. Synthesis of thiol-derivatised gold nanoparticles in a two-phase liquid—liquid system. J. Chem. Soc. Chem. Commun. 1994, 801–802.

  27. Nataraju, B.; Kalenius, E.; Udayabhaskararao, T.; Pradeep, T.; Siegenthaler, H.; Wandlowski, T. Phase transfer induced enhanced stability of monolayer protected silver quantum clusters. J. Clust. Sci. 2018, 29, 41–48.

    CAS  Google Scholar 

  28. Yao, Q. F.; Fung, V.; Sun, C.; Huang, S. D.; Chen, T. K.; Jiang, D. E.; Lee, J. Y.; Xie, J. P. Revealing isoelectronic size conversion dynamics of metal nanoclusters by a noncrystallization approach. Nat. Commun. 2018, 9, 1979.

    Google Scholar 

  29. Dass, A.; Sakthivel, N. A.; Jupally, V. R.; Kumara, C.; Rambukwella, M. Plasmonic nanomolecules: Electrochemical resolution of 22 electronic states in Au329(SR)84. ACS Energy Lett. 2020, 5, 207–214.

    CAS  Google Scholar 

  30. Liu, Y.; Liu, H. Y.; Hu, N. F. Core—shell nanocluster films of hemoglobin and clay nanoparticle: Direct electrochemistry and electrocatalysis. Biophys. Chem. 2005, 117, 27–37.

    CAS  Google Scholar 

  31. Liu, Z.; Zhu, M. Z.; Meng, X. M.; Xu, G. Y.; Jin, R. C. Electron transfer between [Au25(SC2H4Ph)18]TOA+ and oxoammonium cations. J. Phys. Chem. Lett. 2011, 2, 2104–2109.

    CAS  Google Scholar 

  32. Zhu, H. G.; Wang, S. S.; Wang, Y. R.; Song, C. W.; Yao, Q. F.; Yuan, X.; Xie, J. P. Gold nanocluster with AIE: A novel photodynamic antibacterial and deodorant molecule. Biomaterials 2022, 288, 121695.

    CAS  Google Scholar 

  33. Zhang, X.; Yang, Q.; Lang, Y. H.; Jiang, X.; Wu, P. Rationale of 3,3′,5,5′-tetramethylbenzidine as the chromogenic substrate in colorimetric analysis. Anal. Chem. 2020, 92, 12400–12406.

    CAS  Google Scholar 

  34. Misono, Y.; Ohkata, Y.; Morikawa, T.; Itoh, K. Resonance Raman and absorption spectroscopic studies on the electrochemical oxidation processes of 3,3′,5,5′-tetramethylbenzidine. J. Electroanal. Chem. 1997, 436, 203–212.

    CAS  Google Scholar 

  35. Westbrook, R. L.; Bridges, E.; Roberts, J.; Escribano-Gonzalez, C.; Eales, K. L.; Vettore, L. A.; Walker, P. D.; Vera-Siguenza, E.; Rana, H.; Cuozzo, F. et al. Proline synthesis through PYCR1 is required to support cancer cell proliferation and survival in oxygen-limiting conditions. Cell Rep. 2022, 38, 110320.

    CAS  Google Scholar 

  36. Buszewicz, G.; Madro, R. In vitro co-metabolism of ethanol and cyclic ketones. Toxicology 2002, 177, 207–213.

    CAS  Google Scholar 

  37. Kim, S. H.; Chung, G. Y.; Kim, S. H.; Vinothkumar, G.; Yoon, S. H.; Jung, K. D. Electrochemical NADH regeneration and electroenzymatic CO2 reduction on Cu nanorods/glassy carbon electrode prepared by cyclic deposition. Electrochim. Acta 2016, 210, 837–845.

    CAS  Google Scholar 

  38. Kory, N.; De Bos, J. U.; Van Der Rijt, S.; Jankovic, N.; Güra, M.; Arp, N.; Pena, I. A.; Prakash, G.; Chan, S. H.; Kunchok, T. et al. MCART1/SLC25A51 is required for mitochondrial NAD transport. Sci. Adv. 2020, 6, eabe5310.

    CAS  Google Scholar 

  39. Huang, X. H.; El-Sayed, I. H.; Yi, X. B.; El-Sayed, M. A. Gold nanoparticles: Catalyst for the oxidation of NADH to NAD+. J. Photochem. Photobiol. B 2005, 81, 76–83.

    CAS  Google Scholar 

  40. Saba, T.; Burnett, J. W. H.; Li, J. W.; Kechagiopoulos, P. N.; Wang, X. D. A facile analytical method for reliable selectivity examination in cofactor NADH regeneration. Chem. Commun. 2020, 56, 1231–1234.

    CAS  Google Scholar 

  41. de Graaf, R. A.; Behar, K. L. Detection of cerebral NAD+ by in vivo1H NMR spectroscopy. NMR Biomed. 2014, 27, 802–809.

    CAS  Google Scholar 

  42. Henriques Pereira, D. P.; Leethaus, J.; Beyazay, T.; Do Nascimento Vieira, A.; Kleinermanns, K.; Tüysüz, H.; Martin, W. F.; Preiner, M. Role of geochemical protoenzymes (geozymes) in primordial metabolism: Specific abiotic hydride transfer by metals to the biological redox cofactor NAD+. FEBS J. 2022, 289, 3148–3162.

    CAS  Google Scholar 

  43. Crilly, C. J.; Brom, J. A.; Kowalewski, M. E.; Piszkiewicz, S.; Pielak, G. J. Dried protein structure revealed at the residue level by liquid-observed vapor exchange NMR. Biochemistry 2021, 60, 152–159.

    CAS  Google Scholar 

  44. Jain, N.; Khanvilkar, A. N.; Sahoo, S.; Bedekar, A. V. Modification of Kagan’s amide for improved activity as chiral solvating agent in enantiodiscrimination during NMR analysis. Tetrahedron 2018, 74, 68–76.

    CAS  Google Scholar 

  45. Hagspiel, S.; Fantuzzi, F.; Arrowsmith, M.; Gärtner, A.; Fest, M.; Weiser, J.; Engels, B.; Helten, H.; Braunschweig, H. Modulation of the naked-eye and fluorescence color of a protonated boron-doped thiazolothiazole by anion-dependent hydrogen bonding. Chem.—Eur. J. 2022, 28, e202201398.

    CAS  Google Scholar 

  46. Charville, H.; Jackson, D. A.; Hodges, G.; Whiting, A.; Wilson, M. R. The uncatalyzed direct amide formation reaction-mechanism studies and the key role of carboxylic acid H-bonding. Eur. J. Org. Chem. 2011, 2011, 5981–5990.

    CAS  Google Scholar 

  47. Gopalan, A.; Ragupathy, D.; Kim, H. T.; Manesh, K. M.; Lee, K. P. Pd (core)-Au (shell) nanoparticles catalyzed conversion of NADH to NAD+ by UV—vis spectroscopy—A kinetic analysis. Spectrochim. Acta A 2009, 74, 678–684.

    CAS  Google Scholar 

  48. Dou, X. Y.; Yuan, X.; Yao, Q. F.; Luo, Z. T.; Zheng, K. Y.; Xie, J. P. Facile synthesis of water-soluble Au25−xAgx nanoclusters protected by mono- and bi-thiolate ligands. Chem. Commun. 2014, 50, 7459–7462.

    CAS  Google Scholar 

  49. Negishi, Y.; Takasugi, Y.; Sato, S.; Yao, H.; Kimura, K.; Tsukuda, T. Kinetic stabilization of growing gold clusters by passivation with thiolates. J. Phys. Chem. B 2006, 110, 12218–12221.

    CAS  Google Scholar 

  50. Zheng, K. Y.; Yuan, X.; Kuah, K.; Luo, Z. T.; Yao, Q. F.; Zhang, Q. B.; Xie, J. P. Boiling water synthesis of ultrastable thiolated silver nanoclusters with aggregation-induced emission. Chem. Commun. 2015, 51, 15165–15168.

    CAS  Google Scholar 

  51. Zheng, Y. K.; Wang, X. M.; Jiang, H. Label-free detection of Acinetobacter baumannii through the induced fluorescence quenching of thiolated AuAg nanoclusters. Sens. Actuators B 2018, 277, 388–393.

    CAS  Google Scholar 

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Acknowledgements

We acknowledge financial support from National Science Foundation of Anhui Province (No. 2108085J08), the University Synergy Innovation Program of Anhui Province (No. GXXT-2021-023), and the technical support of high-performance computing platform of Anhui University.

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Correspondence to Haizhu Yu or Manzhou Zhu.

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Chen, L., Du, Y., Lv, Y. et al. Nicotinamide adenine dinucleotide (NAD+) reduction enabled by an atomically precise Au-Ag alloy nanocluster. Nano Res. 16, 7770–7776 (2023). https://doi.org/10.1007/s12274-023-5415-6

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