Infrared fluorescence imaging of infarcted hearts with Ag2S nanodots
)
Download citation
640
Views
29
Downloads
36
Crossref
N/A
WoS
38
Scopus
3
CSCD
Ag2S nanodots have already been demonstrated as promising near-infrared (NIR-Ⅱ, 1.0–1.45 μm) emitting nanoprobes with low toxicity, high penetration and high resolution for in vivo imaging of, for example, tumors and vasculature. In this work, we have systematically investigated the potential application of functionalized Ag2S nanodots for accurate imaging of damaged myocardium tissues after a myocardial infarction induced by either partial or global ischemia. Ag2S nanodots surface-functionalized with the angiotensin Ⅱ peptide (ATⅡ) have shown over 10-fold enhanced binding efficiency to damaged tissues than non-specifically (PEG) functionalized Ag2S nanodots due to their interaction with the upregulated angiotensin Ⅱ receptor type Ⅰ (AT1R). It is demonstrated how the NIR-Ⅱ images generated by ATⅡ-functionalized Ag2S nanodots contain valuable information about the location and extension of damaged tissue in the myocardium allowing for a proper identification of the occluded artery as well as an indirect evaluation of the damage level. The potential application of Ag2S nanodots in the near future for in vivo imaging of myocardial infarction was also corroborated by performing proof of concept whole body imaging experiments.
menu
Infrared fluorescence imaging of infarcted hearts with Ag2S nanodots
)
Abstract
Ag2S nanodots have already been demonstrated as promising near-infrared (NIR-Ⅱ, 1.0–1.45 μm) emitting nanoprobes with low toxicity, high penetration and high resolution for in vivo imaging of, for example, tumors and vasculature. In this work, we have systematically investigated the potential application of functionalized Ag2S nanodots for accurate imaging of damaged myocardium tissues after a myocardial infarction induced by either partial or global ischemia. Ag2S nanodots surface-functionalized with the angiotensin Ⅱ peptide (ATⅡ) have shown over 10-fold enhanced binding efficiency to damaged tissues than non-specifically (PEG) functionalized Ag2S nanodots due to their interaction with the upregulated angiotensin Ⅱ receptor type Ⅰ (AT1R). It is demonstrated how the NIR-Ⅱ images generated by ATⅡ-functionalized Ag2S nanodots contain valuable information about the location and extension of damaged tissue in the myocardium allowing for a proper identification of the occluded artery as well as an indirect evaluation of the damage level. The potential application of Ag2S nanodots in the near future for in vivo imaging of myocardial infarction was also corroborated by performing proof of concept whole body imaging experiments.
References(60)
WHO; World Heart Federation; World Stroke Organization. Global Atlas on Cardiovascular Disease Prevention and Control; World Health Organization in Collaboration with the World Heart Federation and the World Stroke Organization: Geneva, 2011; p 155.
Luengo-Fernández, R.; Leal, J.; Gray, A.; Petersen, S.; Rayner, M. Cost of cardiovascular diseases in the United Kingdom. Heart 2006, 92, 1384-1389.
Mahmoudi, M.; Yu, M.; Serpooshan, V.; Wu, J. C.; Langer, R.; Lee, R. T.; Karp, J. M.; Farokhzad, O. C. Multiscale technologies for treatment of ischemic cardiomyopathy. Nat. Nanotechnol. 2017, 12, 845-855.
Ximendes, E. C.; Rocha, U.; del Rosal, B.; Vaquero, A.; Sanz-Rodríguez, F.; Monge, L.; Ren, F. Q.; Vetrone, F.; Ma, D. L.; García-Solé, J. et al. In vivo ischemia detection by luminescent nanothermometers. Adv. Health. Mater. 2017, 6, 1601195.
Ruvinov, E.; Dvir, T.; Leor, J.; Cohen, S. Myocardial repair: From salvage to tissue reconstruction. Expert Rev. Cardiovasc. Ther. 2008, 6, 669-686.
Flachskampf, F. A.; Schmid, M.; Rost, C.; Achenbach, S.; DeMaria, A. N.; Daniel, W. G. Cardiac imaging after myocardial infarction. Eur. Heart J. 2011, 32, 272-283.
Mulder, W. J.; Griffioen, A. W.; Strijkers, G. J.; Cormode, D. P.; Nicolay, K.; Fayad, Z. A. Magnetic and fluorescent nanoparticles for multimodality imaging. Nanomedicine 2007, 2, 307-324.
Lozano, O.; Torres-Quintanilla, A.; García-Rivas, G. Nanomedicine for the cardiac myocyte: Where are we? J. Control. Release 2018, 271, 149-165.
Hu, J.; Ortgies, D. H.; Martín Rodríguez, E.; Rivero, F.; Aguilar Torres, R.; Alfonso, F.; Fernández, N.; Carreño-Tarragona, G.; Monge, L.; Sanz-Rodriguez, F. et al. Optical nanoparticles for cardiovascular imaging. Adv. Opt. Mater. 2018, 6, 1800626.
Dvir, T.; Bauer, M.; Schroeder, A.; Tsui, J. H.; Anderson, D. G.; Langer, R.; Liao, R.; Kohane, D. S. Nanoparticles targeting the infarcted heart. Nano Lett. 2011, 11, 4411-4414.
Jiang, W. S.; Rutherford, D.; Vuong, T.; Liu, H. N. Nanomaterials for treating cardiovascular diseases: A review. Bioact. Mater. 2017, 2, 185-198.
Stendahl, J. C.; Sinusas, A. J. Nanoparticles for cardiovascular imaging and therapeutic delivery, Part 1: Compositions and features. J. Nucl. Med. 2015, 56, 1469-1475.
Sharma, R.; Kwon, S. New applications of nanoparticles in cardiovascular imaging. J. Exp. Nanosci. 2007, 2, 115-126.
Taillefer, R.; Tamaki, N. New Radiotracers in Cardiac Imaging: Principles and Applications; Appleton & Lange: Stamford, Connecticut, 1999.
Sosnovik, D. E.; Schellenberger, E. A.; Nahrendorf, M.; Novikov, M. S.; Matsui, T.; Dai, G.; Reynolds, F.; Grazette, L.; Rosenzweig, A.; Weissleder, R. et al. Magnetic resonance imaging of cardiomyocyte apoptosis with a novel magneto-optical nanoparticle. Magn. Reson. Med. 2005, 54, 718-724.
Ruan, S. B.; Wan, J. Y.; Fu, Y.; Han, K.; Li, X.; Chen, J. T.; Zhang, Q. Y.; Shen, S.; He, Q.; Gao, H. L. PEGylated fluorescent carbon nanoparticles for noninvasive heart imaging. Bioconjug. Chem. 2014, 25, 1061-1068.
Lundy, D. J.; Chen, K. H.; Toh, E. K. W.; Hsieh, P. C. H. Distribution of systemically administered nanoparticles reveals a size-dependent effect immediately following cardiac ischaemia-reperfusion injury. Sci. Rep. 2016, 6, 25613.
Lipinski, M. J.; Albelda, M. T.; Frias, J. C.; Anderson, S. A.; Luger, D.; Westman, P. C.; Escarcega, R. O.; Hellinga, D. G.; Waksman, R.; Arai, A. E. et al. Multimodality imaging demonstrates trafficking of liposomes preferentially to ischemic myocardium. Cardiovasc. Revasc. Med. 2016, 17, 106-112.
Sosnovik, D. E.; Nahrendorf, M.; Deliolanis, N.; Novikov, M.; Aikawa, E.; Josephson, L.; Rosenzweig, A.; Weissleder, R.; Ntziachristos, V. Fluorescence tomography and magnetic resonance imaging of myocardial macrophage infiltration in infarcted myocardium in vivo. Circulation 2007, 115, 1384-1391.
Nahrendorf, M.; Sosnovik, D. E.; Waterman, P.; Swirski, F. K.; Pande, A. N.; Aikawa, E.; Figueiredo, J. L.; Pittet, M. J.; Weissleder, R. Dual channel optical tomographic imaging of leukocyte recruitment and protease activity in the healing myocardial infarct. Circ. Res. 2007, 100, 1218-1225.
Ferreira, M. P. A.; Ranjan, S.; Kinnunen, S.; Correia, A.; Talman, V.; Mäkilä, E.; Barrios-Lopez, B.; Kemell, M.; Balasubramanian, V.; Salonen, J. et al. Drug-loaded multifunctional nanoparticles targeted to the endocardial layer of the injured heart modulate hypertrophic signaling. Small 2017, 13, 1701276.
Sosnovik, D. E.; Garanger, E.; Aikawa, E.; Nahrendorf, M.; Figuiredo, J. L.; Dai, G. P.; Reynolds, F.; Rosenzweig, A.; Weissleder, R.; Josephson, L. Molecular MRI of cardiomyocyte apoptosis with simultaneous delayed-enhancement MRI distinguishes apoptotic and necrotic myocytes in vivo: Potential for midmyocardial salvage in acute ischemia. Circ. Cardiovasc. Imaging 2009, 2, 460-467.
Bashkatov, A. N.; Genina, E. A.; Tuchin, V. V. Optical properties of skin, subcutaneous, and muscle tissues: A review. J. Innov. Opt. Health Sci. 2011, 4, 9-38.
Smith, A. M.; Mancini, M. C.; Nie, S. M. Second window for in vivo imaging. Nat. Nanotechnol. 2009, 4, 710-711.
Jaque, D.; Richard, C.; Viana, B.; Soga, K.; Liu, X. G.; García Solé, J. Inorganic nanoparticles for optical bioimaging. Adv. Opt. Photonics 2016, 8, 1-103.
Welsher, K.; Sherlock, S. P.; Dai, H. J. Deep-tissue anatomical imaging of mice using carbon nanotube fluorophores in the second near-infrared window. Proc. Natl. Acad. Sci. USA 2011, 108, 8943-8948.
Villa, I.; Vedda, A.; Cantarelli, I. X.; Pedroni, M.; Piccinelli, F.; Bettinelli, M.; Speghini, A.; Quintanilla, M.; Vetrone, F.; Rocha, U. et al. 1.3 μm emitting SrF2: Nd3+ nanoparticles for high contrast in vivo imaging in the second biological window. Nano Res. 2015, 8, 649-665.
del Rosal, B.; Villa, I.; Jaque, D.; Sanz-Rodríguez, F. In vivo autofluorescence in the biological windows: The role of pigmentation. J. Biophotonics 2016, 9, 1059-1067.
Zhang, Y. J.; Liu, Y. S.; Li, C. Y.; Chen, X. Y.; Wang, Q. B. Controlled synthesis of Ag2S quantum dots and experimental determination of the exciton Bohr radius. J. Phys. Chem. C 2014, 118, 4918-4923.
Sadovnikov, S. I.; Gusev, A. I. Recent progress in nanostructured silver sulfide: From synthesis and nonstoichiometry to properties. J. Mater. Chem. A 2017, 5, 17676-17704.
Hu, F.; Li, C. Y.; Zhang, Y. J.; Wang, M.; Wu, D. M.; Wang, Q. B. Real-time in vivo visualization of tumor therapy by a near-infrared-Ⅱ Ag2S quantum dot-based theranostic nanoplatform. Nano Res. 2015, 8, 1637-1647.
Kubie, L.; King, L. A.; Kern, M. E.; Murphy, J. R.; Kattel, S.; Yang, Q.; Stecher, J. T.; Rice, W. D.; Parkinson, B. A. Synthesis and characterization of ultrathin silver sulfide nanoplatelets. ACS Nano 2017, 11, 8471-8477.
Li, C. Y.; Li, F.; Zhang, Y. J.; Zhang, W. J.; Zhang, X. E.; Wang, Q. B. Real-time monitoring surface chemistry-dependent in vivo behaviors of protein nanocages via encapsulating an NIR-Ⅱ Ag2S quantum dot. ACS Nano 2015, 9, 12255-12263.
Zhang, Y.; Hong, G. S.; Zhang, Y. J.; Chen, G. C.; Li, F.; Dai, H. J.; Wang, Q. B. Ag2S Quantum dot: A bright and biocompatible fluorescent nanoprobe in the second near-infrared window. ACS Nano 2012, 6, 3695-3702.
Hong, G. S.; Robinson, J. T.; Zhang, Y. J.; Diao, S.; Antaris, A. L.; Wang, Q. B.; Dai, H. J. In vivo fluorescence imaging with Ag2S quantum dots in the second near-infrared region. Angew. Chem. , Int. Ed. 2012, 51, 9818-9821.
Wu, C. X.; Zhang, Y. J.; Li, Z.; Li, C. Y.; Wang, Q. B. A novel photoacoustic nanoprobe of ICG@PEG-Ag2S for atherosclerosis targeting and imaging in vivo. Nanoscale 2016, 8, 12531-12539.
Zhang, Y.; Zhang, Y. J.; Hong, G. S.; He, W.; Zhou, K.; Yang, K.; Li, F.; Chen, G. C.; Liu, Z.; Dai, H. J. et al. Biodistribution, pharmacokinetics and toxicology of Ag2S near-infrared quantum dots in mice. Biomaterials 2013, 34, 3639-3646.
Li, C. Y.; Zhang, Y. J.; Wang, M.; Zhang, Y.; Chen, G. C.; Li, L.; Wu, D. M.; Wang, Q. B. In vivo real-time visualization of tissue blood flow and angiogenesis using Ag2S quantum dots in the NIR-Ⅱ window. Biomaterials 2014, 35, 393-400.
Santos, H. D. A.; Ruiz, D.; Lifante, G.; Jacinto, C.; Juarez, B. H.; Jaque, D. Time resolved spectroscopy of infrared emitting Ag2S nanocrystals for subcutaneous thermometry. Nanoscale 2017, 9, 2505-2513.
Santos, H. D. A.; Ximendes, E. C.; del Carmen Iglesias-de la Cruz, M.; Chaves-Coira, I.; del Rosal, B.; Jacinto, C.; Monge, L.; Rubia-Rodríguez, I.; Ortega, D.; Mateos, S. et al. In vivo early tumor detection and diagnosis by infrared luminescence transient nanothermometry. Adv. Funct. Mater. 2018, 28, 1803924.
Chang, P. J.; Cheng, H. Y.; Lin, W. W.; Li, X. R.; Zhao, F. Y. A stable and active AgxS crystal preparation and its performance as photocatalyst. Chin. J. Catal. 2015, 36, 564-571.
Yang, T.; Tang, Y. A.; Liu, L.; Lv, X. Y.; Wang, Q. L.; Ke, H. T.; Deng, Y. B.; Yang, H.; Yang, X. L.; Liu, G. et al. Size-dependent Ag2S nanodots for second near-infrared fluorescence/photoacoustics imaging and simultaneous photothermal therapy. ACS Nano 2017, 11, 1848-1857.
Hong, G. S.; Lee, J. C.; Jha, A.; Diao, S.; Nakayama, K. H.; Hou, L. Q.; Doyle, T. C.; Robinson, J. T.; Antaris, A. L.; Dai, H. J. et al. Near-infrared Ⅱ fluorescence for imaging hindlimb vessel regeneration with dynamic tissue perfusion measurement. Circ. Cardiovasc. Imaging 2014, 7, 517-525.
Hennig, R.; Pollinger, K.; Tessmar, J.; Goepferich, A. Multivalent targeting of AT1 receptors with angiotensin Ⅱ-functionalized nanoparticles. J. Drug Target. 2015, 23, 681-689.
Molavi, B.; Chen, J. W.; Mehta, J. L. Cardioprotective effects of rosiglitazone are associated with selective overexpression of type 2 angiotensin receptors and inhibition of p42/44 MAPK. Am. J. Physiol. Heart. Circ. Physiol. 2006, 291, H687-H693.
Nio, Y.; Matsubara, H.; Murasawa, S.; Kanasaki, M.; Inada, M. Regulation of gene transcription of angiotensin Ⅱ receptor subtypes in myocardial infarction. J. Clin. Invest. 1995, 95, 46-54.
Busche, S.; Gallinat, S.; Bohle, R. M.; Reinecke, A.; Seebeck, J.; Franke, F.; Fink, L.; Zhu, M. Y.; Sumners, C.; Unger, T. Expression of angiotensin AT1 and AT2 receptors in adult rat cardiomyocytes after myocardial infarction: A single-cell reverse transcriptase-polymerase chain reaction study. Am. J. Pathol. 2000, 157, 605-611.
Bell, R. M.; Mocanu, M. M.; Yellon, D. M. Retrograde heart perfusion: The Langendorff technique of isolated heart perfusion. J. Mol. Cell. Cardiol. 2011, 50, 940-950.
Ostadal, B.; Netuka, I.; Maly, J.; Besik, J.; Ostadalova, I. Gender differences in cardiac ischemic injury and protection-experimental aspects. Exp. Biol. Med. 2009, 234, 1011-1019.
Jeong, S.; Jung, Y.; Bok, S.; Ryu, Y. M.; Lee, S.; Kim, Y. E.; Song, J.; Kim, M.; Kim, S. Y.; Ahn, G. O. et al. Multiplexed in vivo imaging using size-controlled quantum dots in the second near-infrared window. Adv. Health. Mater. 2018, 7, 1800695.
Benayas, A.; Ren, F. Q.; Carrasco, E.; Marzal, V.; del Rosal, B.; Gonfa, B. A.; Juarranz, Á.; Sanz-Rodríguez, F.; Jaque, D.; García-Solé, J. et al. PbS/CdS/ZnS quantum dots: A multifunctional platform for in vivo near-infrared low-dose fluorescence imaging. Adv. Funct. Mater. 2015, 25, 6650-6659.
Robinson, J. T.; Hong, G. S.; Liang, Y. Y.; Zhang, B.; Yaghi, O. K.; Dai, H. J. In vivo fluorescence imaging in the second near-infrared window with long circulating carbon nanotubes capable of ultrahigh tumor uptake. J. Am. Chem. Soc. 2012, 134, 10664-10669.
Bhavane, R.; Starosolski, Z.; Stupin, I.; Ghaghada, K. B.; Annapragada, A. NIR-Ⅱ fluorescence imaging using indocyanine green nanoparticles. Sci. Rep. 2018, 8, 14455.
Carr, J. A.; Franke, D.; Caram, J. R.; Perkinson, C. F.; Saif, M.; Askoxylakis, V.; Datta, M.; Fukumura, D.; Jain, R. K.; Bawendi, M. G. et al. Shortwave infrared fluorescence imaging with the clinically approved near-infrared dye indocyanine green. Proc. Natl. Acad. Sci. USA 2018, 115, 4465-4470.
Ortgies, D. H.; Tan, M. L.; Ximendes, E. C.; del Rosal, B.; Hu, J.; Xu, L.; Wang, X. D.; Martín Rodríguez, E.; Jacinto, C.; Fernandez, N. et al. Lifetime-encoded infrared-emitting nanoparticles for in vivo multiplexed imaging. ACS Nano 2018, 12, 4362-4368.
Yang, B. C.; Li, D. Y.; Phillips, M. I.; Mehta, P.; Mehta, J. L. Myocardial angiotensin Ⅱ receptor expression and ischemia-reperfusion injury. Vasc. Med. 1998, 3, 121-130.
Anversa, P.; Leri, A.; Li, B. S.; Liu, Y.; Di Somma, S.; Kajstura, J. Ischemic cardiomyopathy and the cellular renin-angiotensin system. J. Heart Lung Transplant. 2000, 19, S1-S11.
Sato, M.; Engelman, R. M.; Otani, H.; Maulik, N.; Rousou, J. A.; Flack Ⅲ, J. E.; Deaton, D. W.; Das, D. K. Myocardial protection by preconditioning of heart with losartan, an angiotensin Ⅱ type 1-receptor blocker: Implication of bradykinin-dependent and bradykinin-independent mechanisms. Circulation 2000, 102, Ⅲ346-Ⅲ351.
Greish, K. Enhanced permeability and retention (EPR) effect for anticancer nanomedicine drug targeting. In Cancer Nanotechnology: Methods and Protocols; Grobmyer, S. R.; Moudgil, B. M., Eds.; Humana Press: Totowa, NJ, USA, 2010.
Wang, L. V.; Hu, S. Photoacoustic tomography: In vivo imaging from organelles to organs. Science 2012, 335, 1458-1462.
Publication history
Copyright
Acknowledgements
This work was partially supported by the Ministerio de Economía y Competitividad de España (MAT2016-75362-C3-1-R) and (MAT2017-83111R), by the Instituto de Salud Carlos Ⅲ (PI16/ 00812), by the Comunidad Autónoma de Madrid (B2017/BMD-3867RENIMCM), and co-financed by the European Structural and investment fond. Additional funding was provided by the European Commission Horizon 2020 project NanoTBTech, the Fundación para la Investigación Biomédica del Hospital Universitario Ramón y Cajal project IMP18_38 (2018/0265), and also by COST action CM1403. D. H. O. is grateful to the Instituto de Salud Carlos Ⅲ for a Sara Borrell scholarship (No. CD17/00210).
FEEDBACK 
TOP