Evaluation of upconverting nanoparticles towards heart theranostics
Autoři:
Marc Kermorgant aff001; Jennifer Ben Salem aff001; Julien Santelli aff003; Denis Calise aff004; Anne-Cécile Oster aff001; Olivier Lairez aff005; Christophe Coudret aff006; Marc Verelst aff007; Céline Gales aff001; Jean-Michel Sénard aff001; Francis Beaudry aff002; Anne Pavy-Le Traon aff009; Clément Roux aff006; Robert Mauricot aff003; Dina N. Arvanitis aff001
Působiště autorů:
Institut des Maladies Métaboliques et Cardiovasculaires, INSERM UMR1048, Université de Toulouse, France
aff001; Groupe de Recherche en Pharmacologie Animale du Québec (GREPAQ), Département de Biomédecine Vétérinaire, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec, Canada
aff002; CEMES-CNRS, Université de Toulouse, CNRS, France
aff003; Service Microchirurgie, Centre Régional d'Exploration Fonctionnelle et Ressources Expérimentales (CREFRE- US06, Rangueil)
aff004; Fédération des services de cardiologie, hôpital Rangueil
aff005; Laboratoire des IMRCP, Université de Toulouse, CNRS UMR 5623, Université Toulouse III—Paul Sabatier
aff006; CHROMALYS SAS, France
aff007; Service de Pharmacologie Clinique, CHU de Toulouse, Université de Toulouse, France
aff008; Département de Neurologie et Institut des Neurosciences, Université de Toulouse, France
aff009
Vyšlo v časopise:
PLoS ONE 14(12)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0225729
Souhrn
Restricted and controlled drug delivery to the heart remains a challenge giving frequent off-target effects as well as limited retention of drugs in the heart. There is a need to develop and optimize tools to allow for improved design of drug candidates for treatment of heart diseases. Over the last decade, novel drug platforms and nanomaterials were designed to confine bioactive materials to the heart. Yet, the research remains in its infancy, not only in the development of tools but also in the understanding of effects of these materials on cardiac function and tissue integrity. Upconverting nanoparticles are nanomaterials that recently accelerated interest in theranostic nanomedicine technologies. Their unique photophysical properties allow for sensitive in vivo imaging that can be combined with spatio-temporal control for targeted release of encapsulated drugs.
Here we synthesized upconverting NaYF4:Yb,Tm nanoparticles and show for the first time their innocuity in the heart, when injected in the myocardium or in the pericardial space in mice. Nanoparticle retention and upconversion in the cardiac region did not alter heart rate variability, nor cardiac function as determined over a 15-day time course ensuing the sole injection. Altogether, our nanoparticles show innocuity primarily in the pericardial region and can be safely used for controlled spatiotemporal drug delivery. Our results support the use of upconverting nanoparticles as potential theranostics tools overcoming some of the key limitations associated with conventional experimental cardiology.
Klíčová slova:
Electrocardiography – Lasers – Nanoparticles – Cardiovascular physiology – Drug delivery – Myocardium – Pericardium
Zdroje
1. Roth GA, Johnson C, Abajobir A, Abd-Allah F, Abera SF, Abyu G, et al. Global, regional, and national burden of cardiovascular diseases for 10 causes, 1990 to 2015. J Am Coll Cardiol. 2017;70: 1–25. doi: 10.1016/j.jacc.2017.04.052 28527533
2. Cahill TJ, Kharbanda RK. Heart failure after myocardial infarction in the era of primary percutaneous coronary intervention: Mechanisms, incidence and identification of patients at risk. World J Cardiol. 2017;9: 407. doi: 10.4330/wjc.v9.i5.407 28603587
3. Rider P, Carmi Y, Cohen I. Biologics for Targeting Inflammatory Cytokines, Clinical Uses, and Limitations. Int J Cell Biol. 2016;2016: 9259646. doi: 10.1155/2016/9259646 28083070
4. Rebouças J de S, Santos-Magalhães NS, Formiga FR. Cardiac Regeneration using Growth Factors: Advances and Challenges. Arq Bras Cardiol. 2016;107: 271–275. doi: 10.5935/abc.20160097 27355588
5. Hastings CL, Roche ET, Ruiz-Hernandez E, Schenke-Layland K, Walsh CJ, Duffy GP. Drug and cell delivery for cardiac regeneration. Adv Drug Deliv Rev. 2015;84: 85–106. doi: 10.1016/j.addr.2014.08.006 25172834
6. Venugopal JR, Prabhakaran MP, Mukherjee S, Ravichandran R, Dan K, Ramakrishna S. Biomaterial strategies for alleviation of myocardial infarction. J R Soc Interface. 2012;9: 1–19. doi: 10.1098/rsif.2011.0301 21900319
7. Han S, Hwang C. Pericardial approach for cardiac therapies: old practice with new ideas. Korean Circ J. 2010;40: 479–488. doi: 10.4070/kcj.2010.40.10.479 21088750
8. Chen X, Gambhir SS, Cheon J. Theranostic nanomedicine. Acc Chem Res. 2011;44: 841–841. doi: 10.1021/ar200231d 22004477
9. Dong H, Du S-R, Zheng X-Y, Lyu G-M, Sun L-D, Li L-D, et al. Lanthanide nanoparticles: from design toward bioimaging and therapy. Chem Rev. 2015;115: 10725–10815. doi: 10.1021/acs.chemrev.5b00091 26151155
10. Dong H, Sun L-D, Yan C-H. Energy transfer in lanthanide upconversion studies for extended optical applications. Chem Soc Rev. 2015;44: 1608–1634. doi: 10.1039/c4cs00188e 25242465
11. Ximendes EC, Santos WQ, Rocha U, Kagola UK, Sanz-Rodríguez F, Fernández N, et al. Unveiling in vivo subcutaneous thermal dynamics by infrared luminescent nanothermometers. Nano Lett. 2016;16: 1695–1703. doi: 10.1021/acs.nanolett.5b04611 26845418
12. Park YI, Lee KT, Suh YD, Hyeon T. Upconverting nanoparticles: a versatile platform for wide-field two-photon microscopy and multi-modal in vivo imaging. Chem Soc Rev. 2015;44: 1302–1317. doi: 10.1039/c4cs00173g 25042637
13. Liu Q, Sun Y, Yang T, Feng W, Li C, Li F. Sub-10 nm hexagonal lanthanide-doped NaLuF4 upconversion nanocrystals for sensitive bioimaging in vivo. J Am Chem Soc. 2011;133: 17122–17125. doi: 10.1021/ja207078s 21957992
14. Chen G, Shen J, Ohulchanskyy TY, Patel NJ, Kutikov A, Li Z, et al. (α-NaYbF4: Tm3+)/CaF2 core/shell nanoparticles with efficient near-infrared to near-infrared upconversion for high-contrast deep tissue bioimaging. ACS Nano. 2012;6: 8280–8287. doi: 10.1021/nn302972r 22928629
15. Hilderbrand SA, Weissleder R. Near-infrared fluorescence: application to in vivo molecular imaging. Curr Opin Chem Biol. 2010;14: 71–79. doi: 10.1016/j.cbpa.2009.09.029 19879798
16. Naczynski DJ, Tan MC, Zevon M, Wall B, Kohl J, Kulesa A, et al. Rare-earth-doped biological composites as in vivo shortwave infrared reporters. Nat Commun. 2013;4: 2199. doi: 10.1038/ncomms3199 23873342
17. Sedlmeier A, Gorris HH. Surface modification and characterization of photon-upconverting nanoparticles for bioanalytical applications. Chem Soc Rev. 2015;44: 1526–1560. doi: 10.1039/c4cs00186a 25176175
18. Chen G, Qiu H, Prasad PN, Chen X. Upconversion nanoparticles: design, nanochemistry, and applications in theranostics. Chem Rev. 2014;114: 5161–5214. doi: 10.1021/cr400425h 24605868
19. Tian G, Zheng X, Zhang X, Yin W, Yu J, Wang D, et al. TPGS-stabilized NaYbF4: Er upconversion nanoparticles for dual-modal fluorescent/CT imaging and anticancer drug delivery to overcome multi-drug resistance. Biomaterials. 2015;40: 107–116. doi: 10.1016/j.biomaterials.2014.11.022 25433607
20. Chen S, Weitemier AZ, Zeng X, He L, Wang X, Tao Y, et al. Near-infrared deep brain stimulation via upconversion nanoparticle-mediated optogenetics. Science. 2018;359: 679–684. doi: 10.1126/science.aaq1144 29439241
21. Mudshinge SR, Deore AB, Patil S, Bhalgat CM. Nanoparticles: Emerging carriers for drug delivery. Saudi Pharm J. 2011;19: 129–141. doi: 10.1016/j.jsps.2011.04.001 23960751
22. Rizvi SAA, Saleh AM. Applications of nanoparticle systems in drug delivery technology. Saudi Pharm J. 2018;26: 64–70. doi: 10.1016/j.jsps.2017.10.012 29379334
23. Dvir T, Bauer M, Schroeder A, Tsui JH, Anderson DG, Langer R, et al. Nanoparticles targeting the infarcted heart. Nano Lett. 2011;11: 4411–4414. doi: 10.1021/nl2025882 21899318
24. Cheraghi M, Negahdari B, Daraee H, Eatemadi A. Heart targeted nanoliposomal/nanoparticles drug delivery: An updated review. Biomed Pharmacother. 2017;86: 316–323. doi: 10.1016/j.biopha.2016.12.009 28011379
25. Passaro F, Testa G, Ambrosone L, Costagliola C, Tocchetti CG, Di Nezza F, et al. Nanotechnology-Based Cardiac Targeting and Direct Cardiac Reprogramming: The Betrothed. Stem Cells Int. 2017;2017.
26. Li Z, Zhang Y. An efficient and user-friendly method for the synthesis of hexagonal-phase NaYF4: Yb, Er/Tm nanocrystals with controllable shape and upconversion fluorescence. Nanotechnology. 2008;19: 345606. doi: 10.1088/0957-4484/19/34/345606 21730655
27. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation. 1996;93: 1043–1065. 8598068
28. Li F, Silva MD, Sotak CH, Fisher M. Temporal evolution of ischemic injury evaluated with diffusion-, perfusion-, and T2-weighted MRI. Neurology. 2000;54: 689–689. doi: 10.1212/wnl.54.3.689 10680805
29. Xiong L, Yang T, Yang Y, Xu C, Li F. Long-term in vivo biodistribution imaging and toxicity of polyacrylic acid-coated upconversion nanophosphors. Biomaterials. 2010;31: 7078–7085. doi: 10.1016/j.biomaterials.2010.05.065 20619791
30. Owens III DE, Peppas NA. Opsonization, biodistribution, and pharmacokinetics of polymeric nanoparticles. Int J Pharm. 2006;307: 93–102. doi: 10.1016/j.ijpharm.2005.10.010 16303268
31. Grossman PM, Han Z, Palasis M, Barry JJ, Lederman RJ. Incomplete retention after direct myocardial injection. Catheter Cardiovasc Interv. 2002;55: 392–397. doi: 10.1002/ccd.10136 11870950
32. Stansfield WE, Rojas M, Corn D, Willis M, Patterson C, Smyth SS, et al. Characterization of a model to independently study regression of ventricular hypertrophy. J Surg Res. 2007;142: 387–393. doi: 10.1016/j.jss.2007.01.037 17574596
33. Bonios M, Terrovitis J, Chang CY, Engles JM, Higuchi T, Lautamäki R, et al. Myocardial substrate and route of administration determine acute cardiac retention and lung bio-distribution of cardiosphere-derived cells. J Nucl Cardiol. 2011;18: 443. doi: 10.1007/s12350-011-9369-9 21448759
34. Jahangirian H, Lemraski EG, Webster TJ, Rafiee-Moghaddam R, Abdollahi Y. A review of drug delivery systems based on nanotechnology and green chemistry: green nanomedicine. Int J Nanomedicine. 2017;12: 2957. doi: 10.2147/IJN.S127683 28442906
35. Nakatani T, Shinohara H, Fukuo Y, Morisawa S, Matsuda T. Pericardium of rodents: pores connect the pericardial and pleural cavities. Anat Rec. 1988;220: 132–137. doi: 10.1002/ar.1092200204 3354856
36. Segura-Ibarra V, Cara FE, Wu S, Iruegas-Nunez DA, Wang S, Ferrari M, et al. Nanoparticles administered intrapericardially enhance payload myocardial distribution and retention. J Control Release Off J Control Release Soc. 2017;262: 18–27. doi: 10.1016/j.jconrel.2017.07.012 28700900
37. Longmire M, Choyke PL, Kobayashi H. Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomed. 2008;3: 703–717. doi: 10.2217/17435889.3.5.703 18817471
38. Arami H, Khandhar A, Liggitt D, Krishnan KM. In vivo delivery, pharmacokinetics, biodistribution and toxicity of iron oxide nanoparticles. Chem Soc Rev. 2015;44: 8576–8607. doi: 10.1039/c5cs00541h 26390044
39. Blanco E, Shen H, Ferrari M. Principles of nanoparticle design for overcoming biological barriers to drug delivery. Nat Biotechnol. 2015;33: 941. doi: 10.1038/nbt.3330 26348965
40. Bansal D, Khan M, Salhan AK. A review of measurement and analysis of heart rate variability. Computer and Automation Engineering, 2009 ICCAE’09 International Conference on. IEEE; 2009. pp. 243–246.
41. Véra P, Gardin I, Bok B. Comparative study of three automatic programs of left ventricular ejection fraction evaluation. Nucl Med Commun. 1995;16: 667–674. doi: 10.1097/00006231-199508000-00008 7491179
42. ChuDuc H, NguyenPhan K, NguyenViet D. A Review of Heart Rate Variability and its Applications. APCBEE Procedia. 2013;7: 80–85. doi: 10.1016/j.apcbee.2013.08.016
43. Lee G, Park YI. Lanthanide-Doped Upconversion Nanocarriers for Drug and Gene Delivery. Nanomaterials. 2018;8: 511. doi: 10.3390/nano8070511 29987223
Článok vyšiel v časopise
PLOS One
2019 Číslo 12
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Masturbační chování žen v ČR − dotazníková studie
- Nejasný stín na plicích – kazuistika
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Somatizace stresu – typické projevy a možnosti řešení
Najčítanejšie v tomto čísle
- Methylsulfonylmethane increases osteogenesis and regulates the mineralization of the matrix by transglutaminase 2 in SHED cells
- Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay
- The characteristic of patulous eustachian tube patients diagnosed by the JOS diagnostic criteria
- Parametric CAD modeling for open source scientific hardware: Comparing OpenSCAD and FreeCAD Python scripts