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Research Article

Nanoscale chemical imaging of individual chemotherapeutic cytarabine-loaded liposomal nanocarriers

Karin Wieland1Georg Ramer2,3Victor U. Weiss4Guenter Allmaier4Bernhard Lendl1Andrea Centrone2( )
Institute of Chemical Technologies and Analytics, Research Division Environmental,Process Analytics and Sensors,TU Wien, Vienna,1060,Austria;
Center for Nanoscale Science and Technology,National Institute of Standards and Technology,Gaithersburg, MD,20899,USA;
Institute for Research in Electronics and Applied Physics,University of Maryland,College Park, MD,20742,USA;
Institute of Chemical Technologies and Analytics,Research Division Instrumental and Imaging Analytical Chemistry,TU Wien, Vienna,1060,Austria;
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Abstract

Dosage of chemotherapeutic drugs is a tradeoff between efficacy and side-effects. Liposomes are nanocarriers that increase therapy efficacy and minimize side-effects by delivering otherwise difficult to administer therapeutics with improved efficiency and selectivity. Still, variabilities in liposome preparation require assessing drug encapsulation efficiency at the single liposome level, an information that, for non-fluorescent therapeutic cargos, is inaccessible due to the minute drug load per liposome. Photothermal induced resonance (PTIR) provides nanoscale compositional specificity, up to now, by leveraging an atomic force microscope (AFM) tip contacting the sample to transduce the sampleos photothermal expansion. However, on soft samples (e.g., liposomes) PTIR effectiveness is reduced due to the likelihood of tip-induced sample damage and inefficient AFM transduction. Here, individual liposomes loaded with the chemotherapeutic drug cytarabine are deposited intact from suspension via nano-electrospray gas-phase electrophoretic mobility molecular analysis (nES-GEMMA) collection and characterized at the nanoscale with the chemically-sensitive PTIR method. A new tapping-mode PTIR imaging paradigm based on heterodyne detection is shown to be better adapted to measure soft samples, yielding cytarabine distribution in individual liposomes and enabling classification of empty and drug-loaded liposomes. The measurements highlight PTIR capability to detect ~ 10 cytarabine molecules (~ 1.7 zmol) label-free and non-destructively.

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References

1

Boisselier, E.; Astruc, D. Gold nanoparticles in nanomedicine: Preparations, imaging, diagnostics, therapies and toxicity. Chem. Soc. Rev. 2009, 38, 1759-1782.

2

Ding, J.; Liang, T.; Zhou, Y.; He, Z.; Min, Q.; Jiang, L.; Zhu, J. Hyaluronidase-triggered anticancer drug and siRNA delivery from cascaded targeting nanoparticles for drug-resistant breast cancer therapy. Nano Res. 2017, 10, 690-703.

3

Von Maltzahn, G.; Park, J. H.; Lin, K. Y.; Singh, N.; Schwöppe, C.; Mesters, R.; Berdel, W. E.; Ruoslahti, E.; Sailor, M. J.; Bhatia, S. N. Nanoparticles that communicate in vivo to amplify tumour targeting. Nat. Mater. 2011, 10, 545-552.

4

Lee, D. E.; Koo, H.; Sun, I. C.; Ryu, J. H.; Kim, K.; Kwon, I. C. Multifunctional nanoparticles for multimodal imaging and theragnosis. Chem. Soc. Rev. 2012, 41, 2656-2672.

5

Thakor, A. S.; Gambhir, S. S. Nanooncology: The future of cancer diagnosis and therapy. CA: A Cancer J. Clin. 2013, 63, 395-418.

6

Senapati, S.; Mahanta, A. K.; Kumar, S.; Maiti, P. Controlled drug delivery vehicles for cancer treatment and their performance. Signal Transduct. Target. Ther. 2018, 3, 7.

7

Lammers, T.; Hennink, W. E.; Storm, G. Tumour-targeted nanomedicines: Principles and practice. Br. J. Cancer 2008, 99, 392-397.

8

Peer, D.; Karp, J. M.; Hong, S.; Farokhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2007, 2, 751-760.

9

Torchilin, V. P. Recent advances with liposomes as pharmaceutical carriers. Nat. Rev. Drug Discov. 2005, 4, 145-160.

10

Morton, S. W.; Lee, M. J.; Deng, Z. J.; Dreaden, E. C.; Siouve, E.; Shopsowitz, K. E.; Shah, N. J.; Yaffe, M. B.; Hammond, P. T. A nanoparticle-based combination chemotherapy delivery system for enhanced tumor killing by dynamic rewiring of signaling pathways. Sci. Signal. 2014, 7, ra44.

11

Zhang, Y.; Chan, H. F.; Leong, K. W. Advanced materials and processing for drug delivery: The past and the future. Adv. Drug Deliv. Rev. 2013, 65, 104-120.

12

Venditto, V. J.; Szoka Jr, F. C. Cancer nanomedicines: So many papers and so few drugs! Adv. Drug Deliv. Rev. 2013, 65, 80-88.

13

Allen, T. M.; Cullis, P. R. Liposomal drug delivery systems: From concept to clinical applications. Adv. Drug Deliv. Rev. 2013, 65, 36-48.

14

Sercombe, L.; Veerati, T.; Moheimani, F.; Wu, S. Y.; Sood, A. K.; Hua, S. S. Advances and challenges of liposome assisted drug delivery. Front. Pharmacol. 2015, 6, 286.

15

Young, S. A.; Smith, T. K. Lipids and liposomes in the enhancement of health and treatment of disease. In Drug Discovery and Development-From Molecules to Medicine; Vallisuta, O.; Olimat, S., Eds.; InTech: Croatia, 2015; pp 133-162.

16

Bozzuto, G.; Molinari, A. Liposomes as nanomedical devices. Int. J. Nanomedicine 2015, 10, 975-999.

17

de Araújo Lopes, S. C.; dos Santos Giuberti, C.; Rocha, T. G. R.; dos Santos Ferreira, D.; Leite, E. A.; Oliveira, M. C. Liposomes as carriers of anticancer drugs. In Cancer Treatment-Conventional and Innovative Approaches; Rangel, L., Ed.; InTech: Rijeka, 2013; pp 85-124.

18

Çağdaş, M.; Sezer, A. D.; Bucak, S. Liposomes as potential drug carrier systems for drug delivery. In Application of Nanotechnology in Drug Delivery; Sezer, A. D., Ed.; InTech: Rijeka, 2014; pp 1-50.

19

Schwendener, R. A. Liposomes as vaccine delivery systems: A review of the recent advances. Ther. Adv. Vaccines 2014, 2, 159-182.

20

Rasoulianboroujeni, M.; Kupgan, G.; Moghadam, F.; Tahriri, M.; Boughdachi, A.; Khoshkenar, P.; Ambrose, J. J.; Kiaie, N.; Vashaee, D.; Ramsey, J. D. et al. Development of a DNA-liposome complex for gene delivery applications. Mater. Sci. Eng. C 2017, 75, 191-197.

21

Saffari, M.; Moghimi, H. R.; Dass, C. R. Barriers to liposomal gene delivery: From application site to the target. Iran. J. Pharm. Res. 2016, 15, 3-17.

22

Bulbake, U.; Doppalapudi, S.; Kommineni, N.; Khan, W. Liposomal formulations in clinical use: An updated review. Pharmaceutics 2017, 9, 12.

23

Pillai, G. Nanomedicines for cancer therapy: An update of fda approved and those under various stages of development. Pharm. Pharm. Sci. 2014, 1, 13.

24

El-Subbagh, H. I.; Al-Badr, A. A. Cytarabine. In Profiles of Drug Substances, Excipients, and Related Methodology; Brittain, H. G., Ed.; Elsevier: Amsterdam, 2009; pp 37-113.

25

Germain, M.; Meyre, M. E.; Poul, L.; Paolini, M.; Berjaud, C.; Mpambani, F.; Bergere, M.; Levy, L.; Pottier, A. Priming the body to receive the therapeutic agent to redefine treatment benefit/risk profile. Sci. Rep. 2018, 8, 4797.

26

Park, B. H.; von Maltzahn, G.; Ong, L. L.; Centrone, A.; Hatton, T. A.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Cooperative nanoparticles for tumor detection and photothermally triggered drug delivery. Adv. Mater. 2010, 22, 880-885.

27

Mullen, D. G.; Holl, M. M. B. Heterogeneous ligand-nanoparticle distributions: A major obstacle to scientific understanding and commercial translation. ACC. Chem. Res. 2011, 44, 1135-1145.

28

Lohse, B.; Bolinger, P. Y.; Stamou, D. Encapsulation efficiency measured on single small unilamellar vesicles. J. Am. Chem. Soc. 2008, 130, 14372- 14373.

29

Ernsting, M. J.; Murakami, M.; Roy, A.; Li, S. D. Factors controlling the pharmacokinetics, biodistribution and intratumoral penetration of nanoparticles. J. Control. Release 2013, 172, 782-794.

30

Ohnishi, N.; Yamamoto, E.; Tomida, H.; Hyodo, K.; Ishihara, H.; Kikuchi, H.; Tahara, K.; Takeuchi, H. Rapid determination of the encapsulation efficiency of a liposome formulation using column-switching HPLC. Int. J. Pharm. 2013, 441, 67-74.

31

Zhang, X. M.; Patel, A. B.; de Graaf, R. A.; Behar, K. L. Determination of liposomal encapsulation efficiency using proton NMR spectroscopy. Chem. Phys. Lipids 2004, 127, 113-120.

32

Franzen, U.; Nguyen, T. T. T. N.; Vermehren, C.; Gammelgaard, B.; Østergaard, J. Characterization of a liposome-based formulation of oxaliplatin using capillary electrophoresis: Encapsulation and leakage. J. Pharm. Biomed. Anal. 2011, 55, 16-22.

33

Chen, C. X.; Zhu, S. B.; Wang, S.; Zhang, W. Q.; Cheng, Y.; Yan, X. M. Multiparameter quantification of liposomal nanomedicines at the single- particle level by high-sensitivity flow cytometry. ACS Appl. Mater. Interfaces 2017, 9, 13913-13919.

34

Jesorka, A.; Orwar, O. Liposomes: Technologies and analytical applications. Annu. Rev. Anal. Chem. 2008, 1, 801-832.

35

Weiss, V. U.; Urey, C.; Gondikas, A.; Golesne, M.; Friedbacher, G.; von der Kammer, F.; Hofmann, T.; Andersson, R.; Marko-Varga, G.; Marchetti-Deschmann, M. et al. Nano electrospray gas-phase electrophoretic mobility molecular analysis (nES-GEMMA) of liposomes: Applicability of the technique for nano vesicle batch control. Analyst 2016, 141, 6042-6050.

36

Urey, C.; Weiss, V. U.; Gondikas, A.; von der Kammer, F.; Hofmann, T.; Marchetti-Deschmann, M.; Allmaier, G.; Marko-Varga, G.; Andersson, R. Combining gas-phase electrophoretic mobility molecular analysis (GEMMA), light scattering, field flow fractionation and cryo electron microscopy in a multidimensional approach to characterize liposomal carrier vesicles. Int. J. Pharm. 2016, 513, 309-318.

37

Weiss, V. U.; Lehner, A.; Kerul, L.; Grombe, R.; Kratzmeier, M.; Marchetti-Deschmann, M.; Allmaier, G. Characterization of cross-linked gelatin nanoparticles by electrophoretic techniques in the liquid and the gas phase. Electrophoresis 2013, 34, 3267-3276.

38

Kaufman, S. L.; Skogen, J. W.; Dorman, F. D.; Zarrin, F. Macromolecule analysis based on electrophoretic mobility in air: Globular proteins. Anal. Chem. 1996, 68, 1895-1904.

39

Tycova, A.; Prikryl, J.; Foret, F. Reproducible preparation of nanospray tips for capillary electrophoresis coupled to mass spectrometry using 3D printed grinding device. Electrophoresis 2016, 37, 924-930.

40

Bangham, A. D.; Standish, M. M.; Watkins, J. C. Diffusion of univalent ions across the lamellae of swollen phospholipids. J. Mol. Biol. 1965, 13, 238-252.

41

Kinney, P. D.; Pui, D. Y. H.; Mulliolland, G. W.; Bryner, N. P. Use of the electrostatic classification method to size 0.1µm SRM particles-a feasibility study. J. Res. Natl. Inst. Stand. Technol. 1991, 96, 147-176.

42

Lewis, R. N.; McElhaney, R. N.; Pohle, W.; Mantsch, H. H. Components of the carbonyl stretching band in the infrared spectra of hydrated 1, 2-diacylglycerolipid bilayers: A reevaluation. Biophys. J. 1994, 67, 2367-2375.

43

Socrates, G. Infrared and Raman Characteristic Group Frequencies: Tables and Charts, 3rd ed.; John Wiley and Sons: Chichester, 2001.

44

Centrone, A. Infrared imaging and spectroscopy beyond the diffraction limit. Annu. Rev. Anal. Chem. 2015, 8, 101-126.

45

Dazzi, A.; Prater, C. B. AFM-IR: Technology and applications in nanoscale infrared spectroscopy and chemical imaging. Chem. Rev. 2017, 117, 5146-5173.

46

Dazzi, A.; Glotin, F.; Carminati, R. Theory of infrared nanospectroscopy by photothermal induced resonance. J. Appl. Phys. 2010, 107, 124519.

47

Lahiri, B.; Holland, G.; Centrone, A. Chemical imaging beyond the diffraction limit: Experimental validation of the PTIR technique. Small 2013, 9, 439-445.

48

Katzenmeyer, A. M.; Holland, G.; Kjoller, K.; Centrone, A. Absorption spectroscopy and imaging from the visible through mid-infrared with 20 nm resolution. Anal. Chem. 2015, 87, 3154-3159.

49

Lu, F.; Jin, M. Z.; Belkin, M. A. Tip-enhanced infrared nanospectroscopy via molecular expansion force detection. Nat. Photonics 2014, 8, 307-312.

50

Strelcov, E.; Dong, Q. F.; Li, T.; Chae, J.; Shao, Y. C.; Deng, Y. H.; Gruverman, A.; Huang, J. S.; Centrone, A. CH3NH3PbI3 perovskites: Ferroelasticity revealed. Sci. Adv. 2017, 3, e1602165.

51

Chae, J.; Dong, Q. F.; Huang, J. S.; Centrone, A. Chloride incorporation process in CH3NH3PBI3−xClx perovskites via nanoscale bandgap maps. Nano Lett. 2015, 15, 8114-8121.

52

Dong, R.; Fang, Y. J.; Chae, J.; Dai, J.; Xiao, Z. G.; Dong, Q. F.; Yuan, Y. B.; Centrone, A.; Zeng, X. C.; Huang, J. High-gain and low-driving-voltage photodetectors based on organolead triiodide perovskites. Adv. Mater. 2015, 27, 1912-1918.

53

van Eerdenbrugh, B.; Lo, M.; Kjoller, K.; Marcott, C.; Taylor, L. S. Nanoscale mid-infrared imaging of phase separation in a drug-polymer blend. J. Pharm. Sci. 2012, 101, 2066-2073.

54

Morsch, S.; van Driel, B. A.; van den Berg, K. J.; Dik, J. Investigating the photocatalytic degradation of oil paint using ATR-IR and AFM-IR. Appl. Mater. Interfaces 2017, 9, 10169-10179.

55

Ghosh, S.; Kouamé, N. A.; Ramos, L.; Remita, S.; Dazzi, A.; Deniset- Besseau, A.; Beaunier, P.; Goubard, F.; Aubert, P. H.; Remita, H. Conducting polymer nanostructures for photocatalysis under visible light. Nat. Mater. 2015, 14, 505-511.

56

Tri, P. N.; Prud'homme, R. E. Nanoscale lamellar assembly and segregation mechanism of poly (3-hydroxybutyrate)/poly(ethylene glycol) blends. Macromolecules 2018, 51, 181-188.

57

Morsch, S.; Liu, Y. W.; Lyon, S. B.; Gibbon, S. R. Insights into epoxy network nanostructural heterogeneity using AFM-IR. Appl. Mater. Interfaces 2016, 8, 959-966.

58

Chae, J.; Lahiri, B.; Centrone, A. Engineering near-field SEIRA enhancements in plasmonic resonators. ACS Photonics 2016, 3, 87-95.

59

Lahiri, B.; Holland, G.; Aksyuk, V.; Centrone, A. Nanoscale imaging of plasmonic hot spots and dark modes with the photothermal-induced resonance technique. Nano Lett. 2013, 13, 3218-3224.

60

Katzenmeyer, A. M.; Chae, J.; Kasica, R.; Holland, G.; Lahiri, B.; Centrone, A. Nanoscale imaging and spectroscopy of plasmonic modes with the PTIR technique. Adv. Opt. Mater. 2014, 2, 718-722.

61

Katzenmeyer, A. M.; Canivet, J.; Holland, G.; Farrusseng, D.; Centrone, A. Assessing chemical heterogeneity at the nanoscale in mixed-ligand metal-organic frameworks with the PTIR technique. Angew. Chem. , Int. Ed. 2014, 53, 2852-2856.

62

Brown, L. V; Davanco, M.; Sun, Z. Y.; Kretinin, A.; Chen, Y. G.; Matson, J. R.; Vurgaftman, I.; Sharac, N.; Giles, A. J.; Fogler, M. M. et al. Nanoscale mapping and spectroscopy of nonradiative hyperbolic modes in hexagonal boron nitride nanostructures. Nano Lett. 2018, 18, 1628-1636.

63

Rosenberger, M. R.; Wang, M. C.; Xie, X.; Rogers, J. A.; Nam, S.; King, W. P. Measuring individual carbon nanotubes and single graphene sheets using atomic force microscope infrared spectroscopy. Nanotechnology 2017, 28, 355707.

64

Ramer, G.; Balbekova, A.; Schwaighofer, A.; Lendl, B. Method for time-resolved monitoring of a solid state biological film using photothermal infrared nanoscopy on the example of poly-L-lysine. Anal. Chem. 2015, 87, 4415-4420.

65

Ruggeri, F. S.; Habchi, J.; Cerreta, A.; Dietler, G. AFM-based single molecule techniques: Unraveling the amyloid pathogenic species. Curr. Pharm. Des. 2016, 22, 3950-3970.

66

Dazzi, A.; Prater, C. B.; Hu, Q. C.; Chase, D. B.; Rabolt, J. F.; Marcott, C. AFM-IR: Combining atomic force microscopy and infrared spectroscopy for nanoscale chemical characterization. Appl. Spectrosc. 2012, 66, 1365-1384.

67

Marcott, C.; Lo, M.; Kjoller, K.; Fiat, F.; Baghdadli, N.; Balooch, G.; Luengo, G. S. Localization of human hair structural lipids using nanoscale infrared spectroscopy and imaging. Appl. Spectrosc. 2014, 68, 564-569.

68

Yarrow, F.; Kennedy, E.; Salaun, F.; Rice, J. H. Sub-wavelength infrared imaging of lipids. Biomed. Opt. Express, 2011, 2, 37-43.

69

Pancani, E.; Mathurin, J.; Bilent, S.; Bernet‐Camard, M. F.; Dazzi, A.; Deniset-Besseau, A.; Gref, R. High-resolution label-free detection of biocompatible polymeric nanoparticles in cells. Part. Part. Syst. Charact. 2018, 35, 1700457.

70

Kang, M.; Tuteja, M.; Centrone, A.; Topgaard, D.; Leal, C. Nanostructured lipid-based films for substrate-mediated applications in biotechnology. Adv. Funct. Mater. 2018, 28, 1704356.

71

Tuteja, M.; Kang, M.; Leal, C.; Centrone, A. Nanoscale partitioning of paclitaxel in hybrid lipid-polymer membranes. Analyst 2018, 143, 3808-3813.

72

Ramer, G.; Ruggeri, F. S.; Levin, A.; Knowles, T. P. J.; Centrone, A. Determination of polypeptide conformation with nanoscale resolution in water. ACS Nano 2018, 12, 6612-6619.

73

Jin, M. Z.; Lu, F.; Belkin, M. A. High-sensitivity infrared vibrational nanospectroscopy in water. Light Sci. Appl. 2017, 6, e17096.

74

Xiao, L. F.; Schultz, Z. D. Spectroscopic imaging at the nanoscale: Technologies and recent applications. Anal. Chem. 2018, 90, 440-458.

75

Mayet, C.; Dazzi, A.; Prazeres, R.; Allot, F.; Glotin, F.; Ortega, J. M. Sub-100 nm IR spectromicroscopy of living cells. Opt. Lett. 2008, 33, 1611-1613.

76

Dazzi, A.; Prazeres, R.; Glotin, F.; Ortega, J. M.; Al-Sawaftah, M.; de Frutos, M. Chemical mapping of the distribution of viruses into infected bacteria with a photothermal method. Ultramicroscopy 2008, 108, 635-641.

77

Ramer, G.; Aksyuk, V. A.; Centrone, A. Quantitative chemical analysis at the nanoscale using the photothermal induced resonance technique. Anal. Chem. 2017, 89, 13524-13531.

78

Katzenmeyer, A. M.; Holland, G.; Chae, J.; Band, A.; Kjoller, K.; Centrone, A. Mid-infrared spectroscopy beyond the diffraction limit via direct measurement of the photothermal effect. Nanoscale 2015, 7, 17637-17641.

79

Barlow, D. E.; Biffinger, J. C.; Cockrell-Zugell, A. L.; Lo, M.; Kjoller, K.; Cook, D.; Lee, K. W.; Pehrsson, P. E.; Crookes-Goodson, W. J.; Hung, C. S. et al. The importance of correcting for variable probe-sample interactions in AFM-IR spectroscopy: AFM-IR of dried bacteria on a polyurethane film. Analyst 2016, 141, 4848-4854.

80

Rabe, U.; Janser, K.; Arnold, W. Vibrations of free and surface-coupled atomic force microscope cantilevers: Theory and experiment. Rev. Sci. Instrum. 1996, 67, 3281-3293.

81

Ramer, G.; Reisenbauer, F.; Steindl, B.; Tomischko, W.; Lendl, B. Implementation of resonance tracking for assuring reliability in resonance enhanced photothermal infrared spectroscopy and imaging. Appl. Spectrosc. 2017, 71, 2013-2020.

82

Hu, S. M. Infrared absorption spectra of SiO2 precipitates of various shapes in silicon: Calculated and experimental. J. Appl. Phys. 1980, 51, 5945-5948.

83

Last, J. A.; Russell, P.; Nealey, P. F.; Murphy, C. J. The applications of atomic force microscopy to vision science. Invest. Ophthalmol. Vis. Sci. 2010, 51, 6083-6094.

84

Tetard, L.; Passian, A.; Farahi, R. H.; Thundat, T.; Davison, B. H. Opto- nanomechanical spectroscopic material characterization. Nat. Nanotechnol. 2015, 10, 870-877.

85

Chae, J.; An, S. M.; Ramer, G.; Stavila, V.; Holland, G.; Yoon, Y.; Talin, A. A.; Allendorf, M.; Aksyuk, V. A.; Centrone, A. Nanophotonic atomic force microscope transducers enable chemical composition and thermal conductivity measurements at the nanoscale. Nano Lett. 2017, 17, 5587-5594.

Nano Research
Pages 197-203
Cite this article:
Wieland K, Ramer G, Weiss VU, et al. Nanoscale chemical imaging of individual chemotherapeutic cytarabine-loaded liposomal nanocarriers. Nano Research, 2019, 12(1): 197-203. https://doi.org/10.1007/s12274-018-2202-x
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Received: 29 May 2018
Revised: 30 May 2018
Accepted: 12 September 2018
Published: 27 September 2018
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018
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