A Trimodal Imaging Platform for Tracking Viable Transplanted Pancreatic Islets In Vivo: F-19 MR, Fluorescence, and Bioluminescence Imaging

Overview

Journal Mol Imaging Biol

Publisher Springer

Specialties Molecular Biology
Radiology

Date 2018 Sep 1

PMID 30167995

Citations 14

Authors

A Galisova

V Herynek

E Swider

E Sticova

A Patikova

L Kosinova

J Kriz

M Hajek

M Srinivas

D Jirak

Affiliations

Soon will be listed here.

Abstract

Purpose: Combining specific and quantitative F-19 magnetic resonance imaging (MRI) with sensitive and convenient optical imaging provides complementary information about the distribution and viability of transplanted pancreatic islet grafts. In this study, pancreatic islets (PIs) were labeled with positively charged multimodal nanoparticles based on poly(lactic-co-glycolic acid) (PLGA-NPs) with encapsulated perfluoro-15-crown-5-ether and the near-infrared fluorescent dye indocyanine green.

Procedures: One thousand and three thousand bioluminescent PIs were transplanted into subcutaneous artificial scaffolds, which served as an alternative transplant site. The grafts were monitored using in vivo F-19 MR, fluorescence, and bioluminescence imaging in healthy rats for 2 weeks.

Results: Transplanted PIs were unambiguously localized in the scaffolds by F-19 MRI throughout the whole experiment. Fluorescence was detected in the first 4 days after transplantation only. Importantly, in vivo bioluminescence correlated with the F-19 MRI signal.

Conclusions: We developed a trimodal imaging platform for in vivo examination of transplanted PIs. Fluorescence imaging revealed instability of the fluorescent dye and its limited applicability for longitudinal in vivo studies. A correlation between the bioluminescence signal and the F-19 MRI signal indicated the fast clearance of PLGA-NPs from the transplantation site after cell death, which addresses a major issue with intracellular imaging labels. Therefore, the proposed PLGA-NP platform is reliable for reflecting the status of transplanted PIs in vivo.

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References

Liang S, Dresselaers T, Louchami K, Zhu C, Liu Y, Himmelreich U . Comparison of different compressed sensing algorithms for low SNR F MRI applications-Imaging of transplanted pancreatic islets and cells labeled with perfluorocarbons. NMR Biomed. 2017; 30(11). DOI: 10.1002/nbm.3776. View

Pepper A, Pawlick R, Gala-Lopez B, MacGillivary A, Mazzuca D, White D . Diabetes Is Reversed in a Murine Model by Marginal Mass Syngeneic Islet Transplantation Using a Subcutaneous Cell Pouch Device. Transplantation. 2015; 99(11):2294-300. PMC: 4623852. DOI: 10.1097/TP.0000000000000864. View

Gotoh M, Maki T, Kiyoizumi T, Satomi S, Monaco A . An improved method for isolation of mouse pancreatic islets. Transplantation. 1985; 40(4):437-8. DOI: 10.1097/00007890-198510000-00018. View

Srinivas M, Morel P, Ernst L, Laidlaw D, Ahrens E . Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn Reson Med. 2007; 58(4):725-34. DOI: 10.1002/mrm.21352. View

Fowler M, Virostko J, Chen Z, Poffenberger G, Radhika A, Brissova M . Assessment of pancreatic islet mass after islet transplantation using in vivo bioluminescence imaging. Transplantation. 2005; 79(7):768-76. DOI: 10.1097/01.tp.0000152798.03204.5c. View

Pileggi A, Molano R, Ricordi C, Zahr E, Collins J, Valdes R . Reversal of diabetes by pancreatic islet transplantation into a subcutaneous, neovascularized device. Transplantation. 2006; 81(9):1318-24. DOI: 10.1097/01.tp.0000203858.41105.88. View

Srinivas M, Heerschap A, Ahrens E, Figdor C, de Vries I . (19)F MRI for quantitative in vivo cell tracking. Trends Biotechnol. 2010; 28(7):363-70. PMC: 2902646. DOI: 10.1016/j.tibtech.2010.04.002. View

Srinivas M, Cruz L, Bonetto F, Heerschap A, Figdor C, de Vries I . Customizable, multi-functional fluorocarbon nanoparticles for quantitative in vivo imaging using 19F MRI and optical imaging. Biomaterials. 2010; 31(27):7070-7. DOI: 10.1016/j.biomaterials.2010.05.069. View

Eter W, Bos D, Frielink C, Boerman O, Brom M, Gotthardt M . Graft revascularization is essential for non-invasive monitoring of transplanted islets with radiolabeled exendin. Sci Rep. 2015; 5:15521. PMC: 4614800. DOI: 10.1038/srep15521. View

10.

Liang S, Louchami K, Kolster H, Jacobsen A, Zhang Y, Thimm J . In vivo and ex vivo 19-fluorine magnetic resonance imaging and spectroscopy of beta-cells and pancreatic islets using GLUT-2 specific contrast agents. Contrast Media Mol Imaging. 2016; 11(6):506-513. DOI: 10.1002/cmmi.1712. View

11.

Toso C, Vallee J, Morel P, Ris F, Demuylder-Mischler S, Lepetit-Coiffe M . Clinical magnetic resonance imaging of pancreatic islet grafts after iron nanoparticle labeling. Am J Transplant. 2008; 8(3):701-6. DOI: 10.1111/j.1600-6143.2007.02120.x. View

12.

Lu Y, Dang H, Middleton B, Zhang Z, Washburn L, Campbell-Thompson M . Bioluminescent monitoring of islet graft survival after transplantation. Mol Ther. 2004; 9(3):428-35. DOI: 10.1016/j.ymthe.2004.01.008. View

13.

Srinivas M, Boehm-Sturm P, Aswendt M, Pracht E, Figdor C, de Vries I . In vivo 19F MRI for cell tracking. J Vis Exp. 2013; (81):e50802. PMC: 3992025. DOI: 10.3791/50802. View

14.

Fink C, Gaudet J, Fox M, Bhatt S, Viswanathan S, Smith M . F-perfluorocarbon-labeled human peripheral blood mononuclear cells can be detected in vivo using clinical MRI parameters in a therapeutic cell setting. Sci Rep. 2018; 8(1):590. PMC: 5766492. DOI: 10.1038/s41598-017-19031-0. View

15.

Temme S, Bonner F, Schrader J, Flogel U . 19F magnetic resonance imaging of endogenous macrophages in inflammation. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2012; 4(3):329-43. DOI: 10.1002/wnan.1163. View

16.

Schneider C, Rasband W, Eliceiri K . NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012; 9(7):671-5. PMC: 5554542. DOI: 10.1038/nmeth.2089. View

17.

Liang S, Louchami K, Holvoet B, Verbeke R, Deroose C, Manshian B . Tri-modal In vivo Imaging of Pancreatic Islets Transplanted Subcutaneously in Mice. Mol Imaging Biol. 2018; 20(6):940-951. DOI: 10.1007/s11307-018-1192-0. View

18.

Boehm-Sturm P, Mengler L, Wecker S, Hoehn M, Kallur T . In vivo tracking of human neural stem cells with 19F magnetic resonance imaging. PLoS One. 2012; 6(12):e29040. PMC: 3247235. DOI: 10.1371/journal.pone.0029040. View

19.

Swider E, Staal A, van Riessen N, Jacobs L, White P, Fokkink R . Design of triphasic poly(lactic--glycolic acid) nanoparticles containing a perfluorocarbon phase for biomedical applications. RSC Adv. 2022; 8(12):6460-6470. PMC: 9078287. DOI: 10.1039/c7ra13062g. View

20.

Constantinides C, Maguire M, McNeill E, Carnicer R, Swider E, Srinivas M . Fast, quantitative, murine cardiac 19F MRI/MRS of PFCE-labeled progenitor stem cells and macrophages at 9.4T. PLoS One. 2018; 13(1):e0190558. PMC: 5764257. DOI: 10.1371/journal.pone.0190558. View