nach oben

Magnetic Resonance Materials in Physics, Biology and Medicine

Erschienen in:

16.01.2019 | Research Article

Challenges for labeling and longitudinal tracking of adoptively transferred autoreactive T lymphocytes in an experimental type-1 diabetes model

verfasst von: Shweta Saini, Hannelie Korf, Sayuan Liang, Rein Verbeke, Bella Manshian, Koen Raemdonck, Ine Lentacker, Conny Gysemans, Stefaan C. De Smedt, Uwe Himmelreich

Erschienen in: Magnetic Resonance Materials in Physics, Biology and Medicine | Ausgabe 3/2019

Einloggen, um Zugang zu erhalten

Abstract

Objective

Tracking the autoreactive T-cell migration in the pancreatic region after labeling with fluorinated nanoparticles (1,2-dioleoyl-sn-glycero-3-phosphoethanolamine-N-[3-(2-pyridyldithio)propionate]-perfluoro-15-crown-5-ether nanoparticles, PDP-PFCE NPs) in a diabetic murine model using ¹⁹F MRI.

Materials and methods

Synthesis of novel PDP-PFCE fluorine tracer was performed for in vitro labeling of T cells. Labeling conditions were optimized using different PDP-PFCE NPs concentrations. For in vivo ¹⁹F MRI, mice were longitudinally followed after adoptive transfer of activated, autoreactive, labeled T cells in NOD.SCID mice.

Results

Established MR protocols were used for challenging T cell labeling to track inflammation in a model of diabetes after successful labeling of CD4+ and CD8+ T cells with PDP-PFCE NPs. However, T cells were difficult to be detected in vivo after their engraftment in animals.

Discussion

We showed successful in vitro labeling of T cells using novel fluorinated liposomal nanoparticles. However, insufficient and slow accumulation of labeled T cells and subsequent T cell proliferation in the pancreatic region remains as limitations of in vivo cell imaging by ¹⁹F MRI.

Liang S, Louchami K, Kolster H, Jacobsen A, Zhang Y, Thimm J, Sener A, Thiem J, Malaisse W, Dresselaers T, Himmelreich U (2016) 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 11:506–513. https://doi.org/10.1002/cmmi.1712 CrossRefPubMed

Kriz J, Jirak D, Berkova Z, Herynek V, Lodererova A, Girman P, Habart D, Hajek M, Saudek F (2012) Detection of pancreatic islet allograft impairment in advance of functional failure using magnetic resonance imaging. Transpl Int 25:250–260. https://doi.org/10.1111/j.1432-2277.2011.01403.x CrossRefPubMed

Malosio ML, Esposito A, Brigatti C, Palmisano A, Piemonti L, Nano R, Maffi P, De Cobelli F, Del Maschio A, Secchi A (2015) MR imaging monitoring of iron labeled pancreatic islets in a small series of patients: islets fate in successful, unsuccessful and auto-transplantation. Cell Transplant 24:2285–2296. https://doi.org/10.3727/096368914X684060 CrossRefPubMed

Medarova Z, Moore A (2008) Non-invasive detection of transplanted pancreatic islets. Diabetes Obes Metab 10(Suppl 4):88–97. https://doi.org/10.1111/j.1463-1326.2008.00942.x CrossRefPubMedPubMedCentral

Arifin DR, Bulte JWM (2011) Imaging of pancreatic islet cells. Diabetes Metab Res Rev 27:761–766. https://doi.org/10.1002/dmrr.1248 CrossRefPubMedPubMedCentral

Alanentalo T, Asayesh A, Morrison H, Lorén CE, Holmberg D, Sharpe J, Ahlgren U (2007) Tomographic molecular imaging and 3D quantification within adult mouse organs. Nat Methods 4:31–33. https://doi.org/10.1038/nmeth985 CrossRefPubMed

Alanentalo T, Lorén CE, Larefalk A, Sharpe J, Holmberg D, Ahlgren U (2008) High-resolution three-dimensional imaging of islet-infiltrate interactions based on optical projection tomography assessments of the intact adult mouse pancreas. J Biomed Opt 13:054070. https://doi.org/10.1117/1.3000430 CrossRefPubMed

Peterson JD, Haskins K (1996) Transfer of diabetes in the NOD-scid mouse by CD4 T-cell clones: differential requirement for CD8 T-cells. Diabetes 45:328–336CrossRefPubMed

Wucherpfennig KW, Eisenbarth GS (2001) Type 1 diabetes. Nature 2:767–768. https://doi.org/10.1016/S0140-6736(11)60614-4 CrossRef

10.

Srinivas M, Boehm-Sturm P, Figdor CG, de Vries IJ, Hoehn M (2012) Labeling cells for in vivo tracking using ¹⁹F MRI. Biomaterials 33:8830–8840. https://doi.org/10.1016/j.biomaterials.2012.08.048 CrossRefPubMed

11.

Himmelreich U, Hoehn M (2008) Stem cell labeling for magnetic resonance imaging. Minim Invasive Ther Allied Technol 17:132–142. https://doi.org/10.1080/13645700801969873 CrossRefPubMed

12.

Himmelreich U, Dresselaers T (2009) Cell labeling and tracking for experimental models using Magnetic Resonance Imaging. Methods 48:112–124. https://doi.org/10.1016/j.ymeth.2009.03.020 CrossRefPubMed

13.

Srinivas M, Heerschap A, Ahrens ET, Figdor CG, de Vries IJM (2010) ¹⁹F MRI for quantitative in vivo cell tracking. Trends Biotechnol 28:363–370. https://doi.org/10.1016/j.tibtech.2010.04.002 CrossRefPubMedPubMedCentral

14.

Harms C, Datwyler AL, Wiekhorst F, Trahms L, Lindquist R, Schellenberger E, Mueller S, Schütz G, Roohi F, Ide A, Füchtemeier M, Gertz K, Kronenberg G, Harms U, Endres M, Dirnagl U, Farr TD (2013) Certain types of iron oxide nanoparticles are not suited to passively target inflammatory cells that infiltrate the brain in response to stroke. J Cereb Blood Flow Metab 36(Suppl 1):139–140. https://doi.org/10.1038/jcbfm.2013.22 CrossRef

15.

Ebner B, Behm P, Jacoby C, Burghoff S, French BA, Schrader J, Flögel U (2010) Early assessment of pulmonary inflammation by ¹⁹F MRI in vivo. Circ Cardiovasc Imaging 3:202–210. https://doi.org/10.1161/CIRCIMAGING.109.902312 CrossRefPubMedPubMedCentral

16.

Stoll G, Basse-Lüsebrink T, Weise G, Jakob P (2012) Visualization of inflammation using ¹⁹F-magnetic resonance imaging and perfluorocarbons. Wiley Interdiscip Rev Nanomedicine Nanobiotechnology 4:438–447. https://doi.org/10.1002/wnan.1168 CrossRefPubMed

17.

Shin SH, Kadayakkara DK, Bulte JWM (2017) In Vivo ¹⁹ F MR imaging cell tracking of inflammatory macrophages and site-specific development of colitis-associated dysplasia. Radiology 282:194–201. https://doi.org/10.1148/radiol.2016152387 CrossRefPubMed

18.

Jacoby C, Borg N, Heusch P, Sauter M, Bönner F, Kandolf R, Klingel K, Schrader J, Flögel U (2014) Visualization of immune cell infiltration in experimental viral myocarditis by ¹⁹F MRI in vivo. Magn Reson Mater Phy. https://doi.org/10.1007/s10334-013-0391-6 CrossRef

19.

Tirotta I, Dichiarante V, Pigliacelli C, Cavallo G, Terraneo G, Bombelli FB, Metrangolo P, Resnati G (2015) ¹⁹F magnetic resonance imaging (MRI): from design of materials to clinical applications. Chem Rev 115:1106–1129CrossRefPubMed

20.

Janjic JM, Ahrens ET (2009) Fluorine-containing nanoemulsions for MRI cell tracking. Wiley Interdiscip Rev Nanomedicine Nanobiotechnology 1:492–501CrossRefPubMed

21.

Westermann J, Söllner S, Ehlers E-M, Nohroudi K, Blessenohl M, Kalies K (2003) Analyzing the migration of labeled T cells in vivo: an essential approach with challenging features. Lab Investig 83:459–469. https://doi.org/10.1097/01.LAB.0000062852.80567.90 CrossRefPubMed

22.

Gonzales C, Yoshihara HAI, Dilek N, Leignadier J, Irving M, Mieville P, Helm L, Michielin O, Schwitter J (2016) In-vivo detection and tracking of T cells in various organs in a melanomatumor model by ¹⁹F-fluorine MRS/MRI. PLoS One 11:1–18. https://doi.org/10.1371/journal.pone.0164557 CrossRef

23.

Srinivas M, Morel PA, Ernst LA, Laidlaw DH, Ahrens ET (2007) Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn Reson Med 58:725–734. https://doi.org/10.1002/mrm.21352 CrossRefPubMed

24.

Przybylski S, Gasch M, Marschner A, Ebert M, Ewe A, Helmig G, Hilger N, Fricke S, Rudzok S, Aigner A, Burkhardt J (2017) Influence of nanoparticle-mediated transfection on proliferation of primary immune cells in vitro and in vivo. PLoS One 12:1–16. https://doi.org/10.1371/journal.pone.0176517 CrossRef

25.

Wayteck L, Dewitte H, De Backer L, Breckpot K, Demeester J, De Smedt SC, Raemdonck K (2016) Hitchhiking nanoparticles: reversible coupling of lipid-based nanoparticles to cytotoxic T lymphocytes. Biomaterials 77:243–254. https://doi.org/10.1016/j.biomaterials.2015.11.016 CrossRefPubMed

26.

Liang S, Louchami K, Holvoet B, Verbeke R, Deroose CM, Manshian B, Soenen SJ, Lentacker I, Himmelreich U (2018) Tri-modal in vivo imaging of pancreatic islets transplanted subcutaneously in mice. Mol Imaging Biol 20:940–951. https://doi.org/10.1007/s11307-018-1192-0 CrossRefPubMed

27.

Ferreira GB, Gysemans CA, Demengeot J, da Cunha JPMCM, Vanherwegen A-S, Overbergh L, Van Belle TL, Pauwels F, Verstuyf A, Korf H, Mathieu C (2014) 1,25-Dihydroxyvitamin D3 promotes tolerogenic dendritic cells with functional migratory properties in NOD mice. J Immunol 192:4210–4220. https://doi.org/10.4049/jimmunol.1302350 CrossRefPubMed

28.

Poulin M, Haskins K (2000) Induction of diabetes in nonobese diabetic mice by Th2 T cell clones from a TCR transgenic mouse. J Immunol 164:3072–3078CrossRefPubMed

29.

Eizirik DL, Colli ML, Ortis F (2009) The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol 5:219–226. https://doi.org/10.1038/nrendo.2009.21 CrossRefPubMed

30.

Ahrens ET, Bulte JWM (2013) Tracking immune cells in vivo using magnetic resonance imaging. Nat Rev Immunol 13:755–763CrossRef

31.

van Heeswijk RB, Pellegrin M, Flögel U, Gonzales C, Aubert J-F, Mazzolai L, Schwitter J, Stuber M (2015) Fluorine MR imaging of inflammation in atherosclerotic plaque in vivo. Radiology 275:421–429. https://doi.org/10.1148/radiol.14141371 CrossRefPubMed

32.

Temme S, Bönner F, Schrader J, Flögel U (2012) ¹⁹F magnetic resonance imaging of endogenous macrophages in inflammation. Wiley Interdiscip Rev Nanomedicine Nanobiotechnology 4:329–343. https://doi.org/10.1002/wnan.1163 CrossRefPubMed

33.

Gaglia JL, Guimaraes AR, Harisinghani M, Turvey SE, Jackson R, Benoist C, Mathis D, Weissleder R (2011) Noninvasive imaging of pancreatic islet inflammation in type 1A diabetes patients. J Clin Invest 121:442–445. https://doi.org/10.1172/JCI44339 CrossRef

34.

Chapelin F, Gao S, Okada H, Weber TG, Messer K, Ahrens ET (2017) Fluorine-19 nuclear magnetic resonance of chimeric antigen receptor T cell biodistribution in murine cancer model. Sci Rep 7:1–5. https://doi.org/10.1038/s41598-017-17669-4 CrossRef

35.

O’Hanlon CF, Fedczyna T, Eaker S, Shingleton WD, Helfer BM (2017) Integrating a ¹⁹F MRI tracer agent into the clinical scale manufacturing of a T-cell immunotherapy. Contrast Media Mol Imaging 201:1–7. https://doi.org/10.1155/2017/9548478 CrossRef

36.

Amiri H, Srinivas M, Veltien A, van Uden MJ, de Vries IJM, Heerschap A (2015) Cell tracking using ¹⁹F magnetic resonance imaging: technical aspects and challenges towards clinical applications. Eur Radiol 25:726–735. https://doi.org/10.1007/s00330-014-3474-5 CrossRefPubMed

37.

Boehm-Sturm P, Mengler L, Wecker S, Hoehn M, Kallur T (2011) In Vivo tracking of human neural stem cells with ¹⁹F magnetic resonance imaging. PLoS One 6:e29040. https://doi.org/10.1371/journal.pone.0029040 CrossRefPubMedPubMedCentral

38.

Waiczies S, Millward JM, Starke L, Delgado PR, Huelnhagen T, Prinz C, Marek D, Di Wecker, Wissmann R, Koch SP, Boehm-Sturm P, Waiczies H, Niendorf T, Pohlmann A (2017) Enhanced fluorine-19 MRI sensitivity using a cryogenic radiofrequency probe: technical developments and ex vivo demonstration in a mouse model of neuroinflammation. Sci Rep 7:1–10. https://doi.org/10.1038/s41598-017-09622-2 CrossRef

39.

Liang S, Dresselaers T, Louchami K, Zhu C, Liu Y, Himmelreich U (2017) Comparison of different compressed sensing algorithms for low SNR ¹⁹F MRI applications—imaging of transplanted pancreatic islets and cells labeled with perfluorocarbons. NMR Biomed 30:e3776. https://doi.org/10.1002/nbm.3776 CrossRef

Titel: Challenges for labeling and longitudinal tracking of adoptively transferred autoreactive T lymphocytes in an experimental type-1 diabetes model
verfasst von: Shweta Saini
Hannelie Korf
Sayuan Liang
Rein Verbeke
Bella Manshian
Koen Raemdonck
Ine Lentacker
Conny Gysemans
Stefaan C. De Smedt
Uwe Himmelreich
Publikationsdatum: 16.01.2019
Verlag: Springer International Publishing
Erschienen in: Magnetic Resonance Materials in Physics, Biology and Medicine / Ausgabe 3/2019
Print ISSN: 0968-5243
Elektronische ISSN: 1352-8661
DOI: https://doi.org/10.1007/s10334-018-0720-x

Neu im Fachgebiet Radiologie

23.04.2024 | Pankreaskarzinom | Nachrichten

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Challenges for labeling and longitudinal tracking of adoptively transferred autoreactive T lymphocytes in an experimental type-1 diabetes model

Abstract

Objective

Materials and methods

Results

Discussion

Neu im Fachgebiet Radiologie

S3-Leitlinie zu Pankreaskrebs aktualisiert

Fünf Dinge, die im Kindernotfall besser zu unterlassen sind

„Nur wer sich gut aufgehoben fühlt, kann auch für Patientensicherheit sorgen“

Wie toxische Männlichkeit der Gesundheit von Männern schadet

Update Radiologie

Springer Medizin

Abstract

Objective

Materials and methods

Results

Discussion

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2019

Projection-based respiratory-resolved left ventricular volume measurements in patients using free-breathing double golden-angle 3D radial acquisition

Precision of T1-relaxation time measurements in the hepatic portal vein: influence of measurement technique and sequence parameters

Realization of 19F MRI oximetry method using perfluorodecalin

Feasibility of diffusion-weighted imaging with DWIBS in staging Hodgkin lymphoma in pediatric patients: comparison with PET/CT

The feasibility of a novel limited field of view spiral cine DENSE sequence to assess myocardial strain in dilated cardiomyopathy

A phase-cycled temperature-sensitive fast spin echo sequence with conductivity bias correction for monitoring of mild RF hyperthermia with PRFS

Neu im Fachgebiet Radiologie

S3-Leitlinie zu Pankreaskrebs aktualisiert

Fünf Dinge, die im Kindernotfall besser zu unterlassen sind

„Nur wer sich gut aufgehoben fühlt, kann auch für Patientensicherheit sorgen“

Wie toxische Männlichkeit der Gesundheit von Männern schadet

Update Radiologie