Top

Magnetic Resonance Materials in Physics, Biology and Medicine

Published in:

Open Access 01-02-2019 | Review

Fluorine polymer probes for magnetic resonance imaging: quo vadis?

Authors: Daniel Jirak, Andrea Galisova, Kristyna Kolouchova, David Babuka, Martin Hruby

Published in: Magnetic Resonance Materials in Physics, Biology and Medicine | Issue 1/2019

Abstract

Over the last few years, the development and relevance of ¹⁹F magnetic resonance imaging (MRI) for use in clinical practice has emerged. MRI using fluorinated probes enables the achievement of a specific signal with high contrast in MRI images. However, to ensure sufficient sensitivity of ¹⁹F MRI, fluorine probes with a high content of chemically equivalent fluorine atoms are required. The majority of ¹⁹F MRI agents are perfluorocarbon emulsions, which have a broad range of applications in molecular imaging, although the content of fluorine atoms in these molecules is limited. In this review, we focus mainly on polymer probes that allow higher fluorine content and represent versatile platforms with properties tailorable to a plethora of biomedical in vivo applications. We discuss the chemical development, up to the first imaging applications, of these promising fluorine probes, including injectable polymers that form depots that are intended for possible use in cancer therapy.

Ruiz-Cabello J, Barnett BP, Bottomley PA, Bulte JWM (2011) Fluorine (F-19) MRS and MRI in biomedicine. NMR Biomed 24(2):114–129CrossRef

Peterson KL, Srivastava K, Pierre VC (2018) Fluorinated paramagnetic complexes: sensitive and responsive probes for magnetic resonance spectroscopy and imaging. Front Chem 6

Yu JX, Hallac RR, Chiguru S, Mason RP (2013) New frontiers and developing applications in F-19 NMR. Prog Nucl Mag Res Sp 70:25–49CrossRef

Srinivas M, Heerschap A, Ahrens ET, Figdor CG, de Vries IJM (2010) F-19 MRI for quantitative in vivo cell tracking. Trends Biotechnol 28(7):363–370CrossRef

Bulte JW (2005) Hot spot MRI emerges from the background. Nat Biotechnol 23(8):945–946. https://doi.org/10.1038/nbt0805-945 CrossRefPubMed

Blahut J, Bernasek K, Galisova A, Herynek V, Cisarova I, Kotek J, Lang J, Matejkova S, Hermann P (2017) Paramagnetic (19)F relaxation enhancement in Nickel(II) complexes of N-trifluoroethyl cyclam derivatives and cell labeling for (19)F MRI. Inorg Chem 56(21):13337–13348. https://doi.org/10.1021/acs.inorgchem.7b02119 CrossRefPubMed

Knight JC, Edwards PG, Paisey SJ (2011) Fluorinated contrast agents for magnetic resonance imaging; a review of recent developments. Rsc Adv 1(8):1415–1425. https://doi.org/10.1039/c1ra00627d CrossRef

Ahrens ET, Flores R, Xu H, Morel PA (2005) In vivo imaging platform for tracking immunotherapeutic cells. Nat Biotechnol 23(8):983–987. https://doi.org/10.1038/nbt1121 CrossRefPubMed

Fink C, Gaudet JM, Fox MS, Bhatt S, Viswanathan S, Smith M, Chin J, Foster PJ, Dekaban GA (2018) (19)F-perfluorocarbon-labeled human peripheral blood mononuclear cells can be detected in vivo using clinical MRI parameters in a therapeutic cell setting. Sci Rep 8(1):590. https://doi.org/10.1038/s41598-017-19031-0 CrossRefPubMedPubMedCentral

10.

Gaudet JM, Ribot EJ, Chen Y, Gilbert KM, Foster PJ (2015) Tracking the fate of stem cell implants with fluorine-19 MRI. PLoS One 10(3):e0118544. https://doi.org/10.1371/journal.pone.0118544 CrossRefPubMedPubMedCentral

11.

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(4):725–734. https://doi.org/10.1002/mrm.21352 CrossRefPubMed

12.

Ahrens ET, Helfer BM, O’Hanlon CF, Schirda C (2014) Clinical cell therapy imaging using a perfluorocarbon tracer and fluorine-19 MRI. Magn Reson Med 72(6):1696–1701. https://doi.org/10.1002/mrm.25454 CrossRefPubMedPubMedCentral

13.

Boehm-Sturm P, Aswendt M, Minassian A, Michalk S, Mengler L, Adamczak J, Mezzanotte L, Lowik C, Hoehn M (2014) A multi-modality platform to image stem cell graft survival in the naive and stroke-damaged mouse brain. Biomaterials 35(7):2218–2226. https://doi.org/10.1016/j.biomaterials.2013.11.085 CrossRefPubMed

14.

Tennstaedt A, Mastropietro A, Nelles M, Beyrau A, Hoehn M (2015) In vivo fate imaging of intracerebral stem cell grafts in mouse brain. PLoS One 10(12):e0144262. https://doi.org/10.1371/journal.pone.0144262 CrossRefPubMedPubMedCentral

15.

Constantinides C, Maguire M, McNeill E, Carnicer R, Swider E, Srinivas M, Carr CA, Schneider JE (2018) Fast, quantitative, murine cardiac 19F MRI/MRS of PFCE-labeled progenitor stem cells and macrophages. PLoS One 13(1):e0190558. https://doi.org/10.1371/journal.pone.0190558 CrossRefPubMedPubMedCentral

16.

Temme S, Bonner F, Schrader J, Flogel U (2012) 19F magnetic resonance imaging of endogenous macrophages in inflammation. Wiley Interdiscip Rev Nanomed Nanobiotechnol 4(3):329–343. https://doi.org/10.1002/wnan.1163 CrossRefPubMed

17.

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. https://doi.org/10.1007/s11307-018-1192-0 CrossRefPubMedPubMedCentral

18.

Barnett BP, Ruiz-Cabello J, Hota P, Ouwerkerk R, Shamblott MJ, Lauzon C, Walczak P, Gilson WD, Chacko VP, Kraitchman DL, Arepally A, Bulte JW (2011) Use of perfluorocarbon nanoparticles for non-invasive multimodal cell tracking of human pancreatic islets. Contrast Media Mol Imaging 6(4):251–259. https://doi.org/10.1002/cmmi.424 CrossRefPubMedPubMedCentral

19.

Rolfe BE, Blakey I, Squires O, Peng H, Boase NRB, Alexander C, Parsons PG, Boyle GM, Whittaker AK, Thurecht KJ (2014) Multimodal polymer nanoparticles with combined F-19 magnetic resonance and optical detection for tunable, targeted, multimodal imaging in vivo. J Am Chem Soc 136(6):2413–2419CrossRef

20.

Oishi M, Sumitani S, Nagasaki Y (2007) On-off regulation of F-19 magnetic resonance signals based on pH-sensitive PEGylated nanogels for potential tumor-specific smart F-19 MRI probes. Bioconjugate Chem 18(5):1379–1382. https://doi.org/10.1021/bc7002154 CrossRef

21.

Young SW, Enzmann DR, Long DM, Muller HH (1981) Perfluoroctylbromide contrast enhancement of malignant neoplasms: preliminary observations. AJR Am J Roentgenol 137(1):141–146. https://doi.org/10.2214/ajr.137.1.141 CrossRefPubMed

22.

Zhang C, Moonshi SS, Wang W, Ta HT, Han Y, Han FY, Peng H, Kral P, Rolfe BE, Gooding JJ, Gaus K, Whittaker AK (2018) High F-content perfluoropolyether-based nanoparticles for targeted detection of breast cancer by (19)F magnetic resonance and optical imaging. ACS Nano 12(9):9162–9176. https://doi.org/10.1021/acsnano.8b03726 CrossRefPubMed

23.

Flogel U, Ding Z, Hardung H, Jander S, Reichmann G, Jacoby C, Schubert R, Schrader J (2008) In vivo monitoring of inflammation after cardiac and cerebral ischemia by fluorine magnetic resonance imaging. Circulation 118(2):140–148CrossRef

24.

Ahrens ET, Young WB, Xu H, Pusateri LK (2011) Rapid quantification of inflammation in tissue samples using perfluorocarbon emulsion and fluorine-19 nuclear magnetic resonance. Biotechniques 50(4):229–234. https://doi.org/10.2144/000113652 CrossRefPubMedPubMedCentral

25.

Murugesan R, English S, Reijnders K, Yamada K, Cook JA, Mitchell JB, Subramanian S, Krishna MC (2002) Fluorine electron double resonance imaging for 19F MRI in low magnetic fields. Magn Reson Med 48(3):523–529. https://doi.org/10.1002/mrm.10221 CrossRefPubMed

26.

Waiczies H, Lepore S, Drechsler S, Qadri F, Purfurst B, Sydow K, Dathe M, Kuhne A, Lindel T, Hoffmann W, Pohlmann A, Niendorf T, Waiczies S (2013) Visualizing brain inflammation with a shingled-leg radio-frequency head probe for 19F/1H MRI. Sci Rep 3:1280. https://doi.org/10.1038/srep01280 CrossRefPubMedPubMedCentral

27.

Fox MS, Gaudet JM, Foster PJ (2015) Fluorine-19 MRI contrast agents for cell tracking and lung imaging. Magn Reson Insights 8(Suppl 1):53–67. https://doi.org/10.4137/MRI.S23559 CrossRefPubMed

28.

Morawski AM, Winter PM, Yu X, Fuhrhop RW, Scott MJ, Hockett F, Robertson JD, Gaffney PJ, Lanza GM, Wickline SA (2004) Quantitative “magnetic resonance immunohistochemistry” with ligand-targeted (19)F nanoparticles. Magn Reson Med 52(6):1255–1262. https://doi.org/10.1002/mrm.20287 CrossRefPubMed

29.

Higuchi M, Iwata N, Matsuba Y, Sato K, Sasamoto K, Saido TC (2005) 19F and 1H MRI detection of amyloid beta plaques in vivo. Nat Neurosci 8(4):527–533. https://doi.org/10.1038/nn1422 CrossRefPubMed

30.

Winter PM, Morawski AM, Caruthers SD, Fuhrhop RW, Zhang H, Williams TA, Allen JS, Lacy EK, Robertson JD, Lanza GM, Wickline SA (2003) Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation 108(18):2270–2274. https://doi.org/10.1161/01.CIR.0000093185.16083.95 CrossRefPubMed

31.

Thomas SR, Pratt RG, Millard RW, Samaratunga RC, Shiferaw Y, McGoron AJ, Tan KK (1996) In vivo PO2 imaging in the porcine model with perfluorocarbon F-19 NMR at low field. Magn Reson Imaging 14(1):103–114CrossRef

32.

Stevens AN, Morris PG, Iles RA, Sheldon PW, Griffiths JR (1984) 5-fluorouracil metabolism monitored invivo by F-19 Nmr. Brit J Cancer 50(1):113–117CrossRef

33.

Deutsch CJ, Taylor JS (1989) New class of 19F pH indicators: fluoroanilines. Biophys J 55(4):799–804. https://doi.org/10.1016/S0006-3495(89)82879-6 CrossRefPubMedPubMedCentral

34.

Deutsch CJ, Taylor JS (1987) Intracellular pH as measured by 19F NMR. Ann N Y Acad Sci 508:33–47CrossRef

35.

Metcalfe JC, Hesketh TR, Smith GA (1985) Free cytosolic Ca-2 + measurements with fluorine labeled indicators using F-19-Nmr. Cell Calcium 6(1–2):183–195CrossRef

36.

Du WJ, Xu ZQ, Nystrom AM, Zhang K, Leonard JR, Wooley KL (2008) F-19- and fluorescently labeled micelles as nanoscopic assemblies for chemotherapeutic Delivery. Bioconjugate Chem 19(12):2492–2498CrossRef

37.

Schmieder AH, Caruthers SD, Keupp J, Wickline SA, Lanza GM (2015) Recent advances in (19)Fluorine magnetic resonance imaging with perfluorocarbon emulsions. Engineering (Beijing) 1(4):475–489. https://doi.org/10.15302/J-ENG-2015103 CrossRef

38.

Ashur I, Allouche-Arnon H, Bar-Shir A (2018) Calcium fluoride nanocrystals: tracers for in vivo (19) F magnetic resonance imaging. Angew Chem Int Ed Engl 57(25):7478–7482. https://doi.org/10.1002/anie.201800838 CrossRefPubMed

39.

Kolouchova K, Sedlacek O, Jirak D, Babuka D, Blahut J, Kotek J, Vit M, Trousil J, Konefal R, Janouskova O, Podhorska B, Slouf M, Hruby M (2018) Self-assembled thermoresponsive polymeric nanogels for (19)F MR imaging. Biomacromolecules. https://doi.org/10.1021/acs.biomac.8b00812 CrossRefPubMed

40.

Sedlacek O, Jirák D, Gálisová A, Jager E, Laaser JE, Lodge TP, Stepanek P, Hrubý M (2018) ¹⁹F magnetic resonance imaging of injectable polymeric implants with multiresponsive behavior. Chem Mater 30(15):4892–4896CrossRef

41.

Peng H, Blakey I, Dargaville B, Rasoul F, Whittaker AK (2009) Effect of solvent quality on the solution properties of assemblies of amphiphilic diblock copolymers as potential F-19 MRI agents. Abstr Pap Am Chem S:238

42.

Tirotta I, Mastropietro A, Cordiglieri C, Gazzera L, Baggi F, Baselli G, Bruzzone MG, Zucca I, Cavallo G, Terraneo G, Baldelli Bombelli F, Metrangolo P, Resnati G (2014) A superfluorinated molecular probe for highly sensitive in vivo(19)F-MRI. J Am Chem Soc 136(24):8524–8527. https://doi.org/10.1021/ja503270n CrossRefPubMed

43.

Gálisova A, Herynek V, Swider E, Sticová E, Pátiková A, Kosinová L, Kříž J, Hájek M, Srinivas M, Jirák D (2018) A trimodal imaging platform for tracking viable transplanted pancreatic islets in vivo: 19F MR, fluorescence and bioluminescence imaging. Mol Imaging Biol. https://doi.org/10.1007/s11307-018-1270-3 CrossRefPubMedCentral

44.

Srinivas M, Boehm-Sturm P, Figdor CG, de Vries IJ, Hoehn M (2012) Labeling cells for in vivo tracking using (19)F MRI. Biomaterials 33(34):8830–8840. https://doi.org/10.1016/j.biomaterials.2012.08.048 CrossRefPubMed

45.

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

46.

Waiczies H, Guenther M, Skodowski J, Lepore S, Pohlmann A, Niendorf T, Waiczies S (2013) Monitoring dendritic cell migration using 19F/1H magnetic resonance imaging. J Vis Exp 73:e50251. https://doi.org/10.3791/50251 CrossRef

47.

Weibel S, Basse-Luesebrink TC, Hess M, Hofmann E, Seubert C, Langbein-Laugwitz J, Gentschev I, Sturm VJF, Ye Y, Kampf T, Jakob PM, Szalay AA (2013) Imaging of intratumoral inflammation during oncolytic virotherapy of tumors by F-19-magnetic resonance imaging (MRI). Plos One 8(2):e56317. https://doi.org/10.1371/journal.pone.0056317 CrossRefPubMedPubMedCentral

48.

Ahrens ET, Bulte JWM (2013) Tracking immune cells in vivo using magnetic resonance imaging. Nat Rev Immunol 13(10):755–763CrossRef

49.

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

50.

Nakstad B, Kahler H, Wolfson MR, Lindemann R, Fugelseth D, Shaffer TH, Lyberg T (1999) Perfluorocarbon chemicals do not induce inflammatory responses in human blood leukocytes. Pediatr Res 45(4):214a. https://doi.org/10.1203/00006450-199904020-01272 CrossRef

51.

Nystrom AM, Bartels JW, Du W, Wooley KL (2009) Perfluorocarbon-loaded shell crosslinked knedel-like nanoparticles: lessons regarding polymer mobility and self-assembly. J Polym Sci Pol Chem 47(4):1023–1037. https://doi.org/10.1002/pola.23184 CrossRef

52.

Cheng C, Powell KT, Khoshdel E, Wooley KL (2007) Polydimethylsiloxane-(PDMS-) grafted fluorocopolymers by a “grafting through” strategy based on atom transfer radical (Co)polymerization. Macromolecules 40(20):7195–7207. https://doi.org/10.1021/ma070845w CrossRef

53.

Ahrens ET, Zhong J (2013) In vivo MRI cell tracking using perfluorocarbon probes and fluorine-19 detection. NMR Biomed 26(7):860–871CrossRef

54.

Smith GA, Hesketh RT, Metcalfe JC, Feeney J, Morris PG (1983) Intracellular calcium measurements by F-19 Nmr of fluorine-labeled chelators. Proc Natl Acad Sci-Biol 80(23):7178–7182CrossRef

55.

Robinson SP, Griffiths JR (2004) Current issues in the utility of F-19 nuclear magnetic resonance methodologies for the assessment of tumour hypoxia. Philos T Roy Soc B 359(1446):987–996CrossRef

56.

Bar-Shir A, Yadav NN, Gilad AA, van Zijl PCM, McMahon MT, Bulte JWM (2015) Single F-19 probe for simultaneous detection of multiple metal ions using miCEST MRI. J Am Chem Soc 137(1):78–81CrossRef

57.

Srinivas M, Cruz LJ, Bonetto F, Heerschap A, Figdor CG, de Vries IJ (2010) Customizable, multi-functional fluorocarbon nanoparticles for quantitative in vivo imaging using 19F MRI and optical imaging. Biomaterials 31(27):7070–7077. https://doi.org/10.1016/j.biomaterials.2010.05.069 CrossRefPubMed

58.

Jacoby C, Temme S, Mayenfels F, Benoit N, Krafft MP, Schubert R, Schrader J, Flogel U (2014) Probing different perfluorocarbons for in vivo inflammation imaging by 19F MRI: image reconstruction, biological half-lives and sensitivity. NMR Biomed 27(3):261–271. https://doi.org/10.1002/nbm.3059 CrossRefPubMed

59.

Krafft MP, Riess JG (2007) Perfluorocarbons: Life sciences and biomedical uses—dedicated to the memory of Professor Guy Ourisson, a true RENAISSANCE man. J Polym Sci Pol Chem 45(7):1185–1198. https://doi.org/10.1002/pola.21937 CrossRef

60.

Mason RP, Antich PP, Babcock EE, Gerberich JL, Nunnally RL (1989) Perfluorocarbon imaging invivo—a F-19 Mri study in tumor-bearing mice. Magn Reson Imaging 7(5):475–485. https://doi.org/10.1016/0730-725x(89)90402-5 CrossRefPubMed

61.

Shimizu M, Kobayashi T, Morimoto H, Matsuura N, Shimano T, Nomura N, Itoh S, Yamazaki M, Iriguchi N, Yamamoto T, Yamai S, Furuta T, Maki T, Mori T (1987) Tumor imaging with anti-Cea antibody labeled F-19 emulsion. Magnet Reson Med 5(3):290–295. https://doi.org/10.1002/mrm.1910050311 CrossRef

62.

Zhang C, Moonshi SS, Han YX, Puttick S, Peng H, Magoling BJA, Reid LC, Bernardi S, Searles DJ, Kral P, Whittaker AK (2017) PFPE-based polymeric F-19 MRI agents: a new class of contrast agents with outstanding sensitivity. Macromolecules 50(15):5953–5963. https://doi.org/10.1021/acs.macromol.7b01285 CrossRef

63.

Peng H, Thurecht KJ, Blakey I, Taran E, Whittaker AK (2012) Effect of solvent quality on the solution properties of assemblies of partially fluorinated amphiphilic diblock copolymers. Macromolecules 45(21):8681–8690CrossRef

64.

Peng H, Blakey I, Dargaville B, Rasoul F, Rose S, Whittaker AK (2009) Synthesis and evaluation of partly fluorinated block copolymers as MRI imaging agents. Biomacromol 10(2):374–381. https://doi.org/10.1021/bm801136m CrossRef

65.

Mao J, Ni PH, Mai YY, Yan DY (2007) Multicompartment micelles from hyperbranched star-block copolymers containing polycations and fluoropolymer segment. Langmuir 23(9):5127–5134. https://doi.org/10.1021/la063576w CrossRefPubMed

66.

Yusa S, Yamamoto T, Hashidzume A, Morishima Y (2002) Synthesis and characterization of self-associative perfluoroalkyl-end-capped polystyrene. Polym J 34(3):117–124. https://doi.org/10.1295/polymj.34.117 CrossRef

67.

Andruzzi L, Chiellini E, Galli G, Li XF, Kang SH, Ober CK (2002) Engineering low surface energy polymers through molecular design: synthetic routes to fluorinated polystyrene-based block copolymers. J Mater Chem 12(6):1684–1692. https://doi.org/10.1039/b200891b CrossRef

68.

Shi ZQ, Holdcroft S (2005) Synthesis and proton conductivity of partially sulfonated poly([vinylidene difluoride-co-hexafluoropropylene]-b-styrene) block copolymers. Macromolecules 38(10):4193–4201. https://doi.org/10.1021/ma0477549 CrossRef

69.

Destarac M, Matyjaszewski K, Silverman E, Ameduri B, Boutevin B (2000) Atom transfer radical polymerization initiated with vinylidene fluoride telomers. Macromolecules 33(13):4613–4615. https://doi.org/10.1021/ma9918351 CrossRef

70.

Lebreton P, Ameduri B, Boutevin B, Corpart JM (2002) Use of original omega-perfluorinated dithioesters for the synthesis of well-controlled polymers by reversible addition-fragmentation chain transfer (RAFT). Macromol Chem Phys 203(3):522–537CrossRef

71.

Monteiro MJ, Adamy MM, Leeuwen BJ, van Herk AM, Destarac M (2005) A “living” radical ab initio emulsion polymerization of styrene using a fluorinated xanthate agent. Macromolecules 38(5):1538–1541. https://doi.org/10.1021/ma0478557 CrossRef

72.

Sawada H (1996) Fluorinated peroxides. Chem Rev 96(5):1779–1808. https://doi.org/10.1021/cr9411482 CrossRefPubMed

73.

Sawada H, Ikeno K, Kawase T (2002) Synthesis of amphiphilic fluoroalkoxyl end-capped cooligomers containing oxime-blocked isocyanato segments: architecture and applications of new self-assembled fluorinated molecular aggregates. Macromolecules 35(11):4306–4313. https://doi.org/10.1021/ma012217z CrossRef

74.

Boutevin B, Diaf KO, Pietrasanta Y, Taha M (1986) Synthesis of Block cotelomers involving a perfluorinated chain and a hydrophilic chain. 1. Use of Fluorinated Telogens with Trichloromethyl End Groups. J Polym Sci Pol Chem 24(11):3129–3137. https://doi.org/10.1002/pola.1986.080241137 CrossRef

75.

Su ZH, Wu DC, Hsu SL, McCarthy TJ (1997) Adsorption of end-functionalized poly(ethylene oxide)s to the poly(ethylene oxide)-air interface. Macromolecules 30(4):840–845. https://doi.org/10.1021/ma961396v CrossRef

76.

Kaberov LI, Verbraeken B, Hruby M, Riabtseva A, Kovacik L, Kereiche S, Brus J, Stepanek P, Hoogenboom R, Filippov SK (2017) Novel triphilic block copolymers based on poly(2-methyl-2oxazoline)-block-poly(2-octyl-2-oxazoline) with different terminal perfluoroalkyl fragments: synthesis and self-assembly behaviour. Eur Polym J 88:645–655CrossRef

77.

Aasen SN, Pospisilova A, Eichler TW, Panek J, Hruby M, Stepanek P, Spriet E, Jirak D, Skaftnesmo KO, Thorsen F (2015) A novel nanoprobe for multimodal imaging is effectively incorporated into human melanoma metastatic cell lines. Int J Mol Sci 16(9):21658–21680. https://doi.org/10.3390/ijms160921658 CrossRefPubMedPubMedCentral

78.

Langereis S, Keupp J, van Velthoven JLJ, de Roos IHC, Burdinski D, Pikkemaat JA, Grull H (2009) A temperature-sensitive liposomal H-1 CEST and F-19 contrast agent for mr image-guided drug delivery. J Am Chem Soc 131(4):1380–1381CrossRef

79.

Navath RS, Menjoge AR, Wang B, Romero R, Kannan S, Kannan RM (2010) Amino acid-functionalized dendrimers with heterobifunctional chemoselective peripheral groups for drug delivery applications. Biomacromol 11(6):1544–1563CrossRef

80.

Thurecht KJ, Blakey I, Peng H, Squires O, Hsu S, Alexander C, Whittaker AK (2010) Functional hyperbranched polymers: toward targeted in vivo F-19 magnetic resonance imaging using designed macromolecules. J Am Chem Soc 132(15):5336–5337CrossRef

81.

Rabyk M, Galisova A, Jiratova M, Patsula V, Srbova L, Loukotova L, Parnica J, Jirak D, Stepanek P, Hruby M (2018) Mannan-based conjugates as a multimodal imaging platform for lymph nodes. J Mater Chem B 6(17):2584–2596CrossRef

82.

Hruby M, Filippov SK, Stepanek P (2016) Supramolecular structures and self-association processes in polymer systems. Physiol Res 65 (Supplementum 2):S165–S178

83.

Skodova M, Hruby M, Filippov SK, Karlsson G, Mackova H, Spirkova M, Kankova D, Steinhart M, Stepanek P, Ulbrich K (2011) Novel polymeric nanoparticles assembled by metal ion addition. Macromol Chem Phys 212(21):2339–2348CrossRef

84.

Hruby M, Konak C, Kucka J, Vetrik M, Filippov SK, Vetvicka D, Mackova H, Karlsson G, Edwards K, Rihova B, Ulbrich K (2009) Thermoresponsive, hydrolytically degradable polymer micelles intended for radionuclide delivery. Macromol Biosci 9(10):1016–1027CrossRef

85.

Dardzinski BJ, Sotak CH (1994) Rapid tissue oxygen tension mapping using 19F inversion-recovery echo-planar imaging of perfluoro-15-crown-5-ether. Magn Reson Med 32(1):88–97CrossRef

86.

Lee H, Price RR, Holburn GE, Partain CL, Adams MD, Cacheris WP (1994) In vivo fluorine-19 MR imaging: relaxation enhancement with Gd-DTPA. J Magn Reson Imaging 4(4):609–613CrossRef

87.

Nam SY, Ricles LM, Suggs LJ, Emelianov SY (2015) Imaging strategies for tissue engineering applications. Tissue Eng Part B-Re 21(1):88–102CrossRef

88.

Chalmers KH, Kenwright AM, Parker D, Blamire AM (2011) (19)F-lanthanide complexes with increased sensitivity for (19)F-MRI: optimization of the MR acquisition. Magnet Reson Med 66(4):931–936CrossRef

89.

Bouchoucha M, van Heeswijk RB, Gossuin Y, Kleitz F, Fortin MA (2017) Fluorinated mesoporous silica nanoparticles for binuclear probes in H-1 and F-19 magnetic resonance imaging. Langmuir 33(40):10531–10542CrossRef

90.

Longmire M, Choyke PL, Kobayashi H (2008) Clearance properties of nano-sized particles and molecules as imaging agents: considerations and caveats. Nanomedicine (Lond) 3(5):703–717. https://doi.org/10.2217/17435889.3.5.703 CrossRef

91.

Jokerst JV, Lobovkina T, Zare RN, Gambhir SS (2011) Nanoparticle PEGylation for imaging and therapy. Nanomedicine (Lond) 6(4):715–728. https://doi.org/10.2217/nnm.11.19 CrossRef

92.

Brown GO, Bergquist C, Ferm P, Wooley KL (2005) Unusual, promoted release of guests from amphiphilic cross-linked polymer networks. J Am Chem Soc 127(32):11238–11239. https://doi.org/10.1021/ja0534405 CrossRefPubMed

93.

Du WJ, Nystrom AM, Zhang L, Powell KT, Li YL, Cheng C, Wickline SA, Wooley KL (2008) Amphiphilic hyperbranched fluoropolymers as nanoscopic (19)F magnetic resonance imaging agent assemblies. Biomacromol 9(10):2826–2833CrossRef

94.

Nurmi L, Peng H, Seppala J, Haddleton DM, Blakey I, Whittaker AK (2010) Synthesis and evaluation of partly fluorinated polyelectrolytes as components in F-19 MRI-detectable nanoparticles. Polym Chem-Uk 1(7):1039–1047CrossRef

95.

Loukotova L, Kucka J, Rabyk M, Hocherl A, Venclikova K, Janouskova O, Paral P, Kolarova V, Heizer T, Sefc L, Stepanek P, Hruby M (2017) Thermoresponsive beta-glucan-based polymers for bimodal immunoradiotherapy—are they able to promote the immune system? J Control Release 268:78–91. https://doi.org/10.1016/j.jconrel.2017.10.010 CrossRefPubMed

96.

Zhang H, Ni PH, He JL, Liu CC (2008) Novel fluoroalkyl end-capped amphiphilic diblock copolymers with pH/temperature response and self-assembly behavior. Langmuir 24(9):4647–4654CrossRef

97.

Hoffman AS (2008) The origins and evolution of “controlled” drug delivery systems. J Control Release 132(3):153–163. https://doi.org/10.1016/j.jconrel.2008.08.012 CrossRefPubMed

98.

Maeda H (2010) Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects. Bioconjug Chem 21(5):797–802. https://doi.org/10.1021/bc100070g CrossRefPubMed

99.

Talelli M, Rijcken CJ, van Nostrum CF, Storm G, Hennink WE (2010) Micelles based on HPMA copolymers. Adv Drug Deliv Rev 62(2):231–239. https://doi.org/10.1016/j.addr.2009.11.029 CrossRefPubMed

100.

Hruby M, Filippov SK, Panek J, Novakova M, Mackova H, Kucka J, Vetvicka D, Ulbrich K (2010) Polyoxazoline thermoresponsive micelles as radionuclide delivery systems. Macromol Biosci 10(8):916–924. https://doi.org/10.1002/mabi.201000034 CrossRefPubMed

101.

Jiratova M, Pospisilova A, Rabyk M, Parizek M, Kovar J, Galisova A, Hruby M, Jirak D (2018) Biological characterization of a novel hybrid copolymer carrier system based on glycogen. Drug Deliv Transl Res 8(1):73–82. https://doi.org/10.1007/s13346-017-0436-x CrossRefPubMed

102.

Kucka J, Hruby M, Konak C, Kozempel J, Lebeda O (2006) Astatination of nanoparticles containing silver as possible carriers of 211At. Appl Radiat Isot 64(2):201–206. https://doi.org/10.1016/j.apradiso.2005.07.021 CrossRefPubMed

103.

Sedlacek O, Monnery BD, Filippov SK, Hoogenboom R, Hruby M (2012) Poly(2-oxazoline)s–are they more advantageous for biomedical applications than other polymers? Macromol Rapid Commun 33(19):1648–1662. https://doi.org/10.1002/marc.201200453 CrossRefPubMed

104.

Fu CK, Herbst S, Zhang C, Whittaker AK (2017) Polymeric F-19 MRI agents responsive to reactive oxygen species. Polym Chem-Uk 8(31):4585–4595CrossRef

105.

Bogomolova A, Kaberov L, Sedlacek O, Filippov SK, Stepanek P, Kral V, Wang XY, Liu SL, Ye XD, Hruby M (2016) Double stimuli-responsive polymer systems: how to use crosstalk between pH- and thermosensitivity for drug depots. Eur Polym J 84:54–64CrossRef

106.

Schmaljohann D (2006) Thermo- and pH-responsive polymers in drug delivery. Adv Drug Deliver Rev 58(15):1655–1670. https://doi.org/10.1016/j.addr.2006.09.020 CrossRef

Title: Fluorine polymer probes for magnetic resonance imaging: quo vadis?
Authors: Daniel Jirak
Andrea Galisova
Kristyna Kolouchova
David Babuka
Martin Hruby
Publication date: 01-02-2019
Publisher: Springer International Publishing
Published in: Magnetic Resonance Materials in Physics, Biology and Medicine / Issue 1/2019
Print ISSN: 0968-5243
Electronic ISSN: 1352-8661
DOI: https://doi.org/10.1007/s10334-018-0724-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Fluorine polymer probes for magnetic resonance imaging: quo vadis?

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2019

Urinary detection of corticosteroid in topical treatment of skin disease by 19F MRS

A dual 1H/19F birdcage coil for small animals at 7 T MRI

Longitudinal 19F magnetic resonance imaging of brain oxygenation in a mouse model of vascular cognitive impairment using a cryogenic radiofrequency coil

A 19F magnetic resonance imaging-based diagnostic test for bile acid diarrhea

Quantitative 19F MRI of perfluoro-15-crown-5-ether using uniformity correction of the spin excitation and signal reception

Fluorine-19 MRI at 21.1 T: enhanced spin–lattice relaxation of perfluoro-15-crown-5-ether and sensitivity as demonstrated in ex vivo murine neuroinflammation