Porphyrin–phospholipid liposomes permeabilized by near-infrared light

Abstract

The delivery of therapeutic compounds to target tissues is a central challenge in treating disease. Externally controlled drug release systems hold potential to selectively enhance localized delivery. Here we describe liposomes doped with porphyrin–phospholipid that are permeabilized directly by near-infrared light. Molecular dynamics simulations identified a novel light-absorbing monomer esterified from clinically approved components predicted and experimentally demonstrated to give rise to a more stable porphyrin bilayer. Light-induced membrane permeabilization is enabled with liposomal inclusion of 10 molar % porphyrin–phospholipid and occurs in the absence of bulk or nanoscale heating. Liposomes reseal following laser exposure and permeability is modulated by varying porphyrin–phospholipid doping, irradiation intensity or irradiation duration. Porphyrin–phospholipid liposomes demonstrate spatial control of release of entrapped gentamicin and temporal control of release of entrapped fluorophores following intratumoral injection. Following systemic administration, laser irradiation enhances deposition of actively loaded doxorubicin in mouse xenografts, enabling an effective single-treatment antitumour therapy.

References 58

1. 1.

   Peer D.. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotech. 2, 751–760 (2007 ).

   Not in our library10.1038/nnano.2007.387

2. 2.

   Allen T. M. & Cullis P. R. Liposomal drug delivery systems: from concept to clinical applications. Adv. Drug Deliv. Rev. 65, 36–48 (2013 ).

   Not in our library10.1016/j.addr.2012.09.037

3. 3.

   Li S.-D. & Huang L. Pharmacokinetics and biodistribution of nanoparticles. Mol. Pharm. 5, 496–504 (2008 ).

   Not in our library10.1021/mp800049w

4. 4.

   Alexis F., Pridgen E., Molnar L. K. & Farokhzad O. C. Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol. Pharm. 5, 505–515 (2008 ).

   Not in our library10.1021/mp800051m

5. 5.

   Timko B. P., Dvir T. & Kohane D. S. Remotely triggerable drug delivery systems. Adv. Mater. 22, 4925–4943 (2010 ).

   Not in our library10.1002/adma.201002072

6. 6.

   Fleige E., Quadir M. A. & Haag R. Stimuli-responsive polymeric nanocarriers for the controlled transport of active compounds: concepts and applications. Adv. Drug Deliv. Rev. 64, 866–884 (2012 ).

   Not in our library10.1016/j.addr.2012.01.020

7. 7.

   Ganta S., Devalapally H., Shahiwala A. & Amiji M. A review of stimuli-responsive nanocarriers for drug and gene delivery. J. Control. Release 126, 187–204 (2008 ).

   Not in our library10.1016/j.jconrel.2007.12.017

8. 8.
   Bioresponsive matrices in drug delivery · 2010

   Not checked
9. 9.

   Preiss M. R. Stimuli-responsive liposome-nanoparticle assemblies. Exp. Opin. Drug Deliv. 8, 1025–1040 (2011 ).

   Not in our library10.1517/17425247.2011.584868

10. 10.

    Yatvin M. B., Weinstein J. N., Dennis W. H. & Blumenthal R. Design of liposomes for enhanced local release of drugs by hyperthermia. Science 202, 1290–1293 (1978 ).

    Not in our library10.1126/science.364652

11. 11.

    Needham D., Anyarambhatla G., Kong G. & Dewhirst M. W. A new temperature-sensitive liposome for use with mild hyperthermia: characterization and testing in a human tumor xenograft model. Cancer Res. 60, 1197–1201 (2000 ).

    Not in our library

12. 12.

    Kong G.. Efficacy of liposomes and hyperthermia in a human tumor xenograft model: importance of triggered drug release. Cancer Res. 60, 6950–6957 (2000 ).

    Not in our library

13. 13.

    Manzoor A. A.. Overcoming limitations in nanoparticle drug delivery: triggered, intravascular release to improve drug penetration into tumors. Cancer Res. 72, 5566–5575 (2012 ).

    Not in our library10.1158/0008-5472.can-12-1683

14. 14.

    Dromi S.. Pulsed-high intensity focused ultrasound and low temperature–sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin. Cancer Res. 13, 2722–2727 (2007 ).

    Not in our library10.1158/1078-0432.ccr-06-2443

15. 15.

    Babincová M., Čičmanec P., Altanerová V., Altaner Č. & Babinec P. AC-magnetic field controlled drug release from magnetoliposomes: design of a method for site-specific chemotherapy. Bioelectrochemistry 55, 17–19 (2002 ).

    Not in our library10.1016/s1567-5394(01)00171-2

16. 16.

    Amstad E.. Triggered release from liposomes through magnetic actuation of iron oxide nanoparticle containing membranes. Nano Lett. 11, 1664–1670 (2011 ).

    Not in our library10.1021/nl2001499

17. 17.

    Troutman T. S., Leung S. J. & Romanowski M. Light-induced content release from plasmon-resonant liposomes. Adv. Mater. 21, 2334–2338 (2009 ).

    Not in our library10.1002/adma.200900018

18. 18.

    Volodkin D. V., Skirtach A. G. & Möhwald H. Near‐IR remote release from assemblies of liposomes and nanoparticles. Angew. Chem. Int. Ed. Engl. 48, 1807–1809 (2009 ).

    Not in our library10.1002/anie.200805572

19. 19.

    Wu G.. Remotely triggered liposome release by near-infrared light absorption via hollow gold nanoshells. J. Am. Chem. Soc. 130, 8175–8177 (2008 ).

    Not in our library10.1021/ja802656d

20. 20.

    Agarwal A., Mackey M. A., El-Sayed M. A. & Bellamkonda R. V. Remote triggered release of doxorubicin in tumors by synergistic application of thermosensitive liposomes and gold nanorods. ACS Nano 5, 4919–4926 (2011 ).

    Not in our library10.1021/nn201010q

21. 21.

    You J., Zhang G. & Li C. Exceptionally high payload of doxorubicin in hollow gold nanospheres for near-infrared light-triggered drug release. ACS Nano 4, 1033–1041 (2010 ).

    Not in our library10.1021/nn901181c

22. 22.

    Yavuz M. S.. Gold nanocages covered by smart polymers for controlled release with near-infrared light. Nat. Mater. 8, 935–939 (2009 ).

    Not in our library10.1038/nmat2564

23. 23.

    Shum P., Kim J.-M. & Thompson D. H. Phototriggering of liposomal drug delivery systems. Adv. Drug Deliv. Rev. 53, 273–284 (2001 ).

    Not in our library10.1016/s0169-409x(01)00232-0

24. 24.

    Al-Jamal W. T., Al-Ahmady Z. S. & Kostarelos K. Pharmacokinetics & tissue distribution of temperature-sensitive liposomal doxorubicin in tumor-bearing mice triggered with mild hyperthermia. Biomaterials 33, 4608–4617 (2012 ).

    Not in our library10.1016/j.biomaterials.2012.03.018

25. 25.

    Kong G., Braun R. D. & Dewhirst M. W. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res. 61, 3027–3032 (2001 ).

    Not in our library

26. 26.

    Pagliari L. J.. The multidomain proapoptotic molecules Bax and Bak are directly activated by heat. Proc. Natl Acad. Sci. USA 102, 17975–17980 (2005 ).

    Not in our library10.1073/pnas.0506712102

27. 27.

    Lovell J. F.. Porphysome nanovesicles generated by porphyrin bilayers for use as multimodal biophotonic contrast agents. Nat. Mater. 10, 324–332 (2011 ).

    Not in our library10.1038/nmat2986

28. 28.

    Lovell J. F.. Enzymatic regioselection for the synthesis and biodegradation of porphysome nanovesicles. Angew. Chem. Int. Ed. Engl. 51, 2429–2433 (2012 ).

    Not in our library10.1002/anie.201108280

29. 29.

    Jin C. S., Lovell J. F., Chen J. & Zheng G. Ablation of hypoxic tumors with dose-equivalent photothermal, but not photodynamic, therapy using a nanostructured porphyrin assembly. ACS Nano 7, 2541–2550 (2013 ).

    Not in our library10.1021/nn3058642

30. 30.

    Ethirajan M., Chen Y., Joshi P. & Pandey R. K. The role of porphyrin chemistry in tumor imaging and photodynamic therapy. Chem. Soc. Rev. 40, 340 (2011 ).

    Not in our library10.1039/b915149b

31. 31.

    Lingwood D.. Cholesterol modulates glycolipid conformation and receptor activity. Nat. Chem. Biol. 7, 260–262 (2011 ).

    Not in our library10.1038/nchembio.551

32. 32.

    Róg T., Pasenkiewicz-Gierula M., Vattulainen I. & Karttunen M. What happens if cholesterol is made smoother: importance of methyl substituents in cholesterol ring structure on phosphatidylcholine-sterol interaction. Biophys. J. 92, 3346–3357 (2007 ).

    Not in our library10.1529/biophysj.106.095497

33. 33.

    Oostenbrink C., Soares T. A., van der Vegt N. F. A. & van Gunsteren W. F. Validation of the 53A6 GROMOS force field. Eur. Biophys. J. 34, 273–284 (2005 ).

    Not in our library10.1007/s00249-004-0448-6

34. 34.

    Harris J. M. & Chess R. B. Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. 2, 214–221 (2003 ).

    Not in our library10.1038/nrd1033

35. 35.

    Chang H.-I. & Cheng M.-Y. Clinically-proven liposome-based drug delivery: formulation, characterization and therapeutic efficacy. J. Nanomed. Biother. Discov. 01, (2012 ).

    Not in our library

36. 36.

    Coderch L.. Influence of cholesterol on liposome fluidity by EPR: relationship with percutaneous absorption. J. Control. Release 68, 85–95 (2000 ).

    Not in our library10.1016/s0168-3659(00)00240-6

37. 37.

    Huang Z., Jaafari M. R. & Szoka F. C. Disterolphospholipids: nonexchangeable lipids and their application to liposomal drug delivery. Angew. Chem. Int. Ed. Engl. 121, 4210–4213 (2009 ).

    Not in our library10.1002/anie.200900111

38. 38.

    Lovell J. F.. FRET quenching of photosensitizer singlet oxygen generation. J. Phys. Chem. B 113, 3203–3211 (2009 ).

    Not in our library10.1021/jp810324v

39. 39.

    Charrois G. J. R. & Allen T. M. Drug release rate influences the pharmacokinetics, biodistribution, therapeutic activity, and toxicity of pegylated liposomal doxorubicin formulations in murine breast cancer. Biochim. Biophys. ActaBiomembranes 1663, 167–177 (2004 ).

    Not in our library10.1016/j.bbamem.2004.03.006

40. 40.

    Drulis-Kawa Z. & Dorotkiewicz-Jach A. Liposomes as delivery systems for antibiotics. Int. J. Pharm. 387, 187–198 (2010 ).

    Not in our library10.1016/j.ijpharm.2009.11.033

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