Photodynamic Opening of the Blood–Brain Barrier and the Meningeal Lymphatic System: The New Niche in Immunotherapy for Brain Tumors
Abstract
:1. Photodynamic Therapy of Glioblastoma
2. Photodynamic Opening of the Blood–Brain Barrier
3. PDT-OBBB Modulation of Brain Tumor Immunity
4. Limitations of PDT in Therapy of GBT
First Author, Year | Tissues, mm/Laser, nm | Penetration Depth (mm) and Transmittance (%) |
---|---|---|
Wan et al., 1981 [133] | Scalp + Skull, 9–13 mm | |
400 nm | 10−5–10−4% | |
546 nm | 2 × 10−4–8 × 10−4% | |
630 nm | 2 × 10−3–9 × 10−3% | |
664 nm | 2 × 10−2% | |
703 nm | 3–10−2% | |
856 nm | 2 × 10−2–8 × 10−2% | |
Lychagov et al., 2006 [134] | Skull, 4–14 mm, 810 nm | 1–16% |
Scalp and skull, 7–20 mm, 810 nm | 0.5–5% | |
Svaasand and Ellingsen, 1983 [135] | ♂ Neonatal brain | |
♀ Adult brain | ||
488 nm | ♂ 1.3 mm ♀ 0.4 mm | |
514 nm | ♂ 1.1 mm ♀ 0.4 mm | |
660 nm | ♂ 3.7 mm ♀ 1.2 mm | |
1060 nm | ♂ 7.1 mm ♀ 3.2 mm | |
Stolik et al., 2000 [136] | Adult brain | |
632 nm | 0.92 mm | |
675 nm | 1.38 mm | |
780 nm | 2.17 mm | |
835 nm | 2.52 mm | |
Jagdeo et al., 2012 [137] | Skull 5 mm | |
633 mm | Left parietal lobe 3% | |
Right parietal lobe 3.7% | ||
Frontal lobe 1% | ||
830 mm | Left parietal lobe 9% | |
Right parietal lobe 9.2% | ||
Frontal lobe 5.9% | ||
Yue et al., 2015 [138] | Scalp, skull, and adult brain (total 60 mm) | |
850 nm | Parietal, occipital, temporal, and frontal lobes, 10−4–10−3% | |
Barett and Gonzalez-Lima, 2013 [139] | Skull | |
1064 nm | Frontal lobe 2% |
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
A List of Abbreviations
5-ALA | 5-Aminolevulinic acid |
ARRB1 | Arrestin beta-1 |
Ca | Calcium |
CNS | Central nervous system |
CLDN-5 | Claudin-5 |
CCL-21 | Chemokine (C-C motif) ligand 21 |
CCR7 | C-such as C chemokine receptor type 7 |
CTLA-4 | Cytotoxic T lymphocyte associated protein 4 |
DAMPs | Damage-associated molecular patterns |
dcLNs | Deep cervical lymph nodes |
FDA | Food and Drug Administration |
FaDu | Cancer cell—hypopharyngeal carcinoma cell line |
GM1 | Ganglioside (monosialotetrahexosylganglioside) |
GBM | Glioblastoma |
GMP | Guanosine monophosphate |
HTP | Heme-transport protein |
ICD | Immunogenic cell death |
J | Joule (unit of energy) |
JAM | Junctional adhesion molecule |
LYVE-1 | Lymphatic vessel endothelial hyaluronan receptor 1 |
Ma | Macrophages |
MLVs | Meningeal lymphatic vessels |
MST | Median survival time |
NO | Nitric oxide |
OBBB | Opening of the blood–brain barrier |
ROS | Reactive oxygen species |
PECAM-1 | Platelet/endothelial cell adhesion molecule 1, also known as cluster of differentiation 31 (CD31) |
PDT | Photodynamic therapy |
iPDT | Interstitial photodynamic therapy |
PSs | Photosensitizers |
PpIX | Protoporphyrin IX |
PD1 | programmed death-1 protein |
PTT | Photothermal therapy |
RNA | Ribonucleic acid |
TRITC-Dextran 70 kDa | Tetramethylrhodamine-isothiocyanate-dextran 70 kilodaltons |
TJ | Tight junctions |
VEGF | Vascular endothelial growth factor |
VEGF-C | Vascular endothelial growth factor C |
VEGFR3 | Vascular endothelial growth factor receptor-3 |
VE-cadherin | Vascular endothelial cadherin |
W | Watt (unit of power) |
ZO proteins | Zonula occludens proteins |
References
- Mitusova, K.; Peltek, O.O.; Karpov, T.E.; Muslimov, A.R.; Zyuzin, M.V.; Timin, A.S. Overcoming the blood–brain barrier for the therapy of malignant brain tumor: Current status and prospects of drug delivery approaches. J. Nanobiotechnol. 2022, 20, 412–463. [Google Scholar] [CrossRef] [PubMed]
- Brain, Central Nervous System. Available online: https://gco.iarc.fr/today (accessed on 11 April 2022).
- Ostrom, Q.T.; Cioffi, G.; Gittleman, H.; Patil, N.; Waite, K.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the United States in 2012–2016. Neuro. Oncol. 2019, 21, v1–v100. [Google Scholar] [CrossRef]
- Ostrom, Q.T.; Cote, D.J.; Ascha, M.; Kruchko, C.; Barnholtz-Sloan, J.S. Adult glioma incidence and survival by race or ethnicity in the United States from 2000 to 2014. JAMA Oncol. 2018, 4, 1254–1262. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Minniti, G.; Lombardi, G.; Paolini, S. Glioblastoma in elderly patients: Current management and future perspectives. Cancers 2019, 11, 336. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, R.; Cuthbert, H.; Watts, C. Fluorescence-guided surgery in the surgical treatment of gliomas: Past, present and future. Cancers 2021, 13, 3508. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.M.; Banu, M.A.; Canoll, P.; Bruce, J.N. Rationale and clinical implications of fluorescein-guided supramarginal resection in newly diagnosed high-grade glioma. Front. Oncol. 2021, 11, 666734. [Google Scholar] [CrossRef]
- Davis, M.E. Glioblastoma: Overview of disease and treatment. Clin. J. Oncol. Nurs. 2016, 20, S2–S8. [Google Scholar] [CrossRef] [Green Version]
- Neira, J.A.; Ung, T.H.; Sims, J.S.; Malone, H.R.; Chow, D.S.; Samanamud, J.L.; Zanazzi, G.J.; Guo, X.; Bowden, S.G.; Zhao, B.; et al. Aggressive resection at the infiltrative margins of glioblastoma facilitated by intraoperative fuorescein guidance. J. Neurosurg. 2017, 127, 111–122. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thon, N.; Tonn, J.C.; Kreth, F.W. The surgical perspective in precision treatment of diffuse gliomas. Onco. Targets Ther. 2019, 12, 1497–1508. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, A.C.; Ashley, D.M.; Lopez, G.Y.; Malinzak, M.; Friedman, H.S.; Khasraw, M. Management of glioblastoma: State of the art and future directions. CA Cancer J. Clin. 2020, 70, 299–312. [Google Scholar] [CrossRef] [PubMed]
- Ostrom, Q.T.; Cioffi, G.; Waite, K.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the United States in 2014–2018. Neuro. Oncol. 2021, 23, iii1–iii105. [Google Scholar] [CrossRef] [PubMed]
- Low, J.T.; Ostrom, Q.T.; Cioffi, G.; Neff, C.; Waite, K.A.; Kruchko, C.; Barnholtz-Sloan, J.S. Primary brain and other central nervous system tumors in the United States (2014-2018): A summary of the CBTRUS statistical report for clinicians. Neurooncol. Pract. 2022, 9, 165–182. [Google Scholar] [CrossRef]
- Allemani, C.; Matsuda, T.; Di Carlo, V.; Harewood, R.; Matz, M.; Nikšić, M.; Bonaventure, A.; Valkov, M.; Johnson, C.J.; Estève, J.; et al. Global surveillance of trends in cancer survival 2000–14 (CONCORD-3): Analysis of individual records for 37,513,025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018, 391, 1023–1075. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Löber-Handwerker, R.; Döring, K.; Bock, C.; Rohde, V.; Malinova, V. Defining the impact of adjuvant treatment on the prognosis of patients with inoperable glioblastoma undergoing biopsy only: Does the survival benefit outweigh the treatment effort? Neurosurg. Rev. 2022, 45, 2339–2347. [Google Scholar] [CrossRef] [PubMed]
- Omidi, Y.; Kianinejad, N.; Kwon, Y.; Omidian, H. Drug delivery and targeting to brain tumors: Considerations for crossing the blood-brain barrier. Expert Rev. Clin. Pharmacol. 2021, 14, 357–381. [Google Scholar] [CrossRef] [PubMed]
- Yesudhas, D.; Dharshini, S.A.P.; Taguchi, Y.-H.; Gromiha, M.M. Tumor heterogeneity and molecular characteristics of glioblastoma revealed by single-cell RNA-Seq data analysis. Genes 2022, 13, 428. [Google Scholar] [CrossRef] [PubMed]
- Couturier, C.P.; Ayyadhury, S.; Le, P.U.; Nadaf, J.; Monlong, J.; Riva, G.; Allache, R.; Baig, S.; Yan, X.; Bourgey, M.; et al. Single-cell RNA-seq reveals that glioblastoma recapitulates a normal neurodevelopmental hierarchy. Nat. Commun. 2020, 11, 3406. [Google Scholar] [CrossRef] [PubMed]
- Henderson, B.W.; Dougherty, T.J. How does photodynamic therapy works? Photochem. Photobiol. 1992, 55, 145–157. [Google Scholar] [CrossRef] [PubMed]
- Leroy, H.-A.; Baert, G.; Guerin, L.; Delhem, N.; Mordon, S.; Reyns, N.; Vignion-Dewalle, A.-S. Interstitial photodynamic therapy for glioblastomas: A standardized procedure for clinical use. Cancers 2021, 13, 5754. [Google Scholar] [CrossRef] [PubMed]
- Cramer, S.W.; Chen, C.C. Photodynamic therapy for the treatment of glioblastoma. Front. Surg. 2020, 6, 81. [Google Scholar] [CrossRef]
- Dupont, C.; Vermandel, M.; Leroy, H.; Quidet, M.; Lecomte, F.; Delhem, N.; Mordon, S.; Reyns, N. Intraoperative Photodynamic Therapy for Glioblastomas (INDYGO): Study protocol for a phase I clinical trial. Neurosurgery 2018, 84, E414–E419. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vermandel, M.; Dupont, C.; Lecomte, F.; Leroy, H.-A.; Tuleasca, C.; Mordon, S.; Hadjipanayis, C.G.; Reyns, N. Standardized intraoperative 5-ALA photodynamic therapy for newly diagnosed glioblastoma patients: A preliminary analysis of the INDYGO clinical trial. J. Neuro-Oncol. 2021, 152, 501–514. [Google Scholar] [CrossRef] [PubMed]
- Muragaki, Y.; Akimoto, J.; Maruyama, T.; Iseki, H.; Ikuta, S.; Nitta, M.; Maebayashi, K.; Saito, T.; Okada, Y.; Kaneko, S.; et al. Phase II clinical study on intraoperative photodynamic therapy with Talaporfin sodium and semiconductor laser in patients with malignant brain tumors: Clinical article. J. Neurosurg. 2013, 119, 845–852. [Google Scholar] [CrossRef] [PubMed]
- Hadjipanayis, C.G.; Stummer, W. 5-ALA and FDA approval for glioma surgery. J. Neurooncol. 2019, 141, 479–486. [Google Scholar] [CrossRef] [PubMed]
- Mahmoudi, K.; Garvey, K.L.; Bouras, A.; Cramer, G.; Stepp, H.; Jesu Raj, J.G.; Bozec, D.; Busch, T.M.; Hadjipanayis, C.G. 5-Aminolevulinic acid photodynamic therapy for the treatment of high-grade gliomas. J. Neurooncol. 2019, 141, 595–607. [Google Scholar] [CrossRef]
- Kaneko, S.; Fujimoto, S.; Yamaguchi, H.; Yamauchi, T.; Yoshimoto, T.; Tokuda, K. Photodynamic therapy of malignant gliomas. Prog. Neurol. Surg. 2018, 32, 1–13. [Google Scholar]
- Stepp, H.; Beck, T.; Pongraz, T.; Meinel, T.; Kreth, F.W.; Tonn, J.C.; Stummer, W. ALA and malignant glioma: Fluorescence-guided resection and photodynamic treatment. J. Environ. Pathol. Toxicol. Oncol. 2007, 21, 157–164. [Google Scholar] [CrossRef] [PubMed]
- Beck, T.J.; Kreth, F.W.; Beyer, W.; Mehrkens, J.H.; Obermeier, A.; Stepp, H.; Stummer, W.; Baumgartner, R. Interstitial photodynamic therapy of nonresectable malignant glioma recurrences using 5-aminolevulinic acid induced protoporphyrin IX. Lasers Surg. Med. 2007, 39, 386–393. [Google Scholar] [CrossRef]
- Schwartz, C.; Ruhm, A.; Tonn, J.-C.; Kreth, S.; Kreth, F.-W. Interstital photodynamic therapy of de-novo glioblastoma multiformeWHO IV. Neurooncology 2015, 17, 214–220. [Google Scholar]
- Sokolovski, S.G.; Zolotovskaya, S.A.; Goltsov, A.; Pourreyron, C.; South, A.P.; Rafailov, E.U. Infrared laser pulse triggers increased singlet oxygen production in tumour cells. Sci. Rep. 2013, 3, 3484. [Google Scholar] [CrossRef]
- Khokhlova, A.; Zolotovskii, I.; Sokolovski, S.; Saenko, Y.; Rafailov, E.; Stoliarov, D.; Pogodina, E.; Svetukhin, V.; Sibirny, V.; Fotiadi, A. The light-oxygen effect in biological cells enhanced by highly localized surface plasmon-polaritons. Sci. Rep. 2019, 9, 18435. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khokhlova, A.; Zolotovskii, I.; Stoliarov, D.; Vorsina, S.; Liamina, D.; Pogodina, E.; Fotiadi, A.A.; Sokolovski, S.G.; Saenko, Y.; Rafailov, E.U. The photobiomodulation of vital parameters of the cancer cell culture by low dose of near-IR laser Iirradiation. IEEE J. Sel. Top. Quantum Electron. 2019, 25, 1–10. [Google Scholar] [CrossRef]
- Koeller, K.K.; Henry, J.M. From the archives of the AFIP: Superficial gliomas: Radiologic-pathologic correlation. Armed Forces Institute of Pathology. Radiographics 2001, 21, 1533–1556. [Google Scholar] [CrossRef] [PubMed]
- Blionas, A.; Giakoumettis, D.; Klonou, A.; Neromyliotis, E.; Karydakis, P.; Themistocleous, M.S. Paediatric gliomas: Diagnosis, molecular biology and management. Ann. Transl. Med. 2018, 6, 251. [Google Scholar] [CrossRef]
- Hirschberg, H. Disruption of the blood–brain barrier following ALA-mediated photodynamic therapy. Lasers Surg. Med. 2008, 40, 535–542. [Google Scholar] [CrossRef] [Green Version]
- Madsen, S.J. Site-specific opening of the blood-brain barrier. J. Biophoton. 2010, 3, 356–367. [Google Scholar] [CrossRef] [Green Version]
- Madsen, S.J. Increased nanoparticle-loaded exogenous macrophage migration into the brain following PDT-induced blood-brain barrier disruption. Lasers Surg. Med. 2013, 45, 524–532. [Google Scholar] [CrossRef] [Green Version]
- Madsen, S.J. Nanoparticle-loaded macrophage mediated photothermal therapy: Potential for glioma treatment. Lasers Med. Sci. 2015, 4, 1357–1365. [Google Scholar] [CrossRef] [Green Version]
- Zhang, C.; Feng, W.; Li, Y.; Kürths, J.; Yu, T.; Semyachkina-Glushkovskaya, O.; Zhu, D. Age differences in photodynamic opening of blood-brain barrier through optical clearing skull window in mice. Lasers Surg. Med. 2019, 51, 625–633. [Google Scholar] [CrossRef]
- Zhang, C.; Feng, W.; Vodovosova, E.; Tretiakova, D.; Boldyrev, I.; Li, Y.; Kurths, J.; Yu, T.; Semyachkina-Glushkovskaya, O.; Zhu, D. Photodynamic opening of the blood-brain barrier to high weight molecules and liposomes through an optical clearing skull window. Biomed. Opt. Express 2018, 9, 4850–4862. [Google Scholar] [CrossRef]
- Semyachkina-Glushkovskaya, O.; Kurths, J.; Borisova, E.; Sokolovsky, S.; Mantareva, N.; Angelov, I.; Shirokov, A.; Navolokin, N.; Shushunova, N.; Khorovodov, A.; et al. Photodynamic opening of blood-brain barrier. Biomed. Opt. Express 2017, 8, 5040–5048. [Google Scholar] [CrossRef] [PubMed]
- Semyachkina-Glushkovskaya, O.; Chehonin, V.; Borisova, E.; Fedosov, I.; Namykin, A.; Abdurashitov, A.; Shirokov, A.; Khlebtsov, B.; Lyubun, Y.; Navolokin, N.; et al. Photodynamic opening of the blood-brain barrier and pathways of brain clearing pathways. J. Biophotonics 2018, 11, e201700287. [Google Scholar] [CrossRef] [PubMed]
- Feng, W.; Zhang, C.; Yu, T.; Semyachkina-Glushkovskaya, O.; Zhu, D. In vivo monitoring blood-brain barrier permeability using spectral imaging through optical clearing skull window. J. Biophotonics 2019, 12, e201800330. [Google Scholar] [CrossRef] [PubMed]
- Abbott, N.J.; Patabendige, A.A.K.; Dolman, D.E.M.; Yusof, S.R.; Begley, D.J. Structure and function of the blood–brain barrier. Neurobiol. Dis. 2010, 37, 13–25. [Google Scholar] [CrossRef] [PubMed]
- Sarkaria, J.N.; Hu, L.S.; Parney, I.F.; Pafundi, D.H.; Brinkmann, D.H.; Laack, N.N.; Giannini, C.; Burns, T.C.; Kizilbash, S.H.; Laramy, J.K.; et al. Is the blood-brain barrier really disrupted in all glioblastomas? A critical assessment of existing clinical data. Neuro. Oncol. 2018, 20, 184–191. [Google Scholar] [CrossRef]
- Arvanitis, C.D.; Ferraro, G.B.; Jain, R.K. The blood-brain barrier and blood-tumour barrier in brain tumours and metastases. Nat. Rev. Cancer 2020, 20, 26–41. [Google Scholar] [CrossRef]
- Dubois, L.G.; Campanati, L.; Righy, C.; D’Andrea-Meira, I.; Leite de Sampaio e Spohr, T.C.; Porto-Carreiro, I.; Pereira, C.M.; Balça-Silva, J.; Assad Kahn, S.; DosSantos, M.F.; et al. Gliomas and the vascular fragility of the blood brain barrier. Front. Cell. Neurosci. 2014, 8, 418. [Google Scholar] [CrossRef] [Green Version]
- Noell, S.; Ritz, R.; Wolburg-Buchholz, K.; Wolburg, H.; Fallier-Becker, P. An allograft glioma model reveals the dependence of aquaporin-4 expression on the brain microenvironment. PLoS ONE 2012, 7, e36555. [Google Scholar] [CrossRef] [Green Version]
- Wang, D.; Wang, C.; Wang, L.; Chen, Y. Comprehensive review in improving delivery of small-molecule chemotherapeutic agents overcoming the blood–brain/brain tumor barriers for glioblastoma treatment. Drug Deliv. 2019, 26, 551–565. [Google Scholar] [CrossRef]
- Agarwal, S.; Sane, R.; Oberoi, R.; Ohlfest, J.R.; Elmquist, W.F. 2011 Delivery of molecularly targeted therapy to malignant glioma, a disease of the whole brain. Expert Rev. Mol. Med. 2011, 13, 17. [Google Scholar] [CrossRef] [Green Version]
- Zhang, C.; Feng, W.; Zhao, Y.; Yu, T.; Li, P.; Xu, T.; Luo, Q.; Zhu, D. A large, switchable optical clearing skull window for cerebrovascular imaging. Theranostics 2018, 8, 2696–2708. [Google Scholar] [CrossRef] [PubMed]
- Trinidad, J.; Hong, S.J.; Peng, Q.; Madsen, S.J.; Hirschberg, H. Combined concurrent photodynamic and gold nanoshell loaded macrophagemediated photothermal therapies: An in vitro study on squamous cell head and neck carcinoma. Lasers Surg. Med. 2014, 4, 310–318. [Google Scholar] [CrossRef] [PubMed]
- Hara, M.R.; Kovacs, J.J.; Whalen, E.J.; Rajagopal, S.; Strachan, R.T.; Grant, W.; Towers, A.J.; Williams, B.; Lam, C.M.; Xiao, K.; et al. A stress response pathway regulates DNA damage through β2-adrenoreceptors and β-arrestin-1. Nature 2011, 477, 349–353. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hebda, J.K.; Leclair, H.M.; Azzi, S.; Roussel, C.; Scott, M.G.; Bidère, N.; Gavard, J. The C-terminus region of β-arrestin1 modulates VE-cadherin expression and endothelial cell permeability. Cell Commun. Signal. 2013, 11, 37. [Google Scholar] [CrossRef] [Green Version]
- Hu, S.S.; Cheng, H.B.; Zheng, Y.R.; Zhang, R.Y.; Yue, W.; Zhang, H. Effects of photodynamic therapy on the ultrastructure of glioma cells. Biomed. Environ. Sci. 2007, 20, 269–273. [Google Scholar]
- Buzza, H.; de Fraitas, L.C.F.; Moriayama, L.T.; Rosa, R.; Bagnato, F.; Kurachi, C. Vascular effects of photodynamic therapy with circumin in a chlorioallantoic membrane model. Int. J. Mol. Sci. 2019, 20, 1084. [Google Scholar] [CrossRef] [Green Version]
- Filippidis, S.; Carozza, R.B.; Rekate, H.L. Aquaporins in brain edema and neuropathological conditions. Int. J. Mol. Sci. 2017, 18, 55. [Google Scholar] [CrossRef] [Green Version]
- Clément, T.; Rodriguez-Grandel, B.; Badaut, J. Aquaporins in brain edema. J. Neurosci. Res. 2020, 98, 9–18. [Google Scholar] [CrossRef] [Green Version]
- Ito, S.; Rachinger, W.; Stepp, H.; Reulen, H.J.; Stummer, W. Oedema formation in experimental photoirradiation therapy of brain tumours using 5-ALA. Acta Neurochir. 2005, 147, 57–65. [Google Scholar] [CrossRef]
- Mathews, M.S.; Chighvinadze, D.; Gach, H.M.; Uzal, F.A.; Madsen, S.J.; Hirschberg, H. Cerebral edema following photodynamic therapy using endogenous and exogenous photosensitizers in normal brain. Lasers Surg. Med. 2011, 43, 892–900. [Google Scholar] [CrossRef] [Green Version]
- Dharmajaya, R.; Sari, D.K. Malondialdehyde value as radical oxidative marker and endogenous antioxidant value analysis in brain tumor. Ann. Med. Surg. 2022, 77, 103231. [Google Scholar] [CrossRef] [PubMed]
- Kanamori, M.; Kipnis, J. Meningeal lymphatics “drain” brain tumors. Cell Res. 2020, 30, 191–192. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hu, X.; Deng, Q.; Ma, L.; Li, Q.; Chen, Y.; Liao, Y.; Zhou, F.; Zhang, C.; Shao, L.; Feng, J.; et al. Meningeal lymphatic vessels regulate brain tumor drainage and immunity. Cell Res. 2020, 30, 229–243. [Google Scholar] [CrossRef] [PubMed]
- Ma, Q.; Schlegel, F.; Bachmann, S.B.; Hannah Schneider, H.; Decker, Y.; Rudin, M.; Weller, M.; Proulx, S.T.; Detmar, M. Lymphatic outflow of cerebrospinal fluid is reduced in glioma. Sci. Rep. 2019, 9, 14815. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Norton, E.S.; Whaley, L.A.; Ulloa-Navas, M.J.; Patricia García-Tárraga, P.; Meneses, K.M.; Lara-Velazquez, M.; Zarco, N.; Carrano, A.; Quiñones-Hinojosa, A.; García-Verdugo, J.M.; et al. Glioblastoma disrupts the ependymal wall and extracellular matrix structures of the subventricular zone. Fluids Barriers CNS 2022, 19, 58. [Google Scholar] [CrossRef]
- Xu, D.; Zhou, J.; Mei, H.; Li, H.; Sun, W.; Xu, H. Impediment of cerebrospinal fluid drainage through glymphatic system in glioma. Front. Oncol. 2022, 11, 790821. [Google Scholar] [CrossRef]
- Lan, Y.L.; Wang, H.; Chen, A.; Zhang, J. Update on the current knowledge of lymphatic drainage system and its emerging roles in glioma management. Immunology 2022, 1–15. [Google Scholar] [CrossRef]
- Song, E.; Mao, T.; Dong, H.; Boisserand, L.S.B.; Antila, S.; Bosenberg, M.; Alitalo, K.; Thomas, J.L.; Iwasaki, A. VEGF-C-driven lymphatic drainage enables immunosurveillance of brain tumours. Nature 2020, 577, 689–694. [Google Scholar] [CrossRef]
- Graham, M.S.; Mellinghoff, I.K. Meningeal lymphatics prime tumor immunity in glioblastoma. Cancer Cell 2021, 39, 304–306. [Google Scholar] [CrossRef]
- Bordon, Y. VEGF-C shines a light on brain tumours. Nat. Rev. Immunol. 2020, 20, 140–141. [Google Scholar] [CrossRef]
- Cloughesy, T.F.; Mochizuki, A.Y.; Orpilla, J.R.; Hugo, W.; Lee, A.H.; Davidson, T.B.; Wang, A.C.; Ellingson, B.M.; Rytlewski, J.A.; Sanders, C.M. Neoadjuvant anti-PD-1 immunotherapy promotes a survival benefit with intratumoral and systemic immune responses in recurrent glioblastoma. Nat. Med. 2019, 25, 477–486. [Google Scholar] [CrossRef] [PubMed]
- Semyachkina-Glushkovskaya, O.; Bragin, D.; Bragina, O.; Yang, Y.; Abdurashitov, A.; Esmat, A.; Khorovodov, A.; Terskov, A.; Klimova, M.; Agranovich, I.; et al. Mechanisms of sound-induced opening of the blood-brain barrier. Adv. Exp. Med. Biol. 2021, 1269, 197–202. [Google Scholar] [PubMed]
- Semyachkina-Glushkovskaya, O.; Esmat, A.; Bragin, D.; Bragina, O.; Shirokov, A.A.; Navolokin, N.; Yang, Y.; Abdurashitov, A.; Khorovodov, A.; Terskov, A.; et al. Phenomenon of music-induced opening of the blood-brain barrier in healthy mice. Proc. R. Soc. B 2020, 287, 20202337. [Google Scholar] [CrossRef] [PubMed]
- Semyachkina-Glushkovskaya, O.; Abdurashitov, A.; Klimova, M.; Dubrovsky, A.; Shirokov, A.; Fomin, A.; Terskov, A.; Agranovich, I.; Mamedova, M.; Khorovodov, A.; et al. Photostimulation of cerebral and peripheral lymphatic functions. Translat. Biophot. 2020, 2, e201900036. [Google Scholar] [CrossRef]
- Semyachkina-Glushkovskaya, O.; Khorovodov, A.; Fedosov, I.; Pavlov, A.; Shirokov, A.; Sharif, A.E.; Dubrovsky, A.; Blokhina, I.; Terskov, A.; Navolokin, N.; et al. A novel method to stimulate lymphatic clearance of beta-amyloid from mouse brain using noninvasive music-induced opening of the blood–brain barrier with EEG markers. Appl. Sci. 2021, 11, 10287. [Google Scholar] [CrossRef]
- Mokri, B. The Monro-Kellie hypothesis: Applications in CSF volume depletion. Neurology 2001, 56, 1746–1748. [Google Scholar] [CrossRef] [PubMed]
- Batuk, P.; Fuxe, J.; Hashizume, H.; Romano, T.; Lashnits, E.; Butz, S.; Vestweber, D.; Corada, M.; Molendinin, C.; Dejana, E. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 2004, 204, 2349–2362. [Google Scholar]
- Kesler, C.; Kiao, S.; Munn, L.; Padera, T. Lymphatic vessels in health and diseases. Wiley Interdiscip. Rev. Syst. Biol. Med. 2013, 5, 111–124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Semyachkina-Glushkovskaya, O.; Borisova, E.; Mantareva, V.; Angelov, I.; Eneva, I.; Terskov, A.; Mamedova, A.; Shirokov, A.; Khorovodov, A.; Klimova, M.; et al. Photodynamic opening of the blood–brain barrier using different photosensitizers in mice. Appl. Sci. 2020, 10, 33. [Google Scholar] [CrossRef] [Green Version]
- Karu, T.I.; Pyatibrat, L.V.; Afanasyeva, N.I. Cellular effects of low power laser therapy can be mediated by nitric oxide. Lasers Surg. Med. 2005, 36, 307–314. [Google Scholar] [CrossRef] [PubMed]
- Murad, F. Discovery of some of the biological effects of nitric oxide and its role in cell signaling. Biosci. Rep. 2004, 24, 452–474. [Google Scholar] [CrossRef] [PubMed]
- Li, G.Y.; Liu, S.J.; Yu, T.T.; Liu, Z.; Sun, S.L.; Bragin, D.; Navolokin, N.; Kurths, J.; Glushkovskaya-Semyachkina, O.; Zhu, D. Photostimulation of lymphatic clearance of red blood cells from the mouse brain after intraventricular hemorrhage. bioRxiv 2020. [Google Scholar] [CrossRef]
- Stanley, C.P.; Maghzal, G.J.; Ayer, A.; Talib, J.; Giltrap, A.M.; Shengule, S.; Wolhuter, K.; Wang, Y.; Chadha, P.; Suarna, C.; et al. Singlet molecular oxygen regulates vascular tone and blood pressure in inflammation. Nature 2019, 566, 548–552. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ronsein, G.E.; Oliveira, M.C.; Miyamoto, S.; Medeiros, M.H.G.; Di Mascio, P. Tryptophan oxidation by singlet molecular oxygen [O2(1∆g)]: Mechanistic studies using 18O-labeled hydroperoxides, mass spectrometry, and light emission measurements. Chem. Res. Toxicol. 2008, 21, 1271–1283. [Google Scholar] [CrossRef] [PubMed]
- Nakagawa, M.; Kato, S.; Nakano, K.; Hino, T. Dye-sensitized photooxygenation of tryptophan: 3a-hydroperoxypyrroloindole as a labile precursor of formylkynurenine. Chem. Pharm. Bull. 1981, 29, 1013–1026. [Google Scholar] [CrossRef] [Green Version]
- Hirschberg, H.; Berg, K.; Peng, Q. Photodynamic therapy mediated immune therapy of brain tumors. Neuroimmunol. Neuroinflamm. 2018, 5, 27. [Google Scholar] [CrossRef] [PubMed]
- Alzeibak, R.; Mishchenko, T.A.; Shilyagina, N.Y. Targeting immunogenic cancer cell death by photodynamic therapy: Past, present and future. J. Immun. Ther. Cancer 2021, 9, e001926. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, M.C.; de Sousa Júnior, W.T.; Mundim, T.; Vale, C.L.C.; de Oliveira, J.V.; Ganassin, R.; Pacheco, T.J.A.; Vasconcelos Morais, J.A.; Longo, J.P.F.; Azevedo, R.B. Induction of Immunogenic Cell Death by Photodynamic Therapy Mediated by Aluminum-Phthalocyanine in Nanoemulsion. Pharmaceutics 2022, 14, 196. [Google Scholar] [CrossRef]
- Turubanova, V.D.; Mishchenko, T.A.; Balalaeva, I.V.; Efimova, I.; Peskova, N.N.; Klapshina, L.G.; Lermontova, S.A.; Bachert, C.; Krysko, O.; Vedunova, M.V.; et al. Novel porphyrazine-based photodynamic anti-cancer therapy induces immunogenic cell death. Sci. Rep. 2021, 11, 7205. [Google Scholar] [CrossRef] [PubMed]
- Morais, J.A.V.; Almeida, L.R.; Rodrigues, M.C.; Azevedo, R.B.; Muehlmann, L.A. The induction of immunogenic cell death by photodynamic therapy in B16F10 cells in vitro is effected by the concentration of the photosensitizer. Photodiagnosis Photodyn Ther. 2021, 35, 102392. [Google Scholar] [CrossRef] [PubMed]
- Mishchenko, T.; Balalaeva, I.; Gorokhova, A.; Vedunova, M.; Krysko, D.V. Which cell death modality wins the contest for photodynamic therapy of cancer? Cell Death Dis. 2022, 13, 455. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Wang, J.; Kong, Z.; Sun, X.; He, Z.; Sun, B.; Luo, C.; Sun, J. Emerging photodynamic nanotherapeutics for inducing immunogenic cell death and potentiating cancer immunotherapy. Biomaterials 2022, 282, 121433. [Google Scholar] [CrossRef] [PubMed]
- Wei, X.; Song, M.; Jiang, G.; Liang, M.; Chen, C.; Yang, Z.; Zou, L. Progress in advanced nanotherapeutics for enhanced photodynamic immunotherapy of tumor. Theranostics 2022, 12, 5272–5298. [Google Scholar] [CrossRef] [PubMed]
- Jin, F.; Liu, D.; Xu, X.; Ji, J.; Du, Y. Nanomaterials-Based Photodynamic Therapy with Combined Treatment Improves Antitumor Efficacy Through Boosting Immunogenic Cell Death. Int. J. Nanomed. 2021, 16, 4693–4712. [Google Scholar] [CrossRef] [PubMed]
- Song, H.; Cai, Z.; Li, J.; Xiao, H.; Qi, R.; Zheng, M. Light triggered release of a triple action porphyrin-cisplatin conjugate evokes stronger immunogenic cell death for chemotherapy, photodynamic therapy and cancer immunotherapy. J. Nanobiotech. 2022, 20, 329. [Google Scholar] [CrossRef] [PubMed]
- Zhang, G.; Wang, N.; Sun, H.; Fu, X.; Zhai, S.; Cui, J. Self-adjuvanting photosensitizer nanoparticles for combination photodynamic immunotherapy. Biomater. Sci. 2021, 9, 6940–6949. [Google Scholar] [CrossRef] [PubMed]
- Krysko, D.V.; Garg, A.D.; Kaczmarek, A.; Krysko, O.; Agostinis, P.; Vandenabeele, P. Immunogenic cell death and DAMPs in cancer therapy. Nat. Rev. Cancer 2012, 12, 860–875. [Google Scholar] [CrossRef]
- Kroemer, G.; Galluzzi, L.; Kepp, O.; Zitvogel, L. Immunogenic cell death in cancer therapy. Annu. Rev. Immunol. 2013, 31, 51–72. [Google Scholar] [CrossRef] [PubMed]
- Castano, A.P.; Mroz, P.; Hamblin, M.R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer 2006, 6, 535–545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, X.; Kwon, N.; Gu, T.; Liu, Z.; Yoon, J. Innovative strategies for hypoxic-tumor photodynamic therapy. Angew. Chem. Int. Ed. 2018, 57, 11522–11531. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Ren, J.; Chen, Q.; Liu, W.; Xu, Z.; Cao, Y. A HMCuS@MnO2 nanocomplex responsive to multiple tumor environmental clues for photoacoustic/fluorescence/magnetic resonance trimodal imaging-guided and enhanced photothermal/photodynamic therapy. Nanoscale 2020, 12, 12508–12521. [Google Scholar] [CrossRef] [PubMed]
- Cheng, H.; Zhu, J.-Y.; Li, S.-Y.; Zeng, J.-Y.; Lei, Q.; Chen, K.-W. An O2 self-sufficient biomimetic nanoplatform for highly specific and efficient photodynamic therapy. Adv. Funct. Mater. 2016, 26, 7847–7860. [Google Scholar] [CrossRef]
- Waldman, A.D.; Fritz, J.M.; Lenardo, M.J. A guide to cancer immunotherapy: From T cell basic science to clinical practice. Nat. Rev. Immunol. 2020, 20, 651–668. [Google Scholar] [CrossRef] [PubMed]
- Xia, A.; Zhang, Y.; Xu, J.; Yin, T.; Lu, X.J. T cell dysfunction in cancer immunity and immunotherapy. Front. Immunol. 2019, 10, 1719. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Yu, S.; Wang, X.; Qian, Y.; Wu, W.; Zhang, S.; Zheng, B.; Wei, G.; Gao, S.; Cao, Z.; et al. High affinity of chlorin e6 to immunoglobulin G for intraoperative fluorescence image-guided cancer photodynamic and checkpoint blockade therapy. ACS Nano 2019, 13, 10242–10260. [Google Scholar] [CrossRef]
- Guo, Y.; Liu, Y.; Wu, W.; Ling, D.; Zhang, Q.; Zhao, P.; Hu, X. Indoleamine 2,3-dioxygenase (IDO) inhibitors and their nanomedicines for cancer immunotherapy. Biomaterials 2021, 276, 121018. [Google Scholar] [CrossRef] [PubMed]
- Wu, M.; Huang, Q.; Xie, Y.; Wu, X.; Ma, H.; Zhang, Y.; Xia, Y. Improvement of the anticancer efficacy of PD-1/PD-L1 blockade via combination therapy and PD-L1 regulation. J. Hematol. Oncol. 2022, 15, 24. [Google Scholar] [CrossRef]
- Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12, 252–264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eggermont, A.M.M.; Blank, C.U.; Mandala, M.; Long, G.V.; Atkinson, V.; Dalle, S.; Haydon, A.; Lichinitser, M.; Khattak, A.; Carlino, M.S.; et al. Adjuvant pembrolizumab versus placebo in resected stage III melanoma. N. Engl. J. Med. 2018, 378, 1789–1801. [Google Scholar] [CrossRef] [PubMed]
- Wang, D.; Lin, J.; Yang, X.; Long, J.; Bai, Y.; Yang, X.; Mao, Y.; Sang, X.; Seery, S.; Zhao, H. Combination regimens with PD-1/PD-L1 immune checkpoint inhibitors for gastrointestinal malignancies. J. Hematol. Oncol. 2019, 12, 42. [Google Scholar] [CrossRef]
- Lommatzsch, M.; Bratke, K.; Stoll, P. Neoadjuvant PD-1 blockade in resectable lung cancer. N. Engl. J. Med. 2018, 379, e14. [Google Scholar] [PubMed]
- Madsen, S.J.; Christie, C.; Huynh, K.; Peng, Q.; Uzal, F.A.; Krasieva, T.B.; Hirschberg, H. Limiting glioma development by photodynamic therapy-generated macrophage vaccine and allo-stimulation: An in vivo histological study in rats. J. Biomed. Opt. 2018, 2, 028001. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Etminan, N.; Peters, C.; Lakbir, D.; Bünemann, E.; Börger, V.; Sabel, M.C.; Hänggi, D.; Steiger, H.J.; Stummer, W.; Sorg, R.V. Heat-shock protein 70-dependent dendritic cell activation by 5-aminolevulinic acid-mediated photodynamic treatment of human glioblastoma spheroids in vitro. Br. J. Cancer 2011, 105, 961–969. [Google Scholar] [CrossRef] [PubMed]
- Shixiang, Y.; Xi, S.; Junliang, L.; Shanyi, Z.; Xingke, X.; Meiguang, Z.; Kai, W.; Fangcheng, L. Antitumor efficacy of a photodynamic therapy-generated dendritic cell glioma vaccine. Med. Oncol. 2011, 28, S453–S461. [Google Scholar] [CrossRef] [PubMed]
- Garg, A.D.; Vandenberk, L.; Koks, C.; Verschuere, T.; Boon, L.; Van Gool, S.W.; Agostinis, P. Dendritic cell vaccines based on immunogenic cell death elicit danger signals and T cell-driven rejection of high-grade glioma. Sci. Transl. Med. 2016, 8, 328ra27. [Google Scholar] [CrossRef] [PubMed]
- Bartusik-Aebisher, D.; Żołyniak, A.; Barnaś, E.; Machorowska-Pieniążek, A.; Oleś, P.; Kawczyk-Krupka, A.; Aebisher, D. The use of photodynamic therapy in the treatment of brain tumors—A review of the literature. Molecules 2022, 27, 6847. [Google Scholar] [CrossRef] [PubMed]
- Gunaydin, G.; Gedik, M.; Ayan, S. Photodynamic Therapy—Current Limitations and Novel Approaches. Front. Chem. 2021, 9, 691697. [Google Scholar] [CrossRef]
- Chen, R.; Aghi, M.K. Atypical meningiomas. Handb. Clin. Neurol. 2020, 170, 233–244. [Google Scholar] [PubMed]
- Kiesel, B.; Freund, J.; Reichert, D.; Wadiura, L.; Erkkilae, M.T.; Woehrer, A.; Hervey-Jumper, S.; Berger, M.S.; Widhalm, G. 5-ALA in suspected low-grade gliomas: Current Role, limitations, and new approaches. Front. Oncol. 2021, 11, 699301. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.M.; Darafsheh, A. Light Sources and Dosimetry Techniques for Photodynamic Therapy. Photochem. Photobiol. 2020, 96, 280–294. [Google Scholar] [CrossRef] [Green Version]
- Salehpour, F.; Cassano, P.; Rouhi, N.; Hamblin, M.R.; De Taboada, L.; Farajdokht, F.; Mahmoudi, J. Penetration profiles of visible and near-infrared lasers and light-emitting diode light through the head tissues in animal and human species: A review of literature. Photobiomodul. Photomed. Laser Surg. 2019, 37, 581–595. [Google Scholar] [CrossRef] [PubMed]
- Genina, E.A.; Bashkatov, A.N.; Tuchina, D.K.; Dyachenko-Timoshina, P.A.; Navolokin, N.; Shirokov, A.; Khorovodov, A.; Terskov, A.; Klimova, M.; Mamedova, A.; et al. Optical properties of brain tissues at the different stages of glioma development in rats: Pilot study. Biomed. Opt. Express 2019, 10, 5182–5197. [Google Scholar] [CrossRef] [PubMed]
- Semyachkina-Glushkovskaya, O.; Abdurashitov, A.; Dubrovsky, A.; Klimova, M.; Agranovich, I.; Terskov, A.; Shirokov, A.; Vinnik, V.; Kuzmina, A.; Lezhnev, N.; et al. Photobiomodulation of lymphatic drainage and clearance: Perspective strategy for augmentation of meningeal lymphatic functions. Biomed. Opt. Express 2020, 11, 725–734. [Google Scholar] [CrossRef]
- Semyachkina-Glushkovskaya, O.; Fedosov, I.; Shirokov, A.; Vodovozova, E.; Alekseeva, A.; Khorovodov, A.; Blokhina, I.; Terskov, A.; Mamedova, A.; Klimova, M.; et al. Photomodulation of lymphatic delivery of liposomes to the brain bypassing the blood-brain barrier: New perspectives for glioma therapy. Nanophotonics 2021, 10, 3215–3227. [Google Scholar] [CrossRef]
- Semyachkina-Glushkovskaya, O.; Penzel, T.; Blokhina, I.; Khorovodov, A.; Fedosov, I.; Yu, T.; Karandin, G.; Evsukova, A.; Elovenko, D.; Adushkina, V.; et al. Night photostimulation of clearance of beta-amyloid from mouse brain: New strategies in preventing Alzheimer’s disease. Cells 2021, 10, 3289. [Google Scholar] [CrossRef] [PubMed]
- Zakharov, S.D.; Ivanov, A.V. Light-oxygen effect in cells and its potential applications in tumour therapy (review). Quantum Electron. 1999, 29, 1031–1053. [Google Scholar] [CrossRef]
- Park, J.H.; Lee, H.K. Current understanding of hypoxia in glioblastoma multiforme and its response to immunotherapy. Cancers 2022, 14, 1176. [Google Scholar] [CrossRef] [PubMed]
- Xiao, Z.; Halls, S.; Dickey, D.; Tulip, J.; Moore, R.B. Fractionated versus Standard Continuous Light Delivery in Interstitial Photodynamic Therapy of dunning Prostate Carcinomas. Clin. Cancer Res. 2007, 13, 7496–7505. [Google Scholar] [CrossRef] [Green Version]
- Maragkos, G.A.; Schüpper, A.J.; Lakomkin, N.; Sideras, P.; Price, G.; Baron, R.; Hamilton, T.; Haider, S.; Lee, I.Y.; Hadjipanayis, C.G.; et al. Fluorescence-guided high-grade glioma surgery more than four hours after 5-aminolevulinic acid administration. Front. Neurol. 2021, 12, 644804. [Google Scholar] [CrossRef]
- Stummer, W.; Pichlmeier, U.; Meinel, T.; Wiestler, O.D.; Zanella, F.; Reulen, H.J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: A randomised controlled multicentre phase III trial. Lancet Oncol. 2006, 7, 392–401. [Google Scholar] [CrossRef]
- Senders, J.T.; Muskens, I.S.; Schnoor, R.; Karhade, A.V.; Cote, D.J.; Smith, T.R. Agents for fluorescence-guided glioma surgery: A systematic review of preclinical and clinical results. Acta Neurochir. 2017, 159, 151–167. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wan, S.; Parrish, J.A.; Anderson, R.R.; Madden, M. Transmittance of nonionizing radiation in human tissues. Photochem. Photobiol. 1981, 34, 679–681. [Google Scholar] [CrossRef] [PubMed]
- Lychagov, V.V.; Tuchin, V.V.; Vilensky, M.A.; Reznik, B.N.; Ichim, T.; De Taboada, L. Experimental study of NIR transmittance of the human skull. In Complex Dynamics and Fluctuations in Biomedical Photonics, 3rd ed.; International Society for Optics and Photonics: Bellingham, WA, USA, 2006; p. 60850T. [Google Scholar]
- Svaasand, L.O.; Ellingsen, R. Optical properties of human brain. Photochem. Photobiol. 1983, 38, 293–299. [Google Scholar] [CrossRef] [PubMed]
- Stolik, S.; Delgado, J.; Perez, A.; Anasagasti, L. Measurement of the penetration depths of red and near infrared light in human “ex vivo” tissues. J. Photochem. Photobiol. B 2000, 57, 90–93. [Google Scholar] [CrossRef] [PubMed]
- Jagdeo, J.R.; Adams, L.E.; Brody, N.I.; Siegel, D.M. Transcranial red and near infrared light transmission in a cadaveric model. PLoS ONE 2012, 7, e47460. [Google Scholar] [CrossRef]
- Yue, L.; Monge, M.; Ozgur, M.H. Simulation and measurement of transcranial near infrared light penetration. In Optical Interactions with Tissue and Cells, 26th ed.; International Society for Optics and Photonics: Bellingham, WA, USA, 2015; p. 93210S. [Google Scholar]
- Barrett, D.; Gonzalez-Lima, F. Transcranial infrared laser stimulation produces beneficial cognitive and emotional effects in humans. Neuroscience 2013, 230, 13–23. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Semyachkina-Glushkovskaya, O.; Terskov, A.; Khorovodov, A.; Telnova, V.; Blokhina, I.; Saranceva, E.; Kurths, J. Photodynamic Opening of the Blood–Brain Barrier and the Meningeal Lymphatic System: The New Niche in Immunotherapy for Brain Tumors. Pharmaceutics 2022, 14, 2612. https://doi.org/10.3390/pharmaceutics14122612
Semyachkina-Glushkovskaya O, Terskov A, Khorovodov A, Telnova V, Blokhina I, Saranceva E, Kurths J. Photodynamic Opening of the Blood–Brain Barrier and the Meningeal Lymphatic System: The New Niche in Immunotherapy for Brain Tumors. Pharmaceutics. 2022; 14(12):2612. https://doi.org/10.3390/pharmaceutics14122612
Chicago/Turabian StyleSemyachkina-Glushkovskaya, Oxana, Andrey Terskov, Alexander Khorovodov, Valeria Telnova, Inna Blokhina, Elena Saranceva, and Jürgen Kurths. 2022. "Photodynamic Opening of the Blood–Brain Barrier and the Meningeal Lymphatic System: The New Niche in Immunotherapy for Brain Tumors" Pharmaceutics 14, no. 12: 2612. https://doi.org/10.3390/pharmaceutics14122612
APA StyleSemyachkina-Glushkovskaya, O., Terskov, A., Khorovodov, A., Telnova, V., Blokhina, I., Saranceva, E., & Kurths, J. (2022). Photodynamic Opening of the Blood–Brain Barrier and the Meningeal Lymphatic System: The New Niche in Immunotherapy for Brain Tumors. Pharmaceutics, 14(12), 2612. https://doi.org/10.3390/pharmaceutics14122612