Abstract

In this pilot study, we analyzed effects of transcranial photobiomodulation (tPBM, 1267 nm, 32 J/cm2) on clearance of beta-amyloid (Aβ) from the mouse brain. The immunohistochemical and confocal data clearly demonstrate the significant reduction of deposition of Aβ plaques in mice after tPBM vs. untreated animals. The behavior tests showed that tPBM improved the cognitive, memory and neurological status of mice with Alzheimer’s disease (AD). Using of our original method based on optical coherence tomography (OCT) analysis of clearance of gold nanorods (GNRs) from the brain, we proposed possible mechanism underlying tPBM-stimulating effects on clearance of Aβ via the lymphatic system of the brain and the neck. These results open breakthrough strategies for a non-pharmacological therapy of Alzheimer’s disease and clearly demonstrate that tPBM might be a promising therapeutic target for preventing or delaying Alzheimer’s disease.

© 2019 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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J. Chang, Y. Ren, R. Wang, C. Li, Y. Wang, and X. Chu, “Transcranial Low-Level Laser Therapy for Depression and Alzheimer’s Disease,” Neuropsychiatry (London) 8(2), 477–483 (2018).
[Crossref]

M. R. Hamblin, “Photobiomodulation for traumatic brain injury and stroke,” J. Neurosci. Res. 96(4), 731–743 (2018).
[Crossref] [PubMed]

F. Salehpour, J. Mahmoudi, F. Kamari, S. Sadigh-Eteghad, S. H. Rasta, and M. R. Hamblin, “Brain Photobiomodulation Therapy: a Narrative Review,” Mol. Neurobiol. 55(8), 6601–6636 (2018), doi:.
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S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref] [PubMed]

R. Facchinetti, M. R. Bronzuoli, and C. Scuderi, “An Animal Model of Alzheimer Disease Based on the Intrahippocampal Injection of Amyloid β-Peptide,” Methods Mol. Biol. 1727, 343–352 (2018).
[Crossref] [PubMed]

S. Golovynskyi, I. Golovynska, L. I. Stepanova, O. I. Datsenko, L. Liu, J. Qu, and T. Y. Ohulchanskyy, “Optical windows for head tissues in near-infrared and short-wave infrared regions: Approaching transcranial light applications,” J. Biophotonics 11(12), e201800141 (2018).
[Crossref] [PubMed]

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref] [PubMed]

O. Semyachkina-Glushkovskaya, D. Postnov, and J. Kurths, “Blood−Brain Barrier, Lymphatic Clearance, and Recovery: Ariadne’s Thread in Labyrinths of Hypotheses,” Int. J. Mol. Sci. 19(12), 3818 (2018).
[Crossref] [PubMed]

2017 (8)

O. V. Semyachkina-Glushkovskaya, S. G. Sokolovski, A. Goltsov, A. S. Gekaluyk, O. A. Bragina, E. I. Saranceva, V. V. Tuchin, and E. U. Rafailov, “Laser-induced generation of singlet oxygen and its role in the cerebrovascular physiology,” Prog. Quantum Electron. 55, 112–128 (2017).
[Crossref]

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref] [PubMed]

Z. Xu, X. Guo, Y. Yang, D. Tucker, Y. Lu, N. Xin, G. Zhang, L. Yang, J. Li, X. Du, Q. Zhang, and X. Xu, “Low-level laser irradiation improves depression-like behaviors in mice,” Mol. Neurobiol. 54(6), 4551–4559 (2017).
[Crossref] [PubMed]

S. Kocahan and Z. Doğan, “Mechanisms of Alzheimer’s Disease Pathogenesis and Prevention: The Brain, Neural Pathology, N-methyl-D-aspartate Receptors, Tau Protein and Other Risk Factors,” Clin. Psychopharmacol. Neurosci. 15(1), 1–8 (2017).
[Crossref] [PubMed]

C. da Luz Eltchechem, A. S. I. Salgado, R. A. Zângaro, M. C. da Silva Pereira, I. I. Kerppers, L. A. da Silva, and R. B. Parreira, “Transcranial LED therapy on amyloid-β toxin 25-35 in the hippocampal region of rats,” Lasers Med. Sci. 32(4), 749–756 (2017).
[Crossref] [PubMed]

L. M. Lueptow, “Novel Object Recognition Test for the Investigation of Learning and Memory in Mice,” J. Vis. Exp. 126(126), 55718 (2017).
[Crossref] [PubMed]

J. C. de la Torre, “Treating cognitive impairment with transcranial low level laser therapy,” J. Photochem. Photobiol. B 168(1), 149–155 (2017).
[Crossref] [PubMed]

Y. Lu, R. Wang, Y. Dong, D. Tucker, N. Zhao, M. E. Ahmed, L. Zhu, T. C. Liu, R. M. Cohen, Q. Zhang, and Q. Zhang, “Low-level laser therapy for beta amyloid toxicity in rat hippocampus,” Neurobiol. Aging 49(1), 165–182 (2017).
[Crossref] [PubMed]

2016 (7)

P. Cassano, S. R. Petrie, M. R. Hamblin, T. A. Henderson, and D. V. Iosifescu, “Review of transcranial photobiomodulation for major depressive disorder: targeting brain metabolism, inflammation, oxidative stress, and neurogenesis,” Neurophotonics 3(3), 031404 (2016).
[Crossref] [PubMed]

A. V. Stavrovskaya, N. G. Yamshchikoval, A. S. Ol’shanskiyl, G. A. Babkinl, and S. N. Illarioshkinl, “Evaluation of the effects of new peptide compounds in experimental animals with a toxic model of Alzheimer’s disease,” Ann. Clin. Exp. Neurol. 10, 33–42 (2016).

A. Oron and U. Oron, “Low-level laser therapy to the bone marrow ameliorates neurodegenerative disease progression in a mouse model of Alzheimer’s disease: a minireview,” Photomed. Laser Surg. 34(12), 627–630 (2016).
[Crossref] [PubMed]

H. S. Mohammed, “Transcranial low-level infrared laser irradiation ameliorates depression induced by reserpine in rats,” Lasers Med. Sci. 31(8), 1651–1656 (2016).
[Crossref] [PubMed]

N. Patel, P. Pera, P. Joshi, M. Dukh, W. A. Tabaczynski, K. E. Siters, M. Kryman, R. R. Cheruku, F. Durrani, J. R. Missert, R. Watson, T. Y. Ohulchanskyy, E. C. Tracy, H. Baumann, and R. K. Pandey, “Highly effective dual-function near-infrared (NIR) photosensitizer for fluorescence imaging and photodynamic therapy (PDT) of cancer,” J. Med. Chem. 59(21), 9774–9787 (2016), doi:.
[Crossref] [PubMed]

P. A. Lapchak and P. D. Boitano, “Transcranialnearinfrared laser therapy for stroke: how to recover from futility in the NEST-3 Clinical Trial,” Acta Neurochir. Suppl. (Wien) 121(1), 7–12 (2016).
[Crossref] [PubMed]

W. Xuan, L. Huang, and M. R. Hamblin, “Repeated transcranial low-level laser therapy for traumatic brain injury in mice: biphasic dose response and long-term treatment outcome,” J. Biophotonics 9(11-12), 1263–1272 (2016).
[Crossref] [PubMed]

2015 (9)

L. D. Morries, P. Cassano, and T. A. Henderson, “Treatments for traumatic brain injury with emphasis on transcranial near-infrared laser phototherapy,” Neuropsychiatr. Dis. Treat. 11(1), 2159–2175 (2015).
[PubMed]

B. Smoot, L. Chiavola-Larson, J. Lee, H. Manibusan, and D. D. Allen, “Effect of low-level laser therapy on pain and swelling in women with breast cancer-related lymphedema: a systematic review and meta-analysis,” J. Cancer Surviv. 9(2), 287–304 (2015).
[Crossref] [PubMed]

S. Chakraborty, M. J. Davis, and M. Muthuchamy, “Emerging trends in the pathophysiology of lymphatic contractile function,” Semin. Cell Dev. Biol. 38, 55–66 (2015).
[Crossref] [PubMed]

D. Farfara, H. Tuby, D. Trudler, E. Doron-Mandel, L. Maltz, R. J. Vassar, D. Frenkel, and U. Oron, “Low-level laser therapy ameliorates disease progression in a mouse model of Alzheimer’s disease,” J. Mol. Neurosci. 55(2), 430–436 (2015).
[Crossref] [PubMed]

S. Purushothuman, D. M. Johnstone, C. Nandasena, J. Eersel, L. M. Ittner, J. Mitrofanis, and J. Stone, “Near infrared light mitigates cerebellar pathology in transgenic mouse models of dementia,” Neurosci. Lett. 591(1), 155–159 (2015).
[Crossref] [PubMed]

Z. I. Santini, A. Koyanagi, S. Tyrovolas, J. M. Haro, K. L. Fiori, R. Uwakwa, J. A. Thiyagarajan, M. Webber, M. Prince, and A. M. Prina, “Social network typologies and mortality risk among older people in China, India, and Latin America: A 10/66 Dementia Research Group population-based cohort study,” Soc. Sci. Med. 147, 134–143 (2015).
[Crossref] [PubMed]

P. Cassano, C. Cusin, D. Mischoulon, M. R. Hamblin, L. De Taboada, A. Pisoni, T. Chang, A. Yeung, D. F. Ionescu, S. R. Petrie, A. A. Nierenberg, M. Fava, and D. V. Iosifescu, “Near-Infrared Transcranial Radiation for Major Depressive Disorder: Proof of Concept Study,” Psychiatry J. 2015, 352979 (2015).
[Crossref] [PubMed]

L. A. Demetrius, P. J. Magistretti, and L. Pellerin, “Alzheimer’s disease: the amyloid hypothesis and the Inverse Warburg effect,” Front. Physiol. 5, 522 (2015).
[Crossref] [PubMed]

T. A. Henderson and L. D. Morries, “Near-infrared photonic energy penetration: can infrared phototherapy effectively reach the Human brain?” Neuropsychiatr. Dis. Treat. 11(1), 2191–2208 (2015).
[Crossref] [PubMed]

2013 (7)

S. L. Grillo, N. A. Duggett, A. Ennaceur, and P. L. Chazot, “Non-invasive infra-red therapy (1072 nm) reduces β-amyloid protein levels in the brain of an Alzheimer’s disease mouse model, TASTPM,” J. Photochem. Photobiol. B 123(1), 13–22 (2013).
[Crossref] [PubMed]

S. G. Sokolovski, S. A. Zolotovskaya, A. Goltsov, C. Pourreyron, A. P. South, and E. U. Rafailov, “Infrared laser pulse triggers increased singlet oxygen production in tumour cells,” Sci. Rep. 3(1), 3484 (2013), doi:.
[Crossref] [PubMed]

K. Iqbal, S. Bolognin, X. Wang, G. Basurto-Islas, J. Blanchard, and Y. C. Tung, “Animal models of the sporadic form of Alzheimer’s disease: focus on the disease and not just the lesions,” J. Alzheimers Dis. 37(3), 469–474 (2013).
[Crossref] [PubMed]

U. H. Mitchell and G. L. Mack, “Low-level laser treatment with near-infrared light increases venous nitric oxide levels acutely: a single-blind, randomized clinical trial of efficacy,” Am. J. Phys. Med. Rehabil. 92(2), 151–156 (2013).
[Crossref] [PubMed]

S. Purushothuman, C. Nandasena, D. M. Johnstone, J. Stone, and J. Mitrofanis, “The impact of near-infrared light on dopaminergic cell survival in a transgenic mouse model of Parkinsonism,” Brain Res. 1535(1), 61–70 (2013).
[Crossref] [PubMed]

B. N. Huisa, A. B. Stemer, M. G. Walker, K. Rapp, B. C. Meyer, and J. A. Zivin, “Transcranial laser therapy for acute ischemic stroke: a pooled analysis of NEST-1 and NEST-2,” Int. J. Stroke 8(5), 315–320 (2013).
[Crossref] [PubMed]

D. T. Meneguzzo, L. A. Lopes, R. Pallota, L. Soares-Ferreira, R. A. Lopes-Martins, and M. S. Ribeiro, “Prevention and treatment of mice paw edema by near-infrared low-level laser therapy on lymph nodes,” Lasers Med. Sci. 28(3), 973–980 (2013).
[Crossref] [PubMed]

2012 (6)

M. T. Omar, A. A. Shaheen, and H. Zafar, “A systematic review of the effect of low-level laser therapy in the management of breast cancer-related lymphedema,” Support. Care Cancer 20(11), 2977–2984 (2012).
[Crossref] [PubMed]

J. Liang, L. Liu, and D. Xing, “Photobiomodulation by low-power laser irradiation attenuates Aβ-induced cell apoptosis through the Akt/GSK3β/β-catenin pathway,” Free Radic. Biol. Med. 53(7), 1459–1467 (2012).
[Crossref] [PubMed]

A. P. Sommer, J. Bieschke, R. P. Friedrich, D. Zhu, E. E. Wanker, H. J. Fecht, D. Mereles, and W. Hunstein, “670 nm laser light and EGCG complementarily reduce amyloid-β aggregates in human neuroblastoma cells: basis for treatment of Alzheimer’s disease?” Photomed. Laser Surg. 30(1), 54–60 (2012).
[Crossref] [PubMed]

H. Zhang, S. Wu, and D. Xing, “Inhibition of Aβ(25-35)-induced cell apoptosis by low-power-laser-irradiation (LPLI) through promoting Akt-dependent YAP cytoplasmic translocation,” Cell. Signal. 24(1), 224–232 (2012).
[Crossref] [PubMed]

P. Dunkel, C. L. Chai, B. Sperlágh, P. B. Huleatt, and P. Mátyus, “Clinical utility of neuroprotective agents in neurodegenerative diseases: current status of drug development for Alzheimer’s, Parkinson’s and Huntington’s diseases, and amyotrophic lateral sclerosis,” Expert Opin. Investig. Drugs 21(9), 1267–1308 (2012).
[Crossref] [PubMed]

K. Ubhi and E. Masliah, “Alzheimer’s disease: recent advances and future perspectives,” J. Alzheimers Dis. 33(Suppl 1), S185–S194 (2012).
[Crossref] [PubMed]

2011 (3)

A. Serrano-Pozo, M. P. Frosch, E. Masliah, and B. T. Hyman, “Neuropathological alterations in Alzheimer disease,” Cold Spring Harb. Perspect. Med. 1(1), a006189 (2011).
[Crossref] [PubMed]

M. A. Naeser and M. R. Hamblin, “Potential for transcranial laser or LED therapy to treat stroke, traumatic brain injury, and neurodegenerative disease,” Photomed. Laser Surg. 29(7), 443–446 (2011).
[Crossref] [PubMed]

L. De Taboada, J. Yu, S. El-Amouri, S. Gattoni-Celli, S. Richieri, T. McCarthy, J. Streeter, and M. S. Kindy, “Transcranial laser therapy attenuates amyloid-β peptide neuropathology in amyloid-β protein precursor transgenic mice,” J. Alzheimers Dis. 23(3), 521–535 (2011).
[Crossref] [PubMed]

2010 (2)

Y. Geng, C. Li, J. Liu, G. Xing, L. Zhou, M. Dong, X. Li, and Y. Niu, “Beta-Asarone Improves Cognitive Function by Suppressing Neuronal Apoptosis in the Beta-Amyloid Hippocampus Injection Rats,” Biol. Pharm. Bull. 33(5), 836–843 (2010).
[Crossref] [PubMed]

M. P. Murphy and H. LeVine, “Alzheimer’s disease and the amyloid-β peptide,” J. Alzheimers Dis. 19(1), 311–323 (2010).
[Crossref] [PubMed]

2009 (3)

J. Hardy, “The amyloid hypothesis for Alzheimer’s disease: a critical reappraisal,” J. Neurochem. 110(4), 1129–1134 (2009).
[Crossref] [PubMed]

M. A. Flierl, P. F. Stahel, K. M. Beauchamp, S. J. Morgan, W. R. Smith, and E. Shohami, “Mouse closed head injury model induced by a weight-drop device,” Nat. Protoc. 4(9), 1328–1337 (2009).
[Crossref] [PubMed]

N. L. Lohr, A. Keszler, P. Pratt, M. Bienengraber, D. C. Warltier, and N. Hogg, “Enhancement of nitric oxide release from nitrosyl hemoglobin and nitrosyl myoglobin by red/near infrared radiation: potential role in cardioprotection,” J. Mol. Cell. Cardiol. 47(2), 256–263 (2009).
[Crossref] [PubMed]

2008 (3)

S. Benedicenti, I. M. Pepe, F. Angiero, and A. Benedicenti, “Intracellular ATP level increases in lymphocytes irradiated with infrared laser light of wavelength 904 nm,” Photomed. Laser Surg. 26(5), 451–453 (2008).
[Crossref] [PubMed]

S. Michalikova, A. Ennaceur, R. van Rensburg, and P. L. Chazot, “Emotional responses and memory performance of middle-aged CD1 mice in a 3D maze: effects of low infrared light,” Neurobiol. Learn. Mem. 89(4), 480–488 (2008).
[Crossref] [PubMed]

L. Zhang, D. Xing, D. Zhu, and Q. Chen, “Low-power laser irradiation inhibiting Abeta25-35-induced PC12 cell apoptosis via PKC activation,” Cell. Physiol. Biochem. 22(1-4), 215–222 (2008).
[Crossref] [PubMed]

2002 (2)

A. Mudher and S. Lovestone, “Alzheimer’s disease-do tauists and baptists finally shake hands?” Trends Neurosci. 25(1), 22–26 (2002).
[Crossref] [PubMed]

J. Hardy and D. J. Selkoe, “The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics,” Science 297(5580), 353–356 (2002).
[Crossref] [PubMed]

2000 (1)

K. Yamada and T. Nabeshima, “Animal models of Alzheimer’s disease and evaluation of anti-dementia drugs,” Pharmacol. Ther. 88(2), 93–113 (2000).
[Crossref] [PubMed]

1999 (1)

R. E. Brown, S. C. Corey, and A. K. Moore, “Differences in measures of exploration and fear in MHC-congenic C57BL/6J and B6-H-2K mice,” Behav. Genet. 26(4), 263–271 (1999).
[Crossref]

1994 (1)

M. P. McDonald, E. E. Dahl, J. B. Overmier, P. Mantyh, and J. Cleary, “Effects of an exogenous β-amyloid peptide on retention for spatial learning,” Behav. Neural Biol. 62(1), 60–67 (1994).
[Crossref] [PubMed]

1991 (2)

J. Hardy and D. Allsop, “Amyloid deposition as the central event in the aetiology of Alzheimer’s disease,” Trends Pharmacol. Sci. 12(10), 383–388 (1991).
[Crossref] [PubMed]

N. W. Kowall, M. F. Beal, J. Busciglio, L. K. Duffy, and B. A. Yankner, “An in vivo model for the neurodegenerative effects of beta amyloid and protection by substance P,” Proc. Natl. Acad. Sci. U.S.A. 88(16), 7247–7251 (1991).
[Crossref] [PubMed]

Abdurashitov, A.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref] [PubMed]

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref] [PubMed]

Acton, S. T.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref] [PubMed]

Agranovich, I.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref] [PubMed]

Ahmed, M. E.

Y. Lu, R. Wang, Y. Dong, D. Tucker, N. Zhao, M. E. Ahmed, L. Zhu, T. C. Liu, R. M. Cohen, Q. Zhang, and Q. Zhang, “Low-level laser therapy for beta amyloid toxicity in rat hippocampus,” Neurobiol. Aging 49(1), 165–182 (2017).
[Crossref] [PubMed]

Allen, D. D.

B. Smoot, L. Chiavola-Larson, J. Lee, H. Manibusan, and D. D. Allen, “Effect of low-level laser therapy on pain and swelling in women with breast cancer-related lymphedema: a systematic review and meta-analysis,” J. Cancer Surviv. 9(2), 287–304 (2015).
[Crossref] [PubMed]

Allsop, D.

J. Hardy and D. Allsop, “Amyloid deposition as the central event in the aetiology of Alzheimer’s disease,” Trends Pharmacol. Sci. 12(10), 383–388 (1991).
[Crossref] [PubMed]

Angiero, F.

S. Benedicenti, I. M. Pepe, F. Angiero, and A. Benedicenti, “Intracellular ATP level increases in lymphocytes irradiated with infrared laser light of wavelength 904 nm,” Photomed. Laser Surg. 26(5), 451–453 (2008).
[Crossref] [PubMed]

Babkinl, G. A.

A. V. Stavrovskaya, N. G. Yamshchikoval, A. S. Ol’shanskiyl, G. A. Babkinl, and S. N. Illarioshkinl, “Evaluation of the effects of new peptide compounds in experimental animals with a toxic model of Alzheimer’s disease,” Ann. Clin. Exp. Neurol. 10, 33–42 (2016).

Bai, R.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref] [PubMed]

Baker, W.

S. Da Mesquita, A. Louveau, A. Vaccari, I. Smirnov, R. C. Cornelison, K. M. Kingsmore, C. Contarino, S. Onengut-Gumuscu, E. Farber, D. Raper, K. E. Viar, R. D. Powell, W. Baker, N. Dabhi, R. Bai, R. Cao, S. Hu, S. S. Rich, J. M. Munson, M. B. Lopes, C. C. Overall, S. T. Acton, and J. Kipnis, “Functional aspects of meningeal lymphatics in ageing and Alzheimer’s disease,” Nature 560(7717), 185–191 (2018).
[Crossref] [PubMed]

Basurto-Islas, G.

K. Iqbal, S. Bolognin, X. Wang, G. Basurto-Islas, J. Blanchard, and Y. C. Tung, “Animal models of the sporadic form of Alzheimer’s disease: focus on the disease and not just the lesions,” J. Alzheimers Dis. 37(3), 469–474 (2013).
[Crossref] [PubMed]

Baumann, H.

N. Patel, P. Pera, P. Joshi, M. Dukh, W. A. Tabaczynski, K. E. Siters, M. Kryman, R. R. Cheruku, F. Durrani, J. R. Missert, R. Watson, T. Y. Ohulchanskyy, E. C. Tracy, H. Baumann, and R. K. Pandey, “Highly effective dual-function near-infrared (NIR) photosensitizer for fluorescence imaging and photodynamic therapy (PDT) of cancer,” J. Med. Chem. 59(21), 9774–9787 (2016), doi:.
[Crossref] [PubMed]

Beal, M. F.

N. W. Kowall, M. F. Beal, J. Busciglio, L. K. Duffy, and B. A. Yankner, “An in vivo model for the neurodegenerative effects of beta amyloid and protection by substance P,” Proc. Natl. Acad. Sci. U.S.A. 88(16), 7247–7251 (1991).
[Crossref] [PubMed]

Beauchamp, K. M.

M. A. Flierl, P. F. Stahel, K. M. Beauchamp, S. J. Morgan, W. R. Smith, and E. Shohami, “Mouse closed head injury model induced by a weight-drop device,” Nat. Protoc. 4(9), 1328–1337 (2009).
[Crossref] [PubMed]

Benedicenti, A.

S. Benedicenti, I. M. Pepe, F. Angiero, and A. Benedicenti, “Intracellular ATP level increases in lymphocytes irradiated with infrared laser light of wavelength 904 nm,” Photomed. Laser Surg. 26(5), 451–453 (2008).
[Crossref] [PubMed]

Benedicenti, S.

S. Benedicenti, I. M. Pepe, F. Angiero, and A. Benedicenti, “Intracellular ATP level increases in lymphocytes irradiated with infrared laser light of wavelength 904 nm,” Photomed. Laser Surg. 26(5), 451–453 (2008).
[Crossref] [PubMed]

Bienengraber, M.

N. L. Lohr, A. Keszler, P. Pratt, M. Bienengraber, D. C. Warltier, and N. Hogg, “Enhancement of nitric oxide release from nitrosyl hemoglobin and nitrosyl myoglobin by red/near infrared radiation: potential role in cardioprotection,” J. Mol. Cell. Cardiol. 47(2), 256–263 (2009).
[Crossref] [PubMed]

Bieschke, J.

A. P. Sommer, J. Bieschke, R. P. Friedrich, D. Zhu, E. E. Wanker, H. J. Fecht, D. Mereles, and W. Hunstein, “670 nm laser light and EGCG complementarily reduce amyloid-β aggregates in human neuroblastoma cells: basis for treatment of Alzheimer’s disease?” Photomed. Laser Surg. 30(1), 54–60 (2012).
[Crossref] [PubMed]

Blanchard, J.

K. Iqbal, S. Bolognin, X. Wang, G. Basurto-Islas, J. Blanchard, and Y. C. Tung, “Animal models of the sporadic form of Alzheimer’s disease: focus on the disease and not just the lesions,” J. Alzheimers Dis. 37(3), 469–474 (2013).
[Crossref] [PubMed]

Bodrova, A.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref] [PubMed]

Boitano, P. D.

P. A. Lapchak and P. D. Boitano, “Transcranialnearinfrared laser therapy for stroke: how to recover from futility in the NEST-3 Clinical Trial,” Acta Neurochir. Suppl. (Wien) 121(1), 7–12 (2016).
[Crossref] [PubMed]

Bolognin, S.

K. Iqbal, S. Bolognin, X. Wang, G. Basurto-Islas, J. Blanchard, and Y. C. Tung, “Animal models of the sporadic form of Alzheimer’s disease: focus on the disease and not just the lesions,” J. Alzheimers Dis. 37(3), 469–474 (2013).
[Crossref] [PubMed]

Borisova, E.

O. Semyachkina-Glushkovskaya, V. Chehonin, E. Borisova, I. Fedosov, A. Namykin, A. Abdurashitov, A. Shirokov, B. Khlebtsov, Y. Lyubun, N. Navolokin, M. Ulanova, N. Shushunova, A. Khorovodov, I. Agranovich, A. Bodrova, M. Sagatova, A. E. Shareef, E. Saranceva, T. Iskra, M. Dvoryatkina, E. Zhinchenko, O. Sindeeva, V. Tuchin, and J. Kurths, “Photodynamic opening of the blood-brain barrier and pathways of brain clearing,” J. Biophotonics 11(8), e201700287 (2018).
[Crossref] [PubMed]

Bragin, D.

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref] [PubMed]

Bragina, O.

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref] [PubMed]

Bragina, O. A.

O. V. Semyachkina-Glushkovskaya, S. G. Sokolovski, A. Goltsov, A. S. Gekaluyk, O. A. Bragina, E. I. Saranceva, V. V. Tuchin, and E. U. Rafailov, “Laser-induced generation of singlet oxygen and its role in the cerebrovascular physiology,” Prog. Quantum Electron. 55, 112–128 (2017).
[Crossref]

Bronzuoli, M. R.

R. Facchinetti, M. R. Bronzuoli, and C. Scuderi, “An Animal Model of Alzheimer Disease Based on the Intrahippocampal Injection of Amyloid β-Peptide,” Methods Mol. Biol. 1727, 343–352 (2018).
[Crossref] [PubMed]

Brown, R. E.

R. E. Brown, S. C. Corey, and A. K. Moore, “Differences in measures of exploration and fear in MHC-congenic C57BL/6J and B6-H-2K mice,” Behav. Genet. 26(4), 263–271 (1999).
[Crossref]

Bucharskaya, A.

O. Semyachkina-Glushkovskaya, A. Abdurashitov, A. Dubrovsky, D. Bragin, O. Bragina, N. Shushunova, G. Maslyakova, N. Navolokin, A. Bucharskaya, V. Tuchin, J. Kurths, and A. Shirokov, “Application of optical coherence tomography for in vivo monitoring of the meningeal lymphatic vessels during opening of blood-brain barrier: mechanisms of brain clearing,” J. Biomed. Opt. 22(12), 1–9 (2017).
[Crossref] [PubMed]

Busciglio, J.

N. W. Kowall, M. F. Beal, J. Busciglio, L. K. Duffy, and B. A. Yankner, “An in vivo model for the neurodegenerative effects of beta amyloid and protection by substance P,” Proc. Natl. Acad. Sci. U.S.A. 88(16), 7247–7251 (1991).
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Cao, R.

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Biogen/Eisai Halt Phase 3 Aducanumab Trials. https://www.alzforum.org/news/research-news/biogeneisai-halt-phase-3-aducanumab-trials

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Figures (4)

Fig. 1
Fig. 1 The scheme of intrahippocampal injection of Aβ(1-42) peptide in mice: a) mice preparation after shaving of head and exposure the skin over the skull; b) stereotaxic coordinates for injection of Aβ into the CA1 subregion of the hippocampus of an adult mouse.
Fig. 2
Fig. 2 PBM effects on distribution of Aβ deposition in the mouse brain: A-D – ICH imaging of Aβ depositions in the brain tissues in untreated mice with AD (A), in mice with AD after PBM (B), in the shem group (C) and in intact mice from the control group (D); E-M – Confocal and quantitative analysis of Aβ distribution in the brain tissues of untreated mice with AD (E-G), in mice with AD after PBM (H-J); K-M – quantitative analysis of presence of Aβ plagues in tested tissues in untreated mice with AD and mice with AD, received PBM: K – in the brain (ICH data); L - in dcLN (ICH data); M – in the brain (small and large Aβ plagues, confocal data); N-Q – ICH data of Aβ depositions in dcLNs in untreated mice with AD (N), in mice with AD, received PBM (O), in the shem group (P) and in intact mice from the control group (Q). n = 7 for each group, at least 10 individual tissue sections taken for each animal. † - p<0.001 between groups.
Fig. 3
Fig. 3 The memory and neurological tests: A - the assessment of the neurobehavioral status of mice on the NSS scale (* - p<0.05 vs. intact mice; Δ - p<0.05 vs. sham mice; #- between untreated AD mice and AD mice received tPBM); B - the оbject recognition test, reflecting the processes of learning, recognition and memorization (* - p<0.05 vs. cubes in 1 session; Δ - p<0.05 vs. cube Nº1 («familiar» object) in 2 session). n = 7 for each group.
Fig. 4
Fig. 4 The OCT monitoring of the rate of accumulation of GNRs in dcLN in untreated mice and in mice received tPBM: a - scheme of OCT measurement of GNRs the accumulation in dcLN; c – anatomical position of the deep and superficial cervical lymph nodes in the neck of mice; c – example of OCT image of dcLN before and 60 min after start of OCT recording (more bright square means more high level of GNRs in dcLN); d-g - OCT data of rate of accumulation of GNRs in dcLNs in untreated mice (black line), in mice received PBM (red line) after GNRs injection into: d) the cisterna magna; e) the right lateral ventricle; i) the cortex; g) the hippocampus. * - p<0.05 vs. basal level; † - p<0.05 between groups. n = 7 in each group.

Tables (1)

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Table 1 – Different 1267nm fluence effects on scalp temperature, morphological changes in the brain meninges and Aβ accumulation in the brain

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