Inhibition of photodynamic therapy induced‑immunosuppression with aminolevulinic acid leads to enhanced outcomes of tumors and pre‑cancerous lesions (Review)
- Authors:
- Sharlo Bayless
- Jeffrey B. Travers
- Ravi P. Sahu
- Craig A. Rohan
-
Affiliations: Department of Pharmacology and Toxicology, Boonshoft School of Medicine, Wright State University, Dayton, OH 45435, USA - Published online on: July 14, 2021 https://doi.org/10.3892/ol.2021.12925
- Article Number: 664
-
Copyright: © Bayless et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Dougherty TJ and Marcus SL: Photodynamic therapy. Eur Cancer. 28:1734–1742. 1992. View Article : Google Scholar : PubMed/NCBI | |
Sharman WM, Allen CM and van Lier JE: Photodynamic therapeutics: Basic principles and clinical applications. Drug Disc Today. 4:507–517. 1999. View Article : Google Scholar : PubMed/NCBI | |
Ochsner M: Photophysical and photobiological processes in the photodynamic therapy of tumours. J Photochem Photobiol B. 39:1–18. 1997. View Article : Google Scholar : PubMed/NCBI | |
Moan J: Porphyrin photosensitization and phototherapy. Photochem Photobiol. 43:681–690. 1986. View Article : Google Scholar : PubMed/NCBI | |
Allison RR, Downie GH, Cuenca R, Hu XH, Childs CJ and Sibata CH: Photosensitizers in clinical PDT. Photodiagnosis Photodyn Ther. 1:27–42. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kwiatkowski S, Knap B, Przystupski D, Saczko J, Kędzierska E, Knap-Czop K, Kotlińska J, Michel O, Kotowski K and Kulbacka J: Photodynamic therapy-mechanisms, photosensitizers and combinations. Biomed Pharmacother. 106:1098–1107. 2018. View Article : Google Scholar : PubMed/NCBI | |
Abrahamse H and Hamblin MR: New photosensitizers for photodynamic therapy. Biochem J. 473:347–364. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, Jiang C, Figueiró Longo JP, Azevedo RB, Zhang H and Muehlmann LA: An updated overview on the development of new photosensitizers for anticancer photodynamic therapy. Acta Pharm Sin B. 8:137–146. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chatterjee DK, Fong LS and Zhang Y: Nanoparticles in photodynamic therapy: An emerging paradigm. Adv Drug Deliv Rev. 60:1627–1637. 2008. View Article : Google Scholar : PubMed/NCBI | |
Gold M: ALA-PDT and MAL-PDT: What makes them different. J Clin Aesthet Dermatol. 2:44–47. 2009. | |
Cantisani C, Paolino G, Faina V, Frascani F, Cantoresi F, Bianchini D, Gilda Fazia and Stefano Calvieri: Overview on topical 5-ALA photodynamic therapy use for non melanoma skin cancers. Int J Photoen. 2014:3048622014. View Article : Google Scholar | |
Morton CA and Braathen LR: Daylight photodynamic therapy for actinic keratoses. Am J Clin Dermatol. 19:647–656. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wehner MR: Comparing the efficacy of field treatments for actinic keratosis: A critical appraisal of a randomized trial in the New England Journal of Medicine. Br J Dermatol. 182:1343–1344. 2020. View Article : Google Scholar : PubMed/NCBI | |
Taub AF: Photodynamic therapy in dermatology: History and horizons. J Drugs Dermatol. 3 (Suppl 1):S8–S25. 2004.PubMed/NCBI | |
Armbrecht AM: A prospective study of visual function and quality of life following PDT in patients with wet age related macular degeneration. Br J Ophthalmol. 88:1270–1273. 2004. View Article : Google Scholar : PubMed/NCBI | |
McBride G: Studies expand potential uses of photodynamic therapy. J Natl Cancer Inst. 94:1740–1742. 2002. View Article : Google Scholar : PubMed/NCBI | |
Korbelik M, Banáth J and Saw K: Immunoregulatory cell depletion improves the efficacy of photodynamic therapy-generated cancer vaccines. Int J Mol Sci. 16:27005–27014. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wachowska M, Stachura J, Tonecka K, Fidyt K, Braniewska A, Sas Z, Kotula I, Rygiel TP, Boon L, Golab J and Muchowicz A: Inhibition of IDO leads to IL-6-dependent systemic inflammation in mice when combined with photodynamic therapy. Cancer Immunol Immunother. 69:1101–1112. 2020. View Article : Google Scholar : PubMed/NCBI | |
Reddan JC, Anderson CY, Xu H, Hrabovsky S, Freye K, Fairchild R, Tubesing KA and Elmets CA: Immunosuppressive effects of silicon phthalocyanine photodynamic therapy. Photochem Photobiol. 70:72–77. 1999. View Article : Google Scholar : PubMed/NCBI | |
Lynch DH, Haddad S, King VJ, Ott MK, Straight R and Jolles CJ: Systemic immunosuppression induced by photodynamic therapy (PDT) is adoptively transferred by macrophages. Photochem Photobiol. 49:453–458. 1989. View Article : Google Scholar : PubMed/NCBI | |
Reginato E, Mroz P, Chung H, Kawakubo M, Wolf P and Hamblin MR: Photodynamic therapy plus regulatory T-cell depletion produces immunity against a mouse tumour that expresses a self-antigen. Br J Cancer. 109:2167–2174. 2013. View Article : Google Scholar : PubMed/NCBI | |
Mroz P and Hamblin MR: The immunosuppressive side of PDT. Photochem Photobiol Sci. 10:751–758. 2011. View Article : Google Scholar : PubMed/NCBI | |
Falk-Mahapatra R and Gollnick SO: Photodynamic therapy and immunity: An update. Photochem Photobiol. 96:550–559. 2020. View Article : Google Scholar : PubMed/NCBI | |
Nobbe S, Trüeb RM, French LE and Hofbauer GFL: Herpes simplex virus reactivation as a complication of photodynamic therapy. Photodermatol Photoimmunol Photomed. 27:51–52. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wolf P, Fink-Puches R, Reimann-Weber A and Kerl H: Development of malignant melanoma after repeated topical photodynamic therapy with 5-Aminolevulinic acid at the exposed site. Dermatology. 194:53–54. 1997. View Article : Google Scholar : PubMed/NCBI | |
Fiechter S, Skaria A, Nievergelt H, Anex R, Borradori L and Parmentier L: Facial basal cell carcinomas recurring after photodynamic therapy: A retrospective analysis of histological subtypes. Dermatology. 224:346–351. 2012. View Article : Google Scholar : PubMed/NCBI | |
Castano AP, Mroz P, Wu MX and Hamblin MR: Photodynamic therapy plus low-dose cyclophosphamide generates antitumor immunity in a mouse model. Proc Natl Acad Sci USA. 105:5495–5500. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sun X, Cao Z, Mao K, Wu C, Chen H, Wang J, Wang X, Cong X, Li Y, Meng X, et al: Photodynamic therapy produces enhanced efficacy of antitumor immunotherapy by simultaneously inducing intratumoral release of sorafenib. Biomaterials. 240:1198452020. View Article : Google Scholar : PubMed/NCBI | |
Lindau D, Gielen P, Kroesen M, Wesseling P and Adema GJ: The immunosuppressive tumour network: Myeloid-derived suppressor cells, regulatory T cells and natural killer T cells. Immunology. 138:105–115. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Ma Y, Fang Y, Wu S, Liu L, Fu D and Shen X: Regulatory T cell: A protection for tumour cells. J Cell Mol Med. 16:425–436. 2012. View Article : Google Scholar : PubMed/NCBI | |
Lee CR, Kwak Y, Yang T, Han JH, Park SH, Ye MB, Lee W, Sim KY, Kang JA, Kim YC, et al: Myeloid-derived suppressor cells are controlled by regulatory T cells via TGF-β during murine colitis. Cell Rep. 17:3219–3232. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fujimura T, Kambayashi Y and Aiba S: Crosstalk between regulatory T cells (Tregs) and myeloid derived suppressor cells (MDSCs) during melanoma growth. Onco Immunol. 1:1433–1434. 2012.PubMed/NCBI | |
Ferracini M, Sahu RP, Harrison KA, Waeiss RA, Murphy RC, Jancar S, Konger RL and Travers JB: Topical photodynamic therapy induces systemic immunosuppression via generation of platelet-activating factor receptor ligands. J Invest Dermatol. 135:321–323. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sahu RP, Petrache I, van Demark MJ, Rashid BM, Ocana JA, Tang Y, Yi Q, Turner MJ, Konger RL and Travers JB: Cigarette smoke exposure inhibits contact hypersensitivity via the generation of platelet-activating factor agonists. J Immunol. 190:2447–2454. 2013. View Article : Google Scholar : PubMed/NCBI | |
Zhang Q, Yao Y, Konger RL, Sinn AL, Cai S, Pollok KE and Travers JB: UVB radiation-mediated inhibition of contact hypersensitivity reactions is dependent on the platelet-activating factor system. J Invest Dermatol. 128:1780–1787. 2008. View Article : Google Scholar : PubMed/NCBI | |
Zelenay S, van der Veen AG, Böttcher JP, Snelgrove KJ, Rogers N, Acton SE, Chakravarty P, Girotti MR, Marais R, Quezada SA, et al: Cyclooxygenase-dependent tumor growth through evasion of immunity. Cell. 162:1257–1270. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ke J, Yang Y, Che Q, Jiang F, Wang H, Chen Z, Zhu M, Tong H, Zhang H, Yan X, et al: Prostaglandin E2 (PGE2) promotes proliferation and invasion by enhancing SUMO-1 activity via EP4 receptor in endometrial cancer. Tumor Biol. 37:12203–12211. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, Ohlfest JR and Okada H: COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 71:2664–2674. 2011. View Article : Google Scholar : PubMed/NCBI | |
Makowski M, Grzela T, Niderla J, Łazarczyk M, Mróz P, Kopeé M, Legat M, Strusińska K, Koziak K, Nowis D, et al: Inhibition of cyclooxygenase-2 indirectly potentiates antitumor effects of photodynamic therapy in mice. Clin Cancer Res. 9:5417–5422. 2003.PubMed/NCBI | |
Togashi Y and Nishikawa H: Regulatory T cells: Molecular and cellular basis for immunoregulation. Curr Top Microbiol Immunol. 410:3–27. 2017.PubMed/NCBI | |
Najafi M, Farhood B and Mortezaee K: Contribution of regulatory T cells to cancer: A review. J Cell Physiol. 234:7983–7993. 2019. View Article : Google Scholar : PubMed/NCBI | |
Moreno Ayala MA, Li Z and DuPage M: Treg programming and therapeutic reprogramming in cancer. Immunology. 157:198–209. 2019. View Article : Google Scholar : PubMed/NCBI | |
Yan S, Zhang Y and Sun B: The function and potential drug targets of tumour-associated Tregs for cancer immunotherapy. Sci China Life Sci. 62:179–186. 2019. View Article : Google Scholar : PubMed/NCBI | |
Oh DS, Kim H, Oh JE, Jung HE, Lee YS, Park JH and Lee HK: Intratumoral depletion of regulatory T cells using CD25-targeted photodynamic therapy in a mouse melanoma model induces antitumoral immune responses. Oncotarget. 8:47440–47453. 2017. View Article : Google Scholar : PubMed/NCBI | |
Mellor AL, Lemos H and Huang L: Indoleamine 2,3-Dioxygenase and tolerance: Where are we now? Front Immunol. 8:13602017. View Article : Google Scholar : PubMed/NCBI | |
Baban B, Chandler PR, Sharma MD, Pihkala J, Koni PA, Munn DH and Mellor AL: IDO activates regulatory T cells and blocks their conversion into Th17-Like T cells. J Immuno. 183:2475–2483. 2009. View Article : Google Scholar : PubMed/NCBI | |
Huang Z, Wei G, Zeng Z, Huang Y, Huang L, Shen Y, Sun X, Xu C and Zhao C: Enhanced cancer therapy through synergetic photodynamic/immune checkpoint blockade mediated by a liposomal conjugate comprised of porphyrin and IDO inhibitor. Theranostics. 9:5542–5557. 2019. View Article : Google Scholar : PubMed/NCBI | |
Consonni FM, Porta C, Marino A, Pandolfo C, Mola S, Bleve A and Sica A: Myeloid-derived suppressor cells: Ductile targets in disease. Front Immunol. 10:9492019. View Article : Google Scholar : PubMed/NCBI | |
Pawelec G, Verschoor CP and Ostrand-Rosenberg S: Myeloid-derived suppressor cells: Not only in tumor immunity. Front Immunol. 10:10992019. View Article : Google Scholar : PubMed/NCBI | |
Zuo H, Hou Y, Yu Y, Li Z, Liu H, Liu C, He J and Miao L: Circumventing myeloid-derived suppressor cell-mediated immunosuppression using an oxygen-generated and -economized nanoplatform. ACS ACS Appl Mater Interfaces. 12:55723–55736. 2020. View Article : Google Scholar : PubMed/NCBI | |
Groth C, Hu X, Weber R, Fleming V, Altevogt P, Utikal J and Umansky V: Immunosuppression mediated by myeloid-derived suppressor cells (MDSCs) during tumour progression. Br J Cancer. 120:16–25. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ostrand-Rosenberg S, Sinha P, Beury DW and Clements VK: Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol. 22:275–281. 2012. View Article : Google Scholar : PubMed/NCBI | |
Bruno A, Mortara L, Baci D, Noonan DM and Albini A: Myeloid derived suppressor cells interactions with natural killer cells and pro-angiogenic activities: Roles in tumor progression. Fronti Immunol. 10:7712019. View Article : Google Scholar : PubMed/NCBI | |
Iclozan C, Antonia S, Chiappori A, Chen DT and Gabrilovich D: Therapeutic regulation of myeloid-derived suppressor cells and immune response to cancer vaccine in patients with extensive stage small cell lung cancer. Cancer Immunol Immunother. 62:909–918. 2013. View Article : Google Scholar : PubMed/NCBI | |
Larue L, Myrzakhmetov B, Ben-Mihoub A, Moussaron A, Thomas N, Arnoux P, Baros F, Vanderesse R, Acherar S and Frochot C: Fighting hypoxia to improve PDT. Pharmaceuticals (Basel). 12:1632019. View Article : Google Scholar : PubMed/NCBI | |
Mai X, Zhang Y, Fan H, Song W, Chang Y, Chen B, Shi J, Xin X, Teng Z, Sun J and Teng G: Integration of immunogenic activation and immunosuppressive reversion using mitochondrial-respiration-inhibited platelet-mimicking nanoparticles. Biomaterials. 232:1196992020. View Article : Google Scholar : PubMed/NCBI | |
Zhou Z, Zhang B, Wang H, Yuan A, Hu Y and Wu J: Two-stage oxygen delivery for enhanced radiotherapy by perfluorocarbon nanoparticles. Theranostics. 8:4898–4911. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ji C, Lu Z, Xu Y, Shen B, Yu S and Shi D: Self-production of oxygen system CaO2/MnO2 @PDA-MB for the photodynamic therapy research and switch-control tumor cell imaging. J Biomed Mater Res B Appl Biomater. 106:2544–2552. 2018. View Article : Google Scholar : PubMed/NCBI | |
Cao M, Xu Y, Youn J, Cabrera R, Zhang X, Gabrilovich D, Nelson DR and Liu C: Kinase inhibitor Sorafenib modulates immunosuppressive cell populations in a murine liver cancer model. Lab Invest. 91:598–608. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ferrario A, von Tiehl K, Wong S, Luna M and Gomer CJ: Cyclooxygenase-2 inhibitor treatment enhances photodynamic therapy-mediated tumor response. Cancer Res. 62:3956–3961. 2002.PubMed/NCBI | |
Zhang Z, Huang S, Wu S, Qi J, Li W, Liu S, Cong Y, Chen H, Lu L, Shi S, et al: Clearance of apoptotic cells by mesenchymal stem cells contributes to immunosuppression via PGE2. EBioMedicine. 45:341–350. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kim SH, Roszik J, Cho S-N, Ogata D, Milton DR, Peng W, Menter DG, Ekmekcioglu S and Grimm EA: The COX2 effector microsomal PGE2 synthase 1 is a regulator of immunosuppression in cutaneous melanoma. Clin Cancer Res. 25:1650–1663. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ferrario A and Gomer CJ: Targeting the tumor microenvironment using photodynamic therapy combined with inhibitors of cyclooxygenase-2 or vascular endothelial growth factor. Methods Mol Biol. 635:121–132. 2010. View Article : Google Scholar : PubMed/NCBI | |
Van der Geer S and Krekels GAM: Treatment of actinic keratoses on the dorsum of the hands: ALA-PDT versus diclofenac 3% gel followed by ALA-PDT. A placebo-controlled, double-blind, pilot study. J Dermatolog Treat. 20:259–265. 2009. View Article : Google Scholar : PubMed/NCBI | |
Rollakanti K, Anand S and Maytin EV: Topical calcitriol prior to photodynamic therapy enhances treatment efficacy in non-melanoma skin cancer mouse models. Proc SPIE Int Soc Opt Eng. 9308:93080Q2015.PubMed/NCBI | |
Ni C, Gan X, Li X, Sun H, Chen Z and Lu H: Vitamin D alleviates acute graft-versus-host disease through promoting the generation of Foxp3+ T cells. Ann Transl Med. 7:7482019. View Article : Google Scholar : PubMed/NCBI | |
van der Aar AM, Sibiryak DS, Bakdash G, van Capel TM, van der Kleij HP, Opstelten DJ, Teunissen MB, Kapsenberg ML and de Jong EC: Vitamin D3 targets epidermal and dermal dendritic cells for induction of distinct regulatory T cells. J Allergy Clin Immunol. 127:1532–1540.e7. 2011. View Article : Google Scholar : PubMed/NCBI | |
Rosenberg AR, Tabacchi M, Ngo KH, Wallendorf M, Rosman IS, Cornelius LA and Demehri S: Skin cancer precursor immunotherapy for squamous cell carcinoma prevention. JCI Insight. 4:e1254762019. View Article : Google Scholar : PubMed/NCBI | |
Park J, Halliday GM, Surjana D and Damian DL: Nicotinamide prevents ultraviolet radiation-induced cellular energy loss. Photochem Photobiol. 86:942–948. 2010. View Article : Google Scholar : PubMed/NCBI | |
Gensler HL: Prevention of photoimmunosuppression and photocarcinogenesis by topical nicotinamide. Nutr Cancer. 29:157–162. 1997. View Article : Google Scholar : PubMed/NCBI | |
Gensler HL, Williams T, Huang AC and Jacobson EL: Oral niacin prevents photocarcinogenesis and photoimmunosuppression in mice. Nutr Cancer. 34:36–41. 1999. View Article : Google Scholar : PubMed/NCBI | |
Thanos SM, Halliday GM and Damian DL: Nicotinamide reduces photodynamic therapy-induced immunosuppression in humans. Br J Dermatol. 167:631–636. 2012. View Article : Google Scholar : PubMed/NCBI | |
Surjana D, Halliday GM, Martin AJ, Moloney FJ and Damian DL: Oral nicotinamide reduces actinic keratoses in phase II double-blinded randomized controlled trials. J Invest Dermatol. 132:1497–1500. 2012. View Article : Google Scholar : PubMed/NCBI | |
Knip M, Douek IF, Moore WPT, Gillmor HA, McLean AEM, Bingley PJ and Gale EA; European Nicotinamide Diabetes Intervention Trial Group, : Safety of high-dose nicotinamide: A review. Diabetologia. 43:1337–1345. 2000. View Article : Google Scholar : PubMed/NCBI | |
Foster TH, Murant RS, Bryant RG, Knox RS, Gibson SL and Hilf R: Oxygen consumption and diffusion effects in photodynamic therapy. Radiat Res. 126:296–303. 1991. View Article : Google Scholar : PubMed/NCBI | |
Frost GA, Halliday GM and Damian DL: Photodynamic therapy-induced immunosuppression in humans is prevented by reducing the rate of light delivery. J Invest Dermatol. 131:962–968. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ericson MB, Sandberg C, Stenquist B, Gudmundson F, Karlsson M, Ros A-M, Rosén A, Larkö O, Wennberg AM and Rosdahl I: Photodynamic therapy of actinic keratosis at varying fluence rates: Assessment of photobleaching, pain and primary clinical outcome. Br J Dermatol. 151:1204–1212. 2004. View Article : Google Scholar : PubMed/NCBI |