TUMOR-SPECIFIC IMMUNE RESPONSE AFTER PHOTODYNAMIC THERAPY
https://doi.org/10.15789/1563-0625-2016-5-405-416
Abstract
Increased incidence of malignancies requires a search for new therapeutic approaches. E.g., photodynamic therapy (PDT) is an effective anti-cancer treatment that involves administration of a photosensitizing dye followed by visible light irradiation of the tumor. Pre-clinical studies have shown that local photodynamic therapy enhances systemic antitumor immunity. Moreover, it is well known that the long-term effects of PDT depend on functioning of intact adaptive immune response. In this context, the immune system plays a fundamental role. Interestingly, the PDT action is associated with stimulation of systemic immune response against a locally treated tumor. In fact, PDT has been shown to effectively stimulate both innate and adaptive immune systems of the host, by triggering the release of various pro-inflammatory and acutephase response mediators thus leading to massive infiltration of the treated site with neutrophils, dendritic cells and other inflammatory cells. PDT efficacy depends, in part, on induction of tumor-specific immune response which is dependent on cytotoxic T lymphocytes and natural killer (NK) cells. The set of specific receptors enables NK cells to recognize surface molecules on the target cells. Expression of the latter molecules is indicative of viral infection, tumor formation, or cell stress (e.g., DNA damage). The NK cells are also involved into various biological processes in the organism, playing a critical role in immune surveillance, thus representing a potential tool for cancer therapy. It was shown that the tumor cells have increased sensitivity to NK cell-mediated lytic action following PDT. In this review, we further discuss potential relationships between PDT and antitumor immune response.
About the Authors
Yu. N. Anokhin
National Research Nuclear University “Moscow Engineering Physics Institute”;
A. Tsyb Medical Radiological Research Centre, Branch of the National Medical Research Radiological Centre
Russian Federation
Russian Federation
PhD (Medicine), Head, Nuclear Medicine Department;
Leading Research Associate, Department of Combined Effects,
Obninsk
E. V. Abakushina
National Research Nuclear University “Moscow Engineering Physics Institute”;
A. Tsyb Medical Radiological Research Centre, Branch of the National Medical Research Radiological Centre
Russian Federation
Russian Federation
PhD (Medicine), Associate Professor, Department of Radionuclide Medicine;
Senior Research Associate, Laboratory of Clinical Immunology,
249036, Obninsk, Koroleva, str., 4
References
1. Абакушина Е.В. Роль стресс-индуцированных молекул MICA/В в противоопухолевом иммунном ответе // Злокачественные опухоли, 2012. T. 2, № 2. С. 103-105. [Abakushina E.V. The role of stress-induced molecules MICA/B in the anti-tumor immune response. Zlokachestvennye opukholi = Malignant Tumors, 2012, Vol. 2, no. 2, pp. 103-105. (In Russ.)]
2. Абакушина Е.В. Метод проточной цитометрии для оценки NK-клеток и их активности // Клиническая лабораторная диагностика, 2015. Т. 60, № 11. C. 37-44. [Abakushina E.V. The technique of flow cytometry in evaluation of NK-cells and their activity. Klinicheskaya laboratornaya diagnostika = Clinical Laboratory Diagnostics, 2015, Vol. 60, no. 11, pp. 37-44. (In Russ.)]
3. Абакушина Е.В., Клинкова А.В., Каневский Л.М., Коваленко Е.И. Увеличение растворимых форм стресс-индуцированных молекул MICA при онкологических заболеваниях // Молекулярная медицина, 2014. № 3. С. 34-38. [Abakushina E.V., Klinkova A.V., Kanevsky L.M., Kovalenko E.I. Elevation of serum levels of soluble forms of stress-induced molecules MICA in oncological diseases. Molekulyarnaya meditsina = Molecular Medicine, 2014, no. 3, pp. 34-38. (In Russ.)]
4. Абакушина Е.В., Абакушин Д.Н., Неприна Г.С., Пасова И.А., Бердов Б.А., Клинкова А.В., Коваленко Е.И., Каприн А.Д. Повышение уровня цитокинов и стресс-индуцированных молекул MICA в сыворотке крови больных раком желудка и толстой кишки // Цитокины и воспаление, 2015. Т. 14, № 1. С. 63-67. [Abakushina E.V., Abakushin D.N., Neprina G.S., Pasova I.A., Berdov B.A., Klinkova A.V., Kovalenko E.I., Kaprin A.D. Elevation of serum levels of cytokines and stress-induced molecules MICA in patients with gaster and colon cancer. Tsitokiny i vospalenie = Cytokines and Inflammation, 2015, Vol. 14, no. 1, pp. 63-67. (In Russ.)]
5. Абакушина Е.В., Романко Ю.С., Каплан М.А., Каприн А.Д. Противоопухолевый иммунный ответ и фотодинамическая терапия // Радиация и риск, 2014. Т. 23, № 4. С. 92-98. [Abakushina E.V., Romanko Yu.S., Kaplan M.A., Kaprin A.D. Anticancer immune response and photodynamic therapy. Radiaciya i risk = Radiation and Risk, 2014, Vol. 23, no. 4, pp. 92-98. (In Russ.)]
6. Абакушина Е.В., Маризина Ю.В., Неприна Г.С. Эффективность совместного применения IL-2 и IL-15 для активации цитотоксических лимфоцитов in vitro // Гены и клетки, 2015. Т. 10, № 2. C. 78-85. [Abakushina E.V., Marizina Yu.V., Neprina G.S. Efficiency of IL-2 and IL-15 combined use for activation of cytotoxic lymphocytes in vitro. Geny i kletki = Gene and Cells, 2015, Vol. 10, no. 2, рp. 78-85. (In Russ.)]
7. Васильев Н.Е., Сысоева Г.М, Даниленко Е.Д. Иммунологические аспекты фотодинамической терапии // Медицинская иммунология, 2003. T. 5, № 5-6. C. 507-518. [Vasiliev N.E., Sysoev G.M., Danilenko E.D. Immunological aspects of photodynamic therapy. Meditsinskaya immunologiya = Medical Immunology (Russia), 2003, Vol. 5, no. 5-6. pp. 507-518. (In Russ.)]
8. Каприн А.Д., Старинский В.В., Петрова Г.В. Злокачественные образования в России в 2013 году (заболеваемость и смертность). М.: МНИОИ им. П.А. Герцена – филиал ФГБУ «ФМИЦ им. П.А. Герцена» Министерства здравоохранения РФ, 2015. 250 с. [Kaprin A.D., Starinsky V.V., Petrova G.V. Malignant tumors in Russia in 2013 (morbidity and mortality)]. Moscow: Р. Hertsen Moscow Oncology Research Institute – Branch of the National Medical Research Radiological Centre, 2015. 250 p.
9. Карташова М.Г., Кильдюшевский А.В., Молочков А.В., Федулкина В.А. Трансляционная клеточная иммунотерапия идиотипического и иммуносупрессивного типов саркомы Капоши // Российский журнал кожных и венерических болезней, 2013. № 3. С. 13-18. [Kartashova M.G., Kildyushevsky A.V., Molochkov A.V., Fedulkina V.A. Translation cellular immunotherapy of idiopathic and immunosuppressive kaposi’s sarcoma. Rossijskij zhurnal kozhnyh i venericheskih boleznej = Russian Journal of Skin and Venereal Diseases, 2013, no. 3, pp. 13-18. (In Russ.)]
10. Клинкова А.В., Кузьмина Е.Г., Абакушина Е.В., Каневский Л.М., Неприна Г.С., Павлов В.В., Коваленко Е.И. Циркулирующий белок MICА у больных злокачественными лимфомами // Медицинская иммунология, 2016. Т. 18, № 2. C. 151-162. [Klinkova A.V., Kuzmina E.G., Abakushina E.V., Kanevsky L.M., Neprina G.S., Pavlov V.V., Kovalenko E.I. Сirculating MICA protein in the patients with malignant lymphomas. Meditsinskaya Immunologiya = Medical Immunology (Russia), 2016, Vol. 18, no. 2, pp. 151-162. (In Russ.)] http://dx.doi.org/10.15789/1563-0625-2016-2-151-162
11. Коваленко Е.И., Стрельникова Ю.И., Каневский Л.М., Абакушина Е.В. Влияние стресс-индуцируемой молекулы MICA на активность NK-клеток человека // Омский научный вестник, 2007. № 3 (61). С. 29-31. [Kovalenko E.I., Strelnikova Yu.I., Konevsky L.M., Abakushina E.V. Influence of stress-induced molecule MICA on the activity of human NK-cells. Omsky nauchniy vestnik = Omsk Scientific Bulletin, 2007, no. 3 (61), pp. 29-31. (In Russ.)]
12. Кузнецов В.В. Использование фотодинамической терапии в отечественной онкологии // Исследования и практика в медицине, 2015. Т. 2, № 4. С. 98-105. [Kuznetsov V.V. The use of photodynamic therapy in the domestic oncology. Issledovaniya i praktika v meditsine = Research and Practice in Medicine, 2015, Vol. 2, no. 4, pp. 98-105. (In Russ.)]
13. Маризина Ю.В., Абакушина Е.В., Неприна Г.С., Пасова И.А. NKG2D иммунорецептор и его лиганды в периферической крови больных меланомой и раком кишечника // Злокачественные опухоли, 2015. № 4, спецвыпуск 2. С. 313. [Marizina Yu.V., Abakushina E.V., Neprina G.S., Pasova I.A. NKG2D immunoreceptor and its ligands in peripheral blood of patients with melanoma and colon cancer. Zlokachestvennye opukholi = Malignant Tumors, 2015, no. 4, p. 313. (In Russ.)]
14. Чернышев И.В., Алтунин Д.В., Самсонов Ю.В., Каллаев К.К. Новые возможности фотодинамической диагностики и лечения рака предстательной железы и почки // Экспериментальная и клиническая урология, 2011. № 2-3. С. 92-94. [Chernyshev I.V., Altunin D.V., Samsonov Yu.V., Kallaev K.K. Photodynamic methods of diagnostics and treatment of prostate and kidney cancer: new possibilities. Eksperimental`naya i klinicheskaya urologiya = Experimental and Clinical Urology, 2011, Vol. 2-3, pp. 92-94. (In Russ.)]
15. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science, 1999, Vol. 285, pp. 727-729.
16. Belicha-Villanueva A., Riddell J., Naveen B., Gollnick S.O. The Effect of Photodynamic Therapy on Tumor Cell Expression of Major Histocompatibility Complex (MHC) Class I and MHC Class I-Related. Molecules Lasers Surg. Med., 2012, Vol. 44, no. 1, pp. 60-68.
17. Buytaert E., Dewaele M., Agostinis P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim. Biophys. Acta, 2007, Vol. 1776, pp. 86-107.
18. Cassatella M.A. Neutrophil-derived proteins: selling cytokines by the pound. Adv. Immunol., 1999, Vol. 73, pp. 369-509.
19. Castano A.P., Mroz P., Hamblin M.R. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer, 2006, no. 6, pp. 535-545.
20. Cecic I., Korbelic M. Mediators of peripheral blood neutrophilia induced by photodynamic therapy of solid tumors. Cancer Lett., 2002, Vol. 183, no. 1, pp. 43-51.
21. Chen W.R., Adams R.L., Carubelli R., Nordguist R.E. Laser-photosensitizer assisted immunotherapy: a novel modality for cancer treatment. Cancer Lett., 1997, Vol. 115, no. 1, pp. 25-30.
22. Cruz L.B., Ribeiro A.S., Rech A., Rosa L.G., Castro C.G.Jr., Brunetto A.L. Influence of low-energy laser in the prevention of oral mucositis in children with cancer receiving chemotherapy. Pediatr. Blood Cancer, 2007, Vol. 48, no. 4, pp. 435-440.
23. Dolmans D.E., Fukumura D., Jain R.K. Photodynamic therapy for cancer. Nat. Rev. Cancer, 2003, no. 3, pp. 380-387.
24. Dougherty T.J., Gomer C.J., Henderson B.W., Jori G., Kessel D., Korbelik M., Moan J., Peng Q. Photodynamic therapy. J. Natl. Cancer Inst., 1998, Vol. 90, no. 12, pp. 889-905.
25. Fingar V.H., Wieman T.J., Doak K.W. Role of thromboxane and prostacyclin release on photodynamic therapy-induced tumor destruction. Cancer Res., 1990, Vol. 50, no. 9, pp. 2599-2603.
26. Frost G.A., Halliday G.M., Damian D.L. Photodynamic therapy-induced immunosuppression in humans is prevented by reducing the rate of light delivery. J. Invest. Dermatol., 2011, Vol. 131, pp. 962-968.
27. Gao L., Zhang C., Gao D., Liu H., Yu X., Lai J., Wang F., Lin J., Liu Z. Enhanced Anti-Tumor Efficacy through a Combination of Integrin αvβ6-Targeted Photodynamic Therapy and Immune Checkpoint Inhibition. Theranostics, 2016, Vol. 6, no. 5, pp. 627-637.
28. Genot M.T., Klastersky J. Low-level laser for prevention and therapy of oral mucositis induced by chemotherapy or radiotherapy. Curr. Opin. Oncol., 2005, Vol. 17, no. 3, pp. 236-240.
29. Gholamreza Esmaeeli D., Emami A., Ataie-Fashtami L., Safaeinodehi S.R., Merikh-Baiat F., Fateh M., Zand N. Low Level laser therapy in management of chemotherapy-induced oral mucositis: prophylaxis or treatment? J. Laser Med. Sci., 2011, Vol. 2, no. 1, pp. 12-17.
30. Gollnick S.O., Liu X., Owczarczak B., Musser D.A., Henderson B.W. Altered expression of interleukin 6 and interleukin 10 as result of photodynamic therapy in vitro. Cancer Res., 1997, Vol. 57, no. 18, pp. 3904-3909.
31. Gollnick S.O., Vaughan L., Henderson B.W. Generation of effective antitumor vaccines using photodynamic therapy. Cancer Res., 2002, Vol. 62, no. 6, pp. 1604-1608.
32. Hamblin M.R., Newman E.L. On the mechanism of the tumour-localising effect in photodynamic therapy. J. Photochem. Photobiol., 1994, Vol. 23, no. 1, pp. 3-8.
33. Henderson B.W., Dougherty T.J. How does photodynamic therapy work? Photochem. Photobiol., 1992, Vol. 55, no. 1, pp. 145-157.
34. Hillemanns P., Garcia F., Petry K.U., Dvorak V., Sadovsky O., Iversen O.E., Einstein M.H. A randomized study of hexaminolevulinate photodynamic therapy in patents with cervical intraepithelial neoplasia. Am. J. Obstet. Gynecol., 2015, Vol. 212, no. 4, pp. 465.e1-465.e7.
35. Hugget M.T., Jermyn M., Gillams A., Illing R., Mosse S., Novelli M, Kent E., Bown S.G., Hasan T., Pogue B.W., Pereira S.P. Phase I/II study of verteporfn photodynamic therapy in locally advanced pancreatic cancer. Br. J. Cancer, 2014, Vol. 110, no. 7, pp. 1698-1704.
36. Jalili A., Makowski M., Switaj T., Nowis D., Wilczynski G.M., Wilczek E., Chorazy-Massalska M., Radzikowska A., Maslinski W., Biały L., Sienko J., Sieron A., Adamek M., Basak G., Mróz P., Krasnodebski I.W., Jakóbisiak M., Gołab J. Effective photoimmunotherapy of murine colon carcinoma induced by the combination of photodynamic therapy and dendritic cells. Clin. Cancer Res., 2004, Vol. 13, pp. 4498-4508.
37. Kabingu E., Vaughan L., Owczarczak B., Ramsey K.D., Gollnick S.O. CD8+ T cell-mediated control of distant tumours following local photodynamic therapy is independent of CD4+ T cells and dependent on natural killer cells. Br. J. Cancer., 2007, Vol. 96, no. 12, pp. 1839-1848.
38. Korbelik M., Cecic I., Merchant S., Sun J. Acute phase response induction by cancer treatment with photodynamic therapy. Int. J. Cancer, 2008, Vol. 122, no. 6, pp. 1411-1417.
39. Korbelik M., Cecic I. Contribution of myeloid and lymphoid host cells to the curative outcome of mouse sarcoma treatment by photodynamic therapy. Cancer Letters, 1999, Vol. 137, pp. 91-98.
40. Korbelik M., Dougherty G.J. Photodynamic therapy-mediated immune response against subcutaneous mouse tumors. Cancer Res., 1999, Vol. 59, no. 8, pp. 1941-1946.
41. Korbelik M., Krosl G., Krosl J., Dougherty G.J. The role of host lymphoid populations in the response of mouse EMT6 tumor to photodynamic therapy. Cancer Research, 1996, Vol. 56, pp. 5647-5652.
42. Korbelik M. PDT-associated host response and its role in the therapy outcome. Lasers Surg. Med., 2006, Vol. 38, no. 5, pp. 500-508.
43. Korbelik M., Krosl G. Enhanced macrophage cytotoxicity against tumor cells treated with phptodynamic therapy. Photochem. Photobiol., 1994, Vol. 60, pp. 497-502.
44. Korbelik M., Sun J. Cancer treatment by photodynamic therapy combined with adoptive immunotherapy using genetically altered natural killer cell line. Int. J. Cancer, 2001, Vol. 93, pp. 269-274.
45. Krosl G., Korbelik M., Dougherty G.J. Induction of immune cell infiltration into murine SCCVII tumour by photofrin-based photodynamic therapy. Br. J. Cancer, 1995, Vol. 71, no. 3, pp. 549-555.
46. Lloyd A.R., Oppenheim J.J. Poly’s lament: the neglected role of the polymorphonuclear neutrophil in the afferent limb of the immune response. Immunol. Today, 1992, Vol. 13, no. 5, pp. 169-172.
47. Matthews YJ, Damian DL. Topical photodynamic therapy is immunosuppressive in humans. Br. J. Dermatol., 2010, Vol. 162, pp. 637-641.
48. Mroz P., Hamblin M.R. The immunosuppressive side of PDT. Photochem. Photobiol. Sci., 2011, Vol. 10, pp. 751-758.
49. Musser D.A., Camacho S.H., Manderscheid P.A., Oseroff A.R. The anatomic site of photodynamic therapy is a determinant for immunosuppression in a murine model. Photochem. Photobiol., 1999, Vol. 69, no. 2, pp. 222-225.
50. Nes A.G., Posso M.B. Patients with moderate chemotherapy-induced mucositis: pain therapy using low intensity lasers. Int. Nurs. Rev., 2005, Vol. 52, no. 1, pp. 68-72.
51. Ortel B., Shea C.R., Calzavara-Pinton P. Molecular mechanisms of photodynamic therapy. Front. Biosci., 2009, Vol. 14, pp. 4157-4172.
52. Park M.J., Bae J.H., Chung J.S., Kim S.H., Kang C.D. Induction of NKG2D ligands and increased sensitivity of tumor cells to NK cell-mediated cytotoxicity by hematoporphyrin-based photodynamic therapy. Immunol. Investigat., 2011, Vol. 40, pp. 367-382.
53. Piette J. Signalling pathway activation by photodynamic therapy: NF-κB at the crossroad between oncology and immunology. Photochem. Photobiol. Sci., 2015, Vol. 14, no. 8, pp. 1510-1517.
54. Qin B., Selman S.H., Payne K.M., Keck R.W., Metzger D.W. Enhanced skin allograft survival after photodynamic therapy. Association with lymphocyte inactivation and macrophage stimulation. Transplantation, 1993, Vol. 56, no. 6, pp. 1481-1486.
55. Reginato E., Wolf P., Hamblin M.R. Immune response after photodynamic therapy increases anti-cancer and anti-bacterial effects. World J. Immunol., 2014, Vol. 4, no. 1, pp. 1-11.
56. Sgambato A., Cittadini A. Inflammation and cancer: a multifaceted link. Eur. Rev. Med. Pharmacol. Sci., 2010, Vol. 14, pp. 263-268.
57. Thanos S.M., Halliday G.M., Damian D.L. Nicotinamide reduces photodynamic therapy-induced immunosuppression in humans. Br. J. Dermatol., 2012, Vol. 167, pp. 631-636.
58. de Vree W.J., Essers M.C., de Bruijn H.S., Star W.M., Koster J.F., Sluiter W. Evidence for an important role of neutrophils in the efficacy of photodynamic therapy in vivo. Cancer Res., 1996, Vol. 56, no. 13, pp. 2908-2911.
59. Wachowska M., Gabrysiak M., Muchowicz A., Bednarek W., Barankiewicz J., Rygiel T., Boon L., Mroz P., Hamblin M.R., Golab J. 5-Aza-2’-deoxycytidine potentiates antitumour immune response induced by photodynamic therapy. Eur. J. Cancer, 2014, Vol. 7, pp. 1370-1381.
60. Wachowska M, Muchowicz A., Golab J. Targeting epigenetic processes in photodynamic therapy-induced anticancer immunity. Front. Oncol., 2015, Vol. 5, p. 176.
61. Wachowska M., Muchowicz A., Demkow U. Immunological aspects of antitumor photodynamic therapy outcome. Cent. Eur. J. Immunol., 2015, Vol. 40, no. 4, pp. 481-485.
62. Wieman T.J., Mang T.S., Fingar V.H., Hill T.G., Reed M.W., Corey T.S., Nguyen V.Q., Render E.R.Jr. Effect of photodynamic therapy on blood flow in normal and tumor vessels. Surgery, 1988, Vol. 104, no. 3, pp. 512-517.
63. Zhang C., Wang Y., Zhou Z., Zhang J., Tian Z. Sodium butyrate upregulates expression of NKG2D ligand MICA/B in HeLa and HepG2 cell lines and increases their susceptibility to NK lyses. Cancer Immunol. Immunother., 2009, Vol. 58, pp. 1275-1285.
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Anokhin Yu.N., Abakushina E.V. TUMOR-SPECIFIC IMMUNE RESPONSE AFTER PHOTODYNAMIC THERAPY. Medical Immunology (Russia). 2016;18(5):405-416. (In Russ.) https://doi.org/10.15789/1563-0625-2016-5-405-416
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