Anti-PD1 antibody and not anti-LAG-3 antibody improves the antitumor effect of photodynamic therapy for treating metastatic breast cancer

Shan Long; Yibing Zhao; Yuanyuan Xu; Bo Wang; Haixia Qiu; Hongyou Zhao; Jing Zeng; Defu Chen; Hui Li; Jiakang Shao; Xiaosong Li; Ying Gu

doi:10.1142/S1793545823500207

[1] R. L. Siegel, K. D. Miller, H. E. Fuchs, A. Jemal. Cancer statistics. CA Cancer J. Clin., 72, 7-33(2022).

[2] S. Loibl, P. Poortmans, M. Morrow, C. Denkert, G. Curigliano. Breast cancer. Lancet, 397, 1750-1769(2021).

[3] A. M. Rkein, D. M. Ozog. Photodynamic therapy. Dermatol. Clin., 32, 415-425(2014).

[4] Y. Wang, Y. Gu. Advances in clinical application and study on tumor-targeted photodynamic therapy. Chin. J. Laser Med. Surg., 26, 279-287(2017).

[5] P. Mroz, J. T. Hashmi, Y. Y. Huang, N. Lange, M. R. Hamblin. Stimulation of anti-tumor immunity by photodynamic therapy. Expert Rev. Clin. Immunol., 7, 75-91(2011).

[6] A. P. Castano, P. Mroz, M. R. Hamblin. Photodynamic therapy and anti-tumour immunity. Nat. Rev. Cancer., 6, 535-545(2006).

[7] C. Donohoe, M. O. Senge, L. G. Arnaut, L. C. Gomes-da-Silva. Cell death in photodynamic therapy: From oxidative stress to anti-tumor immunity. Biochim. Biophys. Acta Rev. Cancer., 1872, 188308(2019).

[8] A. D. Garg, L. Vandenberk, C. Koks, T. Verschuere, L. Boon, S. W. Van Gool, P. Agostinis. Dendritic cell vaccines based on immunogenic cell death elicit danger signals and T cell-driven rejection of high-grade glioma. Sci. Transl. Med., 8, 328ra327(2016).

[9] D. Kessel. Apoptosis, paraptosis and autophagy: Death and survival pathways associated with photodynamic therapy. Photochem. Photobiol., 95, 119-125(2019).

[10] D. Kessel, N. L. Oleinick. Photodynamic therapy and cell death pathways. Methods Mol. Biol., 635, 35-46(2010).

[11] S. O. Gollnick. Photodynamic therapy and antitumor immunity. J. Natl. Compr. Canc. Netw., 10, S40-S43(2012).

[12] D. V. Krysko, A. D. Garg, A. Kaczmarek, O. Krysko, P. Agostinis, P. Vandenabeele. Immunogenic cell death and DAMPs in cancer therapy. Nat. Rev. Cancer., 12, 860-875(2012).

[13] H. L. Liu, Y. D. Liu, J. Zeng, H. X. Qiu, Y. Gu. Immunological effect induced by low light dose tumor targeted photodynamic therapy delivered at low fluence rate and underlying mechanisms: A review. Chin. J. Laser Med. Surg., 28, 351-357(2019).

[14] P. S. Thong, K. W. Ong, N. S. Goh, K. W. Kho, V. Manivasager, R. Bhuvaneswari, M. Olivo, K. C. Soo. Photodynamic-therapy-activated immune response against distant untreated tumours in recurrent angiosarcoma. Lancet Oncol., 8, 950-952(2007).

[15] C. Lu, F. Zhou, S. Wu, L. Liu, D. Xing. Phototherapy-induced antitumor immunity: Long-term tumor suppression effects via photoinactivation of respiratory chain oxidase-triggered superoxide anion burst. Antioxid. Redox Signal., 24, 249-262(2016).

[16] F. Anzengruber, P. Avci, L. F. de Freitas, M. R. Hamblin. T-cell mediated anti-tumor immunity after photodynamic therapy: Why does it not always work and how can we improve it?. Photochem. Photobiol. Sci., 14, 1492-1509(2015).

[17] S. Takaya, H. Saito, M. Ikeguchi. Upregulation of immune checkpoint molecules, PD-1 and LAG-3, on CD4+ and CD8+ T cells after gastric cancer surgery. Yonago Acta Med., 58, 39-44(2015).

[18] M. Davern, N. E. Donlon, O. C. F. A. D. Sheppard, C. Hayes, R. King, H. Temperley, C. Butler, A. Bhardwaj, J. Moore, D. Bracken-Clarke, C. Donohoe, N. Ravi, J. V. Reynolds, S. G. Maher, M. J. Conroy, J. Lysaght. Cooperation between chemotherapy and immune checkpoint blockade to enhance anti-tumour T cell immunity in oesophageal adenocarcinoma. Transl. Oncol., 20, 101406(2022).

[19] H. M. Du. Study on the co-expression characteristics and effect of LAG3 and PD-1 on the T cells of breast cancer patients(2020).

[20] S. Long, Y. B. Zhao, Y. Y. Xu, H. Li, H. Y. Zhao, D. F. Chen, J. Zeng, H. X. Qiu, X. S. Li, Y. Gu. Immune response induced by hematoporphyrin derivatives mediated photodynamic therapy: Immunogenic cell death and elevated costimulatory molecules. J. Innov. Opt. Health Sci., 15, 12(2022).

[21] I. Beltrán Hernández, Y. Yu, F. Ossendorp, M. Korbelik, S. Oliveira. Preclinical and clinical evidence of immune responses triggered in oncologic photodynamic therapy: Clinical recommendations. J. Clin. Med., 9, 333(2020).

[22] E. Ostanska, D. Aebisher, D. Bartusik-Aebisher. The potential of photodynamic therapy in current breast cancer treatment methodologies. Biomed. Pharmacother., 137, 111302(2021).

[23] T. G. St Denis, K. Aziz, A. A. Waheed, Y. Y. Huang, S. K. Sharma, P. Mroz, M. R. Hamblin. Combination approaches to potentiate immune response after photodynamic therapy for cancer. Photochem. Photobiol. Sci., 10, 792-801(2011).

[24] A. Juarranz, P. Jaén, F. Sanz-Rodríguez, J. Cuevas, S. González. Photodynamic therapy of cancer. Basic principles and applications. Clin. Transl. Oncol., 10, 148-154(2008).

[25] B. W. Henderson, T. M. Busch, J. W. Snyder. Fluence rate as a modulator of PDT mechanisms. Lasers Surg. Med., 38, 489-493(2006).

[26] M. Shams, B. Owczarczak, P. Manderscheid-Kern, D. A. Bellnier, S. O. Gollnick. Development of photodynamic therapy regimens that control primary tumor growth and inhibit secondary disease. Cancer Immunol Immunother., 64, 287-297(2015).

[27] B. W. Henderson, S. O. Gollnick, J. W. Snyder, T. M. Busch, P. C. Kousis, R. T. Cheney, J. Morgan. Choice of oxygen-conserving treatment regimen determines the inflammatory response and outcome of photodynamic therapy of tumors. Cancer Res., 64, 2120-2126(2004).

[28] S. O. Gollnick, C. M. Brackett. Enhancement of anti-tumor immunity by photodynamic therapy. Immunol. Res., 46, 216-226(2010).

[29] E. Panzarini, V. Inguscio, L. Dini. Immunogenic cell death: Can it be exploited in PhotoDynamic Therapy for cancer?. Biomed. Res. Int., 2013, 482160(2013).

[30] M. Ahmad, R. C. Rees, S. A. Ali. Escape from immunotherapy: Possible mechanisms that influence tumor regression/progression. Cancer Immunol. Immunother., 53, 844-854(2004).

[31] W. Zou. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer., 5, 263-274(2005).

[32] Q. Q. Peng, J. L. Li, P. L. Xin, K. X. Du, X. Y. Lin, J. X. Wu, M. T. Zhang, X. Q. Kong. Assessment of the expression and response of PD-1, LAG-3, and TIM-3 after neoadjuvant radiotherapy in rectal cancer. Neoplasma, 68, 742-750(2021).

[33] V. Sasidharan Nair, H. El Salhat, R. Z. Taha, A. John, B. R. Ali, E. Elkord. DNA methylation and repressive H3K9 and H3K27 trimethylation in the promoter regions of PD-1, CTLA-4, TIM-3, LAG-3, TIGIT, and PD-L1 genes in human primary breast cancer. Clin. Epigen., 10, 1-12(2018).

[34] G. M. Cramer, E. K. Moon, K. A. Cengel, T. M. Busch. Photodynamic therapy and immune checkpoint blockade. Photochem. Photobiol., 96, 954-961(2020).

[35] J. Fourcade, P. Kudela, Z. Sun, H. Shen, S. R. Land, D. Lenzner, P. Guillaume, I. F. Luescher, C. Sander, S. Ferrone, J. M. Kirkwood, H. M. Zarour. PD-1 is a regulator of NY-ESO-1-specific CD8+ T cell expansion in melanoma patients. J. Immunol., 182, 5240-5249(2009).

[36] A. L. Kinter, E. J. Godbout, J. P. McNally, I. Sereti, G. A. Roby, M. A. O’Shea, A. S. Fauci. The common gamma-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J. Immunol., 181, 6738-6746(2008).

[37] M. M. Staron, S. M. Gray, H. D. Marshall, I. A. Parish, J. H. Chen, C. J. Perry, G. Cui, M. O. Li, S. M. Kaech. The transcription factor FoxO1 sustains expression of the inhibitory receptor PD-1 and survival of antiviral CD8(+) T cells during chronic infection. Immunity, 41, 802-814(2014).

[38] J. W. Austin, P. Lu, P. Majumder, R. Ahmed, J. M. Boss. STAT3, STAT4, NFATc1, and CTCF regulate PD-1 through multiple novel regulatory regions in murine T cells. J. Immunol., 192, 4876-4886(2014).

[39] S. O. Gollnick, X. Liu, B. Owczarczak, D. A. Musser, B. W. Henderson. Altered expression of interleukin 6 and interleukin 10 as a result of photodynamic therapy in vivo. Cancer Res., 57, 3904-3909(1997).

[40] S. Evans, W. Matthews, R. Perry, D. Fraker, J. Norton, H. I. Pass. Effect of photodynamic therapy on tumor necrosis factor production by murine macrophages. J. Natl. Cancer Inst., 82, 34-39(1990).

[41] G. Kick, G. Messer, A. Goetz, G. Plewig, P. Kind. Photodynamic therapy induces expression of interleukin 6 by activation of AP-1 but not NF-kappa B DNA binding. Cancer Res., 55, 2373-2379(1995).

[42] I. B. Barsoum, C. A. Smallwood, D. R. Siemens, C. H. Graham. A mechanism of hypoxia-mediated escape from adaptive immunity in cancer cells. Cancer Res., 74, 665-674(2014).

[43] P. Sharma, S. Hu-Lieskovan, J. A. Wargo, A. Ribas. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell, 168, 707-723(2017).

[44] S. Spranger, T. F. Gajewski. Impact of oncogenic pathways on evasion of antitumour immune responses. Nat. Rev. Cancer., 18, 139-147(2018).

[45] K. Mimura, L. F. Kua, J. F. Xiao, B. R. Asuncion, Y. Nakayama, N. Syn, Z. Fazreen, R. Soong, K. Kono, W. P. Yong. Combined inhibition of PD-1/PD-L1, Lag-3, and Tim-3 axes augments antitumor immunity in gastric cancer-T cell coculture models. Gastric Cancer, 24, 611-623(2021).

[46] A. Gao, B. Chen, J. Gao, F. Zhou, M. Saeed, B. Hou, Y. Li, H. Yu. Sheddable prodrug vesicles combating adaptive immune resistance for improved photodynamic immunotherapy of cancer. Nano Lett., 20, 353-362(2020).

[47] Y. Fujiwara, S. Kato, M. Nesline, J. Conroy, P. DePietro, S. Pabla, R. J. C. T. R. Kurzrock. Indoleamine 2,3-dioxygenase (IDO) inhibitors and cancer immunotherapy. Cancer Treat Rev., 110, 102461(2022).

[48] M. J. O’Shaughnessy, K. S. Murray, S. P. La Rosa, S. Budhu, T. Merghoub, A. Somma, S. Monette, K. Kim, R. B. Corradi, A. Scherz, J. A. Coleman. Systemic antitumor immunity by PD-1/PD-L1 inhibition is potentiated by vascular-targeted photodynamic therapy of primary tumors. Clin. Cancer Res., 24, 592-599(2018).

[49] A. Garcia-Diaz, D. S. Shin, B. H. Moreno, J. Saco, H. Escuin-Ordinas, G. A. Rodriguez, J. M. Zaretsky, L. Sun, W. Hugo, X. Wang, G. Parisi, C. P. Saus, D. Y. Torrejon, T. G. Graeber, B. Comin-Anduix, S. Hu-Lieskovan, R. Damoiseaux, R. S. Lo, A. Ribas. Interferon receptor signaling pathways regulating PD-L1 and PD-L2 expression. Cell Rep., 19, 1189-1201(2017).

[50] R. Bao, Y. Wang, J. Lai, H. Zhu, Y. Zhao, S. Li, N. Li, J. Huang, Z. Yang, F. Wang, Z. Liu. Enhancing anti-PD-1/PD-L1 immune checkpoint inhibitory cancer therapy by CD276-targeted photodynamic ablation of tumor cells and tumor vasculature. Mol. Pharm., 16, 339-348(2019).

[51] L. Gao, C. Zhang, D. Gao, H. Liu, X. Yu, J. Lai, F. Wang, J. Lin, Z. Liu. Enhanced anti-tumor efficacy through a combination of integrin αvβ6-targeted photodynamic therapy and immune checkpoint inhibition. Theranostics, 6, 627-637(2016).