Programmed Death Ligand 1 (PD-L1) Expression in Lymphomas: State of the Art
Abstract
:1. Introduction
2. Principal Issues in Assessing PD-L1 Immunohistochemical Expression in Lymphomas
3. cHL and PD1/PD-L1 Axis
4. DLBCL, NOS, Other Aggressive Peripheral B-Cell Lymphomas and PD-1/PD-L1 Axis
5. Peripheral T-Cell Lymphomas (PTCLs) and PD-1/PD-L1 Axis
6. ALCL and PD-1/PD-L1 Axis
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Keir, M.E.; Butte, M.J.; Freeman, G.J.; Sharpe, A.H. Pd-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008, 26, 677–704. [Google Scholar] [CrossRef] [PubMed]
- Jin, H.; Ahmed, R.; Okazaki, T. Role of PD-1 in regulating T-cell immunity. Curr. Top. Microbiol. Immunol. 2011, 350, 17–37. [Google Scholar] [PubMed]
- Weber, J. Immune checkpoint proteins: A new therapeutic paradigm for cancer-preclinical background: CTLA-4 and PD-1 blockade. Semin. Oncol. 2010, 37, 430–439. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Crabill, G.A.; Pritchard, T.S.; McMiller, T.L.; Wei, P.; Pardoll, D.M.; Pan, F.; Topalian, S.L. Mechanisms regulating PD-L1 expression on tumor and immune cells. J. Immunother. Cancer 2019, 7, 305. [Google Scholar] [CrossRef] [PubMed]
- Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12, 252–264. [Google Scholar] [CrossRef] [PubMed]
- Topalian, S.L.; Drake, C.G.; Pardoll, D.M. Immune checkpoint blockade: A common denominator approach to cancer therapy. Cancer Cell 2015, 27, 450–461. [Google Scholar] [CrossRef] [PubMed]
- Palicelli, A.; Bonacini, M.; Croci, S.; Magi-Galluzzi, C.; Cañete-Portillo, S.; Chaux, A.; Bisagni, A.; Zanetti, E.; De Biase, D.; Melli, B.; et al. What do we have to know about PD-L1 expression in prostate cancer? A systematic literature review. Part 1: Focus on immunohistochemical results with discussion of pre-analytical and interpretation variables. Cells 2021, 10, 3166. [Google Scholar] [CrossRef] [PubMed]
- Palicelli, A.; Croci, S.; Bisagni, A.; Zanetti, E.; De Biase, D.; Melli, B.; Sanguedolce, F.; Ragazzi, M.; Zanelli, M.; Chaux, A.; et al. What do we have to know about PD-L1 expression in prostate cancer? A systematic literature review. Part 3: PD-L1, intracellular signaling pathways and tumor microenvironment. Int. J. Mol. Sci. 2021, 22, 12330. [Google Scholar] [CrossRef] [PubMed]
- Blank, C.; Gajewski, T.F.; Mackensen, A. Interaction of PD-L1 on tumor cells with PD.1 on tumor-specific T cells as a mechanism of immune evasion: Implications for tumor immunotherapy. Cancer Immunol. Immunother. 2005, 54, 307–314. [Google Scholar] [CrossRef]
- Broggi, G.; Angelico, G.; Farina, J.; Tinnirello, G.; Barresi, V.; Zanelli, M.; Palicelli, A.; Certo, F.; Barbagallo, G.; Magro, G.; et al. Tumor-associated microenvironment, PD-L1 expression and their relationship with immunotherapy in glioblastoma, IDH-wild type: A comprehensive review with emphasis on the implications for neuropathologists. Pathol. Res. Pract. 2024, 254, 155144. [Google Scholar] [CrossRef]
- Palicelli, A.; Croci, S.; Bisagni, A.; Zanetti, E.; De Biase, D.; Melli, B.; Sanguedolce, F.; Ragazzi, M.; Zanelli, M.; Chaux, A.; et al. What do we have to know about PD-L1 expression in prostate cancer? A systematic literature review—Part 5: Epigenetic regulation of PD-L1. Int. J. Mol. Sci. 2021, 22, 12314. [Google Scholar] [CrossRef]
- Gong, J.; Chehrazi-Raffle, A.; Reddi, S.; Salgia, R. Development of PD-1 and PD-L1 inhibitors as a form of cancer immunotherapy: A comprehensive review of registration trials and future considerations. J. Immunother. Cancer 2018, 6, 8. [Google Scholar] [CrossRef] [PubMed]
- Menter, T.; Bodmer-Haecki, A.; Dirnhofer, S.; Tzankov, A. Evaluation of the diagnostic and prognostic value of PD-L1 expression in Hodgkin and B-cell lymphomas. Hum. Pathol. 2016, 54, 17–24. [Google Scholar] [CrossRef]
- Xie, W.; Medeiros, L.J.; Li, S.; Tang, G.; Fan, G.; Xu, J. PD-1/PD-L1 pathway: A therapeutic target in CD30+ large cell lymphomas. Biomedicines 2022, 10, 1587. [Google Scholar] [CrossRef]
- Kong, J.; Dasari, S.; Feldman, A.L. PD-L1 expression in anaplastic large cell lymphoma. Mod. Pathol. 2020, 33, 1232–1233. [Google Scholar] [CrossRef]
- Shen, J.; Li, S.; Medeiros, L.J.; Lin, P.; Wang, S.A.; Tang, G.; Yin, C.C.; You, M.J.; Khoury, J.D.; Iyer, S.P.; et al. PD-L1 expression is associated with ALK positivity and STAT3 activation, but not outcome in patients with systemic anaplastic large-cell lymphoma. Mod. Pathol. 2019, 33, 324–333. [Google Scholar] [CrossRef]
- Xie, W.; Medeiros, L.J.; Li, S.; Yin, C.C.; Khoury, J.D.; Xu, J. PD-1/PD-L1 pathway and its blockade in patients with classic Hodgkin lymphoma and non-Hodgkin large-cell lymphoma. Curr. Hematol. Malig. Rep. 2020, 15, 372–381. [Google Scholar] [CrossRef]
- Iwafuchi, H.; Nakazawa, A.; Sekimizu, M.; Mori, T.; Osumi, T.; Iijima-Yamashita, Y.; Ohki, K.; Kiyokawa, N.; Fukano, R.; Saito, A.M.; et al. Clinicopathological features and prognostic significance of programmed death ligand 1 in pediatric ALK-positive anaplastic large cell lymphoma: Results of the ALCL99 treatment in Japan. Hum. Pathol. 2021, 116, 112–121. [Google Scholar] [CrossRef]
- Zhang, J.-P.; Song, Z.; Wang, H.-B.; Lang, L.; Yang, Y.-Z.; Xiao, W.; Webster, D.E.; Wei, W.; Barta, S.K.; Kadin, M.E.; et al. A novel model of controlling PD-L1 expression in ALK+ anaplastic large cell lymphoma revealed by CRISPR screening. Blood 2019, 134, 171–185. [Google Scholar] [CrossRef]
- Atsaves, V.; Tsesmetzis, N.; Chioureas, D.; Kis, L.; Leventaki, V.; Drakos, E.; Panaretakis, T.; Grander, D.; Medeiros, L.J.; Young, K.H.; et al. PD-L1 is commonly expressed and transcriptionally regulated by STAT3 and MYC in ALK-negative anaplastic large-cell lymphoma. Leukemia 2017, 31, 1633–1637. [Google Scholar] [CrossRef]
- Festino, L.; Botti, G.; Lorigan, P.; Masucci, G.V.; Hipp, J.D.; Horak, C.E.; Melero, I.; Ascierto, P.A. Cancer treatment with anti-PD-1/PD-L1 agents: Is PD-L1 expression a biomarker for patient selection? Drugs 2016, 76, 925–945. [Google Scholar] [CrossRef]
- Vennapusa, B.; Baker, B.M.; Kowanetz, M.; Boone, J.B.; Menzl, I.; Bruey, J.-M.; Fine, G.; Mariathasan, S.; McCaffery, I.; Mocci, S.; et al. Development of a PD-L1 complementary diagnostic immunohistochemistry assay (SP142) for atezolizumab. Appl. Immunohistochem. Mol. Morphol. 2019, 27, 92–100. [Google Scholar] [CrossRef]
- Tsao, M.S.; Kerr, K.M.; Kockx, M.; Beasley, M.-B.; Borczuk, A.C.; Botling, J.; Bubendorf, L.; Chirieac, L.; Chen, G.; Chou, T.-Y.; et al. PD-L1 immunohistochemistry comparability study in real-life clinical samples: Results of blueprint phase 2 project. J. Thorac. Oncol. 2018, 13, 1302–1311. [Google Scholar] [CrossRef]
- Li, Y.; Vennapusa, B.; Chang, C.-W.; Tran, D.B.; Nakamura, R.B.; Sumiyoshi, T.; Hegde, P.; Molinero, L. Prevalence study of PD-L1 SP142 assay in metastatic triple-negative breast cancer. Appl. Immunohistochem. Mol. Morphol. 2021, 29, 258–264. [Google Scholar] [CrossRef]
- Sankar, K.; Ye, J.C.; Li, Z.; Zheng, L.; Song, W.; Hu-Lieskovan, S. The role of biomarkers in personalized immunotherapy. Biomark. Res. 2022, 10, 32. [Google Scholar] [CrossRef]
- Ghebeh, H.; Mohammed, S.; Al-Omair, A.; Qattant, A.; Lehe, C.; Al-Qudaihi, G.; Elkum, N.; Alshabanah, M.; Bin Amer, S.; Tulbah, A.; et al. The B7-H1 (PD-L1) T-lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: Correlation with important high-risk prognostic factors. Neoplasia 2006, 8, 190–198. [Google Scholar] [CrossRef]
- Thompson, R.H.; Dong, H.; Kwon, E.D. Implications of B7-H1 expression in clear cell carcinoma of the kidney for prognostication and therapy. Clin. Cancer Res. 2007, 13, 709s–715s. [Google Scholar] [CrossRef]
- Chen, X.; Wu, W.; Wei, W.; Zou, L. Immune checkpoint inhibitors in peripheral T-cell lymphoma. Front. Pharmacol. 2022, 13, 869488. [Google Scholar] [CrossRef]
- Scheerens, H.; Malong, A.; Bassett, K.; Boyd, Z.; Gupta, V.; Harris, J.; Mesick, C.; Simnett, S.; Stevens, H.; Gilbert, H.; et al. Current status of companion and complementary diagnostics: Strategic considerations for development and launch. Clin. Transl. Sci. 2017, 10, 84–92. [Google Scholar] [CrossRef]
- Liu, D.; Wang, S.; Bindeman, W. Clinical applications of PD-L1 bioassays for cancer immunotherapy. J. Hematol. Oncol. 2017, 10, 110. [Google Scholar] [CrossRef]
- Conroy, J.M.; Pabla, S.; Nesline, M.K.; Glenn, S.T.; Papanicolau-Sengos, A.; Burgher, B.; Andreas, J.; Giamo, V.; Wang, Y.; Lenzo, F.L.; et al. Next generation sequencing of PD-L1 for predicting response to immune checkpoint inhibitors. J. Immunother. Cancer 2019, 7, 18. [Google Scholar] [CrossRef]
- Yamamoto, R.; Nishikori, M.; Kitawaki, T.; Sakai, T.; Hishizawa, M.; Tashima, M.; Kondo, T.; Ohmori, K.; Kurata, M.; Hayashi, T.; et al. PD-1-PD-L1 ligand interaction contributes to immunosuppressive microenvironment of Hodgkin lymphoma. Blood 2008, 111, 3220–3224. [Google Scholar] [CrossRef]
- Muenst, S.; Hoeller, S.; Dirnhofer, S.; Tzankov, A. Increased programmed death-1 + tumor-infiltrating lymphocytes in classical Hodgkin lymphoma substantiate reduced overall survival. Hum. Pathol. 2009, 40, 1715–1722. [Google Scholar] [CrossRef]
- Jelinek, T.; Mihalyova, J.; Kascak, M.; Duras, J.; Hajek, R. PD-1/PD-L1 inhibitors in haematological neoplasms: Update 2017. Immunology 2017, 152, 357–371. [Google Scholar] [CrossRef]
- Roemer, M.G.M.; Advani, R.H.; Ligon, A.H.; Natkunam, Y.; Redd, R.A.; Homer, H.; Connelly, C.F.; Sun, H.H.; Daadi, S.E.; Freeman, G.J.; et al. PD-L1 and PD-L2 genetic alterations define classical Hodgkin lymphoma and predict outcome. J. Clin. Oncol. 2016, 34, 2690–2697. [Google Scholar] [CrossRef]
- Shi, Y.; Mi, L.; Lai, Y.; Zhao, M.; Jia, L.; Du, T.; Song, Y.; Li, X. PD-L1 immunohistochemistry assay optimization to provide more comprehensive pathological information in classic Hodgkin lymphoma. J. Hematop. 2023, 16, 7–16. [Google Scholar] [CrossRef]
- Chen, B.J.; Chapuy, B.; Ouyang, J.; Sun, H.H.; Roemer, M.G.; Xu, M.L.; Yu, H.; Fletcher, C.D.; Freeman, G.J.; Shipp, M.A.; et al. PD-L1 expression is characteristic of a subset of aggressive B-cell lymphomas and virus-associated malignancies. Clin. Cancer Res. 2013, 19, 3462–3473. [Google Scholar] [CrossRef]
- Green, M.R.; Rodig, S.; Juszczynski, P.; Ouyang, J.; Sinha, P.; O’Donnell, E.; Neuberg, D.; Shipp, M.A. Constitutive AP-1 activity and EBV infection induce PDL1 in Hodgkin lymphomas and posttransplant lymphoproliferative disorders: Implications for targeted therapy. Clin. Cancer Res. 2012, 18, 1611–1618. [Google Scholar] [CrossRef]
- Zanelli, M.; Sanguedolce, F.; Palicelli, A.; Zizzo, M.; Martino, G.; Caprera, C.; Fragliasso, V.; Soriano, A.; Valle, L.; Ricci, S.; et al. EBV-driven lymphoproliferative disorders and lymphomas of the gastrointestinal tract: A spectrum of entities with a common denominator (Part 1). Cancers 2021, 13, 4578. [Google Scholar] [CrossRef]
- Navarro, A.; Diaz, T.; Martinez, A.; Gaya, A.; Pons, A.; Gel, B.; Codony, C.; Ferrer, G.; Martinez, C.; Montserrat, E.; et al. Regulation of JAK2 by miR-135a: Prognostic impact in classic Hodgkin lymphoma. Blood 2009, 114, 2945–2951. [Google Scholar] [CrossRef]
- Carey, C.D.; Gusenleitner, D.; Lipschitz, M.; Roemer, M.G.M.; Stack, E.C.; Gjini, E.; Hu, X.; Redd, R.; Freeman, G.J.; Neuberg, D.; et al. Topological analysis reveals a PD-L1-associated microenvironmental niche for Reed-Sternberg cells in Hodgkin lymphoma. Blood 2017, 130, 2420–2430. [Google Scholar] [CrossRef] [PubMed]
- Ansell, S.M.; Lesokhin, A.M.; Borrello, I.; Halwani, A.; Scott, E.C.; Gutierrez, M.; Schuster, S.J.; Millenson, M.M.; Cattry, D.; Freeman, G.J.; et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin’s lymphoma. N. Engl. J. Med. 2015, 372, 311–319. [Google Scholar] [CrossRef] [PubMed]
- Moy, R.H.; Younes, A. Immune checkpoint inhibition in Hodgkin lymphoma. Hemasphere 2018, 2, e20. [Google Scholar] [CrossRef] [PubMed]
- Younes, A.; Ansell, S.; Fowler, N.; Wilson, W.; de Vos, S.; Seymour, J.; Advani, R.; Forero, A.; Morschhauser, F.; Kersten, M.J.; et al. The landscape of new drugs in lymphoma. Nat. Rev. Clin. Oncol. 2017, 14, 335–346. [Google Scholar] [CrossRef] [PubMed]
- Armand, P.; Chen, Y.-B.; Redd, R.A.; Joyce, R.M.; Bsat, J.; Jeter, E.; Merryman, R.W.; Coleman, K.C.; Dahi, P.B.; Nieto, Y.; et al. PD-1 blockade with pembrolizumab for classical Hodgkin lymphoma after autologous stem cell transplantation. Blood 2019, 134, 22–29. [Google Scholar] [CrossRef] [PubMed]
- Herrera, A.F.; Moskowitz, A.J.; Bartlett, N.L.; Vose, J.M.; Ramchandren, R.; Feldman, T.A.; LaCasce, A.S.; Ansell, S.M.; Moskowitz, C.H.; Fenton, K.; et al. Interim results of brentuximab vedotin in combination with nivolumab in patients with relapsed or refractory Hodgkin lymphoma. Blood 2018, 131, 1183–1194. [Google Scholar] [CrossRef] [PubMed]
- Alaggio, R.; Amador, C.; Anagnostopoulos, I.; Attygalle, A.D.; Araujo, I.B.d.O.; Berti, E.; Bhagat, G.; Borges, A.M.; Boyer, D.; Calaminici, M.; et al. The 5th edition of the World Health Organization Classification of Haematolymphoid Tumours: Lymphoid Neoplasms. Leukemia 2022, 36, 1720–1748. [Google Scholar] [CrossRef] [PubMed]
- Campo, E.; Jaffe, E.S.; Cook, J.R.; Quintanilla-Martinez, L.; Swerdlow, S.H.; Anderson, K.C.; Brousset, P.; Cerroni, L.; de Leval, L.; Dirnhofer, S.; et al. The International Consensus Classification of mature lymphoid neoplasms: A report from the Clinical Advisory Committee. Blood 2022, 140, 1229–1253. [Google Scholar] [CrossRef]
- Zanelli, M.; Sanguedolce, F.; Zizzo, M.; Palicelli, A.; Pellegrini, D.; Farinacci, S.; Soriano, A.; Froio, E.; Cormio, L.; Carrieri, G.; et al. Primary diffuse large B-cell lymphoma of the urinary bladder: Update on a rare disease and potential diagnostics pitfall. Curr. Oncol. 2022, 29, 956–968. [Google Scholar] [CrossRef]
- Georgiou, K.; Chen, L.; Berglund, M.; Ren, W.; de Miranda, N.F.C.C.; Lisboa, S.; Fangazio, M.; Zhu, S.; Hou, Y.; Wu, K.; et al. Genetic basis of PD-L1 overexpression in diffuse large B-cell lymphomas. Blood 2016, 127, 3026–3034. [Google Scholar] [CrossRef]
- Hu, L.-Y.; Xu, X.-L.; Rao, H.-L.; Chen, J.; Lai, R.-C.; Huang, H.-Q.; Jiang, W.-Q.; Lin, T.-Y.; Xia, Z.-J.; Cai, Q.-Q. Expression and clinical value of programmed cell death-ligand 1 (PD-L1) in diffuse large B-cell lymphoma: A retrospective study. Clin. J. Cancer 2017, 36, s40880. [Google Scholar] [CrossRef]
- Kiyasu, J.; Miyoshi, H.; Hirata, A.; Arakawa, F.; Ichikawa, A.; Niino, D.; Sugita, Y.; Yufu, Y.; Choi, I.; Abe, Y.; et al. Expression of programmed cell death ligand 1 is associated with poor overall survival in patients with diffuse large B-cell lymphoma. Blood 2015, 126, 2193–2201. [Google Scholar] [CrossRef]
- Kwiecinska, A.; Tsesmetzis, N.; Ghaderi, M.; Kis, L.; Saft, L.; Rassidakis, G.Z. CD274 (PD-L1)/PDCD1 (PD-1) expression in de novo and transformed diffuse large B-cell lymphoma. Br. J. Haematol. 2018, 180, 744–748. [Google Scholar] [CrossRef]
- McCord, R.; Bolen, C.R.; Koeppen, H.; Kadel, E.E.; Oestergaard, M.Z.; Nielsen, T.; Sehn, L.H.; Venstrom, J.M. PD-L1 and tumor-associated macrophages in de novo DLBCL. Blood Adv. 2019, 3, 531–540. [Google Scholar] [CrossRef]
- Oyama, T.; Yamamoto, K.; Asano, N.; Oshiro, A.; Suzuki, R.; Kagami, Y.; Morishima, Y.; Takeuchi, K.; Izumo, T.; Mori, S.; et al. Age-related EBV-associated B-cell lymphoproliferative disorders constitute a distinct clinicopathologic group: A study of 96 patients. Clin. Cancer Res. 2007, 13, 5124–5132. [Google Scholar] [CrossRef]
- Dojcinov, S.D.; Venkataraman, G.; Pittaluga, S.; Wlodarska, I.; Schrager, J.A.; Raffeld, M.; Hills, R.K.; Jaffe, E.S. Age-related EBV associated lymphoproliferative disorders in the western population: A spectrum of reactive lymphoid hyperplasia and lymphoma. Blood 2011, 117, 4726–4735. [Google Scholar] [CrossRef] [PubMed]
- Swerdlow, S.H.; Campo, E.; Harris, N.L.; Jaffe, E.S.; Pileri, S.A.; Stein, H.; Thiele, J.; Vardiman, J.W. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissue; IARC: Lyon, France, 2008. [Google Scholar]
- Nicolae, A.; Pittaluga, S.; Abdullah, S.; Steinberg, S.M.; Pham, T.A.; Davies-Hill, T.; Xi, L.; Raffeld, M.; Jaffe, E.S. EBV-positive large B-cell lymphomas in young patients: A nodal lymphoma with evidence for a tolerogenic immune environment. Blood 2015, 126, 863–872. [Google Scholar] [CrossRef]
- Uccini, S.; Al-Jadiry, M.F.; Scarpino, S.; Ferraro, D.; Alsaadawi, A.R.; Al-Darraji, A.F.; Moleti, M.L.; Testi, A.M.; Al-Hadad, S.A.; Ruco, L. Epstein-Barr virus-positive diffuse large B-cell lymphoma in children: A disease reminiscent of Epstein Barr virus-positive diffuse large B-cell lymphoma of the elderly. Hum. Pathol. 2015, 46, 716–724. [Google Scholar] [CrossRef]
- Miyagi, S.; Ishikawa, E.; Nakamura, M.; Shimada, K.; Yamamura, T.; Furukawa, K.; Tanaka, T.; Mabuchi, S.; Tsuyuki, Y.; Kohno, K.; et al. Reappraisal of primary Epstein-Barr virus (EBV)-positive diffuse large B-cell lymphoma of the gastrointestinal tract. Am. J. Surg. Pathol. 2020, 44, 1173–1183. [Google Scholar] [CrossRef]
- Ishikawa, E.; Nakamura, M.; Shimada, K.; Tanaka, T.; Satou, A.; Kohno, K.; Sakakibara, A.; Furukawa, K.; Yamamura, T.; Miyahara, R.; et al. Prognostic impact of PD-L1 expression in primary gastric and intestinal diffuse large B-cell lymphoma. J. Gastroenterol. 2020, 55, 39–50. [Google Scholar] [CrossRef]
- Kim, S.J.; Hyeon, J.; Cho, I.; Ko, Y.H.; Kim, W.S. Comparison of efficacy of Pembrolizumab between Epstein-Barr virus-positive and -negative relapsed or refractory non-Hodgkin lymphomas. Cancer Res. Treat. 2019, 51, 611–622. [Google Scholar] [CrossRef]
- Green, M.R.; Monti, S.; Rodig, S.J.; Juszczynski, P.; Currie, T.; O’Donnell, E.; Chapuy, B.; Takeyama, K.; Neuberg, D.; Golub, T.R.; et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood 2010, 116, 3268–3277. [Google Scholar] [CrossRef]
- Chapuy, B.; Roemer, M.G.M.; Stewart, C.; Tan, Y.; Abo, R.P.; Zhang, L.; Dunford, A.J.; Meredith, D.M.; Thorner, A.R.; Jordanova, E.S.; et al. Targetable genetic features of primary testicular and primary central nervous system lymphomas. Blood 2016, 127, 869–881. [Google Scholar] [CrossRef]
- Savage, K.J. Primary mediastinal large B-cell lymphoma. Blood 2022, 140, 955–970. [Google Scholar] [CrossRef]
- Twa, D.D.W.; Chan, F.C.; Ben-Neriah, S.; Woolcock, B.W.; Mottok, A.; Tan, K.L.; Slack, G.W.; Gunawardana, J.; Lim, R.S.; McPherson, A.W.; et al. Genomic rearrangements involving programmed death ligands are recurrent in primary mediastinal large B-cell lymphoma. Blood 2014, 123, 2062–2065. [Google Scholar] [CrossRef]
- Shi, M.; Roemer, M.G.; Chapuy, B.; Liao, X.; Sun, H.B.; Pinkus, G.S.; Shipp, M.A.; Freeman, G.J.; Rodig, S.J. Expression of programmed cell death 1 ligand 2 (PD-L2) is a distinguishing feature of primary mediastinal (thymic) large B-cell lymphoma and associated with PDCD1LG2 copy gain. Am. J. Surg. Pathol. 2014, 38, 1715–1723. [Google Scholar] [CrossRef]
- Zinzani, P.L.; Ribrag, V.; Moskowitz, C.H.; Michot, J.-M.; Kuruvilla, J.; Balakumaran, A.; Zhang, Y.; Chlosta, S.; Shipp, M.A.; Armand, P. Safety and tolerability of pembrolizumab in patients with relapsed/refractory primary mediastinal large B-cell lymphoma. Blood 2017, 130, 267–270. [Google Scholar] [CrossRef]
- Manso, R.; Rodríguez-Perales, S.; Torres-Ruiz, R.; Santonja, C.; Rodríguez-Pinilla, S.-M. PD-L1 expression in peripheral T-cell lymphomas is not related to either PD-L1 gene amplification or rearrangements. Leuk. Lymphoma 2021, 62, 1648–1656. [Google Scholar] [CrossRef]
- Hue, S.S.-S.; Oon, M.L.; Wang, S.; Tan, S.Y.; Ng, S.B. Epstein-Barr virus associated T-and NK-cell lymphoproliferative diseases: An update and diagnostic approach. Pathology 2020, 52, 111–127. [Google Scholar] [CrossRef] [PubMed]
- Kwong, Y.-L.; Chan, T.S.Y.; Tan, D.; Kim, S.J.; Poon, L.-M.; Mow, B.; Khong, P.-L.; Loong, F.; Au-Yeung, R.; Iqbal, J.; et al. PD1 blockade with pembrolizumab is highly effective in relapsed or refractory NK/T-cell lymphoma failing l-asparaginase. Blood 2017, 129, 2437–2442. [Google Scholar] [CrossRef] [PubMed]
- Panjwani, P.K.; Charu, V.; DeLisser, M.; Molina-Kirsch, H.; Natkunam, Y.; Zhao, S. Programmed death1 ligands PD-L1 and PD-L 2 show distinctive and restricted patterns of expression in lymphoma subtypes. Hum. Pathol. 2018, 71, 91–99. [Google Scholar] [CrossRef]
- Shi, Y.; Wu, J.; Wang, Z.; Zhang, L.; Wang, Z.; Zhang, M.; Cen, H.; Peng, Z.; Li, Y.; Fan, L.; et al. Efficay and safety of Geptanolimab (GB226) for relapsed or refractory peripheral T-cell lymphoma: An open-label phase 2 study (Gxplore-002). J. Hematol. Oncol. 2021, 14, 12. [Google Scholar] [CrossRef]
- Jo, J.-C.; Kim, M.; Choi, Y.; Kim, H.-J.; Kim, J.E.; Chae, S.W.; Kim, H.; Cha, H.J. Expression of Programmed cell death 1 and Programmed cell death ligand 1 in extranodal NK/T-cell lymphoma, nasal type. Ann. Hematol. 2017, 96, 25–31. [Google Scholar] [CrossRef]
- Muhamad, H.; Suksawai, N.; Assanasen, T.; Polprasert, C.; Bunworasate, U.; Wudhikarn, K. Programmed cell death 1 and Programmed cell death ligands in extranodal natural killer/T cell lymphoma: Expression pattern and prognostic relevance. Acta Hematol. 2020, 143, 78–88. [Google Scholar] [CrossRef]
- He, H.X.; Gao, Y.; Fu, J.C.; Zhou, Q.H.; Wang, X.X.; Bai, B.; Li, P.F.; Huang, C.; Rong, Q.X.; Ping, L.Q.; et al. VISTA and PD-L1 synergically predict poor prognosis in patients with extranodal natural killer/T-cell lymphoma. Oncoimmunology 2021, 10, e1907059. [Google Scholar] [CrossRef]
- Kim, S.; Kwon, D.; Koh, J.; Nam, S.J.; Kim, Y.A.; Kim, T.M.; Kim, C.W.; Jeon, Y.K. Clinicopathological features of Programmed cell death 1 and Programmed cell death ligand 1 expression in the tumor cells and tumor microenvironment of angioimmunoblastic T cell lymphoma and peripheral T cell lymphoma not otherwise specified. Virchows Arch. 2020, 477, 131–142. [Google Scholar] [CrossRef]
- Morris, S.W.; Kirstein, M.N.; Valentine, M.B.; Dittmer, K.G.; Shapiro, D.N.; Saltman, D.L.; Look, A.T. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin’s lymphoma. Science 1994, 263, 1281–1284. [Google Scholar] [CrossRef]
- Crescenzo, R.; Abate, F.; Lasorsa, E.; Tabbo’, F.; Gaudiano, M.; Chiesa, N.; Di Giacomo, F.; Spaccarotella, E.; Barbarossa, L.; Ercole, E.; et al. Convergent mutations and kinase fusions lead to oncogenic STAT3 activation in anaplastic large cell lymphoma. Cancer Cell 2015, 27, 516–532. [Google Scholar] [CrossRef]
- Castellar, E.R.P.; Jaffe, E.S.; Said, J.W.; Swerdlow, S.H.; Ketterling, R.P.; Knudson, R.A.; Sidhu, J.S.; Hsi, E.D.; Karikehalli, S.; Jiang, L.; et al. ALK-negative anaplastic large cell lymphoma is a genetically heterogeneous disease with widely disparate clinical outcomes. Blood 2014, 124, 1473–1480. [Google Scholar] [CrossRef]
- Vasmatzis, G.; Johnson, S.H.; Knudson, R.A.; Ketterling, R.P.; Braggio, E.; Fonseca, R.; Viswanatha, D.S.; Law, M.E.; Kip, N.S.; Özsan, N.; et al. Genome-wide analysis reveals recurrent structural abnormalities of TP63 and other p53-related genes in peripheral T-cell lymphomas. Blood 2012, 120, 2280–2289. [Google Scholar] [CrossRef]
- Prokoph, N.; Larose, H.; Lim, M.S.; Burke, G.A.A.; Turner, S.D. Treatment options for paediatric anaplastic large cell lymphoma (ALCL): Current standard and beyond. Cancers 2018, 10, 99. [Google Scholar] [CrossRef] [PubMed]
- Fukano, R.; Mori, T.; Kobayashi, R.; Mitsui, T.; Fujita, N.; Iwasaki, F.; Suzumiya, J.; Chin, M.; Goto, H.; Takahashi, Y.; et al. Haematopoietic stem cell transplantation for relapsed or refractory anaplastic large cell lymphoma: A study of children and adolescents in Japan. Br. J. Haematol. 2015, 168, 557–563. [Google Scholar] [CrossRef] [PubMed]
- Morel, A.; Brière, J.; Lamant, L.; Loschi, M.; Haioun, C.; Delarue, R.; Tournilhac, O.; Bachy, E.; Sonet, A.; Amorim, S.; et al. Long-term outcomes of adults with first-relapsed/refractory systemic anaplastic large-cell lymphoma in the pre-brentuximab vedotin era: A LYSA/SFGM-TC study. Eur. J. Cancer 2017, 83, 146–153. [Google Scholar] [CrossRef] [PubMed]
- Mularoni, V.; Donati, B.; Tameni, A.; Manicardi, V.; Reggiani, F.; Sauta, E.; Zanelli, M.; Tigano, M.; Vitale, E.; Torricelli, F.; et al. Long non-coding RNA mitophagy and ALK-negative anaplastic lymphoma-associated transcript: A novel regular of mitophagy in T-cell lymphoma. Haematologica 2023, 108, 3333–3346. [Google Scholar] [CrossRef] [PubMed]
- Tameni, A.; Mallia, S.; Manicardi, V.; Donati, B.; Torricelli, F.; Vitale, E.; Salviato, E.; Gambarelli, G.; Muccioli, S.; Zanelli, M.; et al. HELLS regulates transcription in T-cell Lymphomas by reducing unscheduled R-loops and by facilitating RNAPII progression. Nucleic Acids Res. 2024, 239, gkae239. [Google Scholar] [CrossRef] [PubMed]
- Andorsky, D.J.; Yamada, R.E.; Said, J.; Pinkus, G.S.; Betting, D.J.; Timmerman, J.M. Programmed death ligand 1 is expressed in non-Hodgkin lymphomas and inhibits the activity of tumor-associated T cells. Clin. Cancer Res. 2011, 17, 4232–4244. [Google Scholar] [CrossRef] [PubMed]
- Marzec, M.; Zhang, Q.; Goradia, A.; Raghunath, P.N.; Liu, X.; Paessler, M.; Wang, H.Y.; Wysocka, M.; Cheng, M.; Ruggeri, B.A.; et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc. Natl. Acad. Sci. USA 2008, 105, 20852–20857. [Google Scholar] [CrossRef] [PubMed]
- Khoury, J.D.; Medeiros, L.J.; Rassidakis, G.Z.; Yared, M.A.; Tsioli, P.; Leventaki, V.; Schmitt-Graeff, A.; Herling, M.; Amin, H.M.; Lai, R. Differential expression and clinical significance of tyrosine-phosphorylated STAT3 in ALK+ and ALK− anaplastic large cell lymphoma. Clin. Cancer Res. 2003, 9, 3692–3699. [Google Scholar] [PubMed]
- Gerbe, A.; Alame, M.; Dereure, O.; Gonzalez, S.; Durand, L.; Tempier, A.; De Oliveira, L.; Tourneret, A.; Costes-Martineau, V.; Cacheux, V.; et al. Systemic, primary cutaneous and breast-implant-associated ALK-negative anaplastic large-cell lymphomas present similar biologic features despite distinct clinical behavior. Virchows Archiv. 2019, 475, 163–174. [Google Scholar] [CrossRef]
- Onaindia, A.; de Villambrosía, S.G.; Prieto-Torres, L.; Rodríguez-Pinilla, S.M.; Montes-Moreno, S.; González-Vela, C.; Piris, M.A. DUSP-22 rearranged anaplastic lymphomas are characterized by specific morphological features and a lack of cytotoxic and JAK/STAT surrogate markers. Haematologica 2019, 104, 1158.e162. [Google Scholar] [CrossRef]
- Yamamoto, R.; Nishikori, M.; Tashima, M.; Sakai, T.; Ichinohe, T.; Takaori-Kondo, A.; Ohmori, K.; Uchiyama, T. B7-H1 expression is regulated by MEK/ERK signaling pathway in anaplastic large cell lymphoma and Hodgkin lymphoma. Cancer Sci. 2009, 100, 2093–2100. [Google Scholar] [CrossRef] [PubMed]
- Iyer, S.P.; Xu, J.; Becnel, M.R.; Nair, R.; Steiner, R.; Feng, L.; Lee, H.J.; Strati, P.; Ahmed, S.; Parmar, S.; et al. A phase II study of Pembrolizumab in combination with Romidepsin demonstrates durable response in relapsed or refractory T-cell Lymphoma (TCL). Blood 2020, 136, 40–41. [Google Scholar] [CrossRef]
- Anand, K.; Ensor, J.; Pingali, S.R.; Hwu, P.; Duvic, M.; Chiang, S.; Miranda, R.; Zu, Y.; Iyer, S. T-cell lymphoma secondary to checkpoint inhibitor therapy. J. Immunother. Cancer 2020, 8, e000104. [Google Scholar] [CrossRef] [PubMed]
- Oishi, N.; Brody, G.S.; Ketterling, R.P.; Viswanatha, D.S.; He, R.; Dasari, S.; Mai, M.; Benson, H.K.; Sattler, C.A.; Boddicker, R.L.; et al. Genetic subtyping of breast implant-associated anaplastic large cell lymphoma. Blood 2018, 132, 544–547. [Google Scholar] [CrossRef] [PubMed]
- Laurent, C.; Nicolae, A.; Laurent, C.; Le Bras, F.; Haioun, C.; Fataccioli, V.; Amara, N.; Adélaïde, J.; Guille, A.; Schiano, J.M.; et al. Gene alterations in epigenetic modifiers and the JAK-STAT signaling are frequent in breast implant-associated ALCL. Blood 2020, 135, 360–370. [Google Scholar] [CrossRef] [PubMed]
- Evans, M.G.; Medeiros, L.J.; Marques-Piubelli, M.L.; Wang, H.-Y.; Ortiz-Hidalgo, C.; Pina-Oviedo, S.; Morine, A.; Clemens, M.W.; Hunt, K.K.; Iyer, S.; et al. Breast implant-associated anaplastic large cell lymphoma: Clinical follow-up and analysis of sequential pathologic specimens of untreated patients shows persistent or progressive disease. Mod. Pathol. 2021, 34, 2148–2153. [Google Scholar] [CrossRef] [PubMed]
- Quesada, A.E.; Zhang, Y.; Ptashkin, R.; Ho, C.; Horwitz, S.; Benayed, R.; Dogan, A.; Arcila, M.E. Next generation sequencing of breast implant-associated anaplastic large cell lymphomas reveals a novel STAT3-JAK2 fusion among other activating genetic alterations within the JAK-STAT pathway. Breast J. 2021, 27, 314–321. [Google Scholar] [CrossRef] [PubMed]
- Tabanelli, V.; Corsini, C.; Fiori, S.; Agostinelli, C.; Calleri, A.; Orecchioni, S.; Melle, F.; Motta, G.; Rotili, A.; Di Napoli, A.; et al. Recurrent PDL1 expression and PDL1 (CD274) copy number alterations in breast implant-associated anaplastic large cell lymphomas. Hum. Pathol. 2019, 90, 60–69. [Google Scholar] [CrossRef] [PubMed]
- Kantekure, K.; Yang, Y.; Raghunath, P.; Schaffer, A.; Woetmann, A.; Zhang, Q.; Odum, N.; Wasik, M. Expression pattern of the immunosuppressive proteins PD-1/CD279 and PD-L1/CD274 at different stages of cutaneous T-cell lymphoma/mycosis fungoides. Am. J. Dermatopathol. 2012, 34, 126–128. [Google Scholar] [CrossRef]
- Takahashi, E.; Tsuchida, T.; Baba, S.; Tsuzuki, T.; Shimauchi, T.; Tokura, Y.; Tamada, Y.; Nakamura, S. Enhanced PD-L1 expression on tumor cells in primary cutaneous large T-cell lymphoma with CD30 expression as classic Hodgkin lymphoma mimics: A report of lymph node lesions of two cases. Pathol. Int. 2020, 70, 804–811. [Google Scholar] [CrossRef]
- Takahashi, E.; Imai, H.; Tsuyuki, Y.; Taniguchi, N.; Kogure, Y.; Kataoka, K.; Tsuchida, T.; Baba, S.; Tsuzuki, T.; Shimauchi, T.; et al. Enhanced PD-L1 expression on tumor cells in primary CD30-positive cutaneous large T-cell lymphoma: A report of lymph node lesions of four cases. J. Clin. Exp. Hematop. 2023, 63, 49–57. [Google Scholar] [CrossRef] [PubMed]
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Zanelli, M.; Fragliasso, V.; Parente, P.; Bisagni, A.; Sanguedolce, F.; Zizzo, M.; Broggi, G.; Ricci, S.; Palicelli, A.; Foroni, M.; et al. Programmed Death Ligand 1 (PD-L1) Expression in Lymphomas: State of the Art. Int. J. Mol. Sci. 2024, 25, 6447. https://doi.org/10.3390/ijms25126447
Zanelli M, Fragliasso V, Parente P, Bisagni A, Sanguedolce F, Zizzo M, Broggi G, Ricci S, Palicelli A, Foroni M, et al. Programmed Death Ligand 1 (PD-L1) Expression in Lymphomas: State of the Art. International Journal of Molecular Sciences. 2024; 25(12):6447. https://doi.org/10.3390/ijms25126447
Chicago/Turabian StyleZanelli, Magda, Valentina Fragliasso, Paola Parente, Alessandra Bisagni, Francesca Sanguedolce, Maurizio Zizzo, Giuseppe Broggi, Stefano Ricci, Andrea Palicelli, Moira Foroni, and et al. 2024. "Programmed Death Ligand 1 (PD-L1) Expression in Lymphomas: State of the Art" International Journal of Molecular Sciences 25, no. 12: 6447. https://doi.org/10.3390/ijms25126447