Tiến triển của các chất ức chế điểm kiểm soát miễn dịch CD47 trong liệu pháp điều trị ung thư: một góc nhìn về độc tính huyết học

Advani R, Flinn I, Popplewell L, Forero A, Bartlett NL, Ghosh N et al (2018) CD47 blockade by Hu5F9-G4 and rituximab in non-Hodgkin’s lymphoma. N Engl J Med 379(18):1711–1721 Agoram B, Wang B, Sikic BI, Lakhani NJ, Patnaik A, Liu J et al (2018) Pharmacokinetics of Hu5F9-G4, a first-in-class anti-CD47 antibody, in patients with solid tumors and lymphomas. J Clin Oncol 36(15_suppl):2525 Ansell S, Chen RW, Flinn IW, Maris MB, O’Connor OA, Johnson LD et al (2016) A phase 1 study of TTI-621, a novel immune checkpoint inhibitor targeting CD47, in patients with relapsed or refractory hematologic malignancies. Blood 128(22):1812 Ansell SM, Flinn IW, Maris MB, O’Connor OA, Lesokhin A, Advani AS et al (2017) TTI-621 (SIRPαFc), an immune checkpoint inhibitor blocking the CD47 “do not eat” signal, induces objective responses in patients with advanced, relapsed/refractory diffuse large B-cell lymphoma (DLBCL). Blood 130(Supplement 1):4116 Ansell SM, Maris MB, Lesokhin AM, Chen RW, Flinn IW, Sawas A et al (2021) Phase I study of the CD47 blocker TTI-621 in patients with relapsed or refractory hematologic malignancies. Clin Cancer Res 27(8):2190–2199 Arias CF, Arias CF (2017) How do red blood cells know when to die? R Soc Open Sci 4(4):160850 Barazi HO, Li Z, Cashel JA, Krutzsch HC, Annis DS, Mosher DF et al (2002) Regulation of integrin function by CD47 ligands. Differential effects on alpha vbeta 3 and alpha 4beta1 integrin-mediated adhesion. J Biol Chem 277(45):42859–42866 Becker A, Eichentopf R, Sedlmeier R, Waniek A, Cynis H, Koch B et al (2016) IsoQC (QPCTL) knock-out mice suggest differential substrate conversion by glutaminyl cyclase isoenzymes. Biol Chem 397(1):45–55 Bouchlaka MN, Puro R, Capoccia B, Donio M, Hiebsch R, Carter AJ et al (2018) Development of AO-176, a next generation humanized anti-CD47 antibody with novel anti-cancer properties and negligible binding to red blood cells. Eur J Cancer 103:76 Bruce LJ, Ghosh S, King MJ, Layton DM, Mawby WJ, Stewart GW et al (2002) Absence of CD47 in protein 4.2-deficient hereditary spherocytosis in man: an interaction between the Rh complex and the band 3 complex. Blood 100(5):1878–1885 Buatois V, Johnson Z, Salgado-Pires S, Papaioannou A, Hatterer E, Chauchet X et al (2018) Preclinical development of a bispecific antibody that safely and effectively targets CD19 and CD47 for the treatment of B-Cell lymphoma and leukemia. Mol Cancer Ther 17(8):1739–1751 Chen J, Zhong MC, Guo H, Davidson D, Mishel S, Lu Y et al (2017) SLAMF7 is critical for phagocytosis of haematopoietic tumour cells via Mac-1 integrin. Nature 544(7651):493–497 Chen JY, McKenna KM, Choi TS, Duan J, Brown L, Stewart JJ et al (2018) RBC-specific CD47 pruning confers protection and underlies the transient anemia in patients treated with anti-CD47 antibody 5F9. Blood 132(Supplement 1):2327 Chen Q, Wang C, Zhang X, Chen G, Hu Q, Li H et al (2019) In situ sprayed bioresponsive immunotherapeutic gel for post-surgical cancer treatment. Nat Nanotechnol 14(1):89–97 Dheilly E, Moine V, Broyer L, Salgado-Pires S, Johnson Z, Papaioannou A et al (2017) Selective blockade of the ubiquitous checkpoint receptor CD47 Is enabled by dual-targeting bispecific antibodies. Mol Ther 25(2):523–533 Dheilly E, Majocchi S, Moine V, Didelot G, Broyer L, Calloud S et al (2018) Tumor-directed blockade of CD47 with bispecific antibodies induces adaptive antitumor immunity. Antibodies (basel) 7(1):3 Durand J, Gauttier V, Morello A, Pengam S, Vanhove B, Poirier N (2018) Abstract 1753: SIRPa inhibition monotherapy leads to dramatic change in solid tumor microenvironment and prevents metastasis development. Cancer Res 78(13 Supplement):1753 Feng M, Jiang W, Kim BYS, Zhang CC, Fu YX, Weissman IL (2019) Phagocytosis checkpoints as new targets for cancer immunotherapy. Nat Rev Cancer 19(10):568–586 Fernandes HP, Cesar CL, Barjas-Castro ML (2011) Electrical properties of the red blood cell membrane and immunohematological investigation. Rev Bras Hematol Hemoter 33(4):297–301 Freeman SA, Grinstein S (2014) Phagocytosis: receptors, signal integration, and the cytoskeleton. Immunol Rev 262(1):193–215 Gauttier V, Pengam S, Durand J, Morello A, Conchon S, Vanhove B et al (2018) Abstract 1684: Selective SIRPa blockade potentiates dendritic cell antigen cross-presentation and triggers memory T-cell antitumor responses. Cancer Res 78(13 Supplement):1684 Gauttier V, Pengam S, Durand J, Biteau K, Mary C, Morello A et al (2020) Selective SIRPalpha blockade reverses tumor T cell exclusion and overcomes cancer immunotherapy resistance. J Clin Invest 130(11):6109–6123 Ingram JR, Blomberg OS, Sockolosky JT, Ali L, Schmidt FI, Pishesha N et al (2017) Localized CD47 blockade enhances immunotherapy for murine melanoma. Proc Natl Acad Sci USA 114(38):10184–10189 Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, Majeti R et al (2009) CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 138(2):271–285 Jinnouchi F, Yamauchi T, Yurino A, Nunomura T, Nakano M, Iwamoto C et al (2020) Establishment of a human SIRPA knock-in xenograft mouse model to study human hematopoietic and cancer stem cells. Blood 135(19):1661–1672 Johnson LDS, Banerjee S, Kruglov O, Viller NN, Horwitz SM, Lesokhin A et al (2019) Targeting CD47 in Sezary syndrome with SIRPalphaFc. Blood Adv 3(7):1145–1153 Katz BZ, Herishanu Y (2014) Therapeutic targeting of CD19 in hematological malignancies: past, present, future and beyond. Leuk Lymphoma 55(5):999–1006 Kauder SE, Kuo TC, Harrabi O, Chen A, Sangalang E, Doyle L et al (2018) ALX148 blocks CD47 and enhances innate and adaptive antitumor immunity with a favorable safety profile. PLoS ONE 13(8):e0201832 Kaur S, Kuznetsova SA, Pendrak ML, Sipes JM, Romeo MJ, Li Z et al (2011) Heparan sulfate modification of the transmembrane receptor CD47 is necessary for inhibition of T cell receptor signaling by thrombospondin-1. J Biol Chem 286(17):14991–15002 Killian ML (2014) Hemagglutination assay for influenza virus. Methods Mol Biol 1161:3–9 Kwong LS, Brown MH, Barclay AN, Hatherley D (2014) Signal-regulatory protein alpha from the NOD mouse binds human CD47 with an exceptionally high affinity—implications for engraftment of human cells. Immunology 143(1):61–67 Lindberg FP, Gresham HD, Schwarz E, Brown EJ (1993) Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated in alpha v beta 3-dependent ligand binding. J Cell Biol 123(2):485–496 Liu J, Wang L, Zhao F, Tseng S, Narayanan C, Shura L et al (2015) Pre-clinical development of a humanized Anti-CD47 antibody with anti-cancer therapeutic potential. PLoS ONE 10(9):e0137345 Liu B, Guo H, Xu J, Qin T, Guo Q, Gu N et al (2018a) Elimination of tumor by CD47/PD-L1 dual-targeting fusion protein that engages innate and adaptive immune responses. Mabs 10(2):315–324 Liu X, Liu L, Ren Z, Yang K, Xu H, Luan Y et al (2018b) Dual targeting of innate and adaptive checkpoints on tumor cells limits immune evasion. Cell Rep 24(8):2101–2111 Liu Y, Chang Y, He X, Cai Y, Jiang H, Jia R et al (2020) CD47 enhances cell viability and migration ability but inhibits apoptosis in endometrial carcinoma cells via the PI3K/Akt/mTOR signaling pathway. Front Oncol 10:1525 Logtenberg MEW, Jansen JHM, Raaben M, Toebes M, Franke K, Brandsma AM et al (2019) Glutaminyl cyclase is an enzymatic modifier of the CD47- SIRPalpha axis and a target for cancer immunotherapy. Nat Med 25(4):612–619 Ma L, Zhu M, Gai J, Li G, Chang Q, Qiao P et al (2020) Preclinical development of a novel CD47 nanobody with less toxicity and enhanced anti-cancer therapeutic potential. J Nanobiotechnology 18(1):12 Mair B, Aldridge PM, Atwal RS, Philpott D, Zhang M, Masud SN et al (2019) High-throughput genome-wide phenotypic screening via immunomagnetic cell sorting. Nat Biomed Eng 3(10):796–805 Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD Jr et al (2009) CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 138(2):286–299 Matlung HL, Babes L, Zhao XW, van Houdt M, Treffers LW, van Rees DJ et al (2018) Neutrophils kill antibody-opsonized cancer cells by trogoptosis. Cell Rep 23(13):3946–59 e6 McCracken MN, Cha AC, Weissman IL (2015) Molecular pathways: activating T cells after cancer cell phagocytosis from blockade of CD47 “Don’t Eat Me” signals. Clin Cancer Res 21(16):3597–3601 Meng Z, Wang Z, Guo B, Cao W, Shen H (2019) TJC4, a differentiated anti-CD47 antibody with novel epitope and RBC sparing properties. Blood 134(Supplement_1):4063 Mohammed R, Milne A, Kayani K, Ojha U (2019) How the discovery of rituximab impacted the treatment of B-cell non-Hodgkin’s lymphomas. J Blood Med 10:71–84 Mouro-Chanteloup I, Delaunay J, Gane P, Nicolas V, Johansen M, Brown EJ et al (2003) Evidence that the red cell skeleton protein 4.2 interacts with the Rh membrane complex member CD47. Blood 101(1):338–344 Muramatsu M, Gonzalez HD, Cacciola R, Aikawa A, Yaqoob MM, Puliatti C (2014) ABO incompatible renal transplants: good or bad? World J Transplant 4(1):18–29 Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP (2000) Role of CD47 as a marker of self on red blood cells. Science 288(5473):2051–2054 Olsson M, Oldenborg PA (2008) CD47 on experimentally senescent murine RBCs inhibits phagocytosis following Fcgamma receptor-mediated but not scavenger receptor-mediated recognition by macrophages. Blood 112(10):4259–4267 Olsson M, Bruhns P, Frazier WA, Ravetch JV, Oldenborg PA (2005) Platelet homeostasis is regulated by platelet expression of CD47 under normal conditions and in passive immune thrombocytopenia. Blood 105(9):3577–3582 Oronsky B, Cabrales P, Caroen S, Guo X, Scribner C, Oronsky A et al (2021) RRx-001, a downregulator of the CD47- SIRPalpha checkpoint pathway, does not cause anemia or thrombocytopenia. Expert Opin Drug Metab Toxicol 17(4):355–357 Petrova PS, Viller NN, Wong M, Pang X, Lin GH, Dodge K et al (2017) TTI-621 (SIRPalphaFc): a CD47-blocking innate immune checkpoint inhibitor with broad antitumor activity and minimal erythrocyte binding. Clin Cancer Res 23(4):1068–1079 Pettersen RD, Hestdal K, Olafsen MK, Lie SO, Lindberg FP (1999) CD47 signals T cell death. J Immunol 162(12):7031–7040 Piccione EC, Juarez S, Liu J, Tseng S, Ryan CE, Narayanan C et al (2015) A bispecific antibody targeting CD47 and CD20 selectively binds and eliminates dual antigen expressing lymphoma cells. Mabs 7(5):946–956 Piccione EC, Juarez S, Tseng S, Liu J, Stafford M, Narayanan C et al (2016) SIRPalpha-antibody fusion proteins selectively bind and eliminate dual antigen-expressing tumor cells. Clin Cancer Res 22(20):5109–5119 Puro RJ, Bouchlaka MN, Hiebsch RR, Capoccia BJ, Donio MJ, Manning PT et al (2020) Development of AO-176, a next-generation humanized anti-CD47 antibody with novel anticancer properties and negligible red blood cell binding. Mol Cancer Ther 19(3):835–846 Ribas A, Wolchok JD (2018) Cancer immunotherapy using checkpoint blockade. Science 359(6382):1350–1355 Ring NG, Herndler-Brandstetter D, Weiskopf K, Shan L, Volkmer JP, George BM et al (2017) Anti-SIRPalpha antibody immunotherapy enhances neutrophil and macrophage antitumor activity. Proc Natl Acad Sci USA 114(49):E10578–E10585 Rizzo C, Caruso C, Vasto S (2014) Possible role of ABO system in age-related diseases and longevity: a narrative review. Immun Ageing 11:16 Sallman DA, Asch AS, Al Malki MM, Lee DJ, Donnellan WB, Marcucci G et al (2019) The first-in-class anti-CD47 antibody magrolimab (5F9) in combination with azacitidine is effective in MDS and AML patients: ongoing phase 1b results. American Society of Hematology, Washington Sallman DA, Malki MA, Asch AS, Lee DJ, Kambhampati S, Donnellan WB et al (2020) Tolerability and efficacy of the first-in-class anti-CD47 antibody magrolimab combined with azacitidine in MDS and AML patients: phase Ib results. J Clin Oncol 38(15_suppl):7507 Scheltens P, Hallikainen M, Grimmer T, Duning T, Gouw AA, Teunissen CE et al (2018) Safety, tolerability and efficacy of the glutaminyl cyclase inhibitor PQ912 in Alzheimer’s disease: results of a randomized, double-blind, placebo-controlled phase 2a study. Alzheimers Res Ther 10(1):107 Schwartz AL, Nath PR, Allgauer M, Lessey-Morillon EC, Sipes JM, Ridnour LA et al (2019) Antisense targeting of CD47 enhances human cytotoxic T-cell activity and increases survival of mice bearing B16 melanoma when combined with anti-CTLA4 and tumor irradiation. Cancer Immunol Immunother 68(11):1805–1817 Sharma P, Allison JP (2015) The future of immune checkpoint therapy. Science 348(6230):56–61 Shi R, Chai Y, Duan X, Bi X, Huang Q, Wang Q et al (2020) The identification of a CD47-blocking “hotspot” and design of a CD47/PD-L1 dual-specific antibody with limited hemagglutination. Signal Transduct Target Ther 5:16 Sikic BI, Lakhani N, Patnaik A, Shah SA, Chandana SR, Rasco D et al (2019) First-in-human, first-in-class phase I trial of the anti-CD47 antibody Hu5F9-G4 in patients with advanced cancers. J Clin Oncol 37(12):946–953 Sim J, Sockolosky JT, Sangalang E, Izquierdo S, Pedersen D, Harriman W et al (2019) Discovery of high affinity, pan-allelic, and pan-mammalian reactive antibodies against the myeloid checkpoint receptor SIRPalpha. Mabs 11(6):1036–1052 Subramanian S, Tsai R, Sen S, Dahl KN, Discher DE (2006) Membrane mobility and clustering of Integrin Associated Protein (IAP, CD47)–major differences between mouse and man and implications for signaling. Blood Cells Mol Dis 36(3):364–372 Veillette A, Chen J (2018) SIRPalpha-CD47 immune checkpoint blockade in anticancer therapy. Trends Immunol 39(3):173–184 Velliquette RW, Aeschlimann J, Kirkegaard J, Shakarian G, Lomas-Francis C, Westhoff CM (2019) Monoclonal anti-CD47 interference in red cell and platelet testing. Transfusion 59(2):730–737 Voets E, Parade M, Lutje Hulsik D, Spijkers S, Janssen W, Rens J et al (2019) Functional characterization of the selective pan-allele anti-SIRPalpha antibody ADU-1805 that blocks the SIRPalpha-CD47 innate immune checkpoint. J Immunother Cancer 7(1):340 Wang Y, Ni H, Zhou S, He K, Gao Y, Wu W et al (2020a) Tumor-selective blockade of CD47 signaling with a CD47/PD-L1 bispecific antibody for enhanced anti-tumor activity and limited toxicity. Cancer Immunol Immunother 70(2):365–376 Wang H, Sun Y, Zhou X, Chen C, Jiao L, Li W et al (2020b) CD47/SIRPalpha blocking peptide identification and synergistic effect with irradiation for cancer immunotherapy. J Immunother Cancer 8(2):e000905 Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS et al (2012) The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci USA 109(17):6662–6667 Wu Z, Weng L, Zhang T, Tian H, Fang L, Teng H et al (2019) Identification of Glutaminyl Cyclase isoenzyme isoQC as a regulator of SIRPalpha-CD47 axis. Cell Res 29(6):502–505 Yanagita T, Murata Y, Tanaka D, Motegi SI, Arai E, Daniwijaya EW et al (2017) Anti-SIRPalpha antibodies as a potential new tool for cancer immunotherapy. JCI Insight 2(1):e89140 Yang Y, Guo R, Chen Q, Liu Y, Zhang P, Zhang Z et al (2018) A novel bispecific antibody fusion protein co-targeting EGFR and CD47 with enhanced therapeutic index. Biotechnol Lett 40(5):789–795 Yu WB, Ye ZH, Chen X, Shi JJ, Lu JJ (2020) The development of small-molecule inhibitors targeting CD47. Drug Discov Today 26(2):561–568