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CC-96673 (BMS-986358), an affinity-tuned anti-CD47 and CD20 bispecific antibody with fully functional fc, selectively targets and depletes non-Hodgkin’s lymphoma

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Article: 2310248 | Received 16 Oct 2023, Accepted 22 Jan 2024, Published online: 13 Feb 2024

References

  • Chao MP, Weissman IL, Majeti R. The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications. Curr Opin Immunol. 2012;24:225–18. doi:10.1016/j.coi.2012.01.010. PMID: 22310103.
  • Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, Gordon S. Macrophage receptors and immune recognition. Annu Rev Immunol. 2005;23:901–44. doi:10.1146/annurev.immunol.23.021704.115816. PMID: 15771589.
  • Matozaki T, Murata Y, Okazawa H, Ohnishi H. Functions and molecular mechanisms of the CD47–SIRPα signalling pathway. Trends Cell Biol. 2009;19(2):72–80. doi: 10.1016/j.tcb.2008.12.001. PMID: 19144521.
  • Fujioka Y, Matozaki T, Noguchi T, Iwamatsu A, Yamao T, Takahashi N, Tsuda M, Takada T, Kasuga M. A novel membrane glycoprotein, SHPS-1, that binds the SH2-domain-containing protein tyrosine phosphatase SHP-2 in response to mitogens and cell adhesion. Mol Cell Biol. 1996;16:6887–99. doi:10.1128/MCB.16.12.6887. PMID: 8943344.
  • Russ A, Hua AB, Montfort WR, Rahman B, Riaz IB, Khalid MU, Carew JS, Nawrocki ST, Persky D, Anwer F. Blocking “don’t eat me” signal of CD47-SIRPalpha in hematological malignancies, an in-depth review. Blood Rev. 2018;32:480–89. doi:10.1016/j.blre.2018.04.005. PMID: 29709247.
  • Matlung HL, Szilagyi K, Barclay NA, van den Berg TK. The CD47-SIRPalpha signaling axis as an innate immune checkpoint in cancer. Immunol Rev. 2017;276:145–64. doi:10.1111/imr.12527. PMID: 28258703.
  • Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD Jr., van Rooijen N, Weissman IL. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell. 2009;138:286–99. doi:10.1016/j.cell.2009.05.045. PMID: 19632179.
  • Galli S, Zlobec I, Schurch C, Perren A, Ochsenbein AF, Banz Y. CD47 protein expression in acute myeloid leukemia: a tissue microarray-based analysis. Leuk Res. 2015;39:749–56. doi:10.1016/j.leukres.2015.04.007. PMID: 25943033.
  • Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS, Wang J, Contreras-Trujillo H, Martin R, Cohen JD. et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A. 2012;109:6662–67. doi:10.1073/pnas.1121623109. PMID: 22451913.
  • Yoshida K, Tsujimoto H, Matsumura K, Kinoshita M, Takahata R, Matsumoto Y, Hiraki S, Ono S, Seki S, Yamamoto J. et al. CD47 is an adverse prognostic factor and a therapeutic target in gastric cancer. Cancer Med. 2015;4:1322–33. doi:10.1002/cam4.478. PMID: 26077800.
  • Yuan J, He H, Chen C, Wu J, Rao J, Yan H. Combined high expression of CD47 and CD68 is a novel prognostic factor for breast cancer patients. Cancer Cell Int. 2019;19:238. doi:10.1186/s12935-019-0957-0. PMID: 31528120.
  • Liu J, Wang L, Zhao F, Tseng S, Narayanan C, Shura L, Willingham S, Howard M, Prohaska S, Volkmer J. et al. Pre-clinical development of a humanized anti-CD47 antibody with anti-cancer therapeutic potential. PloS ONE. 2015;10:e0137345. doi:10.1371/journal.pone.0137345. PMID: 26390038.
  • Weiskopf K, Jahchan NS, Schnorr PJ, Cristea S, Ring AM, Maute RL, Volkmer AK, Volkmer JP, Liu J, Lim JS. et al. CD47-blocking immunotherapies stimulate macrophage-mediated destruction of small-cell lung cancer. J Clin Invest. 2016;126:2610–20. doi:10.1172/JCI81603. PMID: 27294525.
  • Ring NG, Herndler-Brandstetter D, Weiskopf K, Shan L, Volkmer JP, George BM, Lietzenmayer M, McKenna KM, Naik TJ, McCarty A. et al. Anti-SIRPalpha antibody immunotherapy enhances neutrophil and macrophage antitumor activity. Proc Natl Acad Sci U S A. 2017;114:E10578–85. doi:10.1073/pnas.1710877114. PMID: 29158380.
  • Petrova PS, Viller NN, Wong M, Pang X, Lin GH, Dodge K, Chai V, Chen H, Lee V, House V. et al. TTI-621 (SIRPalphaFc): a CD47-blocking innate immune checkpoint inhibitor with broad antitumor activity and minimal erythrocyte binding. Clin Cancer Res. 2017;23:1068–79. doi:10.1158/1078-0432.CCR-16-1700. PMID: 27856600.
  • Uno S, Kinoshita Y, Azuma Y, Tsunenari T, Yoshimura Y, Iida S, Kikuchi Y, Yamada-Okabe H, Fukushima N. Antitumor activity of a monoclonal antibody against CD47 in xenograft models of human leukemia. Oncol Rep. 2007;17:1189–1194. https://www.ncbi.nlm.nih.gov/pubmed/17390064. PMID: 17390064.
  • Murata Y, Saito Y, Kotani T, Matozaki T. CD47-signal regulatory protein alpha signaling system and its application to cancer immunotherapy. Cancer Sci. 2018;109:2349–57. doi:10.1111/cas.13663. PMID: 29873856.
  • Peluso MO, Adam A, Armet CM, Zhang L, O’Connor RW, Lee BH, Lake AC, Normant E, Chappel SC, Hill JA. et al. The fully human anti-CD47 antibody SRF231 exerts dual-mechanism antitumor activity via engagement of the activating receptor CD32a. J Immunother Cancer. 2020;8(1):e000413. doi:10.1136/jitc-2019-000413. PMID: 32345627.
  • Puro RJ, Bouchlaka MN, Hiebsch RR, Capoccia BJ, Donio MJ, Manning PT, Frazier WA, Karr RW, Pereira DS. Development of AO-176, a next-generation humanized anti-CD47 antibody with novel anticancer properties and negligible red blood cell binding. Mol Cancer Ther. 2020;19:835–46. doi:10.1158/1535-7163.MCT-19-1079. PMID: 31879362.
  • Lin GHY, Chai V, Lee V, Dodge K, Truong T, Wong M, Johnson LD, Linderoth E, Pang X, Winston J. et al. TTI-621 (SIRPalphaFc), a CD47-blocking cancer immunotherapeutic, triggers phagocytosis of lymphoma cells by multiple polarized macrophage subsets. PloS ONE. 2017;12:e0187262. doi:10.1371/journal.pone.0187262. PMID: 29084248.
  • Narla RK, Modi H, Bauer D, Abbasian M, Leisten J, Piccotti JR, Kopytek S, Eckelman BP, Deveraux Q, Timmer J. et al. Modulation of CD47-SIRPalpha innate immune checkpoint axis with Fc-function detuned anti-CD47 therapeutic antibody. Cancer Immunol Immunother. 2022;71:473–89. doi:10.1007/s00262-021-03010-6. PMID: 34247273.
  • Veillette A, Tang Z. Signaling regulatory protein (Sirp)alpha-CD47 blockade joins the ranks of immune checkpoint inhibition. J Clin Oncol. 2019;37:1012–14. doi:10.1200/JCO.19.00121. PMID: 30811295.
  • Sikic BI, Lakhani N, Patnaik A, Shah SA, Chandana SR, Rasco D, Colevas AD, O’Rourke T, Narayanan S, Papadopoulos K. et al. First-in-human, first-in-class phase I trial of the anti-CD47 antibody Hu5F9-G4 in patients with advanced cancers. J Clin Oncol. 2019;37:946–53. doi:10.1200/JCO.18.02018. PMID: 30811285.
  • Ansell SM, Maris MB, Lesokhin AM, Chen RW, Flinn IW, Sawas A, Minden MD, Villa D, Percival MM, Advani AS. et al. Phase I study of the CD47 blocker TTI-621 in patients with relapsed or refractory hematologic malignancies. Clin Cancer Res. 2021;27:2190–99. doi:10.1158/1078-0432.CCR-20-3706. PMID: 33451977.
  • Zeidan AM, DeAngelo DJ, Palmer J, Seet CS, Tallman MS, Wei X, Raymon H, Sriraman P, Kopytek S, Bewersdorf JP. et al. Phase 1 study of anti-CD47 monoclonal antibody CC-90002 in patients with relapsed/refractory acute myeloid leukemia and high-risk myelodysplastic syndromes. Ann Hematol. 2022;101:557–69. doi:10.1007/s00277-021-04734-2. PMID: 34981142.
  • Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP. Role of CD47 as a marker of self on red blood cells. Sci. 2000;288(5473):2051–54. doi: 10.1126/science.288.5473.2051. PMID: 10856220.
  • Olaoba OT, Ayinde KS, Lateef OM, Akintubosun MO, Lawal KA, Adelusi TI. Is the new angel better than the old devil? Challenges and opportunities in CD47- SIRPalpha-based cancer therapy. Crit Rev Oncol Hematol. 2023;184:103939. doi:10.1016/j.critrevonc.2023.103939. PMID: 36774991.
  • Thaker YR, Rivera I, Pedros C, Singh AR, Rivero-Nava L, Zhou H, Swanson BA, Kerwin L, Zhang Y, Gray JD. et al. A novel affinity engineered anti-CD47 antibody with improved therapeutic index that preserves erythrocytes and normal immune cells. Front Oncol. 2022;12:884196. doi:10.3389/fonc.2022.884196. PMID: 35664753.
  • Ma L, Zhu M, Gai J, Li G, Chang Q, Qiao P, Cao L, Chen W, Zhang S, Wan Y. Preclinical development of a novel CD47 nanobody with less toxicity and enhanced anti-cancer therapeutic potential. J Nanobiotechnology. 2020;18:12. doi:10.1186/s12951-020-0571-2. PMID: 31931812.
  • van Bommel PE, He Y, Schepel I, Hendriks M, Wiersma VR, van Ginkel RJ, van Meerten T, Ammatuna E, Huls G, Samplonius DF. et al. CD20-selective inhibition of CD47-SIRPα “don’t eat me” signaling with a bispecific antibody-derivative enhances the anticancer activity of daratumumab, alemtuzumab and obinutuzumab. Oncoimmunology. 2018;7:e1386361. doi:10.1080/2162402X.2017.1386361. PMID: 29308308.
  • Zhang B, Li W, Fan D, Tian W, Zhou J, Ji Z, Song Y. Advances in the study of CD47-based bispecific antibody in cancer immunotherapy. Immunology. 2022;167:15–27. doi:10.1111/imm.13498. PMID: 35575882.
  • Piccione EC, Juarez S, Liu J, Tseng S, Ryan CE, Narayanan C, Wang L, Weiskopf K, Majeti R. A bispecific antibody targeting CD47 and CD20 selectively binds and eliminates dual antigen expressing lymphoma cells. MAbs. 2015;7:946–56. doi:10.1080/19420862.2015.1062192. PMID: 26083076.
  • Dheilly E, Moine V, Broyer L, Salgado-Pires S, Johnson Z, Papaioannou A, Cons L, Calloud S, Majocchi S, Nelson R. et al. Selective blockade of the Ubiquitous checkpoint receptor CD47 is enabled by dual-targeting bispecific antibodies. Mol Ther. 2017;25:523–33. doi:10.1016/j.ymthe.2016.11.006. PMID: 28153099.
  • Buatois V, Johnson Z, Salgado-Pires S, Papaioannou A, Hatterer E, Chauchet X, Richard F, Barba L, Daubeuf B, Cons L. et al. 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. 2018;17:1739–51. doi:10.1158/1535-7163.MCT-17-1095. PMID: 29743205.
  • Jiang Z, Sun H, Yu J, Tian W, Song Y. Targeting CD47 for cancer immunotherapy. J Hematol Oncol. 2021;14:180. doi:10.1186/s13045-021-01197-w. PMID: 34717705.
  • Chao MP, Alizadeh AA, Tang C, Myklebust JH, Varghese B, Gill S, Jan M, Cha AC, Chan CK, Tan BT. et al. Anti-CD47 antibody synergizes with rituximab to promote phagocytosis and eradicate non-Hodgkin lymphoma. Cell. 2010;142:699–713. doi:10.1016/j.cell.2010.07.044. PMID: 20813259.
  • Weiskopf K, Ring AM, Ho CC, Volkmer JP, Levin AM, Volkmer AK, Ozkan E, Fernhoff NB, van de Rijn M, Weissman IL. et al. Engineered SIRPalpha variants as immunotherapeutic adjuvants to anticancer antibodies. Sci. 2013;341:88–91. doi:10.1126/science.1238856. PMID: 23722425.
  • Advani R, Flinn I, Popplewell L, Forero A, Bartlett NL, Ghosh N, Kline J, Roschewski M, LaCasce A, Collins GP. et al. CD47 blockade by Hu5F9-G4 and Rituximab in non-Hodgkin’s lymphoma. N Engl J Med. 2018;379:1711–21. doi:10.1056/NEJMoa1807315. PMID: 30380386.
  • Hatterer E, Barba L, Noraz N, Daubeuf B, Aubry-Lachainaye JP, von der Weid B, Richard F, Kosco-Vilbois M, Ferlin W, Shang L. et al. Co-engaging CD47 and CD19 with a bispecific antibody abrogates B-cell receptor/CD19 association leading to impaired B-cell proliferation. MAbs. 2019;11:322–34. doi:10.1080/19420862.2018.1558698. PMID: 30569825.
  • Von Kreudenstein TS, Escobar-Carbrera E, Lario PI, D’Angelo I, Brault K, Kelly J, Durocher Y, Baardsnes J, Woods RJ, Xie MH. et al. Improving biophysical properties of a bispecific antibody scaffold to aid developability: quality by molecular design. MAbs. 2013;5:646–54. doi:10.4161/mabs.25632. PMID: 23924797.
  • Molecule Operating Environment (MOE). [Software] 2022.02 chemical computing group ULC, 910-1010 Sherbrooke St. W., Montreal, QC H3A 2R7, Canada; 2023. https://www.chemcomp.com/Research-Citing_MOE.htm.
  • Jawa V, Terry F, Gokemeijer J, Mitra-Kaushik S, Roberts BJ, Tourdot S, De Groot AS. T-Cell dependent immunogenicity of protein therapeutics pre-clinical assessment and mitigation-updated Consensus and review 2020. Front Immunol. 2020;11:1301. doi:10.3389/fimmu.2020.01301. PMID: 32695107.
  • Leclair P, Liu CC, Monajemi M, Reid GS, Sly LM, Lim CJ. CD47-ligation induced cell death in T-acute lymphoblastic leukemia. Cell Death Disease. 2018;9:544. doi:10.1038/s41419-018-0601-2. PMID: 29748606.
  • Leclair P, Lim CJ. CD47 (cluster of differentiation 47): an anti-phagocytic receptor with a multitude of signaling functions. Anim Cells Syst (Seoul). 2020;24:243–52. doi:10.1080/19768354.2020.1818618. PMID: 33224442.
  • Cao A, Yi J, Tang X, Szeto CW, Wu R, Wan B, Fang X, Li S, Wang L, Wang L. et al. CD47-blocking antibody ZL-1201 promotes tumor-associated macrophage phagocytic activity and enhances the efficacy of the therapeutic antibodies and chemotherapy. Cancer Res Commun. 2022;2:1404–17. doi:10.1158/2767-9764.CRC-22-0266. PMID: 36970051.
  • Yang J, Song Y, Li Z, Zhang M, Zhou K, Wang Z, Jing H, Yu L, Ma H, Zhao X. et al. Preliminary results from a phase I/II study of IMM0306, a CD47 and CD20 bispecific monoclonal antibody-trap, in patients with relapsed or refractory CD20-positive B-cell non-Hodgkin’s lymphoma. J Clin Oncol. 2023;41:7527–7527. doi:10.1200/JCO.2023.41.16_suppl.7527.
  • Vulto AG. Biologicals and biosimilars in hematology: the case of Rituximab. Hemasphere. 2019;3:e322. doi:10.1097/HS9.0000000000000322. PMID: 31976491.
  • Enqvist M, Jacobs B, Junlen HR, Schaffer M, Melen CM, Friberg D, Wahlin BE, Malmberg KJ. Systemic and intra-nodal activation of NK cells after rituximab monotherapy for Follicular Lymphoma. Front Immunol. 2019;10:2085. doi:10.3389/fimmu.2019.02085. PMID: 31572357.
  • Berinstein NL, Grillo-Lopez AJ, White CA, Bence-Bruckler I, Maloney D, Czuczman M, Green D, Rosenberg J, McLaughlin P, Shen D. Association of serum Rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin’s lymphoma. Ann Oncol. 1998;9:995–1001. doi:10.1023/A:1008416911099. PMID: 9818074.
  • Yu J, Li S, Chen D, Liu D, Guo H, Yang C, Zhang W, Zhang L, Zhao G, Tu X. et al. IMM0306, a fusion protein of CD20 mAb with the CD47 binding domain of SIRPalpha, exerts excellent cancer killing efficacy by activating both macrophages and NK cells via blockade of CD47-SIRPalpha interaction and fcɣR engagement by simultaneously binding to CD47 and CD20 of B cells. Leukemia. 2023;37:695–98. doi:10.1038/s41375-022-01805-9. PMID: 36575242.
  • Ryan AM, Sokolowski SA, Ng CK, Shirai N, Collinge M, Shen AC, Arrington J, Radi Z, Cummings TR, Ploch SA. et al. Comparative nonclinical assessments of the proposed biosimilar PF-05280586 and rituximab (MabThera(r)). Toxicol Pathol. 2014;42:1069–81. doi:10.1177/0192623313520351. PMID: 24604381.