Blocking the CD47-SIRPα axis by delivery of anti-CD47 antibody induces antitumor effects in glioma and glioma stem cells

References

• Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007;114:97–109. doi:10.1007/s00401-007-0243-4. PMID:17618441.
   PubMed Web of Science ®Google Scholar
• Brown T J, Brennan MC, Li M, Church EW, Brandmeir NJ, Rakszawski KL, Patel AS, Rizk EB, Suki D, Sawaya R et al. Association of the Extent of Resection With Survival in Glioblastoma: A Systematic Review and Meta-analysis. JAMA Oncol. 2016;2:1460–69. doi:10.1001/jamaoncol.2016.1373. PMID:27310651.
   PubMed Web of Science ®Google Scholar
• Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res. 2007;67:1030–37. doi:10.1158/0008-5472.CAN-06-2030. PMID:17283135.
   PubMed Web of Science ®Google Scholar
• Raj D, Aicher A, Heeschen C. Concise Review: Stem Cells in Pancreatic Cancer: From Concept to Translation. Stem Cells. 2015;33:2893–902. doi:10.1002/stem.2114. PMID:26202953.
   PubMed Web of Science ®Google Scholar
• O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106–10. doi:10.1038/nature05372. PMID:17122772.
   PubMed Web of Science ®Google Scholar
• Schatton T, Murphy GF, Frank NY, Yamaura K, Waaga-Gasser AM, Gasser M, Zhan Q, Jordan S, Duncan LM, Weishaupt C, et al. Identification of cells initiating human melanomas. Nature. 2008;451:345–49. doi:10.1038/nature06489. PMID:18202660.
   PubMed Web of Science ®Google Scholar
• Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63:5821–28;PMID:14522905.
   PubMed Web of Science ®Google Scholar
• Guadagno E, Borrelli G, Califano M, Cali G, Solari D, Del B D CM. Immunohistochemical expression of stem cell markers CD44 and nestin in glioblastomas: Evaluation of their prognostic significance. Pathol Res Pract. 2016;212:825–32. doi:10.1016/j.prp.2016.07.002. PMID:27450656.
   PubMed Web of Science ®Google Scholar
• Li Y, Wang H, Sun T, Chen J, Guo L, Shen H, Du Z, Zhou Y. Biological characteristics of a new human glioma cell line transformed into A2B5(+) stem cells. Mol Cancer. 2015;14:75. doi:10.1186/s12943-015-0343-z. PMID:25879429.
   PubMed Web of Science ®Google Scholar
• Brown EJ, Frazier WA. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol. 2001;11:130–35. doi:10.1016/S0962-8924(00)01906-1. PMID:11306274.
   PubMed Web of Science ®Google Scholar
• Oldenborg PA, Zheleznyak A, Fang YF, Lagenaur CF, Gresham HD, Lindberg FP. Role of CD47 as a marker of self on red blood cells. Science. 2000;288:2051–54. doi:10.1126/science.288.5473.2051. PMID:10856220.
   PubMed Web of Science ®Google Scholar
• Oldenborg PA, Gresham HD, Lindberg FP. CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J Exp Med. 2001;193:855–62;PMID:11283158;https://doi.org/10.1084/jem.193.7.855 doi:10.1084/jem.193.7.855. PMID:11283158.
   PubMed Web of Science ®Google Scholar
• Jaiswal S, Jamieson C H, Pang W W, Park C Y, Chao M P, Majeti R, Traver D, van Rooijen N, Weissman I L. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell. 2009;138:271–85. doi:10.1016/j.cell.2009.05.046. PMID:19632178.
   PubMed Web of Science ®Google Scholar
• 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 (SIRPα) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci USA. 2012;109:6662–67. doi:10.1073/pnas.1121623109. PMID:22451913.
   PubMed Web of Science ®Google Scholar
• Cioffi M, Trabulo S, Hidalgo M, Costello E, Greenhalf W, Erkan M, Kleeff J, Sainz BJ, Heeschen C. Inhibition of CD47 Effectively Targets Pancreatic Cancer Stem Cells via Dual Mechanisms. Clin Cancer Res. 2015;21:2325–37. doi:10.1158/1078-0432.CCR-14-1399. PMID:25717063.
   PubMed Web of Science ®Google Scholar
• Liu L, Zhang L, Yang L, Li H, Li R, Yu J, Yang L, Wei F, Yan C, Sun Q et al. Anti-CD47 Antibody As a Targeted Therapeutic Agent for Human Lung Cancer and Cancer Stem Cells. Front Immunol. 2017;8:404. doi:10.3389/fimmu.2017.00404. PMID:28484448.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Chao MP, Jaiswal S, Weissman-Tsukamoto R, Alizadeh AA, Gentles AJ, Volkmer J, Weiskopf K, Willingham SB, Raveh T, Park CY, et al. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci Transl Med. 2010;2:63r–94r. doi:10.1126/scitranslmed.3001375. PMID:21178137.
   PubMed Web of Science ®Google Scholar
• Chao MP, Tang C, Pachynski RK, Chin R, Majeti R, Weissman IL. Extranodal dissemination of non-Hodgkin lymphoma requires CD47 and is inhibited by anti-CD47 antibody therapy. Blood. 2011;118:4890–901. doi:10.1182/blood-2011-02-338020. PMID:21828138.
   PubMed Web of Science ®Google Scholar
• Chao MP, Alizadeh AA, Tang C, Jan M, Weissman-Tsukamoto R, Zhao F, Park CY, Weissman IL, Majeti R. Therapeutic antibody targeting of CD47 eliminates human acute lymphoblastic leukemia. Cancer Res. 2011;71:1374–84. doi:10.1158/0008-5472.CAN-10-2238. PMID:21177380.
   PubMed Web of Science ®Google Scholar
• Chan K S, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J J, Chang H Y, van de Rijn M, et al. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci U S A. 2009;106:14016–21. doi:10.1073/pnas.0906549106. PMID:19666525.
   PubMed Web of Science ®Google Scholar
• Lee TK, Cheung VC, Lu P, Lau EY, Ma S, Tang KH, Tong M, Lo J, Ng IO. Blockade of CD47-mediated cathepsin S/protease-activated receptor 2 signaling provides a therapeutic target for hepatocellular carcinoma. Hepatology. 2014;60:179–91;PMID:24523067;https://doi.org/10.1002/hep.27070 doi:10.1002/hep.27070. PMID:24523067.
   PubMed Web of Science ®Google Scholar
• Xie Q, Flavahan WA, Bao S, Rich J. The tailless root of glioma: cancer stem cells. Cell Stem Cell. 2014;15:114–16. doi:10.1016/j.stem.2014.07.004. PMID:25105574.
   PubMed Web of Science ®Google Scholar
• Gholamin S, Mitra SS, Feroze AH, Liu J, Kahn SA, Zhang M, Esparza R, Richard C, Ramaswamy V, Remke M, et al. Disrupting the CD47-SIRPalpha anti-phagocytic axis by a humanized anti-CD47 antibody is an efficacious treatment for malignant pediatric brain tumors. Sci Transl Med. 2017;9(381). doi:10.1126/scitranslmed.aaf2968. PMID:28298418
   PubMed Web of Science ®Google Scholar
• Mccracken MN, Cha AC, Weissman IL. Molecular Pathways: Activating T Cells after Cancer Cell Phagocytosis from Blockade of CD47 “Don't Eat Me” Signals. Clin Cancer Res. 2015;21:3597–601. doi:10.1158/1078-0432.CCR-14-2520. PMID:26116271.
   PubMed Web of Science ®Google Scholar
• Liu X, Pu Y, Cron K, Deng L, Kline J, Frazier WA, Xu H, Peng H, Fu YX, Xu MM. CD47 blockade triggers T cell-mediated destruction of immunogenic tumors. Nat Med. 2015;21:1209–15. doi:10.1038/nm.3931. PMID:26322579.
   PubMed Web of Science ®Google Scholar
• Huang W, Lv B, Zeng H, Shi D, Liu Y, Chen F, Li F, Liu X, Zhu R, Yu L et al. Paracrine Factors Secreted by MSCs Promote Astrocyte Survival Associated With GFAP Downregulation After Ischemic Stroke via p38 MAPK and JNK. J Cell Physiol. 2015;230:2461–75. doi:10.1002/jcp.24981. PMID:25752945.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25:402–08. doi:10.1006/meth.2001.1262. PMID:11846609.
   PubMed Web of Science ®Google Scholar
• Maes W, Rosas GG, Verbinnen B, Boon L, De Vleeschouwer S, Ceuppens JL, Van Gool SW. DC vaccination with anti-CD25 treatment leads to long-term immunity against experimental glioma. Neuro Oncol. 2009;11:529–42. doi:10.1215/15228517-2009-004. PMID:19336528.
   PubMed Web of Science ®Google Scholar