Immune vulnerability of ovarian cancer stem-like cells due to low CD47 expression is protected by surrounding bulk tumor cells

References

• Allan AL, Vantyghem SA, Tuck AB, Chambers AF. Tumor dormancy and cancer stem cells: implications for the biology and treatment of breast cancer metastasis. Breast Dis. 2006;26:87–13. doi:10.3233/BD-2007-26108.
   PubMedGoogle Scholar
• Meng E, Long B, Sullivan P, McClellan S, Finan MA, Reed E, Shevde L, Rocconi RP. CD44+/CD24- ovarian cancer cells demonstrate cancer stem cell properties and correlate to survival. Clin Exp Metastasis. 2012;29:939–948. doi:10.1007/s10585-012-9482-4.
   PubMed Web of Science ®Google Scholar
• Curley MD, Therrien VA, Cummings CL, Sergent PA, Koulouris CR, Friel AM, Roberts DJ, Seiden MV, Scadden DT, Rueda BR, et al. CD133 expression defines a tumor initiating cell population in primary human ovarian cancer. Stem Cells. 2009;27:2875–2883. doi:10.1002/stem.236.
   PubMed Web of Science ®Google Scholar
• Peng S, Maihle NJ, Huang Y. Pluripotency factors Lin28 and Oct4 identify a sub-population of stem cell-like cells in ovarian cancer. Oncogene. 2010;29:2153–2159. doi:10.1038/onc.2009.500.
   PubMed Web of Science ®Google Scholar
• Ricci F, Bernasconi S, Porcu L, Erba E, Panini N, Fruscio R, Sina F, Torri V, Broggini M, Damia G. ALDH enzymatic activity and CD133 positivity and response to chemotherapy in ovarian cancer patients. Am J Cancer Res. 2013;3:221–229.
   PubMed Web of Science ®Google Scholar
• Szotek PP, Pieretti-Vanmarcke R, Masiakos PT, Dinulescu DM, Connolly D, Foster R, Dombkowski D, Preffer F, Maclaughlin DT, Donahoe PK. Ovarian cancer side population defines cells with stem cell-like characteristics and Mullerian Inhibiting Substance responsiveness. Proc Natl Acad Sci U S A. 2006;103:11154–11159. doi:10.1073/pnas.0603672103.
   PubMed Web of Science ®Google Scholar
• Liao J, Qian F, Tchabo N, Mhawech-Fauceglia P, Beck A, Qian Z, Wang X, Huss WJ, Lele SB, Morrison CD, et al. Ovarian cancer spheroid cells with stem cell-like properties contribute to tumor generation, metastasis and chemotherapy resistance through hypoxia-resistant metabolism. PLoS One. 2014;9:e84941. doi:10.1371/journal.pone.0084941.
   PubMed Web of Science ®Google Scholar
• Rizzo S, Hersey JM, Mellor P, Dai W, Santos-Silva A, Liber D, Luk L, Titley I, Carden CP, Box G, et al. Ovarian cancer stem cell-like side populations are enriched following chemotherapy and overexpress EZH2. Mol Cancer Ther. 2011;10:325–335. doi:10.1158/1535-7163.MCT-10-0788.
   PubMed Web of Science ®Google Scholar
• Steg AD, Bevis KS, Katre AA, Ziebarth A, Dobbin ZC, Alvarez RD, Zhang K, Conner M, Landen CN. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clin Cancer Res. 2012;18:869–881. doi:10.1158/1078-0432.CCR-11-2188.
   PubMed Web of Science ®Google Scholar
• Chang CL, Hsu YT, Wu CC, Lai YZ, Wang C, Yang YC, Wu TC, Hung CF. Dose-dense chemotherapy improves mechanisms of antitumor immune response. Cancer Res. 2013;73:119–127. doi:10.1158/0008-5472.CAN-12-2225.
   PubMed Web of Science ®Google Scholar
• Calcagno AM, Salcido CD, Gillet JP, Wu CP, Fostel JM, Mumau MD, Gottesman MM, Varticovski L, Ambudkar SV. Prolonged drug selection of breast cancer cells and enrichment of cancer stem cell characteristics. J Natl Cancer Inst. 2010;102:1637–1652. doi:10.1093/jnci/djq361.
   PubMedGoogle Scholar
• Morrison BJ, Steel JC, Morris JC. Sphere culture of murine lung cancer cell lines are enriched with cancer initiating cells. PLoS One. 2012;7:e49752. doi:10.1371/journal.pone.0049752.
   PubMed Web of Science ®Google Scholar
• Lopez J, Poitevin A, Mendoza-Martinez V, Perez-Plasencia C, Garcia-Carranca A. Cancer-initiating cells derived from established cervical cell lines exhibit stem-cell markers and increased radioresistance. BMC Cancer. 2012;12:48. doi:10.1186/1471-2407-12-48.
   PubMed Web of Science ®Google Scholar
• Abubaker K, Latifi A, Luwor R, Nazaretian S, Zhu H, Quinn MA, Thompson EW, Findlay JK, Ahmed N. Short-term single treatment of chemotherapy results in the enrichment of ovarian cancer stem cell-like cells leading to an increased tumor burden. Mol Cancer. 2013;12:24. doi:10.1186/1476-4598-12-24.
   PubMed Web of Science ®Google Scholar
• Grulich AE, van Leeuwen MT, Falster MO, Vajdic CM. Incidence of cancers in people with HIV/AIDS compared with immunosuppressed transplant recipients: a meta-analysis. Lancet. 2007;370:59–67. doi:10.1016/S0140-6736(07)61050-2.
   PubMed Web of Science ®Google Scholar
• Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410:1107–1111. doi:10.1038/35074122.
   PubMed Web of Science ®Google Scholar
• Frank NY, Margaryan A, Huang Y, Schatton T, Waaga-Gasser AM, Gasser M, Sayegh MH, Sadee W, Frank MH. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res. 2005;65:4320–4333. doi:10.1158/0008-5472.CAN-04-3327.
   PubMed Web of Science ®Google Scholar
• Schatton T, Frank MH. Antitumor immunity and cancer stem cells. Ann N Y Acad Sci. 2009;1176:154–169. doi:10.1111/j.1749-6632.2009.04568.x.
   PubMed Web of Science ®Google Scholar
• Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol. 2003;31:890–896. doi:10.1016/S0301-472X(03)00110-3.
   PubMed Web of Science ®Google Scholar
• Carretero R, Romero JM, Ruiz-Cabello F, Maleno I, Rodriguez F, Camacho FM, Real LM, Garrido F, Cabrera T. Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy. Immunogenetics. 2008;60:439–447. doi:10.1007/s00251-008-0303-5.
   PubMed Web of Science ®Google Scholar
• Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F, Vescovi AL. Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature. 2006;444:761–765. doi:10.1038/nature05349.
   PubMed Web of Science ®Google Scholar
• Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, et al. Molecular definition of breast tumor heterogeneity. Cancer Cell. 2007;11:259–273. doi:10.1016/j.ccr.2007.01.013.
   PubMed Web of Science ®Google Scholar
• Ghannam S, Pene J, Moquet-Torcy G, Jorgensen C, Yssel H. Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol. 2010;185:302–312. doi:10.4049/jimmunol.0902007.
   PubMed Web of Science ®Google Scholar
• Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, Galun E, Rachmilewitz J. Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood. 2005;105:2214–2219. doi:10.1182/blood-2004-07-2921.
   PubMed Web of Science ®Google Scholar
• Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, Yu XD, Mao N. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood. 2005;105:4120–4126. doi:10.1182/blood-2004-02-0586.
   PubMed Web of Science ®Google Scholar
• Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, Pennesi G. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol. 2005;35:1482–1490. doi:10.1002/eji.200425405.
   PubMed Web of Science ®Google Scholar
• Inoda S, Hirohashi Y, Torigoe T, Morita R, Takahashi A, Asanuma H, Nakatsugawa M, Nishizawa S, Tamura Y, Tsuruma T, et al. Cytotoxic T lymphocytes efficiently recognize human colon cancer stem-like cells. Am J Pathol. 2011;178:1805–1813. doi:10.1016/j.ajpath.2011.01.004.
   PubMed Web of Science ®Google Scholar
• Prince MEP, Zhou L, Moyer JS, Tao H, Lu L, Owen J, Etigen M, Zheng F, Chang AE, Xia J, et al. Evaluation of the immunogenicity of ALDH(high) human head and neck squamous cell carcinoma cancer stem cells in vitro. Oral Oncol. 2016;59:30–42. doi:10.1016/j.oraloncology.2016.05.013.
   PubMed Web of Science ®Google Scholar
• Ning N, Pan Q, Zheng F, Teitz-Tennenbaum S, Egenti M, Yet J, Li M, Ginestier C, Wicha MS, Moyer JS, et al. Cancer stem cell vaccination confers significant antitumor immunity. Cancer Res. 2012;72:1853–1864. doi:10.1158/0008-5472.CAN-11-1400.
   PubMed Web of Science ®Google Scholar
• Brown CE, Starr R, Martinez C, Aguilar B, D’Apuzzo M, Todorov I, Shih CC, Badie B, Hudecek M, Riddell SR, et al. Recognition and killing of brain tumor stem-like initiating cells by CD8+ cytolytic T cells. Cancer Res. 2009;69:8886–8893. doi:10.1158/0008-5472.CAN-09-2687.
   PubMed Web of Science ®Google Scholar
• Brown EJ, Frazier WA. Integrin-associated protein (CD47) and its ligands. Trends Cell Biol. 2001;11:130–135. doi:10.1016/S0962-8924(00)01906-1.
   PubMed Web of Science ®Google Scholar
• Gao AG, Lindberg FP, Dimitry JM, Brown EJ, Frazier WA. Thrombospondin modulates alpha v beta 3 function through integrin-associated protein. J Cell Biol. 1996;135:533–544. doi:10.1083/jcb.135.2.533.
   PubMed Web of Science ®Google Scholar
• Dunkle ET, Zaucke F, Clegg DO. Thrombospondin-4 and matrix three-dimensionality in axon outgrowth and adhesion in the developing retina. Exp Eye Res. 2007;84:707–717. doi:10.1016/j.exer.2006.12.014.
   PubMed Web of Science ®Google Scholar
• Liu Y, Buhring HJ, Zen K, Burst SL, Schnell FJ, Williams IR, Parkos CA. Signal regulatory protein (SIRPalpha), a cellular ligand for CD47, regulates neutrophil transmigration. J Biol Chem. 2002;277:10028–10036. doi:10.1074/jbc.M109720200.
   PubMed Web of Science ®Google Scholar
• Ticchioni M, Deckert M, Mary F, Bernard G, Brown EJ, Bernard A. Integrin-associated protein (CD47) is a comitogenic molecule on CD3-activated human T cells. J Immunol. 1997;158:677–684.
   PubMed Web of Science ®Google Scholar
• Chao MP, Weissman IL, Majeti R. The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications. Curr Opin Immunol. 2012;24:225–232. doi:10.1016/j.coi.2012.01.010.
   PubMed Web of Science ®Google Scholar
• Blazar BR, Lindberg FP, Ingulli E, Panoskaltsis-Mortari A, Oldenborg PA, Iizuka K, Yokoyama WM, Taylor PA. CD47 (integrin-associated protein) engagement of dendritic cell and macrophage counterreceptors is required to prevent the clearance of donor lymphohematopoietic cells. J Exp Med. 2001;194:541–549. doi:10.1084/jem.194.4.541.
   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 (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A. 2012;109:6662–6667. doi:10.1073/pnas.1121623109.
   PubMed Web of Science ®Google Scholar
• Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J Jr., Chang HY, 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;106:14016–14021. doi:10.1073/pnas.0906549106.
   PubMed Web of Science ®Google Scholar
• Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, Majeti R, Traver D, van Rooijen N, Weissman IL. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell. 2009;138:271–285. doi:10.1016/j.cell.2009.05.046.
   PubMed Web of Science ®Google Scholar
• Nonino A, Nascimento JM, Mascarenhas CC, Mazzeu JF, Pereira RW, Jacomo RH. CD47 expression is decreased in hematopoietic progenitor cells in patients with myelofibrosis. Braz J Med Biol Res. 2018;52:e7784. doi:10.1590/1414-431x20187784.
   PubMed Web of Science ®Google Scholar
• Sharrow AC, Perkins B, Collector MI, Yu W, Simons BW, Jones RJ. Characterization of aldehyde dehydrogenase 1 high ovarian cancer cells: towards targeted stem cell therapy. Gynecol Oncol. 2016;142:341–348. doi:10.1016/j.ygyno.2016.03.022.
   PubMed Web of Science ®Google Scholar
• Wang L, Mezencev R, Bowen NJ, Matyunina LV, McDonald JF. Isolation and characterization of stem-like cells from a human ovarian cancer cell line. Mol Cell Biochem. 2012;363:257–268. doi:10.1007/s11010-011-1178-6.
   PubMed Web of Science ®Google Scholar
• Paullin T, Powell C, Menzie C, Hill R, Cheng F, Martyniuk CJ, Westerheide SD. Spheroid growth in ovarian cancer alters transcriptome responses for stress pathways and epigenetic responses. PLoS One. 2017;12:e0182930. doi:10.1371/journal.pone.0182930.
   PubMed Web of Science ®Google Scholar
• Zhang H, Lu H, Xiang L, Bullen JW, Zhang C, Samanta D, Gilkes DM, He J, Semenza GL. HIF-1 regulates CD47 expression in breast cancer cells to promote evasion of phagocytosis and maintenance of cancer stem cells. Proc Natl Acad Sci USA. 2015;112:E6215–6223. doi:10.1073/pnas.1520032112.
   PubMed Web of Science ®Google Scholar
• Mathieu J, Zhang Z, Zhou W, Wang AJ, Heddleston JM, Pinna CM, Hubaud A, Stadler B, Choi M, Bar M, et al. HIF induces human embryonic stem cell markers in cancer cells. Cancer Res. 2011;71:4640–4652. doi:10.1158/0008-5472.CAN-10-3320.
   PubMed Web of Science ®Google Scholar
• Kaur S, Soto-Pantoja DR, Stein EV, Liu C, Elkahloun AG, Pendrak ML, Nicolae A, Singh SP, Nie Z, Levens D, et al. Thrombospondin-1 signaling through CD47 inhibits self-renewal by regulating c-Myc and other stem cell transcription factors. Sci Rep. 2013;3:1673. doi:10.1038/srep01673.
   PubMed Web of Science ®Google Scholar