Immunotherapy utilizing the combination of natural killer- and antibody dependent cellular cytotoxicity (ADCC)-mediating agents with poly (ADP-ribose) polymerase (PARP) inhibition
Open accessAbstract
BACKGROUND: Poly (ADP-ribose) polymerase inhibitors (PARPi) prevent single-stranded DNA repair. Olaparib is a PARPi approved for the treatment of BRCA mutant ovarian and breast carcinoma. Emerging clinical data suggest a benefit of combining olaparib with immunotherapy in prostate cancer patients both with and without somatic BRCA mutations. METHODS: antibody-dependent cellular cytotoxicity (ADCC)-mediating monoclonal antibodies (mAbs) cetuximab (anti-EGFR), or avelumab (anti-PD-L1), would increase tumor cell sensitivity to killing by natural killer (NK) cells independently of BRCA status or mAb target upregulation. BRCA mutant and BRCA wildtype (WT) prostate carcinoma cell lines were pretreated with olaparib and then exposed to NK cells in the presence or absence of cetuximab or avelumab. RESULTS: NK-mediated killing was significantly increased in both cell lines and was further increased using the ADCC-mediating mAbs. Pre-exposure of NK cells to recombinant IL-15/IL-15Rα further increased the lysis of olaparib treated tumor cells. In addition, olaparib treated tumor cells were killed to a significantly greater degree by engineered high-affinity NK cells (haNK). We show here for the first time that (a) olaparib significantly increased tumor cell sensitivity to NK killing and ADCC in both BRCA WT and BRCA mutant prostate carcinoma cells, independent of PD-L1 or EGFR modulation; (b) mechanistically, treatment with olaparib upregulated death receptor TRAIL-R2; and (c) olaparib significantly enhanced NK killing of additional tumor types, including breast, non-small cell lung carcinoma, and chordoma. CONCLUSIONS: These studies support the combined use of NK- and ADCC-mediating agents with correctly timed PARP inhibition.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pharmacological inhibition of PARP1 by veliparib or olaparib produces immunostimulatory effects by causing CGAS-independent upregulation of NKALs and death receptors on malignant cells, increasing their sensitivity to NK cell cytotoxicity.
“pharmacological inhibition of PARP1 by veliparib or olaparib reportedly mediates immunostimulatory effects by favoring the CGAS-independent upregulation of NKALs and death receptors on the surface of malignant cells, ultimately increasing their sensitivity to NKcell cytotoxicity (Fenerty et al., 2018; Paczulla et al., 2019)”
From Immunomodulation by targeted anticancer agents (2021) · cites this paper as Fenerty et al., 2018
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
STRING v10: protein–protein interaction networks, integrated over the tree of life
Szklarczyk, D., Franceschini, A., Wyder, S., Forslund, K., Heller, D., Huerta-Cepas, J., Simonovic, M., Roth, A., Santos, A., Tsafou, K. P., et al. (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1003 · Cited by 10,436 · see citing works
Szklarczyk, D., Morris, J. H., Cook, H., Kuhn, M., Wyder, S., Simonovic, M., Santos, A., Doncheva, N. T., Roth, A., Bork, P., et al. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw937 · Cited by 6,980 · see citing works
Death Receptors: Signaling and Modulation
Ashkenazi, A., & Dixit, V. M. (1998) · Science · doi:10.1126/science.281.5381.1305 · Cited by 5,866 · see citing works
Cartron, G., Dacheux, L., Salles, G., Solal‐Céligny, P., BARDOS, P., Colombat, P., & Watier, H. (2002) · Blood · doi:10.1182/blood.v99.3.754 · Cited by 1,902 · see citing works
Musolino, A., Naldi, N., Bortesi, B., Pezzuolo, D., Capelletti, M., Missale, G., Laccabue, D., Zerbini, A., Camisa, R., Bisagni, G., et al. (2008) · Journal of Clinical Oncology · doi:10.1200/jco.2007.14.8957 · Cited by 981 · see citing works
PARP inhibitor upregulates PD-L1 expression and enhances cancer-associated immunosuppression
Jiao, S., Xia, W., Yamaguchi, H., Wei, Y., Chen, M.-K., Hsu, J.-M., Hsu, J. L., Yu, W.-H., Du, Y., Lee, H.-H., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-3215 · Cited by 981 · see citing works
Bibeau, F., Lopez-Crapez, E., Di Fiore, F., Thezenas, S., Ychou, M., Blanchard, F., Lamy, A., Penault-Llorca, F., Frébourg, T., Michel, P., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.18.0463 · Cited by 521 · see citing works
Zhang, W., Gordon, M. A., Schultheis, A. M., Yang, D., Nagashima, F., Azuma, M., Chang, H.-M., Borucka, E., Lurje, G., Sherrod, A. E., et al. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.08.8021 · Cited by 482 · see citing works
Boyerinas, B., Jochéms, C., Fantini, M. C., Heery, C. R., Gulley, J. L., Tsang, K. Y., & Schlom, J. (2015) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-15-0059 · Cited by 468 · see citing works
Early evidence of anti-PD-1 activity in enzalutamide-resistant prostate cancer
Graff, J. N., Alumkal, J. J., Drake, C. G., THOMAS, G. V., Redmond, W. L., Farhad, M. E., Cetnar, J. P., Ey, F. S., Bergan, R. C., Slottke, R., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.10547 · Cited by 360 · see citing works
Poly (ADP-Ribose) Polymerase Inhibitors: Recent Advances and Future Development
Scott, C. L., Swisher, E. M., & Kaufmann, S. H. (2015) · Journal of Clinical Oncology · doi:10.1200/jco.2014.58.8848 · Cited by 356 · see citing works
The functional characterization of interleukin-10 receptor expression on human natural killer cells
Carson, W. E., Lindemann, M. J., Baiocchi, R. A., Linett, M. L., Tan, J., Chou, C., Narula, S. K., & Caligiuri, M. A. (1995) · Blood · doi:10.1182/blood.v85.12.3577.bloodjournal85123577 · Cited by 187 · see citing works
Jochéms, C., Hodge, J. W., Fantini, M. C., Fujii, R., Morillon, Y. M., Greiner, J. W., Padget, M. R., Tritsch, S. R., Tsang, K. Y., Campbell, K. S., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.13411 · Cited by 182 · see citing works
Self-citationThe DNA Damage Response Arouses the Immune System
Gasser, S., & Raulet, D. H. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-4603 · Cited by 178 · see citing works
Mateo, J., Moreno, V., Gupta, A., Kaye, S. B., Dean, E. J., Middleton, M. R., Friedlander, M. L., Gourley, C., Plummer, R., Rustin, G. J. S., et al. (2016) · Targeted Oncology · doi:10.1007/s11523-016-0435-8 · Cited by 128 · see citing works
Fujii, R., Friedman, E. R., Richards, J., Tsang, K. Y., Heery, C. R., Schlom, J., & Hodge, J. W. (2016) · Oncotarget · doi:10.18632/oncotarget.9256 · Cited by 110 · see citing works
Self-citationPapadimitriou, M., Mountzios, G., & PAPADIMITRIOU, C. A. (2018) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2018.04.010 · Cited by 108 · see citing works
Combination Strategies to Enhance Antitumor ADCC
Kohrt, H. E. K., Houot, R., Marabelle, A., Cho, H. J., Osman, K., Goldstein, M. J., Levy, R., & Brody, J. (2012) · Immunotherapy · doi:10.2217/imt.12.38 · Cited by 97 · see citing works
Dougherty, B. A., Lai, Z., Hodgson, D., Orr, M. C. M., Hawryluk, M. J., Sun, J. X., Yelensky, R., Spencer, S., Robertson, J. D., Ho, T. W., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.17613 · Cited by 97 · see citing works
Avelumab: combining immune checkpoint inhibition and antibody-dependent cytotoxicity
Hamilton, G., & Rath, B. (2017) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2017.1294156 · Cited by 71 · see citing works
Cetuximab Augments Cytotoxicity with Poly (ADP-Ribose) Polymerase Inhibition in Head and Neck Cancer
Nowsheen, S., Bonner, J. A., LoBuglio, A. F., Trummell, H. Q., Whitley, A. C., Dobelbower, M. C., & Yang, E. S.-H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024148 · Cited by 70 · see citing works
Targeting Plk1 to Enhance Efficacy of Olaparib in Castration-Resistant Prostate Cancer
Li, J., Wang, R., Kong, Y., Broman, M. M., Carlock, C., Chen, L., Li, Z., Farah, E., Ratliff, T. L., & Liu, X. (2017) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-16-0361 · Cited by 60 · see citing works
Plummer, R., Swaisland, H., Leunen, K., van Herpen, C. M. L., Jérusalem, G., Grève, J. D., Lolkema, M. P., Soetekouw, P. M. M. B., Mau‐Sørensen, M., Nielsen, D. L., et al. (2015) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-015-2836-2 · Cited by 53 · see citing works
Immunotherapy for Prostate Cancer: Where We Are Headed
Schepisi, G., Farolfi, A., Conteduca, V., Martignano, F., Lisi, D. D., Ravaglia, G., Rossi, L., Menna, C., Bellia, S. R., Barone, D., et al. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18122627 · Cited by 53 · see citing works
Karzai, F., Madan, R. A., Owens, H., Couvillon, A., Hankin, A., Williams, M., Bilusic, M., Cordes, L. M., Trepel, J. B., Killian, K., et al. (2018) · Journal of Clinical Oncology · doi:10.1200/jco.2018.36.6_suppl.163 · Cited by 50 · cited 3× · see citing works
“An ongoing phase 2 study of olaparib and the programmed death-ligand 1 (PD-L1) inhibitor durvalumab in metastatic castration-resistant prostate cancer (mCRPC) patients demonstrated that 8/17 patients (47%) had a decrease in prostate-specific antigen (PSA) of > 50%, with two of those patients having no known mutations…”
BackgroundInfluentialSelf-citationJochéms, C., Hodge, J. W., Fantini, M. C., Tsang, K. Y., Vandeveer, A. J., Gulley, J. L., & Schlom, J. (2017) · International Journal of Cancer · doi:10.1002/ijc.30767 · Cited by 50 · see citing works
Self-citationPreclinical evaluation of olaparib and metformin combination in BRCA1 wildtype ovarian cancer
Hijaz, M., Chhina, J., Mert, İ., Taylor, M., Dar, S. A., Al-Wahab, Z. R., Ali‐Fehmi, R., Buekers, T., Munkarah, A. R., & Rattan, R. (2016) · Gynecologic Oncology · doi:10.1016/j.ygyno.2016.06.005 · Cited by 31 · see citing works
Fujii, R., Schlom, J., & Hodge, J. W. (2017) · Journal of neurosurgery · doi:10.3171/2017.1.jns162610 · Cited by 31 · see citing works
Self-citationGarcía-Parra, J., Dalmases, A., Morancho, B., Arpí, O., Menéndez, S., Sabbaghi, M., Zazo, S., Chamizo, C., Madoz‐Gúrpide, J., Eroles, P., et al. (2014) · European Journal of Cancer · doi:10.1016/j.ejca.2014.07.004 · Cited by 29 · see citing works
Yonemori, K., Tamura, K., Kodaira, M., Fujikawa, K., Sagawa, T., Esaki, T., Shirakawa, T., Hirai, F., Yokoi, Y., Kawata, T., et al. (2016) · Cancer Chemotherapy and Pharmacology · doi:10.1007/s00280-016-3106-7 · Cited by 27 · see citing works
Zhu, Q., Wani, M. A., El-Mahdy, M. A., Wani, G., & Wani, A. A. (2000) · Molecular Carcinogenesis · doi:10.1002/1098-2744(200008)28:4 · Cited by 19 · see citing works
Olaparib and somatic BRCA mutations
George, A. J., Banerjee, S. N., & Kaye, S. B. (2017) · Oncotarget · doi:10.18632/oncotarget.18419 · Cited by 16 · see citing works
NK Cell Phenotypic and Functional Heterogeneities and Molecular Mechanisms of Cytotoxicity
Bonavida, B. (2014) · Critical Reviews™ in Oncogenesis · doi:10.1615/critrevoncog.2014010804 · Cited by 11 · see citing works
Pérez-López, R., Roda, D., Jiménez, B., Brown, J. S., Mateo, J., Carreira, S., Lopez, J. S., Banerji, U., Molife, L. R., Koh, D., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.22303 · Cited by 8 · see citing works
Abiraterone–Olaparib Combo Aids Men with mCRPC
(2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-nb2018-084 · Cited by 2 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Lampert, E. J., Zimmer, A., Padget, M., Cimino-Mathews, A., Nair, J. R., Liu, Y., Swisher, E. M., Hodge, J. W., Nixon, A. B., Nichols, E., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-0056 · Cited by 220 · see citing works
Self-citationImmunomodulation by targeted anticancer agents
Petroni, G., Buqué, A., Zitvogel, L., Kroemer, G., & Galluzzi, L. (2021) · Cancer Cell · doi:10.1016/j.ccell.2020.11.009 · Cited by 212 · see citing works
Targeting oncogene and non-oncogene addiction to inflame the tumour microenvironment
Petroni, G., Buqué, A., Coussens, L. M., & Galluzzi, L. (2022) · Nature Reviews Drug Discovery · doi:10.1038/s41573-022-00415-5 · Cited by 162 · see citing works
Leveraging NKG2D Ligands in Immuno-Oncology
Fuertes, M. B., Domaica, C. I., & Zwirner, N. W. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.713158 · Cited by 151 · see citing works
Dutta, S., Ganguly, A., Chatterjee, K., Spada, S., & Mukherjee, S. (2023) · Biology · doi:10.3390/biology12020218 · Cited by 134 · see citing works
Fabian, K. P., Wolfson, B., & Hodge, J. W. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.728018 · Cited by 125 · see citing works
Self-citationThe DNA Damage Response and Inflammation in Cancer
Klapp, V., Álvarez-Abril, B., Leuzzi, G., Kroemer, G., Ciccia, A., & Galluzzi, L. (2023) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-1220 · Cited by 110 · see citing works
NK cell-based therapeutics for lung cancer
Pockley, A. G., Vaupel, P. W., & Multhoff, G. (2019) · Expert Opinion on Biological Therapy · doi:10.1080/14712598.2020.1688298 · Cited by 86 · see citing works
Natural killer cell therapy for hematologic malignancies: successes, challenges, and the future
Lamb, M. G., Rangarajan, H. G., Tullius, B. P., & Lee, D. A. (2021) · Stem Cell Research & Therapy · doi:10.1186/s13287-021-02277-x · Cited by 79 · see citing works
Harnessing natural killer cells for the treatment of ovarian cancer
Evert, J. S. H., Bekkers, R. L. M., Ottevanger, N. P. B., Jansen, J. H., Massuger, L. F. A. G., & Dolstra, H. (2020) · Gynecologic Oncology · doi:10.1016/j.ygyno.2020.03.020 · Cited by 78 · see citing works
The Synergistic Effect of PARP Inhibitors and Immune Checkpoint Inhibitors
Wu, Z., Cui, P., Tao, H., Zhang, S., Ma, J., Liu, Z., Wang, J., Qian, Y., Chen, S., Huang, Z., et al. (2021) · Clinical Medicine Insights Oncology · doi:10.1177/1179554921996288 · Cited by 71 · see citing works
Lee, E. K., & Konstantinopoulos, P. A. (2020) · Therapeutic Advances in Medical Oncology · doi:10.1177/1758835920944116 · Cited by 71 · see citing works
Recent advances and future perspectives in the therapeutics of prostate cancer
Varaprasad, G. L., Gupta, V., Prasad, K., Kim, E., Tej, M. B., Mohanty, P., Verma, H. K., Raju, G. S. R., Bhaskar, L. V., & Huh, Y. S. (2023) · Experimental Hematology and Oncology · doi:10.1186/s40164-023-00444-9 · Cited by 69 · see citing works
Immunomodulatory Roles of PARP-1 and PARP-2: Impact on PARP-Centered Cancer Therapies
Yélamos, J., Moreno-Lama, L., Jimeno, J., & Ali, S. O. (2020) · Cancers · doi:10.3390/cancers12020392 · Cited by 69 · see citing works
Overcoming hypoxia-induced functional suppression of NK cells
Solocinski, K., Padget, M. R., Fabian, K. P., Wolfson, B., Cecchi, F., Hembrough, T., Benz, S. C., Rabizadeh, S., Soon‐Shiong, P., Schlom, J., et al. (2020) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2019-000246 · Cited by 69 · see citing works
Self-citationPARP mediated DNA damage response, genomic stability and immune responses
Zong, C., Zhu, T., He, J., Huang, R., Jia, R., & Shen, J. (2021) · International Journal of Cancer · doi:10.1002/ijc.33918 · Cited by 67 · see citing works
Natural Born Killers: NK Cells in Cancer Therapy
Franks, S. E., Wolfson, B., & Hodge, J. W. (2020) · Cancers · doi:10.3390/cancers12082131 · Cited by 65 · see citing works
Self-citationBaysal, H., Pauw, I. D., Zaryouh, H., Peeters, M., Vermorken, J. B., Lardon, F., Waele, J. D., & Wouters, A. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.737311 · Cited by 58 · see citing works
Molecular characteristics of BRCA1/2 and PALB2 mutations in pancreatic ductal adenocarcinoma
Seeber, A., Zimmer, K., Kocher, F., Puccini, A., Xiu, J., Nabhan, C., Elliott, A., Goldberg, R. M., Grothey, A. F., Shields, A. F., et al. (2020) · ESMO Open · doi:10.1136/esmoopen-2020-000942 · Cited by 52 · see citing works
PARP inhibitors in head and neck cancer: Molecular mechanisms, preclinical and clinical data
Moutafi, M. K., Economopoulou, P., Rimm, D. L., & Psyrri, A. K. (2021) · Oral Oncology · doi:10.1016/j.oraloncology.2021.105292 · Cited by 44 · see citing works
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. (2021) · Cells · doi:10.3390/cells10113166 · Cited by 41 · see citing works
Palicelli, A., Croci, S., Bisagni, A., Zanetti, E., de Biase, D., Melli, B., Sanguedolce, F., Ragazzi, M., Zanelli, M., Chaux, A., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212330 · Cited by 40 · see citing works
Heidegger, I. M., Necchi, A., Pircher, A., Tsaur, I., Marra, G., Kasivisvanathan, V., Kretschmer, A., Mathiéu, R., Ceci, F., van den Bergh, R. C. N., et al. (2020) · European Urology Oncology · doi:10.1016/j.euo.2020.10.010 · Cited by 38 · see citing works
Harnessing Natural Killer Cells in Non-Small Cell Lung Cancer
Russell, É., Conroy, M. J., & Barr, M. P. (2022) · Cells · doi:10.3390/cells11040605 · Cited by 37 · see citing works
Fabian, K. P., Kowalczyk, J. T., Reynolds, S. T., & Hodge, J. W. (2022) · Cells · doi:10.3390/cells11233826 · Cited by 36 · see citing works
Self-citationOvarian cancer treatment and natural killer cell-based immunotherapy
Fan, Z., Han, D., Fan, X., & Zhao, L. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1308143 · Cited by 34 · see citing works
Schofield, D. J., Percival‐Alwyn, J., Rytelewski, M., Hood, J., Rothstein, R. P., Wetzel, L. K., McGlinchey, K., Adjei, G., Watkins, A., Machiesky, L., et al. (2021) · mAbs · doi:10.1080/19420862.2020.1857100 · Cited by 29 · see citing works
Wolfson, B., Padget, M. R., Schlom, J., & Hodge, J. W. (2021) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2020-002258 · Cited by 28 · see citing works
Self-citationPalicelli, A., Croci, S., Bisagni, A., Zanetti, E., de Biase, D., Melli, B., Sanguedolce, F., Ragazzi, M., Zanelli, M., Chaux, A., et al. (2022) · Biomedicines · doi:10.3390/biomedicines10020236 · Cited by 25 · see citing works
Bound, N. T., Vandenberg, C. J., Kartikasari, A. E. R., Plebanski, M., & Scott, C. L. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.886170 · Cited by 25 · see citing works
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. (2021) · Cells · doi:10.3390/cells10113165 · Cited by 24 · see citing works
Immunotherapy in Advanced Prostate Cancer: Current Knowledge and Future Directions
López‐Campos, F., Gajate, P., Romero-Laorden, N., Zafra, J., Juan, M., Polo, S. H., Conde-Moreno, A. J., & Couñago, F. (2022) · Biomedicines · doi:10.3390/biomedicines10030537 · Cited by 23 · see citing works
Liu, Y., Song, H., Song, H., Feng, X., Zhou, C., & Huo, Z. (2019) · AMB Express · doi:10.1186/s13568-019-0836-z · Cited by 22 · see citing works
Ferretti, L. P., Böhi, F., Pedrioli, D. M. L., Cheng, P. F., Ferrari, E., Baumgaertner, P., Alvarado-Diaz, A., Sella, F., Cereghetti, A., Turko, P., et al. (2023) · Cancer Research · doi:10.1158/0008-5472.can-23-0485 · Cited by 20 · see citing works
Overcoming malignant cell-based mechanisms of resistance to immune checkpoint blockade antibodies
Ajina, R., Zahavi, D. J., Zhang, Y., & Weiner, L. M. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.12.005 · Cited by 18 · see citing works
Wu, Z., Tao, H., Zhang, S., Wang, X., Ma, J., Li, R., Liu, Z., Wang, J., Cui, P., Chen, S., et al. (2021) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-021-02852-4 · Cited by 16 · see citing works
Palicelli, A., Croci, S., Bisagni, A., Zanetti, E., de Biase, D., Melli, B., Sanguedolce, F., Ragazzi, M., Zanelli, M., Chaux, A., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212314 · Cited by 16 · see citing works
Piccinelli, S., Romee, R., & Shapiro, R. M. (2023) · Seminars in Hematology · doi:10.1053/j.seminhematol.2023.02.002 · Cited by 15 · see citing works
New Prospects for Molecular Targets for Chordomas
Ozair, M. Z., Shah, P. P., Mathios, D., Lim, M. K., & Moss, N. S. (2020) · Neurosurgery Clinics of North America · doi:10.1016/j.nec.2019.11.004 · Cited by 15 · see citing works
Palicelli, A., Croci, S., Bisagni, A., Zanetti, E., de Biase, D., Melli, B., Sanguedolce, F., Ragazzi, M., Zanelli, M., Chaux, A., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212297 · Cited by 14 · see citing works
Ke, B., Li, A., Fu, H., Kong, C., Liu, T., Zhu, Q., Zhang, Y., Zhang, Z., Chen, C., & Jin, C. (2021) · Acta Biochimica et Biophysica Sinica · doi:10.3724/abbs.2021011 · Cited by 12 · see citing works
Combining inhibition of immune checkpoints and PARP: rationale and perspectives in cancer treatment
Catalano, M., Iannone, L. F., Cosso, F., Generali, D., Mini, E., & Roviello, G. (2022) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2022.2158813 · Cited by 12 · see citing works
Palicelli, A., Bonacini, M., Croci, S., Bisagni, A., Zanetti, E., de Biase, D., Sanguedolce, F., Ragazzi, M., Zanelli, M., Chaux, A., et al. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11121312 · Cited by 11 · see citing works
Xu, Q., Wen, Y., Huang, T., Li, H., Liu, X., Shi, S.-N., Gong, W., Mills, G. B., Ma, D., Gao, Q., et al. (2025) · Biomarker Research · doi:10.1186/s40364-025-00814-x · Cited by 10 · see citing works
Kowalczyk, J. T., Fabian, K. P., Padget, M. R., Lopez, D. C., Hoke, A. T. K., Allen, C. T., Hermsen, M. A. J. A., London, N. R., & Hodge, J. W. (2022) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2022-005752 · Cited by 9 · see citing works
Self-citationPruitt, M. R., Fabian, K. P., Lee, J., & Hodge, J. W. (2025) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-25-0438 · Cited by 8 · see citing works
Self-citationResearch progress of DNA damage repair (DDR) and DDR inhibitors in tumor immunotherapy
Liu, Q., Zhang, C., Gao, Y., Feng, D., Deng, D., & Pan, Y. (2025) · World Journal of Surgical Oncology · doi:10.1186/s12957-025-04101-9 · Cited by 6 · see citing works
Wolfson, B., & Hodge, J. W. (2021) · ImmunoMedicine · doi:10.1002/imed.1020 · Cited by 6 · see citing works
Self-citationImpact of DNA Damage Response—Targeted Therapies on the Immune Response to Tumours
Lutfi, N., Galindo-Campos, M. A., & Yélamos, J. (2021) · Cancers · doi:10.3390/cancers13236008 · Cited by 6 · see citing works
Zhou, Z., Zhao, K., Xiao, X., Yang, W., Miao, Y., Wu, T., Kong, X., Tao, Y., Wang, W., & Dong, Z. (2026) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2026.105208 · Cited by 5 · see citing works
Moran, J., Mylod, E., Kane, L. E., Marion, C., Keenan, E., Mekhaeil, M., Lysaght, J., Dev, K. K., O'Sullivan, J. N., & Conroy, M. J. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15020360 · Cited by 4 · see citing works
Zhang, Y., Liang, L., Li, Z., Huang, Y., Jiang, M., Zou, B., & Xu, Y. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1295579 · Cited by 3 · see citing works
Oxidative Stress in the Tumor Immune Microenvironment
Wang, Y., Hu, Y., Jiang, Y., & Zhou, S. (2021) · Springer eBooks · doi:10.1007/978-981-16-0522-2_2 · Cited by 3 · see citing works
Kim, C., Cnaani, A., & Kültz, D. (2023) · Scientific Reports · doi:10.1038/s41598-023-37928-x · Cited by 3 · see citing works
Immunotherapeutic strategies and immunotherapy resistance in prostate cancer
Deb, A., Patel, N., Patel, P. A., Kilinc, E., Hachem, S., Elajami, M. K., & Mansour, E. (2023) · Elsevier eBooks · doi:10.1016/b978-0-443-16032-5.00010-5 · Cited by 3 · see citing works
Olaparib for the Treatment of Metastatic Prostate Cancer
Maurice‐Dror, C., Wyatt, A. W., & Chi, K. N. (2021) · Future Oncology · doi:10.2217/fon-2020-1245 · Cited by 3 · see citing works
Liu, Q., Zhang, C., Gao, Y., Feng, D., Deng, D., & Pan, Y. (2025) · Advanced Biology · doi:10.1002/adbi.202400720 · Cited by 1 · see citing works
Dirk, B. S., Weir, G. M., Quinton, T., Hrytsenko, О., & Stanford, M. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-82108-4 · Cited by 1 · see citing works
Current approaches to assessing the biological activity of immunocytokines in vitro
Konoplina, K. M., Kosobokova, E. N., & Kosorukov, V. S. (2022) · Russian Journal of Biotherapy · doi:10.17650/1726-9784-2022-21-3-10-22 · Cited by 1 · see citing works
Schneider, R., Gademann, G., Ochel, H.-J., Neumann, K., Jandrig, B., Hass, P., Walke, M., Schostak, M., Brunner, T. B., & Christoph, F. (2021) · Radiation Oncology · doi:10.1186/s13014-021-01859-6 · Cited by 1 · see citing works
Carving a niche for immunotherapy in ovarian cancer
Gupta, N., Lampert, E. J., & Lee, J. (2021) · Oncotarget · doi:10.18632/oncotarget.27864 · Cited by 1 · see citing works
Self-citationFenerty, K. E., Padget, M. R., Wolfson, B., Gameiro, S. R., Su, Z., Lee, J. H., Rabizadeh, S., Soon‐Shiong, P., & Hodge, J. W. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0715-9
Self-citationNatural Killer Cells in Lung Cancer
Ghobadinezhad, F., Izadi, Z., & Rezaei, N. (2024) · Interdisciplinary cancer research · doi:10.1007/16833_2024_283
Bibliometric analysis of olaparib and pancreatic cancer from 2009 to 2022: A global perspective
Feng, X., Chai, Y.-H., Jiang, K., Jiang, W., Chen, W.-C., & Pan, Y. (2024) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v16.i11.4489
Tao, H., Liu, Y., Wang, L., Wang, J., Ma, J., Zhang, G., Liu, Z., & Hu, Y. (2025) · Cancer Pathogenesis and Therapy · doi:10.1016/j.cpt.2025.08.005
Lee, C.-Y., Schlom, J., Hodge, J. W., & Fabian, K. P. (2025) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-025-04260-4
Self-citationPARP inhibitors restore NK cell function via secretory crosstalk with tumor cells in prostate cancer
Chao, Z., Li, L., Hao, X., Peng, H., Wang, Y., Zhang, C., Guo, X., Liu, P., Ma, S., Zhang, J., et al. (2026) · Journal of Clinical Investigation · doi:10.1172/jci197157
Santiago-Sánchez, G. S., Rosato, F., Fabian, K. P., Padget, M. R., Lee, J.-M., Karzai, F. H., Schlom, J., Gulley, J. L., Hamilton, D. H., Lee, J. K., et al. (2026) · Journal for ImmunoTherapy of Cancer · doi:10.1136/jitc-2025-014518
Self-citation
- Authors
- Fenerty, K. E., Padget, M., Wolfson, B., Gameiro, S. R., Su, Z., Lee, J. H., Rabizadeh, S., Soon-Shiong, P., & Hodge, J. W.
- Affiliations
- National Institutes of Health (US)
- EMD Serono, Inc. (United States) (US)
- NantOmics LLC (United States) (US)
- Corresponding author
- Hodge, James W.
- ORCID
- Venue
- Journal for ImmunoTherapy of Cancer
- Publisher
- BMJ
- Published
- 2018-11-29
- Volume
- 6
- Issue
- 1
- Pages
- 133-133
- ISSN
- 2051-1426 (ISSN-L)
- PMC
- PMC6264611
- OpenAlex
- W2903079493
- Cited by
- 68
- References
- 35
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 2 · 2023: 10 · 2022: 9 · 2021: 24 · 2020: 10 · 2019: 4
- FWCI
- 4.08
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-09-02)
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal for ImmunoTherapy of Cancer (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Cancer Institute (ZIA BC 010661)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immune Cell Function and Interaction
- Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Keywords
- olaparib, PARP inhibition, natural killer cells, antibody-dependent cellular cytotoxicity, cetuximab, avelumab, prostate cancer, BRCA mutations, DR5, combination immunotherapy, DNA repair, non-small cell lung cancer, chordoma, breast cancer
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review