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Prospects for combining immune checkpoint blockade with PARP inhibition
Open accessAbstract
The immunogenicity of a cancer cell is derived from accumulated somatic mutations. However, on the contrary to increased immunogenicity, anti-cancer immune response tends to be feeble. This impaired anti-cancer immunity could be attributed to multiple factors including loss of immunodominant epitopes, downregulation of major histocompatibility complex, and immunosuppressive microenvironment, as well as aberrant negative co-stimulatory signals. Immune checkpoint inhibitors block negative co-stimulatory signals such as programmed cell death-1 and cytotoxic T-lymphocyte-associated protein 4, ultimately reactivating anti-cancer immunity. Immune checkpoint inhibitors elicit potent anti-cancer effect and have been approved for multiple cancers. Nevertheless, there still are significant potential improvements for the applications of checkpoint inhibitor, especially considering frequent resistance. Recent studies demonstrated that additional PARP inhibition could alleviate resistance and enhance efficacy of immune checkpoint blockade therapy via promoting cross-presentation and modifying immune microenvironment. We proposed that PARP inhibitors could enhance the priming and tumor-killing activities of T cell, boost the whole cancer-immunity cycle, and thereby improve the response to immune checkpoint blockade. In this review, we focused the latest understanding of the effect of PARP inhibitors on anti-cancer immunity and PARP inhibitors combining immune checkpoint blockade therapy. Moreover, we summarized the preclinical and clinical evidence and discussed the feasibility of this combination therapy in future clinical practice.
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“However, some HR-deficient (e.g. BRCA1/2 mutant) cancer cells only repair DSB by nonhomologous end joining, which is a low fidelity repair pathway [219].”
From Combination strategies with PD-1/PD-L1 blockade: current advances and future directions (2022) · cites this paper as [219]
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“Normal cells preferentially repair double strand break (DSB) via homologous recombination (HR).”
From Combination strategies with PD-1/PD-L1 blockade: current advances and future directions (2022) · cites this paper as [219]
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Yap, T. A., Bardia, A., Dvorkin, M., Galsky, M. D., Beck, J. T., Wise, D. R., Karyakin, O. B., Rubovszky, G., Kislov, N. V., Rohrberg, K. S., et al. (2022) · JAMA Oncology · doi:10.1001/jamaoncol.2022.5228 · Cited by 116
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Rousset-Rouviere, S., Rochigneux, P., Chrétien, A.-S., Fattori, S., Gorvel, L., Provansal, M., Lambaudie, É., Olive, D., & Sabatier, R. (2021) · Biomedicines · doi:10.3390/biomedicines9060632 · Cited by 60
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“The hypothesis generated in this study should be evaluated further and must be proven in investigational trials.”
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Indini, A., Nigro, O., Lengyel, C. G., Ghidini, M., Petrillo, A., Lopez, S., Raspagliesi, F., Trapani, D., Khakoo, S. S., & Bogani, G. (2021) · Cancers · doi:10.3390/cancers13071663 · Cited by 46
“Available data on the prognostic and predictive significance of PD-1 and PD-L1 expression, as well as the presence of TILs, in OC, are inconsistent.”
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A Tale of Two Checkpoints: ATR Inhibition and PD-(L)1 Blockade
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“However, combination therapy is likely to yield a better response (102).”
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“PARPi-mediated catastrophic DNA damage is a favorable factor for ICI therapy, and the relationship between tumor mutation burden and efficacy of ICI has been confirmed in previous studies (52).”
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Zabransky, D. J., Yarchoan, M. M., & Jaffee, E. M. (2023) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-061421-040258 · Cited by 34
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“In ovarian cancer , PARPis have been shown to enhance the effects of immune checkpoint blockade ( 110), promoting tumor T-cell T-cell activation ( 111 ), which opens new”
Fan, Y., Ying, H., Wu, X., Chen, H., Hu, Y., Zhang, H., Wu, L., Yang, Y., Mao, B., & Zheng, L. (2020) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2020.0089 · Cited by 34
Up-Regulation of PARP1 Expression Significantly Correlated with Poor Survival in Mucosal Melanomas
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“Theoretically, PARPi could increase the clinical sensitivity of tumors to immunotherapy by increasing mutation burden and generating plenty of neoantigens [39].”
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RDGN-based predictive model for the prognosis of breast cancer
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The Emerging Role of Immunotherapy in Intrahepatic Cholangiocarcinoma
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“Poly adenosine diphosphate-ribose polymerase inhibitors (PARPi) represent a novel class of targeted cancer therapy, by exploiting synthetic lethality in tumours which harbour germline and somatic alterations in DNA damage repair (DDR) genes; whereas their combination with immune-oncology appears to be a promising trea…”
BackgroundPARP Inhibitors in Melanoma—An Expanding Therapeutic Option?
Chan, W. Y., Brown, L. J., Reid, L., & Joshua, A. M. (2021) · Cancers · doi:10.3390/cancers13184520 · Cited by 29
“Highly mutated tumours often contain one or more mutations in key components of DDR pathways, such as BRCA1/2 for HR, MSH2 for MMR and POLE for DNA replication deficiency [17,35,48].”
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“Preclinical research and early-phase clinical trials suggested that PARP inhibitors exhibit synergistic activity when administered in combination with ICIs ( 51 ).”
BackgroundAddressing Resistance to Immune Checkpoint Inhibitor Therapy: An Urgent Unmet Need
Hu‐Lieskovan, S., Malouf, G. G., Jacobs, I. A., Chou, J., Liu, L., & Johnson, M. L. (2021) · Future Oncology · doi:10.2217/fon-2020-0967 · Cited by 26
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“In addition to preventing the repair of DNA damage, PARP inhibitors play an activating role in the immunostimulatory cyclic GMP-AMP synthase–stimulator of interferon genes pathway [10].”
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“A robust anti-tumour immune response relies on a cascade of interactions from the presentation of tumour-specific antigens, activation and trafficking of cytotoxic lymphocytes and the recognition and killing of tumour cells (Dunn et al., 2004a; Dunn et al., 2004b; Li et al., 2019).”
BackgroundAdvanced Acral Melanoma Therapies: Current Status and Future Directions
Zhang, Y., Lan, S., & Wu, D. (2022) · Current Treatment Options in Oncology · doi:10.1007/s11864-022-01007-6 · Cited by 26
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“HR, an error-free form of repair with high fidelity, is crucial for cell survival [5, 21].”
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“Several PARP inhibitors, including olaparib, niraparib and talazoparib, were developed principally for patients carrying BRCA1/2 mutations [43].”
BackgroundThe landscape of circRNAs in gliomas temozolomide resistance: Insights into molecular pathways
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“Inhibiting PARP with medicines like olaparib can stimulate neoantigen formation, upregulate PD-L1, enhance type I interferon signaling, and modify TME to enhance tumor suppressive responses when combined with ICI [38].”
BackgroundThe impact of body composition on treatment in ovarian cancer: a current insight
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“This reprogramming induces the recruitment of T-cells into the tumor bed [102], thus transforming “cold tumors” into “hot tumors” through the activation of the immune response.”
BackgroundTherapeutic implications of germline vulnerabilities in DNA repair for precision oncology
Shah, S. M., Demidova, E. V., Lesh, R. W., Hall, M. J., Daly, M. B., Meyer, J. E., Edelman, M. J., & Arora, S. (2022) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2021.102337 · Cited by 17
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“PARPi–ICI combinations may work by increasing the tumour’s neoantigen load, thereby enhancing immune recognition and response [93].”
Manipulating TGF-β signaling to optimize immunotherapy for cervical cancer
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Self-citationThe Potential of PARP Inhibitors as Antitumor Drugs and the Perspective of Molecular Design
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“DDR inhibition can also facilitate cell-intrinsic immunogenicity through upregulation of PD-L1, thereby making tumor cells visible to T cells via modulation of their cell-surface phenotype (36).”
BackgroundXie, H., Wang, W., Qi, W.-C., Jin, W., & Xia, B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.661115 · Cited by 17
“Type I IFN has a substantial influence on systemic immune response and promotes the maturation, migration, and activation of immune cells, especially DCs, natural killer cells, and T cells (Figure 1) (61, 62).”
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“It was hypothesized that combining poly(ADP-ribose) polymerase (PARP) inhibitor with an immune checkpoint inhibitor may improve outcomes in both dMMR and pMMR tumors (Lee and Konstantinopoulos, 2019; Li et al., 2019; Stewart et al., 2018; Wanderley et al., 2022).”
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“Other research has reported PD-L1 expression in CRPC. Notably, studies have demonstrated the effectiveness of combining anti-PD-L1 therapy with treatments targeting myeloid-derived suppressor cells or PARP (poly ADP-ribose polymerase) inhibitors against CRPC [10].”
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“In addition, there is mounting preclinical evidence of a synergistic role with combination ICB and PARP inhibitors to improve antitumor immunity (Li et al. 2019).”
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“Additionally, PARP inhibitors have been found to enhance the priming and killing activity of T cells, thereby improving the response to ICIs [32].”
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Ginsenosides: Allies of gastrointestinal tumor immunotherapy
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Immunotherapy: Review of the Existing Evidence and Challenges in Breast Cancer
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“According to the literature, additional PARP inhibition could promote cross-presentation and modify the immune microenvironment for alleviating resistance as well as strengthening the efficacy exhibited by ICB therapy [62].”
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“By activating the STING pathway, it initiates a series of antitumor immune reactions, such as facilitating the maturation of DCs and amplifying the expression of related pro-inflammatory factors, thereby facilitating CTL activation and proliferation [44, 45].”
Ovarian cancer stem cells: Critical roles in anti-tumor immunity
Ding, J., Zhang, Y., & Che, Y. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.998220 · Cited by 11
“mutations are particularly effective in cancer cells (Li et al., 2019).”
BackgroundEREG is a risk factor for the prognosis of patients with cervical cancer
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Research progress of immune checkpoint inhibitors in ovarian cancer
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In Situ Cancer Vaccines: Redefining Immune Activation in the Tumor Microenvironment
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“…enhancing immune activity has been suggested to be partly related to PARPi-mediated disruption of DNA repair and generation of DNA damage with a subsequent increase in neoantigen expression, which theoretically creates a more sensitive and favorable signal response (high TMB) to ICIs [38–40].”
Background
Metadata
- Authors
- Li, A., Yi, M., Qin, S., Chu, Q., Luo, S., & Wu, K.
- Affiliations
- Zhengzhou University (CN)
- Tongji Hospital (CN)
- Corresponding author
- Luo, Suxia
- Wu, Kongming
- Venue
- Journal of Hematology & Oncology
- Published
- 2019-09-14
- Volume
- 12
- Issue
- 1
- Pages
- 98-98
- ISSN
- 1756-8722 (ISSN-L)
- PMC
- PMC6744711
- OpenAlex
- W2972535107
- Cited by
- 143
- References
- 130
- Citations by year
- 2026: 10 · 2025: 14 · 2024: 14 · 2023: 16 · 2022: 21 · 2021: 36 · 2020: 30 · 2019: 2
- FWCI
- 2.17
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Journal of Hematology & Oncology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (81874120, 81572608, 81672984)
- Wuhan Municipal Science and Technology Bureau (2017060201010170)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Health Sciences › Medicine › Oncology › PARP inhibition in cancer therapy
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Keywords
- immune checkpoint blockade, PARP inhibitors, combination therapy, cancer immunotherapy, tumor immune microenvironment, PD-1, CTLA-4, immunosuppression, tumor immunogenicity, T cell priming, cross-presentation, drug resistance, cancer-immunity cycle
- MeSH terms
- Poly(ADP-ribose) Polymerase Inhibitors, Antineoplastic Agents, Humans, Immunotherapy, Poly(ADP-ribose) Polymerases
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