Beyond PARP1 Single-Target Inhibitors–Combined Therapy Reveals More Possibilities

PARP1 structure and function

In late 2014, the PARP inhibitor Olaparib was approved to treat ovarian cancer with BRCA mutations. Since then, research in the field of PARP has received extensive attention, especially in the development of PARP1 inhibitors.

In addition to the several drugs already approved, there are many clinical inhibitors in development. However, PARP1 inhibitors as monotherapy still have some drawbacks, such as limited efficacy, drug resistance, dose-dependent toxicity, and a limited patient population. To ameliorate these shortcomings, combination therapy has been used to design dual-target inhibitors that simultaneously inhibit PARP1 and other targets, PROTAC of PARP1, prodrugs of PARP1 inhibitors, etc. In the future, scientists may also use other strategies, such as designing covalent inhibitors and AUTACs.

Brief introduction of PARP1 inhibitors

Six PARP inhibitors have been marketed worldwide, namely Olaparib, Rucaparib, Nilapalil, Talazoparib, Fluzoparib, and Pamiparib.

The disease area that PARP1 inhibitor developers mainly focus on is tumors, and the drugs on the market are mostly for the treatment of fallopian tube cancer, peritoneal cancer, ovarian tumor, etc.

PARP1 dual-target inhibitor

As mentioned above, PARP1 inhibitors as monotherapy still have some drawbacks that confine their development. For example, Pfizer discontinued a planned Phase III clinical trial of its PARP1 inhibitor BMN-673 (NCT02127151) due to poor efficacy in advanced endometrial cancer. Combination therapy based on PARP1 inhibitors has gradually emerged in recent years. The basic principle is to use PARP1 inhibitors in combination with other anticancer drugs to inhibit the synergistic effect of two different signaling pathways, such as the combination of PARP1 inhibitors and PD-L1 inhibitors.

PARP1-targeted cancer therapy has experienced rapid development with many novel strategies, such as PARP1-based dual-target inhibitors, PROTAC PARP1 degraders, and prodrugs of PARP1 inhibitors.

Compared with PARP1 inhibitor-based HAART therapy and PARP1 inhibitor monotherapy, PARP1-based multi-target drugs demonstrate the following advantages: the lower likelihood of causing drug interactions, more predictable pharmacokinetic and pharmacodynamic properties, and improved patient compliance.

Thus, the discovery of PARP1 inhibitors with multi-targeting capabilities has gathered great attention over the past few years. The notable findings are:

  • PARP with HDAC
  • PARP with TOPO
  • PARP with BRD4
  • PARP with PI3K
  • PARP with HSP90
  • PARP with AChE
  • PARP with PD-L1

PROTACs of PARP1

Proteolysis targeting chimeras (PROTAC) is a hot research field in recent years. Compared with small molecule inhibitors, PROTAC has the advantage of targeting non-drug targets and completely degrading the whole protein. PROTACs generally consist of three parts: an E3 ligand that binds to an E3 ligase, a ligand that binds to the protein of interest, and a linker connecting the two ligands.

During the application of PARP1 inhibitors, there will be drug resistance which makes it unable to reach efficacy. So many studies on PROTACs of PARP1 have been reported up to date, such as compounds 22-29 (Figure 1). Compounds 22-27 can selectively degrade PARP1 protein and inhibit cell proliferation. Compounds 28 and 29 are dual degraders of EGFR and PARP1, which can degrade not only PARP1 but also EGFR.

Structure and activity of compounds 22-29
Figure 1. Structure and activity of compounds 22-29

Prodrug of PARP1 inhibitor

Although the above PARP1 inhibitors have high antitumor activity, many of them have poor drugability and serious side effects (e.g., hematological toxicity), which limits their further clinical use.

Prodrug strategies are proven to improve drugability and therapeutic effect and reduce toxicity.

The synthesis of macromolecular prodrug 34 of Tazopanib (TLZ) is achieved by covalently coupling a β-elimination releasable spline to a PEG40kDa vector (Figure 2). A single injection of PEG~TLZ conjugate inhibits homologous recombination of defective tumors in mouse xenografts during growth as effectively as a daily oral dose of TLZ for approximately 30 days. Zhou et al. reported the design, synthesis, photodynamic properties, and in vitro evaluation of the photoactivated prodrug 35 (Figure 2) of the PARP1 inhibitor Tarazopanib.

Overactivation of PARP can lead to NAD+ depletion, mitochondrial energy depletion, and cell death. PARP activation promotes the genome but hinders mitochondrial DNA repair, and non-selective PARP inhibitors may have the opposite effect in these cellular compartments. Clark et al. describe the synthesis and evaluation of mitochondrial-targeted PARP inhibitor 36 (XJB-veliparib). Mitochondrial targeting is performed at the major amide sites of Veliparib using flexible splints attached to iso-platoons of hemictilin S pentapeptides without breaking PARP affinity or inhibition.

In addition, there are other prodrug compounds designed and synthesized based on PARP1 inhibitors, such as compounds 37 and 38 (Figure 2).

Structure of the prodrugs of PARP1 inhibitor
Figure 2. Structure of the prodrugs of PARP1 inhibitor

Conclusion

Several PARP inhibitors have become available over the past few years, many of which are already in clinical trials. In particular, specific PARP1 inhibitors and combination strategies have received significant attention in numerous publications and clinical trials.

In addition, dual-target PARP1 inhibitors and TPD techniques are expected to enhance antitumor efficacy and overcome drug resistance. Prodrugs targeting PARP1 may also be developed to improve therapeutic efficacy or reduce the toxicity of PARP1 inhibitors. In the future, it is believed that more PARP1 modulators will be found to fight cancer.

Reference

1.Xiaopeng Peng, Wanyi Pan, Feng Jiang, Weiming Chen, Zetao Qi, Weijie Peng, Jianjun Chen, Selective PARP1 inhibitors, PARP1-based dual-target inhibitors, PROTAC PARP1 degraders, and prodrugs of PARP1 inhibitors for cancer therapy, Pharmacological Research 186 (2022) 106529.

2.S.D. Fontaine, G.W. Ashley, P.J. Houghton, R.T. Kurmasheva, M. Diolaiti, A. Ashworth, C.J. Peer, R. Nguyen, W.D. Figg Sr., D.R. Beckford-Vera, D.V. Santi, A very long-acting PARP inhibitor suppresses cancer cell growth in DNA repair-deficient tumor models, Cancer Res. 81 (2021) 1076–1086.

3.J. Li, D. Xiao, L. Liu, F. Xie, W. Li, W. Sun, X. Yang, X. Zhou, Design, synthesis, and in vitro evaluation of the photoactivatable prodrug of the PARP inhibitor Talazoparib, Molecules 25 (2020).

4.T. Krainz, A.M. Lamade, L. Du, T.S. Maskrey, M.J. Calderon, S.C. Watkins, M. W. Epperly, J.S. Greenberger, H. Bayir, P. Wipf, R.S.B. Clark, Synthesis and evaluation of a mitochondria-targeting poly(ADP-ribose) polymerase-1 inhibitor, ACS Chem. Biol. 13 (2018) 2868–2879.