Poly(ADP-ribosyl)ation polymerases: mechanism and new target of anticancer therapy

References

• Chambon P, Weill JD, Mandel P. Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun.11, 39–43 (1963).
   PubMed Web of Science ®Google Scholar
• Ame JC, Spenlehauer C, de Murcia G. The PARP superfamily. Bioessays26(8), 882–893 (2004).
   PubMed Web of Science ®Google Scholar
• Oliver AW, Ame JC, Roe SM, Good V, de Murcia G, Pearl LH. Crystal structure of the catalytic fragment of murine poly(ADP-ribose) polymerase-2. Nucleic Acids Res.32(2), 456–464 (2004).
   PubMed Web of Science ®Google Scholar
• Ame JC, Rolli V, Schreiber V et al. PARP-2, a novel mammalian DNA damage-dependent poly(ADP-ribose) polymerase. J. Appl. Biol. Chem.274(25), 17860–17868 (1999).
   Google Scholar
• Burkle A. Poly(ADP-ribose). The most elaborate metabolite of NAD+. FEBS J.272(18), 4576–4589 (2005).
   PubMed Web of Science ®Google Scholar
• de Murcia G, Schreiber V, Molinete M et al. Structure and function of poly(ADP-ribose) polymerase. Mol. Cell. Biochem.138(1–2), 15–24 (1994).
   PubMed Web of Science ®Google Scholar
• Gradwohl G, Menissier de Murcia JM, Molinete M et al. The second zinc-finger domain of poly(ADP-ribose) polymerase determines specificity for single-stranded breaks in DNA. Proc. Natl Acad. Sci. USA87(8), 2990–2994 (1990).
   PubMedGoogle Scholar
• Kim MY, Mauro S, Gevry N, Lis JT, Kraus WL. NAD+-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell119(6), 803–814 (2004).
   PubMed Web of Science ®Google Scholar
• Hassa PO, Haenni SS, Elser M, Hottiger MO. Nuclear ADP-ribosylation reactions in mammalian cells: where are we today and where are we going? Microbiol. Mol. Biol. Rev.70(3), 789–829 (2006).
   PubMed Web of Science ®Google Scholar
• Rongvaux A, Andris F, Van Gool F, Leo O. Reconstructing eukaryotic NAD metabolism. Bioessays25(7), 683–690 (2003).
   PubMed Web of Science ®Google Scholar
• Ziegler M. New functions of a long-known molecule. Emerging roles of NAD in cellular signaling. Eur. J. Biochem.267(6), 1550–1564 (2000).
   PubMedGoogle Scholar
• Skidmore CJ, Davies MI, Goodwin PM et al. The involvement of poly(ADP-ribose) polymerase in the degradation of NAD caused by gamma-radiation and N-methyl-N-nitrosourea. Eur. J. Biochem.101(1), 135–142 (1979).
   PubMedGoogle Scholar
• Kreimeyer A, Wielckens K, Adamietz P, Hilz H. DNA repair-associated ADP-ribosylation in vivo. Modification of histone H1 differs from that of the principal acceptor proteins. J. Appl. Biol. Chem.259(2), 890–896 (1984).
   Google Scholar
• Alvarez-Gonzalez R, Althaus FR. Poly(ADP-ribose) catabolism in mammalian cells exposed to DNA-damaging agents. Mutat. Res.218(2), 67–74 (1989).
   PubMed Web of Science ®Google Scholar
• Keith G, Desgres J, de Murcia G. Use of two-dimensional thin-layer chromatography for the components study of poly(adenosine diphosphate ribose). Anal. Biochem.191(2), 309–313 (1990).
   Google Scholar
• Ferro AM, Olivera BM. Poly(ADP-ribosylation) in vitro. Reaction parameters and enzyme mechanism. J. Appl. Biol. Chem.257(13), 7808–7813 (1982).
   Google Scholar
• Mortusewicz O, Ame JC, Schreiber V, Leonhardt H. Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res.35(22), 7665–7675 (2007).
   PubMed Web of Science ®Google Scholar
• Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G. XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol. Cell. Biol.18(6), 3563–3571 (1998).
   PubMed Web of Science ®Google Scholar
• Caldecott KW. XRCC1 and DNA strand break repair. DNA Repair (Amst.)2(9), 955–969 (2003).
   PubMed Web of Science ®Google Scholar
• Mackey ZB, Niedergang C, Murcia JM et al. DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly(ADP-ribose) polymerase. Identification of two functionally distinct DNA binding regions within DNA ligase III. J. Appl. Biol. Chem.274(31), 21679–21687 (1999).
   Google Scholar
• Bryant HE, Petermann E, Schultz N et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J.28(17), 2601–2615 (2009).
   PubMed Web of Science ®Google Scholar
• Audebert M, Salles B, Calsou P. Effect of double-strand break DNA sequence on the PARP-1 NHEJ pathway. Biochem. Biophys. Res. Commun.369(3), 982–988 (2008).
   PubMed Web of Science ®Google Scholar
• Saberi A, Hochegger H, Szuts D et al. RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination-mediated repair. Mol. Cell. Biol.27(7), 2562–2571 (2007).
   PubMed Web of Science ®Google Scholar
• Wang M, Wu W, Wu W et al. PARP-1 and Ku compete for repair of DNA double-strand breaks by distinct NHEJ pathways. Nucleic Acids Res.34(21), 6170–6182 (2006).
   PubMed Web of Science ®Google Scholar
• Cohen-Armon M. PARP-1 activation in the ERK signaling pathway. Trends Pharmacol. Sci.28(11), 556–560 (2007).
   PubMed Web of Science ®Google Scholar
• Cohen-Armon M, Visochek L, Rozensal D et al. DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol. Cell25(2), 297–308 (2007).
   PubMed Web of Science ®Google Scholar
• Carbone M, Rossi MN, Cavaldesi M, Notari A, Amati P, Maione R. Poly(ADP-ribosyl)ation is implicated in the G0–G1 transition of resting cells. Oncogene27(47), 6083–6092 (2008).
   PubMed Web of Science ®Google Scholar
• Berger F, Ramirez-Hernandez MH, Ziegler M. The new life of a centenarian: signalling functions of NAD(P). Trends Biochem. Sci.29(3), 111–118 (2004).
   PubMed Web of Science ®Google Scholar
• Yu SW, Wang H, Poitras MF et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science297(5579), 259–263 (2002).
   PubMed Web of Science ®Google Scholar
• Tentori L, Portarena I, Graziani G. Potential clinical applications of poly(ADP-ribose) polymerase (PARP) inhibitors. Pharmacol. Res.45(2), 73–85 (2002).
   PubMed Web of Science ®Google Scholar
• Fisher AE, Hochegger H, Takeda S, Caldecott KW. Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol. Cell. Biol.27(15), 5597–5605 (2007).
   PubMed Web of Science ®Google Scholar
• Buelow B, Uzunparmak B, Paddock M, Scharenberg AM. Structure/function analysis of PARP-1 in oxidative and nitrosative stress-induced monomeric ADPR formation. PLoS ONE4(7), E6339 (2009).
   Google Scholar
• Shall S. Proceedings: experimental manipulation of the specific activity of poly(ADP-ribose) polymerase. J. Biochem.77(1), p2 (1975).
   Google Scholar
• Purnell MR, Whish WJ. Novel inhibitors of poly(ADP-ribose) synthetase. Biochem. J.185(3), 775–777 (1980).
   PubMed Web of Science ®Google Scholar
• Griffin RJ, Curtin NJ, Newell DR, Golding BT, Durkacz BW, Calvert AH. The role of inhibitors of poly(ADP-ribose) polymerase as resistance-modifying agents in cancer therapy. Biochimie77(6), 408–422 (1995).
   PubMed Web of Science ®Google Scholar
• Southan GJ, Szabo C. Poly(ADP-ribose) polymerase inhibitors. Curr. Med. Chem.10(4), 321–340 (2003).
   PubMed Web of Science ®Google Scholar
• Cepeda V, Fuertes MA, Castilla J et al. Poly(ADP-ribose) polymerase-1 (PARP-1) inhibitors in cancer chemotherapy. Recent Pat. Anticancer Drug Discov.1(1), 39–53 (2006).
   PubMedGoogle Scholar
• Ruf A, de Murcia G, Schulz GE. Inhibitor and NAD+ binding to poly(ADP-ribose) polymerase as derived from crystal structures and homology modeling. Biochemistry37(11), 3893–3900 (1998).
   PubMed Web of Science ®Google Scholar
• Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem.73, 39–85 (2004).
   PubMed Web of Science ®Google Scholar
• Bryant HE, Schultz N, Thomas HD et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature434(7035), 913–917 (2005).
   PubMed Web of Science ®Google Scholar
• Huang SM, Mishina YM, Liu S et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature461(7264), 614–620 (2009).
   PubMed Web of Science ®Google Scholar
• Fearon ER. PARsing the phrase “all in for Axin”– Wnt pathway targets in cancer. Cancer Cell16(5), 366–368 (2009).
   PubMed Web of Science ®Google Scholar
• MacDonald BT, Tamai K, He X. Wnt/β-catenin signaling: components, mechanisms, and diseases. Dev. Cell17(1), 9–26 (2009).
   PubMed Web of Science ®Google Scholar
• D’Amours D, Desnoyers S, D’Silva I, Poirier GG. Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J.342(Pt 2), 249–268 (1999).
   PubMed Web of Science ®Google Scholar
• Lindahl T, Satoh MS, Poirier GG, Klungland A. Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci.20(10), 405–411 (1995).
   PubMed Web of Science ®Google Scholar
• de Murcia JM, Niedergang C, Trucco C et al. Requirement of poly(ADP-ribose) polymerase in recovery from DNA damage in mice and in cells. Proc. Natl Acad. Sci. USA94(14), 7303–7307 (1997).
   PubMed Web of Science ®Google Scholar
• Wang ZQ, Stingl L, Morrison C et al. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev.11(18), 2347–2358 (1997).
   PubMed Web of Science ®Google Scholar
• Saleh-Gohari N, Bryant HE, Schultz N, Parker KM, Cassel TN, Helleday T. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol.25(16), 7158–7169 (2005).
   PubMed Web of Science ®Google Scholar
• Veuger SJ, Hunter JE, Durkacz BW. Ionizing radiation-induced NF-κB activation requires PARP-1 function to confer radioresistance. Oncogene28(6), 832–842 (2009).
   PubMed Web of Science ®Google Scholar
• Munoz-Gamez JA, Martin-Oliva D, Aguilar-Quesada R et al. PARP inhibition sensitizes p53-deficient breast cancer cells to doxorubicin-induced apoptosis. Biochem. J.386(Pt 1), 119–125 (2005).
   PubMed Web of Science ®Google Scholar
• Delaney CA, Wang LZ, Kyle S et al. Potentiation of temozolomide and topotecan growth inhibition and cytotoxicity by novel poly(adenosine diphosphoribose) polymerase inhibitors in a panel of human tumor cell lines. Clin. Cancer Res.6(7), 2860–2867 (2000).
   PubMed Web of Science ®Google Scholar
• Bowman KJ, White A, Golding BT, Griffin RJ, Curtin NJ. Potentiation of anti-cancer agent cytotoxicity by the potent poly(ADP-ribose) polymerase inhibitors NU1025 and NU1064. Br. J. Cancer78(10), 1269–1277 (1998).
   PubMed Web of Science ®Google Scholar
• Bowman KJ, Newell DR, Calvert AH, Curtin NJ. Differential effects of the poly (ADP-ribose) polymerase (PARP) inhibitor NU1025 on topoisomerase I and II inhibitor cytotoxicity in L1210 cells in vitro. Br. J. Cancer84(1), 106–112 (2001).
   PubMedGoogle Scholar
• Farmer H, McCabe N, Lord CJ et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature434(7035), 917–921 (2005).
   PubMed Web of Science ®Google Scholar
• Taylor J, Lymboura M, Pace PE et al. An important role for BRCA1 in breast cancer progression is indicated by its loss in a large proportion of non-familial breast cancers. Int. J. Cancer79(4), 334–342 (1998).
   PubMed Web of Science ®Google Scholar
• Wooster R, Weber BL. Breast and ovarian cancer. N. Engl. J. Med.348(23), 2339–2347 (2003).
   PubMed Web of Science ®Google Scholar
• Ford D, Easton DF, Peto J. Estimates of the gene frequency of BRCA1 and its contribution to breast and ovarian cancer incidence. Am. J. Hum. Genet.57(6), 1457–1462 (1995).
   PubMed Web of Science ®Google Scholar
• Easton DF, Narod SA, Ford D, Steel M. The genetic epidemiology of BRCA1. Breast Cancer Linkage Consortium. Lancet344(8924), 761 (1994).
   PubMed Web of Science ®Google Scholar
• Sorlie T, Perou CM, Tibshirani R et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA98(19), 10869–10874 (2001).
   PubMed Web of Science ®Google Scholar
• Perou CM, Sorlie T, Eisen MB et al. Molecular portraits of human breast tumours. Nature406(6797), 747–752 (2000).
   PubMed Web of Science ®Google Scholar
• Turner NC, Reis-Filho JS. Basal-like breast cancer and the BRCA1 phenotype. Oncogene25(43), 5846–5853 (2006).
   PubMed Web of Science ®Google Scholar
• Nielsen TO, Hsu FD, Jensen K et al. Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin. Cancer Res.10(16), 5367–5374 (2004).
   PubMed Web of Science ®Google Scholar
• Foulkes WD, Stefansson IM, Chappuis PO et al. Germline BRCA1 mutations and a basal epithelial phenotype in breast cancer. J. Natl Cancer Inst.95(19), 1482–1485 (2003).
   PubMed Web of Science ®Google Scholar
• Thompson ME, Jensen RA, Obermiller PS, Page DL, Holt JT. Decreased expression of BRCA1 accelerates growth and is often present during sporadic breast cancer progression. Nat. Genet.9(4), 444–450 (1995).
   PubMed Web of Science ®Google Scholar
• Turner NC, Reis-Filho JS, Russell AM et al. BRCA1 dysfunction in sporadic basal-like breast cancer. Oncogene26(14), 2126–2132 (2007).
   PubMed Web of Science ®Google Scholar
• Marroni F, Aretini P, D’Andrea E et al. Penetrances of breast and ovarian cancer in a large series of families tested for BRCA1/2 mutations. Eur. J. Hum. Genet.12(11), 899–906 (2004).
   Google Scholar
• Berchuck A, Heron KA, Carney ME et al. Frequency of germline and somatic BRCA1 mutations in ovarian cancer. Clin. Cancer Res.4(10), 2433–2437 (1998).
   Google Scholar
• Wang C, Horiuchi A, Imai T et al. Expression of BRCA1 protein in benign, borderline, and malignant epithelial ovarian neoplasms and its relationship to methylation and allelic loss of the BRCA1 gene. J. Pathol.202(2), 215–223 (2004).
   PubMedGoogle Scholar
• Zheng W, Luo F, Lu JJ et al. Reduction of BRCA1 expression in sporadic ovarian cancer. Gynecol. Oncol.76(3), 294–300 (2000).
   Google Scholar
• Wilson CA, Ramos L, Villasenor MR et al. Localization of human BRCA1 and its loss in high-grade, non-inherited breast carcinomas. Nat. Genet.21(2), 236–240 (1999).
   PubMed Web of Science ®Google Scholar
• Thrall M, Gallion HH, Kryscio R, Kapali M, Armstrong DK, DeLoia JA. BRCA1 expression in a large series of sporadic ovarian carcinomas: a Gynecologic Oncology Group study. Int. J. Gynecol. Cancer16(Suppl. 1), 166–171 (2006).
   PubMedGoogle Scholar
• Risch HA, McLaughlin JR, Cole DE et al. Population BRCA1 and BRCA2 mutation frequencies and cancer penetrances: a kin-cohort study in Ontario, Canada. J. Natl Cancer Inst.98(23), 1694–1706 (2006).
   PubMed Web of Science ®Google Scholar
• Willers H, Taghian AG, Luo CM, Treszezamsky A, Sgroi DC, Powell SN. Utility of DNA repair protein foci for the detection of putative BRCA1 pathway defects in breast cancer biopsies. Mol. Cancer Res.7(8), 1304–1309 (2009).
   PubMed Web of Science ®Google Scholar
• Salmena L, Carracedo A, Pandolfi PP. Tenets of PTEN tumor suppression. Cell133(3), 403–414 (2008).
   PubMed Web of Science ®Google Scholar
• Mendes-Pereira AM, Martin SA, Brough R et al. Synthetic lethal targeting of PTEN mutant cells with PARP inhibitors. EMBO Mol. Med.1(6–7), 315–322 (2009).
   PubMed Web of Science ®Google Scholar
• Knight ZA, Shokat KM. Chemically targeting the PI3K family. Biochem. Soc. Trans.35(Pt 2), 245–249 (2007).
   PubMed Web of Science ®Google Scholar
• Bryant HE, Helleday T. Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res.34(6), 1685–1691 (2006).
   PubMed Web of Science ®Google Scholar
• McCabe N, Turner NC, Lord CJ et al. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res.66(16), 8109–8115 (2006).
   PubMed Web of Science ®Google Scholar
• Stilgenbauer S, Schaffner C, Litterst A et al. Biallelic mutations in the ATM gene in T-prolymphocytic leukemia. Nat. Med.3(10), 1155–1159 (1997).
   PubMed Web of Science ®Google Scholar
• Rosenwald A, Chuang EY, Davis RE et al. Fludarabine treatment of patients with chronic lymphocytic leukemia induces a p53-dependent gene expression response. Blood104(5), 1428–1434 (2004).
   PubMed Web of Science ®Google Scholar
• Stankovic T, Weber P, Stewart G et al. Inactivation of ataxia telangiectasia mutated gene in B-cell chronic lymphocytic leukaemia. Lancet353(9146), 26–29 (1999).
   PubMed Web of Science ®Google Scholar
• Austen B, Powell JE, Alvi A et al. Mutations in the ATM gene lead to impaired overall and treatment-free survival that is independent of IGVH mutation status in patients with B-CLL. Blood106(9), 3175–3182 (2005).
   PubMed Web of Science ®Google Scholar
• Bullrich F, Rasio D, Kitada S et al.ATM mutations in B-cell chronic lymphocytic leukemia. Cancer Res.59(1), 24–27 (1999).
   PubMed Web of Science ®Google Scholar
• Edwards SL, Brough R, Lord CJ et al. Resistance to therapy caused by intragenic deletion in BRCA2. Nature451(7182), 1111–1115 (2008).
   PubMed Web of Science ®Google Scholar
• Sakai W, Swisher EM, Jacquemont C et al. Functional restoration of BRCA2 protein by secondary BRCA2 mutations in BRCA2-mutated ovarian carcinoma. Cancer Res.69(16), 6381–6386 (2009).
   PubMed Web of Science ®Google Scholar
• Liu X, Han EK, Anderson M et al. Acquired resistance to combination treatment with temozolomide and ABT-888 is mediated by both base excision repair and homologous recombination DNA repair pathways. Mol. Cancer Res.7(10), 1686–1692 (2009).
   PubMed Web of Science ®Google Scholar
• Yang SX, Kummar S, Steinberg SM et al. Immunohistochemical detection of poly(ADP-ribose) polymerase inhibition by ABT-888 in patients with refractory solid tumors and lymphomas. Cancer Biol. Ther.8(21), 2004–2009 (2009).
   PubMed Web of Science ®Google Scholar
• Kummar S, Kinders R, Gutierrez ME et al. Phase 0 clinical trial of the poly (ADP-ribose) polymerase inhibitor ABT-888 in patients with advanced malignancies. J. Clin. Oncol.27(16), 2705–2711 (2009).
   PubMed Web of Science ®Google Scholar
• Plummer R, Middleton M, Wilson R et al. First in human Phase I trial of the PARP inhibitor AG-014699 with temozolomide (TMZ) in patients (pts) with advanced solid tumors. J. Clin. Oncol.23(16 Suppl.) (2005) (Abstract 8013).
   Google Scholar
• Plummer R, Jones C, Middleton M et al. Phase I study of the poly(ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin. Cancer Res.14(23), 7917–7923 (2008).
   PubMed Web of Science ®Google Scholar
• Fong PC, Spicer J, Reade S et al. Phase I pharmacokinetic (PK) and pharmacodynamic (PD) evaluation of a small molecule inhibitor of Poly ADP-ribose polymerase (PARP), KU-0059436 (Ku) in patients (p) with advanced tumours. J. Clin. Oncol.4(Suppl. 18) (2006) (Abstract 5510).
   Google Scholar
• Fong PC, Boss DS, Carden CP et al. AZD2281 (KU-0059436), a PARP (poly ADP-ribose polymerase) inhibitor with single agent anticancer activity in patients with BRCA deficient ovarian cancer: results from a Phase I study. J. Clin. Oncol.26(Suppl.) 5510 (2008).
   Web of Science ®Google Scholar
• Fong PC, Boss DS, Yap TA et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med.361(2), 123–134 (2009).
   PubMed Web of Science ®Google Scholar
• Kopetz S, Mita MM, Mok I et al. First in human Phase I study of BSI-201, a small molecule inhibitor of poly ADP-ribose polymerase (PARP) in subjects with advanced solid tumors. J. Clin. Oncol.26(Suppl.) (2008) (Abstract 3579).
   Google Scholar
• Mahany JJ, Lewis N, Heath EI et al. A Phase IB study evaluating BSI-201 in combination with chemotherapy in subjects with advanced solid tumors. J. Clin. Oncol.26(Suppl.) (2008) (Abstract 8013).
   Google Scholar
• Plummer R, Lorigan P, Evans J et al. First and final report of a Phase II study of the poly(ADP-ribose) polymerase (PARP) inhibitor, AG014699, in combination with temozolomide (TMZ) in patients with metastatic malignant melanoma (MM). J. Clin. Oncol.24(Suppl. 18) (2006) (Abstract CRA501).
   Google Scholar
• Tutt A, Robson M, Garber JE et al. Phase II trial of the oral PARP inhibitor olaparib in BRCA-deficient advanced breast cancer. J. Clin. Oncol.27(Suppl. 18) (2009) (Abstract 3).
   Google Scholar
• O’Shaughnessy J, Osborne C, Pippen J et al. Efficacy of BSI-201, a poly (ADP-ribose) polymerase-1 (PARP1) inhibitor, in combination with gemcitabine/carboplatin (G/C) in patients with metastatic triple-negative breast cancer (TNBC): results of a randomized Phase II trial. J. Clin. Oncol.27(Suppl. 18) (2009).
   Google Scholar