The role of immune checkpoint inhibition in triple negative breast cancer

References

• Bianchini G, De Angelis C, Licata L, et al. Treatment landscape of triple-negative breast cancer - expanded options, evolving needs. Nat Rev Clin Oncol. 2022 Feb;19(2):91–113. doi: 10.1038/S41571-021-00565-2
   PubMed Web of Science ®Google Scholar
• Kwapisz D. Pembrolizumab and atezolizumab in triple-negative breast cancer. Cancer Immunol Immunother. 2021 Mar;70(3):607–617. doi: 10.1007/s00262-020-02736-z
   PubMed Web of Science ®Google Scholar
• Keenan TE, Tolaney SM. Role of immunotherapy in triple-negative breast cancer. J Natl Compr Canc Netw. 2020 Apr;18(4):479–489. doi: 10.6004/JNCCN.2020.7554
   PubMed Web of Science ®Google Scholar
• Wang X, Collet L, Rediti M, et al. Predictive biomarkers for response to immunotherapy in triple negative breast cancer: promises and challenges. J Clin Med. 2023 Feb;12(3):953. doi: 10.3390/JCM12030953/S1
   PubMed Web of Science ®Google Scholar
• Derakhshan F, Reis-Filho JS. Pathogenesis of triple-negative breast cancer. Annu Rev Pathol. 2022;17:181–204. doi:10.1146/ANNUREV-PATHOL-042420-093238
   PubMed Web of Science ®Google Scholar
• Mittendorf EA, Philips AV, Meric-Bernstam F, et al. PD-L1 expression in triple-negative breast cancer. Cancer Immunol Res. 2014 Apr;2(4):361–370. doi: 10.1158/2326-6066.CIR-13-0127
   PubMed Web of Science ®Google Scholar
• Rugo HS, Loi S, Adams S, et al. PD-L1 Immunohistochemistry Assay Comparison in atezolizumab plus nab -paclitaxel–Treated advanced triple-negative breast cancer. J Natl Cancer Inst. 2021 Dec;113(12):1733–1743. doi: 10.1093/JNCI/DJAB108
   PubMedGoogle Scholar
• Vennapusa B, Baker B, Kowanetz M, et al. Development of a PD-L1 complementary diagnostic immunohistochemistry assay (SP142) for Atezolizumab. Appl Immunohistochem Mol Morphol. 2019 Feb;27(2):92–100. doi: 10.1097/PAI.0000000000000594
   PubMedGoogle Scholar
• Nanda R, Chow LQM, Dees EC, et al. Pembrolizumab in patients with advanced triple-negative breast cancer: phase Ib KEYNOTE-012 study. J Clin Oncol. 2016 Jul;34(21):2460. doi: 10.1200/JCO.2015.64.8931
   PubMed Web of Science ®Google Scholar
• Adams S, Loi S, Toppmeyer D, et al. Pembrolizumab monotherapy for previously untreated, PD-L1-positive, metastatic triple-negative breast cancer: cohort B of the phase II KEYNOTE-086 study. Ann Oncol. 2019 Mar;30(3):405–411. doi: 10.1093/ANNONC/MDY518
   PubMed Web of Science ®Google Scholar
• Adams S, Schmid P, Rugo HS, et al. Pembrolizumab monotherapy for previously treated metastatic triple-negative breast cancer: cohort a of the phase II KEYNOTE-086 study. Ann Oncol. 2019 Mar;30(3):397–404. doi: 10.1093/ANNONC/MDY517
   PubMed Web of Science ®Google Scholar
• Winer EP, Lipatov O, Im S-A, et al. Pembrolizumab versus investigator-choice chemotherapy for metastatic triple-negative breast cancer (KEYNOTE-119): a randomised, open-label, phase 3 trial. Lancet Oncol. 2021 Apr;22(4):499–511. doi: 10.1016/S1470-2045(20)30754-3
   PubMed Web of Science ®Google Scholar
• Dirix LY, Takacs I, Jerusalem G, et al. Avelumab, an anti-PD-L1 antibody, in patients with locally advanced or metastatic breast cancer: a phase 1b JAVELIN solid tumor study. Breast Cancer Res Treat. 2018 Oct;167(3):671–686. doi: 10.1007/S10549-017-4537-5
   PubMed Web of Science ®Google Scholar
• Emens LA, Cruz C, Eder JP, et al. Long-term clinical outcomes and biomarker analyses of atezolizumab therapy for patients with metastatic triple-negative breast cancer: a phase 1 study. JAMA Oncol. 2019 Jan;5(1):74–82. doi: 10.1001/JAMAONCOL.2018.4224
   PubMed Web of Science ®Google Scholar
• Santa-Maria CA, Kato T, Park J-H, et al. A pilot study of durvalumab and tremelimumab and immunogenomic dynamics in metastatic breast cancer. Oncotarget. 2018 Apr;9(27):18985. doi: 10.18632/ONCOTARGET.24867
   PubMedGoogle Scholar
• Adams S, Othus M, Patel SP, et al. A multicenter phase II trial of Ipilimumab and nivolumab in unresectable or metastatic Metaplastic breast cancer: cohort 36 of dual anti–CTLA-4 and anti–PD-1 blockade in rare tumors (DART, SWOG S1609). Clin Cancer Res. 2022 Jan;28(2):271–278. doi: 10.1158/1078-0432.CCR-21-2182
   PubMed Web of Science ®Google Scholar
• Emens LA, Adams S, Barrios CH, et al. First-line atezolizumab plus nab-paclitaxel for unresectable, locally advanced, or metastatic triple-negative breast cancer: IMpassion130 final overall survival analysis. Ann Oncol. 2021 Aug;32(8):983–993. doi: 10.1016/J.ANNONC.2021.05.355
   PubMed Web of Science ®Google Scholar
• Franzoi MA, De Azambuja E. Atezolizumab in metastatic triple-negative breast cancer: IMpassion130 and 131 trials - how to explain different results? ESMO Open. 2020 Nov;5(6):e001112. doi: 10.1136/ESMOOPEN-2020-001112
   PubMed Web of Science ®Google Scholar
• Miles D, Gligorov J, André F, et al. Primary results from IMpassion131, a double-blind, placebo-controlled, randomised phase III trial of first-line paclitaxel with or without atezolizumab for unresectable locally advanced/metastatic triple-negative breast cancer. Ann Oncol. 2021 Aug;32(8):994–1004. doi: 10.1016/J.ANNONC.2021.05.801
   PubMed Web of Science ®Google Scholar
• Schmid P, Adams S, Rugo HS, et al. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer. N Engl J Med. 2018 Nov;379(22):2108–2121. doi: 10.1056/NEJMOA1809615
   PubMed Web of Science ®Google Scholar
• Cortes J, Cescon DW, Rugo HS, et al. Pembrolizumab plus chemotherapy versus placebo plus chemotherapy for previously untreated locally recurrent inoperable or metastatic triple-negative breast cancer (KEYNOTE-355): a randomised, placebo-controlled, double-blind, phase 3 clinical trial. Lancet. 2020 Dec;396(10265):1817–1828. doi: 10.1016/S0140-6736(20)32531-9
   PubMed Web of Science ®Google Scholar
• Cortes J, Rugo HS, Cescon DW, et al. Pembrolizumab plus chemotherapy in advanced triple-negative breast cancer. N Engl J Med. 2022 Jul;387(3):217–226. doi: 10.1056/NEJMOA2202809/SUPPL_FILE/NEJMOA2202809_DATA-SHARING.PDF
   PubMed Web of Science ®Google Scholar
• Barker AD, Sigman CC, Kelloff GJ, et al. I-SPY 2: an adaptive breast cancer trial design in the setting of neoadjuvant chemotherapy. Clin Pharmacol Ther. 2009 Jul;86(1):97–100. doi: 10.1038/CLPT.2009.68
   PubMed Web of Science ®Google Scholar
• Nanda R, Liu MC, Yau C, et al. Effect of pembrolizumab plus neoadjuvant chemotherapy on pathologic complete response in Women with early-stage breast cancer: an analysis of the ongoing phase 2 adaptively randomized I-SPY2 trial. JAMA Oncol. 2020 May;6(5):676–684. doi: 10.1001/JAMAONCOL.2019.6650
   PubMed Web of Science ®Google Scholar
• Wang H, Yee D. I-SPY 2: a neoadjuvant adaptive clinical trial designed to improve outcomes in high-risk breast cancer. Curr Breast Cancer Rep. 2019 Dec;11(4):303–310. doi: 10.1007/S12609-019-00334-2
   PubMed Web of Science ®Google Scholar
• Schmid P, Salgado R, Park YH, et al. Pembrolizumab plus chemotherapy as neoadjuvant treatment of high-risk, early-stage triple-negative breast cancer: results from the phase 1b open-label, multicohort KEYNOTE-173 study. Ann Oncol. 2020 May;31(5):569–581. doi: 10.1016/J.ANNONC.2020.01.072
   PubMed Web of Science ®Google Scholar
• Loibl S, Untch M, Burchardi N, et al. A randomised phase II study investigating durvalumab in addition to an anthracycline taxane-based neoadjuvant therapy in early triple-negative breast cancer: clinical results and biomarker analysis of GeparNuevo study. Ann Oncol. 2019 Aug;30(8):1279–1288. doi: 10.1093/ANNONC/MDZ158
   PubMed Web of Science ®Google Scholar
• Rizzo A, Cusmai A, Acquafredda S, et al. KEYNOTE-522, IMpassion031 and GeparNUEVO: changing the paradigm of neoadjuvant immune checkpoint inhibitors in early triple-negative breast cancer. Future Oncol. 2022 Jun;18(18):2301–2309. doi: 10.2217/FON-2021-1647
   PubMed Web of Science ®Google Scholar
• Schmid P, Cortes J, Pusztai L, et al. Pembrolizumab for early triple-negative breast cancer. N Engl J Med. 2020 Feb;382(9):810–821. doi: 10.1056/NEJMOA1910549/SUPPL_FILE/NEJMOA1910549_DATA-SHARING.PDF
   PubMed Web of Science ®Google Scholar
• Schmid P, Cortes J, Dent R, et al. Event-free survival with pembrolizumab in early triple-negative breast cancer. N Engl J Med. 2022 Feb;386(6):556–567. doi: 10.1056/NEJMOA2112651/SUPPL_FILE/NEJMOA2112651_DATA-SHARING.PDF
   PubMed Web of Science ®Google Scholar
• Mittendorf EA, Zhang H, Barrios CH, et al. Neoadjuvant atezolizumab in combination with sequential nab-paclitaxel and anthracycline-based chemotherapy versus placebo and chemotherapy in patients with early-stage triple-negative breast cancer (IMpassion031): a randomised, double-blind, phase 3 trial. Lancet. 2020 Oct;396(10257):1090–1100. doi: 10.1016/S0140-6736(20)31953-X
   PubMed Web of Science ®Google Scholar
• Gianni L, Huang CS, Egle D, et al. Pathologic complete response (pCR) to neoadjuvant treatment with or without atezolizumab in triple-negative, early high-risk and locally advanced breast cancer: NeoTRIP Michelangelo randomized study. Ann Oncol. 2022 May;33(5):534–543. doi: 10.1016/J.ANNONC.2022.02.004
   PubMed Web of Science ®Google Scholar
• Lee EK, Konstantinopoulos PA. Combined PARP and immune checkpoint inhibition in ovarian cancer. Trends Cancer. 2019 Sep;5(9):524–528. doi: 10.1016/J.TRECAN.2019.06.004
   PubMed Web of Science ®Google Scholar
• Zitvogel L, Galluzzi L, Kepp O, et al. Type I interferons in anticancer immunity. Nat Rev Immunol. 2015 Jun;15(7):405–414. doi: 10.1038/nri3845
   PubMed Web of Science ®Google Scholar
• Vikas P, Borcherding N, Chennamadhavuni A, et al. Therapeutic potential of combining PARP inhibitor and immunotherapy in solid tumors. Front Oncol. 2020 Apr;10. doi: 10.3389/FONC.2020.00570
   PubMed Web of Science ®Google Scholar
• Domchek SM, Postel-Vinay S, Im S-A, et al. Olaparib and durvalumab in patients with germline BRCA-mutated metastatic breast cancer (MEDIOLA): an open-label, multicentre, phase 1/2, basket study. Lancet Oncol. 2020 Sep;21(9):1155–1164. doi: 10.1016/S1470-2045(20)30324-7
   PubMed Web of Science ®Google Scholar
• Vinayak S, Tolaney SM, Schwartzberg L, et al. Open-label clinical trial of niraparib combined with pembrolizumab for treatment of advanced or metastatic triple-negative breast cancer. JAMA Oncol. 2019 Aug;5(8):1132–1140. doi: 10.1001/JAMAONCOL.2019.1029
   PubMed Web of Science ®Google Scholar
• Pusztai L, Yau C, Wolf DM, et al. Durvalumab with olaparib and paclitaxel for high-risk HER2-negative stage II/III breast cancer: results from the adaptively randomized I-SPY2 trial. Cancer Cell. 2021 Jul;39(7):989–998.e5. doi: 10.1016/J.CCELL.2021.05.009
   PubMed Web of Science ®Google Scholar
• Li B, Jin J, Guo D, et al. Immune checkpoint inhibitors combined with targeted therapy: the recent advances and future potentials. Cancers (Basel). 2023 May;15(10):2858. doi: 10.3390/CANCERS15102858/S1
   PubMed Web of Science ®Google Scholar
• Alzahrani AS. PI3K/Akt/mTOR inhibitors in cancer: at the bench and bedside. Semin Cancer Biol. 2019 Dec;59:125–132. doi: 10.1016/J.SEMCANCER.2019.07.009
   PubMed Web of Science ®Google Scholar
• Katso R, Okkenhaug K, Ahmadi K, et al. Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu Rev Cell Dev Biol. 2001;17:615–675. doi: 10.1146/ANNUREV.CELLBIO.17.1.615
   PubMed Web of Science ®Google Scholar
• Cerma K, Piacentini F, Moscetti L, et al. Targeting PI3K/AKT/mTOR Pathway in breast cancer: from biology to clinical challenges. Biomedicines. 2023 Jan;11(1):109. doi: 10.3390/BIOMEDICINES11010109
   PubMed Web of Science ®Google Scholar
• Zhu S, Wu Y, Song B, et al. Recent advances in targeted strategies for triple-negative breast cancer. J Hematol Oncol. 2023 Dec;16(1):100. doi: 10.1186/S13045-023-01497-3
   PubMed Web of Science ®Google Scholar
• Loi S, Dushyanthen S, Beavis PA, et al. RAS/MAPK activation is associated with reduced tumor-infiltrating lymphocytes in triple-negative breast cancer: therapeutic cooperation between MEK and PD-1/PD-L1 immune checkpoint inhibitors. Clin Cancer Res. 2016 Mar;22(6):1499–1509. doi: 10.1158/1078-0432.CCR-15-1125
   PubMed Web of Science ®Google Scholar
• Hosseini M, Seyedpour S, Khodaei B, et al. Cancer vaccines for triple-negative breast cancer: a systematic review. Vaccines (Basel). 2023 Jan;11(1):146. doi: 10.3390/VACCINES11010146/S1
   PubMed Web of Science ®Google Scholar
• Abdou Y, Goudarzi A, Yu JX, et al. Immunotherapy in triple negative breast cancer: beyond checkpoint inhibitors. NPJ Breast Cancer. 2022 Nov;8(1):1–10. doi: 10.1038/s41523-022-00486-y
   PubMed Web of Science ®Google Scholar
• Isakoff SJ, Adams S, Soliman HH, et al. Abstract P3-09-15: a phase 1b study of PVX-410 (PVX) vaccine plus durvalumab (DUR) as adjuvant therapy in HLA-A2+ early stage triple negative breast cancer (eTNBC) to assess safety and immune response. Cancer Res. 2020 Feb;80(4_Supplement):P3-09–15. doi: 10.1158/1538-7445.SABCS19-P3-09-15
   Web of Science ®Google Scholar
• Kachikwu EL, Iwamoto KS, Liao Y-P, et al. Radiation enhances regulatory T cell representation. Int J Radiat Oncol Biol Phys. 2011 Nov;81(4):1128–1135. doi: 10.1016/J.IJROBP.2010.09.034
   PubMed Web of Science ®Google Scholar
• Ho AY, Tabrizi S, Dunn SA, et al. Current advances in immune checkpoint inhibitor combinations with radiation therapy or cryotherapy for breast cancer. Breast Cancer Res Treat. 2022 Jan;191(2):229–241. doi: 10.1007/S10549-021-06408-Z
   PubMed Web of Science ®Google Scholar
• Ho AY, Barker CA, Arnold BB, et al. A phase 2 clinical trial assessing the efficacy and safety of pembrolizumab and radiotherapy in patients with metastatic triple-negative breast cancer. Cancer. 2020 Feb;126(4):850–860. doi: 10.1002/CNCR.32599
   PubMed Web of Science ®Google Scholar
• David S, Savas P, Siva S, et al. Abstract 10-02: a randomised phase II trial of single fraction or multi-fraction SABR (stereotactic ablative body radiotherapy) with atezolizumab in patients with advanced triple negative breast cancer (AZTEC trial). Cancer Res. 2022 Feb;82(4_Supplement):PD10–02. doi: 10.1158/1538-7445.SABCS21-PD10-02
   Web of Science ®Google Scholar
• Emens LA, Molinero L, Loi S, et al. Atezolizumab and nab-paclitaxel in advanced triple-negative breast cancer: biomarker evaluation of the IMpassion130 study. J Natl Cancer Inst. 2021 Aug;113(8):1005–1016. doi: 10.1093/JNCI/DJAB004
   PubMedGoogle Scholar
• Schmid P, Rugo HS, Adams S, et al. Atezolizumab plus nab-paclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (IMpassion130): updated efficacy results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2020 Jan;21(1):44–59. doi: 10.1016/S1470-2045(19)30689-8
   PubMed Web of Science ®Google Scholar
• Cortés J, Lipatov O, Im S-A, et al. KEYNOTE-119: phase III study of pembrolizumab (pembro) versus single-agent chemotherapy (chemo) for metastatic triple negative breast cancer (mTNBC). Ann Oncol. 2019 Oct;30:v859–v860.
   PubMed Web of Science ®Google Scholar
• Loibl S, Schneeweiss A, Huober J, et al. Neoadjuvant durvalumab improves survival in early triple-negative breast cancer independent of pathological complete response. Ann Oncol. 2022 Nov;33(11):1149–1158. doi: 10.1016/J.ANNONC.2022.07.1940
   PubMed Web of Science ®Google Scholar
• Goodman AM, Kato S, Bazhenova L, et al. Tumor mutational burden as an independent predictor of response to immunotherapy in diverse cancers. Mol Cancer Ther. 2017 Nov;16(11):2598–2608. doi: 10.1158/1535-7163.MCT-17-0386
   PubMed Web of Science ®Google Scholar
• Marcus L, Fashoyin-Aje LA, Donoghue M, et al. FDA approval summary: pembrolizumab for the treatment of tumor mutational burden–high solid tumors. Clin Cancer Res. 2021 Sep;27(17):4685–4689. doi: 10.1158/1078-0432.CCR-21-0327
   PubMed Web of Science ®Google Scholar
• Barroso-Sousa R, Keenan TE, Pernas S, et al. Tumor mutational burden and PTEN Alterations as Molecular Correlates of response to PD-1/L1 blockade in metastatic triple-negative breast cancer. Clin Cancer Res. 2020 Jun;26(11):2565–2572. doi: 10.1158/1078-0432.CCR-19-3507
   PubMed Web of Science ®Google Scholar
• Karn T, Denkert C, Weber KE, et al. Tumor mutational burden and immune infiltration as independent predictors of response to neoadjuvant immune checkpoint inhibition in early TNBC in GeparNuevo. Ann Oncol. 2020 Sep;31(9):1216–1222. doi: 10.1016/J.ANNONC.2020.05.015
   PubMed Web of Science ®Google Scholar
• Loi S, Adams S, Schmid P, et al. Relationship between tumor infiltrating lymphocyte (TIL) levels and response to pembrolizumab (pembro) in metastatic triple-negative breast cancer (mTNBC): results from KEYNOTE-086. Ann Oncol. 2017 Sep;28:v608.
   Web of Science ®Google Scholar
• Wen YH, Brogi E, Zeng Z, et al. DNA mismatch repair deficiency in breast carcinoma: a pilot study of triple-negative and non-triple-negative tumors. Am J Surg Pathol. 2012 Nov;36(11):1700–1708. doi: 10.1097/PAS.0B013E3182627787
   PubMed Web of Science ®Google Scholar
• Maio M, Ascierto PA, Manzyuk L, et al. Pembrolizumab in microsatellite instability high or mismatch repair deficient cancers: updated analysis from the phase II KEYNOTE-158 study. Ann Oncol. 2022 Sep;33(9):929–938. doi: 10.1016/J.ANNONC.2022.05.519
   PubMed Web of Science ®Google Scholar
• Marabelle A, Le DT, Ascierto PA, et al. Efficacy of pembrolizumab in patients with noncolorectal high microsatellite instability/mismatch repair–deficient cancer: results from the phase II KEYNOTE-158 study. J Clin Oncol. 2020;38(1):1–10. doi: 10.1200/JCO.19.02105
   PubMed Web of Science ®Google Scholar
• Emens LA, Adams S, Cimino-Mathews A, et al. Society for immunotherapy of cancer (SITC) clinical practice guideline on immunotherapy for the treatment of breast cancer. J Immunother Cancer. 2021 Aug;9(8):2597. doi: 10.1136/JITC-2021-002597
   PubMed Web of Science ®Google Scholar
• Sullivan RJ, Weber JS. Immune-related toxicities of checkpoint inhibitors: mechanisms and mitigation strategies. Nat Rev Drug Discov. 2021 Jul;21(7):495–508. doi: 10.1038/s41573-021-00259-5
   PubMed Web of Science ®Google Scholar
• Johnson DB, Jakubovic BD, Sibaud V, et al. Balancing cancer immunotherapy efficacy and toxicity. J Allergy Clin Immunol Pract. 2020 Oct;8(9):2898. doi: 10.1016/J.JAIP.2020.06.028
   PubMed Web of Science ®Google Scholar
• Zhang Y, Wang J, Hu T, et al. Adverse events of PD-1 or PD-L1 inhibitors in triple-negative breast cancer: a systematic review and meta-analysis. Life. 2022 Dec;12(12):1990. doi: 10.3390/LIFE12121990/S1
   PubMedGoogle Scholar
• Havel JJ, Chowell D, Chan TA. The evolving landscape of biomarkers for checkpoint inhibitor immunotherapy. Nat Rev Cancer. 2019 Feb;19(3):133–150. doi: 10.1038/s41568-019-0116-x
   PubMed Web of Science ®Google Scholar
• Puzanov I, Diab A, Abdallah K, et al. Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for immunotherapy of cancer (SITC) toxicity management working group. J Immunother Cancer. 2017 Nov;5(1). doi: 10.1186/S40425-017-0300-Z
   Google Scholar