A clinical evaluation of treatments that target cell cycle machinery in breast cancer

References

• Nurse P. Genetic control of cell size at cell division in yeast. Nature. 1975;256:547–551.
   PubMed Web of Science ®Google Scholar
• Beach D, Durkacz B, Nurse P. Functionally homologous cell cycle controlgenes in budding andfission yeast. Nature. 1982;300:706–709.
   PubMed Web of Science ®Google Scholar
• Schafer KA. The cell cycle: a review. Vet Pathol. 1998;35:461–478.
   PubMed Web of Science ®Google Scholar
• Wenzel ES, Singh ATK. Cell cycle checkpoints and aneuploidy on the path of cancer. In Vivo. 2018;32:1–5.
   PubMed Web of Science ®Google Scholar
• Arnold A, Papanikolaou A. Cyclin D1 in breast cancer pathogenesis. J Clin Oncol. 2005;23:4215–4224.
   PubMed Web of Science ®Google Scholar
• Rexer BN, Arteaga CL. Intrinsic and acquired resistance to HER2-targeted therapies in HER2 gene-amplified breast cancer: mechanisms and clinical implications. Crit Rev Oncog. 2012;17:1–16.
   PubMedGoogle Scholar
• Robinson TJ, Liu JC, Vizeacoumar F, et al. RB1 status in triple negative breast cancer cells dictates response to radiation treatment and selective therapeutic drugs. PLoS One. 2013;8(11):e78641.
   PubMed Web of Science ®Google Scholar
• Fedele P, Ciccarese M, Surico G, et al. An update on first line therapies for metastatic breast cancer. Exp Opin Pharmac. 2018;19:243–252.
   PubMed Web of Science ®Google Scholar
• Fedele P, Ciccarese M, Surico G, et al. Pharmacotherapeutic options for patients with refractory breast cancer. Exp Opin Pharmac. 2019;7:851–861.
   Google Scholar
• Parìtdee AB. G1 events and regulation of cell proliferation. Science. 1989;246:603–608.
   PubMed Web of Science ®Google Scholar
• VanArsdale T, Boshoff C, Arnd K, et al. Molecular pathways: targeting the cyclin D-CDK 4/6 axis for cancer treatment. Clin Cancer Res. 2015;21(13):2905–2910.
   Web of Science ®Google Scholar
• Matsushime H, Roussel MF, Ashmun RA, et al. Colony –stimulating factor 1 regulates novel cyclins during the G1 phase of cell cycle. Cell. 1991;65:701–713.
   PubMed Web of Science ®Google Scholar
• Xiong Y, Connolly Y, Futhcer B, et al. Human D type cyclin. Cell. 1991;65:691–699.
   PubMed Web of Science ®Google Scholar
• Narasimha AM, Kaulich M, Shapiro GS, et al. Cyclin D activates the Rb tumor suppressor by monophosphorilationn. E Life. 2014;3. DOI:10.7554/el.ife.02872.
   Google Scholar
• Andres L, Ke N, Hubriding P, et al. Asystematic screen for CDK 4/6 substrates link FOXM1 phosphorilation to senescence suppression in cancer cells. Cancer Cell. 2011;20:620–634.
   PubMed Web of Science ®Google Scholar
• Greenblatt MS, Bennett WP, Hollstein M, et al. Mutation in p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 1994;54:4855–4878.
   PubMed Web of Science ®Google Scholar
• Subramanian M, Jones MF, Lal A. Long non-coding RNAs embedded in the Rb and p53 pathways. Cancers (Basel). 2013;5:1655–1675.
   PubMedGoogle Scholar
• Finlay CA, The MDM. 2 oncogene can overcame wild type p53 and MDM 2 protein. Mol Cell Biol. 1993;13:301–306.
   PubMed Web of Science ®Google Scholar
• Peeper DS, Bernards R. Communication between the extracellular environment, cytoplasmic signalling cascades and the nuclear cell cycle machinery. FEBS Lett. 1997;410:11–16.
   PubMed Web of Science ®Google Scholar
• Marshall CJ. Small. GTP-ases and cell cycle regulation. Biochem Soc Trans. 1999;27(3):63–70.
   PubMedGoogle Scholar
• Sherr CJ, Robert JM. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999;13:1501–1512.
   PubMed Web of Science ®Google Scholar
• Ewen ME. Relationship between Ras pathways and cell cycle control. Prog Cell Cycle Res. 2000;4:1–17.
   PubMedGoogle Scholar
• Stepanova L, Leng X, Parker SB, et al. Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev. 1996;10:1491–1502.
   PubMed Web of Science ®Google Scholar
• Parry D, Mahony D, Wills K, et al. Cyclin D-CDK subunit arrangement is dependent on the availability of competing INK4 and p21 class inhibitors. Mol Cell Biol. 1999;19:1775–1783.
   PubMed Web of Science ®Google Scholar
• Serrano M, Lin AW, Mc Currach ME, et al. Oncogenic ras provokes premature senescence associated with accumulation of p53 and p16INK4a. Cell. 1997;88:593–602.
   PubMed Web of Science ®Google Scholar
• Sherr C, Beach D, Shapiro G. Targeting CDK4 and CDK 6: from discovery to therapy. Cancer Discov. 2016;353–367.
   PubMed Web of Science ®Google Scholar
• Diehl JA, Zindy F, Sherr CJ. Inhibition of cyclin D1 phosphorylation on threonine-286 prevents its rapid degradation via the ubiquitinproteasome pathway. Genes Dev. 1997;11:957–972.
   PubMed Web of Science ®Google Scholar
• Diehl JA, Cheng M, Roussel MF, et al. Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev. 1998;12:3499–5126.
   PubMed Web of Science ®Google Scholar
• Alt JR, Clleveland JL, Hannink M, et al. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev. 2000;14:3102–3114.
   PubMed Web of Science ®Google Scholar
• Lin DI, Barbash O, Kumar KG, et al. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell. 2006;24:355–366.
   PubMed Web of Science ®Google Scholar
• Aggarwal P, Lessie MD, Lin DI, et al. Nuclear accumulation of cyclin D1 during S phase inhibits Cul4-dependent Cdt1 proteolysis and triggers p53-dependent DNA rereplication. Genes Dev. 2007;21:2908–2922.
   PubMed Web of Science ®Google Scholar
• Li Y, Chitnis N, Nakagawa H, et al. RMT5 is required for lymphomagenesis triggered by multiple oncogenic drivers. Cancer Discov. 2015;5:288–303.
   PubMed Web of Science ®Google Scholar
• Augello MA, Berman-Booty LD, Carr R, et al. Consequence of the tumor-associated conversion to cyclin D1b. EMBO Mol Med. 2015;7:628–647.
   PubMed Web of Science ®Google Scholar
• Goel S, DeCristo MJ, Watt AC, et al. CDK4/6 inhibition triggers anti-tumor immunity. Nature. 2017;548:471–475.
   PubMed Web of Science ®Google Scholar
• Casimiro MC, Wang C, Li Z, et al. Cyclin D1 determines estrogen signaling in the mammarygland in vivo. Mol Endocrinol. 2013;27:1415–1428.
   PubMed Web of Science ®Google Scholar
• Cicenas J, Kalyan K, Sorokinas A, et al. Highlights of the latest advances in research on CDK inhibitors. Cancers (Basel). 2014;6:2224–2242.
   PubMed Web of Science ®Google Scholar
• Sedlacek H, Czech J, Naik R, et al. Flavopiridol (L86 8275; NSC 649890), a new kinase inhibitor for tumor therapy. Int J Oncol. 1996;9:1143–1168.
   PubMed Web of Science ®Google Scholar
• Turner NC, Huang Bartlett C, Cristofanilli M. Palbociclib in hormone-receptor-positive advanced breast cancer. N Engl J Med. 2015;373(17):1672–1673.
   PubMed Web of Science ®Google Scholar
• Hortobagyi GN, Stemmer SM, Burris HA, et al. Ribociclib as first-line therapy for HR-positive, advanced breast cancer. N Engl J Med. 2016;375(18):1738–1748.
   PubMed Web of Science ®Google Scholar
• Tripathy D, Im S-A, Colleoni M, et al. Ribociclib plus endocrine therapy for premenopausal women with hormone-receptor-positive, advanced breast cancer (MONALEESA-7): a randomised phase 3 trial. Lancet Oncol. 2018;19:904–915.
   PubMed Web of Science ®Google Scholar
• Goetz MP, Toi M, Campone M, et al. MONARCH 3: abemaciclib as initial therapy for advanced breast cancer. J Clin Oncol. 2017;35(32):3638–3646.
   PubMed Web of Science ®Google Scholar
• Cristofanilli M, Turner NC, Bondarenko I, et al. Fulvestrant plus palbociclib versus fulvestrant plus placebo for treatment of hormone-receptor-positive, HER2-negative metastatic breast cancer that progressed on previous endocrine therapy (PALOMA-3): final analysis of the multicentre, double-blind, phase 3 randomized controlled trial. Lancet Oncol. 2016;17(4):425–439.
   PubMed Web of Science ®Google Scholar
• Sledge GW Jr., Toi M, Neven P, et al. MONARCH 2: abemaciclib in combination with fulvestrant in women with HR+/HER2- advanced breast cancer who had progressed while receiving endocrine therapy. J Clin Oncol. 2017;35(25):2875–2884.
   PubMed Web of Science ®Google Scholar
• Slamon DJ, Neven P, Chia S, et al. Phase III randomized study of ribociclib and fulvestrant in hormone receptor-positive, human epidermal growth factor receptor 2-negative advanced breast cancer: MONALEESA-3. J Clin Oncol. 2018;36:2465–2472.
   PubMed Web of Science ®Google Scholar
• Turner NC, Slamon D, Ro J, et al. Overall survival with palbociclib and fulvestrant in advanced breast cancer. N Engl J Med. 2018;379:1926–1936.
   PubMed Web of Science ®Google Scholar
• Kim M, Agarwal S, Tripathy D. Updates on the treatment of human epidermal growth factor receptor type 2-positive breast cancer. Curr Opin Obstet Gynecol. 2014;26:27–33.
   PubMed Web of Science ®Google Scholar
• Kumler I, Tuxen MK, Nielsen DL. A systematic review of dual targeting in HER2- positive breast cancer. Cancer Treat Rev. 2014;40:259–270.
   PubMed Web of Science ®Google Scholar
• Rexer BN, Shyr Y, Arteaga CL. Phosphatase and tensin homolog deficiency and resistance to trastuzumab and chemotherapy. J Clin Oncol. 2013;31:2073–2075.
   PubMed Web of Science ®Google Scholar
• Lim S, Kaldis P. Cdks, cyclins and CKIs: roles beyond cell cycle regulation. Development. 2013;140:3079–3093.
   PubMed Web of Science ®Google Scholar
• Knudsen ES, Wang JY. Targeting the RB-pathway in cancer therapy. Clin Cancer Res. 2010;16:1094–1099.
   PubMed Web of Science ®Google Scholar
• Roberts PJ, Bisi JE, Strum JC, et al. Multiple roles of cyclin-dependent kinase 4/6 inhibitors in cancer therapy. J Natl Cancer Inst. 2012;104:476–487.
   PubMed Web of Science ®Google Scholar
• Agnieszka K, Witkiewicz K, Cox D, et al. CDK 4/6 inhibition provides a potent adjunct to HER 2 target therapies in preclinical breast models. Genes Cancer. 2014;5(7–8):261–272.
   Google Scholar
• Phillips GD, Fields CT, Li G, et al. Dual targeting of HEr positive cancer with trastuzumab emtansine and pertuzumab: critical role for neuregolin blockade in antitumor response to combination therapy. Clin Cancer Res. 2014;20:456–468.
   PubMed Web of Science ®Google Scholar
• Timms JF, White SL, O’Hare MJ, et al. Effects of Erb2 overexpression in mitogenic signaling and cell cycle progression in human breast cancer. Oncogene. 2002;21:6573–6586.
   PubMed Web of Science ®Google Scholar
• Lenkfering AEG, Busse D, Flanagan WM, et al. Erb2/neu kinase modulates cellular p27(kip1) and Ciclin D1 thrpough multiple signaling pathways. Cancer Res. 2001;61:6583.
   PubMed Web of Science ®Google Scholar
• O’Brien N, Conklin D, Beckmann R, et al. Preclinical activity of abemaciclib alone or in combination with antimototic and target therapies in breast cancer. Mol Cancer Ther. 2018;17(5):897–907.
   Google Scholar
• Pernas S, Tolaney SM. HER 2 positive breast cancer: new therapeutic frontiers and overcaming resistance. Ther Adv Med Oncol. 2019;11:1–16.
   Web of Science ®Google Scholar
• Ciruelos E, Villagrasa P, Paré L, et al. SOLTI-1303 PATRICIA phase II trial (STAGE 1) palbociclib and trastuzumab in postmenopausal patients with HER2-positive metastatic breast cancer. Poster presented at the Annual San Antonio Breast Cancer Symposium (SABCS); 2018 Dec 4–8; San Antonio (TX).
   Google Scholar
• DeMichele A, Clark A, Tan KS, et al. CDK4/6 inhibitor palbociclib (PD0332991) in Rb+ advanced breast cancer: phase II activity, safety and predictive biomarker assessment. Clin Cancer Res. 2015;21(5):995–1001.
   PubMed Web of Science ®Google Scholar
• Clark AS, McAndrew NP. Single agent palbociclib with or without trastuzumab for the treatment of Rb+ advanced breast cancer: a phase II trial. Poster presented at: San Antonio Breast Cancer Symposium; 2016 Dec 6–10; San Antonio (TX).
   Google Scholar
• Gianni L, Bisagni G, Colleoni M, et al. Neoadjuvant treatment with trastuzumab and pertuzumab plus palbociclib and fulvestrant in HER2-positive, ER-positive breast cancer (NA-PHER2): an exploratory, open- label, phase 2 study. Lancet Oncol. 2018;19(2):249–256.
   PubMed Web of Science ®Google Scholar
• ClinicalTrials.gov [Internet]. Bethesda (MD): National Library of Medicine (US); 2000 [cited 2019 Jan 18]. Available from: http://clinicaltrials.gov/
   Google Scholar
• Lehmann BD, Bauer JA, Chen X, et al. Identification of human triplenegative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011;121(7):2750–2767.
   PubMed Web of Science ®Google Scholar
• Teo ZL, Versaci S, Dushyanthen S, et al. Combined CDK4/6 and PI3Ka inhibition is synergistic and immunogenic in triple-negative breast cancer. Cancer Res. 2017;77(22):6340–6352. AACR.
   PubMed Web of Science ®Google Scholar
• O’Leary B. Finn RS and turner NC. Treating cancer with selective CDK4/6 inhibitors. Nat Rev Clin Oncol. 2016;13:417–430.
   PubMed Web of Science ®Google Scholar
• Witkiewicz AK, Cox D and Knudsen ES. CDK4/6 inhibition provides a potent adjunct to HER2-targeted therapies in preclinical breast cancer models. Genes Cancer. 2014;5:261–272.
   PubMedGoogle Scholar
• Trere D, Brighenti E, Donati G, et al. High prevalence of retinoblastoma protein loss in triple-negative breast cancers and its association with a good prognosis in patients treated with adjuvant chemotherapy. Ann Oncol. 2009;20(11):1818–1823.
   PubMed Web of Science ®Google Scholar
• Rao SS, Stoehr J, Dokic D, et al. Synergistic effect of eribulin and CDK inhibition for the treatment of triple negative breast cancer. Oncotarget. 2017;8:83925–83939.
   PubMedGoogle Scholar
• Asghar US, Barr AR, Cutts R, et al. Single-cell dynamics determines response to CDK4/6 inhibition in triple-negative breast cancer. Clin Cancer Res. 2017;23(18):5561–5572.
   PubMed Web of Science ®Google Scholar
• Gucalp A, Proverbs-Singh TA, Corben A. Phase I/II trial of palbociclib in combination with bicalutamide for the treatment of androgen receptor (AR)+ metastatic breast cancer (MBC). J Clin Oncol. 2017;34:15.
   Google Scholar
• Kashiwagi S, Asano Y, Goto W, et al. The novel potential of palbociclib (CDK4/6 inhibitor) in the treatment of triple-negative breast cancer. Cancer Res. 2017;77(13 Supplement 1). Abstract number 2351.
   Google Scholar
• Finn RS, Dering J, Conklin D, et al. PD 0332991, a selective cyclin D kinase 4/6 inhibitor, preferentially inhibits proliferation of luminal estrogen receptor-positive human breast cancer cell lines in vitro. Breast Cancer Res. 2009;11(5):R77.
   PubMed Web of Science ®Google Scholar
• Tseng LM, Huang TT, Huang CT, et al. Combination of palbociclib with enzalutamide shows in vitro activity in RB- proficient and androgen receptor-positive triple-negative breast cancer cells (abstract). PLoS One. 2017;12(12):e0189007.
   Web of Science ®Google Scholar
• Clark AS, McAndrew NP, Troxel A. Combination paclitaxel and palbociclib: results of a phase i trial in advanced breast cancer. Clin Cancer Res. 2019;25(7):2072–2079.
   PubMed Web of Science ®Google Scholar