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Molecular Cancer Therapeutics
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Small Molecule Therapeutics

Aurora A–Selective Inhibitor LY3295668 Leads to Dominant Mitotic Arrest, Apoptosis in Cancer Cells, and Shows Potent Preclinical Antitumor Efficacy

Jian Du, Lei Yan, Raquel Torres, Xueqian Gong, Huimin Bian, Carlos Marugán, Karsten Boehnke, Carmen Baquero, Yu-Hua Hui, Sonya C. Chapman, Yanzhu Yang, Yi Zeng, Sarah M. Bogner, Robert T. Foreman, Andrew Capen, Gregory P. Donoho, Robert D. Van Horn, Darlene S. Barnard, Jack A. Dempsey, Richard P. Beckmann, Mark S. Marshall, Li-Chun Chio, Yuewei Qian, Yue W. Webster, Amit Aggarwal, Shaoyou Chu, Shobha Bhattachar, Louis F. Stancato, Michele S. Dowless, Phillip W. Iversen, Jason R. Manro, Jennie L. Walgren, Bartley W. Halstead, Matthew Z. Dieter, Ricardo Martinez, Shripad V. Bhagwat, Emiko L. Kreklau, Maria Jose Lallena, Xiang S. Ye, Bharvin K.R. Patel, Christoph Reinhard, Gregory D. Plowman, David A. Barda, James R. Henry, Sean G. Buchanan and Robert M. Campbell
Jian Du
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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  • For correspondence: du_jian@lilly.com
Lei Yan
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Raquel Torres
2Eli Lilly and Company, Alcobendas (Madrid), Spain.
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Xueqian Gong
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Huimin Bian
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Carlos Marugán
2Eli Lilly and Company, Alcobendas (Madrid), Spain.
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Karsten Boehnke
2Eli Lilly and Company, Alcobendas (Madrid), Spain.
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Carmen Baquero
2Eli Lilly and Company, Alcobendas (Madrid), Spain.
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Yu-Hua Hui
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Sonya C. Chapman
3Eli Lilly and Company, Windlesham, United Kingdom.
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Yanzhu Yang
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Yi Zeng
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Sarah M. Bogner
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Robert T. Foreman
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Andrew Capen
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Gregory P. Donoho
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Robert D. Van Horn
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Darlene S. Barnard
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Jack A. Dempsey
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Richard P. Beckmann
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Mark S. Marshall
4Ped-Hematology/Oncology, Indiana University School of Medicine, Indianapolis, Indiana.
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Li-Chun Chio
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Yuewei Qian
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Yue W. Webster
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Amit Aggarwal
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Shaoyou Chu
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Shobha Bhattachar
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Louis F. Stancato
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Michele S. Dowless
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Phillip W. Iversen
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Jason R. Manro
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Jennie L. Walgren
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Bartley W. Halstead
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Matthew Z. Dieter
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Ricardo Martinez
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Shripad V. Bhagwat
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Emiko L. Kreklau
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Maria Jose Lallena
2Eli Lilly and Company, Alcobendas (Madrid), Spain.
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Xiang S. Ye
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Bharvin K.R. Patel
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Christoph Reinhard
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Gregory D. Plowman
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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David A. Barda
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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James R. Henry
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Sean G. Buchanan
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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Robert M. Campbell
1Lilly Research Laboratories, Eli Lilly and Company, Indianapolis, Indiana.
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DOI: 10.1158/1535-7163.MCT-18-0529 Published December 2019
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    Figure 1.

    LY3295668 is a potent and highly selective Aurora A (AurA) inhibitor. A, LY3295668 chemical structure. B, Kinase binding profile from DiscoverX. All kinases with IC50 less than 0.1 μmol/L are listed. C, LY3295668 dose–response curves on Aurora A, Aurora B enzymatic (left), cell (middle) inhibitions, and mitotic phenotypic (right) profile. Enzymatically, Aurora A inhibition IC50 = 0.00112 ± 0.000148 μmol/L (n = 4, Embedded Image); Aurora B (AurB) IC50 1.51 ± 0.668 μmol/L (n = 5, Embedded Image). In cells, Aurora A inhibition IC50 = 0.00059 ± 0.000784 μmol/L (n = 4, Embedded Image); IC90 of 0.00623 ± 0.00318 μmol/L (n = 4, Embedded Image); and Aurora B inhibition IC50 = 1.42 ± 0.416 μmol/L (n = 4, Embedded Image). Mitotic index (MI; P-H3 increase) IC50 0.108 ± 0.015 μmol/L (n = 4, Embedded Image on left y-axis); G2–M arrest (4N DNA content increase) IC50 = 0.108 ± 0.027 μmol/L (n = 4, Δ on left y-axis); and cell growth inhibition IC50 = 0.053 ± 0.012 μmol/L (n = 4, Embedded Image on right y-axis). D, Multiple regression analysis for Aurora A (left), B (middle), and mitotic arrest (right) cell phenotype potency (on 448, 435, and 627 SAR cpds with available data points, respectively) with Aurora A and B enzymatic activity correlation.

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    Figure 2.

    LY3295668 selective Aurora A (AurA) inhibition leads to most significant apoptosis in HeLa cells. A, In comparison of alisertib and barasertib, LY3295668 showed the most persistent Aurora A inhibition–induced mitotic arrest. LY3295668 cell potency is listed in 1C (middle). Alisertib showed Aurora A cell IC50 0.004 ± 0.004 μmol/L (n = 5); Aurora B cell IC50 0.051 ± 0.010 μmol/L (n = 7); and mitotic index (MI; P-H3 increase) IC50 0.066 ± 0.039 μmol/L (n = 7). Barasertib exhibited Aurora A cell IC50 > 20 μmol/L; Aurora B cell IC50 0.011 ± 0.006 μmol/L (n = 11); and mitotic index (MI; P-H3 increase) IC50 = 0.022 ± 0.007 μmol/L (n = 4). B, LY3295668, alisertib and barasertib cell proliferation inhibition (left), and apoptosis induction (CASP3/7, right) in IncuCyte assay. Each square represents the cell confluency or the Caspase 3/7–positive green dot numbers (y-axis) in the cell culture well from 0 to 48 hours (x-axis). The percentage of cell growth or apoptosis-positive cell numbers is plotted below.

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    Figure 3.

    LY3295668 Aurora A (AurA) inhibition–induced mitotic arrest leads to apoptosis, not polyploidy. A, Immunofluorescent staining on mitotic spindle (β-tubulin), Aurora A, Aurora P-Thr288, histone H3 P-Ser10, and Centrin 1 localization on Hela cells treated with 1 μmol/L of LY3295668, alisertib, or barasertib for 24 hours. B, Quantification of P-Aurora A and P-H3 inhibition by the Aurora inhibitors from three repeated immunofluorescence experiments. Statistical significance is indicated by ***P < 0.001. C, Western blot analysis on mitotic and apoptosis markers with HeLa cells treated by indicated Aurora inhibitors for 24 (left) and 48 (right) hours. D, Western blot analysis on mesenchymal marker E-cadherin and stemness marker Sox2 in NCI-H358 cells. E, DNA histogram by flow cytometry on mitotic arrest and tetraploidy induction from indicated Aurora inhibitor treatment. HeLa cells were treated with 1 μmol/L of each compound for 24 (top) or 48 (bottom) hours.

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    Figure 4.

    LY3295668 shows potent cell viability inhibition in a large panel of cancer cells. A, Waterfall plot of LY3295668 cell viability inhibition potency log(IC50). The cell lines are indicated at the bottom of the plot. B, LY3295668 cell viability inhibition potency log(IC50) in breast cancer cell line subpanel. C, LY3295668 log(IC50) in lung cancer cell line subpanel. The cells at exponent growth phase were treated with LY3295668 for two doubling times and the cell viability inhibition was measured by CellTiter Glo assay.

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    Figure 5.

    LY3295668 inhibits Aurora A in vivo. A, In mouse and rat NCI-H446 xenograft models, animals were treated with LY3295668 at indicated doses for 3 hours. Aurora A P-Thr288 inhibition in tumors (Embedded Image y-axis at left) and compound exposure in animal plasma (Embedded Image y-axis on right) were measured. B, Animals were treated with LY3295668 once. At indicated time points, tumor and plasma samples were collected for Aurora A P-Thr288, P-H3 (Embedded Image and Embedded Image, y-axis on left), and compound exposure (Embedded Image y-axis on right). TED50, threshold effective dose (dose that produces an effect that equals to 50% P-Aurora A inhibition). TEC50, threshold effective concentration (plasma concentration that produces an effect that equals to 50% P-Aurora A inhibition).

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    Figure 6.

    LY3295668 is efficacious in preclinical tumor models. A, LY3295668 was dosed at indicated doses and durations with NCI-H446 (left) and NCI-H69 (middle and right) models. The dosing durations for each treatment is indicated by the red line (left) and lines color coded to match the dosing schedules (middle and right). At the indicated time (red arrow), the average tumor growth inhibitions for each treatment group are plotted in the insert. B, LY3295668 efficacy with SCLC PDX models. LY3295668 was dosed at 50 mg/kg by orally twice a day for 28 days, whereas the standard-of-care was dosed with etoposide 30 mg/kg subcutaneously Q7D×4 (every 7 days for four times) plus cisplatin 3.2 mg/kg s.c. Q7D×4. The dosing duration is indicated by the red line. C, LY3295668 in combination with SoC showed better efficacy in SCLC PDX and head and neck xenograft models. For LXFS 2156 and 573 SCLC PDX models, LY3295668 was dosed at 40 mg/kg orally for 28 days. Standard of care was etoposide at 30 mg/kg s.c. Q7D×3 (every 7 days for three times) plus cisplatin 3.2 mg/kg s.c. Q7D×3. For Detroit 562 xenograft model, LY3295668 was dose at 30 mg/kg orally twice a day for 28 days. Cisplatin was used at 4 mg/kg Q7D×4 and cetuximab was at 20 mg/kg twice a week ×4. The dosing duration is indicated by the red line. The insert plot of tumor response rates at the measured time point are indicated by the red arrow, and the statistical significance is indicated by the P value.

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Molecular Cancer Therapeutics: 18 (12)
December 2019
Volume 18, Issue 12
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Aurora A–Selective Inhibitor LY3295668 Leads to Dominant Mitotic Arrest, Apoptosis in Cancer Cells, and Shows Potent Preclinical Antitumor Efficacy
Jian Du, Lei Yan, Raquel Torres, Xueqian Gong, Huimin Bian, Carlos Marugán, Karsten Boehnke, Carmen Baquero, Yu-Hua Hui, Sonya C. Chapman, Yanzhu Yang, Yi Zeng, Sarah M. Bogner, Robert T. Foreman, Andrew Capen, Gregory P. Donoho, Robert D. Van Horn, Darlene S. Barnard, Jack A. Dempsey, Richard P. Beckmann, Mark S. Marshall, Li-Chun Chio, Yuewei Qian, Yue W. Webster, Amit Aggarwal, Shaoyou Chu, Shobha Bhattachar, Louis F. Stancato, Michele S. Dowless, Phillip W. Iversen, Jason R. Manro, Jennie L. Walgren, Bartley W. Halstead, Matthew Z. Dieter, Ricardo Martinez, Shripad V. Bhagwat, Emiko L. Kreklau, Maria Jose Lallena, Xiang S. Ye, Bharvin K.R. Patel, Christoph Reinhard, Gregory D. Plowman, David A. Barda, James R. Henry, Sean G. Buchanan and Robert M. Campbell
Mol Cancer Ther December 1 2019 (18) (12) 2207-2219; DOI: 10.1158/1535-7163.MCT-18-0529

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Aurora A–Selective Inhibitor LY3295668 Leads to Dominant Mitotic Arrest, Apoptosis in Cancer Cells, and Shows Potent Preclinical Antitumor Efficacy
Jian Du, Lei Yan, Raquel Torres, Xueqian Gong, Huimin Bian, Carlos Marugán, Karsten Boehnke, Carmen Baquero, Yu-Hua Hui, Sonya C. Chapman, Yanzhu Yang, Yi Zeng, Sarah M. Bogner, Robert T. Foreman, Andrew Capen, Gregory P. Donoho, Robert D. Van Horn, Darlene S. Barnard, Jack A. Dempsey, Richard P. Beckmann, Mark S. Marshall, Li-Chun Chio, Yuewei Qian, Yue W. Webster, Amit Aggarwal, Shaoyou Chu, Shobha Bhattachar, Louis F. Stancato, Michele S. Dowless, Phillip W. Iversen, Jason R. Manro, Jennie L. Walgren, Bartley W. Halstead, Matthew Z. Dieter, Ricardo Martinez, Shripad V. Bhagwat, Emiko L. Kreklau, Maria Jose Lallena, Xiang S. Ye, Bharvin K.R. Patel, Christoph Reinhard, Gregory D. Plowman, David A. Barda, James R. Henry, Sean G. Buchanan and Robert M. Campbell
Mol Cancer Ther December 1 2019 (18) (12) 2207-2219; DOI: 10.1158/1535-7163.MCT-18-0529
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