Innovations in Ovarian Cancer Research
A newly formed Ovarian Cancer Innovations Group, envisioned by Saketh Guntupalli, MD, and led by Kian Behbakht, MD, MBA, ...
Benjamin Bitler
“The first prong is looking to determine biomarkers that can be used for early detection,” says CU Cancer Center member <anchor>Benjamin Bitler</anchor>, PhD, an associate professor of reproductive sciences and the D. Thomas and Kay L. Dunton Endowed Chair in Ovarian Cancer Research. “For that effort, we’re leveraging one of the unique resources we have at the CU Cancer Center, which is a gynecologic tumor and fluid bank. This bank has been in existence for more than 15 years, and we have over 1,300 patients on it. This database allows us to ask questions about prevention and early detection in a very translational and real way.”
Faculty Profile | School of Medicine | University of Colorado Denver
# Benjamin Bitler, PhD  Associate Professor, OB-GYN-Basic Repro Science

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#### Publications

- Callaway CS, Mouchantat LM, Bitler BG, Bonetto A. Mechanisms of Ovarian Cancer-Associated Cachexia. Endocrinology. 2023 Nov 19. [Epub ahead of print] PubMed PMID: 37980602

- Seal S, Bitler BG, Ghosh D. SMASH: Scalable Method for Analyzing Spatial Heterogeneity of genes in spatial transcriptomics data. PLoS Genet. 2023 Oct;19(10):e1010983. PubMed PMID: 37862362

- Ahmadian M, Rickert C, Minic A, Wrobel J, Bitler BG, Xing F, Angelo M, Hsieh EWY, Ghosh D, Jordan KR. A platform-independent framework for phenotyping of multiplex tissue imaging data. PLoS Comput Biol. 2023 Sep;19(9):e1011432. PubMed PMID: 37733781

- Bitler BG, Bailey CA, Yamamoto TM, McMellen A, Kim H, Watson ZL. Targeting BRPF3 moderately reverses olaparib resistance in high grade serous ovarian carcinoma. Mol Carcinog. 2023 Nov;62(11):1717-1730. PubMed PMID: 37493106

- Brubaker LW, Backos DS, Nguyen VT, Reigan P, Yamamoto TM, Woodruff ER, Iwanaga R, Wempe MF, Kumar V, Persenaire C, Watson ZL, Bitler BG. Novel chromobox 2 inhibitory peptide decreases tumor progression. Expert Opin Ther Targets. 2023 Apr-May;27(4-5):361-371. PubMed PMID: 37243607

- Johnson J, Kim SY, Sam PK, Asokan R, Cari EL, Bales ES, Luu TH, Perez L, Kallen AN, Nel-Themaat L, Polotsky AJ, Post MD, Orlicky DJ, Jordan KR, Bitler BG. Expression and T cell regulatory action of the PD-1 immune checkpoint in the ovary and fallopian tube. Am J Reprod Immunol. 2023 Mar;89(3):e13649. PubMed PMID: 36394352

- Haag JG, Wolsky RJ, Moroney MR, Sheren J, Sheeder J, Bitler BG, Corr BR. Clinicopathologic Evaluation of CTNNB1 Mutations in High-Intermediate Risk Endometrial Endometrioid Carcinoma. Int J Gynecol Pathol. 2023 Jan 1;42(1):43-53. PubMed PMID: 35283443

- Holmberg R, Robinson M, Gilbert SF, Lujano-Olazaba O, Waters JA, Kogan E, Velasquez CLR, Stevenson D, Cruz LS, Alexander LJ, Lara J, Mu EM, Camillo JR, Bitler BG, Huxford T, House CD. TWEAK-Fn14-RelB Signaling Cascade Promotes Stem Cell-like Features that Contribute to Post-Chemotherapy Ovarian Cancer Relapse. Mol Cancer Res. 2023 Feb 1;21(2):170-186. PubMed PMID: 36214671

- McMellen A, Yamamoto TM, Qamar L, Sanders BE, Nguyen LL, Ortiz Chavez D, Bapat J, Berning A, Post MD, Johnson J, Behbakht K, Nurmemmedov E, Chuong EB, Bitler BG. ATF6-Mediated Signaling Contributes to PARP Inhibitor Resistance in Ovarian Cancer. Mol Cancer Res. 2023 Jan 3;21(1):3-13. PubMed PMID: 36149636

- Bapat J, Yamamoto TM, Woodruff ER, Qamar L, Mikeska RG, Aird KM, Watson ZL, Brubaker LW, Bitler BG. CASC4/GOLM2 drives high grade serous carcinoma anoikis resistance through the recycling of EGFR. Cancer Gene Ther. 2023 Nov 29. [Epub ahead of print] PubMed PMID: 38030811

- Pasquesi GIM, Allen H, Ivancevic A, Barbachano-Guerrero A, Joyner O, Guo K, Simpson DM, Gapin K, Horton I, Nguyen L, Yang Q, Warren CJ, Florea LD, Bitler BG, Santiago ML, Sawyer SL, Chuong EB. Regulation of human interferon signaling by transposon exonization. bioRxiv. 2023 Sep 15. PubMed PMID: 37745311

- Corr BR, Moroney MR, Woodruff E, Watson ZL, Jordan KR, Danhorn T, Bailey C, Wolsky RJ, Bitler BG. Combination CDC-like kinase inhibition (CLK)/Dual-specificity tyrosine-regulated kinase (DYRK) and taxane therapy in CTNNB1-mutated endometrial cancer. bioRxiv. 2023 Apr 6. PubMed PMID: 37066339

- Nguyen LL, Watson ZL, Ortega R, Woodruff ER, Jordan KR, Iwanaga R, Yamamoto TM, Bailey CA, Jeong AD, Guntupalli SR, Behbakht K, Gbaja V, Arnoult N, Chuong EB, Bitler BG. Combinatory EHMT and PARP inhibition induces an interferon response and a CD8 T cell-dependent tumor regression in PARP inhibitor-resistant models. bioRxiv. 2023 Feb 23. PubMed PMID: 36865165

- Sanders BE, Wolsky R, Doughty ES, Wells KL, Ghosh D, Ku L, Pressey JG, Bitler BB, Brubaker LW. Small cell carcinoma of the ovary hypercalcemic type (SCCOHT): A review and novel case with dual germline SMARCA4 and BRCA2 mutations. Gynecol Oncol Rep. 2022 Dec;44:101077. PubMed PMID: 36249907

- Neville MC, Webb PG, Baumgartner HK, Bitler BG. Claudin-4 localization in epithelial ovarian cancer. Heliyon. 2022 Oct;8(10):e10862. PubMed PMID: 36237976

- Huang TT, Burkett SS, Tandon M, Yamamoto TM, Gupta N, Bitler BG, Lee JM, Nair JR. Distinct roles of treatment schemes and BRCA2 on the restoration of homologous recombination DNA repair and PARP inhibitor resistance in ovarian cancer. Oncogene. 2022 Nov;41(46):5020-5031. PubMed PMID: 36224341

- Holmberg R, Robinson M, Gilbert SF, Lujano-Olazaba O, Waters JA, Kogan E, Velasquez CLR, Stevenson D, Cruz LS, Alexander LJ, Lara J, Mu EM, Camillo JR, Bitler BG, Huxford T, House CD. TWEAK-Fn14-RelB signaling cascade promotes stem cell-like features that contribute to post-chemotherapy ovarian cancer relapse. Mol Cancer Res. 2022 Oct 10. [Epub ahead of print] PubMed PMID: 36214671

- McMellen A, Yamamoto TM, Qamar L, Sanders BE, Nguyen LL, Ortiz Chavez D, Bapat J, Berning A, Post MD, Johnson J, Behbakht K, Nurmemmedov E, Chuong EB, Bitler BG. ATF6-mediated signaling contributes to PARP Inhibitor Resistance in Ovarian Cancer. Mol Cancer Res. 2022 Sep 23. [Epub ahead of print] PubMed PMID: 36149636

- Liu H, Lin J, Zhou W, Moses R, Dai Z, Kossenkov AV, Drapkin R, Bitler BG, Karakashev S, Zhang R. KDM5A Inhibits Antitumor Immune Responses Through Downregulation of the Antigen-Presentation Pathway in Ovarian Cancer. Cancer Immunol Res. 2022 Aug 3;10(8):1028-1038. PubMed PMID: 35726891

- Seal S, Wrobel J, Johnson AM, Nemenoff RA, Schenk EL, Bitler BG, Jordan KR, Ghosh D. On clustering for cell-phenotyping in multiplex immunohistochemistry (mIHC) and multiplexed ion beam imaging (MIBI) data. BMC Res Notes. 2022 Jun 20;15(1):215. PubMed PMID: 35725622

- Vu T, Wrobel J, Bitler BG, Schenk EL, Jordan KR, Ghosh D. SPF: A spatial and functional data analytic approach to cell imaging data. PLoS Comput Biol. 2022 Jun;18(6):e1009486. PubMed PMID: 35704658

- Sanders BE, Yamamoto TM, McMellen A, Woodruff ER, Berning A, Post MD, Bitler BG. Targeting DUSP Activity as a Treatment for High-Grade Serous Ovarian Carcinoma. Mol Cancer Ther. 2022 Aug 2;21(8):1285-1295. PubMed PMID: 35587258

- Yamamoto TM, Webb PG, Davis DM, Baumgartner HK, Woodruff ER, Guntupalli SR, Neville M, Behbakht K, Bitler BG. Loss of Claudin-4 Reduces DNA Damage Repair and Increases Sensitivity to PARP Inhibitors. Mol Cancer Ther. 2022 Apr 1;21(4):647-657. PubMed PMID: 35373300

- Haag JG, Wolsky RJ, Moroney MR, Sheren J, Sheeder J, Bitler BG, Corr BR. Clinicopathologic Evaluation of CTNNB1 Mutations in High-Intermediate Risk Endometrial Endometrioid Carcinoma. Int J Gynecol Pathol. 2022 Mar 14. [Epub ahead of print] PubMed PMID: 35283443

- Johnson J, Kim SY, Sam PK, Asokan R, Cari EL, Bales ES, Luu TH, Perez L, Kallen AN, Nel-Themaat L, Polotsky AJ, Post MD, Orlicky DJ, Jordan KR, Bitler BG. Expression and T cell Regulatory Action of the PD-1 Immune Checkpoint in the Ovary and Fallopian Tube. Am J Reprod Immunol. 2022 Nov 17. [Epub ahead of print] PubMed PMID: 36394352

- Sanders BE, Wolsky R, Doughty ES, Wells KL, Ghosh D, Ku L, Pressey JG, Bitler BB, Brubaker LW. Small cell carcinoma of the ovary hypercalcemic type (SCCOHT): A review and novel case with dual germline SMARCA4 and BRCA2 mutations. Gynecol Oncol Rep. 2022 Dec;44:101077. PubMed PMID: 36249907

- Moroney MR, Woodruff E, Qamar L, Bradford AP, Wolsky R, Bitler BG, Corr BR. Inhibiting Wnt/beta-catenin in CTNNB1-mutated endometrial cancer. Mol Carcinog. 2021 Aug;60(8):511-523. PubMed PMID: 34038589

- Clauset A, Behbakht K, Bitler BG. Decoding the dynamic tumor microenvironment. Sci Adv. 2021 Jun;7(23). PubMed PMID: 34088677

- Sanders BE, Ku L, Walker P, Bitler BG. Assessing Genetic Variants in Matched Biocompartments From Patients With Serous Ovarian Cancer. Technol Cancer Res Treat. 2021 Jan-Dec;20:15330338211027917. PubMed PMID: 34169762

- Llerena Cari E, Hagen-Lillevik S, Giornazi A, Post M, Komar AA, Appiah L, Bitler B, Polotsky AJ, Santoro N, Kieft J, Lai K, Johnson J. Integrated stress response control of granulosa cell translation and proliferation during normal ovarian follicle development. Mol Hum Reprod. 2021 Aug 7;27(8). PubMed PMID: 34314477

- Steinhart B, Jordan KR, Bapat J, Post MD, Brubaker LW, Bitler BG, Wrobel J. The Spatial Context of Tumor-Infiltrating Immune Cells Associates with Improved Ovarian Cancer Survival. Mol Cancer Res. 2021 Dec;19(12):1973-1979. PubMed PMID: 34615692

- Lin J, Guo D, Liu H, Zhou W, Wang C, Müller I, Kossenkov AV, Drapkin R, Bitler BG, Helin K, Zhang R. The SETDB1-TRIM28 Complex Suppresses Antitumor Immunity. Cancer Immunol Res. 2021 Dec;9(12):1413-1424. PubMed PMID: 34848497

- Bapat J and Bitler BG. (2021). Chapter: The intersection of anoikis resistance and fatty acid metabolism in cancer. Book - Anoikis - How the extracellular matrix regulates life-or-death decisions. Editor, Frisch S. Publisher, Springer Nature Switzerland AG.

- Jordan KR, Sikora MJ, Slansky JE, Minic A, Richer JK, Moroney MR, Hu J, Wolsky RJ, Watson ZL, Yamamoto TM, Costello JC, Clauset A, Behbakht K, Kumar TR, Bitler BG. The Capacity of the Ovarian Cancer Tumor Microenvironment to Integrate Inflammation Signaling Conveys a Shorter Disease-free Interval. Clin Cancer Res. 2020 Dec 1;26(23):6362-6373. PubMed PMID: 32928797

- McMellen A, Woodruff ER, Corr BR, Bitler BG, Moroney MR. Wnt Signaling in Gynecologic Malignancies. Int J Mol Sci. 2020 Jun 16;21(12). PubMed PMID: 32560059

- Sawyer BT, Qamar L, Yamamoto TM, McMellen A, Watson ZL, Richer JK, Behbakht K, Schlaepfer IR, Bitler BG. Targeting Fatty Acid Oxidation to Promote Anoikis and Inhibit Ovarian Cancer Progression. Mol Cancer Res. 2020 Jul;18(7):1088-1098. PubMed PMID: 32198139

- Li J, Wang W, Zhang Y, Cieslik M, Guo J, Tan M, Green MD, Wang W, Lin H, Li W, Wei S, Zhou J, Li G, Jing X, Vatan L, Zhao L, Bitler B, Zhang R, Cho KR, Dou Y, Kryczek I, Chan TA, Huntsman D, Chinnaiyan AM, Zou W. Epigenetic driver mutations in ARID1A shape cancer immune phenotype and immunotherapy. J Clin Invest. 2020 May 1;130(5):2712-2726. PubMed PMID: 32027624

- Watson ZL, Yamamoto TM, McMellen A, Kim H, Hughes CJ, Wheeler LJ, Post MD, Behbakht K, Bitler BG. Histone methyltransferases EHMT1 and EHMT2 (GLP/G9A) maintain PARP inhibitor resistance in high-grade serous ovarian carcinoma. Clin Epigenetics. 2019 Nov 27;11(1):165. PubMed PMID: 31775874

- Rao DM, Shackleford MT, Bordeaux EK, Sottnik JL, Ferguson RL, Yamamoto TM, Wellberg EA, Bitler BG, Sikora MJ. Wnt family member 4 (WNT4) and WNT3A activate cell-autonomous Wnt signaling independent of porcupine O-acyltransferase or Wnt secretion. J Biol Chem. 2019 Nov 18. [Epub ahead of print] PubMed PMID: 31740580

- Smith LP, Bitler BG, Richer JK, Christenson JL. Tryptophan catabolism in epithelial ovarian carcinoma. Trends Cancer Res. 2019;14:1-9. PubMed PMID: 31736606

- Park PH, Yamamoto TM, Li H, Alcivar AL, Xia B, Wang Y, Bernhardy AJ, Turner KM, Kossenkov AV, Watson ZL, Behbakht K, Casadei S, Swisher EM, Mischel PS, Johnson N, Bitler BG. Amplification of the mutation-carrying BRCA2 allele promotes RAD51 loading and PARP inhibitor resistance in the absence of reversion mutations. Mol Cancer Ther. 2019 Oct 1. [Epub ahead of print] PubMed PMID: 31575654

- Wheeler LJ, Watson ZL, Qamar L, Yamamoto TM, Sawyer BT, Sullivan KD, Khanal S, Joshi M, Ferchaud-Roucher V, Smith H, Vanderlinden LA, Brubaker SW, Caino CM, Kim H, Espinosa JM, Richer JK, Bitler BG. Multi-Omic Approaches Identify Metabolic and Autophagy Regulators Important in Ovarian Cancer Dissemination. iScience. 2019 Sep 27;19:474-491. PubMed PMID: 31437751

- Ramzan AA, Bitler BG, Hicks D, Barner K, Qamar L, Behbakht K, Powell T, Jansson T, Wilson H. Adiponectin receptor agonist AdipoRon induces apoptotic cell death and suppresses proliferation in human ovarian cancer cells. Mol Cell Biochem. 2019 Nov;461(1-2):37-46. PubMed PMID: 31292831

- Yamamoto TM, McMellen A, Watson ZL, Aguilera J, Ferguson R, Nurmemmedov E, Thakar T, Moldovan GL, Kim H, Cittelly DM, Joglar AM, Brennecke EP, Wilson H, Behbakht K, Sikora MJ, Bitler BG. Activation of Wnt signaling promotes olaparib resistant ovarian cancer. Mol Carcinog. 2019 Oct;58(10):1770-1782. PubMed PMID: 31219654

- Dahl ES, Buj R, Leon KE, Newell JM, Imamura Y, Bitler BG, Snyder NW, Aird KM. Targeting IDH1 as a Prosenescent Therapy in High-grade Serous Ovarian Cancer. Mol Cancer Res. 2019 Aug;17(8):1710-1720. PubMed PMID: 31110157

- Breed C, Hicks DA, Webb PG, Galimanis CE, Bitler BG, Behbakht K, Baumgartner HK. Ovarian Tumor Cell Expression of Claudin-4 Reduces Apoptotic Response to Paclitaxel. Mol Cancer Res. 2019 Mar;17(3):741-750. PubMed PMID: 30606772

- Watson ZL, Bitler BG. Type I Protein Arginine Methyltransferases Overexpression Promotes Transformation and Potentiates Her2/Neu-Driven Tumorigenesis. Cancer Res. 2019 Jan 1;79(1):3-4. PubMed PMID: 30602621

- Wheeler LJ, Watson ZL, Qamar L, Yamamoto TM, Post MD, Berning AA, Spillman MA, Behbakht K, Bitler BG. CBX2 identified as driver of anoikis escape and dissemination in high grade serous ovarian cancer. Oncogenesis. 2018 Nov 26;7(11):92. PubMed PMID: 30478317

- Wu S, Fatkhutdinov N, Fukumoto T, Bitler BG, Park PH, Kossenkov AV, Trizzino M, Tang HY, Zhang L, Gardini A, Speicher DW, Zhang R. SWI/SNF catalytic subunits' switch drives resistance to EZH2 inhibitors in ARID1A-mutated cells. Nat Commun. 2018 Oct 8;9(1):4116. PubMed PMID: 30297712

- Gordon MA, Babbs B, Cochrane DR, Bitler BG, Richer JK. The long non-coding RNA MALAT1 promotes ovarian cancer progression by regulating RBFOX2-mediated alternative splicing. Mol Carcinog. 2018 Oct 8. [Epub ahead of print] PubMed PMID: 30294913

- Singha B, Harper SL, Goldman AR, Bitler BG, Aird KM, Borowsky ME, Cadungog MG, Liu Q, Zhang R, Jean S, Drapkin R, Speicher DW. CLIC1 and CLIC4 complement CA125 as a diagnostic biomarker panel for all subtypes of epithelial ovarian cancer. Sci Rep. 2018 Oct 3;8(1):14725. PubMed PMID: 30282979

- Fukumoto T, Park PH, Wu S, Fatkhutdinov N, Karakashev S, Nacarelli T, Kossenkov AV, Speicher DW, Jean S, Zhang L, Wang TL, Shih IM, Conejo-Garcia JR, Bitler BG, Zhang R. Repurposing Pan-HDAC Inhibitors for ARID1A-Mutated Ovarian Cancer. Cell Rep. 2018 Mar 27;22(13):3393-3400. PubMed PMID: 29590609

- Karakashev S, Zhu H, Wu S, Yokoyama Y, Bitler BG, Park PH, Lee JH, Kossenkov AV, Gaonkar KS, Yan H, Drapkin R, Conejo-Garcia JR, Speicher DW, Ordog T, Zhang R. CARM1-expressing ovarian cancer depends on the histone methyltransferase EZH2 activity. Nat Commun. 2018 Feb 12;9(1):631. PubMed PMID: 29434212

- Karakashev S, Zhu H, Yokoyama Y, Zhao B, Fatkhutdinov N, Kossenkov AV, Wilson AJ, Simpkins F, Speicher D, Khabele D, Bitler BG, Zhang R. BET Bromodomain Inhibition Synergizes with PARP Inhibitor in Epithelial Ovarian Cancer. Cell Rep. 2017 Dec 19;21(12):3398-3405. PubMed PMID: 29262321

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