Literature DB >> 24085845

Stabilization of mutant BRCA1 protein confers PARP inhibitor and platinum resistance.

Neil Johnson1, Shawn F Johnson, Wei Yao, Yu-Chen Li, Young-Eun Choi, Andrea J Bernhardy, Yifan Wang, Marzia Capelletti, Kristopher A Sarosiek, Lisa A Moreau, Dipanjan Chowdhury, Anneka Wickramanayake, Maria I Harrell, Joyce F Liu, Alan D D'Andrea, Alexander Miron, Elizabeth M Swisher, Geoffrey I Shapiro.   

Abstract

Breast Cancer Type 1 Susceptibility Protein (BRCA1)-deficient cells have compromised DNA repair and are sensitive to poly(ADP-ribose) polymerase (PARP) inhibitors. Despite initial responses, the development of resistance limits clinical efficacy. Mutations in the BRCA C-terminal (BRCT) domain of BRCA1 frequently create protein products unable to fold that are subject to protease-mediated degradation. Here, we show HSP90-mediated stabilization of a BRCT domain mutant BRCA1 protein under PARP inhibitor selection pressure. The stabilized mutant BRCA1 protein interacted with PALB2-BRCA2-RAD51, was essential for RAD51 focus formation, and conferred PARP inhibitor as well as cisplatin resistance. Treatment of resistant cells with the HSP90 inhibitor 17-dimethylaminoethylamino-17-demethoxygeldanamycin reduced mutant BRCA1 protein levels and restored their sensitivity to PARP inhibition. Resistant cells also acquired a TP53BP1 mutation that facilitated DNA end resection in the absence of a BRCA1 protein capable of binding CtIP. Finally, concomitant increased mutant BRCA1 and decreased 53BP1 protein expression occur in clinical samples of BRCA1-mutated recurrent ovarian carcinomas that have developed resistance to platinum. These results provide evidence for a two-event mechanism by which BRCA1-mutant tumors acquire anticancer therapy resistance.

Entities:  

Keywords:  cancer therapy; homologous recombination

Mesh:

Substances:

Year:  2013        PMID: 24085845      PMCID: PMC3801063          DOI: 10.1073/pnas.1305170110

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  24 in total

1.  BRCA1 mutation analysis of 41 human breast cancer cell lines reveals three new deleterious mutants.

Authors:  Fons Elstrodt; Antoinette Hollestelle; Jord H A Nagel; Michael Gorin; Marijke Wasielewski; Ans van den Ouweland; Sofia D Merajver; Stephen P Ethier; Mieke Schutte
Journal:  Cancer Res       Date:  2006-01-01       Impact factor: 12.701

2.  Human CtIP promotes DNA end resection.

Authors:  Alessandro A Sartori; Claudia Lukas; Julia Coates; Martin Mistrik; Shuang Fu; Jiri Bartek; Richard Baer; Jiri Lukas; Stephen P Jackson
Journal:  Nature       Date:  2007-10-28       Impact factor: 49.962

3.  PALB2 is an integral component of the BRCA complex required for homologous recombination repair.

Authors:  Shirley M H Sy; Michael S Y Huen; Junjie Chen
Journal:  Proc Natl Acad Sci U S A       Date:  2009-04-15       Impact factor: 11.205

Review 4.  HSP90 and the chaperoning of cancer.

Authors:  Luke Whitesell; Susan L Lindquist
Journal:  Nat Rev Cancer       Date:  2005-10       Impact factor: 60.716

5.  Structural consequences of a cancer-causing BRCA1-BRCT missense mutation.

Authors:  R Scott Williams; J N Mark Glover
Journal:  J Biol Chem       Date:  2002-11-08       Impact factor: 5.157

6.  Association of BRCA1 with Rad51 in mitotic and meiotic cells.

Authors:  R Scully; J Chen; A Plug; Y Xiao; D Weaver; J Feunteun; T Ashley; D M Livingston
Journal:  Cell       Date:  1997-01-24       Impact factor: 41.582

7.  Secondary BRCA1 mutations in BRCA1-mutated ovarian carcinomas with platinum resistance.

Authors:  Elizabeth M Swisher; Wataru Sakai; Beth Y Karlan; Kaitlyn Wurz; Nicole Urban; Toshiyasu Taniguchi
Journal:  Cancer Res       Date:  2008-04-15       Impact factor: 12.701

8.  Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors.

Authors:  Janneke E Jaspers; Ariena Kersbergen; Ute Boon; Wendy Sol; Liesbeth van Deemter; Serge A Zander; Rinske Drost; Ellen Wientjens; Jiuping Ji; Amal Aly; James H Doroshow; Aaron Cranston; Niall M B Martin; Alan Lau; Mark J O'Connor; Shridar Ganesan; Piet Borst; Jos Jonkers; Sven Rottenberg
Journal:  Cancer Discov       Date:  2012-10-25       Impact factor: 39.397

9.  Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy.

Authors:  Hannah Farmer; Nuala McCabe; Christopher J Lord; Andrew N J Tutt; Damian A Johnson; Tobias B Richardson; Manuela Santarosa; Krystyna J Dillon; Ian Hickson; Charlotte Knights; Niall M B Martin; Stephen P Jackson; Graeme C M Smith; Alan Ashworth
Journal:  Nature       Date:  2005-04-14       Impact factor: 69.504

Review 10.  The role of BRCA1 in the cellular response to chemotherapy.

Authors:  Richard D Kennedy; Jennifer E Quinn; Paul B Mullan; Patrick G Johnston; D Paul Harkin
Journal:  J Natl Cancer Inst       Date:  2004-11-17       Impact factor: 13.506

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  103 in total

1.  Olaparib monotherapy in patients with advanced cancer and a germline BRCA1/2 mutation.

Authors:  Bella Kaufman; Ronnie Shapira-Frommer; Rita K Schmutzler; M William Audeh; Michael Friedlander; Judith Balmaña; Gillian Mitchell; Georgeta Fried; Salomon M Stemmer; Ayala Hubert; Ora Rosengarten; Mariana Steiner; Niklas Loman; Karin Bowen; Anitra Fielding; Susan M Domchek
Journal:  J Clin Oncol       Date:  2014-11-03       Impact factor: 44.544

2.  β-hCG-induced mutant BRCA1 ignites drug resistance in susceptible breast tissue.

Authors:  Satheesh Kumar Sengodan; Sreelatha K Hemalatha; Revathy Nadhan; Thara Somanathan; Arun Peter Mathew; Arkadiusz Chil; Janusz Kopczynski; Rakesh Sathish Nair; Jerald Mahesh Kumar; Priya Srinivas
Journal:  Carcinogenesis       Date:  2019-11-25       Impact factor: 4.944

Review 3.  Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins.

Authors:  Rohit Prakash; Yu Zhang; Weiran Feng; Maria Jasin
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-04-01       Impact factor: 10.005

4.  The CHK1 Inhibitor Prexasertib Exhibits Monotherapy Activity in High-Grade Serous Ovarian Cancer Models and Sensitizes to PARP Inhibition.

Authors:  Kalindi Parmar; Bose S Kochupurakkal; Jean-Bernard Lazaro; Zhigang C Wang; Sangeetha Palakurthi; Paul T Kirschmeier; Chunyu Yang; Larissa A Sambel; Anniina Färkkilä; Elizaveta Reznichenko; Hunter D Reavis; Connor E Dunn; Lee Zou; Khanh T Do; Panagiotis A Konstantinopoulos; Ursula A Matulonis; Joyce F Liu; Alan D D'Andrea; Geoffrey I Shapiro
Journal:  Clin Cancer Res       Date:  2019-08-13       Impact factor: 12.531

5.  DYNLL1 binds to MRE11 to limit DNA end resection in BRCA1-deficient cells.

Authors:  Yizhou Joseph He; Khyati Meghani; Marie-Christine Caron; Chunyu Yang; Daryl A Ronato; Jie Bian; Anchal Sharma; Jessica Moore; Joshi Niraj; Alexandre Detappe; John G Doench; Gaelle Legube; David E Root; Alan D D'Andrea; Pascal Drané; Subhajyoti De; Panagiotis A Konstantinopoulos; Jean-Yves Masson; Dipanjan Chowdhury
Journal:  Nature       Date:  2018-10-31       Impact factor: 49.962

6.  Emerging Cancer Therapeutic Targets in Protein Homeostasis.

Authors:  Prabhakar Bastola; Derek B Oien; Megan Cooley; Jeremy Chien
Journal:  AAPS J       Date:  2018-08-27       Impact factor: 4.009

7.  Targeted blockade of HSP90 impairs DNA-damage response proteins and increases the sensitivity of ovarian carcinoma cells to PARP inhibition.

Authors:  Rashid Gabbasov; I Daniel Benrubi; Shane W O'Brien; John J Krais; Neil Johnson; Samuel Litwin; Denise C Connolly
Journal:  Cancer Biol Ther       Date:  2019-03-30       Impact factor: 4.742

8.  Reversion and non-reversion mechanisms of resistance to PARP inhibitor or platinum chemotherapy in BRCA1/2-mutant metastatic breast cancer.

Authors:  A G Waks; O Cohen; B Kochupurakkal; D Kim; C E Dunn; J Buendia Buendia; S Wander; K Helvie; M R Lloyd; L Marini; M E Hughes; S S Freeman; S P Ivy; J Geradts; S Isakoff; P LoRusso; V A Adalsteinsson; S M Tolaney; U Matulonis; I E Krop; A D D'Andrea; E P Winer; N U Lin; G I Shapiro; N Wagle
Journal:  Ann Oncol       Date:  2020-02-20       Impact factor: 32.976

9.  RING domain-deficient BRCA1 promotes PARP inhibitor and platinum resistance.

Authors:  Yifan Wang; John J Krais; Andrea J Bernhardy; Emmanuelle Nicolas; Kathy Q Cai; Maria I Harrell; Hyoung H Kim; Erin George; Elizabeth M Swisher; Fiona Simpkins; Neil Johnson
Journal:  J Clin Invest       Date:  2016-07-25       Impact factor: 14.808

Review 10.  BRCA1 Mutations in Cancer: Coordinating Deficiencies in Homologous Recombination with Tumorigenesis.

Authors:  John J Krais; Neil Johnson
Journal:  Cancer Res       Date:  2020-08-03       Impact factor: 12.701

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