Literature DB >> 27894751

Polymerase ε (POLE) ultra-mutation in uterine tumors correlates with T lymphocyte infiltration and increased resistance to platinum-based chemotherapy in vitro.

Stefania Bellone1, Eliana Bignotti2, Silvia Lonardi3, Francesca Ferrari1, Floriana Centritto1, Alice Masserdotti1, Francesca Pettinella1, Jonathan Black1, Gulden Menderes1, Gary Altwerger1, Pei Hui4, Salvatore Lopez5, Christopher de Haydu1, Elena Bonazzoli1, Federica Predolini1, Luca Zammataro1, Emiliano Cocco1, Federico Ferrari2, Antonella Ravaggi6, Chiara Romani6, Fabio Facchetti3, Enrico Sartori7, Franco E Odicino7, Dan-Arin Silasi1, Babak Litkouhi1, Elena Ratner1, Masoud Azodi1, Peter E Schwartz1, Alessandro D Santin8.   

Abstract

OBJECTIVE: Up to 12% of all endometrial-carcinomas (EC) harbor DNA-polymerase-ε-(POLE) mutations. It is currently unknown whether the favorable prognosis of POLE-mutated EC is derived from their low metastatic capability, extraordinary number of somatic mutations thus imparting immunogenicity, or a high sensitivity to chemotherapy.
METHODS: Polymerase-chain-reaction-amplification and Sanger-sequencing were used to test for POLE exonuclease-domain-mutations (exons 9-14) 131 EC. Infiltration of CD4+ and CD8+ T-lymphocytes (TIL) and PD-1-expression in POLE-mutated vs POLE wild-type EC was studied by immunohistochemistry (IHC) and the correlations between survival and molecular features were investigated. Finally, primary POLE-mutated and POLE-wild-type EC cell lines were established and compared in-vitro for their sensitivity to chemotherapy.
RESULTS: Eleven POLE-mutated EC (8.5%) were identified. POLE-mutated tumors were associated with improved progression-free-survival (P<0.05) and displayed increased numbers of CD4+ (44.5 vs 21.8; P=0.001) and CD8+ (32.8 vs 13.5; P<0.001) TILs when compared to wild-type POLE EC. PD-1 receptor was overexpressed in TILs from POLE-mutated vs wild-type-tumors (81% vs 28%; P<0.001). Primary POLE tumor cell lines were significantly more resistant to platinum-chemotherapy in-vitro when compared to POLE-wild-type tumors (P<0.004).
CONCLUSIONS: POLE ultra-mutated EC are heavily infiltrated with CD4+/CD8+ TIL, overexpress PD-1 immune-check-point (i.e., features consistent with chronic antigen-exposure), and have a better prognosis when compared to other molecular subtypes of EC patients. POLE-mutated tumor-cell lines are resistant to platinum-chemotherapy in-vitro suggesting that the better prognosis of POLE-patients is not secondary to a higher sensitivity to chemotherapy but likely linked to enhanced immunogenicity.
Copyright © 2016 Elsevier Inc. All rights reserved.

Entities:  

Keywords:  Cisplatin; Endometrial carcinoma; Polymerase ε; Uterine serous papillary cancer; Whole exome sequencing

Mesh:

Substances:

Year:  2016        PMID: 27894751      PMCID: PMC5183545          DOI: 10.1016/j.ygyno.2016.11.023

Source DB:  PubMed          Journal:  Gynecol Oncol        ISSN: 0090-8258            Impact factor:   5.482


  21 in total

Review 1.  Role of DNA mismatch repair in apoptotic responses to therapeutic agents.

Authors:  Mark Meyers; Arlene Hwang; Mark W Wagner; David A Boothman
Journal:  Environ Mol Mutagen       Date:  2004       Impact factor: 3.216

Review 2.  DNA polymerase epsilon: a polymerase of unusual size (and complexity).

Authors:  Zachary F Pursell; Thomas A Kunkel
Journal:  Prog Nucleic Acid Res Mol Biol       Date:  2008

3.  Immunology. Licence to kill.

Authors:  A Lanzavecchia
Journal:  Nature       Date:  1998-06-04       Impact factor: 49.962

4.  POLE exonuclease domain mutation predicts long progression-free survival in grade 3 endometrioid carcinoma of the endometrium.

Authors:  Bo Meng; Lien N Hoang; John B McIntyre; Máire A Duggan; Gregg S Nelson; Cheng-Han Lee; Martin Köbel
Journal:  Gynecol Oncol       Date:  2014-05-16       Impact factor: 5.482

5.  Landscape of somatic single-nucleotide and copy-number mutations in uterine serous carcinoma.

Authors:  Siming Zhao; Murim Choi; John D Overton; Stefania Bellone; Dana M Roque; Emiliano Cocco; Federica Guzzo; Diana P English; Joyce Varughese; Sara Gasparrini; Ileana Bortolomai; Natalia Buza; Pei Hui; Maysa Abu-Khalaf; Antonella Ravaggi; Eliana Bignotti; Elisabetta Bandiera; Chiara Romani; Paola Todeschini; Renata Tassi; Laura Zanotti; Luisa Carrara; Sergio Pecorelli; Dan-Arin Silasi; Elena Ratner; Masoud Azodi; Peter E Schwartz; Thomas J Rutherford; Amy L Stiegler; Shrikant Mane; Titus J Boggon; Joseph Schlessinger; Richard P Lifton; Alessandro D Santin
Journal:  Proc Natl Acad Sci U S A       Date:  2013-01-28       Impact factor: 11.205

6.  DNA polymerase epsilon and delta proofreading suppress discrete mutator and cancer phenotypes in mice.

Authors:  Tina M Albertson; Masanori Ogawa; James M Bugni; Laura E Hays; Yang Chen; Yanping Wang; Piper M Treuting; John A Heddle; Robert E Goldsby; Bradley D Preston
Journal:  Proc Natl Acad Sci U S A       Date:  2009-09-24       Impact factor: 11.205

Review 7.  A panoply of errors: polymerase proofreading domain mutations in cancer.

Authors:  Emily Rayner; Inge C van Gool; Claire Palles; Stephen E Kearsey; Tjalling Bosse; Ian Tomlinson; David N Church
Journal:  Nat Rev Cancer       Date:  2016-02       Impact factor: 60.716

8.  Induction of a CD8+ cytotoxic T lymphocyte response by cross-priming requires cognate CD4+ T cell help.

Authors:  S R Bennett; F R Carbone; F Karamalis; J F Miller; W R Heath
Journal:  J Exp Med       Date:  1997-07-07       Impact factor: 14.307

9.  Specific T helper cell requirement for optimal induction of cytotoxic T lymphocytes against major histocompatibility complex class II negative tumors.

Authors:  F Ossendorp; E Mengedé; M Camps; R Filius; C J Melief
Journal:  J Exp Med       Date:  1998-03-02       Impact factor: 14.307

10.  Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas.

Authors:  Claire Palles; Jean-Baptiste Cazier; Kimberley M Howarth; Enric Domingo; Angela M Jones; Peter Broderick; Zoe Kemp; Sarah L Spain; Estrella Guarino; Estrella Guarino Almeida; Israel Salguero; Amy Sherborne; Daniel Chubb; Luis G Carvajal-Carmona; Yusanne Ma; Kulvinder Kaur; Sara Dobbins; Ella Barclay; Maggie Gorman; Lynn Martin; Michal B Kovac; Sean Humphray; Anneke Lucassen; Christopher C Holmes; David Bentley; Peter Donnelly; Jenny Taylor; Christos Petridis; Rebecca Roylance; Elinor J Sawyer; David J Kerr; Susan Clark; Jonathan Grimes; Stephen E Kearsey; Huw J W Thomas; Gilean McVean; Richard S Houlston; Ian Tomlinson
Journal:  Nat Genet       Date:  2012-12-23       Impact factor: 38.330

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  19 in total

1.  POLE Mutation Characteristics in a Chinese Cohort with Endometrial Carcinoma.

Authors:  Yiran Li; Qizhi He; Shuangdi Li; Xiaoli Wen; Lei Ye; Kai Wang; Xiaoping Wan
Journal:  Onco Targets Ther       Date:  2020-07-28       Impact factor: 4.147

Review 2.  Immunotherapy in endometrial cancer: rationale, practice and perspectives.

Authors:  Wenyu Cao; Xinyue Ma; Jean Victoria Fischer; Chenggong Sun; Beihua Kong; Qing Zhang
Journal:  Biomark Res       Date:  2021-06-16

3.  Tumor Mutational Burden Guides Therapy in a Treatment Refractory POLE-Mutant Uterine Carcinosarcoma.

Authors:  Munveer S Bhangoo; Peter Boasberg; Pareen Mehta; Julia A Elvin; Siraj M Ali; Winnie Wu; Samuel J Klempner
Journal:  Oncologist       Date:  2018-01-31

Review 4.  Potential role of radiation therapy in augmenting the activity of immunotherapy for gynecologic cancers.

Authors:  Christina H Son; Gini F Fleming; John W Moroney
Journal:  Cancer Manag Res       Date:  2017-10-31       Impact factor: 3.989

5.  Phenotype of POLE-mutated endometrial cancer.

Authors:  Sara Imboden; Denis Nastic; Mehran Ghaderi; Filippa Rydberg; Tilman T Rau; Michael D Mueller; Elisabeth Epstein; Joseph W Carlson
Journal:  PLoS One       Date:  2019-03-27       Impact factor: 3.240

6.  POLE-mutated clear cell cervical cancer associated with in-utero diethylstilbestrol exposure.

Authors:  Elizabeth K Lee; Neal I Lindeman; Ursula A Matulonis; Panagiotis A Konstantinopoulos
Journal:  Gynecol Oncol Rep       Date:  2019-01-29

7.  Endometrial Tumor Microenvironment Alters Human NK Cell Recruitment, and Resident NK Cell Phenotype and Function.

Authors:  Clara Degos; Mellie Heinemann; Julien Barrou; Nicolas Boucherit; Eric Lambaudie; Ariel Savina; Laurent Gorvel; Daniel Olive
Journal:  Front Immunol       Date:  2019-04-26       Impact factor: 7.561

Review 8.  Clinical actionability of molecular targets in endometrial cancer.

Authors:  Mary Ellen Urick; Daphne W Bell
Journal:  Nat Rev Cancer       Date:  2019-08-06       Impact factor: 60.716

9.  Endometrial cancer with a POLE mutation progresses frequently through the type I pathway despite its high-grade endometrioid morphology: a cohort study at a single institution in Japan.

Authors:  Mahina Monsur; Munekage Yamaguchi; Hironori Tashiro; Kumiko Yoshinobu; Fumitaka Saito; Chimeddulam Erdenebaatar; Chenyan Li; Yutaka Iwagoi; Takashi Ohba; Ken-Ichi Iyama; Hidetaka Katabuchi
Journal:  Med Mol Morphol       Date:  2021-01-05       Impact factor: 2.309

10.  Germline POLE mutation in a child with hypermutated medulloblastoma and features of constitutional mismatch repair deficiency.

Authors:  Holly Lindsay; Sarah Scollon; Jacquelyn Reuther; Horatiu Voicu; Surya P Rednam; Frank Y Lin; Kevin E Fisher; Murali Chintagumpala; Adekunle M Adesina; D Will Parsons; Sharon E Plon; Angshumoy Roy
Journal:  Cold Spring Harb Mol Case Stud       Date:  2019-10-23
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