DNA polymerase delta POLD1 endometrial cancer germline hypermutation immunotherapy variant of uncertain significance

Journal

Cancers
ISSN: 2072-6694
Titre abrégé: Cancers (Basel)
Pays: Switzerland
ID NLM: 101526829

Informations de publication

Date de publication:
30 Nov 2023
Historique:
received: 08 11 2023
revised: 28 11 2023
accepted: 29 11 2023
medline: 9 12 2023
pubmed: 9 12 2023
entrez: 9 12 2023
Statut: epublish

Résumé

Mutations in the DNA polymerase delta 1 (POLD1) exonuclease domain cause DNA proofreading defects, hypermutation, hereditary colorectal and endometrial cancer, and are predictive of immunotherapy response. Exonuclease activity is carried out by two magnesium cations, bound to four highly conserved, negatively charged amino acids (AA) consisting of aspartic acid at amino acid position 316 (p.D316), glutamic acid at position 318 (p.E318), p.D402, and p.D515 (termed DEDD motif). Germline polymorphisms resulting in charge-discordant AA substitutions in the DEDD motif are classified as variants of uncertain significance (VUSs) by laboratories and thus would be considered clinically inactionable. We hypothesize this mutation class is clinically pathogenic. A review of clinical presentation was performed in our index patient with a POLD1(p.D402N) heterozygous proband with endometrial cancer. Implications of this mutation class were evaluated by a Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)-guided systematic review, in silico analysis with orthogonal biochemical confirmation, and whole-exome and RNA sequencing analysis of the patient's tumor and engineered cell lines. Our systematic review favored a Mendelian disease mutation class associated with endometrial and colorectal cancers. In silico analysis predicted defective protein function, confirmed by biochemical assay demonstrating loss of nuclease activity. A Charge-discordant AA substitution in the DEDD motif of

Sections du résumé

BACKGROUND BACKGROUND
Mutations in the DNA polymerase delta 1 (POLD1) exonuclease domain cause DNA proofreading defects, hypermutation, hereditary colorectal and endometrial cancer, and are predictive of immunotherapy response. Exonuclease activity is carried out by two magnesium cations, bound to four highly conserved, negatively charged amino acids (AA) consisting of aspartic acid at amino acid position 316 (p.D316), glutamic acid at position 318 (p.E318), p.D402, and p.D515 (termed DEDD motif). Germline polymorphisms resulting in charge-discordant AA substitutions in the DEDD motif are classified as variants of uncertain significance (VUSs) by laboratories and thus would be considered clinically inactionable. We hypothesize this mutation class is clinically pathogenic.
METHODS METHODS
A review of clinical presentation was performed in our index patient with a POLD1(p.D402N) heterozygous proband with endometrial cancer. Implications of this mutation class were evaluated by a Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)-guided systematic review, in silico analysis with orthogonal biochemical confirmation, and whole-exome and RNA sequencing analysis of the patient's tumor and engineered cell lines.
RESULTS RESULTS
Our systematic review favored a Mendelian disease mutation class associated with endometrial and colorectal cancers. In silico analysis predicted defective protein function, confirmed by biochemical assay demonstrating loss of nuclease activity. A
CONCLUSION CONCLUSIONS
Charge-discordant AA substitution in the DEDD motif of

Identifiants

pubmed: 38067377
pii: cancers15235674
doi: 10.3390/cancers15235674
pmc: PMC10705788
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : NCI NIH HHS
ID : K12CA001727, R01CA279840, P30CA033572-39
Pays : United States

Références

Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Genome Res. 2018 Nov;28(11):1747-1756
pubmed: 30341162
JAMA Oncol. 2019 Oct 1;5(10):1504-1506
pubmed: 31415061
Nat Commun. 2020 Nov 20;11(1):5918
pubmed: 33219223
Gigascience. 2021 Feb 16;10(2):
pubmed: 33590861
Oncotarget. 2021 Apr 13;12(8):726-739
pubmed: 33889297
Genome. 2006 Apr;49(4):403-10
pubmed: 16699561
Nat Methods. 2010 Apr;7(4):248-9
pubmed: 20354512
Cancer Med. 2020 Jan;9(2):476-486
pubmed: 31769227
Curr Protoc Bioinformatics. 2013;43:11.10.1-11.10.33
pubmed: 25431634
DNA Cell Biol. 2020 Jan;39(1):50-56
pubmed: 31750734
Nucleic Acids Res. 2018 Jan 4;46(D1):D1062-D1067
pubmed: 29165669
Nat Genet. 2021 Oct;53(10):1434-1442
pubmed: 34594041
J Genet Couns. 2019 Apr;28(2):313-325
pubmed: 30636062
Mol Cell Biol. 2000 Oct;20(20):7490-504
pubmed: 11003646
Nucleic Acids Res. 2003 Jul 1;31(13):3812-4
pubmed: 12824425
Nat Commun. 2022 Aug 27;13(1):5063
pubmed: 36030235
Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15560-5
pubmed: 12429860
Nat Commun. 2020 Feb 28;11(1):1109
pubmed: 32111820
Nature. 2020 May;581(7809):434-443
pubmed: 32461654
Nat Protoc. 2013 Aug;8(8):1551-66
pubmed: 23868073
Bioinformatics. 2018 Sep 1;34(17):i884-i890
pubmed: 30423086
Nat Commun. 2018 May 1;9(1):1746
pubmed: 29717118
Nat Genet. 2022 Jul;54(7):996-1012
pubmed: 35817971
Science. 2021 Dec 03;374(6572):1252-1258
pubmed: 34855483
PLoS One. 2012;7(6):e39156
pubmed: 22723953
Genet Med. 2016 Apr;18(4):325-32
pubmed: 26133394
Genet Med. 2015 May;17(5):405-24
pubmed: 25741868
Nature. 2020 Feb;578(7793):94-101
pubmed: 32025018
Nucleic Acids Res. 2001 Mar 1;29(5):1017-26
pubmed: 11222749
Science. 2018 Oct 12;362(6411):
pubmed: 30309915
Gene. 2016 Sep 15;590(1):128-41
pubmed: 27320729
Nucleic Acids Res. 2011 Sep 1;39(17):e118
pubmed: 21727090
Nat Methods. 2014 Apr;11(4):361-2
pubmed: 24681721
Fam Cancer. 2022 Apr;21(2):197-209
pubmed: 33948826
Cell. 2005 Sep 9;122(5):693-705
pubmed: 16143102

Auteurs

Christina Hsiao Wei (CH)

Department of Pathology, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Edward Wenge Wang (EW)

Department of Oncology & Therapeutics Research, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Lingzi Ma (L)

Department of Cancer Genetics and Epigenetics, Beckman Research Institute at City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Yajing Zhou (Y)

Department of Cancer Genetics and Epigenetics, Beckman Research Institute at City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Li Zheng (L)

Department of Cancer Genetics and Epigenetics, Beckman Research Institute at City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Heather Hampel (H)

Clinical Cancer Genetics, City of Hope Medical Center (COHMC), Duarte, CA 91010, USA.

Susan Shehayeb (S)

Clinical Cancer Genetics, City of Hope Medical Center (COHMC), Duarte, CA 91010, USA.

Stephen Lee (S)

Division of Gynecologic Oncology and Surgery, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Joshua Cohen (J)

Division of Gynecologic Oncology and Surgery, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Adrian Kohut (A)

Division of Gynecologic Oncology and Surgery, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Fang Fan (F)

Department of Pathology, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Steven Rosen (S)

Department of Hematology & Hematopoietic Cell Transplantation, City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.
Beckman Research Institute of City of Hope, Duarte, CA 91010, USA.

Xiwei Wu (X)

Beckman Research Institute of City of Hope, Duarte, CA 91010, USA.

Binghui Shen (B)

Department of Cancer Genetics and Epigenetics, Beckman Research Institute at City of Hope Medical Center (COHNMC), Duarte, CA 91010, USA.

Yuqi Zhao (Y)

Beckman Research Institute of City of Hope, Duarte, CA 91010, USA.

Classifications MeSH