Silencing the GUCA2A-GUCY2C tumor suppressor axis in CIN, serrated, and MSI colorectal neoplasia.


Journal

Human pathology
ISSN: 1532-8392
Titre abrégé: Hum Pathol
Pays: United States
ID NLM: 9421547

Informations de publication

Date de publication:
05 2019
Historique:
received: 12 09 2018
revised: 16 11 2018
accepted: 23 11 2018
pubmed: 5 2 2019
medline: 19 11 2019
entrez: 5 2 2019
Statut: ppublish

Résumé

Colorectal cancers (CRCs) initiate through distinct mutations, including in APC pathway components leading to tubular adenomas (TAs); in BRAF, with epigenetic silencing of CDX2, leading to serrated adenomas (SAs); and in the DNA mismatch repair machinery driving microsatellite instability (MSI). Transformation through the APC pathway involves loss of the hormone GUCA2A that silences the tumor-suppressing receptor GUCY2C. Indeed, oral hormone replacement is an emerging strategy to reactivate GUCY2C and prevent CRC initiation and progression. Moreover, retained expression by tumors arising from TAs has established GUCY2C as a diagnostic and therapeutic target to prevent and treat metastatic CRC. Here, we defined the potential role of the GUCA2A-GUCY2C axis and its suitability as a target in tumors arising through the SA and MSI pathways. GUCA2A hormone expression was eliminated in TAs, SAs, and MSI tumors compared to their corresponding normal adjacent tissues. In contrast to the hormone, the tumor-suppressing receptor GUCY2C was retained in TA and MSI tumors. Surprisingly, GUCY2C expression was nearly eliminated in SAs, reflecting loss of the transcription factor CDX2. Changes in the GUCA2A-GUCY2C axis in human SAs and MSI tumors were precisely recapitulated in genetic mouse models. These data reveal the possibility of GUCA2A loss silencing GUCY2C in the pathophysiology of, and oral hormone replacement to restore GUCY2C signaling to prevent, MSI tumors. Also, they highlight the potential for targeting GUCY2C to prevent and treat metastases arising from TA and MSI tumors. In contrast, loss of GUCY2C excludes patients with SAs as candidates for GUCY2C-based prevention and therapy.

Identifiants

pubmed: 30716341
pii: S0046-8177(19)30007-3
doi: 10.1016/j.humpath.2018.11.032
pmc: PMC6988773
mid: NIHMS1548045
pii:
doi:

Substances chimiques

GUCY2C protein, human EC 4.6.1.2
Receptors, Enterotoxin EC 4.6.1.2

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

103-114

Subventions

Organisme : NCI NIH HHS
ID : F30 CA232469
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA206026
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM008562
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA204481
Pays : United States
Organisme : NIDDK NIH HHS
ID : F30 DK103492
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA056036
Pays : United States

Informations de copyright

Copyright © 2019 Elsevier Inc. All rights reserved.

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Auteurs

Babar Bashir (B)

Department of Pharmacology & Experimental Therapeutics, Thomas Jefferson University, Philadelphia, PA 19107, United States; Department of Medical Oncology, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: babar.bashir@jefferson.edu.

Dante J Merlino (DJ)

Department of Pharmacology & Experimental Therapeutics, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: dante.merlino@jefferson.edu.

Jeffrey A Rappaport (JA)

Department of Pharmacology & Experimental Therapeutics, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: jeffrey.rappaport@jefferson.edu.

Esteban Gnass (E)

Department of Pathology, Anatomy, and Cell Biology, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: estebandgnass@gmail.com.

Juan P Palazzo (JP)

Department of Pathology, Anatomy, and Cell Biology, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: juan.palazzo@jefferson.edu.

Ying Feng (Y)

Departments of Internal Medicine and Pathology, University of Michigan, Ann Arbor, MI 48109, United States. Electronic address: yingfeng@med.umich.edu.

Eric R Fearon (ER)

Departments of Internal Medicine and Pathology, University of Michigan, Ann Arbor, MI 48109, United States; Department of Human Genetics, University of Michigan, Ann Arbor, MI 48109, United States. Electronic address: fearon@med.umich.edu.

Adam E Snook (AE)

Department of Pharmacology & Experimental Therapeutics, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: adam.snook@jefferson.edu.

Scott A Waldman (SA)

Department of Pharmacology & Experimental Therapeutics, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address: scott.waldman@jefferson.edu.

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Classifications MeSH