Diabetes promotes invasive pancreatic cancer by increasing systemic and tumour carbonyl stress in Kras


Journal

Journal of experimental & clinical cancer research : CR
ISSN: 1756-9966
Titre abrégé: J Exp Clin Cancer Res
Pays: England
ID NLM: 8308647

Informations de publication

Date de publication:
10 Aug 2020
Historique:
received: 30 03 2020
accepted: 04 08 2020
entrez: 12 8 2020
pubmed: 12 8 2020
medline: 28 4 2021
Statut: epublish

Résumé

Type 1 and 2 diabetes confer an increased risk of pancreatic cancer (PaC) of similar magnitude, suggesting a common mechanism. The recent finding that PaC incidence increases linearly with increasing fasting glucose levels supports a central role for hyperglycaemia, which is known to cause carbonyl stress and advanced glycation end-product (AGE) accumulation through increased glycolytic activity and non-enzymatic reactions. This study investigated the impact of hyperglycaemia on invasive tumour development and the underlying mechanisms involved. Pdx1-Cre;LSL-Kras Cumulative incidence of invasive PaC at 22 weeks of age was 75% in untreated diabetic vs 25% in FL-926-16-gtreated diabetic and 8.3% in non-diabetic mice. FL-926-16 treatment suppressed systemic and pancreatic carbonyl stress, extracellular signal-regulated kinases (ERK) 1/2 activation, and nuclear translocation of Yes-associated protein (YAP) in pancreas. In vitro, RCS scavenging and AGE elimination completely inhibited cell proliferation stimulated by high glucose, and YAP proved essential in mediating the effects of both glucose-derived RCS and their protein adducts AGEs. However, RCS and AGEs induced YAP activity through distinct pathways, causing reduction of Large Tumour Suppressor Kinase 1 and activation of the Epidermal Growth Factor Receptor/ERK signalling pathway, respectively. An RCS scavenger and AGE inhibitor prevented the accelerating effect of diabetes on PainINs progression to invasive PaC, showing that hyperglycaemia promotes PaC mainly through increased carbonyl stress. In vitro experiments demonstrated that both circulating RCS/AGEs and tumour cell-derived carbonyl stress generated by excess glucose metabolism induce proliferation by YAP activation, hence providing a molecular mechanism underlying the link between diabetes and PaC (and cancer in general).

Sections du résumé

BACKGROUND BACKGROUND
Type 1 and 2 diabetes confer an increased risk of pancreatic cancer (PaC) of similar magnitude, suggesting a common mechanism. The recent finding that PaC incidence increases linearly with increasing fasting glucose levels supports a central role for hyperglycaemia, which is known to cause carbonyl stress and advanced glycation end-product (AGE) accumulation through increased glycolytic activity and non-enzymatic reactions. This study investigated the impact of hyperglycaemia on invasive tumour development and the underlying mechanisms involved.
METHODS METHODS
Pdx1-Cre;LSL-Kras
RESULTS RESULTS
Cumulative incidence of invasive PaC at 22 weeks of age was 75% in untreated diabetic vs 25% in FL-926-16-gtreated diabetic and 8.3% in non-diabetic mice. FL-926-16 treatment suppressed systemic and pancreatic carbonyl stress, extracellular signal-regulated kinases (ERK) 1/2 activation, and nuclear translocation of Yes-associated protein (YAP) in pancreas. In vitro, RCS scavenging and AGE elimination completely inhibited cell proliferation stimulated by high glucose, and YAP proved essential in mediating the effects of both glucose-derived RCS and their protein adducts AGEs. However, RCS and AGEs induced YAP activity through distinct pathways, causing reduction of Large Tumour Suppressor Kinase 1 and activation of the Epidermal Growth Factor Receptor/ERK signalling pathway, respectively.
CONCLUSIONS CONCLUSIONS
An RCS scavenger and AGE inhibitor prevented the accelerating effect of diabetes on PainINs progression to invasive PaC, showing that hyperglycaemia promotes PaC mainly through increased carbonyl stress. In vitro experiments demonstrated that both circulating RCS/AGEs and tumour cell-derived carbonyl stress generated by excess glucose metabolism induce proliferation by YAP activation, hence providing a molecular mechanism underlying the link between diabetes and PaC (and cancer in general).

Identifiants

pubmed: 32778157
doi: 10.1186/s13046-020-01665-0
pii: 10.1186/s13046-020-01665-0
pmc: PMC7418209
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Cell Cycle Proteins 0
Glycation End Products, Advanced 0
KRAS protein, human 0
Reactive Oxygen Species 0
YAP-Signaling Proteins 0
Yap1 protein, mouse 0
Proto-Oncogene Proteins p21(ras) EC 3.6.5.2

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

152

Subventions

Organisme : Associazione Italiana per la Ricerca sul Cancro
ID : IG - 17640
Organisme : Sapienza Università di Roma
ID : N/A

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Auteurs

Stefano Menini (S)

Department of Clinical and Molecular Medicine, "La Sapienza" University, Via di Grottarossa, 1035-1039 -, 00189, Rome, Italy.

Carla Iacobini (C)

Department of Clinical and Molecular Medicine, "La Sapienza" University, Via di Grottarossa, 1035-1039 -, 00189, Rome, Italy.

Luisa de Latouliere (L)

Department of Clinical and Molecular Medicine, "La Sapienza" University, Via di Grottarossa, 1035-1039 -, 00189, Rome, Italy.
SAFU-unit, Department of Research, Advanced Diagnostics, and Technological Innovation, Regina Elena National Cancer Institute, Rome, Italy.

Isabella Manni (I)

SAFU-unit, Department of Research, Advanced Diagnostics, and Technological Innovation, Regina Elena National Cancer Institute, Rome, Italy.

Martina Vitale (M)

Department of Clinical and Molecular Medicine, "La Sapienza" University, Via di Grottarossa, 1035-1039 -, 00189, Rome, Italy.

Emanuela Pilozzi (E)

Department of Clinical and Molecular Medicine, "La Sapienza" University, Via di Grottarossa, 1035-1039 -, 00189, Rome, Italy.
Pathology Unit, University "La Sapienza", Sant'Andrea Hospital, Rome, Italy.

Carlo Pesce (C)

DINOGMI, University of Genoa Medical School, Genoa, Italy.

Paola Cappello (P)

Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin, Italy.

Francesco Novelli (F)

Department of Molecular Biotechnology and Health Sciences, University of Turin, Turin, Italy.

Giulia Piaggio (G)

SAFU-unit, Department of Research, Advanced Diagnostics, and Technological Innovation, Regina Elena National Cancer Institute, Rome, Italy.

Giuseppe Pugliese (G)

Department of Clinical and Molecular Medicine, "La Sapienza" University, Via di Grottarossa, 1035-1039 -, 00189, Rome, Italy. giuseppe.pugliese@uniroma1.it.

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Classifications MeSH