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Serotonin activates glycolysis and mitochondria biogenesis in human breast cancer cells through activation of the Jak1/STAT3/ERK1/2 and adenylate cyclase/PKA, respectively

British journal of cancer, 2020-01, Vol.122 (2), p.194-208 [Peer Reviewed Journal]

2019© The Author(s), under exclusive licence to Cancer Research UK 2019 ;The Author(s), under exclusive licence to Cancer Research UK 2019 ;ISSN: 0007-0920 ;EISSN: 1532-1827 ;DOI: 10.1038/s41416-019-0640-1 ;PMID: 31819176

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Title:
Serotonin activates glycolysis and mitochondria biogenesis in human breast cancer cells through activation of the Jak1/STAT3/ERK1/2 and adenylate cyclase/PKA, respectively
Author: Sola-Penna, Mauro ; Paixão, Larissa P ; Branco, Jessica R ; Ochioni, Alan C ; Albanese, Jamille M ; Mundim, Davi M ; Baptista-de-Souza, Daniela ; Figueiredo, Claudia P ; Coelho, Wagner S ; Marcondes, Mariah C ; Zancan, Patricia
Subjects: Adenylate cyclase ; Adenylyl Cyclases - genetics ; Apoptosis - drug effects ; Biosynthesis ; Breast cancer ; Breast Neoplasms - genetics ; Breast Neoplasms - metabolism ; Breast Neoplasms - pathology ; Carrier Proteins - genetics ; Cell activation ; Cell proliferation ; Cell Proliferation - drug effects ; Cell Survival - drug effects ; Confocal microscopy ; Cytometry ; Disruption ; Enzymology ; Extracellular signal-regulated kinase ; Female ; Glucose ; Glucose - metabolism ; Glycolysis ; Glycolysis - drug effects ; Growth rate ; Humans ; Incubation ; Janus kinase ; Janus Kinase 1 - genetics ; Ketanserin ; Ketanserin - pharmacology ; Lactic acid ; MAP Kinase Signaling System - genetics ; MCF-7 Cells ; Membrane Proteins - genetics ; Metabolism ; Mitochondria ; Mitochondria - drug effects ; Mitochondria - metabolism ; Oxidation ; Protein kinase A ; Pyruvate kinase ; Pyruvic acid ; Serotonin ; Serotonin - pharmacology ; Signal transduction ; Stat3 protein ; STAT3 Transcription Factor - genetics ; Thyroid Hormone-Binding Proteins ; Thyroid Hormones - genetics ; Tumors ; Western blotting
Is Part Of: British journal of cancer, 2020-01, Vol.122 (2), p.194-208
Description: Although produced by several types of tumours, the role of serotonin on cancer biology is yet to be understood. The effects of serotonin (5-HT) on human breast cancer cells proliferation, signalling pathways and metabolic profile were evaluated by cytometry, western blotting, qPCR, enzymology and confocal microscopy. Our results revealed that incubation of MCF-7 cells with 10 µM 5-HT increased cell growth rate by 28%, an effect that was prevented by the 5-HTR antagonist, ketanserin. Conversely, increasing concentrations of 5-HT promoted glucose consumption and lactate production by MCF-7 cells. We also showed that increased glucose metabolism is provoked by the upregulation of pyruvate kinase M2 (PKM2) isoform through 5-HTR -triggered activation of Jak1/STAT3 and ERK1/2 subcellular pathways. However, we noticed a decrease in the rate of produced lactate per consumed glucose as a function of the hormone concentration, suggesting a disruption of the Warburg effect. The latter effect is due to 5-HTR -dependent mitochondrial biogenesis and metabolism, which is triggered by adenylyl cyclase/PKA, enhancing the oxidation of lactate within these cells. We showed that serotonin, through 5-HTR , interferes with breast cancer cells proliferation and metabolism by triggering two distinct signalling pathways: Jak1/STAT3 that boosts glycolysis through upregulation of PKM2, and adenylyl cyclase/PKA that enhances mitochondrial biogenesis.
Publisher: England: Nature Publishing Group
Language: English
Identifier: ISSN: 0007-0920
EISSN: 1532-1827
DOI: 10.1038/s41416-019-0640-1
PMID: 31819176
Source: Geneva Foundation Free Medical Journals at publisher websites
MEDLINE
PubMed Central
ProQuest Central

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Serotonin activates glycolysis and mitochondria biogenesis in human breast cancer cells through activation of the Jak1/STAT3/ERK1/2 and adenylate cyclase/PKA, respectively

2019© The Author(s), under exclusive licence to Cancer Research UK 2019 ;The Author(s), under exclusive licence to Cancer Research UK 2019 ;ISSN: 0007-0920 ;EISSN: 1532-1827 ;DOI: 10.1038/s41416-019-0640-1 ;PMID: 31819176

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