Cited by 564Sphingolipid Metabolism and SignalingCytokine Signaling Pathways and InteractionsCancer, Lipids, and Metabolism

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Sphingosine-1-Phosphate Links Persistent STAT3 Activation, Chronic Intestinal Inflammation, and Development of Colitis-Associated Cancer

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Liang, Jie, Nagahashi, Masayuki, Kim, Eugene Y., Harikumar, Kuzhuvelil B., Yamada, Akimitsu, Huang, Wei-Ching, Hait, Nitai C., Allegood, Jeremy C., Price, Megan M., Avni, Dorit, Takabe, Kazuaki, Kordula, Tomasz, Milstien, Sheldon, Spiegel, Sarah·2013·Cancer Cell

DOI 10.1016/j.ccr.2012.11.013PMC PMC3578577

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Abstract

Inflammatory bowel disease is an important risk factor for colorectal cancer. We show that sphingosine-1-phosphate (S1P) produced by upregulation of sphingosine kinase 1 (SphK1) links chronic intestinal inflammation to colitis-associated cancer (CAC) and both are exacerbated by deletion of Sphk2. S1P is essential for production of the multifunctional NF-κB-regulated cytokine IL-6, persistent activation of the transcription factor STAT3, and consequent upregulation of the S1P receptor, S1PR1. The prodrug FTY720 decreased SphK1 and S1PR1 expression and eliminated the NF-κB/IL-6/STAT3 amplification cascade and development of CAC, even in Sphk2(-/-) mice, and may be useful in treating colon cancer in individuals with ulcerative colitis. Thus, the SphK1/S1P/S1PR1 axis is at the nexus between NF-κB and STAT3 and connects chronic inflammation and CAC.

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Authors: Liang, J., Nagahashi, M., Kim, E. Y., Harikumar, K. B., Yamada, A., Huang, W.-C., Hait, N. C., Allegood, J. C., Price, M. M., Avni, D., Takabe, K., Kordula, T., Milstien, S., & Spiegel, S.
Affiliations: Virginia Commonwealth University (US)
Corresponding author: Spiegel, Sarah
ORCID: Liang, Jie
Nagahashi, Masayuki
Kim, Eugene Y.
Harikumar, Kuzhuvelil B.
Yamada, Akimitsu
Huang, Wei-Ching
Hait, Nitai C.
Allegood, Jeremy C.
Avni, Dorit
Takabe, Kazuaki
Kordula, Tomasz
Milstien, Sheldon
Spiegel, Sarah
Venue: Cancer Cell
Publisher: Elsevier BV
Published: 2013-01
Volume: 23
Issue: 1
Pages: 107-120
ISSN: 1535-6108 (ISSN-L)
DOI: 10.1016/j.ccr.2012.11.013
PMC: PMC3578577
OpenAlex: W2145876349
Cited by: 563
References: 62
Citations by year: 2026: 21 · 2025: 29 · 2024: 35 · 2023: 20 · 2022: 37 · 2021: 45 · 2020: 51 · 2019: 42 · 2018: 44 · 2017: 57 · 2016: 59 · 2015: 48 · 2014: 48 · 2013: 25
FWCI: 15.70
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 378 d)
Locations: Cancer Cell (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: Susan G. Komen
National Institutes of Health (5k12hd055881-05)
Japan Society for the Promotion of Science
National Heart, Lung, and Blood Institute (T32HL094290)
National Cancer Institute (P30CA16059, R01CA160688, R01CA-61774, R01CA061774, P30CA016059)
National Institute of General Medical Sciences (R37GM043880)
National Institute of Allergy and Infectious Diseases (U19AI077435)
National Institute of Neurological Disorders and Stroke (P30NS047463)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (K12-HD055881)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sphingolipid Metabolism and Signaling
Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Lipids, and Metabolism
Keywords: sphingosine-1-phosphate, sphingosine kinase 1, sphingosine kinase 2, S1PR1, STAT3 activation, NF-κB, interleukin-6, colitis-associated colorectal cancer, inflammatory bowel disease, ulcerative colitis, fingolimod, chronic intestinal inflammation, colorectal cancer
MeSH terms: Fingolimod Hydrochloride, Sphingosine Kinase, Animals, Cell Transformation, Neoplastic, Colitis, Colon, Lysophospholipids, Propylene Glycols, Sphingosine, Interleukin-6, Gene Expression Regulation, Neoplastic, NF-kappa B, Gene Deletion, Phosphotransferases (Alcohol Group Acceptor), STAT3 Transcription Factor, Mice, Tumor Microenvironment

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Sphingosine-1-Phosphate Links Persistent STAT3 Activation, Chronic Intestinal Inflammation, and Development of Colitis-Associated Cancer

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