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PMID: 22182838 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov't

Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice.

The Journal of clinical investigation ·Vol. 122 ·No. 1 ·2012-01-00 ·Pages 178-91

Panigrahy D, Edin ML, Lee CR, Huang S, Bielenberg DR, Butterfield CE, Barnés CM, Mammoto A, Mammoto T, Luria A, Benny O, Chaponis DM, Dudley AC, Greene ER, Vergilio JA, Pietramaggiori G, Scherer-Pietramaggiori SS, Short SM, Seth M, Lih FB, Tomer KB, Yang J, Schwendener RA, Hammock BD, Falck JR, Manthati VL, Ingber DE, Kaipainen A, D'Amore PA, Kieran MW, Zeldin DC

Abstract

Epoxyeicosatrienoic acids (EETs) are small molecules produced by cytochrome P450 epoxygenases. They are lipid mediators that act as autocrine or paracrine factors to regulate inflammation and vascular tone. As a result, drugs that raise EET levels are in clinical trials for the treatment of hypertension and many other diseases. However, despite their pleiotropic effects on cells, little is known about the role of these epoxyeicosanoids in cancer. Here, using genetic and pharmacological manipulation of endogenous EET levels, we demonstrate that EETs are critical for primary tumor growth and metastasis in a variety of mouse models of cancer. Remarkably, we found that EETs stimulated extensive multiorgan metastasis and escape from tumor dormancy in several tumor models. This systemic metastasis was not caused by excessive primary tumor growth but depended on endothelium-derived EETs at the site of metastasis. Administration of synthetic EETs recapitulated these results, while EET antagonists suppressed tumor growth and metastasis, demonstrating in vivo that pharmacological modulation of EETs can affect cancer growth. Furthermore, inhibitors of soluble epoxide hydrolase (sEH), the enzyme that metabolizes EETs, elevated endogenous EET levels and promoted primary tumor growth and metastasis. Thus, our data indicate a central role for EETs in tumorigenesis, offering a mechanistic link between lipid signaling and cancer and emphasizing the critical importance of considering possible effects of EET-modulating drugs on cancer.

MeSH Terms
Animals Aryl Hydrocarbon Hydroxylases/genetics,metabolism Cytochrome P-450 CYP2C8 Cytochrome P-450 CYP2J2 Cytochrome P-450 Enzyme Inhibitors Cytochrome P-450 Enzyme System/genetics,metabolism Eicosanoids/metabolism Endothelium, Vascular/metabolism Epoxy Compounds/metabolism Humans Male Mice Mice, Inbred C57BL Mice, Knockout Mice, Transgenic Neoplasm Metastasis/pathology,physiopathology Neoplasms, Experimental/blood supply,metabolism,pathology Neovascularization, Pathologic Recombinant Proteins/genetics,metabolism Vascular Endothelial Growth Factor A/metabolism
Chemicals
Cytochrome P-450 Enzyme Inhibitors Eicosanoids Epoxy Compounds Recombinant Proteins Vascular Endothelial Growth Factor A vascular endothelial growth factor A, mouse Cytochrome P-450 Enzyme System Aryl Hydrocarbon Hydroxylases CYP2C8 protein, human Cytochrome P-450 CYP2C8 Cytochrome P-450 CYP2J2
Authors & Affiliations
31 authors, click to expand affiliations / ORCID
Panigrahy Dipak
Vascular Biology Program, Children's Hospital Boston, Boston, Massachusetts, USA. [email protected]
Edin Matthew L
Lee Craig R
Huang Sui
Bielenberg Diane R
Butterfield Catherine E
Barnés Carmen M
Mammoto Akiko
Mammoto Tadanori
Luria Ayala
Benny Ofra
Chaponis Deviney M
Dudley Andrew C
Greene Emily R
Vergilio Jo-Anne
Pietramaggiori Giorgio
Scherer-Pietramaggiori Sandra S
Short Sarah M
Seth Meetu
Lih Fred B
Tomer Kenneth B
Yang Jun
Schwendener Reto A
Hammock Bruce D
Falck John R
Manthati Vijaya L
Ingber Donald E
Kaipainen Arja
D'Amore Patricia A
Kieran Mark W
Zeldin Darryl C
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Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
1558-8238
Published
2012-01-00
Epub
2011-00-19
Pages
178-91
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC3248288
Subset
IM
Grants
NIGMS NIH HHS · R01 GM088199-02 · United States
NIEHS NIH HHS · R01 ES002710 · United States
NIGMS NIH HHS · R01 GM088199-03 · United States
NIEHS NIH HHS · P42 ES004699 · United States
NIGMS NIH HHS · R01 GM088199 · United States
Intramural NIH HHS · Z01 ES050167 · United States
NCI NIH HHS · R01CA148633-01A1 · United States
NCI NIH HHS · R01 CA148633 · United States
NCI NIH HHS · P01 CA045548 · United States
Intramural NIH HHS · Z01 ES025034 · United States
NIEHS NIH HHS · R01 ES013933 · United States
NCI NIH HHS · CA045548 · United States
NCI NIH HHS · R01 CA177875 · United States
NCI NIH HHS · R00 CA140708 · United States
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