Autotaxin Expression Is Regulated at the Post-transcriptional Level by the RNA-binding Proteins HuR and AUF1

被引:34
作者
Sun, Shuhong [1 ]
Zhang, Xiaotian [1 ]
Lyu, Lin [1 ]
Li, Xixi [2 ]
Yao, Siliang [1 ]
Zhang, Junjie [1 ]
机构
[1] Beijing Normal Univ, Coll Life Sci, Inst Cell Biol, Key Lab Cell Proliferat & Regulat Biol,Minist Edu, Beijing 100875, Peoples R China
[2] Beijing Normal Univ, Coll Life Sci, Minist Educ, Key Lab Biodivers Sci & Ecol Engn, Beijing 100875, Peoples R China
基金
中国国家自然科学基金;
关键词
ANGIOGENIC FACTOR; MESSENGER-RNAS; THP-1; CELLS; ACID; IDENTIFICATION; MOTILITY; TARGET; CARCINOMA; PATHWAYS; SEQUENCE;
D O I
10.1074/jbc.M116.756908
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Autotaxin (ATX) is a key enzyme that converts lysophosphatidylcholine (LPC) into lysophosphatidic acid (LPA), a lysophospholipid mediator that regulates cellular activities through its specific G protein-coupled receptors. The ATX-LPA axis plays an important role in various physiological and pathological processes, especially in inflammation and cancer development. Although the transcriptional regulation of ATX has been widely studied, the post-transcriptional regulation of ATX is largely unknown. In this study, we identified conserved adenylate-uridylate (AU)-rich elements in the ATX mRNA 3'-untranslated region (3'UTR). The RNA-binding proteins HuR and AUF1 directly bound to the ATX mRNA 3'UTR and had antagonistic functions in ATX expression. HuR enhanced ATX expression by increasing ATX mRNA stability, whereas AUF1 suppressed ATX expression by promoting ATX mRNA decay. HuR and AUF1 were involved in ATX regulation in Colo320 human colon cancer cells and the LPS-stimulated human monocytic THP-1 cells. HuR knockdown suppressed ATX expression in B16 mouse melanoma cells, leading to inhibition of cell migration. This effect was reversed by AUF1 knockdown to recover ATX expression or by the addition of LPA. These results suggest that the post-transcriptional regulation of ATX expression by HuR and AUF1 modulates cancer cell migration. In summary, we identified HuR and AUF1 as novel post-transcriptional regulators of ATX expression, thereby elucidating a novel mechanism regulating the ATX-LPA axis.
引用
收藏
页码:25823 / 25836
页数:14
相关论文
共 34 条
[1]   Microarray analysis identifies Autotaxin, a tumour cell motility and angiogenic factor with lysophospholipase D activity, as a specific target of cell transformation by v-Jun [J].
Black, EJ ;
Clair, T ;
Delrow, J ;
Neiman, P ;
Gillespie, DAF .
ONCOGENE, 2004, 23 (13) :2357-2366
[2]   Potential involvement of adipocyte insulin resistance in obesity-associated up-regulation of adipocyte lysophospholipase D/autotaxin expression [J].
Boucher, J ;
Quilliot, D ;
Pradères, JP ;
Simon, MF ;
Grés, S ;
Guigné, C ;
Prévot, D ;
Ferry, G ;
Boutin, JA ;
Carpéné, C ;
Valet, P ;
Saulnier-Blache, JS .
DIABETOLOGIA, 2005, 48 (03) :569-577
[3]   Lysophosphatidic acid-induced interleukin-1β expression is mediated through Gi/Rho and the generation of reactive oxygen species in macrophages [J].
Chang, Chi-Lun ;
Lin, Mu-En ;
Hsu, Hsien-Yeh ;
Yao, Chao-Ling ;
Hwang, Shiaw-Min ;
Pan, Chien-Yuan ;
Hsu, Chi-Yen ;
Lee, Hsinyu .
JOURNAL OF BIOMEDICAL SCIENCE, 2008, 15 (03) :357-363
[4]   Integrin α6β4 promotes expression of autotaxin/ENPP2 autocrine motility factor in breast carcinoma cells [J].
Chen, M ;
O'Connor, KL .
ONCOGENE, 2005, 24 (32) :5125-5130
[5]   Identification of a target RNA motif for RNA-binding protein HuR [J].
de Silanes, IL ;
Zhan, M ;
Lal, A ;
Yang, XL ;
Gorospe, M .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (09) :2987-2992
[6]  
Euer N, 2002, ANTICANCER RES, V22, P733
[7]   HNS, a nuclear-cytoplasmic shuttling sequence in HuR [J].
Fan, XHC ;
Steitz, JA .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1998, 95 (26) :15293-15298
[8]   Constitutive autotaxin transcription by Nmyc-amplified and non-amplified neuroblastoma cells is regulated by a novel AP-1 and SP-mediated mechanism and abrogated by curcumin [J].
Farina, Antonietta R. ;
Cappabianca, Lucia ;
Ruggeri, Pierdomenico ;
Di Ianni, Natalia ;
Ragone, Marzia ;
Merolle, Stefania ;
Sano, Kimihiko ;
Stracke, Mary L. ;
Horowitz, Jonathan M. ;
Gulino, Alberto ;
Mackay, Andrew R. .
FEBS LETTERS, 2012, 586 (20) :3681-3691
[9]   Autotaxin is released from adipocytes, catalyzes lysophosphatidic acid synthesis, and activates preadipocyte proliferation -: Up-regulated expression with adipocyte differentiation and obesity [J].
Ferry, G ;
Tellier, E ;
Try, A ;
Grés, S ;
Naime, I ;
Simon, MF ;
Rodriguez, M ;
Boucher, J ;
Tack, I ;
Gesta, S ;
Chomarat, P ;
Dieu, M ;
Raes, M ;
Galizzi, JP ;
Valet, P ;
Boutin, JA ;
Saulnier-Blache, JS .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2003, 278 (20) :18162-18169
[10]  
Grammatikakis I., 2016, WILEY INTERDISCIP RE, DOI [DOI 10.1002/WRNA.1372, 10.1002/wrna.1372]