Mouse Snail Is a Target Gene for HIF

Luo, Daochun; Wang, Jinxia; Li, Jeff; Post, Martin

doi:10.1158/1541-7786.mcr-10-0214

Cited by 116Cancer, Hypoxia, and MetabolismMechanisms of cancer metastasisCancer Cells and Metastasis

Mouse Snail Is a Target Gene for HIF

Luo, Daochun, Wang, Jinxia, Li, Jeff, Post, Martin·2011·Molecular Cancer Research

DOI 10.1158/1541-7786.mcr-10-0214

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Abstract

The transcriptional inhibitor Snail is a critical regulator for epithelial–mesenchymal transition (EMT). Although low oxygen induces Snail transcription, thereby stimulating EMT, a direct role of hypoxia-inducible factor (HIF) in this process remains to be demonstrated. Here we show that hypoxia induces the expression of Snail via HIF. In silico analysis identified a potential hypoxia-response element (HRE) close to the minimal promoter of the human and mouse genome of the snail gene. Gel shift assays demonstrated that a specific hypoxia-inducible complex is formed with the putative HRE and that the complex contains HIF proteins. ChIP assays confirmed the interaction of HIF proteins with the putative HRE in vivo. Reporter gene analyses showed that the putative HRE responds to hypoxia in its natural position as well as in front of a heterologous promoter and that the HRE is directly activated by HIF-1α or HIF-2α. HIF knockdown with siRNA at 2% oxygen and overexpression of an oxygen-insensitive HIF (HIF-ΔODD) mutant at 21% oxygen showed that HIF regulates Snail activation and subsequent cell migration. Our findings identify snail as a HIF target gene and provide novel insights into the regulation of snail and hypoxia-induced EMT. Mol Cancer Res; 9(2); 234–45. ©2011 AACR.

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HIF has a direct regulatory effect on EMT-related proteins, such as ZEB1, Snail, and Twist.
“Studies have demonstrated that HIF has a direct regulatory effect on EMT‐related proteins, such as zinc finger E‐box binding homeobox 1, Snail and Twist.”
From Hypoxia signaling in cancer: Implications for therapeutic interventions (2023) · cites this paper as [86]
HIF directly regulates key EMT transcription factors ZEB1, Snail, and Twist through functional hypoxia response elements within the regulatory elements of these genes.
“A direct role for HIF in the regulation of key EMT transcription factors such as ZEB1, Snail, and Twist has been demonstrated through the identification of functional hypoxia response elements (HREs) within the regulatory elements of these genes”
From Hypoxic control of metastasis (2016) · cites this paper as [72]

Epithelial-Mesenchymal Transitions in Development and Disease
Thiery, J. P., Acloque, H., Huang, R. Y. J., & Nieto, M. A. (2009) · Cell · doi:10.1016/j.cell.2009.11.007 · Cited by 9,931 · see citing works
HIFα Targeted for VHL-Mediated Destruction by Proline Hydroxylation: Implications for O 2 Sensing
Ivan, M., Kondo, K., Yang, H., Kim, W., Valiando, J., Ohh, M., Salic, A., Asara, J. M., Lane, W. S., & Kaelin Jr., W. G. (2001) · Science · doi:10.1126/science.1059817 · Cited by 4,735 · see citing works
miR-15 and miR-16 induce apoptosis by targeting BCL2
Cimmino, A., Calin, G. A., Fabbri, M., Iorio, M. V., Ferracin, M., Shimizu, M., Wojcik, S. E., Aqeilan, R. I., Zupo, S., Dono, M., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506654102 · Cited by 3,510 · see citing works
Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway.
Kaelin, W. G., & Ratcliffe, P. J. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.04.009 · Cited by 3,251 · see citing works
Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis.
Yang, J., & Weinberg, R. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.05.009 · Cited by 3,135 · see citing works
The snail superfamily of zinc-finger transcription factors
Nieto, M. A. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm757 · Cited by 1,719 · see citing works
Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial–mesenchymal transition
Zhou, B. P., Deng, J., Xia, W., Xu, J., Li, Y. M., Gunduz, M., & Hung, M.-C. (2004) · Nature Cell Biology · doi:10.1038/ncb1173 · Cited by 1,581 · see citing works
Direct regulation of TWIST by HIF-1α promotes metastasis
Yang, M.-H., Wu, M.-Z., Chiou, S.-H., Chen, P.-M., Chang, S.-Y., Liu, C.-J., Teng, S.-C., & Wu, K.-J. (2008) · Nature Cell Biology · doi:10.1038/ncb1691 · Cited by 1,345 · see citing works
Epithelial–mesenchymal transition in development and cancer: role of phosphatidylinositol 3′ kinase/AKT pathways
Larue, L., & Bellacosa, A. (2005) · Oncogene · doi:10.1038/sj.onc.1209091 · Cited by 1,221 · see citing works
Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension
Jiang, B. H., Semenza, G. L., Bauer, C., & Marti, H. H. (1996) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1996.271.4.c1172 · Cited by 1,213 · see citing works
Hypoxia requires Notch signaling to maintain the undifferentiated cell state
Gustafsson, M. V., Zheng, X., Pereira, T., Gradin, K., Jin, S., Lundkvist, J., Ruas, J. L., Poellinger, L., Lendahl, U., & Bondesson, M. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.09.010 · Cited by 1,109 · see citing works
NF-κB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression
Huber, M. A., Azoitei, N., Baumann, B., Grünert, S., Sommer, A., Pehamberger, H., Kraut, N., Beug, H., & Wirth, T. (2004) · Journal of Clinical Investigation · doi:10.1172/jci21358 · Cited by 1,035 · see citing works
A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development
Ema, M., Taya, S., Yokotani, N., Sogawa, K., Matsuda, Y., & Fujii-Kuriyama, Y. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.9.4273 · Cited by 1,016 · see citing works
Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition
Higgins, D. F., Kimura, K., Bernhardt, W. M., Shrimanker, N., Akai, Y., Hohenstein, B., Saito, Y., Johnson, R. S., Kretzler, M., Cohen, C. D., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci30487 · Cited by 976 · see citing works
Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformationPreprint
Timmerman, L., Grego‐Bessa, J., Raya, Á., Bertrán, E., Pérez-Pomares, J. M., Díez, J., Aranda, S., Palomo‐Ponce, S., McCormick, F., Izpisúa‐Belmonte, J. C., et al. (2003) · Genes & Development · doi:10.1101/gad.276304 · Cited by 972 · see citing works
Notch signaling mediates hypoxia-induced tumor cell migration and invasion
Sahlgren, C., Gustafsson, M. V., Jin, S., Poellinger, L., & Lendahl, U. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802047105 · Cited by 823 · see citing works
FGF Signaling Regulates Mesoderm Cell Fate Specification and Morphogenetic Movement at the Primitive Streak
Ciruna, B. G., & Rossant, J. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00017-x · Cited by 695 · see citing works
Transforming Growth Factor β-1 Induces Snail Transcription Factor in Epithelial Cell Lines
Peinado, H., Quintanilla, M., & Cano, A. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211304200 · Cited by 642 · see citing works
The Mouse Snail Gene Encodes a Key Regulator of the Epithelial-Mesenchymal Transition
Carver, E. A., Jiang, R., Lan, Y., Oram, K. F., & Gridley, T. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.23.8184-8188.2001 · Cited by 624 · see citing works
A Wnt–Axin2–GSK3β cascade regulates Snail1 activity in breast cancer cells
Yook, J. I., Li, X.-Y., Ota, I., Hu, C. Y., Kim, H. S., Kim, N. H., Cha, S. Y., Ryu, J. K., Choi, Y. J., Kim, J., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1508 · Cited by 615 · see citing works
Transforming growth factor-β employs HMGA2 to elicit epithelial–mesenchymal transition
Thuault, S., Valcourt, U., Petersen, M., Manfioletti, G., Heldin, C., & Moustakas, A. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200512110 · Cited by 500 · see citing works
Placental apoptosis in preeclampsia
Allaire, A. D. (2000) · Obstetrics and Gynecology · doi:10.1016/s0029-7844(00)00895-4 · Cited by 416 · see citing works
Hypoxia-Inducible Factor-1-Dependent Repression of E-cadherin in von Hippel-Lindau Tumor Suppressor–Null Renal Cell Carcinoma Mediated by TCF3, ZFHX1A, and ZFHX1B
Krishnamachary, B., Zagzag, D., Nagasawa, H., Rainey, K., Okuyama, H., Baek, J. H., & Semenza, G. L. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3719 · Cited by 415 · see citing works
Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription
Bachelder, R. E., Yoon, S.-O., Francı́, C., de Herreros, A. G., & Mercurio, A. M. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200409067 · Cited by 388 · see citing works
Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells
Imai, T., Horiuchi, A., Wang, C., Oka, K., Ohira, S., Nikaido, T., & Konishi, I. (2003) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63501-8 · Cited by 377 · see citing works
NF‐κB and epithelial to mesenchymal transition of cancer
Min, C., Eddy, S. F., Sherr, D. H., & Sonenshein, G. E. (2008) · Journal of Cellular Biochemistry · doi:10.1002/jcb.21695 · Cited by 374 · see citing works
Hepatocyte growth factor induces cell scattering through MAPK/Egr‐1‐mediated upregulation of Snail
Grotegut, S., von Schweinitz, D., Christofori, G., & Lehembre, F. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601213 · Cited by 363 · see citing works
Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation
Weinmann, A. S., & Farnham, P. (2002) · Methods · doi:10.1016/s1046-2023(02)00006-3 · Cited by 349 · see citing works
Hypoxia-Inducible Factor-1-Dependent Repression of E-cadherin in von Hippel-Lindau Tumor Suppressor—Null Renal Cell Carcinoma Mediated by TCF3, ZFHX1A, and ZFHX1B
Gordon, M. S. (2007) · Yearbook of Oncology · doi:10.1016/s1040-1741(08)70352-x · Cited by 346 · see citing works
Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells
Barberà, M. J., Puig, I., Dominguez-Sola, D., Julien-Grille, S., Guaita‐Esteruelas, S., Peiró, S., Baulida, J., Francı́, C., Dedhar, S., Larue, L., et al. (2004) · Oncogene · doi:10.1038/sj.onc.1207990 · Cited by 337 · see citing works
dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo.Preprint
Ip, Y. T., Park, R., Kosman, D., Yazdanbakhsh, K., & Levine, M. (1992) · Genes & Development · doi:10.1101/gad.6.8.1518 · Cited by 313 · see citing works
Expression and Characterization of Hypoxia-Inducible Factor (HIF)-3α in Human Kidney: Suppression of HIF-Mediated Gene Expression by HIF-3α
Hara, S., Hamada, J., Kobayashi, C., Kondo, Y., & Imura, N. (2001) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2001.5659 · Cited by 283 · see citing works
Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level
Kurrey, N. K., Amit, K., & Bapat, S. A. (2005) · Gynecologic Oncology · doi:10.1016/j.ygyno.2004.12.043 · Cited by 261 · see citing works
uPAR induces epithelial–mesenchymal transition in hypoxic breast cancer cells
Lester, R. D., Jo, M., Montel, V., Takimoto, S., & Gonias, S. L. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200701092 · Cited by 251 · see citing works
VHL Promotes E2 Box-Dependent E-Cadherin Transcription by HIF-Mediated Regulation of SIP1 and Snail
Evans, A. J., Russell, R. C., Roche, O., Burry, T. N., Fish, J. E., Chow, V. W. K., Kim, W. Y., Saravanan, A., Maynard, M. A., Gervais, M. L., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00892-06 · Cited by 248 · see citing works
Inhibition of integrin linked kinase (ILK) suppresses β-catenin-Lef/Tcf-dependent transcription and expression of the E-cadherin repressor, snail, in APC−/− human colon carcinoma cells
Tan, C., Costello, P., Sanghera, J. S., Dominguez-Sola, D., Baulida, J., de Herreros, A. G., & Dedhar, S. (2001) · Oncogene · doi:10.1038/sj.onc.1204052 · Cited by 248 · see citing works
Control of Vertebrate Left-Right Asymmetry by a Snail -Related Zinc Finger Gene
Isaac, A., Sargent, M. G., & Cooke, J. (1997) · Science · doi:10.1126/science.275.5304.1301 · Cited by 193 · see citing works
Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation
Li, X., Deng, W., Nail, C. D., Bailey, S. K., Kraus, M. H., Ruppert, J. M., & Lobo-Ruppert, S. M. (2005) · Oncogene · doi:10.1038/sj.onc.1209077 · Cited by 193 · see citing works
The basal‐like breast carcinoma phenotype is regulated by SLUG gene expression
Storci, G., Sansone, P., Treré, D., Tavolari, S., Taffurelli, M., Ceccarelli, C., Guarnieri, T., Paterini, P., Pariali, M., Montanaro, L., et al. (2007) · The Journal of Pathology · doi:10.1002/path.2254 · Cited by 165 · see citing works
A Signaling Pathway Involving TGF-β2 and Snail in Hair Follicle Morphogenesis
Jamora, C., Lee, P., Kocieniewski, P., Azhar, M., Hosokawa, R., Chai, Y., & Fuchs, E. V. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0030011 · Cited by 145 · see citing works
Abnormalities in Oxygen Sensing Define Early and Late Onset Preeclampsia as Distinct Pathologies
Rolfo, A., Many, A., Racano, A., Tal, R., Tagliaferro, A., Ietta, F., Wang, J., Post, M., & Caniggia, I. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013288 · Cited by 112 · see citing works
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Luo, D., Mari, B. P., Stoll, I., & Anglard, P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202494200 · Cited by 82 · see citing works
Self-citation
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Fernandez-Serra, M., Consales, C., Livigni, A., & Arnone, M. I. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2003.12.029 · Cited by 72 · see citing works
Hypoxia-inducible Factors in the First Trimester Human Lung
Groenman, F. A., Rutter, M., Caniggia, I., Tibboel, D., & Post, M. (2006) · Journal of Histochemistry & Cytochemistry · doi:10.1369/jhc.6a7129.2006 · Cited by 71 · see citing works
Self-citation
Effect of chemical stabilizers of hypoxia-inducible factors on early lung development
Groenman, F. A., Rutter, M., Wang, J., Caniggia, I., Tibboel, D., & Post, M. (2007) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00486.2006 · Cited by 66 · see citing works
Self-citation
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Roy, H. K., Iversen, P. L., Hart, J. A. L., Liu, Y., Koetsier, J. L., Kim, Y., Kunte, D. P., Madugula, M., Backman, V., & Wali, R. K. (2004) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.1159.3.9 · Cited by 58 · see citing works
Up-Regulation of α5-Integrin by E-Cadherin Loss in Hypoxia and Its Key Role in the Migration of Extravillous Trophoblast Cells during Early Implantation
Arimoto‐Ishida, E., Sakata, M., Sawada, K., Nakayama, M., Nishimoto, F., Mabuchi, S., Takeda, T., Yamamoto, T., Isobe, A., Okamoto, Y., et al. (2009) · Endocrinology · doi:10.1210/en.2008-1662 · Cited by 57 · see citing works
The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway
Delfini, M.-C., Celle, M. D. L., Gros, J., Serralbo, O., Marics, I., Seux, M., Scaal, M., & Marcelle, C. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.544 · Cited by 55 · see citing works
A 3′ Enhancer Controls Snail Expression in Melanoma Cells
Palmer, M. B., Majumder, P., Green, M. R., Wade, P. A., & Boss, J. M. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4256 · Cited by 33 · see citing works
Identification of an 11-residue portion of CTP–phosphocholine cytidylyltransferase that is required for enzyme–membrane interactions
Yang, J., Wang, J., Tseu, I., Kuliszewski, M. J., Lee, W.-S., & Post, M. (1997) · Biochemical Journal · doi:10.1042/bj3250029 · Cited by 22 · see citing works
Self-citation

Flagged first, then by citations

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Wu, Z.-Q., Li, X.-Y., Hu, C. Y., Ford, M., Kleer, C. G., & Weiss, S. J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205822109 · Cited by 303 · see citing works
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Zhang, L., Huang, G., Li, X., Zhang, Y., Jiang, Y., Shen, J., Liu, J., Wang, Q., Zhu, J., Feng, X., et al. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-108 · Cited by 293 · see citing works
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Luteolin attenuates TGF-β1-induced epithelial–mesenchymal transition of lung cancer cells by interfering in the PI3K/Akt–NF-κB–Snail pathway
Chen, K., Chen, C.-Y., Lin, C.-J., Yang, T., Chen, T.-H., Wu, L.-C., & Wu, C. (2013) · Life Sciences · doi:10.1016/j.lfs.2013.10.004 · Cited by 97 · see citing works
Diallyl trisulfides, a natural histone deacetylase inhibitor, attenuate HIF‐1α synthesis, and decreases breast cancer metastasis
Wei, Z., Shan, Y., Li, T., Liu, Y., Zhu, Z., Liu, Z., Wu, Y., Chen, W., Wang, A., & Lu, Y. (2017) · Molecular Carcinogenesis · doi:10.1002/mc.22686 · Cited by 92 · see citing works
Role of Hypoxic Stress in Regulating Tumor Immunogenicity, Resistance and Plasticity
Terry, S., Zaarour, R. F., Venkatesh, G. H., Francis, A., El‐Sayed, W., Buart, S., Bravo, P. E., Thiery, J., & Chouaı̈b, S. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103044 · Cited by 86 · see citing works
Copper depletion inhibits CoCl2-induced aggressive phenotype of MCF-7 cells via downregulation of HIF-1 and inhibition of Snail/Twist-mediated epithelial-mesenchymal transition
Li, S., Zhang, J., Yang, H., Wu, C., Dang, X., & Liu, Y. (2015) · Scientific Reports · doi:10.1038/srep12410 · Cited by 84 · see citing works
The Inflammatory Tumor Microenvironment, Epithelial Mesenchymal Transition and Lung Carcinogenesis
Heinrich, E. L., Walser, T. C., Krysan, K., Liclican, E. L., Grant, J. L., Rodriguez, N., & Dubinett, S. M. (2011) · Cancer Microenvironment · doi:10.1007/s12307-011-0089-0 · Cited by 84 · see citing works
Acquisition of tumor cell phenotypic diversity along the EMT spectrum under hypoxic pressure: Consequences on susceptibility to cell-mediated cytotoxicity
Terry, S., Buart, S., Tan, T. Z., Gros, G., Noman, M. Z., Lorens, J. B., Mami‐Chouaib, F., Thiery, J. P., & Chouaı̈b, S. (2017) · OncoImmunology · doi:10.1080/2162402x.2016.1271858 · Cited by 78 · see citing works
Hypoxia-induced LncRNA PCGEM1 promotes invasion and metastasis of gastric cancer through regulating SNAI1
Zhang, J., Jin, H., Wu, Y., Zheng, Z., Guo, S., Wang, Y., Yang, D., Meng, X., Xu, X., & Zhao, Y. (2019) · Clinical & Translational Oncology · doi:10.1007/s12094-019-02035-9 · Cited by 75 · see citing works
RETRACTED ARTICLE: CXCR4 Signaling Induced Epithelial-Mesenchymal Transition by PI3K/AKT and ERK Pathways in Glioblastoma
Lv, B., Yang, X., Lv, S., Wang, L., Fan, K., Shi, R., Wang, F., Song, H., Ma, X., Tan, X., et al. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8935-y · Cited by 69 · see citing works
Retracted
Hypoxia inducible factor-1 is activated by transcriptional co-activator with PDZ-binding motif (TAZ) versus WWdomain-containing oxidoreductase (WWOX) in hypoxic microenvironment of bone metastasis from breast cancer
Bendinelli, P., Maroni, P., Matteucci, E., Luzzati, A., Perrucchini, G. G., & Desiderio, M. A. (2013) · European Journal of Cancer · doi:10.1016/j.ejca.2013.03.002 · Cited by 66 · see citing works
ZEB1 Promotes Invasion in Human Fetal Neural Stem Cells and Hypoxic Glioma Neurospheres
Kahlert, U. D., Suwala, A. K., Raabe, E. H., Siebzehnrübl, F. A., Suarez, M. J., Orr, B. A., Bar, E. E., Maciaczyk, J., & Eberhart, C. G. (2014) · Brain Pathology · doi:10.1111/bpa.12240 · Cited by 64 · see citing works
Implications of Hypoxia in Breast Cancer Metastasis to Bone
Gilkes, D. M. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17101669 · Cited by 63 · see citing works
Breast cancers utilize hypoxic glycogen stores via PYGB, the brain isoform of glycogen phosphorylase, to promote metastatic phenotypes
Altemus, M., Goo, L., Little, A. C., Yates, J. A., Cheriyan, H., Wu, Z.-F., & Merajver, S. D. (2019) · PLoS ONE · doi:10.1371/journal.pone.0220973 · Cited by 59 · see citing works
Cross‐Talk between Oxidative Stress and m6A RNA Methylation in Cancer
Yang, B., & Chen, Q. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/6545728 · Cited by 60 · see citing works
Signaling pathways and mesenchymal transition in pediatric high-grade glioma
Meel, M. H., Schaper, S. A., Kaspers, G. J. L., & Hulleman, E. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2714-7 · Cited by 56 · see citing works
Egr-1 Mediates Chronic Hypoxia-Induced Renal Interstitial Fibrosis via the PKC/ERK Pathway
Sun, S., Ning, X., Zhai, Y., Du, R., Lu, Y., He, L., Li, R., Wu, W., Sun, W., & Wang, H. (2014) · American Journal of Nephrology · doi:10.1159/000362249 · Cited by 56 · see citing works
Hypoxia-Induced Snail Expression Through Transcriptional Regulation by HIF-1α in Pancreatic Cancer Cells
Zhu, G., Huang, C., Feng, Z.-Z., Lv, X.-H., & Qiu, Z. (2013) · Digestive Diseases and Sciences · doi:10.1007/s10620-013-2841-4 · Cited by 56 · see citing works
MiR-675-5p supports hypoxia induced epithelial to mesenchymal transition in colon cancer cells
Costa, V., Dico, A. L., Rizzo, A. G., Raiata, F., Tripodi, M., Alessandro, R., & Conigliaro, A. (2017) · Oncotarget · doi:10.18632/oncotarget.14464 · Cited by 55 · see citing works
A novel HIF-1α-integrin-linked kinase regulatory loop that facilitates hypoxia-induced HIF-1α expression and epithelial-mesenchymal transition in cancer cells
Chou, C.-C., Chuang, H.-C., Salunke, S. B., Kulp, S. K., & Chen, C.-S. (2015) · Oncotarget · doi:10.18632/oncotarget.3186 · Cited by 50 · see citing works
Hypoxia promotes production of neural crest cells in the embryonic head
Scully, D. M., Keane, E., Batt, E., Karunakaran, P., Higgins, D. F., & Itasaki, N. (2016) · Development · doi:10.1242/dev.131912 · Cited by 50 · see citing works
Epithelial to Mesenchymal Transition History: From Embryonic Development to Cancers
Lachat, C., Peixoto, P., & Hervouet, É. (2021) · Biomolecules · doi:10.3390/biom11060782 · Cited by 49 · see citing works
The dual PI3K/mTOR inhibitor NVP-BEZ235 prevents epithelial–mesenchymal transition induced by hypoxia and TGF-β1
Lin, G., Gai, R., Chen, Z., Wang, Y., Liao, S., Dong, R., Zhu, H., Gu, Y., He, Q., & Yang, B. (2014) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2014.02.011 · Cited by 48 · see citing works
Face morphogenesis is promoted by Pbx-dependent EMT via regulation of Snail1 during frontonasal prominence fusion
Losa, M., Risolino, M., Li, B., Hart, J. C. A., Quintana, L., Grishina, I., Yang, H., Choi, I. F., Lewicki, P., Khan, S., et al. (2018) · Development · doi:10.1242/dev.157628 · Cited by 44 · see citing works
PI3K/Akt/HIF-1α signaling pathway mediates HPV-16 oncoprotein-induced expression of EMT-related transcription factors in non-small cell lung cancer cells
Liu, J., Huang, B., Xiu, Z., Zhou, Z., Liu, J., Li, X., & Tang, X. (2018) · Journal of Cancer · doi:10.7150/jca.26112 · Cited by 46 · see citing works
Snail1 Mediates Hypoxia-Induced Melanoma Progression
Liu, S., Kumar, S. M., Martin, J. S., Yang, R., & Xu, X. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.08.038 · Cited by 44 · see citing works
Hypoxia-inducible factor as a bridge between healthy barrier function, wound healing, and fibrosis
Steiner, C. A., Cartwright, I. M., Taylor, C. T., & Colgan, S. P. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00227.2022 · Cited by 42 · see citing works
Connexin 43 prevents the progression of diabetic renal tubulointerstitial fibrosis by regulating the SIRT1-HIF-1α signaling pathway
Sun, X., Huang, K., Haiming, X., Lin, Z., Yang, Y., Zhang, M., Liu, P., & Huang, H. (2020) · Clinical Science · doi:10.1042/cs20200171 · Cited by 41 · see citing works
Targeting hypoxia and hypoxia‐inducible factor‐1 in the tumor microenvironment for optimal cancer immunotherapy
Kheshtchin, N., & Hadjati, J. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30643 · Cited by 41 · see citing works
Decreased eIF3e/Int6 expression causes epithelial-to-mesenchymal transition in breast epithelial cells
Gillis, L. D., & Lewis, S. M. (2012) · Oncogene · doi:10.1038/onc.2012.371 · Cited by 40 · see citing works
The role of hypoxic signalling in metastasis: towards translating knowledge of basic biology into novel anti-tumour strategies
Henríquez, J. A., Sleeman, J. P., & Garvalov, B. K. (2018) · Clinical & Experimental Metastasis · doi:10.1007/s10585-018-9930-x · Cited by 37 · see citing works
Identification of pY654-β-catenin as a critical co-factor in hypoxia-inducible factor-1α signaling and tumor responses to hypoxia
Xi, Y., Wei, Y., Sennino, B., Ulsamer, A., Kwan, I., Brumwell, A. L., Tan, K., Aghi, M. K., McDonald, D. M., Jablons, D. M., et al. (2012) · Oncogene · doi:10.1038/onc.2012.530 · Cited by 36 · see citing works
Pharmacological inhibition of β-catenin prevents EndMT in vitro and vascular remodeling in vivo resulting from endothelial Akt1 suppression
Sabbineni, H., Verma, A., Artham, S., Anderson, D. T., Amaka, O., Liu, F., Narayanan, S. P., & Somanath, P. R. (2019) · Biochemical Pharmacology · doi:10.1016/j.bcp.2019.04.016 · Cited by 36 · see citing works
Erratum: Hispidulin prevents hypoxia-induced epithelial-mesenchymal transition in human colon carcinoma cells.
Xie, J., Gao, H. Y., Peng, J., Han, Y., Chen, X., Jiang, Q., & Wang, C. (2015) · PubMed Central · Cited by 36 · see citing works
Retracted
Hypoxia‐inducible transgelin 2 selects epithelial‐to‐mesenchymal transition and γ‐radiation‐resistant subtypes by focal adhesion kinase‐associated insulin‐like growth factor 1 receptor activation in non‐small‐cell lung cancer cells
Kim, I., Lee, J. H., Kim, S., Hwang, H., Kim, T., & Cho, E. (2018) · Cancer Science · doi:10.1111/cas.13791 · Cited by 35 · see citing works
Epithelial–mesenchymal transition (EMT) and its role in acquired epidermal growth factor receptor-tyrosine kinase inhibitor (EGFR-TKI) chemoresistance in non-small cell lung cancer (NSCLC)
Cruz, M. C. P. D., & Medina, P. M. B. (2024) · Cancer Pathogenesis and Therapy · doi:10.1016/j.cpt.2024.07.001 · Cited by 33 · see citing works
Identification, functional insights and therapeutic targeting of EMT tumour states
Dong, A., & Blanpain, C. (2025) · Nature reviews. Cancer · doi:10.1038/s41568-025-00873-0 · Cited by 37 · see citing works
Mesenchymal stem cells protect from hypoxia-induced alveolar epithelial-mesenchymal transition
Uzunhan, Y., Bernard, O., Marchant, D., Dard, N., Vanneaux, V., Larghero, J., Gille, T., Clérici, C., Valeyre, D., Nunès, H., et al. (2015) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00117.2015 · Cited by 32 · see citing works
Stresses in the metastatic cascade: molecular mechanisms and therapeutic opportunitiesPreprint
Shen, M., & Kang, Y. (2020) · Genes & Development · doi:10.1101/gad.343251.120 · Cited by 31 · see citing works
Pharmacological HIF-inhibition attenuates postoperative adhesion formation
Strowitzki, M. J., Ritter, A. S., Radhakrishnan, P., Harnoss, J. M., Opitz, V. M., Biller, M., Wehrmann, J., Keppler, U., Scheer, J., Wallwiener, M., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-13638-z · Cited by 31 · see citing works
Travelling under pressure - hypoxia and shear stress in the metastatic journey
Ildız, E. S., Gvozdenovic, A., Kovacs, W. J., & Aceto, N. (2023) · Clinical & Experimental Metastasis · doi:10.1007/s10585-023-10224-8 · Cited by 29 · see citing works
BRCA1-IRIS promotes human tumor progression through PTEN blockade and HIF-1α activation
Li, A. G., Murphy, E. C., Culhane, A. C., Powell, E., Wang, H., Bronson, R. T., Von, T., Giobbie‐Hurder, A., Gelman, R. S., Briggs, K. J., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807112115 · Cited by 28 · see citing works
Fetal bovine serum induces sustained, but reversible, epithelial-mesenchymal transition in the BEAS-2B cell line
Malm, S. W., Amouzougan, E. A., & Klimecki, W. T. (2018) · Toxicology in Vitro · doi:10.1016/j.tiv.2018.04.008 · Cited by 27 · see citing works
Downregulation of AIF by HIF-1 contributes to hypoxia-induced epithelial–mesenchymal transition of colon cancer
Xiong, Z., Guo, M., Yu, Y., Zhang, F., Ge, M.-K., Chen, G., & Shen, S.-M. (2016) · Carcinogenesis · doi:10.1093/carcin/bgw089 · Cited by 25 · see citing works
β‐N‐Oxalyl‐l‐α,β‐diaminopropionic acid regulates mitogen‐activated protein kinase signaling by down‐regulation of phosphatidylethanolamine‐binding protein 1
Jammulamadaka, N., Burgula, S., Medisetty, R., Ilavazhagan, G., Rao, S. L. N., & Singh, S. S. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07299.x · Cited by 23 · see citing works
Snail/beta-catenin signaling protects breast cancer cells from hypoxia attack
Scherbakov, A. M., Стефанова, Л. Б., Sorokin, D. V., Semina, S. E., Berstein, L. M., & Ma, K. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.08.019 · Cited by 22 · see citing works
Current developments in modelling the tumour microenvironment in vitro: Incorporation of biochemical and physical gradients
Ahmed, M. A. M., & Nagelkerke, A. (2021) · Organs-on-a-Chip · doi:10.1016/j.ooc.2021.100012 · Cited by 21 · see citing works
Regulation of Epithelial-to-Mesenchymal Transition by Alternative Translation Initiation Mechanisms and Its Implications for Cancer Metastasis
Bera, A., & Lewis, S. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21114075 · Cited by 20 · see citing works
Retraction Note to: CXCR4 Signaling Induced Epithelial-Mesenchymal Transition by PI3K/AKT and ERK Pathways in Glioblastoma
Lv, B., Yang, X., Lv, S., Wang, L., Fan, K., Shi, R., Wang, F., Song, H., Ma, X., Tan, X., et al. (2017) · Molecular Neurobiology · doi:10.1007/s12035-017-0464-z · Cited by 20 · see citing works
Retracted
Solasonine Inhibits Cancer Stemness and Metastasis by Modulating Glucose Metabolism via Wnt/β-Catenin/Snail Pathway in Osteosarcoma
Wang, B., Zhou, Y., Zhang, P., Li, J., & Lu, X. (2023) · The American Journal of Chinese Medicine · doi:10.1142/s0192415x23500593 · Cited by 21 · see citing works
Self-citation
Expression and clinical significance of hypoxia-inducible factor 1α, Snail and E-cadherin in human ovarian cancer cell lines
Zhang, Y., Fan, N., & Yang, J. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3786 · Cited by 19 · see citing works
Retracted
Environmental Influences on Endothelial to Mesenchymal Transition in Developing Implanted Cardiovascular Tissue-Engineered Grafts
Muylaert, D. E. P., de Jong, O. G., Slaats, G. G. G., Nieuweboer, F. E., Fledderus, J. O., Goumans, M., Hierck, B. P., & Verhaar, M. C. (2015) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2015.0167 · Cited by 19 · see citing works
The Histone Variant MacroH2A Blocks Cellular Reprogramming by Inhibiting Mesenchymal-to-Epithelial Transition
Pliatska, M., Καπασά, Μ., Kokkalis, A., Polyzos, A., & Thanos, D. (2018) · Molecular and Cellular Biology · doi:10.1128/mcb.00669-17 · Cited by 17 · see citing works
Modulating hypoxia inducible factor‐1 by nanomaterials for effective cancer therapy
Sun, Y. H., Zhou, Z., Yang, S., & Yang, H. (2021) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1766 · Cited by 16 · see citing works
Hypoxia promotes HO-8910PM ovarian cancer cell invasion via Snail-mediated MT1-MMP upregulation
Sun, L., Lin, P., Qin, Z., Liu, Y., Deng, L., & Lu, C. (2015) · Experimental Biology and Medicine · doi:10.1177/1535370215570205 · Cited by 16 · see citing works
Hypoxia as a regulator of tumor stroma and metastasis
Lee, K. E. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00158.2022 · Cited by 15 · see citing works
Oxygen regulates molecular mechanisms of cancer progression and metastasis
Gupta, K., Madan, E., Sayyid, M. M., Arias‐Pulido, H., Moreno, E., Kuppusamy, P., & Gogna, R. (2013) · Cancer and Metastasis Reviews · doi:10.1007/s10555-013-9464-2 · Cited by 15 · see citing works
Downregulation of IQGAP1 inhibits epithelial‐mesenchymal transition via the HIF1α/VEGF‐A signaling pathway in gastric cancer
Liu, J., Ni, X., Li, Y., Chen, M., Chen, W., Wu, Y., Chen, B., Wu, Y. R., & Xu, M. (2019) · Journal of Cellular Biochemistry · doi:10.1002/jcb.28849 · Cited by 14 · see citing works
Spontaneous metastasis xenograft models link CD44 isoform 4 to angiogenesis, hypoxia, EMT and mitochondria‐related pathways in colorectal cancer
Everest‐Dass, A., Nersisyan, S. A., Maar, H., Novosad, V., Schröder‐Schwarz, J., Freytag, V., Stuke, J. L., Beine, M. C., Schiecke, A., Haider, M., et al. (2023) · Molecular Oncology · doi:10.1002/1878-0261.13535 · Cited by 11 · see citing works
Development of small molecule inhibitors of hypoxia-inducible factors for cancer therapy
Semenza, G. L. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100075 · Cited by 10 · see citing works
Metabolic control of cancer progression as novel targets for therapy
Talukdar, S., Emdad, L., Gogna, R., Das, S. K., & Fisher, P. B. (2021) · Advances in cancer research · doi:10.1016/bs.acr.2021.06.002 · Cited by 6 · see citing works
The signature of extracellular vesicles in hypoxic breast cancer and their therapeutic engineering
Zhu, B., Xiang, K., Li, T., Li, X., & Shi, F. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01870-w · Cited by 5 · see citing works
Hypoxia
Jensen, C. C., & Warfel, N. A. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820472-6.00039-6 · Cited by 5 · see citing works
Role of long non-coding RNAs (lncRNAs) in gastric cancer metastasis: A comprehensive review
Shi, Y. X., Men, X., Wang, F., Li, X., & Zhang, B. (2024) · Pathology - Research and Practice · doi:10.1016/j.prp.2024.155484 · Cited by 4 · see citing works
Overexpression of VEGFA mediated by HIF‐1 is associated with higher rate of spread through air spaces in resected lung adenocarcinomas
Guo, L., Li, S., Wang, X., Zhu, Y., & Li, J. (2023) · The Journal of Gene Medicine · doi:10.1002/jgm.3625 · Cited by 4 · see citing works
Self-citation
LncRNAs in hypoxic microenvironment; insight in their impact in cancer biology
Kuriakose, B. B., Hjazi, A., Saleh, R. O., Bishoyi, A. K., Jyothi, S. R., Almalki, S. G., Sridevi, G., Chaudhary, K., Zwamel, A. H., & Matchonov, O. (2025) · Functional & Integrative Genomics · doi:10.1007/s10142-025-01635-9 · Cited by 3 · see citing works
Inflammation and Lung Cancer: The Role of Epithelial–Mesenchymal Transition
Walser, T. C., Park, S. J., Yanagawa, J., & Dubinett, S. M. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2724-1_2 · Cited by 3 · see citing works
Signaling Pathways Underlying Bone Metastasis: Hypoxia Signaling in Bone Metastasis and Beyond
Devignes, C.-S., Aslan, Y., & Provot, S. (2018) · Current Molecular Biology Reports · doi:10.1007/s40610-018-0090-1 · Cited by 3 · see citing works
Expression of prolyl hydroxylases 2 and 3 in chick embryos
Barber, J. N., & Itasaki, N. (2016) · Gene Expression Patterns · doi:10.1016/j.gep.2016.04.001 · Cited by 2 · see citing works
The complex interplay between Notch signaling and Snail1 transcription factor in the regulation of epithelial–mesenchymal transition (EMT)
Brzozowa-Zasada, M., Piecuch, A., Segiet, O. A., Stęplewska, K., Gabriel, A., & Wojnicz, R. (2015) · European surgery. Supplement/European surgery · doi:10.1007/s10353-015-0339-3 · Cited by 2 · see citing works
Metastatic potentials classified with hypoxia‐inducible factor 1 downstream genes in pan‐cancer cell lines
Nakamichi, K., Yamamoto, Y., Semba, K., & Nakayama, J. (2023) · Genes to Cells · doi:10.1111/gtc.13092 · Cited by 2 · see citing works
Pleiotropic Action of Selenium in the Prevention and Treatment of Cancer, and Related Diseases
Rustum, Y. M. (2019) · MDPI eBooks · doi:10.3390/books978-3-03897-693-6 · Cited by 1 · see citing works
MIR193BHG: a novel hypoxia-inducible long noncoding RNA involved in the fine-tuning of cholesterol metabolism
Wu, X. (2016) · IUScholarWorks (Indiana University) · doi:10.7912/c2s89r · Cited by 1 · see citing works
Invadopodia formation in breast cancer
Hashim, F. N. (2012) · UPT. Syiah Kuala University Library (Syiah Kuala University) · Cited by 1 · see citing works

Snail is a Target Gene for HIF
Luo, D., Wang, J., Li, J., & Post, M. (2007) · The FASEB Journal · doi:10.1096/fasebj.21.6.a1032-e · Cited by 2 · see citing works
Self-citation
Snail1 Mediates Hypoxia-Induced Melanoma Progression
Liu, S., Kumar, S. M., Martin, J. S., Yang, R., & Xu, X. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.08.038 · Cited by 44 · see citing works
Transcription factors of snail family in the regulation of resistance of breast cancer cells to hypoxic conditions
Khamidullina, A. I., Yastrebova, M. A., Scherbakov, A. M., & Tatarskiy, V. V. (2019) · Annals of Oncology · doi:10.1093/annonc/mdz238.085
Hypoxia Inducible Factor 1α Promotes the Epithelial-Mesenchymal Transition of HepG2 Cells by Inducing Snail Expression
Jun-we, S. (2013) · Military Medical Journal of South China
SNAIL gene inhibited by hypoxia-inducible factor 1α (HIF-1α) in epithelial ovarian cancer
Zhang, P., Liu, Y., Feng, Y., & Gao, S. (2016) · International Journal of Immunopathology and Pharmacology · doi:10.1177/0394632016641423 · Cited by 11 · see citing works

Authors: Luo, D., Wang, J., Li, J., & Post, M.
Affiliations: University of Toronto (CA)
ORCID: Post, Martin
Venue: Molecular Cancer Research
Publisher: American Association for Cancer Research (AACR)
Published: 2011-02-15
Volume: 9
Issue: 2
Pages: 234-245
ISSN: 1541-7786 (ISSN-L)
1557-3125
DOI: 10.1158/1541-7786.mcr-10-0214
OpenAlex: W2141808185
Cited by: 116
References: 52
Citations by year: 2026: 3 · 2025: 3 · 2024: 4 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 8 · 2019: 7 · 2018: 12 · 2017: 8 · 2016: 9 · 2015: 14 · 2014: 7 · 2013: 10 · 2012: 8
FWCI: 3.26
Type: journal article
Language: en
Open access: closed
Locations: Molecular Cancer Research (publishedVersion)
PubMed (publishedVersion)
Funders: Canadian Institutes of Health Research (MOP-77751)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mechanisms of cancer metastasis
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: snails, hypoxia-inducible factor, HIF-1α, HIF-2α, hypoxia, epithelial-mesenchymal transition, hypoxia response element, transcriptional regulation, cell migration
MeSH terms: Snail Family Transcription Factors, Endothelial PAS Domain-Containing Protein 1, Animals, Base Sequence, Cell Movement, Gene Expression Regulation, Humans, Molecular Sequence Data, Protein Binding, RNA, Messenger, Transcription Factors, Cell Hypoxia, Response Elements, Electrophoretic Mobility Shift Assay, Endothelial Cells, Chromatin Immunoprecipitation, Mice, Basic Helix-Loop-Helix Proteins, Hypoxia-Inducible Factor 1, alpha Subunit, Epithelial-Mesenchymal Transition

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Mouse Snail Is a Target Gene for HIF

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