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Abstract
Deregulated activation of STAT3 is frequently associated with many human hematological and epithelial malignancies, including gastric cancer. While exaggerated STAT3 signaling facilitates an antiapoptotic, proangiogenic, and proproliferative environment for neoplastic cells, the molecular mechanisms leading to STAT3 hyperactivation remain poorly understood. Using the gp130Y757F/Y757F mouse model of gastric cancer, which carries a mutated gp130 cytokine receptor signaling subunit that cannot bind the negative regulator of cytokine signaling SOCS3 and is characterized by hyperactivation of the signaling molecules STAT1 and STAT3, we have provided genetic evidence that IL-11 promotes chronic gastric inflammation and associated tumorigenesis. Expression of IL-11 was increased in gastric tumors in gp130Y757F/Y757F mice, when compared with unaffected gastric tissue in wild-type mice, while gp130Y757F/Y757F mice lacking the IL-11 ligand–binding receptor subunit (IL-11Rα) showed normal gastric STAT3 activation and IL-11 expression and failed to develop gastric tumors. Furthermore, reducing STAT3 activity in gp130Y757F/Y757F mice, either genetically or by therapeutic administration of STAT3 antisense oligonucleotides, normalized gastric IL-11 expression and alleviated gastric tumor burden. Surprisingly, the genetic reduction of STAT1 expression also reduced gastric tumorigenesis in gp130Y757F/Y757F mice and coincided with reduced gastric inflammation and IL-11 expression. Collectively, our data have identified IL-11 as a crucial cytokine promoting chronic gastric inflammation and associated tumorigenesis mediated by excessive activation of STAT3 and STAT1.
Authors
Matthias Ernst, Meri Najdovska, Dianne Grail, Therese Lundgren-May, Michael Buchert, Hazel Tye, Vance B. Matthews, Jane Armes, Prithi S. Bhathal, Norman R. Hughes, Eric G. Marcusson, James G. Karras, Songqing Na, Jonathon D. Sedgwick, Paul J. Hertzog, Brendan J. Jenkins
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Frontiers in immunology | 2014 |
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Revisiting STAT3 signalling in cancer: new and unexpected biological functions
H Yu, H Lee, A Herrmann, R Buettner, R Jove |
Nature Reviews Cancer | 2014 |
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Role of the tumor microenvironment in the pathogenesis of gastric carcinoma
HW Chung, JB Lim |
World journal of gastroenterology : WJG | 2014 |
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Inhibition of the JAK2/STAT3 Pathway Reduces Gastric Cancer Growth In Vitro and In Vivo
LM Judd, TR Menheniott, H Ling, CB Jackson, M Howlett, A Kalantzis, W Priebe, AS Giraud |
PloS one | 2014 |
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p38MAPK Plays a Crucial Role in Stromal-Mediated Tumorigenesis
E Alspach, KC Flanagan, X Luo, MK Ruhland, H Huang, E Pazolli, MJ Donlin, T Marsh, D Piwnica-Worms, J Monahan, DV Novack, SS McAllister, SA Stewart |
Cancer Discovery | 2014 |
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Non-cell-autonomous driving of tumour growth supports sub-clonal heterogeneity
A Marusyk, DP Tabassum, PM Altrock, V Almendro, F Michor, K Polyak |
Nature | 2014 |
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Inhibition of protein kinase II (CK2) prevents induced signal transducer and activator of transcription (STAT) 1/3 and constitutive STAT3 activation
Aparicio-Siegmund S, Sommer J, Monhasery N, Schwanbeck R, Keil E, Finkenstädt D, Pfeffer K, Rose-John S, Scheller J, Garbers C |
Oncotarget | 2014 |
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Autocrine production of Interleukin-11 mediates tumorigenicity in hypoxic cancer cells
Barbara Onnis, Nicole Fer, Annamaria Rapisarda, Victor Perez, Giovanni Melillo |
Journal of Clinical Investigation | 2013 |
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Therapeutic mTorc1 inhibition restricts inflammation-associated gastrointestinal tumorigenesis in mice
Stefan Thiem, Thomas P. Pierce, Michelle Palmieri, Tracy L. Putoczki, Michael Buchert, Adele Preaudet, Ryan O. Farid, Chris Love, Bruno Catimel, Zhengdeng Lei, Steve Rozen, Veena Gopalakrishnan, Fred Schaper, Michael Hallek, Alex Boussioutas, Patrick Tan, Andrew Jarnicki, Matthias Ernst |
Journal of Clinical Investigation | 2013 |
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Mouse Models of Gastric Cancer
Y Hayakawa, J Fox, T Gonda, D Worthley, S Muthupalani, T Wang |
Cancers | 2013 |
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Suppression of cytokine signaling: The SOCS perspective
EM Linossi, JJ Babon, DJ Hilton, SE Nicholson |
Cytokine & Growth Factor Reviews | 2013 |
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SOCS3
CA White, NA Nicola |
JAK-STAT | 2013 |
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The Gastrointestinal Tumor Microenvironment
M Quante, J Varga, TC Wang, FR Greten |
Gastroenterology | 2013 |
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Interleukin-23 is sufficient to induce rapid de novo gut tumorigenesis, independent of carcinogens, through activation of innate lymphoid cells
IH Chan, R Jain, MS Tessmer, D Gorman, R Mangadu, M Sathe, F Vives, C Moon, E Penaflor, S Turner, G Ayanoglu, C Chang, B Basham, JB Mumm, RH Pierce, JH Yearley, TK McClanahan, JH Phillips, DJ Cua, EP Bowman, RA Kastelein, D LaFace |
Mucosal Immunology | 2013 |
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Innate lymphoid cells sustain colon cancer through production of interleukin-22 in a mouse model
S Kirchberger, DJ Royston, O Boulard, E Thornton, F Franchini, RL Szabady, O Harrison, F Powrie |
Journal of Experimental Medicine | 2013 |
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Deletion of Intestinal Epithelial Cell STAT3 Promotes T-Lymphocyte STAT3 Activation and Chronic Colitis Following Acute Dextran Sodium Sulfate Injury in Mice:
TA Willson, I Jurickova, M Collins, LA Denson |
Inflammatory Bowel Diseases | 2013 |
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Exacerbated inflammatory arthritis in response to hyperactive gp130 signalling is independent of IL-17A
GW Jones, CJ Greenhill, JO Williams, MA Nowell, AS Williams, BJ Jenkins, SA Jones |
Annals of the rheumatic diseases | 2013 |
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Interleukin-6 mediates epithelial-stromal interactions and promotes gastric tumorigenesis
H Kinoshita, Y Hirata, H Nakagawa, K Sakamoto, Y Hayakawa, R Takahashi, W Nakata, K Sakitani, T Serizawa, Y Hikiba, M Akanuma, W Shibata, S Maeda, K Koike |
PloS one | 2013 |
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IL-11: a prominent pro-tumorigenic member of the IL-6 family
SI Grivennikov |
Cancer Cell | 2013 |
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Tying the knot between cytokine and toll-like receptor signaling in gastrointestinal tract cancers.
Tye H, Jenkins BJ |
Cancer Science | 2013 |
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Interleukin-6 inhibition of peroxisome proliferator-activated receptor alpha expression is mediated by JAK2- and PI3K-induced STAT1/3 in HepG2 hepatocyte cells.
Chew GS, Myers S, Shu-Chien AC, Muhammad TS |
Molecular and Cellular Biochemistry | 2013 |
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Genetic partitioning of interleukin-6 signalling in mice dissociates Stat3 from Smad3-mediated lung fibrosis
RJ O'Donoghue, DA Knight, CD Richards, CM Prêle, HL Lau, AG Jarnicki, J Jones, S Bozinovski, R Vlahos, S Thiem, BS McKenzie, B Wang, P Stumbles, GJ Laurent, RJ McAnulty, S Rose-John, HJ Zhu, GP Anderson, MR Ernst, SE Mutsaers |
EMBO Molecular Medicine | 2012 |
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Nardilysin and ADAM proteases promote gastric cancer cell growth by activating intrinsic cytokine signalling via enhanced ectodomain shedding of TNF-α
K Kanda, H Komekado, T Sawabu, S Ishizu, Y Nakanishi, M Nakatsuji, R Akitake-Kawano, M Ohno, Y Hiraoka, M Kawada, K Kawada, Y Sakai, K Matsumoto, M Kunichika, T Kimura, H Seno, E Nishi, T Chiba |
EMBO Molecular Medicine | 2012 |
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The biology and mechanism of action of suppressor of cytokine signaling 3
JJ Babon, NA Nicola |
Growth Factors | 2012 |
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Constitutively active mutant gp130 receptor protein from inflammatory hepatocellular adenoma is inhibited by an anti-gp130 antibody that specifically neutralizes interleukin 11 signaling
J Sommer, T Effenberger, E Volpi, GH Waetzig, M Bernhardt, J Suthaus, C Garbers, S Rose-John, DM Floss, J Scheller |
The Journal of biological chemistry | 2012 |
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Transgenic Expression of Interferon-γ in Mouse Stomach Leads to Inflammation, Metaplasia, and Dysplasia
LJ Syu, M El-Zaatari, KA Eaton, Z Liu, M Tetarbe, TM Keeley, J Pero, J Ferris, D Wilbert, A Kaatz, X Zheng, X Qiao, M Grachtchouk, DL Gumucio, JL Merchant, LC Samuelson, AA Dlugosz |
The American Journal of Pathology | 2012 |
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A role for transcription factor STAT3 signaling in oncogene smoothened-driven carcinogenesis
D Gu, Q Fan, X Zhang, J Xie |
The Journal of biological chemistry | 2012 |
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Genetic Aspects of Gastric Cancer Instability
P Hudler |
The Scientific World JOURNAL | 2012 |
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Interleukin-11 Promotes the Progress of Gastric Carcinoma via Abnormally Expressed Versican
Z Zhang, J Zhang, L Miao, K Liu, S Yang, C Pan, B Jiao |
International journal of biological sciences | 2012 |
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Helicobacter pylori CagA Triggers Expression of the Bactericidal Lectin REG3γ via Gastric STAT3 Activation
KS Lee, A Kalantzis, CB Jackson, L O'Connor, N Murata-Kamiya, M Hatakeyama, LM Judd, AS Giraud, TR Menheniott |
PloS one | 2012 |
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Unphosphorylated STAT1 promotes sarcoma development through repressing expression of Fas and bad and conferring apoptotic resistance
MA Zimmerman, NT Rahman, D Yang, G Lahat, AJ Lazar, RE Pollock, D Lev, K Liu |
Cancer research | 2012 |
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MicroRNA-30c targets cytoskeleton genes involved in breast cancer cell invasion
J Bockhorn, K Yee, YF Chang, A Prat, D Huo, C Nwachukwu, R Dalton, S Huang, KE Swanson, CM Perou, OI Olopade, MF Clarke, GL Greene, H Liu |
Breast Cancer Research and Treatment | 2012 |
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The binding characteristics of a cyclic nonapeptide, c(CGRRAGGSC), in LNCaP human prostate cancer cells
C Gu, L Liu, Y He, J Jiang, Z Yang, Q Wu |
Oncology Letters | 2012 |
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Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia
M Quante, G Bhagat, JA Abrams, F Marache, P Good, MD Lee, Y Lee, R Friedman, S Asfaha, Z Dubeykovskaya, U Mahmood, JL Figueiredo, J Kitajewski, C Shawber, CJ Lightdale, AK Rustgi, TC Wang |
Cancer Cell | 2012 |
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STAT1 gene expression is enhanced by nuclear EGFR and HER2 via cooperation With STAT3: STAT1 REGULATION BY NUCLEAR EGFR AND STAT3
W Han, RL Carpenter, X Cao, HW Lo |
Molecular Carcinogenesis | 2012 |
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T lymphocyte Smad4 deficiency leads to the Th17-associated development of premalignant gastro-duodenal lesions in mice
Jennifer Hahn, Vincent Falck, Frank Jirik |
Journal of Clinical Investigation | 2011 |
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Therapeutic strategies for the clinical blockade of IL-6/gp130 signaling
Simon Jones, Jürgen Scheller, Stefan Rose-John |
Journal of Clinical Investigation | 2011 |
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Stat3 and MMP7 Contribute to Pancreatic Ductal Adenocarcinoma Initiation and Progression
A Fukuda, SC Wang, JP 4th, AE Folias, A Liou, GE Kim, S Akira, KM Boucher, MA Firpo, SJ Mulvihill, M Hebrok |
Cancer Cell | 2011 |
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Tripartite motif 24 (Trim24/Tif1α) tumor suppressor protein is a novel negative regulator of interferon (IFN)/signal transducers and activators of transcription (STAT) signaling pathway acting through retinoic acid receptor α (Rarα) inhibition
J Tisserand, K Khetchoumian, C Thibault, D Dembélé, P Chambon, R Losson |
The Journal of biological chemistry | 2011 |
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IL-11 is a parietal cell cytokine that induces atrophic gastritis
M Howlett, HV Chalinor, JN Buzzelli, N Nguyen, IR van Driel, KM Bell, JG Fox, E Dimitriadis, TR Menheniott, AS Giraud, LM Judd |
Gut | 2011 |
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A functional and transcriptomic analysis of NET1 bioactivity in gastric cancer
G Bennett, D Sadlier, PP Doran, P Macmathuna, DW Murray |
BMC Cancer | 2011 |
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Inactivation of IL11 Signaling Causes Craniosynostosis, Delayed Tooth Eruption, and Supernumerary Teeth
P Nieminen, NV Morgan, AL Fenwick, S Parmanen, L Veistinen, ML Mikkola, PJ van der Spek, A Giraud, L Judd, S Arte, LA Brueton, SA Wall, IM Mathijssen, ER Maher, AO Wilkie, S Kreiborg, I Thesleff |
The American Journal of Human Genetics | 2011 |
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The intestinal microbiota, gastrointestinal environment and colorectal cancer: a putative role for probiotics in prevention of colorectal cancer?
MA Azcárate-Peril, M Sikes, JM Bruno-Bárcena |
American journal of physiology. Gastrointestinal and liver physiology | 2011 |
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IL-6 Mediates the Susceptibility of Glycoprotein 130 Hypermorphs to Toxoplasma gondii
JS Silver, JS Stumhofer, S Passos, M Ernst, CA Hunter |
Journal of immunology (Baltimore, Md. : 1950) | 2011 |
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Stat3: linking inflammation to epithelial cancer - more than a "gut" feeling?
A Jarnicki, T Putoczki, M Ernst |
Cell division | 2010 |
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MyD88-mediated signaling prevents development of adenocarcinomas of the colon: role of interleukin 18
R Salcedo, A Worschech, M Cardone, Y Jones, Z Gyulai, RM Dai, E Wang, W Ma, D Haines, C O'hUigin, FM Marincola, G Trinchieri |
Journal of Experimental Medicine | 2010 |
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Immunity, Inflammation, and Cancer
SI Grivennikov, FR Greten, M Karin |
Cell | 2010 |
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A Phosphotyrosine Proteomic Screen Identifies Multiple Tyrosine Kinase Signaling Pathways Aberrantly Activated in Malignant Mesothelioma
CW Menges, Y Chen, BT Mossman, J Chernoff, AT Yeung, JR Testa |
Genes & cancer | 2010 |
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Inflammation and oncogenesis: a vicious connection
SI Grivennikov, M Karin |
Current Opinion in Genetics & Development | 2010 |
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gp130 at the nexus of inflammation, autoimmunity, and cancer
JS Silver, CA Hunter |
Journal of leukocyte biology | 2010 |
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Pulmonary surfactant: an immunological perspective
ZC Chroneos, Z Sever-Chroneos, VL Shepherd |
Cellular physiology and biochemistry : international journal of experimental cellular physiology, biochemistry, and pharmacology | 2009 |
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Gastrin is an essential cofactor for helicobacter-associated gastric corpus carcinogenesis in C57BL/6 mice
S Takaishi, S Tu, ZA Dubeykovskaya, MT Whary, S Muthupalani, BH Rickman, AB Rogers, N Lertkowit, A Varro, JG Fox, TC Wang |
The American Journal of Pathology | 2009 |
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Signal transducer and activator of transcription-3, inflammation, and cancer: how intimate is the relationship?
BB Aggarwal, AB Kunnumakkara, KB Harikumar, SR Gupta, ST Tharakan, C Koca, S Dey, B Sung |
Annals of the New York Academy of Sciences | 2009 |
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STATs in cancer inflammation and immunity: a leading role for STAT3
H Yu, D Pardoll, R Jove |
Nature Reviews Cancer | 2009 |
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IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer
S Grivennikov, E Karin, J Terzic, D Mucida, GY Yu, S Vallabhapurapu, J Scheller, S Rose-John, H Cheroutre, L Eckmann, M Karin |
Cancer Cell | 2009 |
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Stat3 and the Inflammation/Acute Phase Response in Involution and Breast Cancer
S Pensa, CJ Watson, V Poli |
Journal of Mammary Gland Biology and Neoplasia | 2009 |
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Inflammation and Cancer: IL-6 and STAT3 Complete the Link
J Bromberg, TC Wang |
Cancer Cell | 2009 |
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IKK/NF-kappaB and STAT3 pathways: central signalling hubs in inflammation-mediated tumour promotion and metastasis
J Bollrath, FR Greten |
EMBO reports | 2009 |
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Enhanced interferon signaling pathway in oral cancer revealed by quantitative proteome analysis of microdissected specimens using 16O/18O labeling and integrated two-dimensional LC-ESI-MALDI tandem MS
LM Chi, CW Lee, KP Chang, SP Hao, HM Lee, Y Liang, C Hsueh, CJ Yu, IN Lee, YJ Chang, SY Lee, YM Yeh, YS Chang, KY Chien, JS Yu |
Molecular & cellular proteomics : MCP | 2009 |
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Interleukin 11 Inhibits Human Trophoblast Invasion Indicating a Likely Role in the Decidual Restraint of Trophoblast Invasion During Placentation1
P Paiva, LA Salamonsen, U Manuelpillai, E Dimitriadis |
Biology of reproduction | 2009 |
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Expression of anion exchanger 1 is associated with tumor progress in human gastric cancer.
Xu WQ, Song LJ, Liu Q, Zhao L, Zheng L, Yan ZW, Fu GH |
Journal of Cancer Research and Clinical Oncology | 2009 |
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What lurks beneath: IL-11, via Stat3, promotes inflammation-associated gastric tumorigenesis
Juanita L. Merchant |
Journal of Clinical Investigation | 2008 |
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Inflammation and stem cells in gastrointestinal carcinogenesis
M Quante, TC Wang |
Physiology (Bethesda, Md.) | 2008 |
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Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumours
S Rebouissou, M Amessou, G Couchy, K Poussin, S Imbeaud, C Pilati, T Izard, C Balabaud, P Bioulac-Sage, J Zucman-Rossi |
Nature | 2008 |
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