STATs in oncogenesis

Bowman, Tammy; Garcia, Roy; Turkson, James; Jove, Richard

doi:10.1038/sj.onc.1203527

Cited by 1,743Cytokine Signaling Pathways and InteractionsProtein Tyrosine PhosphatasesNF-κB Signaling Pathways

STATs in oncogenesis

Bowman, Tammy, Garcia, Roy, Turkson, James, Jove, Richard·2000·Oncogene

DOI 10.1038/sj.onc.1203527

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Abstract

Since their discovery as key mediators of cytokine signaling, considerable progress has been made in defining the structure-function relationships of Signal Transducers and Activators of Transcription (STATs). In addition to their central roles in normal cell signaling, recent studies have demonstrated that diverse oncoproteins can activate specific STATs (particularly Stat3 and Stat5) and that constitutively-activated STAT signaling directly contributes to oncogenesis. Furthermore, extensive surveys of primary tumors and cell lines derived from tumors indicate that inappropriate activation of specific STATs occurs with surprisingly high frequency in a wide variety of human cancers. Together, these findings provide compelling evidence that aberrant STAT activation associated with oncogenesis is not merely adventitious but instead contributes to the process of malignant transformation. These studies are beginning to reveal the molecular mechanisms leading to STAT activation in the context of oncogenesis, and candidate genes regulated by STATs that may contribute to oncogenesis are being identified. Recent studies suggest that activated STAT signaling participates in oncogenesis by stimulating cell proliferation and preventing apoptosis. This review presents the evidence for critical roles of STATs in oncogenesis and discusses the potential for development of novel cancer therapies based on mechanistic understanding of STAT signaling. Oncogene (2000).

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Mapping of Stat3 serine phosphorylation to a single residue (727) and evidence that serine phosphorylation has no influence on DNA binding of Stat1 and Stat3
Wen, Z. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.11.2062 · Cited by 328 · see citing works
Jak-STAT Signaling Induced by the v- abl oncogene
Danial, N. N., Pernis, A., & Rothman, P. B. (1995) · Science · doi:10.1126/science.7569929 · Cited by 325 · see citing works
An amino acid substitution in the Drosophila hopTum‐l Jak kinase causes leukemia‐like hematopoietic defects.
Luo, H. R., Hanratty, W. P., & Dearolf, C. R. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07127.x · Cited by 322 · see citing works
Regulation of STAT‐dependent pathways by growth factors and cytokines
Leaman, D. W., Leung, S., Li, X.-X., & Stark, G. R. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.14.9002549 · Cited by 318 · see citing works
STAT-related transcription factors are constitutively activated in peripheral blood cells from acute leukemia patients
Gouilleux-Gruart, V, Gouilleux, F., Desaint, C., Claisse, J., Capiod, J., Delobel, J., Weber-Nordt, R., Dusanter-Fourt, I., Dreyfus, F., Groner, B., et al. (1996) · Blood · doi:10.1182/blood.v87.5.1692.1692 · Cited by 316 · see citing works
Constitutive activation of STAT proteins in primary lymphoid and myeloid leukemia cells and in Epstein-Barr virus (EBV)-related lymphoma cell lines
Weber-Nordt, R., Egen, C., Wehinger, J., Ludwig, W. D., Gouilleux‐Gruart, V., Mertelsmann, R. H., & Finke, J. (1996) · Blood · doi:10.1182/blood.v88.3.809.809 · Cited by 314 · see citing works
Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src
Barone, M. V., & Courtneidge, S. A. (1995) · Nature · doi:10.1038/378509a0 · Cited by 312 · see citing works
EGF receptor in neoplasia and metastasis
Khazaie, K., Schirrmacher, V., & Lichtner, R. B. (1993) · Cancer and Metastasis Reviews · doi:10.1007/bf00665957 · Cited by 288 · see citing works
Constitutive activation of JAKs and STATs in BCR-Abl-expressing cell lines and peripheral blood cells derived from leukemic patients
Chai, S. K., NICHOLS, G. L., & Rothman, P. B. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.10.4720 · Cited by 286 · see citing works
Erythropoietin Can Induce the Expression of Bcl-xLthrough Stat5 in Erythropoietin-dependent Progenitor Cell Lines
Silva, M., Benito, A., Sanz, C., Prósper, F., Ekhterae, D., Núñez, G., & Fernández-Luna, J. L. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.32.22165 · Cited by 277 · see citing works
Involvement of pp60c-src with two major signaling pathways in human breast cancer.
Luttrell, D. K., Lee, A., Lansing, T. J., Crosby, R. M., Jung, K., Willard, D., Luther, M., Rodriguez, M., Berman, J., & Gilmer, T. M. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.83 · Cited by 271 · see citing works
Signal Transducer and Activator of Transcription (STAT)5 Activation by BCR/ABL Is Dependent on Intact Src Homology (SH)3 and SH2 Domains of BCR/ABL and Is Required for Leukemogenesis
Nieborowska-Skorska, M., Wasik, M. A., Słupianek, A., Salomoni, P., Kitamura, T., Calabretta, B., & Skórski, T. (1999) · The Journal of Experimental Medicine · doi:10.1084/jem.189.8.1229 · Cited by 271 · see citing works
Proliferation of adult T cell leukemia/lymphoma cells is associated with the constitutive activation of JAK/STAT proteins
Takemoto, S., Mulloy, J. C., Cereseto, A., Migone, T.-S., Patel, B. K. R., Matsuoka, M., Yamaguchi, K., Takatsuki, K., Kamihira, S., White, J. D., et al. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.25.13897 · Cited by 270 · see citing works
Requirement for Ras/Rac1-Mediated p38 and c-Jun N-Terminal Kinase Signaling in Stat3 Transcriptional Activity Induced by the Src Oncoprotein
Turkson, J., Bowman, T. L., Adnane, J., Zhang, Y., Djeu, J. Y., Sekharam, M., Frank, D. A., Holzman, L. B., Wu, J., Sebti, S. M., et al. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.11.7519 · Cited by 256 · see citing works
Self-citation
Rapid inhibition of interleukin-6 signaling and Stat3 activation mediated by mitogen-activated protein kinases.
Sengupta, T. K., Talbot, E. S., Scherle, P., & Ivashkiv, L. (1998) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.95.19.11107 · Cited by 245 · see citing works
Transformation of hematopoietic cell lines to growth‐factor independence and induction of a fatal myelo‐ and lymphoproliferative disease in mice by retrovirally transduced TEL/JAK2 fusion genes
Schwaller, J., Frantsve‐Hawley, J., Aster, J. C., Williams, I. R., Tomasson, M. H., Ross, T. S., Peeters, P. J., Rompaey, L. V., Etten, R. A. V., Ilaria, R. L., et al. (1998) · The EMBO Journal · doi:10.1093/emboj/17.18.5321 · Cited by 245 · see citing works
Inhibition of pp60c-Src reduces Bcl-XL expression and reverses the transformed phenotype of cells overexpressing EGF and HER-2 receptors
Karni, R., Jove, R., & Levitzki, A. (1999) · Oncogene · doi:10.1038/sj.onc.1202835 · Cited by 242 · see citing works
Self-citation
B lymphocytes from patients with chronic lymphocytic leukemia contain signal transducer and activator of transcription (STAT) 1 and STAT3 constitutively phosphorylated on serine residues.
Frank, D. A., Mahajan, S., & Ritz, J. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119869 · Cited by 238 · see citing works
Essential and non‐redundant roles of p48 (ISGF3γ) and IRF‐1 in both type I and type II interferon responses, as revealed by gene targeting studies
Kimura, T., Kadokawa, Y., Harada, H., Matsumoto, M., Sato, M., Kashiwazaki, Y., Tarutani, M., Tan, R. S., Takasugi, T., Matsuyama, T., et al. (1996) · Genes to Cells · doi:10.1046/j.1365-2443.1996.08008.x · Cited by 233 · see citing works
Generation of plasmacytomas with the chromosomal translocation t(12;15) in interleukin 6 transgenic mice
Suematsu, S., Matsusaka, T., Matsuda, T., Ohno, S., Miyazaki, J., Yamamura, K., Hirano, T., & Kishimoto, T. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.1.232 · Cited by 227 · see citing works
Elevated levels of members of the STAT family of transcription factors in breast carcinoma nuclear extracts
Watson, C. J. E., & Miller, W. R. (1995) · British Journal of Cancer · doi:10.1038/bjc.1995.162 · Cited by 226 · see citing works
Serine Phosphorylation and Negative Regulation of Stat3 by JNK
Lim, C. P., & Cao, X. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.43.31055 · Cited by 225 · see citing works
Protein Kinase C δ Associates with and Phosphorylates Stat3 in an Interleukin-6-dependent Manner*
Jain, N., Zhang, T., Wei, H.-K., Li, W.-Q., & Cao, X. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.34.24392 · Cited by 222 · see citing works
Activation of Jak/STAT proteins involved in signal transduction pathway mediated by receptor for interleukin 2 in malignant T lymphocytes derived from cutaneous anaplastic large T-cell lymphoma and Sezary syndrome.
Zhang, Q., Nowak, I. A., Vonderheid, E. C., Rook, A. H., Kadin, M. E., Nowell̀, P. C., Shaw, L. M. J., & Wasik, M. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.17.9148 · Cited by 221 · see citing works
Constitutive activation of a slowly migrating isoform of Stat3 in mycosis fungoides: Tyrphostin AG490 inhibits Stat3 activation and growth of mycosis fungoides tumor cell lines
Nielsen, M., Kaltoft, K., Nordahl, M., Röpke, C., Geisler, C., Mustelin, T., Dobson, P., Svejgaard, A., & Ødum, N. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6764 · Cited by 220 · see citing works
Protein Tyrosine Kinase Inhibitors as Novel Therapeutic Agents
Levitzki, A. (1999) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(98)00066-7 · Cited by 214 · see citing works
Repression of Stat3 activity by activation of mitogen-activated protein kinase (MAPK)
Jain, N., Zhang, T., Fong, S., Lim, C. P., & Cao, X. (1998) · Oncogene · doi:10.1038/sj.onc.1202238 · Cited by 213 · see citing works
STAT3 activation by cytokines utilizing gp130 and related transducers involves a secondary modification requiring an H7-sensitive kinase.
Boulton, T. G., Zhong, Z.-H., Wen, Z., Darnell, J. E., Jr., Stahl, N., & Yancopoulos, G. D. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.15.6915 · Cited by 204 · see citing works
Activation of STAT Transcription Factors in Oncogenic Tyrosine Kinase Signaling
Garcia, R., & Jove, R. (1998) · Journal of Biomedical Science · doi:10.1007/bf02258360 · Cited by 202 · see citing works
Self-citation
STAT5 Activation by BCR-Abl Contributes to Transformation of K562 Leukemia Cells
de Groot, R. P., Raaijmakers, J. A. M., Lammers, J. J., Jove, R., & Koenderman, L. (1999) · Blood · doi:10.1182/blood.v94.3.1108.415k07_1108_1112 · Cited by 188 · see citing works
Self-citation
STAT proteins as novel targets for cancer therapy
Catlett-Falcone, R., Dalton, W. S., & Jove, R. (1999) · Current Opinion in Oncology · doi:10.1097/00001622-199911000-00010 · Cited by 185 · see citing works
Self-citation
Interferon-α Resistance in a Cutaneous T-Cell Lymphoma Cell Line Is Associated With Lack of STAT1 Expression
Sun, W. H., Pabon, C., Alsayed, Y. M., Huang, P. P., Jandeska, S., Shahab Uddin, M. S., Platanias, L. C., & Rosen, S. T. (1998) · Blood · doi:10.1182/blood.v91.2.570 · Cited by 169 · see citing works
Cytosolic Tyrosine Dephosphorylation of STAT5
Yu, C., Jin, Y., & Burakoff, S. J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.1.599 · Cited by 168 · see citing works
Interleukin‐2 activation of STAT5 requires the convergent action of tyrosine kinases and a serine/threonine kinase pathway distinct from the Raf1/ERK2 MAP kinase pathway.
Beadling, C., Ng, J., Babbage, J. W., & Cantrell, D. A. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00541.x · Cited by 167 · see citing works
IL-3 dependent regulation of Bcl-xL gene expression by STAT5 in a bone marrow derived cell line
Dumon, S., Santos, S. C. R., Debierre-Grockiego, F., Gouilleux‐Gruart, V., Petit, L., Boucheron, C., Mollat, P., Gisselbrecht, S., & Gouilleux, F. (1999) · Oncogene · doi:10.1038/sj.onc.1202796 · Cited by 158 · see citing works
Src kinases and not JAKs activate STATs during IL-3 induced myeloid cell proliferation
Chaturvedi, P., Reddy, M. R., & Reddy, E. P. (1998) · Oncogene · doi:10.1038/sj.onc.1201972 · Cited by 145 · see citing works
STAT3 Is a Serine Kinase Target in T Lymphocytes
Ng, J., & Cantrell, D. A. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.39.24542 · Cited by 141 · see citing works
The Functional Synergy Between IL-12 and IL-2 Involves p38 Mitogen-Activated Protein Kinase and Is Associated with the Augmentation of STAT Serine Phosphorylation
Gollob, J., Schnipper, C. P., Murphy, E. A., Ritz, J., & Frank, D. A. (1999) · The Journal of Immunology · doi:10.4049/jimmunol.162.8.4472 · Cited by 139 · see citing works
Rational design of a receptor super‐antagonist of human interleukin‐6.
Savino, R., Ciapponi, L., Lahm, A., Demartis, A., Cabibbo, A., Toniatti, C., Delmastro, P., Altamura, S., & Ciliberto, G. (1994) · EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06931.x · Cited by 134 · see citing works
Involvement of Proteasomes in Regulating Jak-STAT Pathways upon Interleukin-2 Stimulation
Yu, C., & Burakoff, S. J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.22.14017 · Cited by 129 · see citing works
Very high frequency of lymphoma induction by a chemical carcinogen in pim-1 transgenic mice
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A Single Amino Acid Substitution in the v-Eyk Intracellular Domain Results in Activation of Stat3 and Enhances Cellular Transformation
Besser, D., Bromberg, J., Darnell, J. E., Jr., & Hanafusa, H. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.2.1401 · Cited by 123 · see citing works
Negative regulation of cytokine signaling: STAT-induced STAT inhibitor
Naka, T., Fujimoto, M., & Kishimoto, T. (1999) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(99)01454-1 · Cited by 122 · see citing works
STAT Signaling in the Pathogenesis and Treatment of Cancer
Frank, D. A. (1999) · Molecular Medicine · doi:10.1007/bf03403538 · Cited by 116 · see citing works
Transcription factor activity of STAT proteins: structural requirements and regulation by phosphorylation and interacting proteins
Decker, T., & Kovarik, P. (1999) · Cellular and Molecular Life Sciences · doi:10.1007/s000180050393 · Cited by 110 · see citing works
p16 and p21WAF1 Protein Expression in Melanocytic Tumors by Immunohistochemistry
Sparrow, L. E., Eldon, M. J., English, D. R., & Heenan, P. J. (1998) · American Journal of Dermatopathology · doi:10.1097/00000372-199806000-00006 · Cited by 105 · see citing works
Constitutive activation of the Janus kinase-STAT pathway in T lymphoma overexpressing the Lck protein tyrosine kinase
Yu, C., Jove, R., & Burakoff, S. J. (1997) · The Journal of Immunology · doi:10.4049/jimmunol.159.11.5206 · Cited by 105 · see citing works
Self-citation
Abrogation of Interleukin-3 Dependence of Myeloid Cells by the v-src Oncogene Requires SH2 and SH3 Domains Which Specify Activation of STATs
Chaturvedi, P., Sharma, S., & Reddy, E. P. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.6.3295 · Cited by 101 · see citing works
Growth Hormone Regulation of SIRP and SHP-2 Tyrosyl Phosphorylation and Association
Stofega, M. R., Wang, H., Ullrich, A., & Carter‐Su, C. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.12.7112 · Cited by 100 · see citing works
Evidence for the involvement of pim‐2, a new common proviral insertion site, in progression of lymphomas.
Breuer, M. L., Cuypers, H. T. M., & Berns, A. J. M. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03434.x · Cited by 97 · see citing works
Activation of STAT transcription factors by herpesvirus Saimiri Tip-484 requires p56lck
Lund, T. C., Garcia, R., Medveczky, M. M., Jove, R., & Medveczky, P. G. (1997) · Journal of Virology · doi:10.1128/jvi.71.9.6677-6682.1997 · Cited by 96 · see citing works
Self-citation
Fusion of the ets Transcription Factor TEL to Jak2 Results in Constitutive Jak-Stat Signaling
Ho, J. M.-Y., Beattie, B. K., Squire, J. A., Frank, D. A., & Barber, D. L. (1999) · Blood · doi:10.1182/blood.v93.12.4354 · Cited by 96 · see citing works
Stat3 Plays an Important Role in Oncogenic Ros- and Insulin-like Growth Factor I Receptor-induced Anchorage-independent Growth
Zong, C. S., Zeng, L., Jiang, Y., Sadowski, H. B., & Wang, L. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.43.28065 · Cited by 91 · see citing works
Extracellular signal-regulated protein kinase (ERK)-dependent and ERK-independent pathways target STAT3 on serine-727 in human neutrophils stimulated by chemotactic factors and cytokines
Kuroki, M., & O’Flaherty, J. T. (1999) · Biochemical Journal · doi:10.1042/bj3410691 · Cited by 88 · see citing works
The SH3 Domain Contributes to BCR/ABL-Dependent Leukemogenesis In Vivo: Role in Adhesion, Invasion, and Homing
Skórski, T., Nieborowska-Skorska, M., Wlodarski, P. K., Wasik, M. A., Trotta, R., Kanakaraj, P., Salomoni, P., Antonyak, M., Martinez, R., Majewski, M., et al. (1998) · Blood · doi:10.1182/blood.v91.2.406 · Cited by 86 · see citing works
Constitutive Activation of JAK1 in Src-transformed Cells
Campbell, G. S., Yu, C., Jove, R., & Carter‐Su, C. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.5.2591 · Cited by 85 · see citing works
Self-citation
Kinase Activation of the Non-receptor Tyrosine Kinase Etk/BMX Alone Is Sufficient to Transactivate STAT-mediated Gene Expression in Salivary and Lung Epithelial Cells*
Wen, X., Lin, H. H., Shih, H.-M., Kung, H., & Ann, D. K. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.53.38204 · Cited by 80 · see citing works
Unique signal transduction of Eyk: constitutive stimulation of the JAK‐STAT pathway by an oncogenic receptor‐type tyrosine kinase.
Zong, C. S., Yan, R., August, A., Darnell, J. E., Jr., & Hanafusa, H. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00829.x · Cited by 77 · see citing works
Cyclin D1 and cyclin E expression in malignant thyroid cells and in human thyroid carcinomas
Lazzereschi, D., Sambuco, L., Scalzo, C. C., Ranieri, A., Mincione, G., Nardi, F., & Colletta, G. (1998) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19980610)76:6 · Cited by 75 · see citing works
Activation of STAT3 by the c-Fes Protein-tyrosine Kinase
Nelson, K. L., Rogers, J. A., Bowman, T. L., Jove, R., & Smithgall, T. E. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.12.7072 · Cited by 74 · see citing works
Self-citation
Constitutive Activation of the JAK2/STAT5 Signal Transduction Pathway Correlates With Growth Factor Independence of Megakaryocytic Leukemic Cell Lines
Liu, R. Y., Fan, C. L., Garcia, R., Jove, R., & Zuckerman, K. S. (1999) · Blood · doi:10.1182/blood.v93.7.2369 · Cited by 70 · see citing works
Self-citation
Signal Transducer and Activator of Transcription-3 Serine Phosphorylation by Insulin Is Mediated by a Ras/Raf/MEK-Dependent Pathway
Ceresa, B. P., Horvath, C. M., & Pessin, J. E. (1997) · Endocrinology · doi:10.1210/endo.138.10.5266 · Cited by 64 · see citing works
Direct Interaction of Jak1 and v-Abl Is Required for v-Abl-Induced Activation of STATs and Proliferation
Danial, N. N., Losman, J. A., Lu, T., Yip, N. H., Krishnan, K., Krolewski, J. J., Goff, S. P., Wang, J. Y. J., & Rothman, P. B. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.11.6795 · Cited by 63 · see citing works
The role of transforming growth factor-β1, -β2, and -β3 in androgen-responsive growth of NRP-152 rat prostatic epithelial cells
Lucia, M. S., Sporn, M. B., Roberts, A. B., Stewart, L. V., & Danielpour, D. (1998) · Journal of Cellular Physiology · doi:10.1002/(sici)1097-4652(199805)175:2 · Cited by 52 · see citing works
The Lck Binding Domain of Herpesvirus Saimiri Tip-484 Constitutively Activates Lck and STAT3 in T Cells
Lund, T. C., Prator, P. C., Medveczky, M. M., & Medveczky, P. G. (1999) · Journal of Virology · doi:10.1128/jvi.73.2.1689-1694.1999 · Cited by 51 · see citing works
Prolonged STAT1 activation related to the growth arrest of malignant lymphoma cells by interferon-alpha.
Grimley, P., Fang, H., Rui, H., Petricoin, E. F., Ray, S., Dong, F., Fields, K., Hu, R., Zoon, K., Audet, S., et al. (1998) · Blood · doi:10.1182/blood.v91.8.3017.3017_3017_3027 · Cited by 42 · see citing works
Effect of IL-6 receptor antisense oligodeoxynucleotide on in vitro proliferation of myeloma cells.
Keller, E. T., & Ershler, W. B. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.154.8.4091 · Cited by 38 · see citing works
p53, p21(Waf1/Cip1) and cyclin D1 protein expression and prognosis in esophageal cancer *
Kuwahara, M., Hirai, T., Yoshida, K., Yamashita, Y., Hihara, J., Inoue, H., & Toge, T. (1999) · Diseases of the Esophagus · doi:10.1046/j.1442-2050.1999.00034.x · Cited by 34 · see citing works
Expression of v-src in mammary epithelial cells induces transcription via STAT3
Smith, P. D., & CROMPTON, M. R. (1998) · Biochemical Journal · doi:10.1042/bj3310381 · Cited by 33 · see citing works
Expression of p21WAF1/CIP1 in Soft Tissue Sarcomas: A Comparative Immunohistochemical Study with p53 and Ki-67
Pindzola, J. A., Palazzo, J., Kovatich, A. J., Tuma, B., & Nobel, M. (1998) · Pathology - Research and Practice · doi:10.1016/s0344-0338(98)80127-1 · Cited by 21 · see citing works
Cytokine signal transduction in P19 embryonal carcinoma cells: regulation of Stat3-mediated transactivation occurs independently of p21ras-Erk signaling.
van Puijenbroek, A. V., van der Saag, P. T., & Coffer, P. (1999) · Experimental Cell Research · doi:10.1006/excr.1999.4576 · Cited by 15 · see citing works
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(1995) · Aerobiologia · doi:10.1007/bf02447211 · Cited by 2 · see citing works
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Rodriguez-Palmero, M. (1999) · doi:10.1002/(sici)1521-4141(199912)29:12
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Oncogenic kinase signalling.
Blume-Jensen, P., & Hunter, T. (2001) · Nature · doi:10.1038/35077225 · Cited by 3,738 · see citing works
STATs: transcriptional control and biological impact
Levy, D. E., & Darnell, J. E. (2002) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm909 · Cited by 3,201 · see citing works
The STATs of cancer — new molecular targets come of age
Yu, H., & Jove, R. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1275 · Cited by 2,278 · see citing works
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Transcription factors as targets for cancer therapy
Darnell, J. E. (2002) · Nature Reviews Cancer · doi:10.1038/nrc906 · Cited by 1,194 · see citing works
Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells
Wang, T., Niu, G., Kortylewski, M., Burdelya, L. G., Shain, K. H., Zhang, S., Bhattacharya, R., Gabrilovich, D. I., Heller, R. F., Coppola, D., et al. (2003) · Nature Medicine · doi:10.1038/nm976 · Cited by 1,159 · see citing works
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Signaling through the JAK/STAT pathway, recent advances and future challenges
Kisseleva, T., Bhattacharya, S., Braunstein, J., & Schindler, C. (2002) · Gene · doi:10.1016/s0378-1119(02)00398-0 · Cited by 1,158 · see citing works
Cytokine Signaling in 2002
O’Shea, J. J., Gadina, M., & Schreiber, R. D. (2002) · Cell · doi:10.1016/s0092-8674(02)00701-8 · Cited by 1,119 · see citing works
Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention.
Buettner, R., Mora, L. B., & Jove, R. (2002) · PubMed · Cited by 1,021 · see citing works
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Constitutive Stat3 activity up-regulates VEGF expression and tumor angiogenesis
Niu, G., Wright, K. L., Huang, M., Song, L., Haura, E., Turkson, J., Zhang, S., Wang, T., Sinibaldi, D., Coppola, D., et al. (2002) · Oncogene · doi:10.1038/sj.onc.1205260 · Cited by 1,207 · see citing works
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The roles of IFNγ in protection against tumor development and cancer immunoediting
Ikeda, H., Old, L. J., & Schreiber, R. D. (2002) · Cytokine & Growth Factor Reviews · doi:10.1016/s1359-6101(01)00038-7 · Cited by 899 · see citing works
Role of Src expression and activation in human cancer
Irby, R., & Yeatman, T. J. (2000) · Oncogene · doi:10.1038/sj.onc.1203912 · Cited by 856 · see citing works
Stat proteins and oncogenesis
Bromberg, J. (2002) · Journal of Clinical Investigation · doi:10.1172/jci15617 · Cited by 846 · see citing works
Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells
Garcia, R., Bowman, T. L., Niu, G., Yu, H., Minton, S., Muro‐Cacho, C., Cox, C. E., Falcone, R., Fairclough, R., Parsons, S. J., et al. (2001) · Oncogene · doi:10.1038/sj.onc.1204349 · Cited by 747 · see citing works
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Selective chemical probe inhibitor of Stat3, identified through structure-based virtual screening, induces antitumor activity
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“Sorafenib, a small-molecule kinase insert domain receptor inhibitor, activates autophagy in multiple liver cancer cell lines through targeting STAT3 and reducing MCL1 expression (Tai et al., 2013).”
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STAT proteins: From normal control of cellular events to tumorigenesis
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Authors: Bowman, T., Garcia, R., Turkson, J., & Jove, R.
Affiliations: Moffitt Cancer Center (US)
University of South Florida (US)
ORCID: Turkson, James
Venue: Oncogene
Publisher: Springer Science and Business Media LLC
Published: 2000-05-25
Volume: 19
Issue: 21
Pages: 2474-2488
ISSN: 0950-9232 (ISSN-L)
1476-5594
DOI: 10.1038/sj.onc.1203527
OpenAlex: W2024282024
Cited by: 1,743
References: 152
Citations by year: 2026: 16 · 2025: 18 · 2024: 18 · 2023: 22 · 2022: 39 · 2021: 48 · 2020: 44 · 2019: 45 · 2018: 59 · 2017: 63 · 2016: 58 · 2015: 104 · 2014: 80 · 2013: 82 · 2012: 89
FWCI: 7.25
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Oncogene (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Oncology › Cytokine Signaling Pathways and Interactions
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Tyrosine Phosphatases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
Keywords: STAT, signal transducer and activator of transcription, carcinogenesis, STAT3, STAT5, malignant transformation, cytokine signaling, cell proliferation, apoptosis, cancer therapy targets, cancer cell lines
MeSH terms: Animals, Cell Transformation, Neoplastic, DNA-Binding Proteins, Humans, Neoplasms, Phosphorylation, Phosphoserine, Protein-Tyrosine Kinases, Signal Transduction, Oncogene Proteins, Trans-Activators, Gene Expression Regulation, Neoplastic, STAT1 Transcription Factor

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STATs in oncogenesis

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