Interaction of JAK with steroid receptor function

The function of steroid receptors is not only regulated by steroid hormones, but also by multiple cellular signaling cascades activated by membrane-bound receptors which are stimulated by growth factors or cytokines. Cross-talk between JAK and steroid receptors plays a central role in the regulation of a multitude of physiological processes and aberrant signaling is involved in the development of numerous diseases including cancer. In this review we provide a brief summary of the knowledge of interactions between JAK and the function of steroid receptors in normal cells and tissues and in diseases.

[1]  M. Cleary,et al.  Minireview: Obesity and breast cancer: the estrogen connection. , 2009, Endocrinology.

[2]  A. Kornblihtt,et al.  Progestins Induce Transcriptional Activation of Signal Transducer and Activator of Transcription 3 (Stat3) via a Jak- and Src-Dependent Mechanism in Breast Cancer Cells , 2005, Molecular and Cellular Biology.

[3]  M. Krasil'nikov,et al.  Signal transducer and activator of transcription-3 and phosphatidylinositol-3 kinase as coordinate regulators of melanoma cell response to glucocorticoid hormones , 2002, The Journal of Steroid Biochemistry and Molecular Biology.

[4]  S. Collins The role of retinoids and retinoic acid receptors in normal hematopoiesis , 2002, Leukemia.

[5]  N. Moore,et al.  Steroid receptor phosphorylation: a key modulator of multiple receptor functions. , 2007, Molecular endocrinology.

[6]  T. Suga,et al.  Effects of testosterone, hypophysectomy and growth hormone treatment on clofibrate induction of peroxisomal beta-oxidation in female rat liver. , 1994, Biochemical pharmacology.

[7]  O. Silvennoinen,et al.  The Janus kinases (Jaks) , 2004, Genome Biology.

[8]  L. Ivashkiv,et al.  Inhibition of IL-2-induced Jak-STAT signaling by glucocorticoids. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[9]  E. Levin Minireview: Extranuclear steroid receptors: roles in modulation of cell functions. , 2011, Molecular endocrinology.

[10]  N. Weigel,et al.  Ligand-independent activation of steroid hormone receptors , 1998, Journal of Molecular Medicine.

[11]  Béatrice Desvergne,et al.  From molecular action to physiological outputs: peroxisome proliferator-activated receptors are nuclear receptors at the crossroads of key cellular functions. , 2006, Progress in lipid research.

[12]  Neil J. McKenna,et al.  Combinatorial Control of Gene Expression by Nuclear Receptors and Coregulators , 2002, Cell.

[13]  C. Lange Integration of progesterone receptor action with rapid signaling events in breast cancer models , 2008, The Journal of Steroid Biochemistry and Molecular Biology.

[14]  J. Rajasingh,et al.  1,25 Dihydroxyvitamin-D3 modulates JAK-STAT pathway in IL-12/IFNgamma axis leading to Th1 response in experimental allergic encephalomyelitis. , 2006, Journal of neuroscience research.

[15]  J. Peters,et al.  Role of PPAR alpha in the mechanism of action of the nongenotoxic carcinogen and peroxisome proliferator Wy-14,643. , 1997, Carcinogenesis.

[16]  Heather J. Lee,et al.  Regulation of growth hormone signaling by selective estrogen receptor modulators occurs through suppression of protein tyrosine phosphatases. , 2007, Endocrinology.

[17]  J. Parker,et al.  All-trans-retinoic acid effects the growth, differentiation and apoptosis of normal human myeloid progenitors derived from purified CD34+ bone marrow cells , 2000, Leukemia.

[18]  U. Panzer,et al.  15-deoxy-Delta12,14-prostaglandin J2 inhibits INF-gamma-induced JAK/STAT1 signalling pathway activation and IP-10/CXCL10 expression in mesangial cells. , 2008, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[19]  E. Gelmann,et al.  Molecular biology of the androgen receptor. , 2002, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[20]  M. Davidson Effect of growth hormone on carbohydrate and lipid metabolism. , 1987, Endocrine reviews.

[21]  D. Schubert,et al.  Synergistic Effect of Retinoic Acid and Cytokines on the Regulation of Glial Fibrillary Acidic Protein Expression , 2010, The Journal of Biological Chemistry.

[22]  T. Hoang,et al.  Impaired granulocytic differentiation in vitro in hematopoietic cells lacking retinoic acid receptors alpha1 and gamma. , 1998, Blood.

[23]  Carolyn L. Smith,et al.  Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. , 2001, Frontiers in bioscience : a journal and virtual library.

[24]  W. Kraus,et al.  A Global View of Transcriptional Regulation by Nuclear Receptors: Gene Expression, Factor Localization, and DNA Sequence Analysis , 2008, Nuclear receptor signaling.

[25]  M. Murray,et al.  Phospho‐STAT5 accumulation in nuclear fractions from vitamin A‐deficient rat liver , 2005, FEBS letters.

[26]  C. Geserick,et al.  The role of DNA response elements as allosteric modulators of steroid receptor function , 2005, Molecular and Cellular Endocrinology.

[27]  John A Cidlowski,et al.  Mechanisms of glucocorticoid receptor action in noninflammatory and inflammatory cells. , 2004, Proceedings of the American Thoracic Society.

[28]  M. Marrero,et al.  Regulation of angiotensin II-induced JAK2 tyrosine phosphorylation: roles of SHP-1 and SHP-2. , 1998, American journal of physiology. Cell physiology.

[29]  P. Leclerc,et al.  Mediators of the JAK/STAT Signaling Pathway in Human Spermatozoa1 , 2011, Biology of reproduction.

[30]  C. Lange,et al.  Hypothesis: Progesterone primes breast cancer cells for cross-talk with proliferative or antiproliferative signals. , 1999, Molecular endocrinology.

[31]  Ji-ping Wang,et al.  Estrogen utilization of IGF-1-R and EGF-R to signal in breast cancer cells , 2010, The Journal of Steroid Biochemistry and Molecular Biology.

[32]  Zhentao Zhang,et al.  1,25 dihydroxyvitamin D-mediated orchestration of anticancer, transcript-level effects in the immortalized, non-transformed prostate epithelial cell line, RWPE1 , 2010, BMC Genomics.

[33]  N. Binart,et al.  Transcriptional Control of Adrenal Steroidogenesis , 2011, The Journal of Biological Chemistry.

[34]  P. Kelly,et al.  The Prolactin/Growth Hormone Receptor Family: Structure/Function Relationships , 2004, Journal of Mammary Gland Biology and Neoplasia.

[35]  D. Waxman,et al.  Cross-talk between Janus Kinase-Signal Transducer and Activator of Transcription (JAK-STAT) and Peroxisome Proliferator-activated Receptor-α (PPARα) Signaling Pathways , 1999, The Journal of Biological Chemistry.

[36]  W. Farrar,et al.  Transcriptional crosstalk between nuclear receptors and cytokine signal transduction pathways in immunity. , 2004, Cellular & molecular immunology.

[37]  D. Waxman,et al.  Sex-dependent expression and clofibrate inducibility of cytochrome P450 4A fatty acid omega-hydroxylases. Male specificity of liver and kidney CYP4A2 mRNA and tissue-specific regulation by growth hormone and testosterone. , 1992, The Journal of biological chemistry.

[38]  R. Evans,et al.  The RXR heterodimers and orphan receptors , 1995, Cell.

[39]  G. Beatson On the Treatment of Inoperable Cases of Carcinoma of the Mamma: Suggestions for a New Method of Treatment, with Illustrative Cases , 1896, Transactions. Medico-Chirurgical Society of Edinburgh.

[40]  A. Verma,et al.  Jak family of kinases in cancer , 2003, Cancer and Metastasis Reviews.

[41]  D. Mayer,et al.  Janus kinase 2--a novel negative regulator of estrogen receptor α function. , 2012, Cellular signalling.

[42]  Tatsuo Kanda,et al.  Involvement of interleukin-6 and androgen receptor signaling in pancreatic cancer. , 2010, Genes & cancer.

[43]  K. Sjögren,et al.  Estrogen inhibits GH signaling by suppressing GH-induced JAK2 phosphorylation, an effect mediated by SOCS-2 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  S. Bulun,et al.  Aromatase P450 Gene Expression in Human Adipose Tissue. ROLE OF A Jak/STAT PATHWAY IN REGULATION OF THE ADIPOSE-SPECIFIC PROMOTER (*) , 1995, The Journal of Biological Chemistry.

[45]  Very-low-density lipoprotein mediates transcriptional regulation of aldosterone synthase in human adrenocortical cells through multiple signaling pathways , 2012, Cell and Tissue Research.

[46]  L. Barouch,et al.  Leptin signaling and obesity: cardiovascular consequences. , 2007, Circulation research.

[47]  D. Harrison,et al.  The JAK/STAT signaling pathway , 2004, Journal of Cell Science.

[48]  A. Akoum,et al.  Induction of human sperm capacitation and protein tyrosine phosphorylation by endometrial cells and interleukin-6. , 2005, Molecular human reproduction.

[49]  C. Croce,et al.  Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. , 2010, Cancer research.

[50]  J. Frasor,et al.  PRL-induced ERalpha gene expression is mediated by Janus kinase 2 (Jak2) while signal transducer and activator of transcription 5b (Stat5b) phosphorylation involves Jak2 and a second tyrosine kinase. , 2001, Molecular endocrinology.

[51]  S. Collins,et al.  IL-3-induced enhancement of retinoic acid receptor activity is mediated through Stat5, which physically associates with retinoic acid receptors in an IL-3-dependent manner. , 2002, Blood.

[52]  J. Rajasingh,et al.  1,25 dihydroxyvitamin‐D3 modulates JAK–STAT pathway in IL‐12/IFNγ axis leading to Th1 response in experimental allergic encephalomyelitis , 2006 .

[53]  Izumi V. Hinkson,et al.  Androgen-sensitive microsomal signaling networks coupled to the proliferation and differentiation of human prostate cancer cells. , 2011, Genes & cancer.

[54]  Marcel Garcia,et al.  Estrogens and their receptors in breast cancer progression: a dual role in cancer proliferation and invasion. , 2004, Critical reviews in oncology/hematology.

[55]  N. Krett,et al.  Mechanisms of glucocorticoid-mediated apoptosis in hematological malignancies. , 2002, Clinical cancer research : an official journal of the American Association for Cancer Research.

[56]  J. Frasor,et al.  Prolactin regulation of estrogen receptor expression , 2003, Trends in Endocrinology & Metabolism.

[57]  A. Yoshimura,et al.  Interaction and Functional Interference of Glucocorticoid Receptor and SOCS1* , 2008, Journal of Biological Chemistry.

[58]  K. Umesono,et al.  A Unified Nomenclature System for the Nuclear Receptor Superfamily , 1999, Cell.

[59]  A. Giordano,et al.  Leptin signaling in breast cancer: An overview , 2008, Journal of cellular biochemistry.

[60]  A. Sainsbury,et al.  Glucocorticoids as Counterregulatory Hormones of Leptin: Toward an Understanding of Leptin Resistance , 1997, Diabetes.

[61]  K. Umesono,et al.  The nuclear receptor superfamily: The second decade , 1995, Cell.

[62]  M. Maggiolini,et al.  The unfolding stories of GPR30, a new membrane-bound estrogen receptor. , 2010, The Journal of endocrinology.

[63]  C. Johnston Franz Volhard Lecture. Renin-angiotensin system: a dual tissue and hormonal system for cardiovascular control. , 1992, Journal of hypertension. Supplement : official journal of the International Society of Hypertension.

[64]  T. Hoang,et al.  Impaired Granulocytic Differentiation In Vitro in Hematopoietic Cells Lacking Retinoic Acid Receptors α1 and γ , 1998 .

[65]  T. Pineau,et al.  Targeted disruption of the alpha isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators , 1995, Molecular and cellular biology.

[66]  A. Moliterno,et al.  Janus kinase inhibitors: an update on the progress and promise of targeted therapy in the myeloproliferative neoplasms , 2011, Current opinion in oncology.

[67]  T. Sugiyama,et al.  Aldosterone induces angiotensin converting enzyme gene expression via a JAK2-dependent pathway in rat endothelial cells. , 2005, Endocrinology.

[68]  L. Haldosen,et al.  1α,25-Dihydroxyvitamin D3 Inhibits GH-induced Expression of SOCS-3 and CIS and Prolongs Growth Hormone Signaling via the Janus Kinase (JAK2)/Signal Transducers and Activators of Transcription (STAT5) System in Osteoblast-like Cells* , 2002, The Journal of Biological Chemistry.

[69]  M. Rieder,et al.  Regulation of cytokine and cytokine receptor expression by glucocorticoids , 1996, Journal of leukocyte biology.

[70]  R. Ray,et al.  Hepatitis C Virus Core Protein Augments Androgen Receptor-Mediated Signaling , 2008, Journal of Virology.

[71]  W. Leonard,et al.  Jaks and STATs: biological implications. , 1998, Annual review of immunology.

[72]  K. Eguchi,et al.  Rapid Inhibition of Leptin Signaling by Glucocorticoids in Vitro and in Vivo* , 2004, Journal of Biological Chemistry.

[73]  K. Dawson,et al.  Janus Kinase 2 and Calcium Are Required for Angiotensin II-dependent Activation of Steroidogenic Acute Regulatory Protein Transcription in H295R Human Adrenocortical Cells* , 2003, Journal of Biological Chemistry.

[74]  N. Bruchovsky,et al.  Activation of the Androgen Receptor N-terminal Domain by Interleukin-6 via MAPK and STAT3 Signal Transduction Pathways* , 2002, The Journal of Biological Chemistry.

[75]  J. Kovarik,et al.  JAK/STAT signaling pathways and cancer. Janus kinases/signal transducers and activators of transcription. , 2002, Neoplasma.

[76]  Thorsten Heinzel,et al.  Nuclear receptors: overview and classification. , 2004, Current drug targets. Inflammation and allergy.

[77]  N. Binart,et al.  Reproductive role of prolactin. , 2007, Reproduction.

[78]  H. Rui,et al.  Jak2/Stat5 Signaling in Mammogenesis, Breast Cancer Initiation and Progression , 2008, Journal of Mammary Gland Biology and Neoplasia.

[79]  Richard A Gibbs,et al.  Genomic analysis of the nuclear receptor family: new insights into structure, regulation, and evolution from the rat genome. , 2004, Genome research.

[80]  G. Prins,et al.  Molecular biology of the androgen receptor. , 2000, Mayo Clinic proceedings.

[81]  W. Almawi,et al.  Molecular mechanisms of glucocorticoid antiproliferative effects: antagonism of transcription factor activity by glucocorticoid receptor , 2002, Journal of leukocyte biology.

[82]  R. Geney,et al.  Advances in the discovery of selective JAK inhibitors. , 2013, Progress in medicinal chemistry.

[83]  S. Catalano,et al.  The multifactorial role of leptin in driving the breast cancer microenvironment , 2012, Nature Reviews Endocrinology.

[84]  R. Levine,et al.  JAK2 the future: therapeutic strategies for JAK-dependent malignancies. , 2012, Trends in pharmacological sciences.

[85]  J. Fleet Molecular actions of vitamin D contributing to cancer prevention. , 2008, Molecular aspects of medicine.

[86]  D. Modi,et al.  Progesterone activates Janus Kinase 1/2 and activators of transcription 1 (JAK1‐2/STAT1) pathway in human spermatozoa , 2013, Andrologia.

[87]  E. Surmacz,et al.  Leptin and cancer , 2006, Journal of cellular physiology.

[88]  W. Wahli,et al.  Peroxisome proliferator activated receptors: transcriptional regulators of adipogenesis, lipid metabolism and more.... , 1995, Chemistry & biology.

[89]  M. Hou,et al.  Altered p-JAK1 expression is associated with estrogen receptor status in breast infiltrating ductal carcinoma. , 2007, Oncology reports.

[90]  S. Rane,et al.  Janus kinases: components of multiple signaling pathways , 2000, Oncogene.

[91]  D. Waxman,et al.  Cross-talk between janus kinase-signal transducer and activator of transcription (JAK-STAT) and peroxisome proliferator-activated receptor-alpha (PPARalpha) signaling pathways. Growth hormone inhibition of pparalpha transcriptional activity mediated by stat5b. , 1999, The Journal of biological chemistry.

[92]  S. Cl,et al.  Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. , 2001 .

[93]  H. Tamura,et al.  Hormonal modulation of peroxisomal enzyme induction caused by peroxisome proliferators: suppression by growth and thyroid hormones in cultured rat hepatocytes. , 1994, Archives of Biochemistry and Biophysics.