P42/p44 MAPK-mediated Stat3Ser727 phosphorylation is required for progestin-induced full activation of Stat3 and breast cancer growth

Endocrine-Related Cancer

Volumn 20, Issue 2, 2013, Pages 197-212

  Tkach, Mercedes ^a   Rosemblit, Cinthia ^a   Rivas, Martín A ^b   Proietti, Cecilia J ^a   Flaqué, María Celeste Díaz ^a   Mercogliano, María Florencia ^a   Beguelin, Wendy ^a   Maronna, Esteban ^c   Guzmán, Pablo ^d   Gercovich, Felipe G ^e   Deza, Ernesto Gil ^e   Elizalde, Patricia V ^a   Schillaci, Roxana ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b Sanatorio Mater Dei   (Argentina)

^c UNIVERSIDAD DE LA FRONTERA   (Chile)

^d Instituto Henry Moore PROSAM   (Argentina)

^e VALL D HEBRON UNIVERSITY HOSPITAL   (Spain)

Author keywords

Breast cancer; P42 p44 MAPK; Progestin; Stat3

Indexed keywords

ALANINE; GESTAGEN; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN P42; SERINE; STAT3 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST BIOPSY; BREAST CANCER; CANCER GROWTH; CONTROLLED STUDY; CYCLIN D1 GENE; ENZYME ACTIVATION; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN PHOSPHORYLATION;

ANIMALS; BREAST NEOPLASMS; CELL PROLIFERATION; CYCLIN D1; FEMALE; HUMANS; MEDROXYPROGESTERONE ACETATE; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; STAT3 TRANSCRIPTION FACTOR;

EID: 84876756279     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-12-0194     Document Type: Article

References (53)

1. Aziz MH, Hafeez BB, Sand JM, Pierce DB, Aziz SW, Dreckschmidt NE & Verma AK 2010 Protein kinase Cvarepsilon mediates Stat3Ser727 phosphorylation, Stat3-regulated gene expression, and cell invasion in various human cancer cell lines through integration with MAPK cascade (RAF-1, MEK1/2, and ERK1/2). Oncogene 29 3100-3109. (doi:10.1038/onc.2010.63)
2. Balana ME, Lupu R, Labriola L, Charreau EH & Elizalde PV 1999 Interactions between progestins and heregulin (HRG) signaling pathways: HRG acts as mediator of progestins proliferative effects in mouse mammary adenocarcinomas. Oncogene 18 6370-6379. (doi:10.1038/sj.onc.1203028)
3. Ballare C, Uhrig M, Bechtold T, Sancho E, Di Domenico M, Migliaccio A, Auricchio F & Beato M 2003 Two domains of the progesterone receptor interact with the estrogen receptor and are required for progesterone activation of the c-Src/Erk pathway in mammalian cells. Molecular and Cellular Biology 23 1994-2008. (doi:10.1128/MCB.23.6.1994-2008.
4. Beguelin W, Diaz Flaque MC, Proietti CJ, Cayrol F, Rivas MA, Tkach M, Rosemblit C, Tocci JM, Charreau EH, Schillaci R et al. 2010 Progesterone receptor induces ErbB-2 nuclear translocation to promote breast cancer growth via a novel transcriptional effect: ErbB-2 function as a coactivator of Stat3. Molecular and Cellular Biology 30 5456-5472. (doi:10.1128/MCB.00012-10)
5. Beral V 2003 Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 362 419-427. (doi:10.1016/S0140-6736(03)14596-5)
6. Boonyaratanakornkit V, Scott MP, Ribon V, Sherman L, Anderson SM, Maller JL, Miller WT & Edwards DP 2001 Progesterone receptor contains a proline-rich motif that directly interacts with SH3 domains and activates c-Src family tyrosine kinases. Molecular Cell 8 269-280. (doi:10.1016/S1097-2765(01) 00304-5)
7. Boonyaratanakornkit V, McGowan E, Sherman L, Mancini MA, Cheskis BJ & Edwards DP 2007 The role of extranuclear signaling actions of progesterone receptor in mediating progesterone regulation of gene expression and the cell cycle. Molecular Endocrinology 21 359-375. (doi:10.1210/me.2006-0337)
8. Bowman T, Garcia R, Turkson J & Jove R 2000 STATs in oncogenesis. Oncogene 19 2474-2488. (doi:10.1038/sj.onc.1203527)
9. Bromberg JF, Horvath CM, Besser D, Lathem WW & Darnell JE, Jr. 1998 Stat3 activation is required for cellular transformation by v-src. Molecular and Cellular Biology 18 2553-2558.
10. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, Albanese C & Darnell JE, Jr. 1999 Stat3 as an oncogene. Cell 98 295-303. (doi:10.1016/S0092-8674(00)81959-5)
11. Carnevale RP, Proietti CJ, Salatino M, Urtreger A, Peluffo G, Edwards DP, Boonyaratanakornkit V, Charreau EH, Bal de Kier JE, Schillaci R et al. 2007 Progestin effects on breast cancer cell proliferation, proteases activation, and in vivo development of metastatic phenotype all depend on progesterone receptor capacity to activate cytoplasmic signaling pathways. Molecular Endocrinology 21 1335-1358. (doi:10.1210/me.2006-0304)
12. Darnell JE, Jr., Kerr IM & Stark GR 1994 Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264 1415-1421. (doi:10.1126/science. 8197455)
13. Decker T & Kovarik P 2000 Serine phosphorylation of STATs. Oncogene 19 2628-2637. (doi:10.1038/sj.onc.1203481)
14. De Miguel F, Lee SO, Onate SA & Gao AC 2003 Stat3 enhances transactivation of steroid hormone receptors. Nuclear Receptor 1 3. (doi:10.1186/1478-1336-1-3)
15. Dolled-FilhartM, Camp RL, Kowalski DP, Smith BL & Rimm DL 2003 Tissue microarray analysis of signal transducersandactivators of transcription3 (Stat3) and phospho-Stat3 (Tyr705) in node-negative breast cancer shows nuclear localization is associated with a better prognosis. Clinical Cancer Research 9 594-600.
16. Gonzalez FA, Raden DL & Davis RJ 1991 Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases. Journal of Biological Chemistry 66 22159-22163.
17. Gritsko T, Williams A, Turkson J, Kaneko S, Bowman T, Huang M, Nam S, Eweis I, Diaz N, Sullivan D et al. 2006 Persistent activation of Stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clinical Cancer Research 12 11-19. (doi:10.1158/1078-0432. CCR-04-1752)
18. In Guide for the Care and Use of Laboratory Animals 1996. Institute of Laboratory Animal Resources, Commission on Life Sciences National Research Council. Washington, DC: National Academy Press.
19. Hazan-Halevy I, Harris D, Liu Z, Liu J, Li P, Chen X, Shanker S, Ferrajoli A, Keating MJ & Estrov Z 2010 STAT3 is constitutively phosphorylated on serine 727 residues, binds DNA, and activates transcription in CLL cells. Blood 115 2852-2863. (doi:10.1182/blood-2009-10-230060)
20. Heinrich PC, Behrmann I, Muller-Newen G, Schaper F & Graeve L 1998 Interleukin-6-type cytokine signalling through the gp130/Jak/STAT pathway. Biochemical Journal 334 (Pt 2) 297-314.
21. Lee H, Herrmann A, Deng JH, Kujawski M, Niu G, Li Z, Forman S, Jove R, Pardoll DM & Yu H 2009 Persistently activated Stat3 maintains constitutive NF-kB activity in tumors. Cancer Cell 15 283-293. (doi:10.1016/j.ccr.2009.02. 015)
22. Leslie K, Lang C, Devgan G, Azare J, Berishaj M, Gerald W, Kim YB, Paz K, Darnell JE, Albanese C et al. 2006 Cyclin D1 is transcriptionally regulated by and required for transformation by activated signal transducer and activator of transcription 3. Cancer Research 66 2544-2552. (doi:10.1158/0008-5472.CAN-05- 2203)
23. Lanari C, Lamb CA, Fabris VT, Helguero LA, Soldati R, Bottino MC, Giulianelli S, Cerliani JP, Wargon V & Molinolo A 2009 The MPA mouse breast cancer model: evidence for a role of progesterone receptors in breast cancer. Endocrine-Related Cancer 16 333-350. (doi:10.1677/ERC-08-0244)
24. Migliaccio A, Piccolo D, Castoria G, Di Domenico M, Bilancio A, Lombardi M, Gong W, Beato M & Auricchio F 1998 Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO Journal 17 2008-2018. (doi:10.1093/emboj/17.7.2008)
25. Olayioye MA, Beuvink I, Horsch K, Daly JM & Hynes NE 1999 ErbB receptor-induced activation of Stat transcription factors is mediated by Src tyrosine kinases. Journal of Biological Chemistry 274 17209-17218. (doi:10.1074/jbc.274.24.17209)
26. O'Neil BH, Goff LW, Kauh JS, Strosberg JR, Bekaii-Saab TS, Lee RM, Kazi A, Moore DT, Learoyd M, Lush RM et al. 2011 Phase II study of the mitogen-Activated protein kinase 1/2 inhibitor selumetinib in patients with advanced hepatocellular carcinoma. Journal of Clinical Oncology 29 2350-2356. (doi:10.1200/JCO.2010.33.9432)
27. Page DL, Ellis IO & Elston CW 1995 Histologic grading of breast cancer. Let's do it. American Journal of Clinical Pathology 103 123-124.
28. Patel SP & Kim KB 2012 Selumetinib (AZD6244; ARRY-142886) in the treatment of metastatic melanoma. Expert Opinion on Investigational Drugs 21 531-539. (doi:10.1517/13543784.2012.665871)
29. Pietra LD, Bressan A, Pezzotti AR & Serlupi-Crescenzi O 1998 Highly conserved amino-Acid sequence between murine STAT3 and a revised human STAT3 sequence. Gene 213 119-124. (doi:10.1016/S0378-1119(98)00185-1)
30. Proietti C, Salatino M, Rosemblit C, Carnevale R, Pecci A, Kornblihtt AR, Molinolo AA, Frahm I, Charreau EH, Schillaci R et al. 2005 Progestins induce transcriptional activation of signal transducer and activator of transcription 3 (Stat3) via a Jak-And Src-dependent mechanism in breast cancer cells. Molecular and Cellular Biology 25 4826-4840. (doi:10.1128/MCB.25.12.4826-4840.2005)
31. Proietti CJ,RosemblitC,BeguelinW,RivasMA,DiazFlaqueMC,CharreauEH, Schillaci R & Elizalde PV 2009 Activation of Stat3 by heregulin/ErbB-2 through the co-option of progesterone receptor signaling drives breast cancer growth.Molecular and Cellular Biology291249-1265. (doi:10.1128/MCB.00853-08)
32. Real PJ, Sierra A, De Juan A, Segovia JC, Lopez-Vega JM&Fernandez- Luna JL 2002 Resistance to chemotherapy via Stat3-dependent overexpression of Bcl-2 in metastatic breast cancer cells. Oncogene 21 7611-7618. (doi:10.1038/sj.onc.1206004)
33. Richer JK, Lange CA, Manning NG, Owen G, Powell R & Horwitz KB 1998 Convergence of progesterone with growth factor and cytokine signaling in breast cancer. Progesterone receptors regulate signal transducers and activators of transcription expression and activity. Journal of Biological Chemistry 273 31317-31326. (doi:10.1074/jbc.273.31317)
34. Rivas MA, Carnevale RP, Proietti CJ, Rosemblit C, Beguelin W, Salatino M, Charreau EH, Frahm I, Sapia S, Brouckaert P et al. 2008 TNFa acting on TNFR1 promotes breast cancer growth via p42/P44 MAPK, JNK, Akt and NF-kB-dependent pathways. Experimental Cell Research 314 509-529. (doi:10.1016/j.yexcr.2007.10. 005)
35. Rivas MA, Tkach M, Beguelin W, Proietti CJ, Rosemblit C, Charreau EH, Elizalde PV & Schillaci R 2010 Transactivation of ErbB-2 induced by tumor necrosis factor a promotes NF-kB activation and breast cancer cell proliferation. Breast Cancer Research and Treatment 122 111-124. (doi:10.1007/s10549-009-0546-3)
36. Sartorius CA, Groshong SD, Miller LA, Powell RL, Tung L, Takimoto GS & Horwitz KB 1994 New T47D breast cancer cell lines for the independent study of progesterone B-And A-receptors: only antiprogestin-occupied B-receptors are switched to transcriptional agonists by cAMP. Cancer Research 54 3868-3877.
37. Sasse J, Hemmann U, Schwartz C, Schniertshauer U, Heesel B, Landgraf C, Schneider-Mergener J, Heinrich PC & Horn F 1997 Mutational analysis of acute-phase response factor/Stat3 activation and dimerization. Molecular and Cellular Biology 17 4677-4686.
38. Sato T, Neilson LM, Peck AR, Liu C, Tran TH, Witkiewicz A, Hyslop T, Nevalainen MT, Sauter G & Rui H 2011 Signal transducer and activator of transcription-3 and breast cancer prognosis. American Journal of Cancer Research 1 347-355.
39. SchillaciR,SalatinoM,CassataroJ,ProiettiCJ,GiambartolomeiGH,RivasMA, Carnevale RP, Charreau EH & Elizalde PV 2006 Immunization with murine breast cancer cells treated with antisense oligodeoxynucleotides to type I insulin-like growth factor receptor induced an antitumoral effect mediated by a CD8Cresponse involving Fas/Fas ligand cytotoxic pathway. Journal of Immunology 176 3426-3437.
40. Schillaci R, Guzman P, Cayrol F, Beguelin W, Diaz Flaque MC, Proietti CJ, Pineda V, Palazzi J, Frahm I, Charreau EH et al. 2012 Clinical relevance of ErbB-2/HER2 nuclear expression in breast cancer. BMC Cancer 12 74. (doi:10.1186/1471-2407-12-74)
41. Shen T, Horwitz KB & Lange CA 2001 Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-Activated protein kinase-dependent phosphorylation of serine 294. Molecular and Cellular Biology 21 6122-6131. (doi:10.1128/MCB.21. 18.6122-6131.2001)
42. Shen Y, Schlessinger K, Zhu X, Meffre E, Quimby F, Levy DE & Darnell JE, Jr. 2004 Essential role of STAT3 in postnatal survival and growth revealed by mice lacking STAT3 serine 727 phosphorylation. Molecular and Cellular Biology 24 407-419. (doi:10.1128/MCB.24.1.407-419.2004)
43. Silvennoinen O, Schindler C, Schlessinger J & Levy DE 1993 Rasindependent growth factor signaling by transcription factor tyrosine phosphorylation. Science 261 1736-1739. (doi:10.1126/science. 8378775)
44. Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, Borgen PI, Clark G, Edge SB, Hayes DF et al. 2002 Revision of the American Joint Committee on Cancer staging system for breast cancer. Journal of Clinical Oncology 20 3628-3636. (doi:10.1200/JCO.2002.02.026)
45. Skildum A, Faivre E & Lange CA 2005 Progesterone receptors induce cell cycle progression via activation of mitogen-Activated protein kinases. Molecular Endocrinology 19 327-339. (doi:10.1210/me.2004-0306)
46. Sud N, Kumar S, Wedgwood S & Black SM 2009 Modulation of PKCd signaling alters the shear stress-mediated increases in endothelial nitric oxide synthase transcription: role of STAT3. American Journal of Physiology. Lung Cellular and Molecular Physiology 296 L519-L526. (doi:10.1152/ajplung.90534. 2008)
47. Tsai MJ & O'Malley BW 1994 Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annual Review of Biochemistry 63 451-486. (doi:10.1146/annurev.bi.63.070194.002315)
48. Turner NA, Das A, Warburton P, O'Regan DJ, Ball SG & Porter KE 2009 Interleukin-1a stimulates proinflammatory cytokine expression in human cardiac myofibroblasts. American Journal of Physiology. Heart and Circulatory Physiology 297 H1117-H1127. (doi:10.1152/ajpheart. 00372.2009)
49. Wen Z, Zhong Z & Darnell JE, Jr. 1995 Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82 241-250. (doi:10.1016/0092-8674(95)90311-9)
50. Yu H & Jove R 2004 The STATs of cancer -new molecular targets come of age. Nature Reviews. Cancer 4 97-105. (doi:10.1038/nrc1275)
51. Yu Q, Geng Y & Sicinski P 2001 Specific protection against breast cancers by cyclin D1 ablation. Nature 411 1017-1021. (doi:10.1038/35082500)
52. Zhang Q,Nowak I,Vonderheid EC, Rook AH, KadinME,Nowell PC, ShawLM &Wasik MA 1996 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. PNAS 93 9148-9153. (doi:10.1073/pnas.93.17.9148)
53. Zhang Y, Turkson J, Carter-Su C, Smithgall T, Levitzki A, Kraker A, Krolewski JJ, Medveczky P & Jove R 2000 Activation of Stat3 in v-Srctransformed fibroblasts requires cooperation of Jak1 kinase activity. Journal of Biological Chemistry 275 24935-24944. (doi:10.1074/jbc.M002383200)