Mouse mammary tumors display Stat3 activation dependent on leukemia inhibitory factor signaling

Breast Cancer Research

Volumn 9, Issue 5, 2007, Pages

  Quaglino, Ana ^a,b   Schere Levy, Carolina ^a,b   Romorini, Leonardo ^a   Meiss, Roberto Patologia ^b   Kordon, Edith C ^a,b  

^a INSTITUTO DE FISIOLOGÍA   (Argentina)

^b INST DE INVEST HEMATOLOGICAS   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CRYSTAL VIOLET; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN ANTIBODY; STAT3 PROTEIN; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA; LIF PROTEIN, MOUSE; LIFR PROTEIN, MOUSE; MESSENGER RNA; STAT3 PROTEIN, MOUSE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST TUMOR; CELL SURVIVAL; FEMALE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHOSPHORYLATION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; EXPERIMENTAL NEOPLASM; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BLOTTING, WESTERN; CELL SURVIVAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA SUBUNIT; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED; TYROSINE;

EID: 36549016576     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr1777     Document Type: Article

References (52)

1. Gearing DP Gough NM King JA Hilton DJ Nicola NA Simpson RJ Nice EC Kelso A Metcalf D Molecular cloning and expression of cDNA encoding a murine myeloid leukaemia inhibitory factor (LIF) EMBO J 1987, 6:3995-4002. 553879 3127201
2. Taga T Kishimoto T Gp130 and the interleukin-6 family of cytokines Annu Rev Immunol 1997, 15:797-819. 10.1146/annurev.immunol.15.1.797 9143707
3. Dhingra K Sahin A Emami K Hortobagyi GN Estrov Z Expression of leukemia inhibitory factor and its receptor in breast cancer: A potential autocrine and paracrine growth regulatory mechanism Breast Cancer Res Treat 1998, 48:165-174. 10.1023/A:1005942923757 9596488
4. Kellokumpu-Lehtinen P Talpaz M Harris D Van Q Kurzrock R Estrov Z Leukemia-inhibitory factor stimulates breast, kidney and prostate cancer cell proliferation by paracrine and autocrine pathways Int J Cancer 1996, 66:515-519. 10.1002/ (SICI)1097-0215(19960516)66:4<515::AID-IJC15>3.0.CO;2-6 8635867
5. Bamberger AM Thuneke I Schulte HM Differential regulation of the human 'leukemia inhibitory factor' (LIF) promoter in T47D and MDA-MB 231 breast cancer cells Breast Cancer Res Treat 1998, 47:153-161. 10.1023/ A:1005961403898 9497103
6. Estrov Z Samal B Lapushin R Kellokumpu-Lehtinen P Sahin AA Kurzrock R Talpaz M Aggarwal BB Leukemia inhibitory factor binds to human breast cancer cells and stimulates their proliferation J Interferon Cytokine Res 1995, 15:905-913. 8564713
7. Gearing DP Thut CJ VandeBos T Gimpel SD Delaney PB King J Price V Cosman D Beckmann MP Leukemia inhibitory factor receptor is structurally related to the IL-6 signal transducer, gp130 EMBO J 1991, 10:2839-2848. 452994 1915266
8. Gearing DP Comeau MR Friend DJ Gimpel SD Thut CJ McGourty J Brasher KK King JA Gillis S Mosley B The IL-6 signal transducer, gp130: An oncostatin M receptor and affinity converter for the LIF receptor Science 1992, 255:1434-1437. 10.1126/science.1542794 1542794
9. Darnell JE Jr STATs and gene regulation Science 1997 277 1630 1635 10.1126/science.277.5332.1630 9287210
10. Raz R Durbin JE Levy DE Acute phase response factor and additional members of the interferon-stimulated gene factor 3 family integrate diverse signals from cytokines, interferons, and growth factors J Biol Chem 1994, 269:24391-24395. 7523373
11. Lutticken C Wegenka UM Yuan J Buschmann J Schindler C Ziemiecki A Harpur AG Wilks AF Yasukawa K Taga T Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130 Science 1994, 263:89-92. 10.1126/science.8272872 8272872
12. Li M Liu X Robinson G Bar-Peled U Wagner KU Young WS Hennighausen L Furth PA Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution Proc Natl Acad Sci USA 1997, 94:3425-3430. 20386 9096410 10.1073/pnas.94.7.3425
13. Chapman RS Lourenco PC Tonner E Flint DJ Selbert S Takeda K Akira S Clarke AR Watson CJ Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3 Genes Dev 1999 13 2604 2616 317074 10521404 10.1101/gad.13.19.2604
14. Li L Shaw PE Autocrine-mediated activation of STAT3 correlates with cell proliferation in breast carcinoma lines J Biol Chem 2002, 277:17397-17405. 10.1074/jbc.M109962200 11859072
15. Garcia R Bowman TL Niu G Yu H Minton S Muro-Cacho CA Cox CE Falcone R Fairclough R Parsons S Constitutive activation of Stat3 by the Src and JAK tyrosine kinases participates in growth regulation of human breast carcinoma cells Oncogene 2001, 20:2499-2513. 10.1038/sj.onc.1204349 11420660
16. Burke WM Jin X Lin HJ Huang M Liu R Reynolds RK Lin J Inhibition of constitutively active Stat3 suppresses growth of human ovarian and breast cancer cells Oncogene 2001, 20:7925-7934. 10.1038/sj.onc.1204990 11753675
17. Schere-Levy C Buggiano V Quaglino A Gattelli A Cirio MC Piazzon I Vanzulli S Kordon EC Leukemia inhibitory factor induces apoptosis of the mammary epithelial cells and participates in mouse mammary gland involution Exp Cell Res 2003, 282:35-47. 10.1006/excr.2002.5666 12490192
18. Kritikou EA Sharkey A Abell K Came PJ Anderson E Clarkson RW Watson CJ A dual, non-redundant, role for LIF as a regulator of development and STAT3-mediated cell death in mammary gland Development 2003, 130:3459-3468. 10.1242/dev.00578 12810593
19. Minami M Inoue M Wei S Takeda K Matsumoto M Kishimoto T Akira S STAT3 activation is a critical step in gp130-mediated terminal differentiation and growth arrest of a myeloid cell line Proc Natl Acad Sci USA 1996, 93:3963-3966. 39468 8632998 10.1073/pnas.93.9.3963
20. Kodama H Fukuda K Pan J Makino S Baba A Hori S Ogawa S Leukemia inhibitory factor, a potent cardiac hypertrophic cytokine, activates the JAK/STAT pathway in rat cardiomyocytes Circ Res 1997, 81:656-663. 9351438
21. Boeuf H Hauss C Graeve FD Baran N Kedinger C Leukemia inhibitory factor-dependent transcriptional activation in embryonic stem cells J Cell Biol 1997, 138:1207-1217. 10.1083/jcb.138.6.1207 9298977
22. Jenab S Morris PL Testicular leukemia inhibitory factor (LIF) and LIF receptor mediate phosphorylation of signal transducers and activators of transcription (STAT)-3 and STAT-1 and induce c-fos transcription and activator protein-1 activation in rat Sertoli but not germ cells Endocrinology 1998, 139:1883-1890. 10.1210/en.139.4.1883 9528974
23. Cheng JG Chen JR Hernandez L Alvord WG Stewart CL Dual control of LIF expression and LIF receptor function regulate Stat3 activation at the onset of uterine receptivity and embryo implantation Proc Natl Acad Sci USA 2001, 98:8680-8685. 37495 11438698 10.1073/pnas.151180898
24. Buggiano V Levy CS Gattelli A Cirio MC Marfil M Nepomnaschy I Piazzon I Helguero L Vanzulli S Kordon EC Origin and progression of pregnancy-dependent mammary tumors induced by new mouse mammary tumor virus variants Breast Cancer Res Treat 2002, 75:191-202. 10.1023/ A:1019932516887 12353808
25. Gattelli A Cirio MC Quaglino A Schere-Levy C Martinez N Binaghi M Meiss RP Castilla LH Kordon EC Progression of pregnancy-dependent mouse mammary tumors after long dormancy periods. Involvement of Wnt pathway activation Cancer Res 2004, 64:5193-5199. 10.1158/0008-5472.CAN-03-3992 15289324
26. Puricelli L Colombo LL Bal de Kier Joffe E de Lustig ES Invasiveness in vitro of two mammary adenocarcinoma tumors with different metastasizing ability Invasion Metastasis 1984, 4:238-246. 6533095
27. Park JI Strock CJ Ball DW Nelkin BD The Ras/Raf/MEK/extracellular signal-regulated kinase pathway induces autocrine-paracrine growth inhibition via the leukemia inhibitory factor/JAK/STAT pathway Mol Cell Biol 2003, 23:543-554. 151536 12509453 10.1128/MCB.23.2.543-554.2003
28. Golubovskaya VM Gross S Kaur AS Wilson RI Xu LH Yang XH Cance WG Simultaneous inhibition of focal adhesion kinase and SRC enhances detachment and apoptosis in colon cancer cell lines Mol Cancer Res 2003, 1:755-764. 12939401
29. Bradford MM A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3 942051
30. Lopez-Marure R Gutierrez G Mendoza C Ventura JL Sanchez L Reyes Maldonado E Zentella A Montano LF Ceramide promotes the death of human cervical tumor cells in the absence of biochemical and morphological markers of apoptosis Biochem Biophys Res Commun 2002, 293:1028-1036. 10.1016/S0006-291X(02)00315-7 12051763
31. Gattelli A Zimberlin MN Meiss RP Castilla LH Kordon EC Selection of early-occurring mutations dictates hormone-independent progression in mouse mammary tumor lines J Virol 2006, 80:11409-11415. 1642155 16971449 10.1128/JVI.00234-06
32. Haines BP Voyle RB Pelton TA Forrest R Rathjen PD Complex conserved organization of the mammalian leukemia inhibitory factor gene: Regulated expression of intracellular and extracellular cytokines J Immunol 1999, 162:4637-4646. 10202003
33. Hutt JA O'Rourke JP DeWille J Signal transducer and activator of transcription 3 activates CCAAT enhancer-binding protein delta gene transcription in G0 growth-arrested mouse mammary epithelial cells and in involuting mouse mammary gland J Biol Chem 2000, 275:29123-29131. 10.1074/jbc.M004476200 10867011
34. Zhao L Hart S Cheng J Melenhorst JJ Bierie B Ernst M Stewart C Schaper F Heinrich PC Ullrich A Mammary gland remodeling depends on gp130 signaling through Stat3 and MAPK J Biol Chem 2004, 279:44093-44100. 10.1074/jbc.M313131200 15292206
35. Catalano RD Johnson MH Campbell EA Charnock-Jones DS Smith SK Sharkey AM Inhibition of Stat3 activation in the endometrium prevents implantation: a nonsteroidal approach to contraception Proc Natl Acad Sci USA 2005, 102:8585-8590. 1150834 15937114 10.1073/pnas.0502343102
36. Bharti AC Donato N Aggarwal BB Curcumin (diferuloylmethane) inhibits constitutive and IL-6-inducible STAT3 phosphorylation in human multiple myeloma cells J Immunol 2003, 171:3863-3871. 14500688
37. Yu H Jove R The STATs of cancer - new molecular targets come of age Nat Rev Cancer 2004, 4:97-105. 14964307
38. Buettner R Mora LB Jove R Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention Clin Cancer Res 2002, 8:945-954. 11948098
39. Badache A Hynes NE Interleukin 6 inhibits proliferation and, in cooperation with an epidermal growth factor receptor autocrine loop, increases migration of T47D breast cancer cells Cancer Res 2001, 61:383-391. 11196191
40. Mora LB Buettner R Seigne J Diaz J Ahmad N Garcia R Bowman T Falcone R Fairclough R Cantor A Constitutive activation of Stat3 in human prostate tumors and cell lines: Direct inhibition of Stat3 signaling induces apoptosis of prostate cancer cells Cancer Res 2002, 62:6659-6666. 12438264
41. Catlett-Falcone R Landowski TH Oshiro MM Turkson J Levitzki A Savino R Ciliberto G Moscinski L Fernandez-Luna JL Nunez G Constitutive activation of Stat3 signaling confers resistance to apoptosis in human U266 myeloma cells Immunity 1999, 10:105-115. 10.1016/ S1074-7613(00)80011-4 10023775
42. Berishaj M Gao SP Ahmed S Leslie K Al-Ahmadie H Gerald WL Bornmann W Bromberg JF Stat3 is tyrosine-phosphorylated through the interleukin-6/ glycoprotein 130/Janus kinase pathway in breast cancer Breast Cancer Res 2007, 9:R32. 1929096 17531096 10.1186/bcr1680
43. Zhao L Melenhorst JJ Hennighausen L Loss of interleukin 6 results in delayed mammary gland involution: A possible role for mitogen-activated protein kinase and not signal transducer and activator of transcription 3 Mol Endocrinol 2002, 16:2902-2912. 10.1210/me.2001-0330 12456808
44. Ling X Arlinghaus RB Knockdown of STAT3 expression by RNA interference inhibits the induction of breast tumors in immunocompetent mice Cancer Res 2005, 65:2532-2536. 10.1158/0008-5472.CAN-04-2425 15805244
45. Selander KS Li L Watson L Merrell M Dahmen H Heinrich PC Muller-Newen G Harris KW Inhibition of gp130 signaling in breast cancer blocks constitutive activation of Stat3 and inhibits in vivo malignancy Cancer Res 2004, 64:6924-6933. 10.1158/0008-5472.CAN-03-2516 15466183
46. Dolled-Filhart M Camp RL Kowalski DP Smith BL Rimm DL Tissue microarray analysis of signal transducers and activators of transcription 3 (Stat3) and phospho-Stat3 (Tyr705) in node-negative breast cancer shows nuclear localization is associated with a better prognosis Clin Cancer Res 2003, 9:594-600. 12576423
47. Puricelli L Proiettii CJ Labriola L Salatino M Balana ME Aguirre Ghiso J Lupu R Pignataro OP Charreau EH Bal de Kier Joffe E Heregulin inhibits proliferation via ERKs and phosphatidyl-inositol 3-kinase activation but regulates urokinase plasminogen activator independently of these pathways in metastatic mammary tumor cells Int J Cancer 2002, 100:642-653. 10.1002/ijc.10533 12209601
48. Bromberg J Stat proteins and oncogenesis J Clin Invest 2002, 109:1139-1142. 150969 11994401 10.1172/JCI200215617
49. Lu C Kerbel RS Interleukin-6 undergoes transition from paracrine growth inhibitor to autocrine stimulator during human melanoma progression J Cell Biol 1993, 120:1281-1288. 10.1083/jcb.120.5.1281 8436594
50. Ball RK Friis RR Schoenenberger CA Doppler W Groner B Prolactin regulation of beta-casein gene expression and of a cytosolic 120-kd protein in a cloned mouse mammary epithelial cell line EMBO J 1988, 7:2089-2095. 454494 3416834
51. Danielson KG Oborn CJ Durban EM Butel JS Medina D Epithelial mouse mammary cell line exhibiting normal morphogenesis in vivo and functional differentiation in vitro Proc Natl Acad Sci USA 1984, 81:3756-3760. 345298 6587390 10.1073/pnas.81.12.3756
52. Desprez PY Hara E Bissell MJ Campisi J Suppression of mammary epithelial cell differentiation by the helix-loop-helix protein Id-1 Mol Cell Biol 1995, 15:3398-3404. 230574 7760836