Signal transducer and activator of transcription (STAT)-5A and STAT5B differentially regulate human mammary carcinoma cell behavior

Endocrinology

Volumn 151, Issue 1, 2010, Pages 43-55

  Tang, Jian Zhong ^a   Zuo, Ze Hua ^c   Kong, Xiang Jun ^c   Steiner, Michael ^a   Yin, Zhinan ^d   Perry, Jo K ^a   Zhu, Tao ^c   Liu, Dong Xu ^a   Lobie, Peter E ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

SMALL INTERFERING RNA; STAT5A PROTEIN; STAT5B PROTEIN;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CARCINOMA; CARCINOMA CELL; CELL CYCLE; CELL FUNCTION; CELL MIGRATION; CELL MOTILITY; CELL STRAIN MCF 7; CELL SURVIVAL; CONTROLLED STUDY; DEPLETION; DIFFERENTIAL DISPLAY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; XENOGRAFT;

ANIMALS; BREAST NEOPLASMS; CARCINOMA; CELL MOVEMENT; CELL PROLIFERATION; CELL SURVIVAL; DISEASE PROGRESSION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; MICE, NUDE; RNA, SMALL INTERFERING; STAT5 TRANSCRIPTION FACTOR; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 73649093445     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-0651     Document Type: Article

References (65)

1. Grimley PM, Dong F, Rui H 1999 Stat5a and Stat5b: fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev 10:131-157
2. Wood TJ, Sliva D, Lobie PE, Goullieux F, Mui AL, Groner B, Norstedt G, Haldosén LA1997 Specificity of transcription enhancement via the STATresponsive element in the serine protease inhibitor 2.1 promoter. Mol Cell Endocrinol 130:69-81
3. Wakao H, Gouilleux F, Groner B 1994 Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J 13: 2182-2191
4. Wagner K-U, Rui H 2008 Jak2/Stat5 signaling in mammogenesis, breast initiation and progression. J Mammary Gland Biology Neoplasia 13:93-103
5. Yao Z, Cui Y, Watford WT, Bream JH, Yamaoka K, Hissong BD, Li D, Durum SK, Jiang Q, Bhandoola A, Hennighausen L, O'Shea JJ 2006 Stat5a/b are essential for normal lymphoid development and differentiation. Proc Natl Acad Sci USA 103:1000-1005
6. Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L 1997 Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes Dev 11:179-186
7. Cui Y, Riedlinger G, Miyoshi K, Tang W, Li C, Deng CX, Robinson GW, Hennighausen L 2004 Inactivation of Stat5 in mouse mammary epithelium during pregnancy reveals distinct functions in cell proliferation, survival, and differentiation. Mol Cell Biol 24:8037-8047
8. Tan SH, Nevalainen MT 2008 Signal transducer and activator of transcription 5A/B in prostate and breast cancers. Endocr Relat Cancer 15:367-390
9. Yu H, Jove R 2004 The STATs of cancer - new molecular targets come of age. Nat Rev Cancer 4:97-105
10. Xi S, Zhang Q, Gooding WE, Smithgall TE, Grandis JR 2003 Constitutive activation of Stat5b contributes to carcinogenesis in vivo. Cancer Res 63:6763-6771
11. Leong PL, Xi S, Drenning SD, Dyer KF, Wentzel AL, Lerner EC, Smithgall TE, Grandis JR 2002 Differential function of STAT5 isoforms in head and neck cancer growth control. Oncogene 21:2846-2853
12. Lee TK, Man K, Poon RT, Lo CM, Yuen AP, Ng IO, Ng KT, Leonard W, Fan ST 2006 Signal transducers and activators of transcription 5b activation enhances hepatocellular carcinoma aggressiveness through induction of epithelial-mesenchymal transition. Cancer Res 66:9948-9956
13. Ren S, Cai HR, Li M, Furth PA 2002 Loss of Stat5a delays mammary cancer progression in a mouse model. Oncogene 21:4335-4339
14. Humphreys RC, Hennighausen L 1999 Signal transducer and activator of transcription 5a influences mammary epithelial cell survival and tumorigenesis. Cell Growth Differ 10:685-694
15. Iavnilovitch E, Cardiff RD, Groner B, Barash I 2004 Deregulation of Stat5 expression and activation causes mammary tumors in transgenic mice. Int J Cancer 112:607-619
16. Iavnilovitch E, Groner B, Barash I 2002 Overexpression and forced activation of Stat5 in mammary gland of transgenic mice promotes cellular proliferation, enhances differentiation, and delays postlactational apoptosis. Mol Cancer Res 1:32-47
17. Sotgia F, Williams TM, Schubert W, Medina F, Minetti C, Pestell RG, Lisanti MP 2006 Caveolin-1 deficiency (-/-) conveys premalignant alterations in mammary epithelia, with abnormal lumen formation, growth factor independence, and cell invasiveness. Am J Pathol 168:292-309
18. Cotarla I, Ren S, Zhang Y, Gehan E, Singh B, Furth PA 2004 Stat5a is tyrosine phosphorylated and nuclear localized in a high proportion of human breast cancers. Int J Cancer 108:665-671
19. Shan L, Yu M, Clark BD, Snyderwine EG 2004 Possible role of Stat5a in rat mammary gland carcinogenesis. Breast Cancer Res Treat 88:263-272
20. Nevalainen MT, Xie J, Torhorst J, Bubendorf L, Haas P, Kononen J, Sauter G, Rui H 2004 Signal transducer and activator of transcription-5 activation and breast cancer prognosis. J Clin Oncol 22:2053-2060
21. Bratthauer G, Strauss BL, Tavassoli FA 2006 STAT 5a expression in various lesions of the breast. Virchows Arch 448:165-171
22. Strauss BL, Bratthauer GL, Tavassoli FA 2006 STAT 5a expression in the breast is maintained in secretory carcinoma, in contrast to other histologic types. Hum Pathol 37:586-592
23. Mohankumar KM, Perry JK, Kannan N, Kohno K, Gluckman PD, Emerald BS, Lobie PE 2008 Transcriptional activation of signal transducer and activator of transcription (STAT) 3 and STAT5B partially mediate homeobox A1-stimulated oncogenic transformation of the immortalized human mammary epithelial cell. Endocrinology 149:2219-2229
24. Liu DX, Lobie PE 2007 Transcriptional activation of p53 by Pitx1. Cell Death Differ 14:1893-1907
25. Zhang X, Zhu T, Chen Y, Mertani HC, Lee KO, Lobie PE 2003 Human growth hormone-regulated HOXA1 is a human mammary epithelial oncogene. J Biol Chem 278:7580-7590
26. Mukhina S, Mertani HC, Guo K, Lee KO, Gluckman PD, Lobie PE 2004 Phenotypic conversion of human mammary carcinoma cells by autocrine human growth hormone. Proc Natl Acad Sci USA 101: 15166-15171
27. Shtutman M, Levina E, Ohouo P, Baig M, Roninson IB 2006 Cell adhesion molecule L1 disrupts E-Cadherin-containing adherens junctions and increases scattering and motility of MCF7- breast carcinoma cells. Cancer Res 66:11370-11380
28. Pandey V, Perry JK, Mohankumar KM, Kong XJ, Liu SM, Wu ZS, Mitchell MD, Zhu T, Lobie PE 2008 Autocrine human growth hormone stimulates oncogenicity of endometrial carcinoma cells. Endocrinology 149:3909-3919
29. Goh ELK, Pircher TJ, Wood TJ, Norstedt G, Graichen R, Lobie PE 1997 Growth hormone-induced reorganization of the actin cytoskeleton is not required for STAT5 (signal transducer and activator of transcription-5)-mediated transcription. Endocrinology 138: 3207-3215
30. Kang J, Perry JK, Pandey V, Fielder GC, Mei B, Qian PX, Wu ZS, Zhu T, Liu DX, Lobie PE 2009 Artemin is oncogenic for human mammary carcinoma cells. Oncogene 28:2034-2045
31. Hanahan D, Weinberg RA 2000 The hallmarks of cancer. Cell 100: 57-70
32. Thiery JP, Chopin D 1999 Epithelial cell plasticity in development and tumor progression. Cancer Metastasis Rev 18:31-42
33. Bajpai S, Correia J, Feng Y, Figueiredo J, Sun SX, Longmore GD, Suriano G, Wirtz D 2008 α-Catenin mediates initial E-cadherindependent cell to cell recognition and subsequent bond strengthening. Proc Natl Acad Sci USA 105:18331-18336
34. Bajpai S, Feng Y, Krishnamurthy R, Longmore GD, Wirtz D 2009 Loss of α-catenin decreases the strength of single E-cadherin bonds between human cancer cells. J Biol Chem 284:18252-18259
35. Yamashita H, Nishio M, Ando Y, Zhang Z, Hamaguchi M, Mita K, Kobayashi S, Fujii Y, Iwase H 2006 Stat5 expression predicts response to endocrine therapy and improves survival in estrogen receptor-positive breast cancer. Endocr Relat Cancer 13:885-893
36. Dagvadorj A, Kirken RA, Leiby B, Karras J, Nevalainen MT 2008 Transcription factor signal transducer and activator of transcription 5 promotes growth of human prostate cancer cells in vivo. Clin Cancer Res 14:1317-1324
37. Battle TE, Frank DA 2002 The role of STAT sin apoptosis. Curr Mol Med 2:381-392
38. Gao LF, Wen LJ, Yu H, Zhang L, Meng Y, Shao YT, Xu DQ, Zhao XJ 2006 Knockdown of Stat3 expression using RNAi inhibits growth of laryngeal tumors in vivo. Acta Pharmacol Sin 27:347-352
39. Gritsko T, Williams A, Turkson J, Kaneko S, Bowman T, Huang M, Nam S, Eweis I, Diaz N, Sullivan D, Yoder S, Enkemann S, Eschrich S, Lee JH, Beam CA, Cheng J, Minton S, Muro-Cacho CA, Jove R 2006 Persistent activation of Stat3 signaling induces survivin gene expression and confers resistance to apoptosis in human breast cancer cells. Clin Cancer Res 12:11-19
40. Tomita M, Kawakami H, Uchihara JN, Okudaira T, Masuda M, Matsuda T, Tanaka Y, Ohshiro K, Mori N 2006 Inhibition of constitutively active Jak-Stat pathway suppresses cell growth of human T-cell leukemia virus type 1-infected T-cell lines and primary adult T-cell leukemia cells. Retrovirology 3:22
41. Fukuda S, Pelus LM 2006 Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther 5:1087-1098
42. Altieri DC 2008 Survivin, cancer networks and pathway-directed drug discovery. Nat Rev Cancer 8:61-70
43. Klein CA 2009 Parallel progression of primary tumours and metastases. Nat Rev Cancer 9:302-312
44. Harms JF, Welch DR, Miele ME 2003 KISS1 metastasis suppression and emergent pathways. Clin Exp Metastasis 20:11-18
45. Chen RQ, Yang QK, Chen YL, Oliveira VA, Dalton WS, Fearns C, Lee JD 2009 Kinome siRNA screen identifies SMG-1 as a negative regulator of HIF-1alpha in hypoxia. J Biol Chem 284:16752-16758
46. Sultan AS, Xie J, LeBaron MJ, Ealley EL, Nevalainen MT, Rui H 2005 Stat5 promotes homotypic adhesion and inhibits invasive characteristics of human breast cancer cells. Oncogene 24:746-760
47. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA 2004 Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927-939
48. Garber K 2008 Epithelial-to-mesenchymal transition is important to metastasis, but questions remain. J Natl Cancer Inst 100: 232-233, 239
49. Shafiei F, Rahnama F, Pawella L, Mitchell MD, Gluckman PD, Lobie PE 2008 DNMT3A and DNMT3B mediate autocrine hGH repression of plakoglobin gene transcription and consequent phenotypic conversion of mammary carcinoma cells. Oncogene 27: 2602-2612
50. Zou W, Hu CH, Zhou JP 2002 Relationship between the expression of E-cadherin-catenins and α-, β-, γ-catenin and the metastasis and prognosis of breast cancer. Hunan Yi Ke Da Xue Xue Bao 27:499-502
51. De Leeuw WJ, Berx G, Vos CB, Peterse JL, Van de Vijver MJ, Litvinov S, Van Roy F, Cornelisse CJ, Cleton-Jansen AM 1997 Simultaneous loss of E-cadherin and catenins in invasive lobular breast cancer and lobular carcinoma in situ. J Pathol 183:404-411
52. Yoshida R, Kimura N, Harada Y, Ohuchi N 2001 The loss of E-cadherin, α- and β-catenin expression is associated with metastasis and poor prognosis in invasive breast cancer. Int J Oncol 18:513-520
53. Nakopoulou L, Gakiopoulou-Givalou H, Karayiannakis AJ, Giannopoulou I, Keramopoulos A, Davaris P, Pignatelli M 2002 Abnormal α-catenin expression in invasive breast cancer correlates with poor patient survival. Histopathology 40:536-546
54. Han A, Xiong M, Li Z, Liang Y 2001 E-cadherin associated protein expression and its significance in invasive lobular carcinoma and invasive ductal carcinoma of breast. Zhonghua Bing Li Xue Za Zhi 30:27-30
55. Hennighausen L, Robinson GW 2008 Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes Dev 22:711-721
56. Boucheron C, Dumon S, Santos SC, Moriggl R, Hennighausen L, Gisselbrecht S, Gouilleux F 1998 A single amino acid in the DNA binding regions of STAT5A and STAT5B confers distinct DNA binding specificities. J Biol Chem 273:33936-33941
57. Nelson EA, Walker SR, Alvarez JV, Frank DA 2004 Isolation of unique STAT5 targets by chromatin immunoprecipitation-based gene identification. J Biol Chem 279:54724-54730
58. Verdier F, Rabionet R, Gouilleux F, Beisenherz-Huss C, Varlet P, Muller O, Mayeux P, Lacombe C, Gisselbrecht S, Chretien S 1998 A sequence of the CIS gene promoter interacts preferentially with two associated STAT5A dimers: a distinct biochemical difference between STAT5A and STAT5B. Mol Cell Biol 18:5852-5860
59. Soldaini E, John S, Moro S, Bollenbacher J, Schindler U, Leonard WJ 2000 DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites. Mol Cell Biol 20:389-401
60. Tian M, Schiemann WP 2009 The TGF-βparadox in human cancer: an update. Future Oncol 5:259-271
61. Chen H, Lee JS, Liang X, Zhang H, Zhu T, Zhang Z, Taylor ME, Zahnow C, Feigenbaum L, Rein A, Sukumar S 2008 Hoxb7 inhibits transgenic HER-2/neu-induced mouse mammary tumor onset but promotes progression and lung metastasis. Cancer Res 68:3637-3644
62. Liu Q, Teh M, Ito K, Shah N, Ito Y, Yeoh KG 2007 CDX2 expression is progressively decreased in human gastric intestinal metaplasia, dysplasia and cancer. Mod Pathol 20:1286-1297
63. Ha Kim G, Am Song G, Youn Park D, Han Lee S, Hyun Lee D, Oh Kim T, Jae Jo H, Heo J, Hwan Kang D, Cho M 2006 CDX2 expression is increased in gastric cancers with less invasiveness and intestinal mucin phenotype. Scand J Gastroenterol 41:880-886
64. Jäger R, Friedrichs N, Heim I, Büttner R, Schorle H 2005 Dual role of AP-2γ in ErbB-2-induced mammary tumorigenesis. Breast Cancer Res Treat 90:273-280
65. Bai YQ, Yamamoto H, Akiyama Y, Tanaka H, Takizawa T, Koike M, Kenji Yagi O, Saitoh K, Takeshita K, Iwai T, Yuasa Y 2002 Ectopic expression of homeodomain protein CDX2 in intestinal metaplasia and carcinomas of the stomach. Cancer Lett 176:47-55