The cytokine il-6 reactivates breast stromal fibroblasts through transcription factor STAT3-dependent up-regulation of the RNA-binding protein AUF1

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 30962-30976

  Hendrayani, Siti Fauziah ^a   Al Khalaf, Huda H ^a,b   Aboussekhra, Abdelilah ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b KING ABDULAZIZ CITY FOR SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINES; RNA-BINDING PROTEIN; UP-REGULATION;

ALPHA SMOOTH MUSCLE ACTIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2A; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN D; INTERLEUKIN 6; JANUS KINASE 3; MESSENGER RNA; PROTEIN P53; STAT3 PROTEIN; STROMAL CELL DERIVED FACTOR 1; TRANSFORMING GROWTH FACTOR BETA1; CDKN1A PROTEIN, HUMAN; CULTURE MEDIUM; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HNRNP D0; IL6 PROTEIN, HUMAN; STAT3 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER CELL LINE; BREAST CELL; BREAST STROMAL FIBROBLAST; CELL ACTIVATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; MYOFIBROBLAST; PARACRINE SIGNALING; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; UPREGULATION; BREAST TUMOR; CELL MOTION; CELL PROLIFERATION; CHEMISTRY; CULTURE MEDIUM; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; STROMA CELL; TUMOR CELL LINE;

BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P21; FEMALE; FIBROBLASTS; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HUMANS; INTERLEUKIN-6; MYOFIBROBLASTS; RNA, MESSENGER; STAT3 TRANSCRIPTION FACTOR; STROMAL CELLS; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84909607972     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.594044     Document Type: Article

References (49)

1. Hanahan, D., and Weinberg, R. A. (2011) Hallmarks of cancer: the next generation. Cell 144, 646-674
2. Pietras, K., and Ostman, A. (2010) Hallmarks of cancer: interactions with the tumor stroma. Exp. Cell Res. 316, 1324-1331
3. Albini, A., Mirisola, V., and Pfeffer, U. (2008) Metastasis signatures: genes regulating tumor-microenvironment interactions predict metastatic behavior. Cancer Metastasis Rev. 27, 75-83
4. Allen, M., and Louise Jones, J. (2011) Jekyll and Hyde: the role of the microenvironment on the progression of cancer. J. Pathol. 223, 162-176
5. Rønnov-Jessen, L., Petersen, O. W., Koteliansky, V. E., and Bissell, M. J. (1995) The origin of the myofibroblasts in breast cancer: recapitulation of tumor environment in culture unravels diversity and implicates converted fibroblasts and recruited smooth muscle cells. J. Clin. Invest. 95, 859-873
6. Kojima, Y., Acar, A., Eaton, E. N., Mellody, K. T., Scheel, C., Ben-Porath, I., Onder, T. T., Wang, Z. C., Richardson, A. L., Weinberg, R. A., and Orimo, A. (2010) Autocrine TGF-βand stromal cell-derived factor-1 (SDF-1) signaling drives the evolution of tumor-promoting mammary stromal myofibroblasts. Proc. Natl. Acad. Sci. U.S.A. 107, 20009-20014
7. Vaughan, M. B., Howard, E. W., and Tomasek, J. J. (2000) Transforming growth factor-1 promotes the morphological and functional differentiation of the myofibroblast. Exp. Cell Res. 257, 180-189
8. Knüpfer, H., and Preiss, R. (2007) Significance of interleukin-6 (IL-6) in breast cancer (review). Breast Cancer Res. Treat. 102, 129-135
9. Chavey, C., Bibeau, F., Gourgou-Bourgade, S., Burlinchon, S., Boissière, F., Laune, D., Roques, S., and Lazennec, G. (2007) Oestrogen receptor negative breast cancers exhibit high cytokine content. Breast Cancer Res. 9, R15
10. Schafer, Z. T., and Brugge, J. S. (2007) IL-6 involvement in epithelial cancers. J. Clin. Invest. 117, 3660-3663
11. Sansone, P., Storci, G., Tavolari, S., Guarnieri, T., Giovannini, C., Taffurelli, M., Ceccarelli, C., Santini, D., Paterini, P., Marcu, K. B., Chieco, P., and Bonafè, M. (2007) IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland. J. Clin. Invest. 117, 3988-4002
12. Sasser, A. K., Sullivan, N. J., Studebaker, A. W., Hendey, L. F., Axel, A. E., and Hall, B. M. (2007) Interleukin-6 is a potent growth factor for ER- positive human breast cancer. FASEB J. 21, 3763-3770
13. Spaeth, E. L., Dembinski, J. L., Sasser, A. K., Watson, K., Klopp, A., Hall, B., Andreeff, M., and Marini, F. (2009) Mesenchymal stem cell transition to tumor-associated fibroblasts contributes to fibrovascular network expansion and tumor progression. PLoS One 4, e4992
14. Tamm, I., Cardinale, I., Krueger, J., Murphy, J. S., May, L. T., and Sehgal, P. B. (1989) Interleukin 6 decreases cell-cell association and increases motility of ductal breast carcinoma cells. J. Exp. Med. 170, 1649-1669
15. Sullivan, N. J., Sasser, A. K., Axel, A. E., Vesuna, F., Raman, V., Ramirez, N., Oberyszyn, T. M., and Hall, B. M. (2009) Interleukin-6 induces an epithe-lial- mesenchymal transition phenotype in human breast cancer cells. Oncogene 28, 2940-2947
16. Chang, Q., Bournazou, E., Sansone, P., Berishaj, M., Gao, S. P., Daly, L., Wels, J., Theilen, T., Granitto, S., Zhang, X., Cotari, J., Alpaugh, M. L., de Stanchina, E., Manova, K., Li, M., Bonafe, M., Ceccarelli, C., Taffurelli, M., Santini, D., Altan-Bonnet, G., Kaplan, R., Norton, L., Nishimoto, N., Huszar, D., Lyden, D., and Bromberg, J. (2013) The IL-6/JAK/Stat3 feed-forward loop drives tumorigenesis and metastasis. Neoplasia 15, 848-862
17. Akira, S., Nishio, Y., Inoue, M., Wang, X. J., Wei, S., Matsusaka, T., Yoshida, K., Sudo, T., Naruto, M., and Kishimoto, T. (1994) Molecular cloning of APRF, a novel IFN-stimulated gene factor 3 p91-related transcription factor involved in the gp130-mediated signaling pathway. Cell 77, 63-71
18. Gao, S. P., Mark, K. G., Leslie, K., Pao, W., Motoi, N., Gerald, W. L., Travis, W. D., Bornmann, W., Veach, D., Clarkson, B., and Bromberg, J. F. (2007) Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas. J. Clin. Invest. 117, 3846-3856
19. Dethlefsen, C., Højfeldt, G., and Hojman, P. (2013) The role of intratumoral and systemic IL-6 in breast cancer. Breast Cancer Res. Treat. 138, 657-664
20. Lieblein, J. C., Ball, S., Hutzen, B., Sasser, A. K., Lin, H. J., Huang, T. H., Hall, B. M., and Lin, J. (2008) STAT3 can be activated through paracrine signaling in breast epithelial cells. BMC Cancer 8, 302
21. Sriuranpong, V., Park, J. I., Amornphimoltham, P., Patel, V., Nelkin, B. D., and Gutkind, J. S. (2003) Epidermal growth factor receptor-independent constitutive activation of STAT3 in head and neck squamous cell carcinoma is mediated by the autocrine/paracrine stimulation of the interleukin 6/gp130 cytokine system. Cancer Res. 63, 2948-2956
22. Groner, B., Lucks, P., and Borghouts, C. (2008) The function of Stat3 in tumor cells and their microenvironment. Semin. Cell Dev. Biol. 19, 341-350
23. Dolled-Filhart, M., Camp, R. L., Kowalski, D. P., Smith, B. L., and Rimm, D. L. (2003) 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. 9, 594-600
24. Berishaj, M., Gao, S. P., Ahmed, S., Leslie, K., Al-Ahmadie, H., Gerald, W. L., Bornmann, W., and Bromberg, J. F. (2007) Stat3 is tyrosine-phosphorylated through the interleukin-6/glycoprotein 130/Janus kinase pathway in breast cancer. Breast Cancer Res. 9, R32
25. Dauer, D. J., Ferraro, B., Song, L., Yu, B., Mora, L., Buettner, R., Enkemann, S., Jove, R., and Haura, E. B. (2005) Stat3 regulates genes common to both wound healing and cancer. Oncogene 24, 3397-3408
26. Yu, H., Kortylewski, M., and Pardoll, D. (2007) Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat. Rev. Immunol. 7, 41-51
27. Aboussekhra, A. (2011) Role of cancer-associated fibroblasts in breast cancer development and prognosis. Int. J. Dev. Biol. 55, 841-849
28. Al-Ansari, M. M., Hendrayani, S. F., Shehata, A. I., and Aboussekhra, A. (2013) p16(INK4A) Represses the paracrine tumor-promoting effects of breast stromal fibroblasts. Oncogene 32, 2356-2364
29. Hawsawi, N. M., Ghebeh, H., Hendrayani, S. F., Tulbah, A., Al-Eid, M., Al-Tweigeri, T., Ajarim, D., Alaiya, A., Dermime, S., and Aboussekhra, A. (2008) Breast carcinoma-associated fibroblasts and their counterparts display neoplastic-specific changes. Cancer Res. 68, 2717-2725
30. Al-Mohanna, M. A., Al-Khalaf, H. H., Al-Yousef, N., and Aboussekhra, A. (2007) The p16INK4a tumor suppressor controls p21WAF1 induction in response to ultraviolet light. Nucleic Acids Res. 35, 223-233
31. Wang, W., Martindale, J. L., Yang, X., Chrest, F. J., and Gorospe, M. (2005) Increased stability of the p16 mRNA with replicative senescence. EMBO Rep. 6, 158-164 32. Niu, G., Wright, K. L., Ma, Y., Wright, G. M., Huang, M., Irby, R., Briggs, J., Karras, J., Cress, W. D., Pardoll, D., Jove, R., Chen, J., and Yu, H. (2005) Role of Stat3 in regulating p53 expression and function. Mol. Cell Biol. 25, 7432-7440
32. Lal, A., Mazan-Mamczarz, K., Kawai, T., Yang, X., Martindale, J. L., and Gorospe, M. (2004) Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23, 3092-3102
33. Wagner, B. J., DeMaria, C. T., Sun, Y., Wilson, G. M., and Brewer, G. (1998) Structure and genomic organization of the human AUF1 gene: alternative pre-mRNA splicing generates four protein isoforms. Genomics 48, 195-202
34. Batlle, E., Sancho, E., Franc?, C., Dom?nguez, D., Monfar, M., Baulida, J., and Garc?a De Herreros, A. (2000) The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89
35. Yang, J., Mani, S. A., Donaher, J. L., Ramaswamy, S., Itzykson, R. A., Come, C., Savagner, P., Gitelman, I., Richardson, A., and Weinberg, R. A. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939
36. Cano, A., Pe?rez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83
37. Jablonka, S., Bandilla, M., Wiese, S., Bu?hler, D., Wirth, B., Sendtner, M., and Fischer, U. (2001) Co-regulation of survival of motor neuron (SMN) protein and its interactor SIP1 during development and in spinal muscular atrophy. Hum. Mol. Genet. 10, 497-505
38. Rønnov-Jessen, L., and Petersen, O. W. (1993) Induction of -smooth muscle actin by transforming growth factor-1 in quiescent human breast gland fibroblasts. Implications for myofibroblast generation in breast neoplasia. Lab. Invest. 68, 696-707
39. Xu, J., Lu, Y., Qiu, S., Chen, Z. N., and Fan, Z. (2013) A novel role of EMMPRIN/CD147 in transformation of quiescent fibroblasts to cancerassociated fibroblasts by breast cancer cells. Cancer Lett. 335, 380-386
40. Bar, J., Feniger-Barish, R., Lukashchuk, N., Shaham, H., Moskovits, N., Goldfinger, N., Simansky, D., Perlman, M., Papa, M., Yosepovich, A., Rechavi, G., Rotter, V., and Oren, M. (2009) Cancer cells suppress p53 in adjacent fibroblasts. Oncogene 28, 933-936
41. Kiaris, H., Chatzistamou, I., Trimis, G., Frangou-Plemmenou, M., Pafiti- Kondi, A., and Kalofoutis, A. (2005) Evidence for nonautonomous effect of p53 tumor suppressor in carcinogenesis. Cancer Res. 65, 1627-1630
42. Moskovits, N., Kalinkovich, A., Bar, J., Lapidot, T., and Oren, M. (2006) p53 Attenuates cancer cell migration and invasion through repression of SDF-1/CXCL12 expression in stromal fibroblasts. Cancer Res. 66, 10671-10676
43. Trimis, G., Chatzistamou, I., Politi, K., Kiaris, H., and Papavassiliou, A. G. (2008) Expression of p21waf1/Cip1 in stromal fibroblasts of primary breast tumors. Hum. Mol. Genet. 17, 3596-3600
44. Paschoud, S., Dogar, A. M., Kuntz, C., Grisoni-Neupert, B., Richman, L., and Ku?hn, L. C. (2006) Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNAbinding protein AUF1. Mol. Cell Biol. 26, 8228-8241
45. Al-Khalaf, H. H., Colak, D., Al-Saif, M., Al-Bakheet, A., Hendrayani, S. F., Al-Yousef, N., Kaya, N., Khabar, K. S., and Aboussekhra, A. (2011) p16(INK4a) positively regulates cyclin D1 and E2F1 through negative control of AUF1. PLoS One 6, e21111
46. Zucconi, B. E., and Wilson, G. M. (2011) Modulation of neoplastic gene regulatory pathways by the RNA-binding factor AUF1. Front. Biosci. (Landmark Ed.) 16, 2307-2325
47. Gouble, A., Grazide, S., Meggetto, F., Mercier, P., Delsol, G., and Morello, D. (2002) A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice. Cancer Res. 62, 1489-1495
48. Trojanowicz, B., Brodauf, L., Sekulla, C., Lorenz, K., Finke, R., Dralle, H., and Hoang-Vu, C. (2009) The role of AUF1 in thyroid carcinoma progression. Endocr. Relat. Cancer 16, 857-871
49. Abdelmohsen, K., Tominaga-Yamanaka, K., Srikantan, S., Yoon, J. H., Kang, M. J., and Gorospe, M. (2012) RNA-binding protein AUF1 represses Dicer expression. Nucleic Acids Res. 40, 11531-11544