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PMID: 19424782 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Stat3 and the inflammation/acute phase response in involution and breast cancer.

Journal of mammary gland biology and neoplasia ·Vol. 14 ·No. 2 ·2009-06-00 ·Pages 121-9

Pensa S, Watson CJ, Poli V

Abstract

The transcription factor Stat3 is essential for timely initiation of post-lactational regression and orchestrates the processes of cell death and tissue remodelling that occur during the first 6 days of involution in the mouse. Paradoxically, STAT3 is also frequently found to be constitutively active in breast cancer and tumors can become addicted to STAT3. This raises two interesting questions: 1) do the high levels of active Stat3 present in the mammary epithelium during involution promote tumor spread and 2) how do tumor cells escape the pro-apoptotic effects of Stat3? In order to address these questions, it is essential to understand the role of Stat3 in involution and the mechanisms by which Stat3 regulates both cell death and tissue remodelling. A number of studies have been undertaken using genetically modified mice and microarray analyses and two significant findings arose from these investigations. Firstly, post-lactational regression is associated with an acute phase and inflammatory response in addition to cell death and secondly, Stat3 alone is insufficient to induce involution in the absence of the NF-kappaB regulatory kinase IKKbeta. Both Stat3 and NF-kappaB have been shown to regulate the expression of genes involved in inflammatory signalling and the acute phase response. These findings suggest a role for the innate immune response in mammary epithelial cell fate during involution and highlight potential roles for this response in tissue remodelling-associated breast cancer metastasis.

MeSH Terms
Acute-Phase Reaction/physiopathology Animals Apoptosis/physiology Autoimmunity/physiology Breast Neoplasms/immunology,pathology,physiopathology Cytokines/physiology Female Gene Expression Profiling Gene Expression Regulation, Developmental Gene Expression Regulation, Neoplastic Humans I-kappa B Kinase/physiology Immune Tolerance/physiology Inflammation/physiopathology Lactation/physiology Mammary Glands, Animal/physiology Mice NF-kappa B/physiology Neoplasm Metastasis/physiopathology Pregnancy STAT3 Transcription Factor/physiology Transcription, Genetic
Chemicals
Cytokines NF-kappa B STAT3 Transcription Factor STAT3 protein, human Stat3 protein, mouse I-kappa B Kinase Ikbkb protein, mouse
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Pensa Sara
Department of Genetics, Molecular Biotechnology Center, University of Turin, Turin, Italy.
Watson Christine J
Poli Valeria
References (56)
56 references, click to expand
  1. An oligonucleotide decoy for Stat3 activates the immune response of macrophages to breast cancer.
    Immunobiology. 2006;211(3):199-209 PMID: 16530087
  2. Essential role of STAT3 in the control of the acute-phase response as revealed by inducible gene inactivation [correction of activation] in the liver.
    Mol Cell Biol. 2001 Mar;21(5):1621-32 PMID: 11238899
  3. Elevated milk soluble CD14 in bovine mammary glands challenged with Escherichia coli lipopolysaccharide.
    J Dairy Sci. 2003 Jul;86(7):2382-9 PMID: 12906056
  4. STAT proteins: novel molecular targets for cancer drug discovery.
    Oncogene. 2000 Dec 27;19(56):6613-26 PMID: 11426647
  5. Expression and function of serum amyloid A, a major acute-phase protein, in normal and disease states.
    Curr Opin Hematol. 2000 Jan;7(1):64-9 PMID: 10608507
  6. Airway epithelial STAT3 is required for allergic inflammation in a murine model of asthma.
    J Immunol. 2007 May 15;178(10):6191-9 PMID: 17475846
  7. Effects of secretion removal on bovine mammary gland function following an extended milk stasis.
    J Dairy Sci. 1999 Aug;82(8):1723-30 PMID: 10480098
  8. The genes induced by signal transducer and activators of transcription (STAT)3 and STAT5 in mammary epithelial cells define the roles of these STATs in mammary development.
    Mol Endocrinol. 2006 Mar;20(3):675-85 PMID: 16293640
  9. 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 Sep 15;275(37):29123-31 PMID: 10867011
  10. c-myc as a mediator of accelerated apoptosis and involution in mammary glands lacking Socs3.
    EMBO J. 2006 Dec 13;25(24):5805-15 PMID: 17139252
  11. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells.
    Immunity. 2006 Feb;24(2):179-89 PMID: 16473830
  12. Systematic review of the association between circulating interleukin-6 (IL-6) and cancer.
    Eur J Cancer. 2008 May;44(7):937-45 PMID: 18387296
  13. C/EBPdelta is a crucial regulator of pro-apoptotic gene expression during mammary gland involution.
    Development. 2005 Nov;132(21):4675-85 PMID: 16192306
  14. Stat3 regulates microtubules by antagonizing the depolymerization activity of stathmin.
    J Cell Biol. 2006 Jan 16;172(2):245-57 PMID: 16401721
  15. Stat3-induced apoptosis requires a molecular switch in PI(3)K subunit composition.
    Nat Cell Biol. 2005 Apr;7(4):392-8 PMID: 15793565
  16. Serum amyloid P aids complement-mediated immunity to Streptococcus pneumoniae.
    PLoS Pathog. 2007 Sep 28;3(9):1208-19 PMID: 17845072
  17. Targeting STAT3 affects melanoma on multiple fronts.
    Cancer Metastasis Rev. 2005 Jun;24(2):315-27 PMID: 15986140
  18. Impaired involution of mammary glands in the absence of milk fat globule EGF factor 8.
    Proc Natl Acad Sci U S A. 2005 Nov 15;102(46):16886-91 PMID: 16275924
  19. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis.
    Cancer Cell. 2009 Feb 3;15(2):91-102 PMID: 19185844
  20. Activation of the signal transducers and activators of the transcription 3 pathway in alveolar epithelial cells induces inflammation and adenocarcinomas in mouse lung.
    Cancer Res. 2007 Sep 15;67(18):8494-503 PMID: 17875688
  21. Regulation of the IL-23 and IL-12 balance by Stat3 signaling in the tumor microenvironment.
    Cancer Cell. 2009 Feb 3;15(2):114-23 PMID: 19185846
  22. Genome-wide discovery of functional transcription factor binding sites by comparative genomics: the case of Stat3.
    Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5117-22 PMID: 19282476
  23. Innate recognition of bacteria in human milk is mediated by a milk-derived highly expressed pattern recognition receptor, soluble CD14.
    J Exp Med. 2000 May 15;191(10):1807-12 PMID: 10811873
  24. Mammary gland immunity and mastitis susceptibility.
    J Mammary Gland Biol Neoplasia. 2002 Apr;7(2):135-46 PMID: 12463736
  25. Human CD14 mediates recognition and phagocytosis of apoptotic cells.
    Nature. 1998 Apr 2;392(6675):505-9 PMID: 9548256
  26. Acute-phase response factor, a nuclear factor binding to acute-phase response elements, is rapidly activated by interleukin-6 at the posttranslational level.
    Mol Cell Biol. 1993 Jan;13(1):276-88 PMID: 7678052
  27. Signal transducer and activator of transcription 3 is required for hypoxia-inducible factor-1alpha RNA expression in both tumor cells and tumor-associated myeloid cells.
    Mol Cancer Res. 2008 Jul;6(7):1099-105 PMID: 18644974
  28. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis.
    EMBO J. 1999 Sep 1;18(17):4657-68 PMID: 10469645
  29. A dual role for oncostatin M signaling in the differentiation and death of mammary epithelial cells in vivo.
    Mol Endocrinol. 2008 Dec;22(12):2677-88 PMID: 18927239
  30. Stat3 as an oncogene.
    Cell. 1999 Aug 6;98(3):295-303 PMID: 10458605
  31. General nature of the STAT3-activated anti-inflammatory response.
    J Immunol. 2006 Dec 1;177(11):7880-8 PMID: 17114459
  32. Gene expression profiling of mammary gland development reveals putative roles for death receptors and immune mediators in post-lactational regression.
    Breast Cancer Res. 2004;6(2):R92-109 PMID: 14979921
  33. Orosomucoid (alpha1-acid glycoprotein) plasma concentration and genetic variants: effects on human immunodeficiency virus protease inhibitor clearance and cellular accumulation.
    Clin Pharmacol Ther. 2006 Oct;80(4):307-18 PMID: 17015049
  34. Selective expansion of foxp3-positive regulatory T cells and immunosuppression by suppressors of cytokine signaling 3-deficient dendritic cells.
    J Immunol. 2007 Aug 15;179(4):2170-9 PMID: 17675476
  35. Inflammation and cancer: IL-6 and STAT3 complete the link.
    Cancer Cell. 2009 Feb 3;15(2):79-80 PMID: 19185839
  36. Rheumatoid arthritis synoviocyte survival is dependent on Stat3.
    J Immunol. 2002 Dec 1;169(11):6610-6 PMID: 12444174
  37. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer.
    Cancer Cell. 2009 Feb 3;15(2):103-13 PMID: 19185845
  38. Transforming growth factor-beta induces development of the T(H)17 lineage.
    Nature. 2006 May 11;441(7090):231-4 PMID: 16648837
  39. STAT3 and STAT1 mediate IL-11-dependent and inflammation-associated gastric tumorigenesis in gp130 receptor mutant mice.
    J Clin Invest. 2008 May;118(5):1727-38 PMID: 18431520
  40. Stat3 Controls Cell Movements during Zebrafish Gastrulation.
    Dev Cell. 2002 Mar;2(3):363-75 PMID: 11879641
  41. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity.
    Nat Med. 2005 Dec;11(12):1314-21 PMID: 16288283
  42. The role of C/EBP isoforms in the control of inflammatory and native immunity functions.
    J Biol Chem. 1998 Nov 6;273(45):29279-82 PMID: 9792624
  43. The expression of alpha(1)-acid glycoprotein mRNA during rat development. High levels of expression in the decidua.
    J Biol Chem. 1989 Apr 5;264(10):5784-90 PMID: 2925634
  44. Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3.
    Genes Dev. 1999 Oct 1;13(19):2604-16 PMID: 10521404
  45. Stat3 activity in melanoma cells affects migration of immune effector cells and nitric oxide-mediated antitumor effects.
    J Immunol. 2005 Apr 1;174(7):3925-31 PMID: 15778348
  46. Sle1ab mediates the aberrant activation of STAT3 and Ras-ERK signaling pathways in B lymphocytes.
    J Immunol. 2005 Feb 1;174(3):1630-7 PMID: 15661926
  47. Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and -dependent pathways.
    Development. 1996 Jan;122(1):181-93 PMID: 8565829
  48. Disruption of Stat3 reveals a critical role in both the initiation and the promotion stages of epithelial carcinogenesis.
    J Clin Invest. 2004 Sep;114(5):720-8 PMID: 15343391
  49. Tissue involution and the acute phase response.
    Ann N Y Acad Sci. 2003 May;995:94-108 PMID: 12814942
  50. Deletion of Stat3 blocks mammary gland involution and extends functional competence of the secretory epithelium in the absence of lactogenic stimuli.
    Endocrinology. 2002 Sep;143(9):3641-50 PMID: 12193580
  51. Involution of the mouse mammary gland is associated with an immune cascade and an acute-phase response, involving LBP, CD14 and STAT3.
    Breast Cancer Res. 2004;6(2):R75-91 PMID: 14979920
  52. pH-dependency of basic ligand binding to alpha 1-acid glycoprotein (orosomucoid).
    Biochem J. 1991 Nov 15;280 ( Pt 1):277-80 PMID: 1741754
  53. Mfge8 is critical for mammary gland remodeling during involution.
    Mol Biol Cell. 2005 Dec;16(12):5528-37 PMID: 16195353
  54. Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells.
    Nat Med. 2004 Jan;10(1):48-54 PMID: 14702634
  55. Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice.
    J Clin Invest. 2008 Oct;118(10):3367-77 PMID: 18776941
  56. A critical role for Stat3 signaling in immune tolerance.
    Immunity. 2003 Sep;19(3):425-36 PMID: 14499117
Article Info
Journal
Journal of mammary gland biology and neoplasia
Abbr.
J Mammary Gland Biol Neoplasia
ISSN
1573-7039
Published
2009-06-00
Epub
2009-00-08
Pages
121-9
Language
English
Region
United States
NLM ID
9601804
Subset
IM
Grants
Breast Cancer Now · 2006NOVPHD11 · United Kingdom
Wellcome Trust · United Kingdom
Biotechnology and Biological Sciences Research Council · United Kingdom
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