Regulation of adipose oestrogen output by mechanical stress

Nature Communications

Volumn 4, Issue , 2013, Pages

  Ghosh, Sagar ^a   Ashcraft, Keith ^a   Jahid, Md Jamiul ^b   April, Craig ^c   Ghajar, Cyrus M ^d   Ruan, Jianhua ^b   Wang, Howard ^a   Foster, Megan ^a   Hughes, Daniel C ^e   Ramirez, Amelie G ^e   Huang, Tim ^a   Fan, Jian Bing ^c   Hu, Yanfen ^a   Li, Rong ^a  

^a University of Texas Health Science Center   (United States)

^b One UTSA Circle   (United States)

^c ILLUMINA INC   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AROMATASE; BETA1 INTEGRIN; COLLAGEN TYPE 1; DEXAMETHASONE; DISCOIDIN DOMAIN RECEPTOR 1; ESTROGEN; GREEN FLUORESCENT PROTEIN; LETROZOLE; MESSENGER RNA; RECEPTOR; STRESS ACTIVATED PROTEIN KINASE 1; TRANSCRIPTION FACTOR JUNB; UNCLASSIFIED DRUG;

CANCER; CELL ORGANELLE; ENZYME ACTIVITY; ESTROGENIC COMPOUND; HORMONE; MATRIX; MECHANICAL PROPERTY; TUMOR; WOMENS HEALTH;

ABDOMINAL FAT; ADIPOSE TISSUE; ARTICLE; CANCER GROWTH; CELL CONTRACTILITY; CELL CULTURE; CELL FUNCTION; COMPLIANCE (PHYSICAL); CONTROLLED STUDY; ENZYME SUBSTRATE; ESTROGEN SYNTHESIS; EXTRACELLULAR MATRIX; FEMALE; GENE SILENCING; HUMAN; HUMAN TISSUE; INTRACELLULAR SIGNALING; MECHANICAL STIMULATION; MECHANICAL STRESS; MECHANOTRANSDUCTION; MICROENVIRONMENT; PHENOTYPE; PROMOTER REGION; PROTEIN EXPRESSION; STRESS FIBER; STROMA CELL; TUMOR CELL;

ADIPOSE TISSUE; ANIMALS; ANTIGENS, CD29; AROMATASE; BIOMECHANICAL PHENOMENA; BREAST NEOPLASMS; CATTLE; CELL CULTURE TECHNIQUES; COLLAGEN; CULTURE MEDIA, CONDITIONED; CYTOSKELETON; ESTROGENS; EXTRACELLULAR MATRIX; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; MAP KINASE SIGNALING SYSTEM; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; PHOSPHORYLATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, ESTROGEN; RNA, MESSENGER; STRESS, MECHANICAL; STROMAL CELLS; TRANSCRIPTION, GENETIC;

EID: 84878528754     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2794     Document Type: Article

References (60)

1. Alenghat, F. J. & Ingber, D. E. Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci. STKE 2002, pe6 (2002)
2. Nelson, C. M. & Bissell, M. J. Of extracellular matrix, scaffolds, and signalling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol. 22, 287-309 (2006)
3. Paszek, M. J. & Weaver, V. M. The tension mounts: mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia. 9, 325-342 (2004) (Pubitemid 41149140)
4. Provenzano, P. P., Inman, D. R., Eliceiri, K. W. & Keely, P. J. Matrix densityinduced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28, 4326-4343 (2009)
5. Butcher, D. T., Alliston, T. & Weaver, V. M. A tense situation: forcing tumour progression. Nat. Rev. Cancer 9, 108-122 (2009)
6. Bulun, S. E. et al. Regulation of aromatase expression in oestrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol. Rev 57, 359-383 (2005) (Pubitemid 41196955)
7. Kamat, A., Hinshelwood, M. M., Murry, B. A. & Mendelson, C. R. Mechanisms in tissue-specific regulation of oestrogen biosynthesis in humans. Trends Endo. Metab 13, 122-128 (2002) (Pubitemid 36734002)
8. Simpson, E. R. et al. Aromatase-a brief overview. Annu. Rev. Physiol. 64, 93-127 (2002)
9. van de Velde, C. J., Verma, S., van Nes, J. G., Masterman, C. & Pritchard, K. I. Switching from tamoxifen to aromatase inhibitors for adjuvant endocrine therapy in postmenopausal patients with early breast cancer. Cancer Treat Rev. 36, 54-62 (2009)
10. Goldhirsch, A. et al. Progress and promise: highlights of the international expert consensus on the primary therapy of early breast cancer 2007. Ann. Oncol. 18, 1133-1144 (2007) (Pubitemid 47244357)
11. Mouridsen, H. et al. Phase III study of letrozole versus tamoxifen as first-line therapy of advanced breast cancer in postmenopausal women: analysis of survival and update of efficacy from the International Letrozole Breast Cancer Group. J. Clin. Oncol. 21, 2101-2109 (2003) (Pubitemid 46606358)
12. Paridaens, R. J. et al. Phase III study comparing exemestane with tamoxifen as first-line hormonal treatment of metastatic breast cancer in postmenopausal women: the European Organisation for Research and Treatment of Cancer Breast Cancer Cooperative Group. J. Clin. Oncol. 26, 4883-4890 (2008)
13. Meng, L. et al. Tumor necrosis factor alpha and interleukin 11 secreted by malignant breast epithelial cells inhibit adipocyte differentiation by selectively down-regulating CCAAT/enhancer binding protein alpha and peroxisome proliferator-activated receptor gamma: mechanism of desmoplastic reaction. Cancer Res 61, 2250-2255 (2001) (Pubitemid 32692055)
14. Richards, J. A. & Brueggemeier, R. W. Prostaglandin E2 regulates aromatase activity and expression in human adipose stromal cells via two distinct receptor subtypes. J. Clin. Endocrinol. Metab. 88, 2810-2816 (2003) (Pubitemid 36724460)
15. Brueggemeier, R. W., Richards, J. A. & Petrel, T. A. Aromatase and cyclooxygenases: enzymes in breast cancer. J. Steroid Biochem. Mol. Biol. 86, 501-507 (2003) (Pubitemid 37412590)
16. Zhou, J. et al. Interactions between prostaglandin E(2), liver receptor homologue-1, and aromatase in breast cancer. Cancer Res 65, 657-663 (2005)
17. Sillem, M., Prifti, S., Neher, M. & Runnebaum, B. Extracellular matrix remodelling in the endometrium and its possible relevance to the pathogenesis of endometriosis. Hum. Reprod. Update 4, 730-735 (1998) (Pubitemid 29041487)
18. Sha, G. et al. Differentially expressed genes in human endometrial endothelial cells derived from eutopic endometrium of patients with endometriosis compared with those from patients without endometriosis. Hum. Reprod. 22, 3159-3169 (2007) (Pubitemid 351696770)
19. Klemmt, P. A., Carver, J. G., Koninckx, P., McVeigh, E. J. & Mardon, H. J. Endometrial cells from women with endometriosis have increased adhesion and proliferative capacity in response to extracellular matrix components: towards a mechanistic model for endometriosis progression. Hum. Reprod. 22, 3139-3147 (2007) (Pubitemid 351696769)
20. Walker, C. L. & Stewart, E. A. Uterine fibroids: the elephant in the room. Science 308, 1589-1592 (2005) (Pubitemid 40807499)
21. Leppert, P. C., Catherino, W. H. & Segars, J. H. A new hypothesis about the origin of uterine fibroids based on gene expression profiling with microarrays. Am. J. Obstet. Gynecol. 195, 415-420 (2006) (Pubitemid 44142369)
22. Rogers, R. et al. Mechanical homeostasis is altered in uterine leiomyoma. Am. J. Obstet. Gynecol. 198, 474 e471-411 (2008)
23. Hall, H. G., Farson, D. A. & Bissell, M. J. Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture. Proc. Natl Acad. Sci. USA 79, 4672-4676 (1982)
24. Fraley, S. I. et al. A distinctive role for focal adhesion proteins in threedimensional cell motility. Nat. Cell Biol. 12, 598-604 (2010)
25. Pelham, Jr. R. J. & Wang, Y. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl Acad. Sci. USA 94, 13661-13665 (1997) (Pubitemid 28009639)
26. Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 (2005) (Pubitemid 41317594)
27. Winer, J. P., Janmey, P. A., McCormick, M. E. & Funaki, M. Bone marrowderived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tiss. Eng. 15, 147-154 (2009)
28. Trappmann, B. et al. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 11, 642-649 (2012)
29. Yang, M. T., Fu, J., Wang, Y. K., Desai, R. A. & Chen, C. S. Assaying stem cell mechanobiology on microfabricated elastomeric substrates with geometrically modulated rigidity. Nat. Protoc. 6, 187-213 (2011)
30. Tee, S. Y., Bausch, A. R. & Janmey, P. A. The mechanical cell. Curr. Biol. 19, R745-R748 (2009)
31. Thery, M. Micropatterning as a tool to decipher cell morphogenesis and functions. J. Cell Sci. 123, 4201-4213 (2010)
32. Leitinger, B. & Hohenester, E. Mammalian collagen receptors. Matrix Biol. 26, 146-155 (2007) (Pubitemid 46401227)
33. Hidalgo-Carcedo, C. et al. Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 13, 49-58 (2011)
34. Konitsiotis, A. D. et al. Characterization of high affinity binding motifs for the discoidin domain receptor DDR2 in collagen. J. Biol. Chem. 283, 6861-6868 (2008)
35. Xu, H. et al. Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol. 30, 16-26 (2011)
36. Leitinger, B. Transmembrane collagen receptors. Annu. Rev. Cell Dev. Biol 27, 265-290 (2011)
37. Li, B., Tournier, C., Davis, R. J. & Flavell, R. A. Regulation of IL-4 expression by the transcription factor JunB during T helper cell differentiation. EMBO J. 18, 420-432 (1999) (Pubitemid 29041950)
38. Wang, C. Z., Su, H. W., Hsu, Y. C., Shen, M. R. & Tang, M. J. A discoidin domain receptor 1/SHP-2 signaling complex inhibits alpha2beta1-integrinmediated signal transducers and activators of transcription 1/3 activation and cell migration. Mol. Biol. Cell 17, 2839-2852 (2006)
39. Yeh, Y. C., Wang, C. Z. & Tang, M. J. Discoidin domain receptor 1 activation suppresses alpha2beta1 integrin-dependent cell spreading through inhibition of Cdc42 activity. J. Cell Physiol. 218, 146-156 (2009)
40. Christensen, A. P. & Corey, D. P. TRP channels in mechanosensation: direct or indirect activation? Nat. Rev. Neurosci. 8, 510-521 (2007) (Pubitemid 46985360)
41. Arnadottir, J. & Chalfie, M. Eukaryotic mechanosensitive channels. Annu. Rev. Biophys. 39, 111-137 (2010)
42. Meyer zum Gottesberge, A. M., Gross, O., Becker-Lendzian, U., Massing, T. & Vogel, W. F. Inner ear defects and hearing loss in mice lacking the collagen receptor DDR1. Lab. Invest. 88, 27-37 (2008)
43. Alexander, N. R. et al. Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18, 1295-1299 (2008)
44. Levental, K. R. et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009)
45. Lyons, T. R. et al. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat. Med 17, 1109-1115 (2011)
46. Schrader, J. et al. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53, 1192-1205 (2011)
47. Liu, J. et al. Soft fibrin gels promote selection and growth of tumorigenic cells. Nat. Mater 11, 734-741 (2012)
48. Rehman, J. et al. Secretion of angiogenic and antiapoptotic factors by human adipose stromal cells. Circulation 109, 1292-1298 (2004) (Pubitemid 38372789)
49. Walter, M., Liang, S., Ghosh, S., Hornsby, P. J. & Li, R. Interleukin 6 secreted from adipose stromal cells promotes migration and invasion of breast cancer cells. Oncogene 28, 2745-2755 (2009)
50. Finak, G. et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med 14, 518-527 (2008) (Pubitemid 351655218)
51. Chandler, E. M. et al. Implanted adipose progenitor cells as physicochemical regulators of breast cancer. Proc. Natl Acad. Sci. USA 109, 9786-9791 (2012)
52. Simpson, E. R. et al. Oestrogen-the good, the bad, and the unexpected. Endocr. Rev. 26, 332-330 (2005)
53. Amir, E., Seruga, B., Niraula, S., Carlsson, L. & Ocana, A. Toxicity of adjuvant endocrine therapy in postmenopausal breast cancer patients: a systematic review and meta-analysis. J. Natl Cancer Inst. 103, 1299-1309 (2011)
54. Katz, A. J., Tholpady, A., Tholpady, S. S., Shang, H. & Ogle, R. C. Cell surface and transcriptional characterization of human adipose-derived adherent stromal (hADAS) cells. Stem Cells 23, 412-423 (2005) (Pubitemid 40404460)
55. Hu, Y.-F. et al. Modulation of aromatase expression by BRCA1: a possible link to tissue-specific tumor suppression. Oncogene 24, 8343-8348 (2005)
56. Azioune, A., Carpi, N., Tseng, Q., Thery, M. & Piel, M. Protein micropatterns: A direct printing protocol using deep UVs. Methods Cell Biol. 97, 133-146 (2010)
57. Johnson, K. R., Leight, J. L. &Weaver, V. M. Demystifying the effects of a threedimensional microenvironment in tissue morphogenesis. Methods Cell Biol. 83, 547-583 (2007)
58. Ghosh, S., Choudary, A., Musi, N., Hu, Y. & Li, R. IKK{beta} mediates cell shape-induced aromatase expression and estrogen biosynthesis in adipose stromal cells. Mol. Endocrinol. 23, 662-670 (2009)
59. Sun, J. & Li, R. Human negative elongation factor activates transcription and regulates alternative transcription initiation. J. Biol. Chem. 285, 6443-6452 (2010)
60. April, C. et al. Whole-genome gene expression profiling of formalin-fixed, paraffin-embedded tissue samples. PLoS One 4, e8162 (2009).