Obesity-dependent changes in interstitial ECM mechanics promote breast tumorigenesis

Science Translational Medicine

Volumn 7, Issue 301, 2015, Pages

  Seo, Bo Ri ^a   Bhardwaj, Priya ^b   Choi, Siyoung ^a   Gonzalez, Jacqueline ^a   Eguiluz, Roberto C Andresen ^a   Wang, Karin ^a   Mohanan, Sunish ^c   Morris, Patrick G ^d   Du, Baoheng ^b   Zhou, Xi K ^b   Vahdat, Linda T ^b   Verma, Akanksha ^b   Elemento, Olivier ^b   Hudis, Clifford A ^d   Williams, Rebecca M ^a   Gourdon, Delphine ^a   Dannenberg, Andrew J ^b   Fischbach, Claudia ^a  

^a Cornell University   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN;

ADIPOSE STROMAL CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM CELL; CALORIC RESTRICTION; CANCER CELL; CELL DENSITY; CELL DIFFERENTIATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROSING ALVEOLITIS; HUMAN; HUMAN TISSUE; MECHANOTRANSDUCTION; MOUSE; MYOFIBROBLAST; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN UNFOLDING; RIGIDITY; STROMA CELL; ADIPOSE TISSUE; ANIMAL; BREAST NEOPLASMS; CELL CULTURE; CELL TRANSFORMATION; COMPLICATION; FEMALE; GENETICS; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ADIPOSE TISSUE; ANIMALS; BREAST NEOPLASMS; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; EXTRACELLULAR MATRIX; FEMALE; HUMANS; MICE; MICE, OBESE; OBESITY;

EID: 84939817343     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3010467     Document Type: Article

References (58)

1. S. Hefetz-Sela, P. E. Scherer, Adipocytes: Impact on tumor growth and potential sites for therapeutic intervention. Pharmacol. Ther. 138, 197-210 (2013).
2. M. J. Khandekar, P. Cohen, B. M. Spiegelman, Molecular mechanisms of cancer development in obesity. Nat. Rev. Cancer 11, 886-895 (2011).
3. C. Henegar, J. Tordjman, V. Achard, D. Lacasa, I. Cremer,M. Guerre-Millo, C. Poitou, A. Basdevant, V. Stich, N. Viguerie, D. Langin, P. Bedossa, J. D. Zucker, K. Clemen, Adipose tissue transcriptomic signature highlights the pathological relevance of extracellular matrix in human obesity. Genome Biol. 9, R14 (2008).
4. J. Park, P. E. Scherer, Adipocyte-derived endotrophin promotes malignant tumor progression. J. Clin. Invest. 122, 4243-4256 (2012).
5. J. Schrader, T. T. Gordon-Walker, R. L. Aucott, M. van Deemter, A. Quaas, S. Walsh, D. Benten, S. J. Forbes, R. G. Wells, J. P. Iredale, Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53, 1192-1205 (2011).
6. M. Egeblad, M. G. Rasch, V. M. Weaver, Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22, 697-706 (2010).
7. P. P. Provenzano, D. R. Inman, K. W. Eliceiri, P. J. Keely, Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28, 4326-4343 (2009).
8. M. J. Paszek, N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, V. M. Weaver, Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254 (2005).
9. A. Mammoto, K. M. Connor, T. Mammoto, C. W. Yung, D. Huh, C. M. Aderman, G. Mostoslavsky, L. E. Smith, D. E. Ingber, A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457, 1103-1108 (2009).
10. A. J. Engler, S. Sen, H. L. Sweeney, D. E. Discher, Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689 (2006).
11. E. M. Chandler, B. R. Seo, J. P. Califano, R. C. Andresen Eguiluz, J. S. Lee, C. J. Yoon, D. T. Tims, J. X. Wang, L. Cheng, S. Mohanan, M. R. Buckley, I. Cohen, A. Y. Nikitin, R. M. Williams, D. Gourdon, C. A. Reinhart-King, C. Fischbach, Implanted adipose progenitor cells as physicochemical regulators of breast cancer. Proc. Natl. Acad. Sci. U.S.A. 109, 9786-9791 (2012).
12. J. J. Tomasek, G. Gabbiani, B. Hinz, C. Chaponnier, R. A. Brown, Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3, 349-363 (2002).
13. K. R. Levental, H. Yu, L. Kass, J. N. Lakins, M. Egeblad, J. T. Erler, S. F. Fong, K. Csiszar, A. Giaccia, W. Weninger, M. Yamauchi, D. L. Gasser, V. M. Weaver, Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906 (2009).
14. H. Yadav, C. Quijano, A. K. Kamaraju, O. Gavrilova, R. Malek, W. Chen, P. Zerfas, D. Zhigang, E. C. Wright, C. Stuelten, P. Sun, S. Lonning, M. Skarulis, A. E. Sumner, T. Finkel, S. G. Rane, Protection from obesity and diabetes by blockade of TGF-b/Smad3 signaling. Cell Metab. 14, 67-79 (2011).
15. M. C. Vohl, R. Sladek, J. Robitaille, S. Gurd, P. Marceau, D. Richard, T. J. Hudson, A. Tchernof, A survey of genes differentially expressed in subcutaneous and visceral adipose tissue in men. Obes. Res. 12, 1217-1222 (2004).
16. A. Divoux, J. Tordjman, D. Lacasa, N. Veyrie, D. Hugol, A. Aissat, A. Basdevant, M. Guerre-Millo, C. Poitou, J.-D. Zucker, P. Bedossa, K. Clément, Fibrosis in human adipose tissue: Composition, distribution, and link with lipid metabolism and fat mass loss. Diabetes 59, 2817-2825 (2010).
17. Y. Zhang, R. Proenca, M. Maffei, M. Barone, L. Leopold, J. M. Friedman, Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425-432 (1994).
18. E. E. Calle, R. Kaaks, Overweight, obesity and cancer: Epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4, 579-591 (2004).
19. K. Subbaramaiah, L. R. Howe, P. Bhardwaj, B. Du, C. Gravaghi, R. K. Yantiss, X. K. Zhou, V. A. Blaho, T. Hla, P. Yang, L. Kopelovich, C. A. Hudis, A. J. Dannenberg, Obesity is associated with inflammation and elevated aromatase expression in the mouse mammary gland. Cancer Prev. Res. 4, 329-346 (2011).
20. M. W. Conklin, J. C. Eickhoff, K. M. Riching, C. A. Pehlke, K. W. Eliceiri, P. P. Provenzano, A. Friedl, P. J. Keely, Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am. J. Pathol. 178, 1221-1232 (2011).
21. A. Orimo, R. A. Weinberg, Stromal fibroblasts in cancer: A novel tumor-promoting cell type. Cell Cycle 5, 1597-1601 (2006).
22. H. P. Ehrlich, T. M. Krummel, Regulation of wound healing from a connective tissue perspective. Wound Repair Regen. 4, 203-210 (1996).
23. F. Shi, J. Harman, K. Fujiwara, J. Sottile, Collagen I matrix turnover is regulated by fibronectin polymerization. Am. J. Physiol. Cell Physiol. 298, C1265-C1275 (2010).
24. K. E. Kadler, A. Hill, E. G. Canty-Laird, Collagen fibrillogenesis: Fibronectin, integrins, and minor collagens as organizers and nucleators. Curr. Opin. Cell Biol. 20, 495-501 (2008).
25. P. Singh, C. Carraher, J. E. Schwarzbauer, Assembly of fibronectin extracellular matrix. Annu. Rev. Cell Dev. Biol. 26, 397-419 (2010).
26. E. M. Chandler, M. P. Saunders, C. J. Yoon, D. Gourdon, C. Fischbach, Adipose progenitor cells increase fibronectin matrix strain and unfolding in breast tumors. Phys. Biol. 8, 015008 (2011).
27. K. Wang, R. C. Andresen Eguiluz, F. Wu, B. R. Seo, C. Fischbach, D. Gourdon, Stiffening and unfolding of early deposited-fibronectin increase proangiogenic factor secretion by breast cancer-Associated stromal cells. Biomaterials 54, 63-71 (2015).
28. A. Krammer, D. Craig, W. E. Thomas, K. Schulten, V. Vogel, A structural model for force regulated integrin binding to fibronectin's RGD-synergy site. Matrix Biol. 21, 139-147 (2002).
29. J. L. Balestrini, S. Chaudhry, V. Sarrazy, A. Koehler, B. Hinz, The mechanical memory of lung myofibroblasts. Integr. Biol. 4, 410-421 (2012).
30. F. Calvo, N. Ege, A. Grande-Garcia, S. Hooper, R. P. Jenkins, S. I. Chaudhry, K. Harrington, P. Williamson, E. Moeendarbary, G. Charras, E. Sahai, Mechanotransduction and YAPdependent matrix remodelling is required for the generation and maintenance of cancerassociated fibroblasts. Nat. Cell Biol. 15, 637-646 (2013).
31. L. Buscemi, D. Ramonet, F. Klingberg, A. Formey, J. Smith-Clerc, J.J. Meister, B. Hinz, The single-molecule mechanics of the latent TGF-b1 complex. Curr. Biol. 21, 2046-2054 (2011).
32. J. C. Friedland, M. H. Lee, D. Boettiger, Mechanically activated integrin switch controls a5b1 function. Science 323, 642-644 (2009).
33. P. P. Provenzano, P. J. Keely, Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J. Cell Sci. 124, 1195-1205 (2011).
34. S. Dupont, L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, N. Elvassore, S. Piccolo, Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183 (2011).
35. J. Debnath, S. K. Muthuswamy, J. S. Brugge, Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30, 256-268 (2003).
36. O. Chaudhuri, S. T. Koshy, C. Branco da Cunha, J.-W. Shin, C. S. Verbeke, K. H. Allison, D. J. Mooney, Extracellular matrix stiffness and composition jointly regulate the induction of malignant phenotypes in mammary epithelium. Nat. Mater. 13, 970-978 (2014).
37. P. G. Morris, C. A. Hudis, D. Giri, M. Morrow, D. J. Falcone, X. K. Zhou, B. Du, E. Brogi, C. B. Crawford, L. Kopelovich, K. Subbaramaiah, A. J. Dannenberg, Inflammation and increased aromatase expression occur in the breast tissue of obese women with breast cancer. Cancer Prev. Res. 4, 1021-1029 (2011).
38. M. Tanaka, K. Ikeda, T. Suganami, C. Komiya, K. Ochi, I. Shirakawa, M. Hamaguchi, S. Nishimura, I. Manabe, T. Matsuda, K. Kimura, H. Inoue, Y. Inagaki, S. Aoe, S. Yamasaki, Y. Ogawa, Macrophage-inducible C-Type lectin underlies obesity-induced adipose tissue fibrosis. Nat. Commun. 5, 4982 (2014).
39. E. Fuentes-Mattei, G. Velazquez-Torres, L. Phan, F. Zhang, P.-C. Chou, J.-H. Shin, H. H. Choi, J.-S. Chen, R. Zhao, J. Chen, C. Gully, C. Carlock, Y. Qi, Y. Zhang, Y. Wu, F. J. Esteva, Y. Luo, W. L. McKeehan, J. Ensor, G. N. Hortobagyi, L. Pusztai, W. Fraser Symmans, M.-H. Lee, S.-C. Yeung, Effects of obesity on transcriptomic changes and cancer hallmarks in estrogen receptor-positive breast cancer. J. Natl. Cancer Inst. 106, dju158 (2014).
40. R. Cancello, A. Zulian, D. Gentilini, M. Mencarelli, A. Della Barba, M. Maffei, P. Vitti, C. Invitti, A. Liuzzi, A. M. Di Blasio, Permanence of molecular features of obesity in subcutaneous adipose tissue of ex-obese subjects. Int. J. Obes. 37, 867-873 (2013).
41. P. Bhardwaj, B. Du, X. K. Zhou, E. Sue, M. D. Harbus, D. J. Falcone, D. Giri, C. A. Hudis, L. Kopelovich, K. Subbaramaiah, A. J. Dannenberg, Caloric restriction reverses obesity-induced mammary gland inflammation in mice. Cancer Prev. Res. 6, 282-289 (2013).
42. S. I. Grivennikov, F. R. Greten, M. Karin, Immunity, inflammation, and cancer. Cell 140, 883-899 (2010).
43. M. J. Bissell, D. C. Radisky, A. Rizki, V. M. Weaver, O. W. Petersen, The organizing principle: Microenvironmental influences in the normal and malignant breast. Differentiation 70, 537-546 (2002).
44. M. Nielsen, P. C. Pettersen, P. Alexandersen, G. Karemore, J. Raundahl, M. Loog, C. Christiansen, Breast density changes associated with postmenopausal hormone therapy: Post hoc radiologistand computer-based analyses. Menopause 17, 772-778 (2010).
45. K. M. Riching, B. L. Cox, M. R. Salick, C. Pehlke, A. S. Riching, S. M. Ponik, B. R. Bass, W. C. Crone, Y. Jiang, A. M. Weaver, K. W. Eliceiri, P. J. Keely, 3D collagen alignment limits protrusions to enhance breast cancer cell persistence. Biophys. J. 107, 2546-2558 (2014).
46. N. C. Direkze, S. J. Forbes,M. Brittan, T. Hunt, R. Jeffery, S. L. Preston, R. Poulsom, K. Hodivala-Dilke, M. R. Alison, N. A. Wright, Multiple organ engraftment by bone-marrow-derived myofibroblasts and fibroblasts in bone-marrow-Transplanted mice. Stem Cells 21, 514-520 (2003).
47. K. Y. Wolin, K. Carson, G. A. Colditz, Obesity and cancer. Oncologist 15, 556-565 (2010).
48. V. D. Longo, L. Fontana, Calorie restriction and cancer prevention: Metabolic and molecular mechanisms. Trends Pharmacol. Sci. 31, 89-98 (2010).
49. Y. Higami, J. L. Barger, G. P. Page, D. B. Allison, S. R. Smith, T. A. Prolla, R. Weindruch, Energy restriction lowers the expression of genes linked to inflammation, the cytoskeleton, the extracellular matrix, and angiogenesis in mouse adipose tissue. J. Nutr. 136, 343-352 (2006).
50. N. Halberg, T. Khan, M. E. Trujillo, I. Wernstedt-Asterholm, A. D. Attie, S. Sherwani, Z. V. Wang, S. Landskroner-Eiger, S. Dineen, U. J. Magalang, R. A. Brekken, P. E. Scherer, Hypoxiainducible factor 1a induces fibrosis and insulin resistance in white adipose tissue. Mol. Cell. Biol. 29, 4467-4483 (2009).
51. J. Peres, Understanding breast density and breast cancer risk. J. Natl. Cancer Inst. 104, 1345-1346 (2012).
52. F. Bertolini, V. Lohsiriwat, J.-Y. Petit, M. G. Kolonin, Adipose tissue cells, lipotransfer and cancer: A challenge for scientists, oncologists and surgeons. Biochim. Biophys. Acta 1826, 209-214 (2012).
53. A. C. Boquest, A. Shahdadfar, J. E. Brinchmann, P. Collas, Isolation of stromal stem cells from human adipose tissue. Methods Mol. Biol. 325, 35-46 (2006).
54. R. M. Williams, A. Flesken-Nikitin, L. H. Ellenson, D. C. Connolly, T. C. Hamilton, A. Y. Nikitin, W. R. Zipfel, Strategies for high-resolution imaging of epithelial ovarian cancer by laparoscopic nonlinear microscopy. Transl. Oncol. 3, 181-194 (2010).
55. M. L. Smith, D. Gourdon, W. C. Little, K. E. Kubow, R. A. Eguiluz, S. Luna-Morris, V. Vogel, Forceinduced unfolding of fibronectin in the extracellularmatrix of living cells. PLOS Biol. 5, e268 (2007).
56. R. Castelló-Cros, E. Cukierman, Stromagenesis during tumorigenesis: Characterization of tumor-Associated fibroblasts and stroma-derived 3D matrices. Methods Mol. Biol. 522, 275-305 (2009).
57. K. L. Johnson, Contact Mechanics (Cambridge Univ. Press, 1985).
58. D. W. Huang, B. T. Sherman, R. A. Lempicki, Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).