P190B RhoGAP Overexpression in the Developing Mammary Epithelium Induces TGFβ-dependent Fibroblast Activation

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Gillette, Melissa ^a,b   Bray, Kristi ^a,b   Blumenthaler, Alisa ^a,b   Vargo Gogola, Tracy ^a,b  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; COLLAGEN TYPE 1; FIBRONECTIN; LAMININ; MESSENGER RNA; PROTEIN LYSINE 6 OXIDASE; PROTEIN P190; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMAD2 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BREAST DEVELOPMENT; BREAST EPITHELIUM; CELL ACTIVATION; CELL ISOLATION; COCULTURE; CONTROLLED STUDY; EXTRACELLULAR MATRIX; FIBROBLAST; IMMUNOHISTOCHEMISTRY; MORPHOGENESIS; MOUSE; NONHUMAN; PARACRINE SIGNALING; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STROMA CELL; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; EPITHELIUM; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; GTPASE-ACTIVATING PROTEINS; MAMMARY GLANDS, ANIMAL; MICE; REAL-TIME POLYMERASE CHAIN REACTION; REPRESSOR PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84878064597     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065105     Document Type: Article

References (44)

1. Lu P, Takai K, Weaver VM, Werb Z, (2011) Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 3: a005058.
2. Lu P, Weaver VM, Werb Z, (2012) The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 196: 395-406.
3. Schedin P, Keely PJ, (2011) Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb Perspect Biol 3: a003228.
4. Shimoda M, Mellody KT, Orimo A, (2010) Carcinoma-associated fibroblasts are a rate-limiting determinant for tumour progression. Semin Cell Dev Biol 21: 19-25.
5. Cichon MA, Degnim AC, Visscher DW, Radisky DC, (2010) Microenvironmental influences that drive progression from benign breast disease to invasive breast cancer. J Mammary Gland Biol Neoplasia 15: 389-397.
6. Keely PJ, (2011) Mechanisms by which the extracellular matrix and integrin signaling act to regulate the switch between tumor suppression and tumor promotion. J Mammary Gland Biol Neoplasia 16: 205-219.
7. Fritz G, Just I, Kaina B, (1999) Rho GTPases are over-expressed in human tumors. Int J Cancer 81: 682-687.
8. Fritz G, Brachetti C, Bahlmann F, Schmidt M, Kaina B, (2002) Rho GTPases in human breast tumours: expression and mutation analyses and correlation with clinical parameters. Br J Cancer 87: 635-644.
9. McHenry PR, Vargo-Gogola T, (2010) Pleiotropic functions of Rho GTPase signaling: a Trojan horse or Achilles' heel for breast cancer treatment? Curr Drug Targets 11: 1043-1058.
10. Hall A, (2009) The cytoskeleton and cancer. Cancer Metastasis Rev 28: 5-14.
11. Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ, (2003) ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 163: 583-595.
12. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
13. Provenzano PP, Inman DR, Eliceiri KW, Keely PJ, (2009) Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28: 4326-4343.
14. Samuel MS, Lopez JI, McGhee EJ, Croft DR, Strachan D, et al. (2011) Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth. Cancer Cell 19: 776-791.
15. Burbelo PD, Miyamoto S, Utani A, Brill S, Yamada KM, et al. (1995) p190-B, a new member of the Rho GAP family, and Rho are induced to cluster after integrin cross-linking. J Biol Chem 270: 30919-30926.
16. Bustos RI, Forget MA, Settleman JE, Hansen SH, (2008) Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr Biol 18: 1606-1611.
17. Heckman BM, Chakravarty G, Vargo-Gogola T, Gonzales-Rimbau M, Hadsell DL, et al. (2007) Crosstalk between the p190-B RhoGAP and IGF signaling pathways is required for embryonic mammary bud development. Dev Biol 309: 137-149.
18. Vargo-Gogola T, Heckman BM, Gunther EJ, Chodosh LA, Rosen JM, (2006) P190-B Rho GTPase-activating protein overexpression disrupts ductal morphogenesis and induces hyperplastic lesions in the developing mammary gland. Mol Endocrinol 20: 1391-1405.
19. Heckman-Stoddard BM, Vargo-Gogola T, McHenry PR, Jiang V, Herrick MP, et al. (2009) Haploinsufficiency for p190B RhoGAP inhibits MMTV-Neu tumor progression. Breast Cancer Res 11(4): R61.
20. McHenry PR, Sears JC, Herrick MP, Chang P, Heckman-Stoddard BM, et al. (2010) P190B RhoGAP has pro-tumorigenic functions during MMTV-Neu mammary tumorigenesis and metastasis. Breast Cancer Res 12(5): R73.
21. Gunther EJ, Belka GK, Wertheim GB, Wang J, Hartman JL, et al. (2002) A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology. FASEB J Mar 16(3): 283-92.
22. Sternlicht MD, (2006) Key stages in mammary gland development: the cues that regulate ductal branching morphogenesis. Breast Cancer Res 8: 201.
23. Barker HE, Cox TR, Erler JT, (2012) The rationale for targeting the LOX family in cancer. Nat Rev Cancer 12: 540-552.
24. Kalluri R, Zeisberg M, (2006) Fibroblasts in cancer. Nat Rev Cancer 6: 392-401.
25. Shi-Wen X, Leask A, Abraham D, (2008) Regulation and function of connective tissue growth factor/CCN2 in tissue repair, scarring and fibrosis. Cytokine Growth Factor Rev 19: 133-144.
26. Gressner OA, Gressner AM, (2008) Connective tissue growth factor: a fibrogenic master switch in fibrotic liver diseases. Liver Int 28: 1065-1079.
27. Sakai N, Tager AM (2013) Fibrosis of two: Epithelial cell-fibroblast interactions in pulmonary fibrosis. Biochim Biophys Acta: S0925-4439(13)00075-6.
28. Derynck R, Zhang YE, (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-584.
29. Leask A, Abraham DJ, (2004) TGF-beta signaling and the fibrotic response. FASEB J 18: 816-827.
30. Nakerakanti SS, Bujor AM, Trojanowska M, (2011) CCN2 is required for the TGF-beta induced activation of Smad1-Erk1/2 signaling network. PLoS One 6: e21911.
31. Hu Y, Peng J, Feng D, Chu L, Li X, et al. (2006) Role of extracellular signal-regulated kinase, p38 kinase, and activator protein-1 in transforming growth factor-beta1-induced alpha smooth muscle actin expression in human fetal lung fibroblasts in vitro. Lung 184: 33-42.
32. Serini G, Bochaton-Piallat ML, Ropraz P, Geinoz A, Borsi L, et al. (1998) The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1. J Cell Biol 142: 873-881.
33. Ewan KB, Shyamala G, Ravani SA, Tang Y, Akhurst R, et al. (2002) Latent transforming growth factor-beta activation in mammary gland: regulation by ovarian hormones affects ductal and alveolar proliferation. Am J Pathol 160: 2081-2093.
34. Nelson CM, Vanduijn MM, Inman JL, Fletcher DA, Bissell MJ, (2006) Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science 314: 298-300.
35. Moses H, Barcellos-Hoff MH, (2011) TGF-beta biology in mammary development and breast cancer. Cold Spring Harb Perspect Biol 3: a003277.
36. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, et al. (1999) The integrin alpha v beta 6 binds and activates latent TGF beta 1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 96: 319-328.
37. Wipff PJ, Rifkin DB, Meister JJ, Hinz B, (2007) Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. J Cell Biol 179: 1311-1323.
38. Wipff PJ, Hinz B, (2008) Integrins and the activation of latent transforming growth factor beta1- an intimate relationship. Eur J Cell Biol 87: 601-615.
39. Polyak K, Kalluri R, (2010) The role of the microenvironment in mammary gland development and cancer. Cold Spring Harb Perspect Biol 2: a003244.
40. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, et al. (2008) Collagen density promotes mammary tumor initiation and progression. BMC Med 6: 11.
41. Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139: 891-906.
42. Guo F, Carter DE, (2011) Leask (2011) A Mechanical tension increases CCN2/CTGF expression and proliferation in gingival fibroblasts via a TGFbeta-dependent mechanism. PLoS One 6: e19756.
43. Hinz B, (2009) Tissue stiffness, latent TGF-beta1 activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis. Curr Rheumatol Rep 11: 120-126.
44. Cheng N, Chytil A, Shyr Y, Joly A, Moses HL, (2008) Transforming growth factor-beta signaling-deficient fibroblasts enhance hepatocyte growth factor signaling in mammary carcinoma cells to promote scattering and invasion. Mol Cancer Res 6: 1521-1533.