RhoA is down-regulated at cell-cell contacts via p190RhoGAP-B in response to tensional homeostasis

Molecular Biology of the Cell

Volumn 24, Issue 11, 2013, Pages 1688-1699

  Ponik, Suzanne M ^a   Trier, Steven M ^a,b   Wozniak, Michele A ^c   Eliceiri, Kevin W ^a   Keely, Patricia J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b University of Pittsburgh   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATENIN; COLLAGEN GEL; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; CELL ADHESION; CELL CULTURE; DOWN REGULATION; HOMEOSTASIS; HUMAN; MORPHOGENESIS; PRIORITY JOURNAL;

CATENINS; CELL ADHESION; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL LINE; COLLAGEN; EPITHELIAL CELLS; FEMALE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GELS; GENE EXPRESSION REGULATION; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INTERCELLULAR JUNCTIONS; MAMMARY GLANDS, HUMAN; PLIABILITY; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SURFACE TENSION;

EID: 84878709987     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-05-0386     Document Type: Article

References (71)

1. Avizienyte E, Wyke AW, Jones RJ, McLean GW, Westhoff MA, Brunton VG, Frame MC (2002). Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat Cell Biol 4, 632-638.
2. Boyd NF et al. (2007). Mammographic density and the risk and detection of breast cancer. N Engl J Med 356, 227-236. (Pubitemid 46143226)
3. Boyd NF, Lockwood GA, Martin LJ, Knight JA, Byng JW, Yaffe MJ, Tritchler DL (1998). Mammographic densities and breast cancer risk. Breast Dis 10, 113-126. (Pubitemid 28470207)
4. Burbelo PD, Drechsel D, Hall A (1995a). A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biol Chem 270, 29071-29074.
5. Burbelo PD, Finegold AA, Kozak CA, Yamada Y, Takami H (1998). Cloning, genomic organization and chromosomal assignment of the mouse p190-B gene. Biochim Biophys Acta 1443, 203-210. (Pubitemid 29016025)
6. Burbelo PD, Miyamoto S, Utani A, Brill S, Yamada KM, Hall A, Yamada Y (1995b). 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. (Pubitemid 26012175)
7. Bustos RI, Forget MA, Settleman JE, Hansen SH (2008). Coordination of Rho and Rac GTPase function via p190B RhoGAP. Curr Biol 18, 1606-1611.
8. Campagnola PJ, Loew LM (2003). Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat Biotechnol 21, 1356-1360. (Pubitemid 37356622)
9. Chakravarty G, Hadsell D, Buitrago W, Settleman J, Rosen JM (2003). p190-B RhoGAP regulates mammary ductal morphogenesis. Mol Endocrinol 17, 1054-1065. (Pubitemid 36683713)
10. Chakravarty G, Roy D, Gonzales M, Gay J, Contreras A, Rosen JM (2000). P190-B, a Rho-GTPase-activating protein, is differentially expressed in terminal end buds and breast cancer. Cell Growth Differ 11, 343-354. (Pubitemid 30619562)
11. Chamberlain CE, Kraynov VS, Hahn KM (2000). Imaging spatiotemporal dynamics of Rac activation in vivo with FLAIR. Methods Enzymol 325, 389-400.
12. Choquet D, Felsenfeld DP, Sheetz MP (1997). Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48. (Pubitemid 27180329)
13. Collins TJ (2007). ImageJ for microscopy. Biotechniques 43 (1 Suppl), 25-30.
14. de Rooij J, Kerstens A, Danuser G, Schwartz MA, Waterman-Storer CM (2005). Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J Cell Biol 171, 153-164. (Pubitemid 41434610)
15. Discher DE, Janmey P, Wang YL (2005). Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139-1143. (Pubitemid 41681732)
16. Eger A, Stockinger A, Schaffhauser B, Beug H, Foisner R (2000). Epithelial mesenchymal transition by c-Fos estrogen receptor activation involves nuclear translocation of beta-catenin and upregulation of beta-catenin/lymphoid enhancer binding factor-1 transcriptional activity. J Cell Biol 148, 173-188.
17. Gehler S, Baldassarre M, Lad Y, Leight JL, Wozniak MA, Riching KM, Eliceiri KW, Weaver VM, Calderwood DA, Keely PJ (2009). Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. Mol Biol Cell 20, 3224-3238.
18. Giannone G, Sheetz MP (2006). Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 16, 213-223.
19. Guo YP, Martin LJ, Hanna W, Banerjee D, Miller N, Fishell E, Khokha R, Boyd NF (2001). Growth factors and stromal matrix proteins associated with mammographic densities. Cancer Epidemiol Biomarkers Prev 10, 243-248. (Pubitemid 34288536)
20. Heasman SJ, Ridley AJ (2008). Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9, 690-701.
21. Heck JN, Ponik SM, Garcia-Mendoza MG, Pehlke CA, Inman DR, Eliceiri KW, Keely PJ (2012). Microtubules regulate GEF-H1 in response to extracellular matrix stiffness. Mol Biol Cell 23, 2583-2592.
22. Heckman-Stoddard BM, Vargo-Gogola T, McHenry PR, Jiang V, Herrick MP, Hilsenbeck SG, Settleman J, Rosen JM (2009). Haploinsufficiency for p190B RhoGAP inhibits MMTV-Neu tumor progression. Breast Cancer Res 11, R61.
23. Husmark J, Heldin NE, Nilsson M (1999). N-cadherin-mediated adhesion and aberrant catenin expression in anaplastic thyroid-carcinoma cell lines. Int J Cancer 83, 692-699. (Pubitemid 29508052)
24. Jiang W, Sordella R, Chen GC, Hakre S, Roy AL, Settleman J (2005). An FF domain-dependent protein interaction mediates a signaling pathway for growth factor-induced gene expression. Mol Cell 17, 23-35. (Pubitemid 40075362)
25. Kardash E, Reichman-Fried M, Maitre JL, Boldajipour B, Papusheva E, Messerschmidt EM, Heisenberg CP, Raz E (2010). A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nat Cell Biol 12, 47-53.
26. Keely PJ, Conklin MW, Gehler S, Ponik SM, Provenzano PP (2007). Investigating integrin regulation and signaling events in three-dimensional systems. Methods Enzymol 426, 27-45.
27. Keely PJ, Fong AM, Zutter MM, Santoro SA (1995). Alteration of collagen-dependent adhesion, motility, and morphogenesis by the expression of antisense alpha 2 integrin mRNA in mammary cells. J Cell Sci 108, 595-607.
28. Kurley SJ, Bierie B, Carnahan RH, Lobdell NA, Davis MA, Hofmann I, Moses HL, Muller WJ, Reynolds AB (2012). p120-catenin is essential for terminal end bud function and mammary morphogenesis. Development 139, 1754-1764.
29. Kurokawa K, Matsuda M (2005). Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol Biol Cell 16, 4294-4303. (Pubitemid 41262897)
30. Lakowicz JR (1999). Principles of Fluorescence Spectroscopy, New York: Plenum.
31. Ludwig K, Parsons SJ (2011). The tumor suppressor, p190RhoGAP, differentially initiates apoptosis and confers docetaxel sensitivity to breast cancer cells. Genes Cancer 2, 20-30.
32. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, Abell A, Johnson GL, Hahn KM, Danuser G (2009). Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99-103.
33. Malliri A, Collard JG (2003). Role of Rho-family proteins in cell adhesion and cancer. Curr Opin Cell Biol 15, 583-589. (Pubitemid 37176967)
34. Matheson SF, Hu KQ, Brouns MR, Sordella R, VanderHeide JD, Settleman J (2006). Distinct but overlapping functions for the closely related p190 RhoGAPs in neural development. Dev Neurosci 28, 538-550. (Pubitemid 44532982)
35. McGlade J, Brunkhorst B, Anderson D, Mbamalu G, Settleman J, Dedhar S, Rozakis-Adcock M, Chen LB, Pawson T (1993). The N-terminal region of GAP regulates cytoskeletal structure and cell adhesion. EMBO J 12, 3073-3081. (Pubitemid 23232738)
36. McHenry et al. (2010). P190B RhoGAP has pro-tumorigenic functions during MMTV-Neu mammary tumorigenesis and metastasis. Breast Cancer Res 12, R73.
37. Nalbant P, Hodgson L, Kraynov V, Toutchkine A, Hahn KM (2004). Activation of endogenous Cdc42 visualized in living cells. Science 305, 1615-1619. (Pubitemid 39296355)
38. Numaguchi K, Eguchi S, Yamakawa T, Motley ED, Inagami T (1999). Mechanotransduction of rat aortic vascular smooth muscle cells requires RhoA and intact actin filaments. Circ Res 85, 5-11. (Pubitemid 29321036)
39. Ohkubo T, Ozawa M (2004). The transcription factor Snail downregulates the tight junction components independently of E-cadherin downregulation. J Cell Sci 117, 1675-1685. (Pubitemid 38559300)
40. Omelchenko T, Hall A (2012). Myosin-IXA regulates collective epithelial cell migration by targeting RhoGAP activity to cell-cell junctions. Curr Biol 22, 278-288.
41. Parsons M et al. (2005). Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells. Mol Cell Biol 25, 1680-1695. (Pubitemid 40280137)
42. Paszek MJ, Weaver VM (2004). The tension mounts: mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 9, 325-342. (Pubitemid 41149140)
43. Paszek MJ et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254. (Pubitemid 41317594)
44. Pavalko FM, Chen NX, Turner CH, Burr DB, Atkinson S, Hsieh YF, Qiu J, Duncan RL (1998). Fluid shear-induced mechanical signaling in MC3T3-E1 osteoblasts requires cytoskeleton-integrin interactions. Am J Physiol 275, C1591-C1601.
45. Pertz O (2010). Spatio-temporal Rho GTPase signaling-where are we now? J Cell Sci 123, 1841-1850.
46. Pertz O, Hodgson L, Klemke RL, Hahn KM (2006). Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072.
47. Provenzano PP, Eliceiri KW, Yan L, Ada-Nguema A, Conklin MW, Inman DR, Keely PJ (2008a). Nonlinear optical imaging of cellular processes in breast cancer. Microsc Microanal 14, 532-548.
48. 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.
49. Provenzano PP, Inman DR, Eliceiri KW, Trier SM, Keely PJ (2008b). Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys J 95, 5374-5384.
50. Ridley AJ, Self AJ, Kasmi F, Paterson HF, Hall A, Marshall CJ, Ellis C (1993). Rho family GTPase activating proteins p190, BCR and RhoGAP show distinct specificities in vitro and in vivo. EMBO J 12, 5151-5160. (Pubitemid 23358505)
51. Roeder BA, Kokini K, Sturgis JE, Robinson JP, Voytik-Harbin SL (2002). Tensile mechanical properties of three-dimensional type I collagen extracellular matrices with varied microstructure. J Biomech Eng 124, 214-222. (Pubitemid 34407065)
52. Roof RW, Dukes BD, Chang JH, Parsons SJ (2000). Phosphorylation of the p190 RhoGAP N-terminal domain by c-Src results in a loss of GTP binding activity. FEBS Lett 472, 117-121. (Pubitemid 30224598)
53. Roof RW, Haskell MD, Dukes BD, Sherman N, Kinter M, Parsons SJ (1998). Phosphotyrosine (p-Tyr)-dependent and -independent mechanisms of p190 RhoGAP-p120 RasGAP interaction: Tyr 1105 of p190, a substrate for c-Src, is the sole p-Tyr mediator of complex formation. Mol Cell Biol 18, 7052-7063. (Pubitemid 28533025)
54. Sahai E, Marshall CJ (2003). Differing modes of tumour cell invasion have distinct requirements for Rho/ROCK signalling and extracellular proteolysis. Nat Cell Biol 5, 711-719. (Pubitemid 36986778)
55. Settleman J, Albright CF, Foster LC, Weinberg RA (1992a). Association between GTPase activators for Rho and Ras families. Nature 359, 153-154.
56. Settleman J, Narasimhan V, Foster LC, Weinberg RA (1992b). Molecular cloning of cDNAs encoding the GAP-associated protein p190: implications for a signaling pathway from ras to the nucleus. Cell 69, 539-549.
57. Su L, Pertz O, Mikawa M, Hahn K, Parsons SJ (2009). p190RhoGAP negatively regulates Rho activity at the cleavage furrow of mitotic cells. Exp Cell Res 315, 1347-1359.
58. Tadross MR, Veeramani BPS, Yue DT (2009). Robust approaches to quantitative ratiometric FRET imaging of CFP/YFP fluorophores under confocal microscopy. J Microsc 233, 192-204.
59. Tang Y, Olufemi L, Wang MT, Nie D (2008). Role of Rho GTPases in breast cancer. Front Biosci 13, 759-776. (Pubitemid 351599780)
60. Timpson P et al. (2011). Spatial regulation of RhoA activity during pancreatic cancer cell invasion driven by mutant p53. Cancer Res 71, 747-757.
61. Tran NL, Nagle RB, Cress AE, Heimark RL (1999). N-cadherin expression in human prostate carcinoma cell lines. An epithelial-mesenchymal transformation mediating adhesion with stromal cells. Am J Pathol 155, 787-798. (Pubitemid 29426824)
62. Vandewalle C, Comijn J, De Craene B, Vermassen P, Bruyneel E, Andersen H, Tulchinsky E, Van Roy F, Berx G (2005). SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res 33, 6566-6578. (Pubitemid 41806421)
63. 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. (Pubitemid 43801239)
64. White JG (1987). An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy. J Cell Biol 105, 41-48.
65. Wildenberg GA, Dohn MR, Carnahan RH, Davis MA, Lobdell NA, Settleman J, Reynolds AB (2006). p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 127, 1027-1039. (Pubitemid 44792253)
66. Wokosin DL, Squirrell JM, Eliceiri KW, White JG (2003). Optical workstation with concurrent, independent multiphoton imaging and experimental laser microbeam capabilities. Rev Sci Instrum 74, 193-201.
67. 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. (Pubitemid 37429871)
68. Wozniak MA, Keely PJ (2005). Use of three-dimensional collagen gels to study mechanotransduction in T47D breast epithelial cells. Biol Proced Online 7, 144-161. (Pubitemid 41574308)
69. Yanagisawa M, Anastasiadis PZ (2006). p120 catenin is essential for mesenchymal cadherin-mediated regulation of cell motility and invasiveness. J Cell Biol 174, 1087-1096. (Pubitemid 44455195)
70. Yanagisawa M, Huveldt D, Kreinest P, Lohse CM, Cheville JC, Parker AS, Copland JA, Anastasiadis PZ (2008). A p120 catenin isoform switch affects Rho activity, induces tumor cell invasion, and predicts metastatic disease. J Biol Chem 283, 18344-18354.
71. Yoshizaki H, Ohba Y, Kurokawa K, Itoh RE, Nakamura T, Mochizuki N, Nagashima K, Matsuda M (2003). Activity of Rho-family GTPases during cell division as visualized with FRET-based probes. J Cell Biol 162, 223-232. (Pubitemid 36928836)