Tensin 2 modulates cell contractility in 3D collagen gels through the RhoGAP DLC1

Journal of Cellular Biochemistry

Volumn 109, Issue 4, 2010, Pages 808-817

  Clark, Katherine ^a   Howe, Jonathan D ^a   Pullar, Christine E ^a   Green, J Angelo ^b   Artym, Vira V ^b,c   Yamada, Kenneth M ^b   Critchley, David R ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c GEORGETOWN UNIVERSITY   (United States)

Author keywords

Collagen contraction; DLC1; Fibrillar adhesion; Fibronectin matrix assembly; RhoGAP; Tensin

Indexed keywords

COLLAGEN GEL; COMPLEMENTARY DNA; CYTOSKELETON PROTEIN; FIBRONECTIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MYOSIN ADENOSINE TRIPHOSPHATASE; RHO FACTOR; SMALL INTERFERING RNA; TENSIN; TENSIN 2; UNCLASSIFIED DRUG;

ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STRAIN HEK293; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FOCAL ADHESION; HUMAN; HUMAN CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ACTOMYOSIN; CELL ADHESION; CELLS, CULTURED; COLLAGEN; CYTOSKELETON; FIBROBLASTS; FOCAL ADHESIONS; GELS; GTPASE-ACTIVATING PROTEINS; HUMANS; MICROFILAMENT PROTEINS; MOVEMENT; PHOSPHORIC MONOESTER HYDROLASES; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 77749311395     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22460     Document Type: Article

References (46)

1. Auger KR, Songyang Z, Lo SH, Roberts TM, Chen LB. 1996. Platelet-derived growth factor-induced formation of tensin and phosphoinositide 3-kinase complexes. J Biol Chem 271:23452-23457.
2. Benzing T, Gerke P, Hopker K, Hildebrandt F, Kim E, Walz G. 2001. Nephrocystin interacts with Pyk2, p130(Cas), and tensin and triggers phosphorylation of Pyk2. Proc Natl Acad Sci USA 98:9784-9789.
3. Brancaccio M, Guazzone S, Menini N, Sibona E, Hirsch E, De Andrea M, Rocchi M, Altruda F, Tarone G, Silengo L. 1999. Melusin is a new musclespecific interactor for beta(1) integrin cytoplasmic domain. J Biol Chem 274: 29282-29288.
4. Calderwood DA, Fujioka Y, de Pereda JM, Garcia-Alvarez B, Nakamoto T, Margolis B, McGlade CJ, Liddington RC, Ginsberg MH. 2003. Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: A structural prototype for diversity in integrin signaling. Proc Natl Acad Sci USA 100:2272-2277.
5. Carver W, Molano I, Reaves TA, Borg TK, Terracio L. 1995. Role of the alpha 1 beta 1 integrin complex in collagen gel contraction in vitro by fibroblasts. J Cell Physiol 165:425-437.
6. Chan LK, Ko FC, Ng IO, Yam JW. 2009. Deleted in liver cancer 1 (DLC1) utilizes a novel binding site for Tensin2 PTB domain interaction and is required for tumor-suppressive function. PLoS ONE 4:e5572.
7. Chen H, Lo SH. 2003. Regulation of tensin-promoted cell migration by its focal adhesion binding and Src homology domain 2. Biochem J 370:1039-1045.
8. Chen H, Duncan IC, Bozorgchami H, Lo SH. 2002. Tensin1 and a previously undocumented family member, tensin2, positively regulate cell migration. Proc Natl Acad Sci USA 99:733-7338.
9. Chuang JZ, Lin DC, Lin S. 1995. Molecular cloning, expression, and mapping of the high affinity actin-capping domain of chicken cardiac tensin. J Cell Biol 128:1095-1109.
10. Cooke ME, Sakai T, Mosher DF. 2000. Contraction of collagen matrices mediated by alpha2beta1A and alpha(v)beta3 integrins. J Cell Sci 113(Pt 13): 2375-2383.
11. Cui Y, Liao YC, Lo SH. 2004. Epidermal growth factor modulates tyrosine phosphorylation of a novel tensin family member, tensin3. Mol Cancer Res 2:225-232.
12. Endo Y, Even-Ram S, Pankov R, Matsumoto K, Yamada KM. 2006. Inhibition of rho GTPases by RNA interference. Methods Enzymol 406: 345-361.
13. Feral CC, Zijlstra A, Tkachenko E, Prager G, Gardel ML, Slepak M, Ginsberg MH. 2007. CD98hc (SLC3A2) participates in fibronectin matrix assembly by mediating integrin signaling. J Cell Biol 178:701-711.
14. Green JA, Berrier AL, Pankov R, Yamada KM. 2009. beta 1 integrin cytoplasmic domain residues selectively modulate fibronectin matrix assembly and cell spreading through talin and AKT-1. J Biol Chem
15. Grinnell F. 2000. Fibroblast-collagen-matrix contraction: Growth-factor signalling and mechanical loading. Trends Cell Biol 10:362-365.
16. Grinnell F. 2003. Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 13:264-269.
17. Guo L, Wu C. 2002. Regulation of fibronectin matrix deposition and cell proliferation by the PINCH-ILK-CH-ILKBP complex. FASEB J 16:1298-1300.
18. Hall EH, Daugherty AE, Choi CK, Horwitz AF, Brautigan DL. 2009. Tensin1 requires protein phosphatase 1a in addition to RHO(GAP) DLC-1 to control cell polarization, migration and invasion. J Biol Chem 284:34713-34722.
19. Katz M, Amit I, Citri A, Shay T, Carvalho S, Lavi S, Milanezi F, Lyass L, Amariglio N, Jacob-Hirsch J, Ben-Chetrit N, Tarcic G, Lindzen M, Avraham R, Liao YC, Trusk P, Lyass A, Rechavi G, Spector NL, Lo SH, Schmitt F, Bacus SS, Yarden Y. 2007. A reciprocal tensin-3-cten switch mediates EGF-driven mammary cell migration. Nat Cell Biol 9:961-969.
20. Kawai K, Yamaga M, Iwamae Y, Kiyota M, Kamata H, Hirata H, Homma Y, Yagisawa H. 2004. A PLCdelta1-binding protein, p122RhoGAP, is localized in focal adhesions. Biochem Soc Trans 32:1107-1109.
21. Kim TY, Healy KD, Der CJ, Sciaky N, Bang YJ, Juliano RL. 2008. Effects of structure of Rho GTPase-activating protein DLC-1 on cell morphology and migration. J Biol Chem 283:32762-32770.
22. Legate KR, Fassler R. 2009. Mechanisms that regulate adaptor binding to {beta}-integrin cytoplasmic tails. J Cell Sci 122:187-198.
23. Liao YC, Lo SH. 2008. Deleted in liver cancer-1 (DLC-1): A tumor suppressor not just for liver. Int J Biochem Cell Biol 40:843-847.
24. Liao YC, Si L, deVere White RW, Lo SH. 2007. The phosphotyrosineindependent interaction of DLC-1 and the SH2 domain of cten regulates focal adhesion localization and growth suppression activity of DLC-1. J Cell Biol 176:43-49.
25. Lo SH. 2004. Tensin. Int J Biochem Cell Biol 36:31-34.
26. Lo SH, Janmey PA, Hartwig JH, Chen LB. 1994. Interactions of tensin with actin and identification of its three distinct actin-binding domains. J Cell Biol 125:1067-1075.
27. McCleverty CJ, Lin DC, Liddington RC. 2007. Structure of the PTB domain of tensin1 and a model for its recruitment to fibrillar adhesions. Protein Sci 16:1223-1229.
28. Otey CA, Vasquez GB, Burridge K, Erickson BW. 1993. Mapping of the alphaactinin binding site within the beta 1 integrin cytoplasmic domain. J Biol Chem 268:21193-21197.
29. Oxley CL, Anthis NJ, Lowe ED, Vakonakis I, Campbell ID, Wegener KL. 2008. An integrin phosphorylation switch: The effect of beta3 integrin tail phosphorylation on Dok1 and talin binding. J Biol Chem 283:5420-5426.
30. Pankov R, Cukierman E, Katz BZ, Matsumoto K, Lin DC, Lin S, Hahn C, Yamada KM. 2000. Integrin dynamics and matrix assembly: Tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J Cell Biol 148:1075-1090.
31. Qian X, Li G, Asmussen HK, Asnaghi L, Vass WC, Braverman R, Yamada KM, Popescu NC, Papageorge AG, Lowy DR. 2007. Oncogenic inhibition by a deleted in liver cancer gene requires cooperation between tensin binding and Rho-specific GTPase-activating protein activities. Proc Natl Acad Sci USA 104:9012-9017.
32. Reddy KB, Gascard P, Price MG, Negrescu EV, Fox JE. 1998. Identification of an interaction between the m-band protein skelemin and beta-integrin subunits. Colocalization of a skelemin-like protein with beta1- and beta3-integrins in non-muscle cells. J Biol Chem 273:35039-35047.
33. Saintigny G, Bernard FX, Juchaux F, Pedretti N, Mahe C. 2008. Reduced expression of the adhesion protein tensin1 in cultured human dermal fibroblasts affects collagen gel contraction. Exp Dermatol 17:788-789.
34. Salgia R, Brunkhorst B, Pisick E, Li JL, Lo SH, Chen LB, Griffin JD. 1995. Increased tyrosine phosphorylation of focal adhesion proteins in myeloid cell lines expressing p210BCR/ABL. Oncogene 11:1149-1155.
35. Shi X, Qu H, Kretzler M, Wu C. 2008. Roles of PINCH-2 in regulation of glomerular cell shape change and fibronectin matrix deposition. Am J Physiol Renal Physiol 295:F253-F263.
36. Stanchi F, Grashoff C, Nguemeni Yonga CF, Grall D, Fassler R, Van Obberghen-Schilling E. 2009. Molecular dissection of the ILK-PINCH-parvin triad reveals a fundamental role for the ILK kinase domain in the late stages of focal-adhesion maturation. J Cell Sci 122:1800-1811.
37. Szabo IL, Pai R, Jones MK, Ehring GR, Kawanaka H, Tarnawski AS. 2002. Indomethacin delays gastric restitution: Association with the inhibition of focal adhesion kinase and tensin phosphorylation and reduced actin stress fibers. Exp Biol Med (Maywood) 227:412-424.
38. Volberg T, Romer L, Zamir E, Geiger B. 2001. pp60(c-src) and related tyrosine kinases: A role in the assembly and reorganization of matrix adhesions. J Cell Sci 114:2279-2289.
39. Wavreille AS, Pei D. 2007. A chemical approach to the identification of tensin-binding proteins. ACS Chem Biol 2:109-118.
40. Wierzbicka-Patynowski I, Mao Y, Schwarzbauer JE. 2007. Continuous requirement for pp60-Src and phospho-paxillin during fibronectin matrix assembly by transformed cells. J Cell Physiol 210:750-756.
41. Wright PE, Dyson HJ. 2009. Linking folding and binding. Curr Opin Struct Biol 19:31-38.
42. Wu C, Keightley SY, Leung-Hagesteijn C, Radeva G, Coppolino M, Goicoechea S, McDonald JA, Dedhar S. 1998. Integrin-linked protein kinase regulates fibronectin matrix assembly, E-cadherin expression, and tumorigenicity. J Biol Chem 273:528-536.
43. Yam JW, Ko FC, Chan CY, Jin DY, Ng IO. 2006. Interaction of deleted in liver cancer 1 with tensin2 in caveolae and implications in tumor suppression. Cancer Res 66:8367-8372.
44. Yang XY, Guan M, Vigil D, Der CJ, Lowy DR, Popescu NC. 2009. p120Ras-GAP binds the DLC1 Rho-GAP tumor suppressor protein and inhibits its RhoA GTPase and growth-suppressing activities. Oncogene
45. Zamir E, Katz BZ, Aota S, Yamada KM, Geiger B, Kam Z. 1999. Molecular diversity of cell-matrix adhesions. J Cell Sci 112(Pt 11):1655-1669.
46. Zamir E, Katz M, Posen Y, Erez N, Yamada KM, Katz BZ, Lin S, Lin DC, Bershadsky A, Kam Z, Geiger B. 2000. Dynamics and segregation of cellmatrix adhesions in cultured fibroblasts. Nat Cell Biol 2:191-196.