AMPK negatively regulates tensin-dependent integrin activity

Journal of Cell Biology

Volumn 216, Issue 4, 2017, Pages 1107-1121

  Georgiadou, Maria ^a   Lilja, Johanna ^a   Jacquemet, Guillaume ^a   Guzmán, Camilo ^a   Rafaeva, Maria ^a   Alibert, Charlotte ^b,c   Yan, Yan ^d   Sahgal, Pranshu ^a   Lerche, Martina ^a   Manneville, Jean Baptiste ^b,c   Mäkelä, Tomi P ^d   Ivaska, Johanna ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b INSTITUT CURIE   (France)

^c CNRS   (France)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; FIBRONECTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; TENSIN; TENSIN 1; TENSIN 3; UNCLASSIFIED DRUG; ACTIN BINDING PROTEIN; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SPREADING; CONTROLLED STUDY; FEMALE; FIBROBLAST; GENE SILENCING; MECHANICAL STRESS; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; TRANSIENT EXPRESSION; CELL LINE; HEK293 CELL LINE; HUMAN; METABOLISM; PHYSIOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANTIGENS, CD29; CELL ADHESION; CELL LINE; FIBROBLASTS; FIBRONECTINS; HEK293 CELLS; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MICROFILAMENT PROTEINS; PROTEIN BINDING; TENSINS;

EID: 85020268113     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201609066     Document Type: Article

References (65)

1. Alanko, J., A. Mai, G. Jacquemet, K. Schauer, R. Kaukonen, M. Saari, B. Goud, and J. Ivaska. 2015. Integrin endosomal signalling suppresses anoikis. Nat. Cell Biol. 17:1412-1421. http://dx.doi.org/10.1038/ncb3250
2. Askari, J.A., C.J. Tynan, S.E. Webb, M.L. Martin-Fernandez, C. Ballestrem, and M.J. Humphries. 2010. Focal adhesions are sites of integrin extension. J. Cell Biol. 188:891-903. http://dx.doi.org/10.1083/jcb.200907174
3. Azioune, A., M. Storch, M. Bornens, M. Théry, and M. Piel. 2009. Simple and rapid process for single cell micro-patterning. Lab Chip. 9:1640-1642. http://dx.doi.org/10.1039/b821581m
4. Baker, E.L., R.T. Bonnecaze, and M.H. Zaman. 2009. Extracellular matrix stiffness and architecture govern intracellular rheology in cancer. Biophys. J. 97:1013-1021. http://dx.doi.org/10.1016/j.bpj.2009.05.054
5. Banko, M.R., J.J. Allen, B.E. Schaffer, E.W. Wilker, P. Tsou, J.L. White, J. Villén, B. Wang, S.R. Kim, K. Sakamoto, et al. 2011. Chemical genetic screen for AMPKa2 substrates uncovers a network of proteins involved in mitosis. Mol. Cell. 44:878-892. http://dx.doi.org/10.1016/j.molcel.2011.11.005
6. Bausch, A.R., W. Möller, and E. Sackmann. 1999. Measurement of local viscoelasticity and forces in living cells by magnetic tweezers. Biophys. J. 76:573-579. http://dx.doi.org/10.1016/S0006-3495(99)77225-5
7. Beauloye, C., L. Bertrand, S. Horman, and L. Hue. 2011. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc. Res. 90:224-233. http://dx.doi.org/10.1093/cvr/cvr034
8. Betz, T., D. Koch, Y.B. Lu, K. Franze, and J.A. Käs. 2011. Growth cones as soft and weak force generators. Proc. Natl. Acad. Sci. USA. 108:13420-13425. http://dx.doi.org/10.1073/pnas.1106145108
9. Bouvard, D., J. Pouwels, N. De Franceschi, and J. Ivaska. 2013. Integrin inactivators: balancing cellular functions in vitro and in vivo. Nat. Rev. Mol. Cell Biol. 14:430-442. http://dx.doi.org/10.1038/nrm3599
10. Butler, J.P., I.M. Tolic-Nørrelykke, B. Fabry, and J.J. Fredberg. 2002. Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282:C595-C605. http://dx.doi.org/10.1152/ajpcell.00270.2001
11. Byron, A., J.D. Humphries, J.A. Askari, S.E. Craig, A.P. Mould, and M.J. Humphries. 2009. Anti-integrin monoclonal antibodies. J. Cell Sci. 122:4009-4011. http://dx.doi.org/10.1242/jcs.056770
12. Byron, A., J.A. Askari, J.D. Humphries, G. Jacquemet, E.J. Koper, S. Warwood, C.K. Choi, M.J. Stroud, C.S. Chen, D. Knight, and M.J. Humphries. 2015. A proteomic approach reveals integrin activation state-dependent control of microtubule cortical targeting. Nat. Commun. 6:6135. http://dx.doi.org/10.1038/ncomms7135
13. Calderwood, D.A., I.D. Campbell, and D.R. Critchley. 2013. Talins and kindlins: partners in integrin-mediated adhesion. Nat. Rev. Mol. Cell Biol. 14:503-517. http://dx.doi.org/10.1038/nrm3624
14. Chan, C.J., A.E. Ekpenyong, S. Golfier, W. Li, K.J. Chalut, O. Otto, J. Elgeti, J. Guck, and F. Lautenschläger. 2015. Myosin II activity softens cells in suspension. Biophys. J. 108:1856-1869. http://dx.doi.org/10.1016/j.bpj.2015.03.009
15. Chen, K.H., H.H. Hsu, C.C. Lee, T.H. Yen, Y.C. Ko, C.W. Yang, and C.C. Hung. 2014. The AMPK agonist AIC AR inhibits TGF-β1 induced activation of kidney myofibroblasts. PLoS One. 9:e106554. http://dx.doi.org/10.1371/journal.pone.0106554
16. Chen, P.I., K. Schauer, C. Kong, A.R. Harding, B. Goud, and P.D. Stahl. 2014. Rab5 isoforms orchestrate a "division of labor" in the endocytic network; Rab5C modulates Rac-mediated cell motility. PLoS One. 9:e90384. http://dx.doi.org/10.1371/journal.pone.0090384
17. 1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. J. Cell Sci. 118:291-300. http://dx.doi.org/10.1242/jcs.01623
18. Clark, K., J.D. Howe, C.E. Pullar, J.A. Green, V.V. Artym, K.M. Yamada, and D.R. Critchley. 2010. Tensin 2 modulates cell contractility in 3D collagen gels through the RhoGAP DLC1. J. Cell. Biochem. 109:808-817
19. Faubert, B., G. Boily, S. Izreig, T. Griss, B. Samborska, Z. Dong, F. Dupuy, C. Chambers, B.J. Fuerth, B. Viollet, et al. 2013. AMPK is a negative regulator of the Warburg effect and suppresses tumor growth in vivo. Cell Metab. 17:113-124. http://dx.doi.org/10.1016/j.cmet.2012.12.001
20. Geiger, B., and K.M. Yamada. 2011. Molecular architecture and function of matrix adhesions. Cold Spring Harb. Perspect. Biol. 3:a005033. http://dx.doi.org/10.1101/cshperspect.a005033
21. Geiger, B., A. Bershadsky, R. Pankov, and K.M. Yamada. 2001. Transmembrane crosstalk between the extracellular matrix and the cytoskeleton crosstalk. Nat. Rev. Mol. Cell Biol. 2:793-805. http://dx.doi.org/10.1038/35099066
22. Gudzenko, T., and C.M. Franz. 2015. Studying early stages of fibronectin fibrillogenesis in living cells by atomic force microscopy. Mol. Biol. Cell. 26:3190-3204. http://dx.doi.org/10.1091/mbc.E14-05-1026
23. Guet, D., K. Mandal, M. Pinot, J. Hoffmann, Y. Abidine, W. Sigaut, S. Bardin, K. Schauer, B. Goud, and J.B. Manneville. 2014. Mechanical role of actin dynamics in the rheology of the Golgi complex and in Golgi-associated trafficking events. Curr. Biol. 24:1700-1711. http://dx.doi.org/10.1016/j.cub.2014.06.048
24. Hardie, D.G. 2013. AMPK: a target for drugs and natural products with effects on both diabetes and cancer. Diabetes. 62:2164-2172. http://dx.doi.org/10.2337/db13-0368
25. Hardie, D.G., F.A. Ross, and S.A. Hawley. 2012. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13:251-262. http://dx.doi.org/10.1038/nrm3311
26. Horton, E.R., A. Byron, J.A. Askari, D.H. Ng, A. Millon-Frémillon, J. Robertson, E.J. Koper, N.R. Paul, S. Warwood, D. Knight, et al. 2015. Definition of a consensus integrin adhesome and its dynamics during adhesion complex assembly and disassembly. Nat. Cell Biol. 17:1577-1587. http://dx.doi.org/10.1038/ncb3257
27. Horton, E.R., P. Astudillo, M.J. Humphries, and J.D. Humphries. 2016. Mechanosensitivity of integrin adhesion complexes: role of the consensus adhesome. Exp. Cell Res. 343:7-13. http://dx.doi.org/10.1016/j.yexcr.2015.10.025
28. Hughes, P.E., B. Oertli, M. Hansen, F.L. Chou, B.M. Willumsen, and M.H. Ginsberg. 2002. Suppression of integrin activation by activated Ras or Raf does not correlate with bulk activation of ERK MAP kinase. Mol. Biol. Cell. 13:2256-2265. http://dx.doi.org/10.1091/mbc.01-10-0480
29. Humphrey, J.D., E.R. Dufresne, and M.A. Schwartz. 2014. Mechanotransduction and extracellular matrix homeostasis. Nat. Rev. Mol. Cell Biol. 15:802-812. http://dx.doi.org/10.1038/nrm3896
30. Hynes, R.O. 2002. Integrins: bidirectional, allosteric signaling machines. Cell. 110:673-687. http://dx.doi.org/10.1016/S0092-8674(02)00971-6
31. 1 recycling suppresses Rac and promotes RhoA activity via the RacGAP1-IQG AP1 complex. J. Cell Biol. 202:917-935. http://dx.doi.org/10.1083/jcb.201302041
32. Kim, C., F. Ye, and M.H. Ginsberg. 2011. Regulation of integrin activation. Annu. Rev. Cell Dev. Biol. 27:321-345. http://dx.doi.org/10.1146/annurev-cellbio-100109-104104
33. Lee, J.H., H. Koh, M. Kim, Y. Kim, S.Y. Lee, R.E. Karess, S.H. Lee, M. Shong, J.M. Kim, J. Kim, and J. Chung. 2007. Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature. 447:1017-1020. http://dx.doi.org/10.1038/nature05828
34. Lemmon, C.A., C.S. Chen, and L.H. Romer. 2009. Cell traction forces direct fibronectin matrix assembly. Biophys. J. 96:729-738. http://dx.doi.org/10.1016/j.bpj.2008.10.009
35. Lemons, J.M., X.J. Feng, B.D. Bennett, A. Legesse-Miller, E.L. Johnson, I. Raitman, E.A. Pollina, H.A. Rabitz, J.D. Rabinowitz, and H.A. Coller. 2010. Quiescent fibroblasts exhibit high metabolic activity. PLoS Biol. 8:e1000514. http://dx.doi.org/10.1371/journal.pbio.1000514
36. Lim, J.Y., M.A. Oh, W.H. Kim, H.Y. Sohn, and S.I. Park. 2012. AMP-activated protein kinase inhibits TGF-β-induced fibrogenic responses of hepatic stellate cells by targeting transcriptional coactivator p300. J. Cell. Physiol. 227:1081-1089. http://dx.doi.org/10.1002/jcp.22824
37. Lin, G.L., D.M. Cohen, R.A. Desai, M.T. Breckenridge, L. Gao, M.J. Humphries, and C.S. Chen. 2013. Activation of beta 1 but not beta 3 integrin increases cell traction forces. FEBS Lett. 587:763-769. http://dx.doi.org/10.1016/j.febslet.2013.01.068
38. Liu, J., W. Liu, H. Ying, W. Zhao, and H. Zhang. 2013. Analysis of microRNA expression profile induced by AIC AR in mouse hepatocytes. Gene. 512:364-372. http://dx.doi.org/10.1016/j.gene.2012.09.118
39. Lo, S.H., Q. An, S. Bao, W.K. Wong, Y. Liu, P.A. Janmey, J.H. Hartwig, and L.B. Chen. 1994. Molecular cloning of chick cardiac muscle tensin. Full-length cDNA sequence, expression, and characterization. J. Biol. Chem. 269:22310-22319
40. Lo, S.H., P.A. Janmey, J.H. Hartwig, and L.B. Chen. 1994. Interactions of tensin with actin and identification of its three distinct actin-binding domains. J. Cell Biol. 125:1067-1075. http://dx.doi.org/10.1083/jcb.125.5.1067
41. Mandal, K., A. Asnacios, B. Goud, and J.B. Manneville. 2016. Mapping intracellular mechanics on micropatterned substrates. Proc. Natl. Acad. Sci. USA. 113:E7159-E7168. http://dx.doi.org/10.1073/pnas.1605112113
42. McCleverty, C.J., D.C. Lin, and R.C. Liddington. 2007. Structure of the PTB domain of tensin1 and a model for its recruitment to fibrillar adhesions. Protein Sci. 16:1223-1229. https://doi.org/10.1110/ps.072798707
43. Mihaylova, M.M., and R.J. Shaw. 2011. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat. Cell Biol. 13:1016-1023. http://dx.doi.org/10.1038/ncb2329
44. Mirouse, V., and M. Billaud. 2011. The LKB1/AMPK polarity pathway. FEBS Lett. 585:981-985. http://dx.doi.org/10.1016/j.febslet.2010.12.025
45. Nakano, A., H. Kato, T. Watanabe, K.D. Min, S. Yamazaki, Y. Asano, O. Seguchi, S. Higo, Y. Shintani, H. Asanuma, et al. 2010. AMPK controls the speed of microtubule polymerization and directional cell migration through CLIP-170 phosphorylation. Nat. Cell Biol. 12:583-590. http://dx.doi.org/10.1038/ncb2060
46. Nevo, J., A. Mai, S. Tuomi, T. Pellinen, O.T. Pentikäinen, P. Heikkilä, J. Lundin, H. Joensuu, P. Bono, and J. Ivaska. 2010. Mammary-derived growth inhibitor (MDGI) interacts with integrin a-subunits and suppresses integrin activity and invasion. Oncogene. 29:6452-6463. http://dx.doi.org/10.1038/onc.2010.376
47. 1 integrins promotes early fibronectin fibrillogenesis. J. Cell Biol. 148:1075-1090. http://dx.doi.org/10.1083/jcb.148.5.1075
48. Pellinen, T., J.K. Rantala, A. Arjonen, J.P. Mpindi, O. Kallioniemi, and J. Ivaska. 2012. A functional genetic screen reveals new regulators of β1-integrin activity. J. Cell Sci. 125:649-661. http://dx.doi.org/10.1242/jcs.090704
49. Pelouch, V., I.M. Dixon, L. Golfman, R.E. Beamish, and N.S. Dhalla. 1993. Role of extracellular matrix proteins in heart function. Mol. Cell. Biochem. 129:101-120. http://dx.doi.org/10.1007/BF00926359
50. Pylayeva, Y., and F.G. Giancotti. 2007. Tensin relief facilitates migration. Nat. Cell Biol. 9:877-879. http://dx.doi.org/10.1038/ncb0807-877
51. Rainero, E., J.D. Howe, P.T. Caswell, N.B. Jamieson, K. Anderson, D.R. Critchley, L. Machesky, and J.C. Norman. 2015. Ligand-occupied integrin internalization links nutrient signaling to invasive migration. Cell Reports. 10:398-413
52. Rantala, J.K., J. Pouwels, T. Pellinen, S. Veltel, P. Laasola, E. Mattila, C.S. Potter, T. Duffy, J.P. Sundberg, O. Kallioniemi, et al. 2011. SHA RPIN is an endogenous inhibitor of β1-integrin activation. Nat. Cell Biol. 13:1315-1324. http://dx.doi.org/10.1038/ncb2340
53. Robertson, J., G. Jacquemet, A. Byron, M.C. Jones, S. Warwood, J.N. Selley, D. Knight, J.D. Humphries, and M.J. Humphries. 2015. Defining the phospho-adhesome through the phosphoproteomic analysis of integrin signalling. Nat. Commun. 6:6265. http://dx.doi.org/10.1038/ncomms7265
54. Satriano, J., K. Sharma, R.C. Blantz, and A. Deng. 2013. Induction of AMPK activity corrects early pathophysiological alterations in the subtotal nephrectomy model of chronic kidney disease. Am. J. Physiol. Renal Physiol. 305:F727-F733. http://dx.doi.org/10.1152/ajprenal.00293.2013
55. Schaffer, B.E., R.S. Levin, N.T. Hertz, T.J. Maures, M.L. Schoof, P.E. Hollstein, B.A. Benayoun, M.R. Banko, R.J. Shaw, K.M. Shokat, and A. Brunet. 2015. Identification of AMPK phosphorylation sites reveals a network of proteins involved in cell invasion and facilitates large-scale substrate prediction. Cell Metab. 22:907-921. http://dx.doi.org/10.1016/j.cmet.2015.09.009
56. Schiller, H.B., M.R. Hermann, J. Polleux, T. Vignaud, S. Zanivan, C.C. Friedel, Z. Sun, A. Raducanu, K.E. Gottschalk, M. Théry, et al. 2013. β1-and av-class integrins cooperate to regulate myosin II during rigidity sensing of fibronectin-based microenvironments. Nat. Cell Biol. 15:625-636. http://dx.doi.org/10.1038/ncb2747
57. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, et al. 2012. Fiji: an opensource platform for biological-image analysis. Nat. Methods. 9:676-682. http://dx.doi.org/10.1038/nmeth.2019
58. Schwarz, U.S., and M.L. Gardel. 2012. United we stand: integrating the actin cytoskeleton and cell-matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125:3051-3060. http://dx.doi.org/10.1242/jcs.093716
59. Suh, E.J., M.Y. Remillard, A. Legesse-Miller, E.L. Johnson, J.M. Lemons, T.R. Chapman, J.J. Forman, M. Kojima, E.S. Silberman, and H.A. Coller. 2012. A microRNA network regulates proliferative timing and extracellular matrix synthesis during cellular quiescence in fibroblasts. Genome Biol. 13:R121. http://dx.doi.org/10.1186/gb-2012-13-12-r121
60. Tadokoro, S., S.J. Shattil, K. Eto, V. Tai, R.C. Liddington, J.M. de Pereda, M.H. Ginsberg, and D.A. Calderwood. 2003. Talin binding to integrin β tails: a final common step in integrin activation. Science. 302:103-106. http://dx.doi.org/10.1126/science.1086652
61. Theodosiou, M., M. Widmaier, R.T. Böttcher, E. Rognoni, M. Veelders, M. Bharadwaj, A. Lambacher, K. Austen, D.J. Müller, R. Zent, and R. Fässler. 2016. Kindlin-2 cooperates with talin to activate integrins and induces cell spreading by directly binding paxillin. eLife. 5:e10130. http://dx.doi.org/10.7554/eLife.10130
62. Wang, S., C. Zhang, M. Zhang, B. Liang, H. Zhu, J. Lee, B. Viollet, L. Xia, Y. Zhang, and M.H. Zou. 2012. Activation of AMP-activated protein kinase a2 by nicotine instigates formation of abdominal aortic aneurysms in mice in vivo. Nat. Med. 18:902-910. http://dx.doi.org/10.1038/nm.2711
63. Yan, Y., S. Ollila, I.P. Wong, T. Vallenius, J.J. Palvimo, K. Vaahtomeri, and T.P. Mäkelä. 2015. SUMOylation of AMPKa1 by PIAS4 specifically regulates mTORC1 signalling. Nat. Commun. 6:8979. http://dx.doi.org/10.1038/ncomms9979
64. Zamir, E., M. Katz, Y. Posen, N. Erez, K.M. Yamada, B.Z. Katz, S. Lin, D.C. Lin, A. Bershadsky, Z. Kam, and B. Geiger. 2000. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2:191-196
65. Zhang, L., J. Li, L.H. Young, and M.J. Caplan. 2006. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc. Natl. Acad. Sci. USA. 103:17272-17277. http://dx.doi.org/10.1073/pnas.0608531103