Probing the GTPase cycle with real-time NMR: GAP and GEF activities in cell extracts

Methods

Volumn 57, Issue 4, 2012, Pages 473-485

  Marshall, Christopher B ^a,b   Meiri, David ^a   Smith, Matthew J ^a,b   Mazhab Jafari, Mohammad T ^a,b   Gasmi Seabrook, Geneviève M C ^a,b   Rottapel, Robert ^a,b,c,d   Stambolic, Vuk ^a,b   Ikura, Mitsuhiko ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

GTPase activating proteins (GAPs); Guanine nucleotide exchange factors (GEFs); Lfc GEF H1; Real time NMR; Small GTPase cycle; Tuberous sclerosis complex (TSC)

Indexed keywords

CELL EXTRACT; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PDZ PROTEIN; RAS PROTEIN; RHEB PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

CELL CULTURE; CELL FUNCTION; CELL LYSATE; CELL TYPE; CYTOLYSIS; DATA PROCESSING; DNA TRANSFECTION; ENZYME ASSAY; GENETIC TRANSFECTION; HUMAN; HYDROLYSIS; MAMMAL CELL; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STANDARDIZATION;

ANIMALS; CELL EXTRACTS; DYNEINS; ENZYME ASSAYS; FLUORESCENT DYES; GTP PHOSPHOHYDROLASES; GTPASE-ACTIVATING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; GUANOSINE TRIPHOSPHATE; HEK293 CELLS; HUMANS; HYDROLYSIS; MAGNETIC RESONANCE SPECTROSCOPY; MONOMERIC GTP-BINDING PROTEINS; NEUROPEPTIDES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

MAMMALIA;

EID: 84866354687     PISSN: 10462023     EISSN: 10959130     Source Type: Journal    
DOI: 10.1016/j.ymeth.2012.06.014     Document Type: Review

References (117)

1. Wennerberg K., Rossman K.L., Der C.J. J. Cell Sci. 2005, 118:843-846.
2. Rojas A.M., Fuentes G., Rausell A., Valencia A. J. Cell Biol. 2012, 196:189-201.
3. Ahmadian M.R., Wiesmuller L., Lautwein A., Bischoff F.R., Wittinghofer A. J. Biol. Chem. 1996, 271:16409-16415.
4. Rubio I., Pusch R., Wetzker R. J. Biochem. Biophys. Methods 2004, 58:111-117.
5. Self A.J., Hall A. Methods Enzymol. 1995, 256:67-76.
6. Neal S.E., Eccleston J.F., Webb M.R. Proc. Natl. Acad. Sci. USA 1990, 87:3562-3565.
7. Derewenda U., Oleksy A., Stevenson A.S., Korczynska J., Dauter Z., Somlyo A.P., Otlewski J., Somlyo A.V., Derewenda Z.S. Structure 2004, 12:1955-1965.
8. Oleksy A., Barton H., Devedjiev Y., Purdy M., Derewenda U., Otlewski J., Derewenda Z.S. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:740-742.
9. Hutchinson J.P., Eccleston J.F. Biochemistry 2000, 39:11348-11359.
10. Tan Y.C., Wu H., Wang W.N., Zheng Y., Wang Z.X. Anal. Biochem. 2002, 310:156-162.
11. Hemsath L., Ahmadian M.R. Methods 2005, 37:173-182.
12. Eberth A., Dvorsky R., Becker C.F., Beste A., Goody R.S., Ahmadian M.R. Biol. Chem. 2005, 386:1105-1114.
13. Mazhab-Jafari M.T., Marshall C.B., Smith M., Gasmi-Seabrook G.M., Stambolic V., Rottapel R., Neel B.G., Ikura M. J. Biol. Chem. 2010, 285:5132-5136.
14. Nixon A.E., Brune M., Lowe P.N., Webb M.R. Biochemistry 1995, 34:15592-15598.
15. Kunzelmann S., Webb M.R. Biochem. J. 2011, 440:43-49.
16. Bos J.L., Rehmann H., Wittinghofer A. Cell 2007, 129:865-877.
17. Downward J., Graves J.D., Warne P.H., Rayter S., Cantrell D.A. Nature 1990, 346:719-723.
18. Gibbs J.B., Marshall M.S., Scolnick E.M., Dixon R.A., Vogel U.S. J. Biol. Chem. 1990, 265:20437-20442.
19. Yamagata K., Sanders L.K., Kaufmann W.E., Yee W., Barnes C.A., Nathans D., Worley P.F. J. Biol. Chem. 1994, 269:16333-16339.
20. Li Y., Inoki K., Guan K.L. Mol. Cell. Biol. 2004, 24:7965-7975.
21. Li Y., Inoki K., Vikis H., Guan K.L. Methods Enzymol. 2006, 407:46-54.
22. Zhang Y., Gao X., Saucedo L.J., Ru B., Edgar B.A., Pan D. Nat. Cell Biol. 2003, 5:578-581.
23. Tee A.R., Manning B.D., Roux P.P., Cantley L.C., Blenis J. Curr. Biol. 2003, 13:1259-1268.
24. Im E., von Lintig F.C., Chen J., Zhuang S., Qui W., Chowdhury S., Worley P.F., Boss G.R., Pilz R.B. Oncogene 2002, 21:6356-6365.
25. Inoki K., Li Y., Xu T., Guan K.L. Gene Dev. 2003, 17:1829-1834.
26. de Rooij J., Bos J.L. Oncogene 1997, 14:623-625.
27. Taylor S.J., Shalloway D. Curr. Biol. 1996, 6:1621-1627.
28. Benard V., Bokoch G.M. Methods Enzymol. 2002, 345:349-359.
29. Ren X.D., Kiosses W.B., Schwartz M.A. EMBO J. 1999, 18:578-585.
30. Stofega M., DerMardirossian C., Bokoch G.M. Methods Mol. Biol. 2006, 332:269-279.
31. Garcia-Mata R., Wennerberg K., Arthur W.T., Noren N.K., Ellerbroek S.M., Burridge K. Methods Enzymol. 2006, 406:425-437.
32. Anderson E.L., Hamann M.J. Biochem. J. 2011, 441:869-879.
33. Nakamura T., Aoki K., Matsuda M. Methods 2005, 37:146-153.
34. Aoki K., Matsuda M. Nat. Protoc. 2009, 4:1623-1631.
35. Hodgson L., Pertz O., Hahn K.M. Methods Cell Biol. 2008, 85:63-81.
36. Pertz O., Hahn K.M. J. Cell Sci. 2004, 117:1313-1318.
37. Marshall C.B., Ho J., Buerger C., Plevin M.J., Li G.Y., Li Z., Ikura M., Stambolic V. Sci. Signal. 2009, 2:ra3.
38. Vigil D., Cherfils J., Rossman K.L., Der C.J. Nat. Rev. Cancer 2010, 10:842-857.
39. Aittaleb M., Boguth C.A., Tesmer J.J. Mol. Pharmacol. 2010, 77:111-125.
40. Huang J., Manning B.D. Biochem. J. 2008, 412:179-190.
41. Cox A.D., Der C.J. Small GTPases 2010, 1:2-27.
42. Reuther G.W., Der C.J. Curr. Opin. Cell Biol. 2000, 12:157-165.
43. Tabancay A.P., Gau C.L., Machado I.M., Uhlmann E.J., Gutmann D.H., Guo L., Tamanoi F. J. Biol. Chem. 2003, 278:39921-39930.
44. Kwiatkowski D.J., Manning B.D. Hum. Mol. Genet. 2005, 14 Spec No. 2:R251-R258.
45. DeYoung M.P., Horak P., Sofer A., Sgroi D., Ellisen L.W. Gene Dev. 2008, 22:239-251.
46. Inoki K., Li Y., Zhu T., Wu J., Guan K.L. Nat. Cell Biol. 2002, 4:648-657.
47. Manning B.D., Tee A.R., Logsdon M.N., Blenis J., Cantley L.C. Mol. Cell 2002, 10:151-162.
48. Avruch J., Hara K., Lin Y., Liu M., Long X., Ortiz-Vega S., Yonezawa K. Oncogene 2006, 25:6361-6372.
49. Inoki K., Zhu T., Guan K.L. Cell 2003, 115:577-590.
50. Stocker H., Radimerski T., Schindelholz B., Wittwer F., Belawat P., Daram P., Breuer S., Thomas G., Hafen E. Nat. Cell Biol. 2003, 5:559-565.
51. Saucedo L.J., Gao X., Chiarelli D.A., Li L., Pan D., Edgar B.A. Nat. Cell Biol. 2003, 5:566-571.
52. Garami A., Zwartkruis F.J., Nobukuni T., Joaquin M., Roccio M., Stocker H., Kozma S.C., Hafen E., Bos J.L., Thomas G. Mol. Cell 2003, 11:1457-1466.
53. Hsu Y.C., Chern J.J., Cai Y., Liu M., Choi K.W. Nature 2007, 445:785-788.
54. Rehmann H., Bruning M., Berghaus C., Schwarten M., Kohler K., Stocker H., Stoll R., Zwartkruis F.J., Wittinghofer A. FEBS Lett. 2008, 582:3005-3010.
55. Wang X., Fonseca B.D., Tang H., Liu R., Elia A., Clemens M.J., Bommer U.A., Proud C.G. J. Biol. Chem. 2008, 283:30482-30492.
56. Etienne-Manneville S., Hall A. Nature 2002, 420:629-635.
57. Rossman K.L., Der C.J., Sondek J. Nat. Rev. Mol. Cell Biol. 2005, 6:167-180.
58. Hoffman G.R., Cerione R.A. FEBS Lett. 2002, 513:85-91.
59. Schmidt A., Hall A. Gene Dev. 2002, 16:1587-1609.
60. Glaven J.A., Whitehead I., Bagrodia S., Kay R., Cerione R.A. J. Biol. Chem. 1999, 274:2279-2285.
61. Krendel M., Zenke F.T., Bokoch G.M. Nat. Cell Biol. 2002, 4:294-301.
62. Westwick J.K., Lee R.J., Lambert Q.T., Symons M., Pestell R.G., Der C.J., Whitehead I.P. J. Biol. Chem. 1998, 273:16739-16747.
63. Birukova A.A., Adyshev D., Gorshkov B., Bokoch G.M., Birukov K.G., Verin A.D. Am. J. Physiol. Lung Cell. Mol. Physiol. 2006, 290:L540-L548.
64. Cohn M. Curr. Top. Cell. Regul. 1984, 24:1-13.
65. Mildvan A.S., Cohn M. Adv. Enzymol. Relat. Areas Mol. Biol. 1970, 33:1-70.
66. Mildvan A.S. Adv. Enzymol. Relat. Areas Mol. Biol. 1979, 49:103-126.
67. Schlichting I., Wittinghofer A., Rosch P. Biochem. Biophys. Res. Commun. 1988, 150:444-448.
68. Burk S.C., Papastavros M.Z., McCormick F., Redfield A.G. Proc. Natl. Acad. Sci. USA 1989, 86:817-820.
69. Yamasaki K., Kawai G., Ito Y., Muto Y., Fujita J., Miyazawa T., Nishimura S., Yokoyama S. Biochem. Biophys. Res. Commun. 1989, 162:1054-1062.
70. Harper S.M., Neil L.C., Day I.J., Hore P.J., Gardner K.H. J. Am. Chem. Soc. 2004, 126:3390-3391.
71. Zeeb M., Balbach J. Methods 2004, 34:65-74.
72. Schanda P., Forge V., Brutscher B. Proc. Natl. Acad. Sci. USA 2007, 104:11257-11262.
73. Furukawa A., Nagata T., Matsugami A., Habu Y., Sugiyama R., Hayashi F., Kobayashi N., Yokoyama S., Takaku H., Katahira M. EMBO J. 2009, 28:440-451.
74. Selenko P., Frueh D.P., Elsaesser S.J., Haas W., Gygi S.P., Wagner G. Nat. Struct. Mol. Biol. 2008, 15:321-329.
75. Low A., Sprinzl M., Limmer S. Eur. J. Biochem. 1993, 213:781-788.
76. Scheidig A.J., Franken S.M., Corrie J.E., Reid G.P., Wittinghofer A., Pai E.F., Goody R.S. J. Mol. Biol. 1995, 253:132-150.
77. John J., Sohmen R., Feuerstein J., Linke R., Wittinghofer A., Goody R.S. Biochemistry 1990, 29:6058-6065.
78. Scheffzek K., Lautwein A., Kabsch W., Ahmadian M.R., Wittinghofer A. Nature 1996, 384:591-596.
79. Maruta H., Holden J., Sizeland A., D'Abaco G. J. Biol. Chem. 1991, 266:11661-11668.
80. Scheffzek K., Ahmadian M.R., Kabsch W., Wiesmuller L., Lautwein A., Schmitz F., Wittinghofer A. Science 1997, 277:333-338.
81. Barbacid M. Annu. Rev. Biochem. 1987, 56:779-827.
82. Krengel U., Schlichting I., Scherer A., Schumann R., Frech M., John J., Kabsch W., Pai E.F., Wittinghofer A. Cell 1990, 62:539-548.
83. Cales C., Hancock J.F., Marshall C.J., Hall A. Nature 1988, 332:548-551.
84. Daumke O., Weyand M., Chakrabarti P.P., Vetter I.R., Wittinghofer A. Nature 2004, 429:197-201.
85. Scrima A., Thomas C., Deaconescu D., Wittinghofer A. EMBO J. 2008, 27:1145-1153.
86. Rittinger K., Walker P.A., Eccleston J.F., Smerdon S.J., Gamblin S.J. Nature 1997, 389:758-762.
87. Jones A.C., Shyamsundar M.M., Thomas M.W., Maynard J., Idziaszczyk S., Tomkins S., Sampson J.R., Cheadle J.P. Am. J. Hum. Genet. 1999, 64:1305-1315.
88. Maheshwar M.M., Cheadle J.P., Jones A.C., Myring J., Fryer A.E., Harris P.C., Sampson J.R. Hum. Mol. Genet. 1997, 6:1991-1996.
89. Dabora S.L., Jozwiak S., Franz D.N., Roberts P.S., Nieto A., Chung J., Choy Y.S., Reeve M.P., Thiele E., Egelhoff J.C., Kasprzyk-Obara J., Domanska-Pakiela D., Kwiatkowski D.J. Am. J. Hum. Genet. 2001, 68:64-80.
90. Au K.S., Rodriguez J.A., Finch J.L., Volcik K.A., Roach E.S., Delgado M.R., Rodriguez E., Northrup H. Am. J. Hum. Genet. 1998, 62:286-294.
91. Au K.S., Williams A.T., Roach E.S., Batchelor L., Sparagana S.P., Delgado M.R., Wheless J.W., Baumgartner J.E., Roa B.B., Wilson C.M., Smith-Knuppel T.K., Cheung M.Y., Whittemore V.H., King T.M., Northrup H. Genet. Med. 2007, 9:88-100.
92. Langkau N., Martin N., Brandt R., Zugge K., Quast S., Wiegele G., Jauch A., Rehm M., Kuhl A., Mack-Vetter M., Zimmerhackl L.B., Janssen B. Eur. J. Pediatr. 2002, 161:393-402.
93. Rendtorff N.D., Bjerregaard B., Frodin M., Kjaergaard S., Hove H., Skovby F., Brondum-Nielsen K., Schwartz M. Hum. Mutat. 2005, 26:374-383.
94. Beauchamp R.L., Banwell A., McNamara P., Jacobsen M., Higgins E., Northrup H., Short P., Sims K., Ozelius L., Ramesh V. Hum. Mutat. 1998, 12:408-416.
95. Ali M., Girimaji S.C., Markandaya M., Shukla A.K., Sacchidanand S., Kumar A. Acta Neurol. Scand. 2005, 111:54-63.
96. Gasmi-Seabrook G.M., Marshall C.B., Cheung M., Kim B., Wang F., Jang Y.J., Mak T.W., Stambolic V., Ikura M. J. Biol. Chem. 2010, 285:5137-5145.
97. Mok K.H., Nagashima T., Day I.J., Jones J.A., Jones C.J., Dobson C.M., Hore P.J. J. Am. Chem. Soc. 2003, 125:12484-12492.
98. Tugarinov V., Kanelis V., Kay L.E. Nat. Protoc. 2006, 1:749-754.
99. Meiri D., Marshall C.B., Greeve M.A., Kim B., Balan M., Suarez F., Wu C., Larose J., Fine N., Ikura M., Rottapel R. Mol. Cell 2012, 45:642-655.
100. Long X., Lin Y., Ortiz-Vega S., Yonezawa K., Avruch J. Curr. Biol. 2005, 15:702-713.
101. Onda H., Crino P.B., Zhang H., Murphey R.D., Rastelli L., Gould Rothberg B.E., Kwiatkowski D.J. Mol. Cell. Neurosci. 2002, 21:561-574.
102. Ren Y., Li R., Zheng Y., Busch H. J. Biol. Chem. 1998, 273:34954-34960.
103. Meiri D., Greeve M.A., Brunet A., Finan D., Wells C.D., LaRose J., Rottapel R. Mol. Cell. Biol. 2009, 29:5963-5973.
104. Traut T.W. Mol. Cell. Biochem. 1994, 140:1-22.
105. Gureasko J., Galush W.J., Boykevisch S., Sondermann H., Bar-Sagi D., Groves J.T., Kuriyan J. Nat. Struct. Mol. Biol. 2008, 15:452-461.
106. Groves J.T., Kuriyan J. Nat. Struct. Mol. Biol. 2010, 17:659-665.
107. Margarit S.M., Sondermann H., Hall B.E., Nagar B., Hoelz A., Pirruccello M., Bar-Sagi D., Kuriyan J. Cell 2003, 112:685-695.
108. Boykevisch S., Zhao C., Sondermann H., Philippidou P., Halegoua S., Kuriyan J., Bar-Sagi D. Curr. Biol. 2006, 16:2173-2179.
109. Yu B., Martins I.R., Li P., Amarasinghe G.K., Umetani J., Fernandez-Zapico M.E., Billadeau D.D., Machius M., Tomchick D.R., Rosen M.K. Cell 2010, 140:246-256.
110. Li P., Martins I.R., Amarasinghe G.K., Rosen M.K. Nat. Struct. Mol. Biol. 2008, 15:613-618.
111. Amarasinghe G.K., Rosen M.K. Biochemistry 2005, 44:15257-15268.
112. Aghazadeh B., Lowry W.E., Huang X.Y., Rosen M.K. Cell 2000, 102:625-633.
113. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. J. Biomol. NMR 1995, 6:277-293.
114. Johnson B.A., Blevins R.A. J. Biol. NMR 1994, 4:603-614.
115. Park S.H., Weinberg R.A. Oncogene 1995, 11:2349-2355.
116. Kim E., Goraksha-Hicks P., Li L., Neufeld T.P., Guan K.L. Nat. Cell Biol. 2008, 10:935-945.
117. Sancak Y., Peterson T.R., Shaul Y.D., Lindquist R.A., Thoreen C.C., Bar-Peled L., Sabatini D.M. Science 2008, 320:1496-1501.