Protons as second messenger regulators of G protein signaling

Molecular Cell

Volumn 51, Issue 4, 2013, Pages 531-538

  Isom, DanielG ^a   Sridharan, Vishwajith ^a   Baker, Rachael ^a   Clement, SarahT ^a   Smalley, DavidM ^a,b   Dohlman, HenrikG ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; PROTON;

ARTICLE; CELL PH; CONTROLLED STUDY; GENE EXPRESSION; HYDROLYSIS; LIQUID CHROMATOGRAPHY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SECOND MESSENGER; STRUCTURAL PROTEOMICS; THERMOSTABILITY;

ALGORITHMS; GTP-BINDING PROTEIN ALPHA SUBUNITS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HUMANS; HYDROGEN-ION CONCENTRATION; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTONS; RECEPTORS, G-PROTEIN-COUPLED; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TEMPERATURE;

EID: 84882600742     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.07.012     Document Type: Article

References (46)

1. Alexov E., Mehler E.L., Baker N., Baptista A.M., Huang Y., Milletti F., Nielsen J.E., Farrell D., Carstensen T., Olsson M.H., et al. Progress in the prediction of pKa values in proteins. Proteins 2011, 79:3260-3275.
2. Benovic J.L., Strasser R.H., Caron M.G., Lefkowitz R.J. Beta-adrenergic receptor kinase: identification of a novel protein kinase that phosphorylates the agonist-occupied form of the receptor. Proc. Natl. Acad. Sci. USA 1986, 83:2797-2801.
3. Bopassa J.C. Protection of the ischemic myocardium during the reperfusion: between hope and reality. Am J Cardiovasc Dis 2012, 2:223-236.
4. Bush J., Makhatadze G.I. Statistical analysis of protein structures suggests that buried ionizable residues in proteins are hydrogen bonded or form salt bridges. Proteins 2011, 79:2027-2032.
5. Chung K.Y., Rasmussen S.G., Liu T., Li S., DeVree B.T., Chae P.S., Calinski D., Kobilka B.K., Woods V.L., Sunahara R.K. Conformational changes in the G protein Gs induced by the β2 adrenergic receptor. Nature 2011, 477:611-615.
6. Clapham D.E. Calcium signaling. Cell 2007, 131:1047-1058.
7. Dechant R., Binda M., Lee S.S., Pelet S., Winderickx J., Peter M. Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J. 2010, 29:2515-2526.
8. Gjetting K.S., Ytting C.K., Schulz A., Fuglsang A.T. Live imaging of intra- and extracellular pH in plants using pHusion, a novel genetically encoded biosensor. J.Exp. Bot. 2012, 63:3207-3218.
9. Gunner M.R., Saleh M.A., Cross E., ud-Doula A., Wise M. Backbone dipoles generate positive potentials in all proteins: origins and implications of the effect. Biophys. J. 2000, 78:1126-1144.
10. Hellwig N., Plant T.D., Janson W., Schäfer M., Schultz G., Schaefer M. TRPV1 acts as proton channel to induce acidification in nociceptive neurons. J.Biol. Chem. 2004, 279:34553-34561.
11. Higashijima T., Ferguson K.M., Sternweis P.C., Ross E.M., Smigel M.D., Gilman A.G. The effect of activating ligands on the intrinsic fluorescence of guanine nucleotide-binding regulatory proteins. J.Biol. Chem. 1987, 262:752-756.
12. Hong S.P., Leiper F.C., Woods A., Carling D., Carlson M. Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc. Natl. Acad. Sci. USA 2003, 100:8839-8843.
13. Isom D.G., Cannon B.R., Castañeda C.A., Robinson A., García-Moreno B. High tolerance for ionizable residues in the hydrophobic interior of proteins. Proc. Natl. Acad. Sci. USA 2008, 105:17784-17788.
14. Isom D.G., Castañeda C.A., Cannon B.R., Velu P.D., García-Moreno E.B. Charges in the hydrophobic interior of proteins. Proc. Natl. Acad. Sci. USA 2010, 107:16096-16100.
15. Isom D.G., Vardy E., Oas T.G., Hellinga H.W. Picomole-scale characterization of protein stability and function by quantitative cysteine reactivity. Proc. Natl. Acad. Sci. USA 2010, 107:4908-4913.
16. Isom D.G., Castañeda C.A., Cannon B.R., García-Moreno B. Large shifts in pKa values of lysine residues buried inside a protein. Proc. Natl. Acad. Sci. USA 2011, 108:5260-5265.
17. Isom D.G., Marguet P.R., Oas T.G., Hellinga H.W. A miniaturized technique for assessing protein thermodynamics and function using fast determination of quantitative cysteine reactivity. Proteins 2011, 79:1034-1047.
18. Kader M.A., Lindberg S. Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal. Behav. 2010, 5:233-238.
19. Kajander T., Kahn P.C., Passila S.H., Cohen D.C., Lehtiö L., Adolfsen W., Warwicker J., Schell U., Goldman A. Buried charged surface in proteins. Structure 2000, 8:1203-1214.
20. Kim J., Mao J., Gunner M.R. Are acidic and basic groups in buried proteins predicted to be ionized?. J.Mol. Biol. 2005, 348:1283-1298.
21. Ludwig M.G., Vanek M., Guerini D., Gasser J.A., Jones C.E., Junker U., Hofstetter H., Wolf R.M., Seuwen K. Proton-sensing G-protein-coupled receptors. Nature 2003, 425:93-98.
22. Miesenböck G., De Angelis D.A., Rothman J.E. Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 1998, 394:192-195.
23. Nag S., Ma Q., Wang H., Chumnarnsilpa S., Lee W.L., Larsson M., Kannan B., Hernandez-Valladares M., Burtnick L.D., Robinson R.C. Ca2+ binding by domain 2 plays a critical role in the activation and stabilization of gelsolin. Proc. Natl. Acad. Sci. USA 2009, 106:13713-13718.
24. Neves S.R., Ram P.T., Iyengar R. G protein pathways. Science 2002, 296:1636-1639.
25. Nielsen J.E., Gunner M.R., García-Moreno B.E. The pKa Cooperative: a collaborative effort to advance structure-based calculations of pKa values and electrostatic effects in proteins. Proteins 2011, 79:3249-3259.
26. O'Rourke J. Computational Geometry in C 1998, 182-189. Cambridge University Press, New York.
27. Orij R., Postmus J., Ter Beek A., Brul S., Smits G.J. Invivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiology 2009, 155:268-278.
28. Orij R., Brul S., Smits G.J. Intracellular pH is a tightly controlled signal in yeast. Biochim. Biophys. Acta 2011, 1810:933-944.
29. Perutz M.F. Electrostatic effects in proteins. Science 1978, 201:1187-1191.
30. Peters L.Z., Hazan R., Breker M., Schuldiner M., Ben-Aroya S. Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. J.Cell Biol. 2013, 201:663-671.
31. Rashin A.A., Honig B. On the environment of ionizable groups in globular proteins. J.Mol. Biol. 1984, 173:515-521.
32. Rasmussen S.G., DeVree B.T., Zou Y., Kruse A.C., Chung K.Y., Kobilka T.S., Thian F.S., Chae P.S., Pardon E., Calinski D., et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 2011, 477:549-555.
33. Rubenstein E.M., Schmidt M.C. The glucose signal and metabolic p[H+]lux. EMBO J. 2010, 29:2473-2474.
34. Rubenstein E.M., McCartney R.R., Zhang C., Shokat K.M., Shirra M.K., Arndt K.M., Schmidt M.C. Access denied: Snf1 activation loop phosphorylation is controlled by availability of the phosphorylated threonine 210 to the PP1 phosphatase. J.Biol. Chem. 2008, 283:222-230.
35. Schroeder M.A., Swietach P., Atherton H.J., Gallagher F.A., Lee P., Radda G.K., Clarke K., Tyler D.J. Measuring intracellular pH in the heart using hyperpolarized carbon dioxide and bicarbonate: a 13C and 31P magnetic resonance spectroscopy study. Cardiovasc. Res. 2010, 86:82-91.
36. Schweins T., Geyer M., Scheffzek K., Warshel A., Kalbitzer H.R., Wittinghofer A. Substrate-assisted catalysis as a mechanism for GTP hydrolysis of p21ras and other GTP-binding proteins. Nat. Struct. Biol. 1995, 2:36-44.
37. Srivastava J., Barber D.L., Jacobson M.P. Intracellular pH sensors: design principles and functional significance. Physiology (Bethesda) 2007, 22:30-39.
38. Studier F.W. Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 2005, 41:207-234.
39. Tews I., Findeisen F., Sinning I., Schultz A., Schultz J.E., Linder J.U. The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 2005, 308:1020-1023.
40. Torres M.P., Clement S.T., Cappell S.D., Dohlman H.G. Cell cycle-dependent phosphorylation and ubiquitination of a G protein alpha subunit. J.Biol. Chem. 2011, 286:20208-20216.
41. Trivedi B., Danforth W.H. Effect of pH on the kinetics of frog muscle phosphofructokinase. J.Biol. Chem. 1966, 241:4110-4112.
42. Van Eps N., Preininger A.M., Alexander N., Kaya A.I., Meier S., Meiler J., Hamm H.E., Hubbell W.L. Interaction of a G protein with an activated receptor opens the interdomain interface in the alpha subunit. Proc. Natl. Acad. Sci. USA 2011, 108:9420-9424.
43. Wall M.A., Coleman D.E., Lee E., Iñiguez-Lluhi J.A., Posner B.A., Gilman A.G., Sprang S.R. The structure of the G protein heterotrimer Gi alpha 1 beta 1 gamma 2. Cell 1995, 83:1047-1058.
44. Webb B.A., Chimenti M., Jacobson M.P., Barber D.L. Dysregulated pH: a perfect storm for cancer progression. Nat. Rev. Cancer 2011, 11:671-677.
45. Westfield G.H., Rasmussen S.G., Su M., Dutta S., DeVree B.T., Chung K.Y., Calinski D., Velez-Ruiz G., Oleskie A.N., Pardon E., et al. Structural flexibility of the G alpha s alpha-helical domain in the beta2-adrenoceptor Gs complex. Proc. Natl. Acad. Sci. USA 2011, 108:16086-16091.
46. Young B.P., Shin J.J., Orij R., Chao J.T., Li S.C., Guan X.L., Khong A., Jan E., Wenk M.R., Prinz W.A., et al. Phosphatidic acid is a pH biosensor that links membrane biogenesis to metabolism. Science 2010, 329:1085-1088.