Exploring G protein-coupled receptor signaling networks using SILAC-based phosphoproteomics

Methods

Volumn 92, Issue , 2016, Pages 36-50

  Williams, Grace R ^a   Bethard, Jennifer R ^a   Berkaw, Mary N ^a   Nagel, Alexis K ^a,b   Luttrell, Louis M ^a,c   Ball, Lauren E ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

G protein coupled receptor; Mass spectrometry; Osteoblast; Parathyroid hormone receptor; Phosphoproteomics

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CYCLIC AMP DEPENDENT PROTEIN KINASE; G PROTEIN COUPLED RECEPTOR; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PARATHYROID HORMONE; PARATHYROID HORMONE RECEPTOR 1; PTH1R PROTEIN, HUMAN;

ANALYTIC METHOD; ARTICLE; BIOINFORMATICS; CELL ADHESION; CELL MOTILITY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOSKELETON; ENZYME REGULATION; IN VITRO STUDY; ISOTOPIC LABELING BY AMINO ACIDS IN CELL CULTURE; MASS SPECTROMETRY; MOLECULAR PROBE; OSTEOBLAST; PHOSPHOPROTEOMICS; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEOMICS; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; SUICIDE SUBSTRATE; UPREGULATION; ANIMAL; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MOUSE; PHYSIOLOGY; PROCEDURES; TANDEM MASS SPECTROMETRY; TRANSFORMED CELL LINE;

ANIMALS; CELL LINE, TRANSFORMED; GENE REGULATORY NETWORKS; MICE; PARATHYROID HORMONE; PROTEOMICS; RECEPTOR, PARATHYROID HORMONE, TYPE 1; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84983113110     PISSN: 10462023     EISSN: 10959130     Source Type: Journal    
DOI: 10.1016/j.ymeth.2015.06.022     Document Type: Article

References (94)

1. Galandrin S., Bouvier M. Distinct signaling profiles of beta1 and beta2 adrenergic receptor ligands toward adenylyl cyclase and mitogen-activated protein kinase reveals the pluridimensionality of efficacy. Mol. Pharmacol. 2006, 70:1575-1584.
2. Luttrell L.M., Gesty-Palmer D. Beyond desensitization: physiological relevance of arrestin-dependent signaling. Pharmacol. Rev. 2010, 62:305-330.
3. Kenakin T., Miller L.E. Seven transmembrane receptors as shapeshifting proteins: the impact of allosteric modulation and functional selectivity on new drug discovery. Pharmacol. Rev. 2010, 62:265-304.
4. Christopoulos A., Kenakin T. G protein-coupled receptor allosterism and complexing. Pharmacol. Rev. 2002, 54:323-374.
5. Kenakin T.P. Functional selectivity through protean and biased agonism: who steers the ship?. Mol. Pharmacol. 2007, 72:1393-1401.
6. Luttrell L.M. Minireview: more than just a hammer: ligand "bias" and pharmaceutical discovery. Mol. Endocrinol. 2014, 28:281-294.
7. Olsen J.V., Blagoev B., Gnad F., Macek B., Kumar C., Mortensen P., Mann M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127:635-648.
8. Roux P.P., Thibault P. The coming of age of phosphoproteomics - from large data sets to inference of protein functions. Mol. Cell. Proteomics 2013, 12:3453-3464.
9. Sharma K., D'Souza R.C., Tyanova S., Schaab C., Wisniewski J.R., Cox J., Mann M. Ultradeep human phosphoproteome reveals a distinct regulatory nature of Tyr and Ser/Thr-based signaling. Cell Rep. 2014, 8:1583-1594.
10. Xiao K., Sun J., Kim J., Rajagopal S., Zhai B., Villen J., Haas W., Kovacs J.J., Shukla A.K., Hara M.R., Hernandez M., Lachmann A., Zhao S., Lin Y., Cheng Y., Mizuno K., Ma'ayan A., Gygi S.P., Lefkowitz R.J. Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc. Natl. Acad. Sci. U.S.A. 2010, 107:15299-15304.
11. Christensen G.L., Kelstrup C.D., Lyngso C., Sarwar U., Bogebo R., Sheikh S.P., Gammeltoft S., Olsen J.V., Hansen J.L. Mol. Cell. Proteomics 2010, 9:1540-1553.
12. Kendall R.T., Strungs E.G., Rachidi S.M., Lee M.H., El-Shewy H.M., Luttrell D.K., Janech M.G., Luttrell L.M. The beta-arrestin pathway-selective type 1A angiotensin receptor (AT1A) agonist [Sar1, Ile4, Ile8]-angiotensin II regulates a robust G protein-independent signaling network. J. Biol. Chem. 2011, 286:19880-19891.
13. Douglass J., Gunaratne R., Bradford D., Saeed F., Hoffert J.D., Steinbach P.J., Knepper M.A., Pisitkun T. Identifying protein kinase target preferences using mass spectrometry. Am. J. Physiol. Cell Physiol. 2012, 303:C715-727.
14. Bogebo R., Horn H., Olsen J.V., Gammeltoft S., Jensen L.J., Hansen J.L., Christensen G.L. Predicting kinase activity in angiotensin receptor phosphoproteomes based on sequence-motifs and interactions. PLoS ONE 2014, 9:e94672.
15. Lundby A., Andersen M.N., Steffensen A.B., Horn H., Kelstrup C.D., Francavilla C., Jensen L.J., Schmitt N., Thomsen M.B., Olsen J.V. In vivo phosphoproteomics analysis reveals the cardiac targets of β-adrenergic receptor signaling. Sci. Signal. 2013, 6:rs11.
16. Gesty-Palmer D., Chen M., Reiter E., Ahn S., Nelson C.D., Wang S., Eckhardt A.E., Cowan C.L., Spurney R.F., Luttrell L.M., Lefkowitz R.J. Distinct conformations of the parathyroid hormone receptor mediate G protein and beta-arrestin dependent activation of ERK1/2. J. Biol. Chem. 2006, 281:10856-10864.
17. Gesty-Palmer D., Flannery P., Yuan L., Spurney R., Lefkowitz R.J., Luttrell L.M. A beta-arrestin biased agonist of the parathyroid hormone receptor (PTH1R) promotes bone formation independent of G protein activation. Science Transl. Med. 2009, 1:1ra1.
18. Appleton K.M., Lee M.-H., Alele C., Alele C., Luttrell D.K., Peterson Y.K., Morinelli T.A., Luttrell L.M. Biasing the parathyroid hormone receptor: relating in vitro ligand efficacy to in vivo biological activity. Methods Enzymol. 2013, 522:229-262.
19. Olsen J.V., Mann M. Status of large-scale analysis of post-translational modifications by mass spectrometry. Mol. Cell. Proteomics 2013, 12:3444-3452.
20. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
21. Huttlin E.L., Jedrychowski M.P., Elias J.E., Goswami T., Rad R., Beausoleil S.A., Villen J., Haas W., Sowa M.E., Gygi S.P. A tissue-specific atlas of mouse protein phosphorylation and expression. Cell 2010, 143:1174-1189.
22. Wang D., Christensen K., Chawla K., Xiao G., Krebsbach P.H., Franceschi R.T. Isolation and characterization of MC3T3-E1 preosteoblast subclones with distinct in vitro and in vivo differentiation/mineralization potential. J. Bone Miner. Res. 1999, 14:893-903.
23. Franceschi R.T., Iyer B.S., Cui Y. Effects of ascorbic acid on collagen matrix formation and osteoblast differentiation in murine MC3T3-E1 cells. J. Bone Miner. Res. 1994, 9:843-854.
24. Franceschi R.T. The role of ascorbic acid in mesenchymal differentiation. Nutr. Rev. 1992, 50:65-70.
25. Franceschi R.T., Iyer B.S. Relationship between collagen synthesis and expression of the osteoblast phenotype in MC3T3-E1 cells. J. Bone Miner. Res. 1992, 7:235-246.
26. Schiller P.C., D'Ippolito G., Roos B.A., Howard G.A. Anabolic or catabolic responses of MC3T3-E1 osteoblastic cells to parathyroid hormone depend on time and duration of treatment. J. Bone Miner. Res. 1999, 14:1504-1512.
27. Spurney R.F. Regulated expression of G protein-coupled receptor kinases (GRK's) and beta-arrestins in osteoblasts. Calcif. Tissue Int. 2003, 73:153-160.
28. Sudo H., Kodama H.A., Amagai Y., Yamamoto S., Kasai S. In vitro differentiation and calcification in a new clonal osteogenic cell line derived from newborn mouse calvaria. J. Biol. Chem. 1983, 96:191-198.
29. Lanucara F., Eyers C.E. Mass spectrometric-based quantitative proteomics using SILAC. Meth Enzymol. 2011, 500:133-150.
30. Park S.S., Wu W.W., Zhou Y., Shen R.F., Martin B., Maudsley S. Effective correction of experimental errors in quantitative proteomics using stable isotope labeling by amino acids in cell culture (SILAC). J Proteomics. 2012, 75:3720-3732.
31. Cañas B., Piñeiro C., Calvo E., López-Ferrer D., Gallardo J.M. Trends in sample preparation for classical and second generation proteomics. J. Chromatogr. A 2007, 1153:235-258.
32. Hu L., Ye M., Zou H. Recent advances in mass spectrometry-based peptidome analysis. Expert Rev. Proteomics 2009, 6:433-447.
33. Villén J., Gygi S.P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry. Nat. Protoc. 2008, 2008(3):1630-1638.
34. Gilar M., Jaworski A., Olivova P., Gebler J.C. Peptide retention prediction applied to proteomic data analysis. Rapid Commun. Mass Spectrom. 2007, 21:2813-2821.
35. Gilar M., Olivova P., Daly A.E., Gebler J.C. Orthogonality of separation in two-dimensional liquid chromatography. Anal. Chem. 2005, 77:6426-6434.
36. Wang Y., Yang F., Gritsenko M.A., Wang Y., Clauss T., Liu T., Shen Y., Monroe M.E., Lopez-Ferrer D., Reno T., Moore R.J., Klemke R.L., Camp D.G., Smith R.D. Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells. Proteomics 2011, 11:2019-2026.
37. Yang F., Shen Y., Camp D.G., Smith R.D. High-pH reversed-phase chromatography with fraction concatenation for 2D proteomic analysis. Expert Rev. Proteomics 2012, 9:129-134.
38. Udeshi N.D., Mertins P., Svinkina T., Carr S.A. Large-scale identification of ubiquitination sites by mass spectrometry. Nat. Protoc. 2013, 8:1950-1960.
39. Batth T.S., Francavilla C., Olsen J.V. Off-line high-pH reversed-phase fractionation for in-depth phosphoproteomics. J. Proteome Res. 2014, 13:6176-6186.
40. de Graaf E.L., Giansanti P., Altelaar A.F., Heck A.J. Single-step enrichment by Ti4+-IMAC and label-free quantitation enables in-depth monitoring of phosphorylation dynamics with high reproducibility and temporal resolution. Mol. Cell. Proteomics 2014, 13:2426-2434.
41. Erickson B.K., Jedrychowski M.P., McAlister G.C., Everley R.A., Kunz R., Gygi S.P. Evaluating multiplexed quantitative phosphopeptide analysis on a hybrid quadrupole mass filter/linear ion trap/orbitrap mass spectrometer. Anal. Chem. 2015, 87:1241-1249.
42. Zhang Y.I., Wolf-Yadlin A., Ross P.L., Pappin D.J., Rush J., Lauffenburger D.A., White F.M. Time-resolved mass spectrometry of tyrosine phosphorylation sites in the epidermal growth factor receptor signaling network reveals dynamic modules. Mol. Cell. Proteomics 2005, 4(9):240-250.
43. Larsen M.R., Thingholm T.E., Jensen O.N., Roepstorff P., Jørgensen T.J. Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 2005, 4:873-886.
44. Mertins P., Qiao J.W., Patel J., Udeshi N.D., Clauser K.R., Mani D.R., Burgess M.W., Gillette M.A., Jaffe J.D., Carr S.A. Integrated proteomic analysis of post-translational modifications by serial enrichment. Nat. Methods 2013, 10:634-637.
45. Compton P.D., Strukl J.V., Bai D.L., Shabanowitz J., Hunt D.F. Optimization of electron transfer dissociation via informed selection of reagents and operating parameters. Anal. Chem. 2012, 84(3):1781-1785.
46. Beausoleil S.A., Villen J., Gerber S.A., Rush J., Gygi S.P. A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 2006, 24:1285-1292.
47. Taus T., Kocher T., Pichler P., Paschke C., Schmidt A., Henrich C., Mechtler K. Universal and confident phosphorylation site localization using phosphoRS. J. Proteome Res. 2011, 10:5354-5362.
48. Bern M., Kil Y.J., Becker C. Byonic: advanced peptide and protein identification software. Curr. Protoc. Bioinformatics 2012, Chapter 13, Unit 13.20.
49. Baker P.R., Trinidad J.C., Chalkley R.J. Modification site localization scoring integrated into a search engine. Mol. Cell. Proteomics 2011, 10. M111.008078.
50. Cox J., Neuhauser N., Michalski A., Scheltema R.A., Olsen J.V., Mann M. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011, 10:1794-1805.
51. Schwartz D., Gygi S.P. An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets. Nat. Biotechnol. 2005, 23:1391-1398.
52. Hornbeck P.V., Zhang B., Murray B., Kornhauser J.M., Latham V., Skrzypek E. PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 2015, 43:D512-520.
53. Maddelein D., Colaert N., Buchanan I., Hulstaert N., Gevaert K., Martens L. The iceLogo web server and SOAP service for determining protein consensus sequences. Nucleic Acids Res. 2015, pii: gkv385.
54. Cox J., Mann M. 1D and 2D annotation enrichment: a statistical method integrating quantitative proteomics with complementary high-throughput data. BMC Bioinformatics 2012, 13(Suppl 16):S12.
55. Horn H., Schoof E.M., Kim J., Robin X., Miller M.L., Diella F., Palma A., Cesareni G., Jensen L.J., Lindin R. KinomeXplorer: an integrated platform for kinome biology studies. Nat. Methods 2014, 11:603-604.
56. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
57. Cox J., Matic I., Hilger M., Nagaraj N., Selbach M., Olsen J.V., Mann M. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protocol. 2009, 4:698-705.
58. Geiger T., Velic A., Macek B., Lundberg E., Kampf C., Nagaraj N., Uhlen M., Cox J., Mann M. Initial quantitative proteomic map of 28 mouse tissues using the SILAC mouse. Mol. Cell. Proteomics 2013, 12:1709-1722.
59. Ritchie M.E., Phipson B., Wu D., Hu Y., Law C.W., Shi W., Smyth G.K. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015, 43:e47.
60. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc., Series B (Methodol.) 1995, 57:289-300.
61. Hunter T., Sefton B.M. Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. Proc. Natl. Acad. Sci. U.S.A. 1980, 77:1311-1315.
62. Datta N.S., Kolailat R., Fite A., Pettway G., Abbou-Samra A.B. Distinct roles for mitogen-activated protein kinase phosphatase-1 (MKP-1) and ERK-MAPK in PTH1R signaling during osteoblast proliferation and differentiation. Cell. Signal. 2010, 3:457-466.
63. Miedlich S.U., Abou-Samra A.B. Eliminating phosphorylation sites of the parathyroid hormone receptor type 1 differentially affects stimulation of phospholipase C and receptor internalization. Am J Physiol Endocrinol Metab 2008, 295:E665-671.
64. Tawfeek H.A., Qian F., Abou-Samra A.B. Phosphorylation of the receptor for PTH and PTHrP is required for internalization and regulates receptor signaling. Mol. Endocrinol. 2002, 16:1-13.
65. Blind E., Bambino T., Huang Z., Bliziotes M., Nissenson R.A. Phosphorylation of the cytoplasmic tail of the PTH/PTHrP receptor. J. Bone Miner. Res. 1996, 11:578-586.
66. Manning G., Whyte D.B., Martinez R., Hunter T., Sudarsanam S. The protein kinase complement of the human genome. Science 2002, 298:1912-1934.
67. Udeshi N.D., Mani D.R., Eisenhaure T., Mertins P., Jaffe J.D., Clauser K.R., Hacohen N., Carr S.A. Methods for quantification of in vivo changes in protein ubiquitination following proteasome and deubiquitinase inhibition. Mol. Cell. Proteomics 2012, 11:148-159.
68. Caenepeel S., Charydczak G., Sudarsanam S., Hunter T., Manning G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:11707-11712.
69. Echols N., Harrison P., Balasubramanian S., Luscombe N.M., Bertone P., Zhang Z., Gerstein M. Comprehensive analysis of amino acid and nucleotide composition in eukaryotic genomes, comparing genes and pseudogenes. Nucleic Acids Res. 2002, 30:2515-2523.
70. Ubersax J.A., Ferrell J.E. Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 2007, 8:530-541.
71. Linding R., Jensen L.J., Ostheimer G.J., van Vugt M.S., Jørgensen C., Miron I.M., Diella F., Colwill K., Taylor L., Elder K., Metalnikov P., Nguyen V., Pasculescu A., Jin J., Park J.G., Samson L.D., Woodgett J.R., Russell R.B., Bork P., Yaffe M.B., Pawson T. Systematic discovery of in vivo phosphorylation networks. Cell 2007, 129:1415-1426.
72. Linding R., Jensen L.J., Pasculescu A., Olhovsky M., Colwill K., Bork P., Yaffe M.B., Pawson T. NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res. 2008, 36:D695-9.
73. Letunic I., Bork P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011, 39:W475-478.
74. Rigbolt K.T., Prokhorova T.A., Akimov V., Henningsen J., Johansen P.T., Kratchmarova I., Kassem M., Mann M., Olsen J.V., Blagoev B. System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci. Signal. 2011, 4:rs3.
75. Cheung M., Sharma A., Madhunapantula S.V., Robertson G.P. Akt3 and mutant V600E B-Raf cooperate to promote early melanoma development. Cancer Res. 2008, 68:3429-3439.
76. Zhang B.H., Guan K.L. Regulation of the Raf kinase by phosphorylation. Exp. Lung Res. 2001, 27:269-295.
77. Guan K.L., Figueroa C., Brtva T.R., Zhu T., Taylor J., Barber T.D., Vojtek A.B. Negative regulation of the serine/threonine kinase B-Raf by Akt. J. Biol. Chem. 2000, 275:27354-27359.
78. Baljuls A., Schmitz W., Mueller T., Zahedi R.P., Sickmann A., Hekman M., Rapp U.R. Positive regulation of A-RAF by phosphorylation of isoform-specific hinge segment and identification of novel phosphorylation sites. J. Biol. Chem. 2008, 283:27239-27254.
79. Li T., Zhang J., Zhu F., Wen W., Zykova T., Li X., Liu K., Peng C., Ma W., Shi G., Dong Z., Bode A.M., Dong Z. P21-activated protein kinase (PAK2)-mediated c-Jun phosphorylation at 5 threonine sites promotes cell transformation. Carcinogenesis 2011, 32:659-666.
80. Kruiswijk F., Yuniati L., Magliozzi R., Low T.Y., Lim R., Bolder R., Mohammed S., Proud C.G., Heck A.J., Pagano M., Guardavaccaro D. Coupled activation and degradation of eEF2K regulates protein synthesis in response to genotoxic stress. Sci. Signal. 2012, 5:ra40.
81. Kim S.-Y., Volsky D.J. PAGE: parametric analysis of geneset enrichment. BMC Bioinformatics 2005, 6:144-156.
82. Maudsley S., Chadwick W., Wang L., Zhou Y., Martin B., Park S.S. Bioinformatic approaches to metabolic pathways analysis. Methods Mol. Biol. 2011, 756:99-130.
83. Maudsley S., Siddiqui S., Martin B. Systems analysis of arrestin pathway functions. Prog. Mol. Biol. Transl. Sci. 2013, 118:431-467.
84. ten Klooster J.P., Jaffer Z.M., Chernoff J., Hordijk P.L. PL, Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J. Cell Biol. 2006, 172:759-769.
85. Chahdi A., Sorkin A. Protein kinase A-dependent phosphorylation modulates beta1Pix guanine nucleotide exchange factor activity through 14-3-3beta binding. Mol. Cell. Biol. 2008, 28:1679-1687.
86. Premont R.T., Perry S.J., Schmalzigaug R., Roseman J.T., Xing Y., Claing A. The GIT/PIX complex: an oligomeric assembly of GIT family ARF GTPase-activating proteins and PIX family Rac1/Cdc42 guanine nucleotide exchange factors. Cell. Signal. 2004, 16:1001-1011.
87. Gesty-Palmer D., Yuan L., Martin B., Wood W.H., Lee M.H., Janech M.G., Tsoi L.C., Zheng W.J., Luttrell L.M., Maudsley S. β-arrestin-selective G protein-coupled receptor agonists engender unique biological efficacy in vivo. Mol. Endocrinol. 2013, 27:296-314.
88. Yoshida T., Clark M.F., Stern P.H. The small GTPase RhoA is crucial for MC3T3-E1 osteoblastic cell survival. J. Cell. Biochem. 2009, 106:896-902.
89. Hamamura K., Swarnkar G., Tanjung N., Cho E., Li J., Na S., Yokota H. RhoA-mediated signaling in mechanotransduction of osteoblasts. Connect. Tissue Res. 2012, 53:398-406.
90. Wan Q., Cho E., Yokota H., Na S. Rac1 and Cdc42 GTPases regulate shear stress-driven β-catenin signaling in osteoblasts. Biochem. Biophys. Res. Commun. 2013, 433:502-507.
91. Lefkowitz R.J., Pierce K.L., Luttrell L.M. Dancing with different partners: protein kinase a phosphorylation of seven membrane-spanning receptors regulates their G protein-coupling specificity. Mol. Pharmacol. 2002, 62:971-974.
92. Merrill A.E., Hebert A.S., MacGilvray M.E., Rose C.M., Bailey D.J., Bradley J.C., Wood W.W., El Masri M., Westphall M.S., Gasch A.P., Coon J.J. NeuCode labels for relative protein quantification. Mol. Cell. Proteomics 2014, 13:2503-2512.
93. Paulo J.A., McAllister F.E., Everley R.A., Beausoleil S.A., Banks A.S., Gygi S.P. Effects of MEK inhibitors GSK1120212 and PD0325901 in vivo using 10-plex quantitative proteomics and phosphoproteomics. Proteomics 2015, 15:462-473.
94. Maudsley S., Martin B., Gesty-Palmer D., Cheung H., Johnson C., Patel S., Becker K.G., Wood W.H., Zhang Y., Lehrmann E., Luttrell L.M. Delineation of a conserved arrestin-biased signaling repertoire in vivo. Mol. Pharmacol. 2015, 87:706-717.