Residue specific contributions to stability and activity inferred from saturation mutagenesis and deep sequencing

Current Opinion in Structural Biology

Volumn 24, Issue 1, 2014, Pages 63-71

  Tripathi, Arti ^a   Varadarajan, Raghavan ^a,b  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING AFFINITY; CODON; DNA LIBRARY; DNA SCREENING; EPISTASIS; GENE SEQUENCE; HUMAN; LIGAND BINDING; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; REVIEW; SINGLE SITE SATURATION MUTAGENESIS; UBIQUITINATION; DEEP SEQUENCING; DNA SEQUENCE; GENE MUTATION; GENETIC PROCEDURES; MATHEMATICAL COMPUTING; MOLECULAR MODEL; MUTANT; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; GENE LIBRARY; GENETICS; HIGH THROUGHPUT SEQUENCING; PROCEDURES;

PROTEIN;

ANIMALS; GENE LIBRARY; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MODELS, MOLECULAR; MUTAGENESIS; PROTEINS;

EID: 84891899052     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.12.001     Document Type: Review

References (52)

1. Araya C.L., Fowler D.M. Deep mutational scanning: assessing protein function on a massive scale. Trends Biotechnol 2011, 29:435-442.
2. Fowler D.M., Araya C.L., Fleishman S.J., Kellogg E.H., Stephany J.J., Baker D., Fields S. High-resolution mapping of protein sequence-function relationships. Nat Methods 2010, 7:741-746.
3. Hietpas R., Roscoe B., Jiang L., Bolon D.N.A. Fitness analyses of all possible point mutations for regions of genes in yeast. Nat Protoc 2012, 7:1382-1396.
4. Hietpas R.T., Jensen J.D., Bolon D.N. Experimental illumination of a fitness landscape. Proc Natl Acad Sci U S A 2011, 108:7896-7901.
5. Jain P.C., Varadarajan R. A rapid, efficient and economical inverse PCR-based method for generating a Site-Saturation Mutant library. Analytical Biochemistry 2013, 10.1016/j.ab.2013.12.002.
6. Firnberg E., Ostermeier M. PFunkel: efficient, expansive, user-defined mutagenesis. PLoS ONE 2012, 7:e52031.
7. Tang L., Gao H., Zhu X., Wang X., Zhou M., Jiang R. Construction of "small-intelligent" focused mutagenesis libraries using well-designed combinatorial degenerate primers. Biotechniques 2012, 52:149-158.
8. Weiss G.A., Watanabe C.K., Zhong A., Goddard A., Sidhu S.S. Rapid mapping of protein functional epitopes by combinatorial alanine scanning. Proc Natl Acad Sci U S A 2000, 97:8950-8954.
9. Fields S., Song O. A novel genetic system to detect protein-protein interactions. Nature 1989, 340:245-246.
10. Karimova G., Pidoux J., Ullmann A., Ladant D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci U S A 1998, 95:5752-5756.
11. Weimann M., Grossmann A., Woodsmith J., Ozkan Z., Birth P., Meierhofer D., Benlasfer N., Valovka T., Timmermann B., Wanker E.E., et al. A Y2H-seq approach defines the human protein methyltransferase interactome. Nat Methods 2013, 10:339-342.
12. Foit L., Morgan G.J., Kern M.J., Steimer L.R., von Hacht A.A., Titchmarsh J., Warriner S.L., Radford S.E., Bardwell J.C. Optimizing protein stability in vivo. Mol Cell 2009, 36:861-871.
13. Cabantous S., Rogers Y., Terwilliger T.C., Waldo G.S. New molecular reporters for rapid protein folding assays. PLoS ONE 2008, 3:e2387.
14. Levin A.M., Weiss G.A. Optimizing the affinity and specificity of proteins with molecular display. Mol Biosyst 2006, 2:49-57.
15. Granieri L., Baret J.C., Griffiths A.D., Merten C.A. High-throughput screening of enzymes by retroviral display using droplet-based microfluidics. Chem Biol 2010, 17:229-235.
16. Colas P., Cohen B., Jessen T., Grishina I., McCoy J., Brent R. Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2. Nature 1996, 380:548-550.
17. Chen T.S., Palacios H., Keating A.E. Structure-based redesign of the binding specificity of anti-apoptotic Bcl-xL. J Mol Biol 2013, 425:171-185.
18. Tinberg C.E., Khare S.D., Dou J., Doyle L., Nelson J.W., Schena A., Jankowski W., Kalodimos C.G., Johnsson K., Stoddard B.L., et al. Computational design of ligand-binding proteins with high affinity and selectivity. Nature 2013, 501:212-216.
19. Araya C.L., Fowler D.M., Chen W., Muniez I., Kelly J.W., Fields S. A fundamental protein property, thermodynamic stability, revealed solely from large-scale measurements of protein function. Proc Natl Acad Sci U S A 2012, 109:16858-16863.
20. Roscoe B.P., Thayer K.M., Zeldovich K.B., Fushman D., Bolon D.N.A. Analyses of the effects of all ubiquitin point mutants on yeast growth rate. J Mol Biol 2013, 425:1363-1377.
21. Adkar B.V., Tripathi A., Sahoo A., Bajaj K., Goswami D., Chakrabarti P., Swarnkar M.K., Gokhale R.S., Varadarajan R. Protein model discrimination using mutational sensitivity derived from deep sequencing. Structure 2012, 20:371-381.
22. Deng Z., Huang W., Bakkalbasi E., Brown N.G., Adamski C.J., Rice K., Muzny D., Gibbs R.A., Palzkill T. Deep sequencing of systematic combinatorial libraries reveals β-lactamase sequence constraints at high resolution. J Mol Biol 2012, 424:150-167.
23. McLaughlin R.N., Poelwijk F.J., Raman A., Gosal W.S., Ranganathan R. The spatial architecture of protein function and adaptation. Nature 2012, 491:138-142.
24. Kinde I., Wu J., Papadopoulos N., Kinzler K.W., Vogelstein B. Detection and quantification of rare mutations with massively parallel sequencing. Proc Natl Acad Sci U S A 2011, 108:9530-9535.
25. Schmitt M.W., Kennedy S.R., Salk J.J., Fox E.J., Hiatt J.B., Loeb L.A. Detection of ultra-rare mutations by next-generation sequencing. Proc Natl Acad Sci U S A 2012, 109:14508-14513.
26. Pace C.N. Conformational stability of globular proteins. Trends Biochem Sci 1990, 15:14-17.
27. Starita L.M., Pruneda J.N., Lo R.S., Fowler D.M., Kim H.J., Hiatt J.B., Shendure J., Brzovic P.S., Fields S., Klevit R.E. Activity-enhancing mutations in an E3 ubiquitin ligase identified by high-throughput mutagenesis. Proc Natl Acad Sci U S A 2013, 110:E1263-E1272.
28. Schlinkmann K.M., Honegger A., Tureci E., Robison K.E., Lipovsek D., Pluckthun A. Critical features for biosynthesis, stability, and functionality of a G protein-coupled receptor uncovered by all-versus-all mutations. Proc Natl Acad Sci U S A 2012, 109:9810-9815.
29. Traxlmayr M.W., Hasenhindl C., Hackl M., Stadlmayr G., Rybka J.D., Borth N., Grillari J., Ruker F., Obinger C. Construction of a stability landscape of the CH3 domain of human IgG1 by combining directed evolution with high throughput sequencing. J Mol Biol 2012, 423:397-412.
30. Kim I., Miller C.R., Young D.L., Fields S. High-throughput analysis of in vivo protein stability. Mol Cell Proteomics 2013, 12:3370-3378.
31. Clackson T., Wells J.A. A hot spot of binding energy in a hormone-receptor interface. Science 1995, 267:383-386.
32. Bajaj K., Chakrabarti P., Varadarajan R. Mutagenesis-based definitions and probes of residue burial in proteins. Proc Natl Acad Sci U S A 2005, 102:16221-16226.
33. Moreira I.S., Fernandes P.A., Ramos M.J. Hot spots - a review of the protein-protein interface determinant amino-acid residues. Proteins 2007, 68:803-812.
34. Treynor T.P., Vizcarra C.L., Nedelcu D., Mayo S.L. Computationally designed libraries of fluorescent proteins evaluated by preservation and diversity of function. Proc Natl Acad Sci U S A 2007, 104:48-53.
35. DeBartolo J., Dutta S., Reich L., Keating A.E. Predictive Bcl-2 family binding models rooted in experiment or structure. J Mol Biol 2012, 422:124-144.
36. Dutta S., Chen T.S., Keating A.E. Peptide ligands for pro-survival protein Bfl-1 from computationally guided library screening. ACS Chem Biol 2013, 8:778-788.
37. Whitehead T.A., Chevalier A., Song Y., Dreyfus C., Fleishman S.J., De Mattos C., Myers C.A., Kamisetty H., Blair P., Wilson I.A., et al. Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing. Nat Biotechnol 2012, 30:543-548.
38. Tan K.P., Nguyen T.B., Patel S., Varadarajan R., Madhusudhan M.S. Depth: a web server to compute depth, cavity sizes, detect potential small-molecule ligand-binding cavities and predict the pKa of ionizable residues in proteins. Nucleic Acids Res 2013, 41:W314-W321.
39. Chakravarty S., Varadarajan R. Residue depth: a novel parameter for the analysis of protein structure and stability. Structure 1999, 7:723-732.
40. Moretti R., Fleishman S.J., Agius R., Torchala M., Bates P.A., Kastritis P.L., Rodrigues J.P., Trellet M., Bonvin A.M., Cui M., et al. Community-wide evaluation of methods for predicting the effect of mutations on protein-protein interactions. Proteins 2013, 81:1980-1987.
41. Mondal K., Dastidar A.G., Singh G., Madhusudhanan S., Gande S.L., VijayRaghavan K., Varadarajan R. Design and isolation of temperature-sensitive mutants of Gal4 in yeast and Drosophila. J Mol Biol 2007, 370:939-950.
42. Bajaj K., Dewan P.C., Chakrabarti P., Goswami D., Barua B., Baliga C., Varadarajan R. Structural correlates of the temperature sensitive phenotype derived from saturation mutagenesis studies of CcdB. Biochemistry 2008, 47:12964-12973.
43. Bershtein S., Mu W., Serohijos A.W., Zhou J., Shakhnovich E.I. Protein quality control acts on folding intermediates to shape the effects of mutations on organismal fitness. Mol Cell 2013, 49:133-144.
44. Bershtein S., Mu W., Shakhnovich E.I. Soluble oligomerization provides a beneficial fitness effect on destabilizing mutations. Proc Natl Acad Sci U S A 2012, 109:4857-4862.
45. Chrunyk B.A., Evans J., Lillquist J., Young P., Wetzel R. Inclusion body formation and protein stability in sequence variants of interleukin-1 beta. J Biol Chem 1993, 268:18053-18061.
46. Parsell D.A., Sauer R.T. Induction of a heat shock-like response by unfolded protein in Escherichia coli: dependence on protein level not protein degradation. Genes Dev 1989, 3:1226-1232.
47. Varshavsky A. The N-end rule pathway and regulation by proteolysis. Protein Sci 2011, 20:1298-1345.
48. Brodsky J.L. Cleaning up: ER-associated degradation to the rescue. Cell 2012, 151:1163-1167.
49. Melamed D., Young D.L., Gamble C.E., Miller C.R., Fields S. Deep mutational scanning of an RRM domain of the Saccharomyces cerevisiae poly(A)-binding protein. RNA 2013, 19:1537-1551.
50. Hinkley T., Martins J., Chappey C., Haddad M., Stawiski E., Whitcomb J.M., Petropoulos C.J., Bonhoeffer S. A systems analysis of mutational effects in HIV-1 protease and reverse transcriptase. Nat Genet 2011, 43:487-489.
51. Metzker M.L. Sequencing technologies - the next generation. Nat Rev Genet 2010, 11:31-46.
52. Liu L., Li Y., Li S., Hu N., He Y., Pong R., Lin D., Lu L., Law M. Comparison of next-generation sequencing systems. J Biomed Biotechnol 2012, 2012:251364.