Widespread macromolecular interaction perturbations in human genetic disorders

Cell

Volumn 161, Issue 3, 2015, Pages 647-660

  Sahni, Nidhi ^a,b   Yi, Song ^a,b   Taipale, Mikko ^c   Fuxman Bass, Juan I ^d   Coulombe Huntington, Jasmin ^e   Yang, Fan ^a,f,g,h   Peng, Jian ⁱ   Weile, Jochen ^a,f,g,h   Karras, Georgios I ^c   Wang, Yang ^a,b   Kovács, István A ^a,j   Kamburov, Atanas ^a,b   Krykbaeva, Irina ^c   Lam, Mandy H ^g   Tucker, George ⁱ   Khurana, Vikram ^c   Sharma, Amitabh ^a,j   Liu, Yang Yu ^a,j   Yachie, Nozomu ^a,f,g,h   Zhong, Quan ^a,b   Shen, Yun ^a,b   Palagi, Alexandre ^a,b   San Miguel, Adriana ^a,b   Fan, Changyu ^a,b   Balcha, Dawit ^a,b   Dricot, Amelie ^a,b   Jordan, Daniel M ^b,k   Walsh, Jennifer M ^a,b   Shah, Akash A ^a,b   Yang, Xinping ^a,b   Stoyanova, Ani K ^a,b   Leighton, Alex ⁱ   Calderwood, Michael A ^a,b   Jacob, Yves ^a,b,l   Cusick, Michael E ^a,b   Salehi Ashtiani, Kourosh ^a,b   Whitesell, Luke J ^c,m   Sunyaev, Shamil ^b,n   Berger, Bonnie ^i,m   Barabási, Albert László ^a,b,j   Charloteaux, Benoit ^a,b   Hill, David E ^a,b   Hao, Tong ^a,b   Roth, Frederick P ^a,f,g,h,o   Xia, Yu ^a,e   Walhout, Albertha J M ^a,d   Lindquist, Susan ^c,m,p   Vidal, Marc ^a,b   more..

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e MCGILL UNIVERSITY   (Canada)

^f UNIVERSITY OF TORONTO   (Canada)

^g UNIVERSITY OF TORONTO   (Canada)

^h MOUNT SINAI HOSPITAL   (Canada)

ⁱ MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^j NORTHEASTERN UNIVERSITY   (United States)

^k HARVARD UNIVERSITY   (United States)

^l INSTITUT PASTEUR   (France)

^m MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

ⁿ BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^o CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^p HOWARD HUGHES MEDICAL INSTITUTE   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; CONTROLLED STUDY; GENETIC DISORDER; GENOTYPE PHENOTYPE CORRELATION; HEK293 CELL LINE; HUMAN; HUMAN CELL; MACROMOLECULE; MISSENSE MUTATION; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; DISEASES; GENETIC ASSOCIATION; GENETICS; METABOLISM; OPEN READING FRAME;

DNA BINDING PROTEIN; PROTEIN;

DISEASE; DNA-BINDING PROTEINS; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MUTATION, MISSENSE; OPEN READING FRAMES; PROTEIN FOLDING; PROTEIN INTERACTION MAPS; PROTEIN STABILITY; PROTEINS;

EID: 84928389942     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.04.013     Document Type: Article

References (70)

1. 1000 Genomes Project Consortium G.R. Abecasis, A. Auton, L.D. Brooks, M.A. DePristo, R.M. Durbin, R.E. Handsaker, H.M. Kang, G.T. Marth, and G.A. McVean An integrated map of genetic variation from 1,092 human genomes Nature 491 2012 56 65
2. I.A. Adzhubei, S. Schmidt, L. Peshkin, V.E. Ramensky, A. Gerasimova, P. Bork, A.S. Kondrashov, and S.R. Sunyaev A method and server for predicting damaging missense mutations Nat. Methods 7 2010 248 249
3. J. Amberger, C. Bocchini, and A. Hamosh A new face and new challenges for Online Mendelian Inheritance in Man (OMIM) Hum. Mutat. 32 2011 564 567
4. S. Balasubramanian, Y. Xia, E. Freinkman, and M. Gerstein Sequence variation in G-protein-coupled receptors: analysis of single nucleotide polymorphisms Nucleic Acids Res. 33 2005 1710 1721
5. P. Braun, M. Tasan, M. Dreze, M. Barrios-Rodiles, I. Lemmens, H. Yu, J.M. Sahalie, R.R. Murray, L. Roncari, and A.-S. de Smet An experimentally derived confidence score for binary protein-protein interactions Nat. Methods 6 2009 91 97
6. J.D. Carpten, A.L. Faber, C. Horn, G.P. Donoho, S.L. Briggs, C.M. Robbins, G. Hostetter, S. Boguslawski, T.Y. Moses, and S. Savage A transforming mutation in the pleckstrin homology domain of AKT1 in cancer Nature 448 2007 439 444
7. P. Cassonnet, C. Rolloy, G. Neveu, P.O. Vidalain, T. Chantier, J. Pellet, L. Jones, M. Muller, C. Demeret, and G. Gaud Benchmarking a luciferase complementation assay for detecting protein complexes Nat. Methods 8 2011 990 992
8. L. Chin, W.C. Hahn, G. Getz, and M. Meyerson Making sense of cancer genomic data Genes Dev. 25 2011 534 555
9. N.F. Clarke, H. Kolski, D.E. Dye, E. Lim, R.L. Smith, R. Patel, M.C. Fahey, R. Bellance, N.B. Romero, and E.S. Johnson Mutations in TPM3 are a common cause of congenital fiber type disproportion Ann. Neurol. 63 2008 329 337
10. W. de Nooy, A. Mrvar, and V. Batagelj Exploratory Social Network Analysis with Pajek 2005 Cambridge University Press
11. S.F. Falsone, S. Leptihn, A. Osterauer, M. Haslbeck, and J. Buchner Oncogenic mutations reduce the stability of SRC kinase J. Mol. Biol. 344 2004 281 291
12. A. Flora, J.J. Garcia, C. Thaller, and H.Y. Zoghbi The E-protein Tcf4 interacts with Math1 to regulate differentiation of a specific subset of neuronal progenitors Proc. Natl. Acad. Sci. USA 104 2007 15382 15387
13. J.I. Fuxman Bass, N. Sahni, S. Shrestha, A. Garcia-Gonzalez, A. Mori, N. Bhat, S. Yi, D.E. Hill, M. Vidal, and A.J.M. Walhout Human Gene-Centered Transcription Factor Networks for Enhancers and Disease Variants Cell 161 2015 661 673 this issue
14. B. Gerull, A. Heuser, T. Wichter, M. Paul, C.T. Basson, D.A. McDermott, B.B. Lerman, S.M. Markowitz, P.T. Ellinor, and C.A. MacRae Mutations in the desmosomal protein plakophilin-2 are common in arrhythmogenic right ventricular cardiomyopathy Nat. Genet. 36 2004 1162 1164
15. K.I. Goh, M.E. Cusick, D. Valle, B. Childs, M. Vidal, and A.L. Barabási The human disease network Proc. Natl. Acad. Sci. USA 104 2007 8685 8690
16. K.W. Gripp, D. Wotton, M.C. Edwards, E. Roessler, L. Ades, P. Meinecke, A. Richieri-Costa, E.H. Zackai, J. Massagué, M. Muenke, and S.J. Elledge Mutations in TGIF cause holoprosencephaly and link NODAL signalling to human neural axis determination Nat. Genet. 25 2000 205 208
17. R. Guerois, J.E. Nielsen, and L. Serrano Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations J. Mol. Biol. 320 2002 369 387
18. P. Gunning, M. Gordon, R. Wade, R. Gahlmann, C.S. Lin, and E. Hardeman Differential control of tropomyosin mRNA levels during myogenesis suggests the existence of an isoform competition-autoregulatory compensation control mechanism Dev. Biol. 138 1990 443 453
19. L.A. Hindorff, P. Sethupathy, H.A. Junkins, E.M. Ramos, J.P. Mehta, F.S. Collins, and T.A. Manolio Potential etiologic and functional implications of genome-wide association loci for human diseases and traits Proc. Natl. Acad. Sci. USA 106 2009 9362 9367
20. R.P. Huntley, T. Sawford, P. Mutowo-Meullenet, A. Shypitsyna, C. Bonilla, M.J. Martin, and C. O'Donovan The GOA database: gene Ontology annotation updates for 2015 Nucleic Acids Res. 43 2015 D1057 D1063
21. I. Köllner, B. Sodeik, S. Schreek, H. Heyn, N. von Neuhoff, M. Germeshausen, C. Zeidler, M. Krüger, B. Schlegelberger, K. Welte, and C. Beger Mutations in neutrophil elastase causing congenital neutropenia lead to cytoplasmic protein accumulation and induction of the unfolded protein response Blood 108 2006 493 500
22. N.G. Laing, S.D. Wilton, P.A. Akkari, S. Dorosz, K. Boundy, C. Kneebone, P. Blumbergs, S. White, H. Watkins, and D.R. Love A mutation in the alpha tropomyosin gene TPM3 associated with autosomal dominant nemaline myopathy Nat. Genet. 9 1995 75 79
23. M.J. Landrum, J.M. Lee, G.R. Riley, W. Jang, W.S. Rubinstein, D.M. Church, and D.R. Maglott ClinVar: public archive of relationships among sequence variation and human phenotype Nucleic Acids Res. 42 2014 D980 D985
24. Y. Lee, I. Hur, S.Y. Park, Y.K. Kim, M.R. Suh, and V.N. Kim The role of PACT in the RNA silencing pathway EMBO J. 25 2006 522 532
25. S. Lesage, and A. Brice Parkinson's disease: from monogenic forms to genetic susceptibility factors Hum. Mol. Genet. 18 R1 2009 R48 R59
26. A. McArdle, C.S. Broome, A.C. Kayani, M.D. Tully, G.L. Close, A. Vasilaki, and M.J. Jackson HSF expression in skeletal muscle during myogenesis: implications for failed regeneration in old mice Exp. Gerontol. 41 2006 497 500
27. J.S. Reece-Hoyes, A.R. Barutcu, R.P. McCord, J.S. Jeong, L. Jiang, A. MacWilliams, X. Yang, K. Salehi-Ashtiani, D.E. Hill, and S. Blackshaw Yeast one-hybrid assays for gene-centered human gene regulatory network mapping Nat. Methods 8 2011 1050 1052
28. J.S. Reece-Hoyes, A. Diallo, B. Lajoie, A. Kent, S. Shrestha, S. Kadreppa, C. Pesyna, J. Dekker, C.L. Myers, and A.J. Walhout Enhanced yeast one-hybrid assays for high-throughput gene-centered regulatory network mapping Nat. Methods 8 2011 1059 1064
29. B. Reva, Y. Antipin, and C. Sander Predicting the functional impact of protein mutations: application to cancer genomics Nucleic Acids Res. 39 2011 e118
30. T. Rolland, M. Taşan, B. Charloteaux, S.J. Pevzner, Q. Zhong, N. Sahni, S. Yi, I. Lemmens, C. Fontanillo, and R. Mosca A proteome-scale map of the human interactome network Cell 159 2014 1212 1226
31. J.F. Rual, T. Hirozane-Kishikawa, T. Hao, N. Bertin, S. Li, A. Dricot, N. Li, J. Rosenberg, P. Lamesch, and P.O. Vidalain Human ORFeome version 1.1: a platform for reverse proteomics Genome Res. 14 10B 2004 2128 2135
32. N. Sahni, S. Yi, Q. Zhong, N. Jailkhani, B. Charloteaux, M.E. Cusick, and M. Vidal Edgotype: a fundamental link between genotype and phenotype Curr. Opin. Genet. Dev. 23 2013 649 657
33. J. Schymkowitz, J. Borg, F. Stricher, R. Nys, F. Rousseau, and L. Serrano The FoldX web server: an online force field Nucleic Acids Res. 33 2005 W382 W388
34. T. Shimamura, A.M. Lowell, J.A. Engelman, and G.I. Shapiro Epidermal growth factor receptors harboring kinase domain mutations associate with the heat shock protein 90 chaperone and are destabilized following exposure to geldanamycins Cancer Res. 65 2005 6401 6408
35. K. Sörgjerd, B. Ghafouri, B.H. Jonsson, J.W. Kelly, S.Y. Blond, and P. Hammarström Retention of misfolded mutant transthyretin by the chaperone BiP/GRP78 mitigates amyloidogenesis J. Mol. Biol. 356 2006 469 482
36. P.D. Stenson, M. Mort, E.V. Ball, K. Shaw, A. Phillips, and D.N. Cooper The Human Gene Mutation Database: building a comprehensive mutation repository for clinical and molecular genetics, diagnostic testing and personalized genomic medicine Hum. Genet. 133 2014 1 9
37. S. Subramanian, and S. Kumar Evolutionary anatomies of positions and types of disease-associated and neutral amino acid mutations in the human genome BMC Genomics 7 2006 306
38. S.R. Sunyaev Inferring causality and functional significance of human coding DNA variants Hum. Mol. Genet. 21 R1 2012 R10 R17
39. M. Taipale, I. Krykbaeva, M. Koeva, C. Kayatekin, K.D. Westover, G.I. Karras, and S. Lindquist Quantitative analysis of HSP90-client interactions reveals principles of substrate recognition Cell 150 2012 987 1001
40. M. Taipale, G. Tucker, J. Peng, I. Krykbaeva, Z.Y. Lin, B. Larsen, H. Choi, B. Berger, A.C. Gingras, and S. Lindquist A quantitative chaperone interaction network reveals the architecture of cellular protein homeostasis pathways Cell 158 2014 434 448
41. M.H. Tervaniemi, H.A. Siitonen, C. Söderhäll, G. Minhas, J. Vuola, I. Tiala, R. Sormunen, L. Samuelsson, S. Suomela, J. Kere, and O. Elomaa Centrosomal localization of the psoriasis candidate gene product, CCHCR1, supports a role in cytoskeletal organization PLoS ONE 7 2012 e49920
42. K. Venkatesan, J.F. Rual, A. Vazquez, U. Stelzl, I. Lemmens, T. Hirozane-Kishikawa, T. Hao, M. Zenkner, X. Xin, and K.I. Goh An empirical framework for binary interactome mapping Nat. Methods 6 2009 83 90
43. M. Vidal, M.E. Cusick, and A.L. Barabási Interactome networks and human disease Cell 144 2011 986 998
44. A. Visel, S. Minovitsky, I. Dubchak, and L.A. Pennacchio VISTA Enhancer Browser - a database of tissue-specific human enhancers Nucleic Acids Res. 35 2007 D88 D92
45. L. Whitesell, and S.L. Lindquist HSP90 and the chaperoning of cancer Nat. Rev. Cancer 5 2005 761 772
46. D. Yamashita, Y. Sano, Y. Adachi, Y. Okamoto, H. Osada, T. Takahashi, T. Yamaguchi, T. Osumi, and F. Hirose hDREF regulates cell proliferation and expression of ribosomal protein genes Mol. Cell. Biol. 27 2007 2003 2013
47. X. Yang, J.S. Boehm, X. Yang, K. Salehi-Ashtiani, T. Hao, Y. Shen, R. Lubonja, S.R. Thomas, O. Alkan, and T. Bhimdi A public genome-scale lentiviral expression library of human ORFs Nat. Methods 8 2011 659 661
48. Q. Zhong, N. Simonis, Q.R. Li, B. Charloteaux, F. Heuze, N. Klitgord, S. Tam, H. Yu, K. Venkatesan, and D. Mou Edgetic perturbation models of human inherited disorders Mol. Syst. Biol. 5 2009 321
49. C.A. Andersen, A.G. Palmer, S. Brunak, and B. Rost Continuum secondary structure captures protein flexibility Structure 10 2002 175 184
50. J.H. Bullard, E. Purdom, K.D. Hansen, and S. Dudoit Evaluation of statistical methods for normalization and differential expression in mRNA-Seq experiments BMC Bioinformatics 11 2010 94
51. Z. Dosztányi, V. Csizmok, P. Tompa, and I. Simon IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content Bioinformatics 21 2005 3433 3434
52. M. Dreze, D. Monachello, C. Lurin, M.E. Cusick, D.E. Hill, M. Vidal, and P. Braun High-quality binary interactome mapping Methods Enzymol. 470 2010 281 315
53. R.D. Finn, J. Clements, and S.R. Eddy HMMER web server: interactive sequence similarity searching Nucleic Acids Res. 39 2011 W29 W37
54. K. Heise, H. Oppermann, J. Meixensberger, R. Gebhardt, and F. Gaunitz Dual luciferase assay for secreted luciferases based on Gaussia and NanoLuc Assay Drug Dev. Technol. 11 2013 244 252
55. M. Källberg, H. Wang, S. Wang, J. Peng, Z. Wang, H. Lu, and J. Xu Template-based protein structure modeling using the RaptorX web server Nat. Protoc. 7 2012 1511 1522
56. H.J. Kang, Y.I. Kawasawa, F. Cheng, Y. Zhu, X. Xu, M. Li, A.M. Sousa, M. Pletikos, K.A. Meyer, and G. Sedmak Spatio-temporal transcriptome of the human brain Nature 478 2011 483 489
57. W.J. Kent BLAT - the BLAST-like alignment tool Genome Res. 12 2002 656 664
58. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
59. B. Langmead, and S.L. Salzberg Fast gapped-read alignment with Bowtie 2 Nat. Methods 9 2012 357 359
60. M.A. Larkin, G. Blackshields, N.P. Brown, R. Chenna, P.A. McGettigan, H. McWilliam, F. Valentin, I.M. Wallace, A. Wilm, and R. Lopez Clustal W and Clustal X version 2.0 Bioinformatics 23 2007 2947 2948
61. B. Lee, and F.M. Richards The interpretation of protein structures: estimation of static accessibility J. Mol. Biol. 55 1971 379 400
62. R. Mosca, A. Céol, and P. Aloy Interactome3D: adding structural details to protein networks Nat. Methods 10 2013 47 53
63. J.S. Reece-Hoyes, C. Pons, A. Diallo, A. Mori, S. Shrestha, S. Kadreppa, J. Nelson, S. Diprima, A. Dricot, and B.R. Lajoie Extensive rewiring and complex evolutionary dynamics in a C. elegans multiparameter transcription factor network Mol. Cell 51 2013 116 127
64. I. Remy, and S.W. Michnick A highly sensitive protein-protein interaction assay based on Gaussia luciferase Nat. Methods 3 2006 977 979
65. P.W. Rose, C. Bi, W.F. Bluhm, C.H. Christie, D. Dimitropoulos, S. Dutta, R.K. Green, D.S. Goodsell, A. Prlic, and M. Quesada The RCSB Protein Data Bank: new resources for research and education Nucleic Acids Res. 41 2013 D475 D482
66. A.I. Saeed, N.K. Bhagabati, J.C. Braisted, W. Liang, V. Sharov, E.A. Howe, J. Li, M. Thiagarajan, J.A. White, and J. Quackenbush TM4 microarray software suite Methods Enzymol. 411 2006 134 193
67. M.F. Sanner, A.J. Olson, and J.C. Spehner Reduced surface: an efficient way to compute molecular surfaces Biopolymers 38 1996 305 320
68. UniProt Consortium Activities at the Universal Protein Resource (UniProt) Nucleic Acids Res. 42 2014 D191 D198
69. A.J. Walhout, and M. Vidal A genetic strategy to eliminate self-activator baits prior to high-throughput yeast two-hybrid screens Genome Res. 9 1999 1128 1134
70. A.Y. Yam, Y. Xia, H.T. Lin, A. Burlingame, M. Gerstein, and J. Frydman Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies Nat. Struct. Mol. Biol. 15 2008 1255 1262