Rewiring of PDZ Domain-Ligand Interaction Network Contributed to Eukaryotic Evolution

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PDZ domain-mediated interactions have greatly expanded during metazoan evolution, becoming important for controlling signal flow via the assembly of multiple signaling components. The evolutionary history of PDZ domain-mediated interactions has never been explored at the molecular level. It is of great interest to understand how PDZ domain-ligand interactions emerged and how they become rewired during evolution. Here, we constructed the first human PDZ domain-ligand interaction network (PDZNet) together with binding motif sequences and interaction strengths of ligands. PDZNet includes 1,213 interactions between 97 human PDZ proteins and 591 ligands that connect most PDZ protein-mediated interactions (98%) in a large single network via shared ligands. We examined the rewiring of PDZ domain-ligand interactions throughout eukaryotic evolution by tracing changes in the C-terminal binding motif sequences of the PDZ ligands. We found that interaction rewiring by sequence mutation frequently occurred throughout evolution, largely contributing to the growth of PDZNet. The rewiring of PDZ domain-ligand interactions provided an effective means of functional innovations in nervous system development. Our findings provide empirical evidence for a network evolution model that highlights the rewiring of interactions as a mechanism for the development of new protein functions. PDZNet will be a valuable resource to further characterize the organization of the PDZ domain-mediated signaling proteome.

Vyšlo v časopise: Rewiring of PDZ Domain-Ligand Interaction Network Contributed to Eukaryotic Evolution. PLoS Genet 8(2): e32767. doi:10.1371/journal.pgen.1002510
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002510

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Zdroje

1. GoodMCZalatanJGLimWA 2011 Scaffold proteins: hubs for controlling the flow of cellular information. Science 332 680 686

2. SakaryaOConacoCEgeciogluOSollaSAOakleyTH 2010 Evolutionary expansion and specialization of the PDZ domains. Mol Biol Evol 27 1058 1069

3. JinJXieXChenCParkJGStarkC 2009 Eukaryotic protein domains as functional units of cellular evolution. Sci Signal 2 ra76

4. BeltraoPSerranoL 2007 Specificity and evolvability in eukaryotic protein interaction networks. PLoS Comput Biol 3 e25 doi:10.1371/journal.pcbi.0030025

5. HeXZhangJ 2005 Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169 1157 1164

6. NeduvaVRussellRB 2005 Linear motifs: evolutionary interaction switches. FEBS Lett 579 3342 3345

7. WangXSommerRJ 2011 Antagonism of LIN-17/Frizzled and LIN-18/Ryk in Nematode Vulva Induction Reveals Evolutionary Alterations in Core Developmental Pathways. PLoS Biol 9 e1001110 doi:10.1371/journal.pbio.1001110

8. TanCSBodenmillerBPasculescuAJovanovicMHengartnerMO 2009 Comparative analysis reveals conserved protein phosphorylation networks implicated in multiple diseases. Sci Signal 2 ra39

9. BeltraoPTrinidadJCFiedlerDRoguevALimWA 2009 Evolution of phosphoregulation: comparison of phosphorylation patterns across yeast species. PLoS Biol 7 e1000134 doi:10.1371/journal.pbio.1000134

10. KimDSHahnY 2011 Identification of novel phosphorylation modification sites in human proteins that originated after the human-chimpanzee divergence. Bioinformatics

11. AloyPRussellRB 2006 Structural systems biology: modelling protein interactions. Nat Rev Mol Cell Biol 7 188 197

12. KimPMLuLJXiaYGersteinMB 2006 Relating three-dimensional structures to protein networks provides evolutionary insights. Science 314 1938 1941

13. MoscaRPonsCFernandez-RecioJAloyP 2009 Pushing structural information into the yeast interactome by high-throughput protein docking experiments. PLoS Comput Biol 5 e1000490 doi:10.1371/journal.pcbi.1000490

14. SteinAAloyP 2008 Contextual specificity in peptide-mediated protein interactions. PLoS ONE 3 e2524 doi:10.1371/journal.pone.0002524

15. BarabasiALOltvaiZN 2004 Network biology: understanding the cell's functional organization. Nat Rev Genet 5 101 113

16. RamaniAKLiZHartGTCarlsonMWBoutzDR 2008 A map of human protein interactions derived from co-expression of human mRNAs and their orthologs. Mol Syst Biol 4 180

17. LageKKarlbergEOStorlingZMOlasonPIPedersenAG 2007 A human phenome-interactome network of protein complexes implicated in genetic disorders. Nat Biotechnol 25 309 316

18. StifflerMAChenJRGrantcharovaVPLeiYFuchsD 2007 PDZ domain binding selectivity is optimized across the mouse proteome. Science 317 364 369

19. VaccaroPBrannettiBMontecchi-PalazziLPhilippSHelmer CitterichM 2001 Distinct binding specificity of the multiple PDZ domains of INADL, a human protein with homology to INAD from Drosophila melanogaster. J Biol Chem 276 42122 42130

20. TonikianRZhangYSazinskySLCurrellBYehJH 2008 A specificity map for the PDZ domain family. PLoS Biol 6 e239 doi:10.1371/journal.pbio.0060239

21. BeumingTSkrabanekLNivMYMukherjeePWeinsteinH 2005 PDZBase: a protein-protein interaction database for PDZ-domains. Bioinformatics 21 827 828

22. WesPDXuXZLiHSChienFDobersteinSK 1999 Termination of phototransduction requires binding of the NINAC myosin III and the PDZ protein INAD. Nat Neurosci 2 447 453

23. van HuizenRMillerKChenDMLiYLaiZC 1998 Two distantly positioned PDZ domains mediate multivalent INAD-phospholipase C interactions essential for G protein-coupled signaling. EMBO J 17 2285 2297

24. HarrisBZLimWA 2001 Mechanism and role of PDZ domains in signaling complex assembly. J Cell Sci 114 3219 3231

25. GislerSMKittanakomSFusterDWongVBerticM 2008 Monitoring protein-protein interactions between the mammalian integral membrane transporters and PDZ-interacting partners using a modified split-ubiquitin membrane yeast two-hybrid system. Mol Cell Proteomics 7 1362 1377

26. WiedemannUBoisguerinPLebenRLeitnerDKrauseG 2004 Quantification of PDZ domain specificity, prediction of ligand affinity and rational design of super-binding peptides. J Mol Biol 343 703 718

27. PiserchioAPellegriniMMehtaSBlackmanSMGarciaEP 2002 The PDZ1 domain of SAP90. Characterization of structure and binding. J Biol Chem 277 6967 6973

28. GfellerDButtyFWierzbickaMVerschuerenEVanheeP 2011 The multiple-specificity landscape of modular peptide recognition domains. Mol Syst Biol 7 484

29. EmesRDPocklingtonAJAndersonCNBayesACollinsMO 2008 Evolutionary expansion and anatomical specialization of synapse proteome complexity. Nat Neurosci 11 799 806

30. WapinskiIPfefferAFriedmanNRegevA 2007 Natural history and evolutionary principles of gene duplication in fungi. Nature 449 54 61

31. JaffreySRSnowmanAMEliassonMJCohenNASnyderSH 1998 CAPON: a protein associated with neuronal nitric oxide synthase that regulates its interactions with PSD95. Neuron 20 115 124

32. SalwinskiLMillerCSSmithAJPettitFKBowieJU 2004 The Database of Interacting Proteins: 2004 update. Nucleic Acids Res 32 D449 451

33. StarkCBreitkreutzBJChatr-AryamontriABoucherLOughtredR 2011 The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 39 D698 704

34. YuJPacificoSLiuGFinleyRLJr 2008 DroID: the Drosophila Interactions Database, a comprehensive resource for annotated gene and protein interactions. BMC genomics 9 461

35. YamadaTBorkP 2009 Evolution of biomolecular networks: lessons from metabolic and protein interactions. Nat Rev Mol Cell Biol 10 791 803

36. RadziwillGErdmannRAMargelischUMoellingK 2003 The Bcr kinase downregulates Ras signaling by phosphorylating AF-6 and binding to its PDZ domain. Mol Cell Biol 23 4663 4672

37. ZhouHXuYYangYHuangAWuJ 2005 Solution structure of AF-6 PDZ domain and its interaction with the C-terminal peptides from Neurexin and Bcr. J Biol Chem 280 13841 13847

38. EloweSHollandSJKulkarniSPawsonT 2001 Downregulation of the Ras-mitogen-activated protein kinase pathway by the EphB2 receptor tyrosine kinase is required for ephrin-induced neurite retraction. Mol Cell Biol 21 7429 7441

39. NorenNKPasqualeEB 2004 Eph receptor-ephrin bidirectional signals that target Ras and Rho proteins. Cell Signal 16 655 666

40. SansNPrybylowskiKPetraliaRSChangKWangYX 2003 NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat Cell Biol 5 520 530

41. HamoshAScottAFAmbergerJSBocchiniCAMcKusickVA 2005 Online Mendelian Inheritance in Man (OMIM), a knowledgebase of human genes and genetic disorders. Nucleic Acids Res 33 D514 517

42. GohKICusickMEValleDChildsBVidalM 2007 The human disease network. Proc Natl Acad Sci U S A 104 8685 8690

43. JamainSQuachHBetancurCRastamMColineauxC 2003 Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34 27 29

44. YamakawaHOyamaSMitsuhashiHSasagawaNUchinoS 2007 Neuroligins 3 and 4X interact with syntrophin-gamma2, and the interactions are affected by autism-related mutations. Biochem Biophys Res Commun 355 41 46

45. LaumonnierFBonnet-BrilhaultFGomotMBlancRDavidA 2004 X-linked mental retardation and autism are associated with a mutation in the NLGN4 gene, a member of the neuroligin family. Am J Hum Genet 74 552 557

46. ScottJDPawsonT 2009 Cell signaling in space and time: where proteins come together and when they're apart. Science 326 1220 1224

47. KitanoH 2004 Biological robustness. Nat Rev Genet 5 826 837

48. VavouriTSempleJIGarcia-VerdugoRLehnerB 2009 Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 138 198 208

49. OhnoSWolfUAtkinNB 1968 Evolution from fish to mammals by gene duplication. Hereditas 59 169 187

50. BertasoFZhangCScheschonkaAde BockFFontanaudP 2008 PICK1 uncoupling from mGluR7a causes absence-like seizures. Nat Neurosci 11 940 948

51. VidalMCusickMEBarabasiAL 2011 Interactome networks and human disease. Cell 144 986 998

52. HockBBohmeBKarnTYamamotoTKaibuchiK 1998 PDZ-domain-mediated interaction of the Eph-related receptor tyrosine kinase EphB3 and the ras-binding protein AF6 depends on the kinase activity of the receptor. Proc Natl Acad Sci U S A 95 9779 9784

53. SonnhammerELEddySRBirneyEBatemanADurbinR 1998 Pfam: multiple sequence alignments and HMM-profiles of protein domains. Nucleic Acids Res 26 320 322

54. RanganathanRRossEM 1997 PDZ domain proteins: scaffolds for signaling complexes. Curr Biol 7 R770 773

55. ChenJRChangBHAllenJEStifflerMAMacBeathG 2008 Predicting PDZ domain-peptide interactions from primary sequences. Nat Biotechnol 26 1041 1045

56. YaffeMBLeparcGGLaiJObataTVoliniaS 2001 A motif-based profile scanning approach for genome-wide prediction of signaling pathways. Nat Biotechnol 19 348 353

57. FauchereJLChartonMKierLBVerloopAPliskaV 1988 Amino acid side chain parameters for correlation studies in biology and pharmacology. Int J Pept Protein Res 32 269 278

58. GranthamR 1974 Amino acid difference formula to help explain protein evolution. Science 185 862 864

59. ZimmermanJMEliezerNSimhaR 1968 The characterization of amino acid sequences in proteins by statistical methods. J Theor Biol 21 170 201

60. ArgosPRaoJKHargravePA 1982 Structural prediction of membrane-bound proteins. Eur J Biochem 128 565 575

61. CosicI 1994 Macromolecular bioactivity: is it resonant interaction between macromolecules?–Theory and applications. IEEE Trans Biomed Eng 41 1101 1114

62. ChartonMChartonBI 1982 The structural dependence of amino acid hydrophobicity parameters. J Theor Biol 99 629 644

63. EddySR 1998 Profile hidden Markov models. Bioinformatics 14 755 763

64. D'HaeseleerP 2006 What are DNA sequence motifs? Nat Biotechnol 24 423 425

65. StormoGDHartzellGW3rd 1989 Identifying protein-binding sites from unaligned DNA fragments. Proc Natl Acad Sci U S A 86 1183 1187

66. BrombergKDMa'ayanANevesSRIyengarR 2008 Design logic of a cannabinoid receptor signaling network that triggers neurite outgrowth. Science 320 903 909

67. ParkSYangJ-sShinY-eParkJJangSK 2011 Protein localization as a principal feature of the etiology and comorbidity of genetic diseases. Molecular Systems Biology 7 1 11

68. Huang daWShermanBTLempickiRA 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4 44 57

69. LundbergEFagerbergLKlevebringDMaticIGeigerT 2010 Defining the transcriptome and proteome in three functionally different human cell lines. Mol Syst Biol 6 450