An evolutionary roadmap to the microtubule-associated protein MAP Tau

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Sündermann, Frederik ^a   Fernandez, Maria Pilar ^b   Morgan, Reginald O ^b  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

^b UNIVERSITY OF OVIEDO   (Spain)

Author keywords

Domain architecture; Gene phylogeny; MAPT gene); Microtubule associated protein Tau (MAPT protein; Microtubule binding domain; Molecular evolution; Profile hidden Markov models; Saitohin (STH); Structure function prediction

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 2; MICROTUBULE ASSOCIATED PROTEIN 4; TAU PROTEIN;

ARTICLE; CHROMOSOME DUPLICATION; EXON; GENE; HAGFISH; HIDDEN MARKOV MODEL; INTRON; KANSL GENE; KANSL1L GENE; LAMPREY; MICROTUBULE BINDING DOMAIN; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIMATE; PROTEIN DOMAIN; PROTEIN INTERACTION; SAITOHIN GENE; ANIMAL; BAYES THEOREM; BINDING SITE; GENETICS; HUMAN; MARKOV CHAIN; MULTIGENE FAMILY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; STATISTICAL MODEL;

ANIMALS; BAYES THEOREM; BINDING SITES; EVOLUTION, MOLECULAR; HUMANS; LIKELIHOOD FUNCTIONS; MARKOV CHAINS; MULTIGENE FAMILY; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TAU PROTEINS;

EID: 85007593131     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2590-9     Document Type: Article

References (81)

1. Derisbourg M, Leghay C, Chiapetta G, Fernandez-Gomez FJ, Laurent C, Demeyer D, Carrier S, Buée-Scherrer V, Blum D, Vinh J, Sergeant N, Verdier Y, Buée L, Hamdane M. Role of the Tau N-terminal region in microtubule stabilization revealed by new endogenous truncated forms. Sci Rep. 2015;5:9659.
2. Dehmelt L, Halpain S. The MAP2/Tau family of microtubule-associated proteins. Genome Biol. 2005;6:1-10.
3. Fichou Y, Heyden M, Zaccai G, Weik M, Tobias DJ. Molecular dynamics simulations of a powder model of the intrinsically disordered protein Tau. J Phys Chem B. 2015; doi:10.1021/acs.jpcb.5b05849
4. Li XH, Culver JA, Rhoades E. Tau binds to multiple tubulin dimers with helical structure. J Am Chem Soc. 2015;Jul 12. doi:10.1021/jacs.5b04561.
5. Wright PE, Dyson HJ. Intrinsically disordered proteins in cellular signalling and regulation. Nat Publ Gr. 2015;16:18-29.
6. Kadavath H, Jaremko M, Jaremko L, Biernat J, Mandelkow E, Zweckstetter M. Folding of the tau protein on microtubules. Angew Chem Int Ed Engl. 2015;54:10347-51.
7. Avila J, Lucas JJ, Perez M, Hernandez F. Role of tau protein in both physiological and pathological conditions. Physiol Rev. 2004;84:361-84.
8. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, et al. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell. 2010;142:387-97.
9. Morris M, Maeda S, Vossel K, Mucke L. The many faces of tau. Neuron. 2011;70:410-26.
10. Fontaine SN, Sabbagh JJ, Baker J, Martinez-Licha CR, Darling A, Dickey CA. Cellular factors modulating the mechanism of tau protein aggregation. Cell Mol Life Sci. 2015;72:1863-79.
11. Shahani N, Subramaniam S, Wolf T, Tackenberg C, Brandt R. Tau aggregation and progressive neuronal degeneration in the absence of changes in spine density and morphology after targeted expression of Alzheimer's disease-relevant tau constructs in organotypic hippocampal slices. J Neurosci. 2006;26:6103-14.
12. Andreadis A. Tau splicing and the intricacies of dementia. J Cell Physiol. 2012;227:1220-5.
13. Caillet-Boudin ML, Buée L, Sergeant N, Lefebvre B. Regulation of human MAPT gene expression. Mol Neurodegener. 2015;10:28.
14. Mandelkow EM, Mandelkow E. Biochemistry and cell biology of Tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Biol. 2011;3:1-25.
15. Shaw-Smith C, Pittman AM, Willatt L, Martin H, Rickman L, Gribble S, et al. Microdeletion encompassing MAPT at chromosome 17q21.3 is associated with developmental delay and learning disability. Nat Genet. 2006;38:1032-7.
16. Dubourg C, Sanlaville D, Doco-Fenzy M, Le Caignec C, Missirian C, Jaillard S, et al. Clinical and molecular characterization of 17q21.31 microdeletion syndrome in 14 French patients with mental retardation. Eur J Med Genet. 2011;54:144-51.
17. Cookson MR. Evolution of neurodegeneration. Curr Biol. 2012;22:R753-61.
18. Elbaum-Garfinkle S, Rhoades E. Identification of an aggregation-prone structure of tau. J Am Chem Soc. 2012;134:16607-13.
19. Moss SE, Morgan RO. The annexins. (protein family review). Genome Biol. 2004;5:219.1-8.
20. Morgan RO, Martin-Almedina S, Garcia M, Jhoncon-Kooyip J, Fernández MP. Deciphering function and mechanism of calcium-binding proteins from their evolutionary imprints. Biochim Biophys Acta. 1763;2006:1238-49.
21. Morgan RO, Fernández M. Molecular phylogeny and evolution of the coronin gene family. In: Clemen CS, Eichinger L, Rybakin V, editors. The Coronin Family of Proteins. Austin, New York: Landes Bioscience and Springer Science; 2008. p. 41-55. Subcell Biochem. 2008;48:41-55.
22. Clark GB, Morgan RO, Fernandez MP, Roux SJ. Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytol. 2012;196:695-712.
23. Ramachandran G, Udgaonkar JB. Mechanistic studies unravel the complexity inherent in tau aggregation leading to Alzheimer's disease and the tauopathies. Biochemistry. 2013;52:4107-26.
24. Janning D, Igaev M, Sundermann F, Bruhmann J, Beutel O, Heinisch JJ, Bakota L, Piehler J, Junge W, Brandt R. Single-molecule tracking of tau reveals fast kiss-and-hop interaction with microtubules in living neurons. Mol Biol Cell. 2014;25:3541-51.
25. National Center for Biotechnology Information (NCBI). http://www.ncbi.nlm. nih.gov/. Accessed 15 Sep 2015.
26. Itsara A, Vissers LELM, Steinberg KM, Meyer KJ, Zody MC, Koolen DA, de Ligt J, Cuppen E, Baker C, Lee C, Graves TA, Wilson RK, Jenkins RB, Veltman JA, Eichler EE. Resolving the breakpoints of the 17q21.31 microdeletion syndrome with next-generation sequencing. Am J Hum Genet. 2012;90:599-613.
27. Koolen DA, Kramer JM, Neveling K, Nillesen WM, Moore-Barton HL, Elmslie FV, et al. Mutations in the chromatin modifier gene KANSL1 cause the 17q21.31 microdeletion syndrome. Nat Genet. 2012;44:639-41.
28. Hokamp K, McLysaght A, Wolfe KH. The 2R hypothesis and the human genome sequence. J Struct Funct Genomics. 2003;3:95-110.
29. Ambreen S, Khalil F, Abbasi AA. Integrating large-scale phylogenetic datasets to dissect the ancient evolutionary history of vertebrate genome. Mol Phylogenet Evol. 2014;78:1-13.
30. McLysaght A, Hokamp K, Wolfe KH. Extensive genomic duplication during early chordate evolution. Nat Genet. 2002;31:200-4. Update on Human Chromosomal Paralogons. http://wolfe.ucd.ie/dup/human5.28/. Accessed 5 Jan 2015.
31. Ensembl Compara. http://www.ensembl.org/index.html. Accessed 10 Nov 2014.
32. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C. STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res. 2015;43:D447-52. http://string-db.org/. Accessed 15 Sep 2015.
33. Mukhopadhyay R, Hoh JH. AFM force measurements on microtubuleassociated proteins: the projection domain exerts a long-range repulsive force. FEBS Lett. 2001;505:374-8.
34. Hammesfahr B, Odronitz F, Hellkamp M, Kollmar M. diArk 2.0 provides detailed analyses of the ever increasing eukaryotic genome sequencing data. BMC Res Notes. 2011;4:338. DiArk 3.0. http://www.diark.org/. Accessed 1 Oct 2014.
35. Mazin PV, Gelfand MS, Mironov AA, Rakhmaninova AB, Rubinov AR, Russell RB, Kalinina OV. An automated stochastic approach to the identification of the protein specificity determinants and functional subfamilies. Algorithms Mol Biol. 2010;5:29.
36. Barré P, Eliezer D. Structural transitions in tau K18 on micelle binding suggest a hierarchy in the efficacy of individual microtubule-binding repeats in filament nucleation. Protein Sci. 2013;22:1037-48.
37. Georgieva ER, Xiao S, Borbat PP, Freed JH, Eliezer D. Tau binds to lipid membrane surfaces via short amphipathic helices located in its microtubule-binding repeats. Biophys J. 2014;107:1441-52.
38. Nelson PT, Stefansson K, Gulcher J, Saper CB. Molecular evolution of tau protein: implications for Alzheimer's disease. J Neurochem. 1996;67:1622-32.
39. Stieler JT, Bullmann T, Kohl F, Tøien O, Brückner MK, Härtig W, Barnes BM, Arendt T. The physiological link between metabolic rate depression and tau phosphorylation in mammalian hibernation. PLoS One. 2011;6, e14530. doi:10.1371/journal.pone.0014530.
40. Detrich HW, Parker SK, Williams RC, Nogales E, Downing KH. Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the alpha-and beta-tubulins of Antarctic fishes. J Biol Chem. 2000;275:37038-47.
41. Schweers O, Mandelkow EM, Biernat J, Mandelkow E. Oxidation of cysteine-322 in the repeat domain of microtubule-associated protein tau controls the in vitro assembly of paired helical filaments. Proc Natl Acad Sci U S A. 1995;92:8463-7.
42. Walker S, Ullman O, Stultz CM. Using intramolecular disulfide bonds in tau protein to deduce structural features of aggregation-resistant conformations. J Biol Chem. 2012;287:9591-600.
43. Stoothoff WH, Johnson GVW. Tau phosphorylation: Physiological and pathological consequences. Biochim Biophys Acta-Mol Basis Dis. 1739; 2005:280-97.
44. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc. 2010;5:725-38. I-Tasser v4.1. http://zhanglab.ccmb.med.umich.edu/I-TASSER/. Accessed 16 Jun 2014.
45. Holzer M, Craxton M, Jakes R, Arendt T, Goedert M. Tau gene (MAPT) sequence variation among primates. Gene. 2004;341:313-22.
46. Wang Y, Gao L, Conrad CG, Andreadis A. Saitohin, which is nested within the tau gene, interacts with tau and Abl and its human-specific allele influences Abl phosphorylation. J Cell Biochem. 2011;112:3482-8.
47. Chen M, Martins RN, Lardelli M. Complex splicing and neural expression of duplicated tau genes in zebrafish embryos. J Alzheimer's Dis. 2009;18:305-17.
48. Smith JJ, Keinath MC. The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications. Genome Res. 2015. doi:10.1101/gr. 184135.114.
49. Gauthier-Kemper A, Weissmann C, Golovyashkina N, Sebö-Lemke Z, Drewes G, Gerke V, Heinisch JJ, Brandt R. The frontotemporal dementia mutation R406W blocks tau's interaction with the membrane in an annexin A2-dependent manner. J Cell Biol. 2011;192:647-61.
50. Pooler AM, Usardi A, Evans CJ, Philpott KL, Noble W, Hanger DP. Dynamic association of tau with neuronal membranes is regulated by phosphorylation. Neurobiol Aging. 2012;33:431. e27-431.e38.
51. Gómez-Ramos A, Díaz-Hernández M, Rubio A, Miras-Portugal MT, Avila J. Extracellular tau promotes intracellular calcium increase through M1 and M3 muscarinic receptors in neuronal cells. Mol Cell Neurosci. 2008;37:673-81.
52. Lee G, Thangavel R, Sharma VM, Litersky JM, Bhaskar K, Fang SM, et al. Phosphorylation of Tau by Fyn: implications for Alzheimer's disease. J Neurosci. 2004;24:2304-12.
53. Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell. 2009;138:366-76.
54. Gozes I, Sragovich S, Schirer Y, Idan-Feldman A. D-SAL and NAP: Two peptides sharing a SIP domain. J Mol Neurosci. 2016 [Epub ahead of print]
55. Rapuano BE, MacDonald DE. Structure-activity relationship of human bone sialoprotein peptides. Eur J Oral Sci. 2013;121:600-9.
56. Simões I, Mueller EC, Otto A, Bur D, Cheung AY, Faro C, Pires E. Molecular analysis of the interaction between cardosin A and phospholipase D(alpha). Identification of RGD/KGE sequences as binding motifs for C2 domains. FEBS J. 2005;272:5786-98.
57. Camero S, Benítez MJ, Cuadros R, Hernández F, Avila J, Jiménez JS. Thermodynamics of the interaction between Alzheimer's disease related tau protein and DNA. PLoS One. 2014;9, e104690.
58. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389-402.
59. Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, Bateman A, Eddy SR. HMMER web server: Update. Nucleic Acids Res. 2015; doi: 10.1093/nar/gkv397. HMMER. http://hmmer.org/. Accessed 3 Apr 2015.
60. Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, et al. RefSeq: An update on mammalian reference sequences. Nucleic Acids Res. 2014;42:756-63.
61. Consortium TU. UniProt: a hub for protein information. Nucleic Acids Res. 2009;43:D204-12. UniProtKB databases. http://www.uniprot.org/. Accessed 7 Apr 2015.
62. Do CB, Mahabhashyam MS, Brudno M, Batzoglou S. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res. 2005;15:330-40.
63. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7.
64. Eddy SR. Accelerated profile HMM searches. PLoS Comput Biol. 2011;7.
65. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics. 2005;21:951-60.
66. Horan K, Shelton CR, Girke T. Predicting conserved protein motifs with Sub-HMMs. BMC Bioinformatics. 2010;11:205.
67. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30:2725-9. MEGA v6.0 software. http://www.megasoftware.net/. Accessed 12 Jan 2015.
68. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics. 2014;30:1312-3.
69. Kozlov AM, Aberer AJ, Stamatakis A. ExaML Version 3: A Tool for Phylogenomic Analyses on Supercomputers. Bioinformatics. 2015. doi:10. 1093/bioinformatics/btv184.
70. Lartillot N, Philippe H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol. 2004;21:1095-109.
71. Aberer AJ, Kobert K, Stamatakis A. ExaBayes: Massively Parallel Bayesian Tree Inference for the Whole-Genome Era. Mol Biol Evol. 2014;31:2553-6.
72. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969-73.
73. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: Fast selection of best-fit models of protein evolution. Bioinformatics. 2011;27:1164-5. PROTEST v3 software. http://darwin.uvigo.es/. 10 Feb 2014.
74. Whelan S, Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol. 2001;18:691-9.
75. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci. 1992;8:275-82.
76. Wheeler TJ, Clements J, Finn RD. Skylign: a tool for creating informative, interactive logos representing sequence alignments and profile hidden Markov models. BMC Bioinformatics. 2014;15:7. SKYLIGN HMM logo website. http://skylign.org. Accessed 14 Nov 2015.
77. Protein Data Bank. http://www.rcsb.org/pdb/. Accessed 20 Mar 2015.
78. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. UCSF Chimera-A visualization system for exploratory research and analysis. J Comput Chem. 2004;25:1605-12.
79. Celniker G, Nimrod G, Ashkenazy H, Glaser F, Martz E, Mayrose I, Pupko T, Ben-Tal N. ConSurf: Using evolutionary data to raise testable hypotheses about protein function. Isr J Chem. 2013;53:199-206. CONSURF server. http://consurf.tau.ac.il/. Accessed 16 Jul 2015.
80. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A. 2001;98:10037-41.
81. Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G, Baker NA. PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res. 2007; 35:522-5. PDB2PQR-APBS server. http://www.poissonboltzmann.org/apbs/. Accessed 21 Apr 2014.