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Helical Assemblies

  • Natalya Kurochkina
Chapter

Abstract

Repeating structural motifs in proteins exist in many forms as groups of amino acids, secondary structure elements, domains or molecules. Protein assemblies of ankyrins, ARM/HEAT, tetratricopeptide and other repeats contain a repeating unit for which major part represents a pair of antiparallel alpha-helices. These repeating units are packed parallel to each other in a super-helix shaped as solenoid or barrels and rings. Ankyrin repeats form a left-handed spiral whereas ARM and HEAT repeats assemble into a right-handed spiral. Ankyrin repeats contain 24 whereas tetratricopeptide 8 repeats per turn. Repeats such as leucine-rich repeats and TIM-barrel contain one external row of alpha-helices and one internal row of beta-strands. Most of the repeats function as modules for binding other proteins. Amino acid sequence, specific interactions, and distribution on the surface of the secondary structure elements of amino acids determine structure of the assembly.

Keywords

Helix Assembly Helix interface Chirality Enantioselectivity 

References

  1. Abad MA, Medina B, Santamaria A, Zou J, Plasberg-Hill C, Madhumalar A et al (2014) Structural basis for microtubule recognition by the human kinetochore Ska complex. Nat Commun 5:2964.  https://doi.org/10.1038/ncomms3964 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Abil Z, Gumy LF, Zhao H, Hoogenraad CC (2017) Inducible control of mRNA transport using reprogrammable RNA-binding proteins. ACS Synth Biol 6(6):950–956.  https://doi.org/10.1021/acssynbio.7b00025. Epub 2017 Mar 8. PubMed PMID: 28260376; PubMed Central PMCID: PMC5477001CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ahmad S, Pecqueur L, Dreier B, Hamdane D, Aumont-Nicaise M, Plückthun A et al (2016) Destabilizing an interacting motif strengthens the association of a designed ankyrin repeat protein with tubulin. Sci Rep 6:28922.  https://doi.org/10.1038/srep28922 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alber T, Banner DW, Bloomer AC, Petsko GA, Phillips D, Rivers PS, Wilson IA (1981) On the three-dimensional structure and catalytic mechanism of triose phosphate isomerase. Philos Trans R Soc London 293:159–171CrossRefGoogle Scholar
  5. Allan RK, Ratajczak T (2011) Versatile TPR domains accommodate different modes of target protein recognition and function. Cell Stress and Chaperones 16:353–367PubMedCrossRefGoogle Scholar
  6. Andrade MA, Bork P (1995) HEAT repeats in the Huntington’s disease protein. Nat Genet 11:115–116PubMedCrossRefGoogle Scholar
  7. Andrade MA, Perez-Iratxeta C, Ponting CP (2001a) Protein repeats: structures, functions, and evolutions. J Struct Biol 134:117–131PubMedCrossRefGoogle Scholar
  8. Andrade MA, Petosa C, O’Donoghue SI, Müller CW, Bork P (2001b) Comparison of ARM and HEAT protein repeats. J Mol Biol 309:1–18PubMedCrossRefGoogle Scholar
  9. Arana ME, Holmes SF, Fortune JM, Moon AF, Pedersen LC, Kunkel TA (2010) Functional Residues on the Surface of the N-terminal domain of Yeast Pms1. DNA Repair 9(4):448–457.  https://doi.org/10.1016/j.dnarep.2010.01.010 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bai Y, Luo Y, Liu S, Zhang L, Shen K, Dong Y et al (2011) PRL-1 protein promotes ERK1/2 and RhoA protein activation through a non-canonical interaction with the Src homology 3 domain of p115 Rho GTPase-activating protein. J Bioll Chem 286(49):42316–42324.  https://doi.org/10.1074/jbc.M111.286302 CrossRefGoogle Scholar
  11. Bent CJ, Isaacs NW, Mitchell TJ, Riboldi-Tunnicliffe A (2004) Crystal structure of the response regulator 02 receiver domain, the essential YycF two-component system of Streptococcus pneumoniae in both complexed and native states. J Bacteriol 186(9):2872–2879.  https://doi.org/10.1128/JB.186.9.2872-2879.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Binz HK, Stumpp MT, Forrer P, Amstutz P, Pluckthun A (2003) Designing Repeat Proteins: Well-expressed, Soluble and Stable Proteins from Combinatorial Libraries of Consensus Ankyrin Repeat Proteins. J Mol Biol 332:489–503PubMedCrossRefGoogle Scholar
  13. Bochtler M (2012) Structural basis of the TAL effector–DNA interaction. Biol Chem 393:1055–1066PubMedCrossRefGoogle Scholar
  14. Chothia C, Levitt M, Richardson D (1981) Helix to helix packing in proteins. J Mol Biol 145:215–250PubMedCrossRefGoogle Scholar
  15. Chua TK, Bujnicki JM, Tan T-C, Huynh F, Patel BKC, Sivaraman J (2008) The structure of sucrose phosphate synthase from halothermothrix orenii reveals its mechanism of action and binding mode. Plant Cell 20:1059–1072PubMedPubMedCentralCrossRefGoogle Scholar
  16. Clapham DE, Miller C (2011) A thermodynamic framework for understanding temperature-sensing by TRP channels. Proc Natl Acad Sci USA 108:19492–19497PubMedPubMedCentralCrossRefGoogle Scholar
  17. Cordero-Morales JF, Gracheva EO, Julius D (2011) Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc Natl Acad Sci 108:E1184–E1191PubMedCrossRefGoogle Scholar
  18. Crick F (1953) Acta Crystallogr 6:689CrossRefGoogle Scholar
  19. Cunha ES, Hatem CL, Barrick D (2016) Synergistic enhancement of cellulase pairs linked by consensus ankyrin repeats: determination of the roles of spacing, orientation and enzyme identity. Proteins 84(8):1043–1054.  https://doi.org/10.1002/prot.25047 CrossRefPubMedPubMedCentralGoogle Scholar
  20. D’Andrea LD, Regan L (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28(12):655–662. Review. PubMed PMID: 14659697PubMedCrossRefPubMedCentralGoogle Scholar
  21. Dautant A, Velours J, Giraud MF (2010) Crystal structure of the Mg·ADP-inhibited state of the yeast F1c10-ATP synthase. J Biol Chem 285(38):29502–29510.  https://doi.org/10.1074/jbc.M110.124529. Epub 2010 Jul 7. PubMed PMID: 20610387; PubMed Central PMCID: PMC2937982CrossRefPubMedPubMedCentralGoogle Scholar
  22. Delmar M (2012) Connexin43 regulates sodium current; ankyrin-G modulates gap junctions: the intercalated disc exchanger. Cardiovasc Res 93(2):220–222.  https://doi.org/10.1093/cvr/cvr343. Epub 2011 Dec 16. PubMed PMID: 22180603CrossRefPubMedPubMedCentralGoogle Scholar
  23. Deng L, Guindon J, Vemuri VK, Thakur GA, White FA, Makriyannis A, Hohmann AG (2012) The maintenance of cisplatin- and paclitaxel-induced mechanical and cold allodynia is suppressed by cannabinoid CB2 receptor activation and independent of CXCR4 signaling in models of chemotherapy-induced peripheral neuropathy. Mol Pain 8:71–83PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dluzewski AR, Fryer PR, Griffiths S, Wilson RJ, Gratzer WB (1989) Red cell membrane protein distribution during malarial invasion. J Cell Sci 92(Pt4):691–699. PubMed PMID: 2532219PubMedPubMedCentralGoogle Scholar
  25. Dodonova SO, Diestelkoetter-Bachert P, von Appen A, Hagen WJ, Beck R, Beck M, Wieland F, Briggs JA (2015) Vesicular transport. A structure of the COPI coat and the role of coat proteins in membrane vesicle assembly. Science 349(6244):195–198.  https://doi.org/10.1126/science.aab1121. PubMed PMID: 26160949CrossRefPubMedGoogle Scholar
  26. Edwards RA, Lee MS, Tsutakawa SE, Williams RS, Tainer JA, Glover JNM (2008) The BARD1 C-terminal domain structure and interactions with polyadenylation factor CstF-50. Biochemistry 47:11446–11456PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ferreiro DU, Cervantes CF, Truhlar Stephanie ME, Cho SS, Wolynes PG, Komives EA (2007) Stabilizing IκBα by ‘consensus’ design. J Mol Biol 365:1201–1216PubMedCrossRefGoogle Scholar
  28. Filippakopoulos P, Müller S, Knapp S (2009) SH2 domains: modulators of nonreceptor tyrosine kinase activity. Curr Opin Struct Biol 19(6):643–649.  https://doi.org/10.1016/j.sbi.2009.10.001. Epub 2009 Nov 18. Review. PubMed PMID: 19926274; PubMed Central PMCID: PMC2791838CrossRefPubMedPubMedCentralGoogle Scholar
  29. Forwood JK, Lange A, Zachariae U, Marfori M, Preast C, Grubmüller H, Stewart M, Corbett AH, Kobe B (2010) Quantitative structural analysis of importin-β flexibility: paradigm for solenoid protein structures. Structure 18:1171–1183PubMedCrossRefGoogle Scholar
  30. Gernert KM, Surles MC, Labean TH, Richardson JS, Richardson DC (1995) Alacoil: a very tight, antiparallel coiled-coil of helices. Protein Science 4:2252–2260PubMedPubMedCentralCrossRefGoogle Scholar
  31. Gmeiner WH, Horita DA (2001) Implications of SH3 domain structure and dynamics for protein regulation and drug design. Cell Biochem Biophys 35(2):127–140. Review. PubMed PMID: 11892788PubMedCrossRefGoogle Scholar
  32. Groothuizen FS, Winkler I, Cristóvão M, Fish A, Winterwerp HH, Reumer A et al (2015) MutS/MutL crystal structure reveals that the MutS sliding clamp loads MutL onto DNA. eLife 4:e06744.  https://doi.org/10.7554/eLife.06744 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Groves MR, Hanlon N, Turowski P, Hemmings BA, Barford D (1999) The structure of the PROTEIN Phosphatase 2A PR65/A Subunit Reveals the Conformation of Its 15 Tandemly Repeated HEAT Motifs. Cell 96:99–110PubMedCrossRefGoogle Scholar
  34. Gu L, Hong Y, McCulloch S, Watanabe H, Li GM (1998) ATP-dependent interaction of human mismatch repair proteins and dual role of PCNA in mismatch repair. Nucleic Acids Res 26(5):1173–1178. PubMed PMID: 9469823; PubMed Central PMCID: PMC147380PubMedPubMedCentralCrossRefGoogle Scholar
  35. Guarné A, Junop MS, Yang W (2001) Structure and function of the N-terminal 40 kDa fragment of human PMS2: a monomeric GHL ATPase. The EMBO Journal 20(19):5521–5531.  https://doi.org/10.1093/emboj/20.19.5521 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Han D, Kim K, Oh J, Park J, Kim Y (2007) TPR domain of NrfG mediates complex formation between heme lyase and formate-dependent nitrite reductase in Escherichia coli O157:H7. Proteins 70:900–914CrossRefGoogle Scholar
  37. Hausmann J, Kamtekar S, Christodoulou E, Day JE, Wu T, Fulkerson Z et al (2011) Structural basis for substrate discrimination and integrin binding by autotaxin. Nat Struct Mol Biol 18(2):198–204.  https://doi.org/10.1038/nsmb.1980 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Heldwein EE, Macia E, Wang J, Yin HL, Kirchhausen T, Harrison SC (2004) Crystal structure of the clathrin adaptor protein 1 core. Proc Natl Acad Sci U S A 101(39):14108–14113. Epub 2004 Sep 17. PubMed PMID: 15377783; PubMed Central PMCID: PMC521094PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hendrickson WA, Ward KB (1977) Pseudosymmetry in the structure of myohemerythrin. J Biol Chem 252:3012–3018PubMedPubMedCentralGoogle Scholar
  40. Hinderlich S, Weidemann W, Yardeni T, Horstkorte R, Huizing M (2015) UDP-GlcNAc 2-epimerase/ManNAc kinase (GNE), a master regulator of sialic acid synthesis. Topics in Current Chemistry 366:97–137.  https://doi.org/10.1007/128_2013_464 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Holm L, Sander C (1993) Structural alignment of globins, phycocyanins and colicin A. FEBS letters 315:301–306PubMedCrossRefGoogle Scholar
  42. Holzer S, Ban N, Klinge S (2013) Crystal structure of the yeast ribosomal protein rpS3 in complex with its chaperone Yar1. J Mol Biol 425(22):4154–4160.  https://doi.org/10.1016/j.jmb.2013.08.022. Epub 2013 Sep 7. PubMed PMID: 24021814CrossRefPubMedGoogle Scholar
  43. Holzer P, Izzo AA (2014) The pharmacology of TPR channels. British J of Pharmacology 171:2469–2473CrossRefGoogle Scholar
  44. Huber AH, Nelson WJ, Weis WI (1997) Three-Dimensional Structure of the Armadillo Repeat Region of b-Catenin. Cell 90:871–882PubMedCrossRefGoogle Scholar
  45. Jenkins HT, Baker-Wilding R, Edwards TA (2009) Structure and RNA binding of the mouse Pumilio-2 Puf domain. J Struct Biol. 167(3):271–276.  https://doi.org/10.1016/j.jsb.2009.06.007. Epub 2009 Jun 18. PubMed PMID: 19540345PubMedCrossRefGoogle Scholar
  46. Jin AJ, Lafer EM, Peng JQ, Smith PD, Nossal R (2013) Unraveling protein–protein interactions in clathrin assemblies via atomic force spectroscopy. Methods 59:316–327PubMedCrossRefGoogle Scholar
  47. Jínek M, Rehwinkel J, Lazarus BD, Izaurralde E, Hanover JA, Conti E (2004) The superhelical TPR-repeat domain of O-linked GlcNAc transferase exhibits structural similarities to importin alpha. Nat Struct Mol Biol 11(10):1001–1007. Epub 2004 Sep 12. PubMed PMID: 15361863PubMedCrossRefGoogle Scholar
  48. Kajander T, Cortajarena AL, Mochrieb S, Regan L (2007) Structure and stability of designed TPR protein superhelices: unusual crystal packing and implications for natural TPR proteins. Acta Cryst D63:800–811Google Scholar
  49. Kajander T, Cortajarena AL, Regan L (2006) Consensus design as a tool for engineering repeat proteins. Methods Mol Biol 340:151–170PubMedGoogle Scholar
  50. Kajava AV (1998) Structural diversity of leucine-rich repeat proteins. J Mol Biol 277:519–527PubMedCrossRefGoogle Scholar
  51. Karasik A, Shanmuganathan A, Howard MJ, Fierke CA, Koutmos M (2016) Nuclear protein-only ribonuclease P2 structure and biochemical characterization provide insight into the conserved properties of tRNA 5′ end processing enzymes. J Mol Biol 428(1):26–40.  https://doi.org/10.1016/j.jmb.2015.11.025. Epub 2015 Dec 3. PubMed PMID: 26655022; PubMed Central PMCID: PMC4738078CrossRefPubMedGoogle Scholar
  52. Kaszas K, Keller JM, Coddou C, Mishra SK, Hoon MA, Stojilkovic S, Jacobson KA, Iadarola MJ (2012) Small molecule positive allosteric modulation of TRPV1 activation by Vanilloids and Acidic pH. J. Pharm. Exp. Therapeutics 340:152–160CrossRefGoogle Scholar
  53. Kato K, Nishimasu H, Okudaira S, Mihara E, Ishitani R, Takagi J et al (2012) Crystal structure of Enpp1, an extracellular glycoprotein involved in bone mineralization and insulin signaling. Proc Natl Acad Sciences U S A 109(42):16876–16881.  https://doi.org/10.1073/pnas.1208017109 CrossRefGoogle Scholar
  54. Ke J, Chen RZ, Ban T, Zhou XE, Gu X, Tan MH, Chen C, Kang Y, Brunzelle JS, Zhu JK, Melcher K, Xu HE (2013) Structural basis for RNA recognition by a dimeric PPR-protein complex. Nat Struct Mol Biol 20(12):1377–1382. doi: 10.1038/nsmb.2710. Epub 2013 Nov 3. PubMed PMID: 24186060CrossRefGoogle Scholar
  55. Kefalas P, Brown TR, Brickell PM (1995) Signalling by the p60c-src family of protein-tyrosine kinases. Int J Biochem Cell Biol 27(6):551–563. Review. PubMed PMID: 7545532CrossRefGoogle Scholar
  56. Kim DH, Park M-J, Gwon GH, Silkov A, Xu Z-Y, Yang EC, Song S, Song K, Kim Y, Yoon HS, Honig B, Cho W, Cho Y, Hwang I (2014) Chloroplast targeting factor AKR2 evolved from an ankyrin repeat domain coincidentally binds two chloroplast lipids. Dev Cell 30(5):598–609PubMedPubMedCentralCrossRefGoogle Scholar
  57. Kobe B (1999) Autoinhibition by an internal nuclear localization signal revealed by the crystal structure of mammalian importin. Nat Str Biol 6:388–397CrossRefGoogle Scholar
  58. Kobe B, Deisenhofer J (1996) Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A. J Mol Biol 264:1028–1043PubMedCrossRefGoogle Scholar
  59. Kohl A, Binz HK, Forrer P, Stumpp MT, Plőckthun A, Grőtter MG (2002) Designed to be stable: crystal structure of a consensus ankyrin repeat protein. Proc Natl Acad Sci 100:1700–1705CrossRefGoogle Scholar
  60. Kohn WD, Mant CT, Hodges RS (1977) Helical protein assembly motifs. J Biol Chem 272:2583–2586CrossRefGoogle Scholar
  61. Krylov D, Mikhailenko I, Vinson C (1994) A thermodynamic scale for leucine zipper stability and dimerization specificity: e and g interhelical interactions. EMBO J. 13:2849–2861PubMedPubMedCentralCrossRefGoogle Scholar
  62. Krzywda S, Brzozowski AM, Higashitsuji H, Fujita J, Welchman R, Dawson S, Mayer RJ, Wilkinson AJ (2004) The Crystal Structure of Gankyrin, an Oncoprotein Found in Complexes with Cyclin-dependent Kinase 4, a 19 S Proteasomal ATPase Regulator, and the Tumor Suppressors Rb and p53. J Biol Chem 279:1541–1545CrossRefGoogle Scholar
  63. Kummel D, Muller JJ, Roske Y, Henke N, Heinemann U (2006) Structure of the Bet3-Tpc6b core of trapp: two Tpc6 paralogs form trimeric complexes with Bet3 and Mum2. Ref J Mol Biol 361:22–32CrossRefGoogle Scholar
  64. Kümmel D, Oeckinghaus A, Wanga C, Krappmann D, Heinemann U (2008) Distinct isocomplexes of the TRAPP trafficking factor coexist inside human cells. FEBS Lett 582:3729–3733PubMedCrossRefGoogle Scholar
  65. Kurochkina N (2007) J Theor Biol 247:110–121PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kurochkina N (2008) J Theor Biol 255:188–198PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kurochkina N, Choekyi T (2011) Helix-helix interfaces and ligand binding. J Theor Biol 283:92–102PubMedPubMedCentralCrossRefGoogle Scholar
  68. de Lange O, Binder A, Lahaye T (2014) From dead leaf, to new life: TAL effectors as tools for synthetic biology. Plant J 78:753–771PubMedCrossRefGoogle Scholar
  69. Lee G, Abdi K, Jiang Y, Michaely P, Bennett V, Marszalek PE (2006) Nanospring behaviour of ankyrin repeats. Nature 440:246–249PubMedPubMedCentralCrossRefGoogle Scholar
  70. Lee SJ, Imamoto N, Sakai H, Nakagawa A, Kose S, Koike M, Yamamoto M, Kumasaka T, Yoneda Y, Tsukihara T (2000) The Adoption of a Twisted Structure of Importin-b is Essential for the Protein-protein Interaction Required for Nuclear Transport. J Mol Biol 302:251–264PubMedCrossRefGoogle Scholar
  71. Lepage PK, Lussier MP, Barajas-Martinez H, Bousquet SM, Blanchard AP, Francoeur N, Dumaine R, Boulay G (2006) Identification of two domains involved in the Assembly of Transient Receptor Potential Canonical Channels. J Biol Chem 2006(281):30356–30364CrossRefGoogle Scholar
  72. Li Y, Meng X, Xiang Y, Deng J (2010) Structure function studies of vaccinia virus host range protein K1 reveal a novel functional surface for Ankyrin repeat proteins. J Virol 84:3331PubMedPubMedCentralCrossRefGoogle Scholar
  73. Li X, Song B, Chen X, Wang Z, Zeng M, Yu D, Hu D, Chen Z, Jin L, Yang S, Yang C, Chen B (2013) Crystal structure of a four-layer aggregate of engineered TMV CP implies the importance of terminal residues for oligomer assembly. PLoS One 8(11):e77717.  https://doi.org/10.1371/journal.pone.0077717. eCollection 2013. PubMed PMID: 24223721; PubMed Central PMCID: PMC3817195CrossRefPubMedPubMedCentralGoogle Scholar
  74. Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R (2007) The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54:905–918PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lu G, Dolgner SJ, Hall TM (2009) Understanding and engineering RNA sequence specificity of PUF proteins. Curr Opin Struct Biol 19(1):110–115. doi:  https://doi.org/10.1016/j.sbi.2008.12.009. Epub 2009 Jan 29. PubMed PMID: 19186050; PubMed Central PMCID: PMC2748946PubMedPubMedCentralCrossRefGoogle Scholar
  76. Madhurantakam C, Varadamsetty G, Grütter MG, Plückthun A, Mittl PRE (2012) Structure-based optimization of designed Armadillo-repeat proteins. Protein Sci 21:1015–1028PubMedPubMedCentralCrossRefGoogle Scholar
  77. Maeda S, Nakagawa S, Suga M, Yamashita E, Oshima A, Fujiyoshi Y, Tsukihara T (2009) Structure of the connexin 26 gap junction channel at 3.5 A resolution. Nature 458(7238):597–602.  https://doi.org/10.1038/nature07869. PubMed PMID: 19340074CrossRefPubMedGoogle Scholar
  78. Main ER, Xiong Y, Cocco MJ, D’Andrea L, Regan L (2003) Design of stable alpha-helical arrays from an idealized TPR motif. Structure 11(5):497–508. PubMed PMID: 12737816PubMedCrossRefGoogle Scholar
  79. Mak AN-S, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335:716–719PubMedPubMedCentralCrossRefGoogle Scholar
  80. Malik HS, Eickbush TH, Goldfarb DS (1997) Evolutionary specialization of the nuclear targeting apparatus. Proc Natl Acad Sci 94:13738–13742PubMedCrossRefGoogle Scholar
  81. Martinez J, Nguyen LD, Hinderlich S, Zimmer R, Tauberger E, Reutter W et al (2012) Crystal structures of N-Acetylmannosamine Kinase provide insights into enzyme activity and inhibition. J Biol Chem 287(17):13656–13665.  https://doi.org/10.1074/jbc.M111.318170 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Maxson ME, Grinstein S (2014) The vacuolar-type H?-ATPase at a glance - more than a proton pump. J Cell Sci 127(Pt 23):4987–4993.  https://doi.org/10.1242/jcs.158550. Review. PubMed PMID: 25453113CrossRefPubMedGoogle Scholar
  83. Mayer BJ (2001) SH3 domains: complexity in moderation. J Cell Science 114:1253–1263PubMedGoogle Scholar
  84. Meier T, Krah A, Bond PJ, Pogoryelov D, Diederichs K, Faraldo-Gómez JD (2009) Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J Mol Biol. 391(2):498–507. doi: https://doi.org/10.1016/j.jmb.2009.05.082. Epub 2009 Jun 3. PubMed PMID: 19500592PubMedCrossRefGoogle Scholar
  85. Michaely P, Tomchick DR, Machius M, Anderson RGW (2002) Crystal structure of a 12 ANK repeat stack from human ankyrinR. EMBO J 21:6387–6396PubMedPubMedCentralCrossRefGoogle Scholar
  86. Milburn CC, Boudeau J, Deak M, Alessi DR, van Aalten DMF (2004) Crystal structure of MO25α in complex with the C terminus of the pseudo kinase STE20-related adaptor. Nat Str & Mol Biol 11:193–200CrossRefGoogle Scholar
  87. Mills RD, Mulhern TD, Cheng H-C, Culvenor JG (2012) Analysis of LRRK2 accessory repeat domains: prediction of repeat length, number and sites of Parkinson’s disease mutations. Biochem Soc Trans 40:1086–1089PubMedCrossRefGoogle Scholar
  88. Miyanari Y (2014) TAL effector-mediated genome visualization (TGV). Methods 69:198–204PubMedCrossRefGoogle Scholar
  89. Mizutani K, Yamamoto M, Suzuki K, Yamato I, Kakinuma Y, Shirouzu M, Walker JE, Yokoyama S, Iwata S, Murata T (2011) Structure of the rotor ring modified with N,N′-dicyclohexylcarbodiimide of the Na+-transporting vacuolar ATPase. Proc Natl Acad Sci U S A 108(33):13474–13479.  https://doi.org/10.1073/pnas.1103287108. Epub 2011 Aug 3. PubMed PMID: 21813759; PubMed Central PMCID: PMC3158168CrossRefPubMedPubMedCentralGoogle Scholar
  90. Monecke T, Haselbach D, Vo B, Russek A, Neumann P, Thomson E, Hurt E, Zachariae U, Stark H, Grubmüller H, Dickmanns A, Ficner R (2012) Structural basis for cooperativity of CRM1 export complex formation. Proc Natl Acad Sci 110:960–965PubMedCrossRefGoogle Scholar
  91. Mosavi LK, Cammett TJ, Desrosiers DC, Peng Z (2004) The ankyrin repeat as molecular architecture for protein recognition. Protein Sci 13:1435–1448PubMedPubMedCentralCrossRefGoogle Scholar
  92. Mosavi LK, Minor DL, Peng Z (2002) Consensus-derived structural determinants of the ankyrin repeat motif. Proc Natl Acad Sci 99:16031–16034CrossRefGoogle Scholar
  93. Nagatomo K, Ishii H, Yamamoto T, Nakajo K, Kubo Y (2010) The Met268Pro mutation of mouse TRPA1 changes the effect of caffeine from activation to suppression. Biophys J 99:3609–3618PubMedPubMedCentralCrossRefGoogle Scholar
  94. Narayanan A, Kumar S, Evrard AN, Paul LN, Yernool DA (2014) Asymmetric hetero-domain interface stabilizes a response regulator-DNA complex. Nat Commun 5:3282.  https://doi.org/10.1038/ncomms4282 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Natrajan G, Lamers MH, Enzlin JH, Winterwerp HHK, Perrakis A, Sixma TK (2003) Structures of Escherichia coli DNA mismatch repair enzyme MutS in complex with different mismatches: a common recognition mode for diverse substrates. Nucleic Acids Res 31(16):4814–4821PubMedPubMedCentralCrossRefGoogle Scholar
  96. Nawrotek A, Knossow M, Gigant B (2011) The determinants that govern microtubule assembly from the atomic structure of GTP-tubulin. J Mol Biol 412(1):35–42.  https://doi.org/10.1016/j.jmb.2011.07.029 CrossRefPubMedGoogle Scholar
  97. Nilius N, Prenen J, Owsianik G (2011) Irritating channels: the case of TRPA1. J Physiol 589(7):1543–1549PubMedPubMedCentralCrossRefGoogle Scholar
  98. O’Shea EK, Klemm JD, Kim PS, Alber T (1991) Crystal structure of GCN4 leucine zipper, a two-stranded parallel coiled coil. Science 254:539PubMedCrossRefGoogle Scholar
  99. Padmanabhan B, Adachi N, Kataoka K, Horikoshi M (2004) Crystal structure of the homolog of the oncoprotein gankyrin, an interactor of Rb and CDK4/6. J Biol Chem 279:1546–1552PubMedCrossRefGoogle Scholar
  100. Pan X, Xu S, Wu J, Duan Y, Zheng Z, Wang J, Song X, Zhou M (2018) Ankyrin-like protein AnkB interacts with CatB, affects catalase activity, and enhances resistance of Xanthomonas oryzae pv. oryzae and Xanthomonas oryzae pv. oryzicola to Phenazine-1-Carboxylic Acid. Appl Environ Microbiol. 84(4). pii: e02145–17.  https://doi.org/10.1128/AEM.02145-17. Print 2018 Feb 15. PubMed PMID: 29180371; PubMed Central PMCID: PMC5795068
  101. Pareek TK, Keller J, Kesavapany S, Agarwal N, Kuner R, Pant H, Iadarola MJ, Brady RO, Kulkarni AB (2006) Cyclin-dependent kinase 5 modulates nociceptive signaling through direct phosphorylation of transient receptor potential vanilloid 1. Proc Natl Acad Sci 104:660–665CrossRefGoogle Scholar
  102. Pauling L, Corey RB, Branson HR (1951) The structure of proteins: two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci USA 37:205PubMedCrossRefPubMedCentralGoogle Scholar
  103. Paulson AR, Tong L (2012) Crystal structure of the Rna14-Rna15 complex. RNA Jun;18(6):1154–1162.  https://doi.org/10.1261/rna.032524.112. Epub 2012 Apr 18. PubMed PMID: 22513198; PubMed Central PMCID: PMC3358638PubMedPubMedCentralCrossRefGoogle Scholar
  104. Pecqueur L, Duellberg C, Dreier B, Jiang Q, Wang C, Plückthun A et al (2012) A designed ankyrin repeat protein selected to bind to tubulin caps the microtubule plus end. Proc Natl Acad Sci USA 109(30):12011–12016.  https://doi.org/10.1073/pnas.1204129109 CrossRefPubMedPubMedCentralGoogle Scholar
  105. Perry AJ, Hulett JM, Likić VA, Lithgow T, Gooley PR (2006) Convergent evolution of receptors for protein import into mitochondria. Curr Biol 16:221–229PubMedCrossRefPubMedCentralGoogle Scholar
  106. Phelps CB, Huang RJ, Lishko PV, Wang RR, Gaudet R (2008) Structural analyses of the Ankyrin Repeat Domain of TRPV6 and related TRPV ion channels. Biochemistry 47:2476–2484PubMedPubMedCentralCrossRefGoogle Scholar
  107. Preiss L, Yildiz O, Hicks DB, Krulwich TA, Meier T (2010) A new type of proton coordination in an F(1)F(o)-ATP synthase rotor ring. PLoS Biol 8(8):e1000443.  https://doi.org/10.1371/journal.pbio.1000443. PubMed PMID: 20689804; PubMed Central PMCID: PMC2914638.PubMedPubMedCentralCrossRefGoogle Scholar
  108. Rak A, Pylypenko O, Durek T, Watzke A, Kushnir S, Brunsveld L, Waldmann H, Goody RS, Alexandrov K (2003) Structure of Rab GDP-dissociation inhibitor in complex with prenylated YPT1 GTPase. Science 302:646PubMedCrossRefPubMedCentralGoogle Scholar
  109. Rao ST, Rossmann MG (1973) Comparison of super-secondary structure in proteins. J Mol Biol 76:241–256PubMedCrossRefPubMedCentralGoogle Scholar
  110. Ringel R, Sologub M, Morozov YI, Litonin D, Cramer P, Temiakov D (2011) Structure of human mitochondrial RNA polymerase. Nature 478(7368):269–273.  https://doi.org/10.1038/nature10435. PubMed PMID: 21947009PubMedCrossRefGoogle Scholar
  111. Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Baslé A, Morland C, Day AM, Zheng H, Rogers TE, Thompson P, Hawkins AR, Yadav MP, Henrissat B, Martens EC, Dupree P, Gilbert HJ, Bolam DN (2015) Glycan complexity dictates microbial resource allocation in the large intestine. Nat Commun. 6:7481.  https://doi.org/10.1038/ncomms8481. Erratum in: Nat Commun. 2016;7:10705. PubMed PMID: 26112186; PubMed Central PMCID: PMC4491172
  112. Sanders SS, Mui KKN, Sutton LM, Hayden MR (2014) Identification of binding sites in Huntingtin for the Huntingtin Interacting Proteins HIP14 and HIP14L. PlosOne 28:e90669CrossRefGoogle Scholar
  113. Scheraga HA, Chou KC, Nemethy G (1982) In: Srinivasan R, Sarma RH (eds) Conformation in biology. Adenine Press, GilderlandGoogle Scholar
  114. Schmidt H, Hansen G, Singh S, Hanuszkiewicz A, Lindner B, Fukase K et al (2012) Structural and mechanistic analysis of the membrane-embedded glycosyltransferase WaaA required for lipopolysaccharide synthesis. Proc Natl Acad Sci USA 109(16):6253–6258.  https://doi.org/10.1073/pnas.1119894109 CrossRefPubMedGoogle Scholar
  115. Scholze H, Boch J (2011) TAL effectors are remote controls for gene activation. Curr Opin Microbiol 14:47–53PubMedCrossRefGoogle Scholar
  116. Schulman (2000) 1fqv 1fs1Google Scholar
  117. Schulz GE, Schirmer RH (1982) Principles of protein structure. Ed: Cantor, C. R.,Google Scholar
  118. Chen S-C, Huang C-H, Lai S-J, Yang CS, Hsiao T-H, Lin C-H, Fu P-K, Ko T-P, Chen Y (2016) Mechanism and inhibition of human UDP-GlcNAc 2-epimerase, the key enzyme in sialic acid biosynthesis. Sci Rep 6:23274.  https://doi.org/10.1038/srep23274 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Shin H, Renatus M, Eckelman BP, Nunes VA, Sampaio CA, Salvesen GS (2005) The BIR domain of IAP-like protein 2 is conformationally unstable: implications for caspase inhibition. Biochem J 385(Pt 1):1–10. PubMed PMID: 15485395; PubMed Central PMCID: PMC1134667PubMedCrossRefGoogle Scholar
  120. Smith DF (2004) Tetratricopeptide repeat cochaperones in steroid receptor complexes. Cell Stress Chaperones 9:109–121PubMedPubMedCentralCrossRefGoogle Scholar
  121. Stahlberg H, Müller DJ, Suda K, Fotiadis D, Engel A, Meier T, Matthey U, Dimroth P (2001) Bacterial Na(+)-ATP synthase has an undecameric rotor. EMBO Rep 2(3):229–233. PubMed PMID: 11266365; PubMed Central PMCID: PMC1083843PubMedPubMedCentralCrossRefGoogle Scholar
  122. Stoll VS, Kimber MS, Pai EF (1996) Insights into substrate binding by D-2-ketoacid dehydrogenases from the structure of Lactobacillus pentosus D-lactate dehydrogenase. Structure 4(4):437–447. PubMed PMID: 8740366PubMedCrossRefGoogle Scholar
  123. Stone D, Kiem H-P, Jerome KR (2013) Targeted gene disruption to cure HIV. Curr Opin HIV AIDS 8:217–223PubMedPubMedCentralCrossRefGoogle Scholar
  124. Tewary SK, Liang L, Lin Z, Lynn A, Cotmore SF, Tattersall P et al (2015) Structures of minute virus of mice replication initiator protein N-terminal domain: insights into DNA nicking and origin binding. Virology 476:61–71.  https://doi.org/10.1016/j.virol.2014.11.022 CrossRefPubMedGoogle Scholar
  125. Toro-Roman A, Wu T, Stock AM (2005) A common dimerization interface in bacterial response regulators KdpE and TorR. Protein Science?: A Publication of the Protein Society 14(12):3077–3088.  https://doi.org/10.1110/ps.051722805 CrossRefGoogle Scholar
  126. Tu D, Li W, Ye Y, Brunger AT (2007) Structure and function of the yeast U-box-containing ubiquitin ligase Ufd2p. Proc Natl Acad Sci 104:15599–15606PubMedCrossRefGoogle Scholar
  127. Urosev D, Ferrer-Navarro M, Pastorello I, Cartocci E, Costenaro L, Zhulenkovs D, Maréchal JD, Leonchiks A, Reverter D, Serino L, Soriani M, Daura X (2013) Crystal structure of c5321: a protective antigen present in uropathogenic Escherichia coli strains displaying an SLR fold. BMC Struct Biol. 13:19.  https://doi.org/10.1186/1472-6807-13-19. PubMed PMID: 24099525; PubMed Central PMCID: PMC3851747PubMedPubMedCentralCrossRefGoogle Scholar
  128. Vollmar M, Schlieper D, Winn M, Büchner C, Groth G (2009) Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J Biol Chem 284(27):18228–18235.  https://doi.org/10.1074/jbc.M109.006916. Epub 2009 May 7. PubMed PMID: 19423706; PubMed Central PMCID: PMC2709358PubMedCrossRefGoogle Scholar
  129. Yan J, Zhang Q, Guan Z, Wang Q, Li L, Ruan F, Lin R, Zou T, Yin P (2017) MORF9 increases the RNA-binding activity of PLS-type pentatricopeptide repeat protein in plastid RNA editing. Nat Plants 3:17037.  https://doi.org/10.1038/nplants.2017.37. PubMed PMID: 28394309
  130. Wang M, Ogé L, Perez-Garcia MD, Hamama L, Sakr S (2018) The PUF protein family: overview on PUF RNA targets, biological functions, and post transcriptional regulation. Int J Mol Sci 19(2). pii: E410.  https://doi.org/10.3390/ijms19020410. Review. PubMed PMID: 29385744; PubMed Central PMCID: PMC5855632
  131. Wang X, McLachlan J, Zamore PD, Hall TM (2002) Modular recognition of RNA by a human pumilio-homology domain. Cell;110(4):501–512. PubMed PMID: 12202039PubMedCrossRefGoogle Scholar
  132. Wierenga RK, Noble MEM, Vriend G, Naughe S, Hol WGJ (1991) Refined 1.83 Angstrom structure of trypanosomal triosephospate isomerase, crystallized in presence of 2.4M- Ammonium sulphate. A comparison with the structure of the trypanosomal triosephosphate isomerase-glycerol-3-phosphate complex. J Mol Biol 220:995–1015PubMedPubMedCentralCrossRefGoogle Scholar
  133. Wierenga RK (2001) The TIM-barrel fold: a versatile framework for efficient enzymes. FEBS Lett 492:193–198PubMedCrossRefGoogle Scholar
  134. Willhoft O, Kerr R, Patel D, Zhang W, Al-Jassar C, Daviter T et al (2017) The crystal structure of the Sgt1-Skp1 complex: the link between Hsp90 and both SCF E3 ubiquitin ligases and kinetochores. Sci Rep 7:41626.  https://doi.org/10.1038/srep41626 CrossRefPubMedPubMedCentralGoogle Scholar
  135. Wong K, Perpich JD, Kozlov G, Cygler M, Abu Kwaik Y, Gehring K (2017) Structural mimicry by a bacterial F box effector hijacks the host ubiquitin-proteasome system. Structure 25(2):376–383.  https://doi.org/10.1016/j.str.2016.12.015 CrossRefPubMedPubMedCentralGoogle Scholar
  136. Wu H, Zeng H, Lam R, Tempel W, Kerr ID, Min J (2015) Structure of the human MLH1 N-terminus: implications for predisposition to Lynch syndrome. Acta Crystallogr Sect F Struct Biol Commun 71(Pt 8):981–985.  https://doi.org/10.1107/S2053230X15010183 CrossRefGoogle Scholar
  137. Yang H, Jiang X, Li B, Yang HJ, Miller M, Yang A, Dhar A, Pavletich NP (2017) Mechanisms of mTORC1 activation by RHEB and inhibition by PRAS40. Nature 552(7685): 368–373.  https://doi.org/10.1038/nature25023. Epub 2017 Dec 13. PubMed PMID: 29236692; PubMed Central PMCID: PMC5750076PubMedPubMedCentralCrossRefGoogle Scholar
  138. Yuan T, Liu L, Zhang Y, Wei L, Zhao S, Zheng X, Huang X, Boulanger J, Gueudry C, Lu J, Xie L, Du W, Zong W, Yang L, Salamero J, Liu Y, Chen L (2015) Diacylglycerol guides the hopping of clathrin-coated pits along microtubules for exo-endocytosis coupling. Dev Cell 35(1):120-130.  https://doi.org/10.1016/j.devcel.2015.09.004. Epub 2015 Oct 1. PubMed PMID: 26439397PubMedCrossRefGoogle Scholar
  139. Zhang Q, Harding R, Hou F, Dong A, Walker JR, Bteich J, Tong Y (2016) Structural basis of the recruitment of ubiquitin-specific protease USP15 by spliceosome recycling factor SART3. J Biol Chem 291(33):17283–17292.  https://doi.org/10.1074/jbc.M116.740787. Epub 2016 Jun 2. PubMed PMID: 27255711; PubMed Central PMCID: PMC5016127PubMedCrossRefGoogle Scholar
  140. Zhang Z, Devarajan P, Dorfman AL, Morrow JS (1998) Structure of the ankyrin-binding domain of alpha-Na,K-ATPase. J Biol Chem;273(30):18681–18684. PubMed PMID: 9668035Google Scholar
  141. Zhavoronkov A, Izumchenko E, Kanherkar RR, Teka M, Cantor C, Manaye K et al (2016) Pro-fibrotic pathway activation in trabecular meshwork and lamina cribrosa is the main driving force of glaucoma. Cell Cycle 15(12):1643–1652.  https://doi.org/10.1080/15384101.2016.1170261 CrossRefPubMedPubMedCentralGoogle Scholar
  142. Zweifel ME, Leahy DJ, Hughson FM, Barrick D (2003) Structure and stability of the ankyrin domain of the Drosophila Notch receptor. Protein Sci 12:2622–2632PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Natalya Kurochkina
    • 1
  1. 1.Department of BiophysicsSchool of Theoretical ModelingWashington, DCUSA

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