Advertisement

Archives of Virology

, Volume 163, Issue 6, pp 1531–1547 | Cite as

New tetrameric forms of the rotavirus NSP4 with antiparallel helices

  • Sushant Kumar
  • Raghavendra Ramappa
  • Kiranmayee Pamidimukkala
  • C. D. Rao
  • K. Suguna
Original Article

Abstract

Rotavirus nonstructural protein 4, the first viral enterotoxin to be identified, is a multidomain, multifunctional glycoprotein. Earlier, we reported a Ca2+-bound coiled-coil tetrameric structure of the diarrhea-inducing region of NSP4 from the rotavirus strains SA11 and I321 and a Ca2+-free pentameric structure from the rotavirus strain ST3, all with a parallel arrangement of α-helices. pH was found to determine the oligomeric state: a basic pH favoured a tetramer, whereas an acidic pH favoured a pentamer. Here, we report two novel forms of the coiled-coil region of NSP4 from the bovine rotavirus strains MF66 and NCDV. These crystallized at acidic pH, forming antiparallel coiled-coil tetrameric structures without any bound Ca2+ ion. Structural and mutational studies of the coiled-coil regions of NSP4 revealed that the nature of the residue at position 131 (Tyr/His) plays an important role in the observed structural diversity.

Notes

Acknowledgements

This research was funded by the Department of Biotechnology (DBT) – Indian Institute of Science (IISc) Partnership Program for Advanced Research in Biological Sciences and Bioengineering. Diffraction data were collected at the X-ray Facility for Structural Biology at the Molecular Biophysics Unit, IISc, supported by the Department of Science and Technology, Government of India. SK acknowledges the Council of Scientific and Industrial Research, Government of India, for providing a research fellowship.

Compliance of ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical approval

Necessary approvals from Institutional Biosafety Committee and Animal Ethics Committee were obtained prior to the start of animal experiments. This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

705_2018_3753_MOESM1_ESM.pdf (28 kb)
Supplementary Material 1 Lack of correlation between the diarrhea-inducing ability of NSP4ΔN72 deletion mutant proteins and the virulence of rotavirus strains. The DD50 of ΔN72 recombinant protein from the bovine strain MF66 was determined in this study. The values for the protein from other strains were reported by us previously (PDF 27 kb)
705_2018_3753_MOESM2_ESM.pdf (895 kb)
Supplementary Material 2 Sequence alignment of NSP4 from different strains of rotavirus. Residues at positions 120, 131 and 133 are highlighted in yellow, green and blue, respectively (PDF 894 kb)

References

  1. 1.
    Roberts L (2004) Vaccines. Rotavirus vaccines’ second chance. Science 305(5692):1890–1893.  https://doi.org/10.1126/science.305.5692.1890 CrossRefPubMedGoogle Scholar
  2. 2.
    Ball JM, Tian P, Zeng CQ, Morris AP, Estes MK (1996) Age-dependent diarrhea induced by a rotaviral nonstructural glycoprotein. Science 272(5258):101–104CrossRefPubMedGoogle Scholar
  3. 3.
    Ball JM, Mitchell DM, Gibbons TF, Parr RD (2005) Rotavirus NSP4: a multifunctional viral enterotoxin. Viral Immunol 18(1):27–40.  https://doi.org/10.1089/vim.2005.18.27 CrossRefPubMedGoogle Scholar
  4. 4.
    Lopez T, Camacho M, Zayas M, Najera R, Sanchez R, Arias CF, Lopez S (2005) Silencing the morphogenesis of rotavirus. J Virol 79(1):184–192.  https://doi.org/10.1128/JVI.79.1.184-192.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Silvestri LS, Tortorici MA, Vasquez-Del Carpio R, Patton JT (2005) Rotavirus glycoprotein NSP4 is a modulator of viral transcription in the infected cell. J Virol 79(24):15165–15174.  https://doi.org/10.1128/JVI.79.24.15165-15174.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bergmann CC, Maass D, Poruchynsky MS, Atkinson PH, Bellamy AR (1989) Topology of the non-structural rotavirus receptor glycoprotein NS28 in the rough endoplasmic reticulum. EMBO J 8(6):1695–1703PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Mirazimi A, Magnusson KE, Svensson L (2003) A cytoplasmic region of the NSP4 enterotoxin of rotavirus is involved in retention in the endoplasmic reticulum. J Gen Virol 84(Pt 4):875–883.  https://doi.org/10.1099/vir.0.18786-0 CrossRefPubMedGoogle Scholar
  8. 8.
    Taylor JA, O’Brien JA, Yeager M (1996) The cytoplasmic tail of NSP4, the endoplasmic reticulum-localized non-structural glycoprotein of rotavirus, contains distinct virus binding and coiled coil domains. EMBO J 15(17):4469–4476PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Storey SM, Gibbons TF, Williams CV, Parr RD, Schroeder F, Ball JM (2007) Full-length, glycosylated NSP4 is localized to plasma membrane caveolae by a novel raft isolation technique. J Virol 81(11):5472–5483.  https://doi.org/10.1128/JVI.01862-06 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Xu A, Bellamy AR, Taylor JA (2000) Immobilization of the early secretory pathway by a virus glycoprotein that binds to microtubules. EMBO J 19(23):6465–6474.  https://doi.org/10.1093/emboj/19.23.6465 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Bugarcic A, Taylor JA (2006) Rotavirus nonstructural glycoprotein NSP4 is secreted from the apical surfaces of polarized epithelial cells. J Virol 80(24):12343–12349.  https://doi.org/10.1128/JVI.01378-06 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Zhang M, Zeng CQ, Morris AP, Estes MK (2000) A functional NSP4 enterotoxin peptide secreted from rotavirus-infected cells. J Virol 74(24):11663–11670CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Jagannath MR, Kesavulu MM, Deepa R, Sastri PN, Kumar SS, Suguna K, Rao CD (2006) N- and C-terminal cooperation in rotavirus enterotoxin: novel mechanism of modulation of the properties of a multifunctional protein by a structurally and functionally overlapping conformational domain. J Virol 80(1):412–425.  https://doi.org/10.1128/JVI.80.1.412-425.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Au KS, Mattion NM, Estes MK (1993) A subviral particle binding domain on the rotavirus nonstructural glycoprotein NS28. Virology 194(2):665–673.  https://doi.org/10.1006/viro.1993.1306 CrossRefPubMedGoogle Scholar
  15. 15.
    Taylor JA, O’Brien JA, Lord VJ, Meyer JC, Bellamy AR (1993) The RER-localized rotavirus intracellular receptor: a truncated purified soluble form is multivalent and binds virus particles. Virology 194(2):807–814.  https://doi.org/10.1006/viro.1993.1322 CrossRefPubMedGoogle Scholar
  16. 16.
    Dong Y, Zeng CQ, Ball JM, Estes MK, Morris AP (1997) The rotavirus enterotoxin NSP4 mobilizes intracellular calcium in human intestinal cells by stimulating phospholipase C-mediated inositol 1,4,5-trisphosphate production. Proc Natl Acad Sci USA 94(8):3960–3965CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Estes MK, Kang G, Zeng CQ, Crawford SE, Ciarlet M (2001) Pathogenesis of rotavirus gastroenteritis. Novartis Found Symp 238:82–96 (discussion 96–100) PubMedGoogle Scholar
  18. 18.
    Tian P, Hu Y, Schilling WP, Lindsay DA, Eiden J, Estes MK (1994) The nonstructural glycoprotein of rotavirus affects intracellular calcium levels. J Virol 68(1):251–257PubMedPubMedCentralGoogle Scholar
  19. 19.
    Newton K, Meyer JC, Bellamy AR, Taylor JA (1997) Rotavirus nonstructural glycoprotein NSP4 alters plasma membrane permeability in mammalian cells. J Virol 71(12):9458–9465PubMedPubMedCentralGoogle Scholar
  20. 20.
    Tian P, Ball JM, Zeng CQ, Estes MK (1996) The rotavirus nonstructural glycoprotein NSP4 possesses membrane destabilization activity. J Virol 70(10):6973–6981PubMedPubMedCentralGoogle Scholar
  21. 21.
    Ousingsawat J, Mirza M, Tian Y, Roussa E, Schreiber R, Cook DI, Kunzelmann K (2011) Rotavirus toxin NSP4 induces diarrhea by activation of TMEM16A and inhibition of Na+ absorption. Pflugers Arch 461(5):579–589.  https://doi.org/10.1007/s00424-011-0947-0 CrossRefPubMedGoogle Scholar
  22. 22.
    Seo NS, Zeng CQ, Hyser JM, Utama B, Crawford SE, Kim KJ, Hook M, Estes MK (2008) Integrins alpha1beta1 and alpha2beta1 are receptors for the rotavirus enterotoxin. Proc Natl Acad Sci USA 105(26):8811–8818.  https://doi.org/10.1073/pnas.08039341050803934105 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Boshuizen JA, Rossen JW, Sitaram CK, Kimenai FF, Simons-Oosterhuis Y, Laffeber C, Buller HA, Einerhand AW (2004) Rotavirus enterotoxin NSP4 binds to the extracellular matrix proteins laminin-beta3 and fibronectin. J Virol 78(18):10045–10053.  https://doi.org/10.1128/JVI.78.18.10045-10053.200478/18/10045 CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Mirazimi A, Nilsson M, Svensson L (1998) The molecular chaperone calnexin interacts with the NSP4 enterotoxin of rotavirus in vivo and in vitro. J Virol 72(11):8705–8709PubMedPubMedCentralGoogle Scholar
  25. 25.
    Parr RD, Storey SM, Mitchell DM, McIntosh AL, Zhou M, Mir KD, Ball JM (2006) The rotavirus enterotoxin NSP4 directly interacts with the caveolar structural protein caveolin-1. J Virol 80(6):2842–2854.  https://doi.org/10.1128/JVI.80.6.2842-2854.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Hyser JM, Collinson-Pautz MR, Utama B, Estes MK (2010) Rotavirus disrupts calcium homeostasis by NSP4 viroporin activity. mBio 1(5).  https://doi.org/10.1128/mbio.00265-10e00265-10
  27. 27.
    Michelangeli F, Liprandi F, Chemello ME, Ciarlet M, Ruiz MC (1995) Selective depletion of stored calcium by thapsigargin blocks rotavirus maturation but not the cytopathic effect. J Virol 69(6):3838–3847PubMedPubMedCentralGoogle Scholar
  28. 28.
    Poruchynsky MS, Maass DR, Atkinson PH (1991) Calcium depletion blocks the maturation of rotavirus by altering the oligomerization of virus-encoded proteins in the ER. J Cell Biol 114(4):651–656CrossRefPubMedGoogle Scholar
  29. 29.
    Rajasekaran D, Sastri NP, Marathahalli JR, Indi SS, Pamidimukkala K, Suguna K, Rao CD (2008) The flexible C terminus of the rotavirus non-structural protein NSP4 is an important determinant of its biological properties. J Gen Virol 89(Pt 6):1485–1496.  https://doi.org/10.1099/vir.0.83617-089/6/1485 CrossRefPubMedGoogle Scholar
  30. 30.
    Sastri NP, Pamidimukkala K, Marathahalli JR, Kaza S, Rao CD (2011) Conformational differences unfold a wide range of enterotoxigenic abilities exhibited by rNSP4 peptides from different rotavirus strains. Open Virol J 5:124–135.  https://doi.org/10.2174/1874357901105010124 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Bowman GD, Nodelman IM, Levy O, Lin SL, Tian P, Zamb TJ, Udem SA, Venkataraghavan B, Schutt CE (2000) Crystal structure of the oligomerization domain of NSP4 from rotavirus reveals a core metal-binding site. J Mol Biol 304(5):861–871.  https://doi.org/10.1006/jmbi.2000.4250S0022-2836(00)94250-5 CrossRefPubMedGoogle Scholar
  32. 32.
    Deepa R, Durga Rao C, Suguna K (2007) Structure of the extended diarrhea-inducing domain of rotavirus enterotoxigenic protein NSP4. Arch Virol 152(5):847–859.  https://doi.org/10.1007/s00705-006-0921-x CrossRefPubMedGoogle Scholar
  33. 33.
    Chacko AR, Arifullah M, Sastri NP, Jeyakanthan J, Ueno G, Sekar K, Read RJ, Dodson EJ, Rao DC, Suguna K (2011) Novel pentameric structure of the diarrhea-inducing region of the rotavirus enterotoxigenic protein NSP4. J Virol 85(23):12721–12732.  https://doi.org/10.1128/JVI.00349-11JVI.00349-11 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Sastri NP, Viskovska M, Hyser JM, Tanner MR, Horton LB, Sankaran B, Prasad BV, Estes MK (2014) Structural plasticity of the coiled-coil domain of rotavirus NSP4. J Virol 88(23):13602–13612.  https://doi.org/10.1128/JVI.02227-14JVI.02227-14 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Varshney B, Jagannath MR, Vethanayagam RR, Kodhandharaman S, Jagannath HV, Gowda K, Singh DK, Rao CD (2002) Prevalence of, and antigenic variation in, serotype G10 rotaviruses and detection of serotype G3 strains in diarrheic calves: implications for the origin of G10P11 or P11 type reassortant asymptomatic strains in newborn children in India. Arch Virol 147(1):143–165CrossRefPubMedGoogle Scholar
  36. 36.
    Shenoy AR, Visweswariah SS (2003) Site-directed mutagenesis using a single mutagenic oligonucleotide and DpnI digestion of template DNA. Anal Biochem 319(2):335–336CrossRefPubMedGoogle Scholar
  37. 37.
    Leslie AG (2006) The integration of macromolecular diffraction data. Acta Crystallogr Sect D Biol Crystallogr 62(Pt 1):48–57.  https://doi.org/10.1107/S0907444905039107 CrossRefGoogle Scholar
  38. 38.
    Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr Sect D Biol Crystallogr 62(Pt 1):72–82.  https://doi.org/10.1107/S0907444905036693 CrossRefGoogle Scholar
  39. 39.
    Pannu NS, Waterreus WJ, Skubak P, Sikharulidze I, Abrahams JP, de Graaff RA (2011) Recent advances in the CRANK software suite for experimental phasing. Acta Crystallogr Sect D Biol Crystallogr 67(Pt 4):331–337.  https://doi.org/10.1107/S0907444910052224 CrossRefGoogle Scholar
  40. 40.
    Schneider TR, Sheldrick GM (2002) Substructure solution with SHELXD. Acta Crystallogr Sect D Biol Crystallogr 58(Pt 10 Pt 2):1772–1779CrossRefGoogle Scholar
  41. 41.
    Cowtan K (2010) Recent developments in classical density modification. Acta Crystallogr Sect D Biol Crystallogr 66(Pt 4):470–478.  https://doi.org/10.1107/S090744490903947X CrossRefGoogle Scholar
  42. 42.
    Abrahams JP, Leslie AG (1996) Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr Sect D Biol Crystallogr 52(Pt 1):30–42.  https://doi.org/10.1107/S0907444995008754 CrossRefGoogle Scholar
  43. 43.
    Skubak P, Waterreus WJ, Pannu NS (2010) Multivariate phase combination improves automated crystallographic model building. Acta Crystallogr Sect D Biol Crystallogr 66(Pt 7):783–788.  https://doi.org/10.1107/S0907444910014642 CrossRefGoogle Scholar
  44. 44.
    Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr Sect D Biol Crystallogr 62(Pt 9):1002–1011.  https://doi.org/10.1107/s0907444906022116 CrossRefGoogle Scholar
  45. 45.
    Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr Sect D Biol Crystallogr 66(Pt 4):486–501.  https://doi.org/10.1107/S0907444910007493 CrossRefGoogle Scholar
  46. 46.
    Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr Sect D Biol Crystallogr 53(Pt 3):240–255.  https://doi.org/10.1107/S0907444996012255S0907444996012255 CrossRefGoogle Scholar
  47. 47.
    Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Biol Crystallogr 66(Pt 2):213–221.  https://doi.org/10.1107/S0907444909052925 CrossRefGoogle Scholar
  48. 48.
    McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40(Pt 4):658–674.  https://doi.org/10.1107/S0021889807021206 CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Morris AL, MacArthur MW, Hutchinson EG, Thornton JM (1992) Stereochemical quality of protein structure coordinates. Proteins 12(4):345–364.  https://doi.org/10.1002/prot.340120407 CrossRefPubMedGoogle Scholar
  50. 50.
    Krissinel E, Henrick K (2007) Inference of macromolecular assemblies from crystalline state. J Mol Biol 372(3):774–797.  https://doi.org/10.1016/j.jmb.2007.05.022 CrossRefPubMedGoogle Scholar
  51. 51.
    Kumar P, Bansal M (2012) HELANAL-Plus: a web server for analysis of helix geometry in protein structures. J Biomol Struct Dyn 30(6):773–783.  https://doi.org/10.1080/07391102.2012.689705 CrossRefPubMedGoogle Scholar
  52. 52.
    Cohen GH (1997) ALIGN: a program to superimpose protein coordinates, accounting for insertions and deletions. J Appl Crystallogr 30:1160–1161.  https://doi.org/10.1107/S0021889897006729 CrossRefGoogle Scholar
  53. 53.
    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera—a visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612.  https://doi.org/10.1002/jcc.20084 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Poisson–Boltzmann electrostatics calculations. Nucleic Acids Res 32:W665–W667.  https://doi.org/10.1093/nar/gkh381 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Banner DW, Kokkinidis M, Tsernoglou D (1987) Structure of the ColE1 rop protein at 1.7 A resolution. J Mol Biol 196(3):657–675CrossRefPubMedGoogle Scholar
  56. 56.
    Lewis M, Chang G, Horton NC, Kercher MA, Pace HC, Schumacher MA, Brennan RG, Lu P (1996) Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 271(5253):1247–1254CrossRefPubMedGoogle Scholar
  57. 57.
    Liu J, Zheng Q, Deng Y, Li Q, Kallenbach NR, Lu M (2007) Conformational specificity of the lac repressor coiled-coil tetramerization domain. Biochemistry 46(51):14951–14959.  https://doi.org/10.1021/bi701930d CrossRefPubMedGoogle Scholar
  58. 58.
    Yadav MK, Leman LJ, Price DJ, Brooks CL 3rd, Stout CD, Ghadiri MR (2006) Coiled coils at the edge of configurational heterogeneity. Structural analyses of parallel and antiparallel homotetrameric coiled coils reveal configurational sensitivity to a single solvent-exposed amino acid substitution. Biochemistry 45(14):4463–4473.  https://doi.org/10.1021/bi060092q CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Liu J, Zheng Q, Deng Y, Kallenbach NR, Lu M (2006) Conformational transition between four and five-stranded phenylalanine zippers determined by a local packing interaction. J Mol Biol 361(1):168–179.  https://doi.org/10.1016/j.jmb.2006.05.063 CrossRefPubMedGoogle Scholar
  60. 60.
    Foster AW, Osman D, Robinson NJ (2014) Metal preferences and metallation. J Biol Chem 289(41):28095–28103.  https://doi.org/10.1074/jbc.R114.588145 CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Sadler PJ, Viles JH (1996) 1H and (113)Cd NMR investigations of Cd(2+) and Zn(2+) binding sites on serum albumin: competition with Ca(2+), Ni(2+), Cu(2+), and Zn(2+). Inorg Chem 35(15):4490–4496CrossRefPubMedGoogle Scholar
  62. 62.
    Appenzeller-Herzog C, Hauri HP (2006) The ER-Golgi intermediate compartment (ERGIC): in search of its identity and function. J Cell Sci 119(Pt 11):2173–2183.  https://doi.org/10.1242/jcs.03019 CrossRefPubMedGoogle Scholar
  63. 63.
    Casey JR, Grinstein S, Orlowski J (2010) Sensors and regulators of intracellular pH. Nat Rev Mol Cell Biol 11(1):50–61.  https://doi.org/10.1038/nrm2820 CrossRefPubMedGoogle Scholar
  64. 64.
    Presnell SR, Cohen FE (1989) Topological distribution of four-alpha-helix bundles. Proc Natl Acad Sci USA 86(17):6592–6596CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Harris NL, Presnell SR, Cohen FE (1994) Four helix bundle diversity in globular proteins. J Mol Biol 236(5):1356–1368CrossRefPubMedGoogle Scholar
  66. 66.
    Bloomer AC, Champness JN, Bricogne G, Staden R, Klug A (1978) Protein disk of tobacco mosaic virus at 2.8 A resolution showing the interactions within and between subunits. Nature 276(5686):362–368CrossRefPubMedGoogle Scholar
  67. 67.
    Testa OD, Moutevelis E, Woolfson DN (2009) CC+: a relational database of coiled-coil structures. Nucleic Acids Res 37(Database issue):D315–D322.  https://doi.org/10.1093/nar/gkn675 CrossRefPubMedGoogle Scholar
  68. 68.
    Fujiwara Y, Minor DL Jr (2008) X-ray crystal structure of a TRPM assembly domain reveals an antiparallel four-stranded coiled-coil. J Mol Biol 383(4):854–870.  https://doi.org/10.1016/j.jmb.2008.08.059 CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Liu Y, Cheney MD, Gaudet JJ, Chruszcz M, Lukasik SM, Sugiyama D, Lary J, Cole J, Dauter Z, Minor W, Speck NA, Bushweller JH (2006) The tetramer structure of the Nervy homology two domain, NHR2, is critical for AML1/ETO’s activity. Cancer Cell 9(4):249–260.  https://doi.org/10.1016/j.ccr.2006.03.012 CrossRefPubMedGoogle Scholar
  70. 70.
    Scholey JE, Nithianantham S, Scholey JM, Al-Bassam J (2014) Structural basis for the assembly of the mitotic motor Kinesin-5 into bipolar tetramers. eLife 3:e02217.  https://doi.org/10.7554/elife.02217 CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Weninger K, Bowen ME, Chu S, Brunger AT (2003) Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations. Proc Natl Acad Sci USA 100(25):14800–14805.  https://doi.org/10.1073/pnas.2036428100 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Tsatskis Y, Kwok SC, Becker E, Gill C, Smith MN, Keates RA, Hodges RS, Wood JM (2008) Core residue replacements cause coiled-coil orientation switching in vitro and in vivo: structure-function correlations for osmosensory transporter ProP. Biochemistry 47(1):60–72.  https://doi.org/10.1021/bi7018173 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Sushant Kumar
    • 1
  • Raghavendra Ramappa
    • 2
  • Kiranmayee Pamidimukkala
    • 2
  • C. D. Rao
    • 2
  • K. Suguna
    • 1
  1. 1.Molecular Biophysics UnitIndian Institute of ScienceBangaloreIndia
  2. 2.Department of Microbiology and Cell BiologyIndian Institute of ScienceBangaloreIndia

Personalised recommendations