Group “Protein-protein interactions”

Nikolai N. Sluchanko
Ph.D. (Biology)
Head of the Group
INBI, build. 1, room 335
Телефон+7 (495) 660-34-30 ext. 462

Main achievements:

The main focus of studies on universal adaptor proteins of the 14-3-3 family is on investigation of their interaction with different medically relevant protein partners and its regulation by phosphorylation, from biochemical and structural point of view, with a perspective of therapeutic intervention in a long run. The research interests also include structural-functional studies of the steroidogenic acute regulatory protein (StAR), responsible for the delivery of cholesterol to mitochondria during steroidogenesis, and its ligand selectivity; alpha-synuclein and tau protein involved in the process of neurodegeneration accompanying a range of human disorders.

The second direction is devoted i) to studies of protein-protein interactions in the context of the cyanobacterial photoprotection mechanism regulated by the orange carotenoid protein (OCP) and fluorescence recovery protein (FRP), ii) to the unique protein-to-protein carotenoid transfer process discovered in 2017 and iii) to the structural rearrangements within OCP upon its photoactivation.


Selected publications:

  1. Maksimov EG, Zamaraev AV, Parshina EY, Slonimskiy YB, Slastnikova TA, Abdrakhmanov AA, Babaev PA, Efimova SS, Ostroumova OS, Stepanov AV, Slutskaya EA, Ryabova AV, Friedrich T, Sluchanko NN. Soluble Cyanobacterial Carotenoprotein as a Robust Antioxidant Nanocarrier and Delivery Module. Antioxidants (Basel). 2020 Sep 15;9(9):E869. doi: 10.3390/antiox9090869. PMID: 32942578.
  2. Maksimov EG, Laptev GY, Blokhin DS, Klochkov VV, Slonimskiy YB, Sluchanko NN, Friedrich T, Chang CF, Polshakov VI. NMR resonance assignment and backbone dynamics of a C-terminal domain homolog of orange carotenoid protein. Biomol NMR Assign. 2020 Sep 16. doi: 10.1007/s12104-020-09976-1. Epub ahead of print. PMID: 32939684.
  3. Bezsudnova, E.Y.; Nikolaeva, A.Y.; Kleymenov, S.Y.; Petrova, T.E.; Zavialova, S.A.; Tugaeva, K.V.; Sluchanko, N.N.; Popov, V.O. Counterbalance of Stability and Activity Observed for Thermostable Transaminase from Thermobaculum terrenum in the Presence of Organic Solvents. Catalysts 2020, 10, 1024.
  4. Kulbatskii DS, Shulepko MA, Sluchanko NN, Yablokov EO, Kamyshinsky RA, Chesnokov YM, Kirpichnikov MP, Lyukmanova EN. Efficient screening of ligand-receptor complex formation using fluorescence labeling and size-exclusion chromatography. Biochem Biophys Res Commun. 2020 Aug 20:S0006-291X(20)31566-7. doi: 10.1016/j.bbrc.2020.08.021. Epub ahead of print. PMID: 32828540.
  5. Tugaeva KV, Remeeva A, Gushchin I, Cooley RB, Sluchanko NN. Design, expression, purification and crystallization of human 14-3-3ζ protein chimera with phosphopeptide from proapoptotic protein BAD. Protein Expr Purif. 2020. Nov;175:105707. doi: 10.1016/j.pep.2020.105707. Epub 2020 Jul 16. PMID: 32682909.
  6. Maksimov EG, Protasova EA, Tsoraev GV, Yaroshevich IA, Maydykovskiy AI, Shirshin EA, Gostev TS, Jelzow A, Moldenhauer M, Slonimskiy YB, Sluchanko NN, Friedrich T. Probing of carotenoid-tryptophan hydrogen bonding dynamics in the single-tryptophan photoactive Orange Carotenoid Protein. Sci Rep. 2020 July. 16;10(1):11729. doi: 10.1038/s41598-020-68463-8. PMID: 32678150; PMCID: PMC7366913.
  7. Tugaeva KV, Titterington J, Sotnikov DV, Maksimov EG, Antson AA, Sluchanko NN. Molecular basis for the recognition of steroidogenic acute regulatory protein by the 14-3-3 protein family. FEBS J. 2020 Jul 6. doi: 10.1111/febs.15474. Epub ahead of print. PMID: 32633081.
  8. Gogl G, Jane P, Caillet-Saguy C, Kostmann C, Bich G, Cousido-Siah A, Nyitray L, Vincentelli R, Wolff N, Nomine Y, Sluchanko NN, Trave G. Dual Specificity PDZ- and 14-3-3-Binding Motifs: A Structural and Interactomics Study. Structure. 2020 Jul 7;28(7):747-759.e3. doi: 10.1016/j.str.2020.03.010. Epub 2020 Apr 14. PMID: 32294469.
  9. Sluchanko NN. Reading the phosphorylation code: binding of the 14-3-3 protein to multivalent client phosphoproteins. Biochem J. 2020 Apr 17;477(7):1219-1225. doi: 10.1042/BCJ20200084. PMID: 32271882.
  10. Slonimskiy YB, Maksimov EG, Sluchanko NN. Fluorescence recovery protein: a powerful yet underexplored regulator of photoprotection in cyanobacteria. Photochem Photobiol Sci. 2020 Apr 9. doi: 10.1039/d0pp00015a. Epub ahead of print. PMID: 32270166.
  11. Slonimskiy YB, Maksimov EG, Lukashev EP, Moldenhauer M, Friedrich T, Sluchanko NN. Engineering the photoactive orange carotenoid protein with redox- controllable structural dynamics and photoprotective function. Biochim Biophys Acta Bioenerg. 2020 Jun 1;1861(5-6):148174. doi: 10.1016/j.bbabio.2020.148174. Epub 2020 Feb 12. PMID: 32059843.
  12. Y.V. Faletrov, V.S. Efimova, M.S. Horetski, K.V. Tugaeva, N.S. Frolova, Q. Lin, L.V. Isaeva, M.A. Rubtsov, N.N. Sluchanko, L.A. Novikova, V.M. Shkumatov, New 20-hydroxycholesterol-like compounds with fluorescent NBD or alkyne labels: Synthesis, in silico interactions with proteins and uptake by yeast cells, Chem Phys Lipids, 227 (2019) 104850.
  13. R.Y. Pishchalnikov, I.A. Yaroshevich, T.A. Slastnikova, A.A. Ashikhmin, A.V. Stepanov, E.A. Slutskaya, T. Friedrich, N.N. Sluchanko, E.G. Maksimov, Structural peculiarities of keto-carotenoids in water-soluble proteins revealed by simulation of linear absorption, Phys Chem Chem Phys, 21 (2019) 25707-25719.
  14. K.V. Tugaeva, D.I. Kalacheva, R.B. Cooley, S.V. Strelkov, N.N. Sluchanko, Concatenation of 14-3-3 with partner phosphoproteins as a tool to study their interaction, Sci Rep, 9 (2019) 15007.
  15. N.N. Sluchanko, D.M. Bustos, Intrinsic disorder associated with 14-3-3 proteins and their partners, Prog Mol Biol Transl Sci, 166 (2019) 19-61.
  16. T.B. Eronina, V.V. Mikhaylova, N.A. Chebotareva, V.V. Shubin, N.N. Sluchanko, B.I. Kurganov, Comparative effects of trehalose and 2-hydroxypropyl-beta-cyclodextrin on aggregation of UV-irradiated muscle glycogen phosphorylase b, Biochimie, 165 (2019) 196-205.
  17. E.G. Maksimov, W.J. Li, E.A. Protasova, T. Friedrich, B. Ge, S. Qin, N.N. Sluchanko, Hybrid coupling of R-phycoerythrin and the orange carotenoid protein supports the FRET-based mechanism of cyanobacterial photoprotection, Biochem Biophys Res Commun, 516 (2019) 699-704.
  18. E.G. Maksimov, I.A. Yaroshevich, G.V. Tsoraev, N.N. Sluchanko, E.A. Slutskaya, O.G. Shamborant, T.V. Bobik, T. Friedrich, A.V. Stepanov, A genetically encoded fluorescent temperature sensor derived from the photoactive Orange Carotenoid Protein, Sci Rep, 9 (2019) 8937.
  19. K.V. Tugaeva, N.N. Sluchanko, Steroidogenic Acute Regulatory Protein: Structure, Functioning, and Regulation, Biochemistry (Mosc), 84 (2019) S233-S253.
  20. Slonimskiy YB, Muzzopappa F, Maksimov EG, Wilson A, Friedrich T, Kirilovsky D, Sluchanko NN., Light-controlled carotenoid transfer between water-soluble proteins related to cyanobacterial photoprotection. FEBS J. 2019 Mar 7. doi: 10.1111/febs.14803.
  21. Chebotareva NA, Eronina TB, Roman SG, Mikhaylova VV, Sluchanko NN, Gusev NB, Kurganov BI., Oligomeric state of αB-crystallin under crowded conditions. Biochem Biophys Res Commun. 2019 Jan 22;508(4):1101-1105. doi: 10.1016/j.bbrc.2018.12.015.
  22. Klementiev KE, Maksimov EG, Gvozdev DA, Tsoraev GV, Protopopov FF, Elanskaya IV, Abramov SM, Dyakov MY, Ilyin VK, Nikolaeva NA, Moisenovich MM, Moisenovich AM, Slonimskiy YB, Sluchanko NN, Lebedev VM, Spassky AV, Friedrich T, Maksimov GV, Paschenko VZ, Rubin AB., Radioprotective role of cyanobacterial phycobilisomes. Biochim Biophys Acta Bioenerg. 2019 Feb 1;1860(2):121-128. doi: 10.1016/j.bbabio.2018.11.018.
  23. Sluchanko NN, Slonimskiy YB, Shirshin EA, Moldenhauer M, Friedrich T, Maksimov EG, OCP–FRP protein complex topologies suggest a mechanism for controlling high light tolerance in cyanobacteria, Nature communications (2018) 9: 3869, doi: 10.1038/s41467-018-06195-0.
  24. Harris D, Wilson A, Muzzopappa F, Sluchanko NN, Friedrich T, Maksimov EG, Kirilovsky D, Adir N. Structural rearrangements in the C-terminal domain homolog of Orange Carotenoid Protein are crucial for carotenoid transfer, Communications Biology (2018) 1: 125, doi: 10.1038/s42003-018-0132-5.
  25. Klychnikov OI, Shamorkina TM, Weeks SD, van Leeuwen HC, Corver J, Drijfhout JW, van Veelen PA, Sluchanko NN, Strelkov SV, Hensbergen PJ (2018) Discovery of a new Pro-Pro endopeptidase, PPEP-2, provides mechanistic insights into the differences in substrate specificity within the PPEP family. J Biol Chem 293: 11154-11165
  26. Rovnyagina NR, Sluchanko NN, Tikhonova TN, Fadeev VV, Litskevich AY, Maskevich AA, Shirshin EA (2018) Binding of thioflavin T by albumins: An underestimated role of protein oligomeric heterogeneity. Int J Biol Macromol 108: 284-290
  27. Slonimskiy YB, Maksimov EG, Lukashev EP, Moldenhauer M, Jeffries CM, Svergun DI, Friedrich T, Sluchanko NN (2018) Functional interaction of low-homology FRPs from different cyanobacteria with Synechocystis OCP. Biochim Biophys Acta 1859: 382-393
  28. Sluchanko NN (2018) Association of Multiple Phosphorylated Proteins with the 14-3-3 Regulatory Hubs: Problems and Perspectives. J Mol Biol 430: 20-26
  29. Tikhonova TN, Rovnyagina NR, Zherebker AY, Sluchanko NN, Rubekina AA, Orekhov AS, Nikolaev EN, Fadeev VV, Uversky VN, Shirshin EA (2018) Dissection of the deep-blue autofluorescence changes accompanying amyloid fibrillation. Arch Biochem Biophys 651: 13-20
  30. Tugaeva KV, Faletrov YV, Allakhverdiev ES, Shkumatov VM, Maksimov EG, Sluchanko NN (2018) Effect of the NBD-group position on interaction of fluorescently-labeled cholesterol analogues with human steroidogenic acute regulatory protein STARD1. Biochem Biophys Res Commun 497: 58-64
  31. K.V. Tugaeva, P.O. Tsvetkov, N.N. Sluchanko, Bacterial co-expression of human Tau protein with protein kinase A and 14-3-3 for studies of 14-3-3/phospho-Tau interaction, PLoS One, 12 (2017) e0178933.
  32.  N.N. Sluchanko, K.V. Tugaeva, E.G. Maksimov, Solution structure of human steroidogenic acute regulatory protein STARD1 studied by small-angle X-ray scattering, Biochem Biophys Res Commun, 489 (2017) 445-450.
  33. N.N. Sluchanko, Y.B. Slonimskiy, M. Moldenhauer, T. Friedrich, E.G. Maksimov, Deletion of the short N-terminal extension in OCP reveals the main site for FRP binding, FEBS Lett, 591 (2017) 1667-1676.
  34. N.N. Sluchanko, Y.B. Slonimskiy, E.G. Maksimov, Features of Protein−Protein Interactions in the Cyanobacterial Photoprotection Mechanism, Biochemistry (Moscow), 82 (2017) 1592-1614.
  35. N.N. Sluchanko, K.E. Klementiev, E.A. Shirshin, G.V. Tsoraev, T. Friedrich, E.G. Maksimov, The purple Trp288Ala mutant of Synechocystis OCP persistently quenches phycobilisome fluorescence and tightly interacts with FRP, Biochim Biophys Acta, 1858 (2017) 1-11.
  36. N.N. Sluchanko, K.V. Tugaeva, S.J. Greive, A.A. Antson, Chimeric 14-3-3 proteins for unraveling interactions with intrinsically disordered partners, Sci Rep, 7 (2017) 12014.
  37. N.N. Sluchanko, N.B. Gusev, Moonlighting chaperone-like activity of the universal regulatory 14-3-3 proteins, FEBS J, 284 (2017) 1279-1295.
  38. N.N. Sluchanko, S. Beelen, A.A. Kulikova, S.D. Weeks, A.A. Antson, N.B. Gusev, S.V. Strelkov, Structural Basis for the Interaction of a Human Small Heat Shock Protein with the 14-3-3 Universal Signaling Regulator, Structure, 25 (2017) 305-316.
  39. E.A. Shirshin, E.E. Nikonova, F.I. Kuzminov, N.N. Sluchanko, I.V. Elanskaya, M.Y. Gorbunov, V.V. Fadeev, T. Friedrich, E.G. Maksimov, Biophysical modeling of in vitro and in vivo processes underlying regulated photoprotective mechanism in cyanobacteria, Photosynth Res, 133 (2017) 261-271.
  40. M. Moldenhauer, N.N. Sluchanko, N.N. Tavraz, C. Junghans, D. Buhrke, M. Willoweit, L. Chiappisi, F.J. Schmitt, V. Vukojevic, E.A. Shirshin, V.Y. Ponomarev, V.Z. Paschenko, M. Gradzielski, E.G. Maksimov, T. Friedrich, Interaction of the signaling state analog and the apoprotein form of the orange carotenoid protein with the fluorescence recovery protein, Photosynth Res, (2017). doi: 10.1007/s11120-017-0346-2
  41. M. Moldenhauer, N.N. Sluchanko, D. Buhrke, D.V. Zlenko, N.N. Tavraz, F.J. Schmitt, P. Hildebrandt, E.G. Maksimov, T. Friedrich, Assembly of photoactive orange carotenoid protein from its domains unravels a carotenoid shuttle mechanism, Photosynth Res, 133 (2017) 327-341.
  42. E.G. Maksimov, N.N. Sluchanko, Y.B. Slonimskiy, E.A. Slutskaya, A.V. Stepanov, A.M. Argentova-Stevens, E.A. Shirshin, G.V. Tsoraev, K.E. Klementiev, O.V. Slatinskaya, E.P. Lukashev, T. Friedrich, V.Z. Paschenko, A.B. Rubin, The photocycle of orange carotenoid protein conceals distinct intermediates and asynchronous changes in the carotenoid and protein components, Sci Rep, 7 (2017) 15548.
  43. E.G. Maksimov, N.N. Sluchanko, Y.B. Slonimskiy, K.S. Mironov, K.E. Klementiev, M. Moldenhauer, T. Friedrich, D.A. Los, V.Z. Paschenko, A.B. Rubin, The Unique Protein-to-Protein Carotenoid Transfer Mechanism, Biophys J, 113 (2017) 402-414.
  44. E.G. Maksimov, N.N. Sluchanko, K.S. Mironov, E.A. Shirshin, K.E. Klementiev, G.V. Tsoraev, M. Moldenhauer, T. Friedrich, D.A. Los, S.I. Allakhverdiev, V.Z. Paschenko, A.B. Rubin, Fluorescent Labeling Preserving OCP Photoactivity Reveals Its Reorganization during the Photocycle, Biophys J, 112 (2017) 46-56.
  45. N.N. Sluchanko, K.V. Tugaeva, Y.V. Faletrov, D.I. Levitsky, High-yield soluble expression, purification and characterization of human steroidogenic acute regulatory protein (StAR) fused to a cleavable Maltose-Binding Protein (MBP), Protein Expr Purif, 119 (2016) 27-35.
  46. E.G. Maksimov, M. Moldenhauer, E.A. Shirshin, E.A. Parshina, N.N. Sluchanko, K.E. Klementiev, G.V. Tsoraev, N.N. Tavraz, M. Willoweit, F.J. Schmitt, J. Breitenbach, G. Sandmann, V.Z. Paschenko, T. Friedrich, A.B. Rubin, A comparative study of three signaling forms of the orange carotenoid protein, Photosynth Res, 130 (2016) 389-401.
  47. A.A. Karpulevich, E.G. Maksimov, N.N. Sluchanko, A.N. Vasiliev, V.Z. Paschenko, Highly efficient energy transfer from quantum dot to allophycocyanin in hybrid structures, J Photochem Photobiol B, 160 (2016) 96-101.
  48. M.V. Sudnitsyna, N.N. Sluchanko, N.B. Gusev, HspB6 (Hsp20) as a versatile molecular regulator, Springer, Switzerland, 2015. The Big Book on Small Heat Shock Proteins, Chapter 9, pp. 229-253
  49. N.N. Sluchanko, V.N. Uversky, Hidden disorder propensity of the N-terminal segment of universal adapter protein 14-3-3 is manifested in its monomeric form: Novel insights into protein dimerization and multifunctionality, Biochim Biophys Acta, 1854 (2015) 492-504.
  50. N.N. Sluchanko, N.A. Chebotareva, N.B. Gusev, Quaternary structure of human small heat shock protein HSPB6 (Hsp20) in crowded media modeled by trimethylamine N-oxide (TMAO): Effect of protein phosphorylation, Biochimie, 108 (2015) 68-75.
  51. A.M. Matyushenko, N.V. Artemova, N.N. Sluchanko, D.I. Levitsky, Effects of two stabilizing substitutions, D137L and G126R, in the middle part of alpha-tropomyosin on the domain structure of its molecule, Biophys Chem, 196 (2015) 77-85.
  52. E.G. Maksimov, E.A. Shirshin, N.N. Sluchanko, D.V. Zlenko, E.Y. Parshina, G.V. Tsoraev, K.E. Klementiev, G.S. Budylin, F.J. Schmitt, T. Friedrich, V.V. Fadeev, V.Z. Paschenko, A.B. Rubin, The Signaling State of Orange Carotenoid Protein, Biophys J, 109 (2015) 595-607.
  53. D.S. Logvinova, D.I. Markov, O.P. Nikolaeva, N.N. Sluchanko, D.S. Ushakov, D.I. Levitsky, Does Interaction between the Motor and Regulatory Domains of the Myosin Head Occur during ATPase Cycle? Evidence from Thermal Unfolding Studies on Myosin Subfragment 1, PLoS One, 10 (2015) e0137517.
  54. N.A. Chebotareva, T.B. Eronina, N.N. Sluchanko, B.I. Kurganov, Effect of Ca2+ and Mg2+ ions on oligomeric state and chaperone-like activity of alphaB-crystallin in crowded media, Int J Biol Macromol, 76 (2015) 86-93.
  55. N.N. Sluchanko, S.G. Roman, N.A. Chebotareva, N.B. Gusev, Chaperone-like activity of monomeric human 14-3-3zeta on different protein substrates, Arch Biochem Biophys, 549 (2014) 32-39.
  56. A.M. Matyushenko, N.V. Artemova, D.V. Shchepkin, G.V. Kopylova, S.Y. Bershitsky, A.K. Tsaturyan, N.N. Sluchanko, D.I. Levitsky, Structural and functional effects of two stabilizing substitutions, D137L and G126R, in the middle part of alpha-tropomyosin molecule, FEBS J, 281 (2014) 2004-2016.
  57. T.B. Eronina, N.A. Chebotareva, N.N. Sluchanko, V.V. Mikhaylova, V.F. Makeeva, S.G. Roman, S.Y. Kleymenov, B.I. Kurganov, Dual effect of arginine on aggregation of phosphorylase kinase, Int J Biol Macromol, 68 (2014) 225-232.
  58. N.N. Sluchanko, N.A. Chebotareva, N.B. Gusev, Modulation of 14-3-3/phosphotarget interaction by physiological concentrations of phosphate and glycerophosphates, PLoS One, 8 (2013) e72597.
  59. N.N. Sluchanko, N.V. Artemova, M.V. Sudnitsyna, I.V. Safenkova, A.A. Antson, D.I. Levitsky, N.B. Gusev, Monomeric 14-3-3zeta has a chaperone-like activity and is stabilized by phosphorylated HspB6, Biochemistry, 51 (2012) 6127-6138.
  60. P.N. Datskevich, E.V. Mymrikov, N.N. Sluchanko, A.A. Shemetov, M.V. Sudnitsyna, N.B. Gusev, Expression, purification and some properties of fluorescent chimeras of human small heat shock proteins, Protein Expr Purif, 82 (2012) 45-54.
  61. N.N. Sluchanko, N.B. Gusev, Oligomeric structure of 14-3-3 protein: what do we know about monomers?, FEBS Lett, 586 (2012) 4249-4256.
  62. N.N. Sluchanko, M.V. Sudnitsyna, A.S. Seit-Nebi, A.A. Antson, N.B. Gusev, Properties of the monomeric form of human 14-3-3zeta protein and its interaction with tau and HspB6, Biochemistry, 50 (2011) 9797-9808.
  63. N.N. Sluchanko, N.B. Gusev, Probable participation of 14-3-3 in tau protein oligomerization and aggregation, J Alzheimers Dis, 27 (2011) 467-476.
  64. N.N. Sluchanko, M.V. Sudnitsyna, I.S. Chernik, A.S. Seit-Nebi, N.B. Gusev, Phosphomimicking mutations of human 14-3-3zeta affect its interaction with tau protein and small heat shock protein HspB6, Arch Biochem Biophys, 506 (2011) 24-34.
  65. E.G. Maksimov, T.S. Gostev, F.I. Kuz’minov, N.N. Sluchanko, I.N. Stadnichuk, V.Z. Pashchenko, A.B. Rubin, Hybrid systems of quantum dots mixed with the photosensitive protein phycoerythrin, Nanotechnologies in Russia, 5 (2010) 531-537.
  66. N.N. Sluchanko, N.B. Gusev, 14-3-3 proteins and regulation of cytoskeleton, Biochemistry (Mosc), 75 (2010) 1528-1546.
  67. N.N. Sluchanko, A.S. Seit-Nebi, N.B. Gusev, Effect of phosphorylation on interaction of human tau protein with 14-3-3zeta, Biochem Biophys Res Commun, 379 (2009) 990-994.
  68. N.N. Sluchanko, A.S. Seit-Nebi, N.B. Gusev, Phosphorylation of more than one site is required for tight interaction of human tau protein with 14-3-3zeta, FEBS Lett, 583 (2009) 2739-2742.
  69. N.N. Sluchanko, I.S. Chernik, A.S. Seit-Nebi, A.V. Pivovarova, D.I. Levitsky, N.B. Gusev, Effect of mutations mimicking phosphorylation on the structure and properties of human 14-3-3zeta, Arch Biochem Biophys, 477 (2008) 305-312.