Skip to main content
SpringerLink
Log in

ATP-Dependent Lon Proteases in the Cellular Protein Quality Control System

  • REVIEW ARTICLE
  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

Abstract

The Protein Quality Control (PQC) system plays a leading role in maintaining the safety of the cellular proteome in all natural kingdoms. This review summarizes information about the structural and functional characteristics of molecular chaperones and energy-dependent proteases that form the PQC system, emphasizing the crucial role of proteins belonging to the AAA+ superfamily, with the focus on ATP-dependent Lon proteases as a special family in the PQC. Similarities and differences among the enzymes of individual Lon subfamilies are discussed in detail using up-to-date data, elucidating the structural features and unique mechanisms of functioning of these proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.
Fig. 11.

Similar content being viewed by others

REFERENCES

  1. Balchin, D., Hayer-Hartl, M., and Hartl, F.U., Science, 2016, vol. 353, p. aac4354. https://doi.org/10.1126/science.aac4354

    Article  CAS  PubMed  Google Scholar 

  2. Gottesman, S., Wickner, S., and Maurizi, M.R., Genes Dev., 1997, vol. 11, pp. 815–823. https://doi.org/10.1101/gad.11.7.815

    Article  CAS  PubMed  Google Scholar 

  3. Kovacs, D., Szabo, B., Pancsa, R., and Tompa, P., Arch. Biochem. Biophys., 2013, vol. 531, pp. 80–89. https://doi.org/10.1016/j.abb.2012.09.010

    Article  CAS  PubMed  Google Scholar 

  4. Jeng, W., Lee, S., Sung, N., Lee, J., and Tsai, F.T.F., F1000Res., 2015, vol. 4, p. 1448. https://doi.org/10.12688/f1000research.7214.1

    Article  Google Scholar 

  5. Schubert, U., Antón, L.C., Gibbs, J., Norbury, C.C., Yewdell, J.W., and Bennink, J.R., Nature, 2000, vol. 404, pp. 770–774. https://doi.org/10.1038/35008096

    Article  CAS  PubMed  Google Scholar 

  6. Clausen, L., Abildgaard, A.B., Gersing, S.K., Stein, A., Lindorff-Larsen, K., and Hartmann-Petersen, R., Adv. Protein Chem. Struct. Biol., 2019, vol. 114, pp. 61–83. https://doi.org/10.1016/bs.apcsb.2018.09.002

    Article  CAS  PubMed  Google Scholar 

  7. Mogk, A., Huber, D., and Bukau, B., Cold Spring Harb. Perspect. Biol., 2011, vol. 3, p. e02373-20. https://doi.org/10.1101/cshperspect.a004366

    Article  CAS  Google Scholar 

  8. Finka, A., Mattoo, R.U.H., and Goloubinoff, P., Annu. Rev. Biochem., 2016, vol. 85, pp. 715–742. https://doi.org/10.1146/annurev-biochem-060815-014124

    Article  CAS  PubMed  Google Scholar 

  9. Melnikov, E.E. and Rotanova, T.V., Russ. J. Bioorg. Chem., 2010, vol. 36, pp. 1–10. https://doi.org/10.1134/S1068162010010012

    Article  CAS  Google Scholar 

  10. Hoffmann, A., Bukau, B., and Kramer, G., Biochim. Biophys. Acta, 2010, vol. 1803, pp. 650–661. https://doi.org/10.1016/j.bbamcr.2010.01.017

    Article  CAS  PubMed  Google Scholar 

  11. Jee, H., J. Exerc. Rehabil., 2016, vol. 12, pp. 255–259. https://doi.org/10.12965/jer.1632642.321

    Article  PubMed  PubMed Central  Google Scholar 

  12. Richter, K., Haslbeck, M., and Buchner, J., Mol. Cell., 2010, vol. 40, pp. 253–266. https://doi.org/10.1016/j.molcel.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  13. Saibil, H., Nat. Rev. Mol. Cell Biol., 2013, vol. 14, pp. 630–642. https://doi.org/10.1038/nrm3658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dahiya, V. and Buchner, J., Adv. Protein Chem. Struct. Biol., 2019, vol. 114, pp. 1–60. https://doi.org/10.1016/bs.apcsb.2018.10.001

    Article  CAS  PubMed  Google Scholar 

  15. Mattoo, R.U.H. and Goloubinoff, P., Cell. Mol. Life Sci., 2014, vol. 71, pp. 3311–3325. https://doi.org/10.1007/s00018-014-1627-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Weibezahn, J., Bukau, B., and Mogk, A., Microbial. Cell Fact., 2004, vol. 3, p. 1. https://doi.org/10.1186/1475-2859-3-1

    Article  Google Scholar 

  17. Bascos, N.A.D. and Landry, S.J., Int. J. Mol. Sci., 2019, vol. 20, p. 6195. https://doi.org/10.3390/ijms20246195

    Article  CAS  PubMed Central  Google Scholar 

  18. Voos, W., Biochim. Biophys. Acta, 2013, vol. 1833, pp. 388–399. https://doi.org/10.1016/j.bbamcr.2012.06.005

    Article  CAS  PubMed  Google Scholar 

  19. Chakafana, G., Zininga, T., and Shonhai, A., Biomolecules, 2019, vol. 9, p. 543. https://doi.org/10.3390/biom9100543

    Article  CAS  PubMed Central  Google Scholar 

  20. Rosenzweig, R., Nillegoda, N.B., Mayer, M.P., and Bukau, B., Nat. Rev. Mol. Cell Biol., 2019, vol. 20, pp. 665–680. https://doi.org/10.1038/s41580-019-0133-3

    Article  CAS  PubMed  Google Scholar 

  21. Kampinga, H.H. and Craig, E.A., Nat. Rev. Mol. Cell Biol., 2010, vol. 11, pp. 579–592. https://doi.org/10.1038/nrm2941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Takakuwa, J.E., Nitika, Knighton, L.E., and Truman, A.W., Front. Mol. Biosci., 2019, vol. 6, p. 81. https://doi.org/10.3389/fmolb.2019.00081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Walter, S., Cell. Mol. Life Sci., 2002, vol. 59, pp. 1589–1597. https://doi.org/10.1007/pl00012485

    Article  CAS  PubMed  Google Scholar 

  24. Bar-Lavan, Y., Shemesh, N., and Ben-Zvi, A., Essays Biochem., 2016, vol. 60, pp. 237–253. https://doi.org/10.1042/EBC20160004

    Article  PubMed  Google Scholar 

  25. Taguchi, H., J. Mol. Biol., 2015, vol. 427, pp. 2912–2918. https://doi.org/10.1016/j.jmb.2015.04.007

    Article  CAS  PubMed  Google Scholar 

  26. Chaudhuri, T.K., Verma, V.K., and Maheshwari, A., Prog. Biophys. Mol. Biol., 2009, vol. 99, pp. 42–50. https://doi.org/10.1016/j.pbiomolbio.2008.10.007

    Article  CAS  PubMed  Google Scholar 

  27. Prodromou, C., Biochem. J., 2016, vol. 473, pp. 2439–2452. https://doi.org/10.1042/BCJ20160005

    Article  CAS  PubMed  Google Scholar 

  28. Li, J. and Buchner, J., Biomed. J., 2013, vol. 36, pp. 106–117. https://doi.org/10.4103/2319-4170.113230

    Article  PubMed  Google Scholar 

  29. Pearl, L.H., Biopolymers, 2016, vol. 105, pp. 594–607. https://doi.org/10.1002/bip.22835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Luengo, T.M., Mayer, M.P., and Rüdiger, S.G.D., Trends Cell Biol., 2019, vol. 29, pp. 164–177. https://doi.org/10.1016/j.tcb.2018.10.004

    Article  CAS  Google Scholar 

  31. Genest, O., Wickner, S., and Doyle, S.M., J. Biol. Chem., 2019, vol. 294, pp. 2109–2120. https://doi.org/10.1074/jbc.REV118.002806

    Article  CAS  PubMed  Google Scholar 

  32. Haslbeck, M. and Vierling, E., J. Mol. Biol., 2015, vol. 427, pp. 1537–1548. https://doi.org/10.1016/j.jmb.2015.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mogk, A., Ruger-Herreros, C., and Bukau, B., Annu. Rev. Microbiol., 2019, vol. 73, pp. 89–110. https://doi.org/10.1146/annurev-micro-020518-115515

    Article  CAS  PubMed  Google Scholar 

  34. Obuchowski, I. and Liberek. K., Cell Stress Chaperones, 2020, vol. 25, pp. 593–600. https://doi.org/10.1007/s12192-020-01094-0

    Article  PubMed  PubMed Central  Google Scholar 

  35. Haslbeck, M., Weinkauf, S., and Buchner, J., J. Biol. Chem., 2019, vol. 294, pp. 2121–2132. https://doi.org/10.1074/jbc.REV118.002809

    Article  CAS  PubMed  Google Scholar 

  36. Riedl, M., Strauch, A., Catici, D.A.M., and Haslbeck, M., Int. J. Mol. Sci., 2020, vol. 21, p. 5448. https://doi.org/10.3390/ijms21155448

    Article  CAS  PubMed Central  Google Scholar 

  37. Waters, E.R. and Vierling E., New Phytol., 2020, vol. 227, pp. 24–37. https://doi.org/10.1111/nph.16536

    Article  CAS  PubMed  Google Scholar 

  38. Neuwald, A.F., Aravind, L., Spouge, J.L., and Koonin, E.V., Genome Res., 1999, vol. 9, pp. 27–43. https://doi.org/10.1101/gr.9.1.27

    Article  CAS  PubMed  Google Scholar 

  39. Puchades, C., Sandate, C.R., and Lander G.C., Nat. Rev. Mol. Cell Biol., 2020, vol. 21, pp. 43–58. https://doi.org/10.1038/s41580-019-0183-6

    Article  CAS  PubMed  Google Scholar 

  40. Ogura, T. and Wilkinson, A.J., Genes Cells, 2001, vol. 6, pp. 575–597. https://doi.org/10.1046/j.1365-2443.2001.00447.x

    Article  CAS  PubMed  Google Scholar 

  41. Dougan, D.A., Mogk, A., Zeth, K., Turgay, K., and Bukau, B., FEBS Lett., 2002, vol. 529, pp. 6–10. https://doi.org/10.1016/s0014-5793(02)03179-4

    Article  CAS  PubMed  Google Scholar 

  42. Voos, W., Jaworek, W., Wilkening, A., and Bruderek, M., Essays Biochem., 2016, vol. 60, pp. 213–225. https://doi.org/10.1042/EBC20160009

    Article  PubMed  Google Scholar 

  43. Abrahão, J., Mokry, D.Z., and Ramos, C.H.I., Front. Mol. Biosci., 2017, vol. 4, p. 60. https://doi.org/10.3389/fmolb.2017.00060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Yokom, A.L., Gate, S.N., Jackrel, M.E., Mack, K.L., Su, M., Shorter, J., and Southworth, D.R., Nat. Struct. Mol. Biol., 2016, vol. 23, pp. 830–837. https://doi.org/10.1038/nsmb.3277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Barends, T.R., Werbeck, N.D., and Reinstein, J., Curr. Opin. Struct. Biol., 2010, vol. 20, pp. 46–53. https://doi.org/10.1016/j.sbi.2009.12.014

    Article  CAS  PubMed  Google Scholar 

  46. Miller, J.M., Lin, J., Li, T., and Lucius, A.L., J. Mol. Biol., 2013, vol. 425, pp. 2795–2812. https://doi.org/10.1016/j.jmb.2013.04.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Doyle, S.M. and Wickner, S., Trends Biochem. Sci., 2009, vol. 34, pp. 40–48. https://doi.org/10.1016/j.tibs.2008.09.010

    Article  CAS  PubMed  Google Scholar 

  48. Zolkiewski, M., Zhang, T., and Nagy, M., Arch. Biochem. Biophys., 2012, vol. 520, pp. 1–6. https://doi.org/10.1016/j.abb.2012.01.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lee, S., Sowa, M.E., Watanabe, Y.H., Sigler, P.B., Chiu, W., Yoshida, M., and Tsai, F.T., Cell, 2003, vol. 115, pp. 229–240. https://doi.org/10.1016/s0092-8674(03)00807-9

    Article  CAS  PubMed  Google Scholar 

  50. Schramm, F.D., Schroeder, K., and Jonas K., FEMS Microbiol. Rev., 2020, vol. 44, pp. 54–72. https://doi.org/10.1093/femsre/fuz026

    Article  CAS  PubMed  Google Scholar 

  51. Voos, W., Res. Microbiol., 2009, vol. 160, pp. 718–725. https://doi.org/10.1016/j.resmic.2009.08.003

    Article  CAS  PubMed  Google Scholar 

  52. Mogk, A., Kummer, E., and Bukau, B., Front. Mol. Biosci., 2015, vol. 2, pp. 22. https://doi.org/10.3389/fmolb.2015.00022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Watanabe, Y.H., Nakazaki, Y., Suno, R., and Yoshida, M., Biochem. J., 2009, vol. 421, pp. 71–77. https://doi.org/10.1042/BJ20082238

    Article  CAS  PubMed  Google Scholar 

  54. Gottesman, S., Annu. Rev. Cell Dev. Biol., 2003, vol. 19, pp. 565–587. https://doi.org/10.1146/annurev.cellbio.19.110701.153228

    Article  CAS  PubMed  Google Scholar 

  55. Koodathingal, P., Jaffe, N.E., Kraut, D.A., Prakash, S., Fishbain, S., Herman, C., and Matouschek, A., J. Biol. Chem., 2009, vol. 284, pp. 18674–18684. https://doi.org/10.1074/jbc.M900783200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Sauer, R.T. and Baker, T.A., Annu. Rev. Biochem., 2011, vol. 80, pp. 587–612. https://doi.org/10.1146/annurev-biochem-060408-172623

    Article  CAS  PubMed  Google Scholar 

  57. Mahmoud, S.A. and Chien, P., Annu. Rev. Biochem., 2018, vol. 87, pp. 677–696. https://doi.org/10.1146/annurev-biochem-062917-012848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Maupin-Furlow, J.A., Subcell Biochem., 2013, vol. 66, pp. 297–327. https://doi.org/10.1007/978-94-007-5940-4_11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Ciechanover, A., Cell, 1994, vol. 79, pp. 13–21. https://doi.org/10.1016/0092-8674(94)90396-4

    Article  CAS  PubMed  Google Scholar 

  60. Bard, J.A.M., Goodall, E.A., Green, E.R., Jonsson, E., Dong, K.C., and Martin, A., Annu. Rev. Biochem., 2018, vol. 87, pp. 697–724. https://doi.org/10.1146/annurev-biochem-062917-011931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ciechanover, A. and Stanhill, A., Biochim. Biophys. Acta, 2014, vol. 1843, pp. 86–96. https://doi.org/10.1016/j.bbamcr.2013.07.007

    Article  CAS  PubMed  Google Scholar 

  62. Kudriaeva, A., Kuzina, E.S., Zubenko, O., Smirnov, I.V., Belogurov, A., Jr., FASEB J., 2019, vol. 33, pp. 6852–6866. https://doi.org/10.1096/fj.201802237R

    Article  CAS  PubMed  Google Scholar 

  63. Iyer, L.M., Leipe, D.D., Koonin E.V., and Aravind, L., J. Struct. Biol., 2004, vol. 146, pp. 11–31. https://doi.org/10.1016/j.jsb.2003.10.010

    Article  CAS  PubMed  Google Scholar 

  64. Lupas, A.N. and Martin, J., Curr. Opin. Struct. Biol., 2002, vol. 12, pp. 746–753. https://doi.org/10.1016/s0959-440x(02)00388-3

    Article  CAS  PubMed  Google Scholar 

  65. Chang, C.W., Lee, S., and Tsai, F.T.F., Front. Mol. Biosci., 2017, vol. 4, pp. 27. https://doi.org/10.3389/fmolb.2017.00027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Miller, J.M. and Enemark, E.J., Archaea, 2016, vol. 2016, p. 9294307. https://doi.org/10.1155/2016/9294307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Wendler, P., Ciniawsky, S., Kock, M., and Kube, S., Biochim. Biophys. Acta, 2012, vol. 1823, pp. 2–14. https://doi.org/10.1016/j.bbamcr.2011.06.014

    Article  CAS  PubMed  Google Scholar 

  68. Ogura, T., Whiteheart, S.W., and Wilkinson, A.J., J. Struct. Biol., 2004, vol. 146, pp. 106–112. https://doi.org/10.1016/j.jsb.2003.11.008

    Article  CAS  PubMed  Google Scholar 

  69. Martin, A., Baker, T.A., and Sauer, R.T., Mol. Cell., 2008, vol. 29, pp. 441–450. https://doi.org/10.1016/j.molcel.2008.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Gur, E., Ottofueling, R., and Dougan, D.A., Subcell. Biochem., 2013, vol. 66, pp. 3–33. https://doi.org/10.1007/978-94-007-5940-4_1

    Article  CAS  PubMed  Google Scholar 

  71. Kirstein, J., Schlothauer, T., Dougan, D.A., Lilie, H., Tischendorf, G., Mogk, A., Bukau, B., and Turgay K., EMBO J., 2006, vol. 25, pp. 1481–1491. https://doi.org/10.1038/sj.emboj.7601042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Mogk, A. and Bukau, B., Curr. Biol., 2004, vol. 14, pp. 78–80. https://doi.org/10.1016/j.cub.2003.12.051

    Article  CAS  Google Scholar 

  73. Rotanova, T.V. and Melnikov, E.E., Biochem. Moscow Suppl. Ser. B. Biomed. Chem., 2008, vol. 2, pp. 245–257. https://doi.org/10.1134/S1990750808030049

    Article  Google Scholar 

  74. Sauer, R.T., Bolon, D.N., Burton, B.M., Burton, R.E., Flynn, J.M., Grant, R.A., Hersch, G.L., Joshi, S.A., Kenniston, J.A., Levchenko, I., Neher, S.B., Oakes, E.S., Siddiqui, S.M., Wah, D.A., and Baker, T.A., Cell, 2004, vol. 119, pp. 9–18. https://doi.org/10.1016/j.cell.2004.09.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kim, Y.I., Levchenko, I., Fraczkowska, K., Woodruff, R.V., Sauer, R.T., and Baker, T.A., Nat. Struct. Biol., 2001, vol. 8, pp. 230–233. https://doi.org/10.1038/84967

    Article  CAS  PubMed  Google Scholar 

  76. Olivares, A.O., Baker, T.A., and Sauer R.T., Nat. Rev. Microbiol., 2016, vol. 14, pp. 33–44. https://doi.org/10.1038/nrmicro.2015.4

    Article  CAS  PubMed  Google Scholar 

  77. Kirstein, J., Molière, N., Dougan, D.A., and Turgay, K., Nat. Rev. Microbiol., 2009, vol. 7, pp. 589–599. https://doi.org/10.1038/nrmicro2185

    Article  CAS  PubMed  Google Scholar 

  78. Mukherjee, S., Bree, A.C., Liu, J, Patrick, J.E., Chien, P., and Kearns, D.B., Proc. Natl. Acad. Sci. U.S.A., 2015, vol. 112, pp. 250–255. https://doi.org/10.1073/pnas.1417419112

    Article  CAS  PubMed  Google Scholar 

  79. Lo, J.H., Baker, T.A., and Sauer, R.T., Protein Sci., 2001, vol. 10, pp. 551–559. https://doi.org/10.1110/ps.41401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Kojetin, D.J., McLaughlin, P.D., Thompson, R.J., Dubnau, D., Prepiak, P., Rance, M., and Cavanagh, J., J. Mol. Biol., 2009, vol. 387, pp. 639–652. https://doi.org/10.1016/j.jmb.2009.01.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Elsholz, A.K.W., Birk, M.S., Charpentier, E., and Turgay, K., Front. Mol. Biosci., 2017, vol. 4, p. 44. https://doi.org/10.3389/fmolb.2017.00044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Hinnerwisch, J., Reid, B.G., Fenton, W.A., and Horwich, A.L., J. Biol. Chem., 2005, vol. 280, pp. 40838–40844. https://doi.org/10.1074/jbc.M507879200

    Article  CAS  PubMed  Google Scholar 

  83. Dougan, D.A., Reid, B.G., Horwich, A.L., and Bukau, B., Mol. Cell, 2002, vol. 9, pp. 673–683. https://doi.org/10.1016/s1097-2765(02)00485-9

    Article  CAS  PubMed  Google Scholar 

  84. Wang, F., Mei, Z., Qi, Y., Yan, C., Qi, H., Wang, J., and Shi, Y., Nature, 2011, vol. 471, pp. 331–335. https://doi.org/10.1038/nature09780

    Article  CAS  PubMed  Google Scholar 

  85. Mogk, A., Schlieker, C., Strub, C., Rist, W., Weibezahn, J., and Bukau, B., J. Biol. Chem., 2003, vol. 278, pp. 17615–17624. https://doi.org/10.1074/jbc.M209686200

    Article  CAS  PubMed  Google Scholar 

  86. Cashikar, A.G., Schirmer, E.C., Hattendorf, D.A., Glove,r J.R., Ramakrishnan, M.S., Ware, D.M., and Lindquist, S.L., Mol. Cell, 2002, vol. 9, pp. 751–760. https://doi.org/10.1016/S1097-2765(02)00499-9

    Article  CAS  PubMed  Google Scholar 

  87. Wendler, P., Shorter, J., Snead, D., Plisson, C., Clare, D.K., Lindquist, S., and Saibil, H.R., Mol. Cell, 2009, vol. 34, pp. 81–92. https://doi.org/10.1016/j.molcel.2009.02.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Donaldson, L.W., Wojtyra, U., and Houry, W.A., J. Biol. Chem., 2003, vol. 278, pp. 48991–48996. https://doi.org/10.1074/jbc.M307826200

    Article  CAS  PubMed  Google Scholar 

  89. Miethke, M., Hecker, M., and Gerth, U., J. Bacteriol., 2006, vol. 188, pp. 4610–4619. https://doi.org/10.1128/JB.00287-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Tomko, R.J., Jr. and Hochstrasser, M., Cell Biochem. Biophys., 2011, vol. 60, pp. 13–20. https://doi.org/10.1007/s12013-011-9178-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Zhang, F., Hu, M., Tian, G., Zhang, P., Finley, D., Jeffrey, P.D., and Shi, Y., Mol. Cell, 2009, vol. 34, pp. 473–484. https://doi.org/10.1016/j.molcel.2009.04.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Djuranovic, S., Hartmann, M.D., Habeck, M., Ursinus, A., Zwickl, P., Martin, J., Lupas, A.N., and Zeth, K., Mol. Cell, 2009, vol. 34, pp. 580–590. https://doi.org/10.1016/j.molcel.2009.04.030

    Article  CAS  PubMed  Google Scholar 

  93. Zhang, F., Wu, Z., Zhang, P., Tian, G., Finley, D., and Shi, Y., Mol. Cell, 2009, vol. 34, pp. 485–496. https://doi.org/10.1016/j.molcel.2009.04.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Sousa, M.C., Trame, C.B., Tsuruta, H., Wilbanks, S.M., Reddy, V.S., and McKay, D.B., Cell, 2000, vol. 103, pp. 633–643. https://doi.org/10.1016/S0092-8674(00)00166-5

    Article  CAS  PubMed  Google Scholar 

  95. Sundar, S., Baker, T.A., and Sauer, R.T., Protein Sci., 2012, vol. 21, pp. 188–198. https://doi.org/10.1002/pro.2001

    Article  CAS  PubMed  Google Scholar 

  96. Scharfenberg, F., Serek-Heuberger, J., Coles, M., Hartmann, M.D., Habeck, M., Martin, J., Lupas, A.N., and Alva, V., J. Mol. Biol., 2015, vol. 427, pp. 910–923. https://doi.org/10.1016/j.jmb.2014.12.024

    Article  CAS  PubMed  Google Scholar 

  97. Ramelot, T.A., Yang, Y., Sahu, I.D., Lee, H.W., Xiao, R., Lorigan, G.A., Montelione, G.T., and Kennedy, M.A., FEBS Lett., 2013., vol. 587, pp. 3522–3528. https://doi.org/10.1016/j.febslet.2013.09.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. An, J.Y., Sharif, H., Kang, G.B., Park, K.J., Lee, J.G., Lee, S., Jin, M.S., Song, J.J., Wang, J., and Eom, S.H., Biochem. Biophys. Res. Commun., 2018, vol. 495, pp. 1201–1207. https://doi.org/10.1016/j.bbrc.2017.11.158

    Article  CAS  PubMed  Google Scholar 

  99. Langklotz, S., Baumann, U., and Narberhaus, F., Biochim. Biophys. Acta, 2012, vol. 1823, pp. 40–48. https://doi.org/10.1016/j.bbamcr.2011.08.015

    Article  CAS  PubMed  Google Scholar 

  100. Rotanova, T.V., Melnikov, E.E., Khalatova, A.G., Makhovskaya, O.V., Botos, I., Wlodawer, A., and Gustchina, A., Eur. J. Biochem., 2004, vol. 271, pp. 4865–4871. https://doi.org/10.1111/j.1432-1033.2004.04452.x

    Article  CAS  PubMed  Google Scholar 

  101. Rotanova, T.V., Dergousova, N.I., and Morozkin, A.D., Russ. J. Bioorg. Chem., 2013, vol. 39, pp. 268–282. https://doi.org/10.1134/S1068162013030114

    Article  CAS  Google Scholar 

  102. Li, M., Rasulova, F., Melnikov, E.E., Rotanova, T.V., Gustchina, A., Maurizi, M.R., and Wlodawer, A., Protein Sci., 2005, vol. 14, pp. 2895–2900. https://doi.org/10.1110/ps.051736805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Duman, R.E. and Löwe, J., J. Mol. Biol., 2010, vol. 401, pp. 653–670. https://doi.org/10.1016/j.jmb.2010.06.030

    Article  CAS  PubMed  Google Scholar 

  104. Li, M., Gustchina, A., Rasulova, F.S., Melnikov, E.E., Maurizi, M.R., Rotanova, T.V., Dauter, Z., and Wlodawer, A., Acta Cryst., 2010, vol. 66, pp. 865–873. https://doi.org/10.1107/S0907444910019554

    Article  CAS  Google Scholar 

  105. Rotanova, T.V., Andrianova, A.G., Kudzhaev, A.M., Li, M., Botos, I., Wlodawer, A., and Gustchina, A., FEBS Open Bio, 2019, vol. 9, pp. 1536–1551. https://doi.org/10.1002/2211-5463.12691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Makhovskaya, O.V., Kozlov, S., Botos, I., Stepnov, A.A., Andrianova, A.G., Gustchina, A.E., Wlodawer, A., Melnikov, E.E., and Rotanova, T.V., Russ. J. Bioorg. Chem., 2007, vol. 33, pp. 610–613. https://doi.org/10.1134/S1068162007060131

    Article  CAS  Google Scholar 

  107. Liao, J.H., Kuo, C.I., Huang, Y.Y., Lin, Y.C., Lin, Y.C., Yang, C.Y., Wu, W.L., Chang, W.H., Liaw, Y.C., Lin, L.H., Chang, C.I., Wu, S.H., Liao, J.H., Kuo, C.I., Huang, Y.Y., Lin, Y.C., and Lin, Y.C., PLoS One, 2012, vol. 7, p. e40226. https://doi.org/10.1371/journal.pone.0040226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Li, J.K., Liao, J.H., Li, H., Kuo, C.I., Huang, K.F., Yang, L.W., Wu, S.H., and Chang, C.I., Acta Cryst., 2013, vol. 69, pp. 1789–1797. https://doi.org/10.1107/S090744491301500X

    Article  CAS  Google Scholar 

  109. Gur, E. and Sauer, R.T., Genes Dev., 2008, vol. 22, pp. 2267–2277. https://doi.org/10.1101/gad.1670908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Ngo, J.K., Pomatto, L.C.D., and Davies, K.J.A., Redox Biol., 2013, vol. 1, pp. 258–264. https://doi.org/10.1016/j.redox.2013.01.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Cheng, C.W., Kuo, C.Y., Fan, C.C., Fang, W.C., Jiang, S.S., Lo, Y.K., Wang, T.Y., Kao, M.C., and Lee, A.Y.L., Cell Death Dis., 2013, vol. 4, p. e681. https://doi.org/10.1038/cddis.2013.204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Liu, Y., Lan, L., Huang, K., Wang, R., Xu, C., Shi, Y., Wu, X., Wu, Z., Zhang, J., Chen, L., Wang, L., Yu, X., Zhu, H., and Lu, B., Oncotarget, 2014, vol. 5, pp. 11209–11224. https://doi.org/10.18632/oncotarget.2026

    Article  PubMed  PubMed Central  Google Scholar 

  113. Bulteau, A.L. and Bayot, A., Biochim. Biophys. Acta, 2011, vol. 1807, pp. 595–601. https://doi.org/10.1016/j.bbabio.2010.12.011

    Article  CAS  PubMed  Google Scholar 

  114. Voos, W. and Pollecker, K., Biomolecules, 2020, vol. 10, pp. 253. https://doi.org/10.3390/biom10020253

    Article  CAS  PubMed Central  Google Scholar 

  115. Lu, B., Adv. Exp. Med. Biol., 2017, vol. 1038, pp. 8173–8182. https://doi.org/10.1007/978-981-10-6674-0_12

    Article  CAS  Google Scholar 

  116. Pinti, M., Gibellini, L., Liu, Y., Xu, S., Lu, B., and Cossarizza, A., Cell. Mol. Life Sci., 2015, vol. 72, pp. 4807–4824. https://doi.org/10.1007/s00018-015-2039-3

    Article  CAS  PubMed  Google Scholar 

  117. Quirós, P.M., Español, Y., Acín-Pérez, R., Rodríguez, F., Bárcena, C., Watanabe, K., Calvo, E., Loureiro, M., Fernández-García, M.S., Fueyo, A., Vázquez, J., Enríquez, J.A., and López-Otín, C., Cell Rep., 2014, vol. 8, pp. 542–556. https://doi.org/10.1016/j.celrep.2014.06.018

    Article  CAS  PubMed  Google Scholar 

  118. Bota, D.A. and Davies, K.J.A., Free Rad. Biol. Med., 2016, vol. 100, pp. 188–198. https://doi.org/10.1016/j.freeradbiomed.2016.06.031

    Article  CAS  PubMed  Google Scholar 

  119. Rawlings, N.D., Barrett, A.J., Thomas, P.D., Huang, X., Bateman, A., and Finn, R.D., Nucl. Acids Res., 2018, vol. 46., pp. 624–632. https://doi.org/10.1093/nar/gkx1134

    Article  CAS  Google Scholar 

  120. Swamy, K.S. and Goldberg, A.L., Nature, 1981, vol. 292, pp. 652–654. https://doi.org/10.1038/292652a0

    Article  CAS  PubMed  Google Scholar 

  121. Liao, J.H., Ihara, K., Kuo, C.I., Huang, K.F., Wakatsuki, S., Wu, S.H., and Chang, C.I., Acta Cryst., 2013, vol. 69, pp. 1395–1402. https://doi.org/10.1107/S0907444913008214

    Article  CAS  Google Scholar 

  122. Bittner, L.M., Arends, J., and Narberhaus, F., Biopolymers, 2016, vol. 105, pp. 505–517. https://doi.org/10.1002/bip.22831

    Article  CAS  PubMed  Google Scholar 

  123. Goldberg, A.L. and Waxman, L., J. Biol. Chem., 1985, vol. 260, pp. 12029–12034. https://doi.org/10.1016/S0021-9258(17)38980-9

    Article  CAS  PubMed  Google Scholar 

  124. Patterson-Ward, J., Tedesco, J., Hudak, J., Fishovitz, J., Becker, J., Frase, H., McNamara, K., and Lee, I., Biochim. Biophys. Acta, 2009, vol. 1794, pp. 1355–1363. https://doi.org/10.1016/j.bbapap.2009.02.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Vineyard, D., Patterson-Ward, J., Berdis, A.J., and Lee, I., Biochemistry, 2005, vol. 44, pp. 1671–1682. https://doi.org/10.1021/bi048618z

    Article  CAS  PubMed  Google Scholar 

  126. Besche, H., Tamura, N., Tamura, T., and Zwickl, P., FEBS Lett., 2004, vol. 574, pp. 161–166. https://doi.org/10.1016/j.febslet.2004.08.021

    Article  CAS  PubMed  Google Scholar 

  127. Botos, I., Melnikov, E.E., Cherry, S., Kozlov, S., Makhovskaya, O.V., Tropea, J.E., Gusthchina, A., Rotanova, T.V., and Wlodawer, A., J. Mol. Biol., 2005, vol. 351, pp. 144–157. https://doi.org/10.1016/j.jmb.2005.06.008

    Article  CAS  PubMed  Google Scholar 

  128. Botos, I., Melnikov, E.E., Cherry, S., Tropea, J., Khalatova, A.G., Rasulova, F.S., Dauter, Z., Maurizi, M.R., Rotanova, T.V., Wlodawer, A., and Gustchina, A., J. Biol. Chem., 2004, vol. 279, pp. 8140–8148. https://doi.org/10.1074/jbc.M312243200

    Article  CAS  PubMed  Google Scholar 

  129. Botos, I., Melnikov, E.E., Cherry, S., Khalatova, A.G., Rasulova, F.S., Tropea, J.E., Maurizi, M.R., Rotanova, T.V., Gustchina, A., and Wlodawer, A., J. Struct. Biol., 2004, vol. 146, pp. 113–122. https://doi.org/10.1016/j.jsb.2003.09.003

    Article  CAS  PubMed  Google Scholar 

  130. Lee, A.Y., Chen, Y.D., Chang, Y.Y., Lin, Y.C., Chang, C.F., Huang, S.J., Wu, S.H., and Hsu, C.H., Acta Cryst., 2014, vol. 70, pp. 218–230. https://doi.org/10.1107/S139900471302631X

    Article  CAS  Google Scholar 

  131. Lin, C.C., Su, S.C., Su, M.Y., Liang, P.H., Feng, C.C., Wu, S.H., and Chang, C.I., Structure, 2016, vol. 24, pp. 667–675. https://doi.org/10.1016/j.str.2016.03.001

    Article  CAS  PubMed  Google Scholar 

  132. Tzeng, S.R., Tseng, Y.C., Lin, C.C., Hsu, C.Y., Huang, S.J., Kuo, Y.T., and Chang, C.I., eLife, 2021, vol. 10, pp. e64056. https://doi.org/10.7554/eLife.64056

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Su, S.C., Lin, C.C., Tai, H.C., Chang, M.Y., Ho, M.R., Babu, C.S., Liao, J.H., Wu, S.H., Chang, Y.C., Lim, C., and Chang, C.I., Structure, 2016. vol. 24. pp. 676–686. https://doi.org/10.1016/j.str.2016.03.003

    Article  CAS  PubMed  Google Scholar 

  134. Chen, X., Zhang, S., Bi, F., Guo, C., Feng, L., Wang, H., Yao, H., and Lin, D., Protein Sci., 2019, vol. 28, pp. 1720–1726. https://doi.org/10.1002/pro.3687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. García-Nafría, J., Ondrovičová, G., Blagova, E., Levdikov, V.M., Bauer, J.A., Suzuki, C.K., Kutejová, E., Wilkinson, A.J., and Wilson, K.S., Protein Sci., 2010, vol. 19, pp. 987–999. https://doi.org/10.1002/pro.376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Bertonati, C., Punta, M., Fischer, M., Yachdav, G., Forouhar, F., Zhou, W., Kuzin, A.P., Seetharaman, J., Abashidze, M., Ramelot, T.A., Kennedy, M.A., Cort, J.R., Belachew, A., Hunt, J.F., Tong, L., Montelione, G.T., and Rost, B., Proteins, 2009, vol. 75, pp. 760–773. https://doi.org/10.1002/prot.22287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Kudzhaev, A.M., Dubovtseva, E.S., Serova, O.V., Andrianova, A.G., and Rotanova, T.V., Russ. J. Bioorg. Chem., 2016, vol. 42, pp. 381–388. https://doi.org/10.1134/S1068162016040142

    Article  CAS  Google Scholar 

  138. Andrianova, A.G., Kudzhaev, A.M., Dubovtseva, E.S., and Rotanova, T.V., Russ. J. Bioorg. Chem., 2017, vol. 43, pp. 368–376. https://doi.org/10.1134/S1068162017040021

    Article  CAS  Google Scholar 

  139. Kudzhaev, A.M., Andrianova, A.G., Dubovtseva, E.S., Serova, O.V., and Rotanova, T.V., Acta Naturae, 2017, vol. 9, pp. 75–81. https://doi.org/10.32607/20758251-2017-9-2-75-81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Kudzhaev, A.M., Dubovtseva, E.S., Serova, O.V., Andrianova, A.G., and Rotanova, T.V., Russ. J. Bioorg. Chem., 2018, vol. 44, pp. 518–527. https://doi.org/10.1134/S1068162018050084

    Article  CAS  Google Scholar 

  141. Kudzhaev, A.M., Andrianova, A.G., Serova, O.V., Arkhipova, V.A., Dubovtseva, E.S., and Rotanova, T.V., Russ. J. Bioorg. Chem., 2015, vol. 41, pp. 518–524. https://doi.org/10.1134/S1068162015050076

    Article  CAS  Google Scholar 

  142. Andrianova, A.G., Kudzhaev, A.M., Abrikosova, V.A., Gustchina, A., Smirnov, I.V., and Rotanova, T.V., Acta Naturae, 2020, vol. 12, pp. 102–113. https://doi.org/10.32607/actanaturae.11197

    Article  Google Scholar 

  143. Glynn, S.E., Kardon, J.L., Mueller-Cajar, O., and Cho, C., Nat. Struct. Mol. Biol., 2020, vol. 27, pp. 515–518. https://doi.org/10.1038/s41594-020-0444-2

    Article  CAS  PubMed  Google Scholar 

  144. Gates, S.N. and Martin, A., Protein Sci., 2019, vol. 29, pp. 407–419. https://doi.org/10.1002/pro.3743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Matyskiela, M.E., Lander, G.C., and Martin, A., Nat. Struct. Mol. Biol., 2013, vol. 20, pp. 781–788. https://doi.org/10.1038/nsmb.2616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Puchades, C., Rampello, A.J., Shin, M., Giuliano, C.J., Wiseman, R.L., Glynn, S.E., and Lander, G.C., Science, 2017, vol. 358, p. eaao0464. https://doi.org/10.1126/science.aao0464

  147. Uchihashi, T., Watanabe, Y.H., Nakazaki, Y., Yamasaki, T., Watanabe, H., Maruno, T., Ishii, K., Uchiyama, S., Song, C.H., Murata, K., Iino, R., and Ando, T., Nat. Commun., 2018, vol. 9, pp. 2147. https://doi.org/10.1038/s41467-018-04587-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Rizo, A.N., Lin, J.B., Gates, S.N., Tse, E., Bart, S.M., Castellano, L.M., DiMaio, F., Shorter, J., and Southworth, D.R., Nat. Commun., 2019, vol. 10, pp. 2393. https://doi.org/10.1038/s41467-019-10150-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Majumder, P., Rudack, T., Beck, F., Danev, R., Pfeifer, G., Nagy, I., and Baumeister, W., Proc. Natl. Acad. Sci. U.S.A., 2019, vol. 116, pp. 534–539. https://doi.org/10.1073/pnas.1817752116

    Article  CAS  PubMed  Google Scholar 

  150. Lee, S., Roh, S.H., Lee, J., Sung, N., Liu, J., and Tsai, F.T.F., Cell Rep., 2019, vol. 26, pp. 29–36. https://doi.org/10.1016/j.celrep.2018.12.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Zhang, S. and Mao, Y., Biomolecules, 2020, vol. 10, pp. 629. https://doi.org/10.3390/biom10040629

  152. de la Peña, A.H., Goodall, E.A., Gates, S.N., Lander, G.C., and Martin, A., Science, 2018, vol. 362, p. eaav0725. https://doi.org/10.1126/science.aav0725

  153. Fei, X., Bell, T.A., Jenni, S., Stinson, B.M., Baker, T.A., Harrison, S.C., and Sauer, R.T., eLife, 2020, vol. 9, p. e52774. https://doi.org/10.7554/eLife.52774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Botos, I., Lountos, G.T., Wu, W., Cherry, S., Ghirlando, R., Kudzhaev, A.M., Rotanova, T.V., de Val, N., Tropea, J., Gustchina, A., and Wlodawer, A., Curr. Res. Struct. Biol., 2019, vol. 1, pp. 13–20. https://doi.org/10.1016/j.crstbi.2019.10.001

    Article  PubMed  PubMed Central  Google Scholar 

  155. Li, S., Hsieh, K.Y., Su, S.C., Pintilie, G.D., Zhang, K., and Chang, C.I., J. Biol. Chem., 2021, vol. 297, pp. 101239. https://doi.org/10.1016/j.jbc.2021.101239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Shin, M., Puchades, C., Asmita, A., Puri, N., Adjei, E., Wiseman, R.L., Karzai, A.W., and Lander, G.C., Sci. Adv., 2020, vol. 6, p. eaba8404. https://doi.org/10.1126/sciadv.aba8404

  157. Shin, M., Watson, E.R., Song, A.S., Mindrebo, J.T., Novick, S.J., Griffin, P.R., Wiseman, R.L., and Lander, G.C., Nat. Commun., 2021, vol. 12, pp. 3239. https://doi.org/10.1038/s41467-021-23495-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Kereïche, S., Kováčik, L., Bednár, J., Pevala, V., Kunová, N., Ondrovičová, G., Bauer, J., Ambro, L., Bellová, J., Kutejová, E., and Raška, I., Sci. Rep., 2016, vol. 6, p. 33631. https://doi.org/10.1038/srep33631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Coscia, F. and Löwe, J., FEBS Lett., 2021, vol. 595, pp. 2691–2700. https://doi.org/10.1002/1873-3468.14199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Gesé, G.V., Shahzad, S., Pardo-Hernández, C., Wramstedt, A., Falkenberg, M., and Hällberg, B.M., bioRxiv, 2021. https://doi.org/10.1101/2021.06.09.447696

  161. Mohammed, I., Schmitz, K.A., Schenck, N., Topitsch, A., Maier, T., and Abrahams, J.P., bioRxiv, 2021. https://doi.org/10.1101/2021.07.28.454137

  162. Vieux, E.F., Wohlever, M.L., Chen, J.Z., Sauer, R.T., and Baker, T.A., Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, pp. E2002–E2008. https://doi.org/10.1073/pnas.1307066110

    Article  PubMed  PubMed Central  Google Scholar 

  163. Brown, B.L., Vieux, E.F., Kalastavadi, T., Kim, S.R., Chen, J.Z., and Baker, T.A., Protein Sci., 2018, vol. 28, pp. 1239–1251. https://doi.org/10.1002/pro.3553

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Russian Foundation for Basic Research (project no. 19-04-00646-a, characterization of the cellular protein quality control system) and the Russian Science Foundation (project no. 21-74-20154, analysis of the structural features and mechanism of functioning of LonA proteases).

Author information

Authors and Affiliations

  1. Shemyakin−Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    A. M. Kudzhaev, A. G. Andrianova, I. V. Smirnov & T. V. Rotanova

  2. Protein Structure Section, Center for Structural Biology, National Cancer Institute, MD 21702, Frederick, USA

    A. E. Gustchina

Authors
  1. A. M. Kudzhaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. G. Andrianova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. E. Gustchina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. I. V. Smirnov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. V. Rotanova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. V. Rotanova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any research involving humans or animals as research objects.

Conflict of Interests

The authors declare no conflicts of interest.

Additional information

Translated by N. Onishchenko

Abbreviations: PQC, protein quality control system; cryo-EM, cryo-electron microscopy; ATP-γ-S, adenosine-5'-[γ-thio]triphosphate; CC, coiled-coil conformation.

Corresponding author; phone: +7(495)335-42-22.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kudzhaev, A.M., Andrianova, A.G., Gustchina, A.E. et al. ATP-Dependent Lon Proteases in the Cellular Protein Quality Control System. Russ J Bioorg Chem 48, 678–709 (2022). https://doi.org/10.1134/S1068162022040136

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162022040136

Keywords:

Search

Navigation