The function of the conserved “non-functional” residues in apomyoglobin is to provide and preserve the correct protein topology

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

In this paper the answer to O. B. Ptitsyn’s question “What is the role of conserved non-functional residues in apomyoglobin” is presented, which is based on the research results of three laboratories. The role of conserved non-functional apomyoglobin residues in formation of native topology in the molten globule state of this protein is revealed. This fact allows suggesting that the conserved non-functional residues in this protein are indispensable for fixation and maintaining main elements of the correct topology of its secondary structure in the intermediate state. The correct topology is a native element in the intermediate state of the protein.

About the authors

V. E Bychkova

Institute of Protein Research, Russian Academy of Sciences

142290 Pushchino, Moscow Region, Russia

D. A Dolgikh

Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences

117871 Moscow, Russia

V. A Balobanov

Institute of Protein Research, Russian Academy of Sciences

Email: balobanov@phys.protres.ru
142290 Pushchino, Moscow Region, Russia

References

  1. Kim, P. S., and Baldwin, R. L. (1990) Intermediates in the folding reactions of small proteins, Ann. Rev. Biochem., 59, 631-660, doi: 10.1146/annurev.bi.59.070190.003215.
  2. Ptitsyn, O. B. (1991) How does protein synthesis give rise to the 3D-structure? FEBS Lett., 285, 176-181, doi: 10.1016/0014-5793(91)80799-9.
  3. Dill, K. A., Fiebig, K. M., and Chan, H. S. (1993) Cooperativity in protein folding kinetics, Proc. Natl. Acad. Sci. USA, 90, 1942-1946, doi: 10.1073/pnas.90.5.1942.
  4. Ptitsyn, O. B. (1973) Stages in the mechanism of self-organisation of protein molecules, Dokl. Akad. Nauk SSSR, 210, 1213-1215.
  5. Karplus, M., and Weaver, D. L. (1994) Protein folding dynamics: the diffusion-collision model and experimental data, Protein Sci., 3, 650-668, doi: 10.1002/pro.5560030413.
  6. Abkevich, V. I., Gutin, A. M., and Shakhnovich, E. I. (1994) Specific nucleus as the transition state for protein folding: evidence from the lattice model, Biochemistry, 33, 10026-10036, doi: 10.1021/bi00199a029.
  7. Guo, Z., and Thirumalai, D. (1995) Kinetics of protein folding: nucleation mechanism, time scales, and pathways, Biopolymers, 36, 83-102, doi: 10.1002/bip.360360108.
  8. Wolynes, P. G., Onuchic, J. N., and Thirumalai, D. (1995) Navigating the folding routes, Science, 267, 1619-1620, doi: 10.1126/science.7886447.
  9. Finkelstein, A. V., and Badretdinov, A. Y. (1997) Rate of protein folding near the point of thermodynamic equilibrium between the coil and the most stable chain fold, Fold. Des., 2, 115-121, doi: 10.1016/s1359-0278(97)00016-3.
  10. Fersht, A. R. (1995) Optimization of rates of protein folding: The nucleation-condensation mechanism and its implications, Proc. Natl. Acad. Sci. USA, 92, 10869-10873, doi: 10.1073/pnas.92.24.10869.
  11. Shakhnovich, E. I., Abkevich, V., and Ptitsyn, O. B. (1996) Conserved residues and the mechanism of protein folding, Nature, 379, 96-98, doi: 10.1038/379096a0.
  12. Ptitsyn, O. B., and Ting, K. L. (1999) Non-functional conserved residues in globins and their possible role as a folding nucleus, J. Mol. Biol., 291, 671-682, doi: 10.1006/jmbi.1999.2920.
  13. Jennings, P., and Wright, P. E. (1993) Formation of a molten globule intermediate early in the kinetic folding pathway of myoglobin, Science, 262, 892-896, doi: 10.1126/science.8235610.
  14. Samatova, E. N., Melnik, B. S., Balobanov, V. A., Katina, N. S., Dolgikh, D. A., Semisotnov, G. V., Finkelstein, A. V., and Bychkova, V. E. (2010) Folding intermediate and folding nucleus for I-N and U-I-N transitions in apomyoglobin: Contributions by conserved and non-conserved residues, Biophys. J., 98, 1694-1702, doi: 10.1016/j.bpj.2009.12.4326.
  15. Elieser, D., Jennings, P. A., Wright, P. E., Doniach, S., Hodgson, K. O., and Tsuruta, H. (1995) The radius of gyration of an apomyoglobin folding intermediate, Science, 270, 487-488, doi: 10.1126/science.270.5235.487.
  16. Hughson, F. M., Wright, P. E., and Baldwin, R. L. (1990) Structural characterization of a partly folded apomyoglobin intermediate, Science, 249, 1544-1548, doi: 10.1126/science.2218495.
  17. Jamin, M., and Baldwin, R. L. (1998) Two forms of the pH 4 folding intermediate of apomyoglobin, J. Mol. Biol., 276, 491-504, doi: 10.1006/jmbi.1997.1543.
  18. Shastry, M. C. R., and Roder, H. (2004) Evidence for barrier-limited protein folding kinetics on the microsecond time scale, Nat. Struct. Biol., 5, 385-392, doi: 10.1038/nsb0598-385.
  19. Roder, H., Maki, K., and Cheng, H. (2006) Early events in protein folding explored by rapid mixing methods, Chem. Rev., 106, 1836-1861, doi: 10.1021/cr040430y.
  20. Xu, M., Beresneva, O., Rosario, R., and Roder, H. (2012) Microsecond folding dynamics of apomyoglobin at acidic pH, J. Phys. Chem. B, 116, 7014-7025, doi: 10.1021/jp3012365.
  21. Mizukami, T., Xu, M., Fazlieva, R., Bychkova, V. E., and Roder, H. (2018) Complex folding landscape of apomyoglobin at acidic pH revealed by ultrafast kinetic analysis of core mutants, J. Phys. Chem. B, 122, 11228-11239, doi: 10.1021/acs.jpcb.8b06895.
  22. Nishimura, C., Dyson, H. J., and Wright, P. E. (2006) Identification of native and non-native structure in kinetic folding intermediates of apomyoglobin, J. Mol. Biol., 355, 139-156, doi: 10.1016/j.jmb.2005.10.047.
  23. Aoto, P. C., Nishimura, C., Dyson, H. J., and Wright, P. E. (2014) Probing the non-native H helix translocation in apomyoglobin folding intermediates, Biochemistry, 53, 3767-3780, doi: 10.1021/bi500478m.
  24. Musto, R., Bigotti, M. G., Travaglini-Allocatelli, C., Brunori, M., and Cutruzzola, F. (2004) Folding of Aplysia limacina apomyoglobin involves an intermediate in common with other evolutionarily distant globins, Biochemistry, 43, 230-236, doi: 10.1021/bi035319l.
  25. Балобанов В. А., Ильина Н. Б., Катина Н. С., Кашпаров И. А., Долгих Д. А., Бычкова В. Е. (2010) Кинетика взаимодействия между апомиоглобином и фосфолипидными мембранами, Мол. Биол. (Москва), 44, 708-711.
  26. Bychkova, V. E., Basova, L. V., and Balobanov, V. A. (2014) How membrane surface affects protein structure, Biochemistry (Moscow), 79, 1483-1514, doi: 10.1134/S0006297914130045.
  27. Ptitsyn, O. B. (1998) Protein folding and protein evolution: common folding nucleus in different subfamily of c-type cytochromes? J. Mol. Biol., 278, 655-666, doi: 10.1006/jmbi.1997.1620.
  28. Rotondi, K. S., and Gierasch, L. M. (2003) Local sequence information in cellular retinoic acid-binding protein I: specific residue roles in beta-turns, Biopolymers, 71, 638-651, doi: 10.1002/bip.10592.
  29. Rotondi, K. S., and Gierasch, L. M. (2003) Role of local sequence in the folding of cellular retinoic acid-binding protein I: structural propensities of reverse turns, Biochemistry, 42, 7976-7985, doi: 10.1021/bi034304k.
  30. Gunasekaran, K., Haqler, A. T., and Gierasch, L. M. (2004) Sequence and structural analysis of cellular retinoic acid-binding proteins reveal a network of conserved hydrophobic interactions, Proteins, 54, 179-194, doi: 10.1002/prot.10520.
  31. Ting, K.-L. H., and Jernigan, R. L. (2002) Identifiing a folding nucleus for the lysozyme/alfa-lactalbumin family from sequence conservation clusters, J. Mol. Evol., 54, 425-436, doi: 10.1007/s00239-001-0033-x.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2023 Russian Academy of Sciences