Tryptophan versus nitric oxide, nitrogen dioxide and carbonate radicals: differences in reactivity and implications for oxidative damage to proteins

  • Adriana Pérez-González
  • Leonardo Muñoz-Rugeles
  • Juan Raúl Alvarez-Idaboy
Regular Article
First Online:
Received:
Accepted:
Part of the following topical collections:
  1. Festschrift in honour of A. Vela

Abstract

The reactions of carbonate (CO 3 ·− ), nitric oxide (NO·) and nitrogen dioxide (NO 2 · ) radicals with free zwitterionic tryptophan and N-formyl-tryptophanamide (a model for tryptophan as a protein residue) have been studied using density functional theory and transition state theory. All possible reactions mechanisms have been analyzed. They are single electron transfer (SET), radical adduct formation and formal hydrogen transfer. The aqueous solution has been mimicked at physiological pH. Thermochemical and kinetic data are reported for both tryptophan models. We find that the reaction rate constants for CO 3 ·− with both tryptophan models are limited by diffusion, while for reaction with NO 2 · they are approximately 3.00 × 106 M−1 s−1, and NO· does not react at all. The overall rate constants of free zwitterionic tryptophan with NO 2 · and CO 3 ·− are 1.11 and 1.29 times larger than those of the N-formyl-tryptophanamide model, respectively. Therefore, it seems that the free amino acid and the residue in the protein have similar reactivities. While CO 3 ·− reacts via all three studied mechanisms at similar rates, NO 2 · reacts exclusively via SET. Our work suggests that free tryptophan has some scavenging activity and protective effect, but that bonded tryptophan could be a target for oxidative stress.

Keywords

Rate constants Reaction mechanisms Alpha amino acid tryptophan Oxidative stress Protein damage 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

We gratefully acknowledge the Dirección General de Servicios de Cómputo Académico (DGTIC) at Universidad Nacional Autónoma de México. This work was partially supported by project SEP-CONACyT 167430 and DGAPA PAPIIT-IN220215. A.P.-G. acknowledges the economic support of the Program of Postdoctoral Scholarships from DGAPA (UNAM) 2014–2015. L.M.-R. thanks CONACyT for scholarship 270309.

Supplementary material

214_2016_1913_MOESM1_ESM.pdf (649 kb)
Supplementary material 1 (PDF 648 kb)

References

  1. 1.
    Fukumura D, Kashiwagi S, Jain RK (2006) Nat Rev Cancer 6:521CrossRefGoogle Scholar
  2. 2.
    Hyue JJ, Jae HL, Da HK, Kee-Tae K, Gyu WL, Seung JC, Pahn-Shick C, Hyun-Dong P (2015) Food Sci Biotechnol 24:1555CrossRefGoogle Scholar
  3. 3.
    Yamakura F, Ikeda K (2006) Nitric Oxide 14:152CrossRefGoogle Scholar
  4. 4.
    Greenacre CB, Young DW, Behrend EN, Wilson GH (2001) Am J Vet Res 62:1750CrossRefGoogle Scholar
  5. 5.
    Pacher P, Beckman JS, Liaudet L (2007) Physiol Rev 87:315CrossRefGoogle Scholar
  6. 6.
    Alvarez B (2003) Amino Acids 25:295CrossRefGoogle Scholar
  7. 7.
    Mayer B, Klatt P, Werner ER, Schmidt K (1995) J Biol Chem 270:655CrossRefGoogle Scholar
  8. 8.
    Lymar SV, Hurst JK (1995) J Am Chem Soc 117:8867CrossRefGoogle Scholar
  9. 9.
    Augusto O, Bonini MG, Amanso AM, Linares E, Santos CCX, De Menezes SL (2002) Free Radic Biol Med 32:841CrossRefGoogle Scholar
  10. 10.
    Kirsch M, Korth HG, Sustmann R, deGroot H (2002) Biol Chem 383:389CrossRefGoogle Scholar
  11. 11.
    Zhang H, Joseph J, Crow JP, Kalyanaraman B (2004) Free Radic Biol Med 37:2018CrossRefGoogle Scholar
  12. 12.
    Medinas DB, Gozzo FC, Santos LFA, Iglesias AH, Augusto O (2010) Free Radic Biol Med 49:1046CrossRefGoogle Scholar
  13. 13.
    Huie RE (1994) Toxicology 89:193CrossRefGoogle Scholar
  14. 14.
    Pryor WA (1981) Science 214:435CrossRefGoogle Scholar
  15. 15.
    Singh RJ, Goss SPA, Joseph J (1998) Proc Natl Acad Sci USA 95:12912CrossRefGoogle Scholar
  16. 16.
    Huie RE, Neta P (1986) J Phys Chem 90:1193CrossRefGoogle Scholar
  17. 17.
    Ford E, Hughes MN, Wardman P (2002) Free Radic Biol Med 32:1314CrossRefGoogle Scholar
  18. 18.
    Prütz WA, Monig H, Butler J, Land EJ (1985) Arch Biochem Biophys 243:125CrossRefGoogle Scholar
  19. 19.
    Domazou AS, Gebicka L, Didik J, Gebicki JL, van der Meijden B, Koppenol WH (2014) Free Radic Biol Med 69:172CrossRefGoogle Scholar
  20. 20.
    Domazou AS, Koppenol WH (2007) J Biol Inorg Chem 12:118CrossRefGoogle Scholar
  21. 21.
    Prutz WA, Mijnig H, Butler J, Land EJ (1985) Arch FB Iochem D Biophys 243:125CrossRefGoogle Scholar
  22. 22.
    Schoen-nan C, Hoffman MZ (1973) Radiat Res 56:40CrossRefGoogle Scholar
  23. 23.
    Adamsg E, Aldrichj E, Bisby RH, Cundallr B, Redpath JL, Willson RL (1972) Radiat Res 49:278CrossRefGoogle Scholar
  24. 24.
    Bravo R, Matito S, Cubero J, Paredes SD, Franco L, Rivero M, Rodríguez AB, Barriga C (2013) Age (Dordr) 35:1277CrossRefGoogle Scholar
  25. 25.
    Watanabe S, Togashi S, Takanashi N, Fukui T (2002) J Nutr Sci Vitaminol 48:36CrossRefGoogle Scholar
  26. 26.
    Perez-Gonzalez A, Muñoz-Rugeles L, Alvarez-Idaboy JR (2014) RSC Adv 4:56128CrossRefGoogle Scholar
  27. 27.
    Christen S, Peterhans E, Stocker R (1990) Proc Nati Acad Sci USA 87:2506CrossRefGoogle Scholar
  28. 28.
    Weiss G, Diez-Ruiz A, Murr C, Theur I, Fuchs D (2002) Pteridines 13:140CrossRefGoogle Scholar
  29. 29.
    Chan B, O’Reilly RJ, Easton CJ, Radom L (2012) J Org Chem 77:9807CrossRefGoogle Scholar
  30. 30.
    Castañeda-Arriaga R, Mora-Diez N, Alvarez-Idaboy JR (2015) RSC Adv 5:96714CrossRefGoogle Scholar
  31. 31.
    Reid DL, Armstrong DA, Rauk A, von Sonntag C (2003) Phys Chem Chem Phys 5:3994CrossRefGoogle Scholar
  32. 32.
    Doan HQ, Davis AC, Francisco JS (2010) J Phys Chem A 114:5342CrossRefGoogle Scholar
  33. 33.
    O’Reilly RJ, Chan B, Taylor MS, Ivanic S, Bacskay GB, Easton CJ, Radom L (2011) J Am Chem Soc 133:16553CrossRefGoogle Scholar
  34. 34.
    Owen MC, Szori M, Csizmadia IG, Viskolcz B (2012) J Phys Chem B 116:1143CrossRefGoogle Scholar
  35. 35.
    Mujika JI, Uranga J, Matxain JM (2013) Chem Eur J 19:6862CrossRefGoogle Scholar
  36. 36.
    Thomas DA, Sohn CH, Gao J, Beauchamp JL (2014) J Phys Chem A 118:8380CrossRefGoogle Scholar
  37. 37.
    Amos RIJ, Chan B, Easton CJ, Radom L (2015) J Phys Chem B 19:783CrossRefGoogle Scholar
  38. 38.
    Medina ME, Galano A, Alvarez-Idaboy JR (2015) Phys Chem Chem Phys 17:4970CrossRefGoogle Scholar
  39. 39.
    Muñoz-Rugeles L, Alvarez-Idaboy JR (2015) Phys Chem Chem Phys 17:28525CrossRefGoogle Scholar
  40. 40.
    Hohenberg P, Kohn W (1964) Phys Rev 136:B864CrossRefGoogle Scholar
  41. 41.
    Kohn W, Sham L (1965) J Phys Rev 140:A1133CrossRefGoogle Scholar
  42. 42.
    Marenich AV, Cramer CJ, Truhlar DG (2009) J Phys Chem B 113:6378CrossRefGoogle Scholar
  43. 43.
    Zhao Y, Schultz NE, Truhlar DG (2006) J Chem Theory Comput 2:364CrossRefGoogle Scholar
  44. 44.
    Velez E, Quijano J, Notario R, Pabón E, Murillo J, Leal J, Zapata E, Alarcon G (2009) J Phys Org Chem 22:971CrossRefGoogle Scholar
  45. 45.
    Galano A, Alvarez-Idaboy JR (2009) Org Lett 11:5114CrossRefGoogle Scholar
  46. 46.
    Black G, Simmie JM (2010) J Comput Chem 31:1236Google Scholar
  47. 47.
    Furuncuoglu T, Ugur I, Degirmenci I, Aviyente V (2010) Macromolecules 43:1823CrossRefGoogle Scholar
  48. 48.
    Galano A, Alvarez-Idaboy JR (2014) J Comput Chem 35:2019CrossRefGoogle Scholar
  49. 49.
    Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR et al (2009) Gaussian 09. Gaussian Inc, WallingfordGoogle Scholar
  50. 50.
    Okuno Y (1997) Chem Eur J 3:212CrossRefGoogle Scholar
  51. 51.
    Benson SW (1960) The foundations of chemical kinetics, chapter XV 504. McGraw-Hill, New YorkGoogle Scholar
  52. 52.
    Eyring H (1935) J Chem Phys 3:63CrossRefGoogle Scholar
  53. 53.
    Evans MG, Polanyi M (1935) Trans Faraday Soc 31:875CrossRefGoogle Scholar
  54. 54.
    Truhlar DG, Hase WL, Hynes JT (1983) J Phys Chem 87:2664CrossRefGoogle Scholar
  55. 55.
    Galano A, Alvarez-Idaboy JR (2013) J Comp Chem 34:2430CrossRefGoogle Scholar
  56. 56.
    Collins FC, Kimball GE (1949) J Colloid Sci 4:425CrossRefGoogle Scholar
  57. 57.
    Smoluchowski M (1917) Z Phys Chem 92:129Google Scholar
  58. 58.
    Einstein A (1905) Ann Phys 17:549CrossRefGoogle Scholar
  59. 59.
    Stokes GG (1903) Math Phys Pap 3:55Google Scholar
  60. 60.
    Umschlag Th, Herrmann H (1999) Acta Hydrochim Hydrobiol 27:214CrossRefGoogle Scholar
  61. 61.
    Czapski G, Lymar SV, Schwarz HA (1999) J Phys Chem A 103:3447CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Adriana Pérez-González
    • 1
  • Leonardo Muñoz-Rugeles
    • 1
  • Juan Raúl Alvarez-Idaboy
    • 1
  1. 1.Departamento de Física y Química Teórica, Facultad de QuímicaUniversidad Nacional Autónoma de MéxicoMexicoMexico

Personalised recommendations