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In vitro reactive oxygen species production by histatins and copper(I,II)

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Abstract

The ability of the histidine-rich peptides, histatin-5 (Hst-5) and histatin-8 (Hst-8), to support the generation of reactive oxygen species during the Cu-catalyzed oxidation of ascorbate and cysteine has been evaluated. High levels of hydrogen peroxide (70–580 mol/mol Cu/h) are produced by aqueous solutions containing Cu(II), Hst-8 or Hst-5, and a reductant, either ascorbate or cysteine, as determined by the postreaction Amplex Red assay. When the reactions are conducted in the presence of superoxide dismutase, the total hydrogen peroxide produced is decreased, more so in the presence of the peptides (up to 50%), suggesting the intermediacy of superoxide in these reactions. On the other hand, the presence of sodium azide or sodium formate, traps for hydroxyl radicals, has no appreciable effect on the total hydrogen peroxide production for the Cu–Hst systems. EPR spin-trapping studies using 5-(2,2-dimethyl-1,3-propoxy cyclophosphoryl)-5-methyl-1-pyrroline N-oxide (CYPMPO) in the cysteine–Cu(II) reactions reveal the formation of the CYPMPO–hydroperoxyl and CYPMPO–hydroxyl radical adducts in the presence of Hst-8, whereas only the latter was observed with Cu alone.

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References

  1. Kavanagh K, Dowd S (2004) J Pharm Pharmacol 56:285–289

    Article  PubMed  CAS  Google Scholar 

  2. Helmerhorst EJ, van’t Hof W, Veerman ECI, Simoons-Smit I, Nieuw AV (1997) Biochem J 326:39–45

    PubMed  CAS  Google Scholar 

  3. Edgerton M, Koshlukova S, Lo T, Chrzan BG, Straubinger RM, Raj PA (1998) J Biol Chem 32:20438–20447

    Article  Google Scholar 

  4. Fitzgerald DH, Coleman DC, O’Connell BC (2003) Antimicrob Agents Chemother 47:70–76

    Article  PubMed  CAS  Google Scholar 

  5. Murakami Y, Xu T, Helmerhorst EJ, Ori G, Troxler RF, Lally ET, Oppenheim FG (2002) Oral Microbiol Immun 17:143–149

    Article  CAS  Google Scholar 

  6. Li XS, Reddy MS, Baev D, Edgerton M (2003) J Biol Chem 278:28553–28561

    Article  PubMed  CAS  Google Scholar 

  7. Li XS, Sun JN, Okamoto-Shibayama K, Edgerton M (2006) J Biol Chem 281:22453–22463

    Article  PubMed  CAS  Google Scholar 

  8. Koshlukova SE, Araujo MWB, Baev D, Edgerton M (2000) Infect Immunity 68:6848–6856

    Article  CAS  Google Scholar 

  9. Helmerhorst EJ, Troxler RF, Oppenheim FG (2001) Proc Natl Acad Sci USA 98:14637–14642

    Article  PubMed  CAS  Google Scholar 

  10. Helmerhorst EJ, Breeuwer P, van’t Hof W, Walgreen-Weteringst E, Oomen LCJM, Veermant ECI, Nieuw Amerongen AV, Abee T (1999) J Biol Chem 274:7286–7291

    Article  PubMed  CAS  Google Scholar 

  11. Veerman ECI, Nazmi K, van’t Hof W, Bolscher JGM, den Hertog AL, Nieuw Amerongen AV (2004) Biochem J 38:1447–1452

    Google Scholar 

  12. den Hertog AL, van Marle J, van Veen HA, van’t Hof W, Bolscher JGM, Veerman ECI, Nieuw Amerongen AV (2005) Biochem J 388:689–695

    Article  CAS  Google Scholar 

  13. Diaz G, Polonelli L, Conti S, Messana I, Cabras T, Putzolu M, Falchi AM, Fadda ME, Cosentino S, Isola R (2005) Microsc Res Techn 66:219–228

    Article  CAS  Google Scholar 

  14. Petruzzelli R, Clementi ME, Marini S, Coletta M, Di Stasio E, Giardina B, Misiti F (2003) Biochem Biophys Res Commun 311:1034–1040

    Article  PubMed  CAS  Google Scholar 

  15. Wunder D, Dong J, Baev D, Edgerton M (2004) Antimicrob Agents Chemother 48:110–115

    Article  PubMed  CAS  Google Scholar 

  16. Gusman H, Lendenmann U, Grogan J, Troxler RF, Oppenheim FG (2001) Biochim Biophys Acta 1545:86–95

    PubMed  CAS  Google Scholar 

  17. Grogan J, McKnight CJ, Troxler RF, Oppenheim FG (2001) FEBS Lett 491:76–80

    Article  PubMed  CAS  Google Scholar 

  18. Tang CC, Davalian D, Huang P, Breslow R (1978) J Am Chem Soc 100:3918–3922

    Article  CAS  Google Scholar 

  19. Brewer D, Lajoie G (2000) Rapid Commun Mass Spectrom 14:1736–1745

    Article  PubMed  CAS  Google Scholar 

  20. Rachmilovich-Calis S, Masarwa A, Meyerstein N, Meyerstein D (2005) Eur J Inorg Chem 2005:2875–2880

    Article  CAS  Google Scholar 

  21. RA Sheldon, JK Kochi (1981) Metal catalyzed oxidations of organic compounds. Academic Press, New York, p 3

  22. Sutton HC, Winterbourn CC (1989) Free Radic Biol Med 6:53–60

    Article  PubMed  CAS  Google Scholar 

  23. Urbanski NK, Beresewicz A (2000) Acta Biochim Pol 47:951–962

    PubMed  CAS  Google Scholar 

  24. Lynch T, Cherny RA, Bush AI (2000) Exp Gerontol 35:445–451

    Article  PubMed  CAS  Google Scholar 

  25. Valko M, Morris H, Cronin MTD (2005) Curr Med Chem 12:1161–1208

    Article  PubMed  CAS  Google Scholar 

  26. Brewer GJ (2007) Exp Biol Med 232:323–335

    CAS  Google Scholar 

  27. Harper M-E, Bevilacqua L, Hagopian K, Weindruch R, Ramsey JJ (2004) Acta Physiol Scand 182:321–331

    Article  PubMed  CAS  Google Scholar 

  28. Vina J, Lloret A, Orti R, Alonso D (2004) In: Ozben T, Chevion M (eds) NATO science series, series I: life and behavioural sciences. Frontiers in neurodegenerative disorders and aging: fundamental aspects, clinical perspectives and new insights, vol 358. IOS Press, Amsterdam, pp 182–188

  29. Aslan M, Ozben T (2004) In: Ozben T, Chevion M (eds) NATO science series, series I: life and behavioural sciences. Frontiers in neurodegenerative disorders and aging: fundamental aspects, clinical perspectives and new insights, vol 358. IOS Press, Amsterdam, pp 158–169

  30. Patel M (2004) Free Radic Biol Med 37:1951–1962

    Article  PubMed  CAS  Google Scholar 

  31. Leonard SS, Harris GK, Shi X (2004) Free Radic Biol Med 37:1921–1942

    Article  PubMed  CAS  Google Scholar 

  32. Burkitt MJ (2001) Arch Biochem Biophys 394:117–135

    Article  PubMed  CAS  Google Scholar 

  33. Lassegue B, Griendling KK (2004) Am J Hypertens 17:852–860

    Article  PubMed  CAS  Google Scholar 

  34. Lovstad RA (2002) BioMetals 15:351–355

    Article  PubMed  CAS  Google Scholar 

  35. Bar-Or D, Rael LT, Lau EP, Rao NKR, Thomas GW, Winkler JV, Yukl RL, Kingston RG, Curtis CG (2001) Biochem Biophys Res Commun 284:856–862

    Article  PubMed  CAS  Google Scholar 

  36. Jin Y, Cowan JA (2005) J Am Chem Soc 127:8408–8415

    Article  PubMed  CAS  Google Scholar 

  37. Schoeneich C (2004) Ann N Y Acad Sci 1012:164–170

    Article  CAS  Google Scholar 

  38. Lim J, Vachet RW (2003) Anal Chem 75:1164–1172

    Article  PubMed  CAS  Google Scholar 

  39. Bridgewater JD, Lim J, Vachet RW (2006) Anal Chem 78:2432–2438

    Article  PubMed  CAS  Google Scholar 

  40. Hlavaty JJ, Benner JS, Hornstra LJ, Schildkraut I (2000) Biochem 39:3097–3105

    Article  CAS  Google Scholar 

  41. Uchida K, Kawakishi S (1990) Arch Biochem Biophys 283:20–26

    Article  PubMed  CAS  Google Scholar 

  42. Riley DP (1999) Chem Rev 99:2573–2587

    Article  PubMed  CAS  Google Scholar 

  43. DE Cabelli, D Riley, JA Rodriguez, JS Valentine, H Zhu (2000). In: B Meunier (ed) Biomimetic oxidations catalyzed by transition metal complexes. Imperial College Press, London, pp 461–508

  44. Ueda J-I, Sudo A, Mori A, Ozawa T (1994) Arch Biochem Biophys 315:185–189

    Article  PubMed  CAS  Google Scholar 

  45. Bacic G, Spasojevic I, Secerov B, Mojovic M (2008) Spectrochimica Acta Part A Mol Biomol Spectrosc 69:1354–1366

    Article  CAS  Google Scholar 

  46. Kamibayashi M, Oowada S, Kameda H, Okada T, Inanami O, Ohta S, Ozawa T, Makino K, Kotake Y (2006) Free Radic Res 40:1166–1172

    Article  PubMed  CAS  Google Scholar 

  47. Stolze K, Udilova KN, Nohl H (2000) Free Radic Biol Med 29:1005–1014

    Article  PubMed  CAS  Google Scholar 

  48. Flora B, Gusman H, Helmerhorst EJ, Troxler RF, Oppenheim FG (2001) Protein Expr Purif 23:198–206

    Article  PubMed  CAS  Google Scholar 

  49. Held P (2002) Am Biotechnol Lab 20:18–19

    CAS  Google Scholar 

  50. Strlic M, Kolar J, Selih V-S, Kocar D, Pihlar B (2003) Acta Chim Slov 50:619–632

    CAS  Google Scholar 

  51. Khossravi M, Borchardt RT (1998) Pharma Res 15:1096–1102

    Article  CAS  Google Scholar 

  52. Winterbourn CC, Peskin AV, Parsons-Mair HN (2002) J Biol Chem 277:1906–1911

    Article  PubMed  CAS  Google Scholar 

  53. Dikalov SI, Vitek MP, Mason RP (2004) Free Radic Biol Med 36:340–347

    Article  PubMed  CAS  Google Scholar 

  54. Oroskar AA, Lambert C, Peak MJ (1996) Free Radic Biol Med 20:751–756

    Article  PubMed  CAS  Google Scholar 

  55. Farhataziz A, Ross B (1977) National standard reference data series, vol 59. US Government Printing Office, Washington

    Google Scholar 

  56. Yim MB, Chock PB, Stadtman ER (1990) Proc Natl Acad Sci USA 87:5006–5010

    Article  PubMed  CAS  Google Scholar 

  57. Hodgson EK, Fridovich I (1975) Biochemistry 14:5294–5299

    Article  PubMed  CAS  Google Scholar 

  58. Tuccio B, Lauricella R, Frejaville C, Bouteiller J-C, Tordo P (1995) J Chem Soc Perkin Trans 2, pp 295–298

  59. Sato H, Tani A, Ikeya M (2003) Jpn J Appl Phys 42:428–433

    Article  CAS  Google Scholar 

  60. Houghton EA, Nicholas KM (2007) Unpublished results

  61. Zhou L, Powell D, Nicholas KM (2006) Inorg Chem 45:3840–3842

    Article  PubMed  CAS  Google Scholar 

  62. Zhou L, Powell D, Nicholas KM (2007) Inorg Chem 46:2316–2321

    Article  PubMed  CAS  Google Scholar 

  63. Zhou L, Powell D, Nicholas KM (2007) Inorg Chem 46:7789–7799

    Article  PubMed  CAS  Google Scholar 

  64. Breslow R, Hunt JT, Smiley R, Tarnowski T (1983) J Am Chem Soc 105:5337–5342

    Article  CAS  Google Scholar 

  65. Sorrell TN, Borovik AS (1987) J Am Chem Soc 109:4255–4260

    Article  CAS  Google Scholar 

  66. Sorrell TN, Allen WE, White PS (1995) Inorg Chem 34:952–960

    Article  CAS  Google Scholar 

  67. Cross JB, Currier RP, Torraco DJ, Vanderberg LA, Wagner GL, Gladen PD (2003) Appl Environ Microbiol 69:2245–2252

    Article  PubMed  CAS  Google Scholar 

  68. Song B, Wang G, Yuan J (2007) Talanta 72:231–236

    Article  PubMed  CAS  Google Scholar 

  69. Villamena FA, Hadad CM, Zweier JL (2003) J Phys Chem A 107:4407–4414

    Article  CAS  Google Scholar 

  70. Keszler A, Kalyanaraman B, Hogg N (2003) Free Radic Biol Med 35:1149–1157

    Article  PubMed  CAS  Google Scholar 

  71. Iqbal M, Sharma SD, Mizote A, Fujisawa M, Okada S (2003) Teratog Carcinog Mutagen 23(Suppl 1):13–21

    Google Scholar 

  72. Ohta Y, Shiraishi N, Inai Y, Lee ISM, Iwahashi H, Nishikimi M (2001) Biochem Biophys Res Commun 287:888–894

    Article  PubMed  CAS  Google Scholar 

  73. Huang X, Atwood CS, Hartshorn MA, Multhaup G, Goldstein LE, Scarpa RC, Cuajungco MP, Gray DN, Lim J, Moir RD, Tanzi RE, Bush AI (1999) Biochemistry 38:7609–7616

    Article  PubMed  CAS  Google Scholar 

  74. Opazo C, Huang X, Cherny RA, Moir RD, Roher AE, White AR, Cappai R, Masters CL, Tanzi RE, Inestrosa NC, Bush AI (2002) J Biol Chem 277:40302–40308

    Article  PubMed  CAS  Google Scholar 

  75. Jiang H, Wu Y-C, Nakamura M, Liang Y, Tanaka Y, Holmes S, Dawson VL, Dawson TM, Ross CA, Smith WW (2007) Neurobiol Aging 28:1709–1717

    Article  PubMed  CAS  Google Scholar 

  76. Gupte A, Mumper RJ (2007) J Inorg Biochem 101:594–602

    Article  PubMed  CAS  Google Scholar 

  77. Khan MMT, Martell AE (1967) J Am Chem Soc 89:7104–7111

    Article  PubMed  CAS  Google Scholar 

  78. Peled T, Glukhman E, Hasson N, Adi S, Assor H, Yudin D, Landor C, Mandel J, Landau E, Prus E, Nagler A, Fibach E (2005) Exp Hematol 33:1092–1100

    Article  PubMed  CAS  Google Scholar 

  79. Heick HMC, Graff GLA, Humpers JEC (1972) Can J Microbiol 18:597–600

    Article  PubMed  CAS  Google Scholar 

  80. Murakawa S, Sano S, Yamashita H, Takahashi T (1977) Agric Biol Chem 41:1799–1800

    CAS  Google Scholar 

  81. Izawa S, Inoue Y, Kimura A (1995) FEBS Lett 368:73–76

    Article  PubMed  CAS  Google Scholar 

  82. Grant CM, MacIver FH, Dawes IW (1996) Curr Genet 29:511–515

    Article  PubMed  CAS  Google Scholar 

  83. Stephen DWS, Jamieson DJ (1996) FEMS Microbiol Lett 141:207–212

    Article  PubMed  CAS  Google Scholar 

  84. Yamashoji S, Kajimoto G (1986) Biochim Biophys Acta Bioenergy 852:25–29

    Article  CAS  Google Scholar 

  85. Witt I, Kronau R, Holzer H (1966) Biochim Biophys Acta 118:522–537

    PubMed  CAS  Google Scholar 

  86. Jamnik P, Raspor P (2005) J Biochem Mol Toxicol 19:195–203

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful for partial financial support of this research by the Petroleum Research Fund of the American Chemical Society. We are especially thankful to Yashige Kotake of the Oklahoma Medical Research Foundation for valuable assistance with the EPR spin-trapping experiments. We also appreciate helpful discussions with P. Cook and M. Ashby and the use of equipment in the Cook laboratory.

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  1. Department of Chemistry and Biochemistry, University of Oklahoma, Norman, OK, 73019, USA

    Eric A. Houghton & Kenneth M. Nicholas

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  1. Eric A. Houghton
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Correspondence to Kenneth M. Nicholas.

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Houghton, E.A., Nicholas, K.M. In vitro reactive oxygen species production by histatins and copper(I,II). J Biol Inorg Chem 14, 243–251 (2009). https://doi.org/10.1007/s00775-008-0444-x

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