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Phosphinic Peptides as Potent Inhibitors of Zinc-Metalloproteases

  • Dimitris GeorgiadisEmail author
  • Vincent Dive
Chapter
Part of the Topics in Current Chemistry book series (TOPCURRCHEM, volume 360)

Abstract

The development of transition-state analogs is a major objective in enzymology, not only for developing potent inhibitors of enzymes but also for dissecting enzyme catalytic mechanisms. Phosphinic peptides, which share closed structural similarities with the transition-state of peptide substrate upon hydrolysis, have thus been considered for identifying potent inhibitors of proteases. Focusing on the zinc-proteases family, this review presents the most important synthetic efforts performed to obtain the desired compounds. Crystal structures of the phosphinic peptides in interaction with their zinc-protease targets are reported to illustrate the structural features which may explain the potency of these compounds and how they contribute to uncover key enzyme catalytic residues. Based on a remarkable metabolic stability, phosphinic peptides can be used to probe the in vivo function of zinc-proteases. Progress on chemistry and better understanding on the functional roles of zinc-proteases should allow transferring these compounds from shelf to clinic.

Keywords

Inhibitors Phosphinic peptides Zn-proteases 

References

  1. 1.
    Turk B (2006) Nat Rev Drug Discov 5:785–799Google Scholar
  2. 2.
    Puente XS, Sanchez LM, Overall CM, Lopez-Otin C (2003) Nat Rev Genet 4:544–558Google Scholar
  3. 3.
    Lopez-Otin C, Matrisian LM (2007) Nat Rev Cancer 7:800–808Google Scholar
  4. 4.
    Zaman MA, Oparil S, Calhoun DA (2002) Nat Rev Drug Discov 1:621–636Google Scholar
  5. 5.
    Peyman A, Budt KH, Spanig J, Ruppert D (1993) Angew Chem Int Ed Engl 32:1720–1722Google Scholar
  6. 6.
    Sheng XC, Casarez A, Cai R, Clarke MO, Chen X, Cho A, Delaney Iv WE, Doerffler E, Ji M, Mertzman M, Pakdaman R, Pyun HJ, Rowe T, Wu Q, Xu J, Kim CU (2012) Bioorg Med Chem Lett 22:1394–1396Google Scholar
  7. 7.
    Ondetti MA, Condon ME, Reid J, Sabo EF, Cheung HS, Cushman DW (1979) Biochemistry 18:1427–1430Google Scholar
  8. 8.
    Holmes MA, Matthews BW (1981) Biochemistry 20:6912–6920Google Scholar
  9. 9.
    Petrillo EW Jr, Ondetti MA (1982) Med Res Rev 2:1–41Google Scholar
  10. 10.
    Devel L, Czarny B, Beau F, Georgiadis D, Stura E, Dive Vincent V (2010) Biochimie 92:1501–1508Google Scholar
  11. 11.
    Christianson DW, Lipscomb WN (1988) J Am Chem Soc 110:5560–5565Google Scholar
  12. 12.
    Holden HM, Tronrud DE, Monzingo AF, Weaver LH, Matthews BW (1987) Biochemistry 26:8542–8553Google Scholar
  13. 13.
    Hanson JE, Kaplan AP, Bartlett PA (1989) Biochemistry 28:6294–6305Google Scholar
  14. 14.
    Mookhtiar KA, Marlowe CK, Bartlett PA, Van Wart HE (1987) Biochemistry 26:1962–1965Google Scholar
  15. 15.
    Dive V, Yiotakis A, Nicolaou A, Toma F (1990) Eur J Biochem 191:685–693Google Scholar
  16. 16.
    Yiotakis A, Lecoq A, Nicolaou A, Labadie J, Dive V (1994) Biochem J 303:323–327Google Scholar
  17. 17.
    Merz KM Jr, Kollman PA (1989) J Am Chem Soc 111:5649–5658Google Scholar
  18. 18.
    Morgan BP, Scholtz JM, Ballinger MD, Zipkin ID, Bartlett PA (1991) J Am Chem Soc 113:297–307Google Scholar
  19. 19.
    Yiotakis A, Georgiadis D, Matziari M, Makaritis A, Dive V (2004) Curr Org Chem 8:1135–1158Google Scholar
  20. 20.
    Mucha A (2012) Molecules 17:13530–13568Google Scholar
  21. 21.
    Thottathil JK, Ryono DE, Przybyla CA, Moniot JL, Neubeck R (1984) Tetrahedron Lett 25:4741–4744Google Scholar
  22. 22.
    McKittrick BA, Stamford AW, Weng X, Ma K, Chackalamannil S, Czarniecki M, Cleven RM, Fawzi AB (1996) Bioorg Med Chem Lett 6:1629–1634Google Scholar
  23. 23.
    Miller DJ, Hammond SM, Anderluzzi D, Bugg TDH (1998) J Chem Soc. Perkin Trans 1:131–142Google Scholar
  24. 24.
    Baylis EK, Campbell CD, Dingwall JG (1984) J Chem Soc. Perkin Trans 1:2845–2853Google Scholar
  25. 25.
    Cowart M, Kowaluk EA, Kohlhaas KL, Alexander KM, Kerwin JF Jr (1996) Bioorg Med Chem Lett 6:999–1002Google Scholar
  26. 26.
    Lecoq A, Yiotakis A, Dive V (1994) Synth Commun 24:2877–2882Google Scholar
  27. 27.
    Khomutov AR, Osipova TI, Khurs EN, Alferov KV, Khomutov RM (1996) Russ Chem Bull 45:1961–1964Google Scholar
  28. 28.
    Belyankin AV, Khomutov AR, Zhukov YN, Kartasheva ON, Khomutov RM (1997) Russ Chem Bull 46:133–136Google Scholar
  29. 29.
    Zhukov YN, Khomutov AR, Osipova TI, Khomutov RM (1999) Russ Chem Bull 48:1348–1351Google Scholar
  30. 30.
    Alferov KV, Zhukov YN, Khurs EN, Osipova TI, Khomutov RM (2001) Russ Chem Bull 50:316–318Google Scholar
  31. 31.
    Liboska R, Pícha J, Hančlová I, Buděšínský M, Šanda M, Jiráček J (2008) Tetrahedron Lett 49:5629–5631Google Scholar
  32. 32.
    Jiao XJ, Verbruggen C, Borloo M, Bollaert W, De Groot A, Dommisse R, Haemers A (1994) Synthesis 23–24Google Scholar
  33. 33.
    Li S, Whitehead JK, Hammer RP (2007) J Org Chem 72:3116–3118Google Scholar
  34. 34.
    Olszewski TK, Boduszek B (2011) Synthesis 437–442Google Scholar
  35. 35.
    Borloo M, Jiao XY, Wojtowicz H, Rajan P, Verbruggen C, Augustyns K, Haemers A (1995) Synthesis 1074–1076Google Scholar
  36. 36.
    Boyd EA, Chan WC, Loh VM Jr (1996) Tetrahedron Lett 37:1647–1650Google Scholar
  37. 37.
    Hatam M, Martens J (1995) Synth Commun 25:2553–2559Google Scholar
  38. 38.
    Mores A, Matziari M, Beau F, Cuniasse P, Yiotakis A, Dive V (2008) J Med Chem 51:2216–2226Google Scholar
  39. 39.
    Yamagishi T, Mori JI, Haruki T, Yokomatsu T (2011) Tetrahedron: Asymmetry 22:1358–1363Google Scholar
  40. 40.
    Haruki T, Yamagishi T, Yokomatsu T (2007) Tetrahedron: Asymmetry 18:2886–2893Google Scholar
  41. 41.
    McCleery PP, Tuck B (1989) J Chem Soc. Perkin Trans 1:1319–1329Google Scholar
  42. 42.
    Yao Q, Yuan C (2013) J Org Chem 78:6962–6974Google Scholar
  43. 43.
    Cristau HJ, Coulombeau A, Genevois-Borella A, Pirat JL (2001) Tetrahedron Lett 42:4491–4494Google Scholar
  44. 44.
    Cristau HJ, Coulombeau A, Genevois-Borella A, Sanchez F, Pirat JL (2002) J Organomet Chem 643–644:381–391Google Scholar
  45. 45.
    Buchardt J, Meldal M (2000) J Chem Soc Perkin Trans 1:3306–3310Google Scholar
  46. 46.
    Dorff PH, Chiu G, Goldstein SW, Morgan BP (1998) Tetrahedron Lett 39:3375–3378Google Scholar
  47. 47.
    Manzenrieder F, Kessler H (2009) Adv Exp Med Biol 611:11–12Google Scholar
  48. 48.
    Vassiliou S, Tzouma E (2013) J Org Chem 78:10069–10076Google Scholar
  49. 49.
    Schoen WR, Parsons WH (1988) Tetrahedron Lett 29:5201–5204Google Scholar
  50. 50.
    Gurulingappa H, Buckhaults P, Kumar SK, Kinzler KW, Vogelstein B, Khan SR (2003) Tetrahedron Lett 44:1871–1873Google Scholar
  51. 51.
    Gurulingappa H, Buckhalts P, Kinzler KW, Vogelstein B, Khan SR (2004) Bioorg Med Chem Lett 14:3531–3533Google Scholar
  52. 52.
    Matziari M, Nasopoulou M, Yiotakis A (2006) Org Lett 8:2317–2319Google Scholar
  53. 53.
    Chen S, Coward JK (1996) Tetrahedron Lett 37:4335–4338Google Scholar
  54. 54.
    Matziari M, Yiotakis A (2005) Org Lett 7:4049–4052Google Scholar
  55. 55.
    Rozhko LF, Ragulin VV (2005) Amino Acids 29:139–143Google Scholar
  56. 56.
    Dmitriev ME, Ragulin VV (2010) Tetrahedron Lett 51:2613–2616Google Scholar
  57. 57.
    Dmitriev ME, Ragulin VV (2012) Tetrahedron Lett 53:1634–1636Google Scholar
  58. 58.
    Ross FC, Botting NP, Leeson PD (1996) Bioorg Med Chem Lett 6:2643–2646Google Scholar
  59. 59.
    Bertenshaw SR, Rogers RS, Stern MK, Norman BH, Moore WM, Jerome GM, Branson LM, McDonald JF, McMahon EG, Palomo MA (1993) J Med Chem 36:173–176Google Scholar
  60. 60.
    Štrancar K, Boniface A, Blanot D, Gobec S (2007) Arch Pharm (Weinheim) 340:127–134Google Scholar
  61. 61.
    Chackalamannil S, Chung S, Stamford AW, McKittrick BA, Wang Y, Tsai H, Cleven R, Fawzi A, Czarniecki M (1996) Bioorg Med Chem Lett 6:1257–1260Google Scholar
  62. 62.
    Reiter LA, Rizzi JP, Pandit J, Lasut MJ, McGahee SM, Parikh VD, Blake JF, Danley DE, Laird ER, Lopez-Anaya A, Lopresti-Morrow LL, Mansour MN, Martinelli GJ, Mitchell PG, Owens BS, Pauly TA, Reeves LM, Schulte GK, Yocum SA (1999) Bioorg Med Chem Lett 9:127–132Google Scholar
  63. 63.
    Goulet JL, Kinneary JF, Durette PL, Stein RL, Harrison RK, Izquierdo-Martin M, Kuo DW, Lin TY, Hagmann WK (1994) Bioorg Med Chem Lett 4:1221–1224Google Scholar
  64. 64.
    Georgiadis D, Dive V, Yiotakis A (2001) J Org Chem 66:6604–6610Google Scholar
  65. 65.
    Reiter LA, Jones BP (1997) J Org Chem 62:2808–2812Google Scholar
  66. 66.
    Krapcho J, Turk C, Cushman DW, Powell JR, DeForrest JM, Spitzmiller ER, Karanewsky DS, Duggan M, Rovnyak G, Schwartz J, Natarajan S, Godfrey JD, Ryono DE, Neubeck R, Atwal KS, Petrillo EW Jr (1988) J Med Chem 31:1148–1160Google Scholar
  67. 67.
    Yiotakis A, Lecoq A, Vassiliou S, Raynal I, Cuniasse P, Dive V (1994) J Med Chem 37:2713–2720Google Scholar
  68. 68.
    Kende AS, Dong HQ, Liu X, Ebetino FH (2002) Tetrahedron Lett 43:4973–4976Google Scholar
  69. 69.
    Campagne JM, Coste J, Guillou L, Heitz A, Jouin P (1993) Tetrahedron Lett 34:4181–4184Google Scholar
  70. 70.
    Chen H, Noble F, Coric P, Fournie-Zaluski MC, Roques BP (1998) Proc Natl Acad Sci U S A 95:12028–12033Google Scholar
  71. 71.
    Reiter LA, Mitchell PG, Martinelli GJ, Lopresti-Morrow LL, Yocum SA, Eskra JD (2003) Bioorg Med Chem Lett 13:2331–2336Google Scholar
  72. 72.
    Manzenrieder F, Frank AO, Huber T, Dorner-Ciossek C, Kessler H (2007) Bioorg Med Chem 15:4136–4143Google Scholar
  73. 73.
    Chen H, Noble F, Mothé A, Meudal H, Coric P, Danascimento S, Roques BP, George P, Fournié-Zaluski MC (2000) J Med Chem 43:1398–1408Google Scholar
  74. 74.
    Makaritis A, Georgiadis D, Dive V, Yiotakis A (2003) Chem Eur J 9:2079–2094Google Scholar
  75. 75.
    Matziari M, Bauer K, Dive V, Yiotakis A (2008) J Org Chem 73:8591–8593Google Scholar
  76. 76.
    Lloyd J, Schmidt JB, Hunt JT, Barrish JC, Little DK, Tymiak AA (1996) Bioorg Med Chem Lett 6:1323–1326Google Scholar
  77. 77.
    Yiotakis A, Vassiliou S, Jiráček J, Dive V (1996) J Org Chem 61:6601–6605Google Scholar
  78. 78.
    Jiracek J, Yiotakis A, Vincent B, Lecoq A, Nicolaou A, Checler F, Dive V (1995) J Biol Chem 270:21701–21706Google Scholar
  79. 79.
    Jirácek J, Yiotakis A, Vincent B, Checler F, Dive V (1996) J Biol Chem 271:19606–19611Google Scholar
  80. 80.
    Dive V, Cotton J, Yiotakis A, Michaud A, Vassiliou S, Jiracek J, Vazeux G, Chauvet MT, Cuniasse P, Corvol P (1999) Proc Natl Acad Sci U S A 96:4330–4335Google Scholar
  81. 81.
    Buchardt J, Ferreras M, Krog-Jensen C, Delaissé JM, Foged NT, Meldal M (1999) Chem Eur J 5:2877–2884Google Scholar
  82. 82.
    Buchardt J, Schiødt CB, Krog-Jensen C, Delaissé JM, Foged NT, Meldal M (2000) J Comb Chem 2:624–638Google Scholar
  83. 83.
    Christensen C, Groth T, Schiødt CB, Foged NT, Meldal M (2003) QSAR Comb Sci 22:737–744Google Scholar
  84. 84.
    Devel L, Rogakos V, David A, Makaritis A, Beau F, Cuniasse P, Yiotakis A, Dive V (2006) J Biol Chem 281:11152–11160Google Scholar
  85. 85.
    Fields GB, Lauer-Fields J, Brew K, Lauer-Fields J, Hammer RP, Li S, Whitehead JK (2007) J Am Chem Soc 129:10408–10417Google Scholar
  86. 86.
    Bhowmick M, Sappidi RR, Fields GB, Lepore SD (2011) Biopolymers 96:1–3Google Scholar
  87. 87.
    Bhowmick M, Fields GB (2012) Int J Pept Res Ther 18:335–339Google Scholar
  88. 88.
    Georgiadis D, Matziari M, Yiotakis A (2001) Tetrahedron 57:3471–3478Google Scholar
  89. 89.
    Nasopoulou M, Matziari M, Dive V, Yiotakis A (2006) J Org Chem 71:9525–9527Google Scholar
  90. 90.
    Vitharana D, France JE, Scarpetti D, Bonneville GW, Majer P, Tsukamoto T (2002) Tetrahedron: Asymmetry 13:1609–1614Google Scholar
  91. 91.
    Chen H, Noble F, Roques BP, Fournié-Zaluski MC (2001) J Med Chem 44:3523–3530Google Scholar
  92. 92.
    Jullien N, Makritis A, Georgiadis D, Beau F, Yiotakis A, Dive V (2010) J Med Chem 53:208–220Google Scholar
  93. 93.
    Matziari M, Dellis D, Dive V, Yiotakis A, Samios J (2010) J Phys Chem B 114:421–428Google Scholar
  94. 94.
    Yiotakis A, Makaritis A, Georgiadis D, Matziari M, Dive V (2002) Peptides 2002:330–331Google Scholar
  95. 95.
    Parsons WH, Patchett AA, Bull HG, Schoen WR, Taub D, Davidson J, Combs PL, Springer JP, Gadebusch H, Weissberger B, Valiant ME, Mellin TN, Busch RD (1988) J Med Chem 31:1772–1778Google Scholar
  96. 96.
    Liu X, Hu XE, Tian X, Mazur A, Ebetino FH (2002) J Organomet Chem 646:212–222Google Scholar
  97. 97.
    Cristau HJ, Pirat JL, Virieux D, Monbrun J, Ciptadi C, Bekro YA (2005) J Organomet Chem 690:2472–2481Google Scholar
  98. 98.
    Monbrun J, Dayde B, Cristau HJ, Volle JN, Virieux D, Pirat JL (2011) Tetrahedron 67:540–545Google Scholar
  99. 99.
    Yamagishi T, Ichikawa H, Haruki T, Yokomatsu T (2008) Org Lett 10:4347–4350Google Scholar
  100. 100.
    Georgiadis D, Matziari M, Vassiliou S, Dive V, Yiotakis A (1999) Tetrahedron 55:14635–14648Google Scholar
  101. 101.
    Matziari M, Georgiadis D, Dive V, Yiotakis A (2001) Org Lett 3:659–660Google Scholar
  102. 102.
    Matziari M, Beau F, Cuniasse P, Dive V, Yiotakis A (2004) J Med Chem 47:325–336Google Scholar
  103. 103.
    David A, Steer D, Bregant S, Devel L, Makaritis A, Beau F, Yiotakis A, Dive V (2007) Angew Chem Int Ed Engl 46:3275–3277Google Scholar
  104. 104.
    Bregant S, Huillet C, Devel L, Dabert-Gay AS, Beau F, Thai R, Czarny B, Yiotakis A, Dive V (2009) J Proteome Res 8:2484–2494Google Scholar
  105. 105.
    Aminoethylphosphinic acid derivatives (1988) EP282219,Google Scholar
  106. 106.
    Vassiliou S, Xeilari M, Yiotakis A, Grembecka J, Pawełczak M, Kafarski P, Mucha A (2007) Bioorg Med Chem 15:3187–3200Google Scholar
  107. 107.
    Rogakos V, Georgiadis D, Dive V, Yiotakis A (2009) Org Lett 11:4696–4699Google Scholar
  108. 108.
    Nasopoulou M, Georgiadis D, Matziari M, Dive V, Yiotakis A (2007) J Org Chem 72:7222–7228Google Scholar
  109. 109.
    Yamagishi T, Kinbara A, Okubo N, Sato S, Fukaya H (2012) Tetrahedron: Asymmetry 23:1633–1639Google Scholar
  110. 110.
    Georgiadis D, Beau F, Czarny B, Cotton J, Yiotakis A, Dive V (2003) Circ Res 93:148–154Google Scholar
  111. 111.
    Georgiadis D, Cuniasse P, Cotton J, Yiotakis A, Dive V (2004) Biochemistry 43:8048–8054Google Scholar
  112. 112.
    Demange L, Dugave C (2001) Tetrahedron Lett 42:6295–6297Google Scholar
  113. 113.
    Yamagishi T, Tashiro N, Yokomatsu T (2011) J Org Chem 76:5472–5476Google Scholar
  114. 114.
    Anthony CS, Masuyer G, Sturrock ED, Acharya KR (2012) Curr Med Chem 19:845–855Google Scholar
  115. 115.
    Dive V, Chang CF, Yiotakis A, Sturrock ED (2009) Curr Pharm Des 15:3606–3621Google Scholar
  116. 116.
    Redelinghuys P, Nchinda AT, Sturrock ED (2005) Ann N Y Acad Sci 1056:160–175Google Scholar
  117. 117.
    Anthony CS, Corradi HR, Schwager SLU, Redelinghuys P, Georgiadis D, Dive V, Acharya KR, Sturrock ED (2010) J Biol Chem 285:35685–35693Google Scholar
  118. 118.
    Corradi HR, Chitapi I, Sewell BT, Georgiadis D, Dive V, Sturrock ED, Acharya KR (2007) Biochemistry 46:5473–5478Google Scholar
  119. 119.
    Roques BP, Noble F, Dauge V, Fournie-Zaluski MC, Beaumont A (1993) Pharmacol Rev 45:87–146Google Scholar
  120. 120.
    Patey G, De La Baume S, Schwartz JC, Gros C, Roques B, Fournie-Zaluski MC, Soroca-Lucas E (1981) Science 212:1153–1155Google Scholar
  121. 121.
    Roques BP, Lucas-Soroca E, Chaillet P, Costentin J, Fournie-Zaluski MC (1983) Proc Natl Acad Sci U S A 80:3178–3182Google Scholar
  122. 122.
    Matthews BW (1988) Acc Chem Res 21:341–347Google Scholar
  123. 123.
    Tiraboschi G, Jullian N, Thery V, Antonczak S, Fournie-Zaluski MC, Roques BP (1999) Protein Eng 12:141–149Google Scholar
  124. 124.
    Selkti M, Tomas A, Gaucher JF, Prange T, Fournie-Zaluski MC, Chen H, Roques BP (2003) Acta Crystallogr D Biol Crystallogr 59:1200–1205Google Scholar
  125. 125.
    Samuelsson B, Dahlen SE, Lindgren JA, Rouzer CA, Serhan CN (1987) Science 237:1171–1176Google Scholar
  126. 126.
    Thunnissen MM, Nordlund P, Haeggstrom JZ (2001) Nat Struct Biol 8:131–135Google Scholar
  127. 127.
    Tholander F, Muroya A, Roques BP, Fournie-Zaluski MC, Thunnissen MM, Haeggstrom JZ (2008) Chem Biol 15:920–929Google Scholar
  128. 128.
    Tanioka T, Hattori A, Masuda S, Nomura Y, Nakayama H, Mizutani S, Tsujimoto M (2003) J Biol Chem 278:32275–32283Google Scholar
  129. 129.
    Zervoudi E, Saridakis E, Birtley JR, Seregin SS, Reeves E, Kokkala P, Aldhamen YA, Amalfitano A, Mavridis IM, James E, Georgiadis D, Stratikos E (2013) Proc Natl Acad Sci U S A 110:19890–19895Google Scholar
  130. 130.
    McGowan S, Oellig CA, Birru WA, Caradoc-Davies TT, Stack CM, Lowther J, Skinner-Adams T, Mucha A, Kafarski P, Grembecka J, Trenholme KR, Buckle AM, Gardiner DL, Dalton JP, Whisstock JC (2010) Proc Natl Acad Sci U S A 107:2449–2454Google Scholar
  131. 131.
    Wang YX, Zhao L, Nagashima M, Vincelette J, Sukovich D, Li W, Subramanyam B, Yuan S, Emayan K, Islam I, Hrvatin P, Bryant J, Light DR, Vergona R, Morser J, Buckman BO (2007) Thromb Haemost 97:45–53Google Scholar
  132. 132.
    Adler M, Bryant J, Buckman B, Islam I, Larsen B, Finster S, Kent L, May K, Mohan R, Yuan S, Whitlow M (2005) Biochemistry 44:9339–9347Google Scholar
  133. 133.
    Adler M, Buckman B, Bryant J, Chang Z, Chu K, Emayan K, Hrvatin P, Islam I, Morser J, Sukovich D, West C, Yuan S, Whitlow M (2008) Acta Crystallogr Sect D Biol Crystallogr 64:149–157Google Scholar
  134. 134.
    Zhou J, Neale JH, Pomper MG, Kozikowski AP (2005) Nat Rev Drug Discov 4:1015–1026Google Scholar
  135. 135.
    Bostwick DG, Pacelli A, Blute M, Roche P, Murphy GP (1998) Cancer 82:2256–2261Google Scholar
  136. 136.
    Barinka C, Hlouchova K, Rovenska M, Majer P, Dauter M, Hin N, Ko YS, Tsukamoto T, Slusher BS, Konvalinka J, Lubkowski J (2008) J Mol Biol 376:1438–1450Google Scholar
  137. 137.
    Gomis-Ruth FX, Trillo-Muyo S, Stocker W (2012) Biol Chem 393:1027–1041Google Scholar
  138. 138.
    Grams F, Dive V, Yiotakis A, Yiallouros I, Vassiliou S, Zwilling R, Bode W, Stocker W (1996) Nat Struct Biol 3:671–675Google Scholar
  139. 139.
    Yiallouros I, Vassiliou S, Yiotakis A, Zwilling R, Stocker W, Dive V (1998) Biochem J 331:375–379Google Scholar
  140. 140.
    Yiallouros I, Grosse Berkhoff E, Stocker W (2000) FEBS Lett 484:224–228Google Scholar
  141. 141.
    Kawasaki A, Nakano H, Hosokawa A, Nakatsu T, Kato H, Watanabe K (2010) J Biol Chem 285:34972–34980Google Scholar
  142. 142.
    McGowan S, Porter CJ, Lowther J, Stack CM, Golding SJ, Skinner-Adams TS, Trenholme KR, Teuscher F, Donnelly SM, Grembecka J, Mucha A, Kafarski P, Degori R, Buckle AM, Gardiner DL, Whisstock JC, Dalton JP (2009) Proc Natl Acad Sci U S A 106:2537–2542Google Scholar
  143. 143.
    Fournie-Zaluski MC, Poras H, Roques BP, Nakajima Y, Ito K, Yoshimoto T (2009) Acta Crystallogr D Biol Crystallogr 65:814–822Google Scholar
  144. 144.
    Jozic D, Bourenkow G, Bartunik H, Scholze H, Dive V, Henrich B, Huber R, Bode W, Maskos K (2002) Structure 10:1097–1106Google Scholar
  145. 145.
    Czarny B, Stura EA, Devel L, Vera L, Cassar-Lajeunesse E, Beau F, Calderone V, Fragai M, Luchinat C, Dive V (2013) J Med Chem 56:1149–1159Google Scholar
  146. 146.
    Morrison RA, Singhvi SM, Peterson AE, Pocetti DA, Migdalof BH (1990) Drug Metab Dispos 18:253–257Google Scholar
  147. 147.
    Junot C, Gonzales MF, Ezan E, Cotton J, Vazeux G, Michaud A, Azizi M, Vassiliou S, Yiotakis A, Corvol P, Dive V (2001) J Pharmacol Exp Ther 297:606–611Google Scholar
  148. 148.
    Dive V, Andarawewa KL, Boulay A, Matziari M, Beau F, Guerin E, Rousseau B, Yiotakis A, Rio MC (2005) Int J Cancer 113:775–781Google Scholar
  149. 149.
    Defamie V, Laurens M, Patrono D, Devel L, Brault A, Saint-Paul MC, Yiotakis A, Barbry P, Gugenheim J, Crenesse D, Dive V, Huet PM, Mari B (2008) Hepatology 47:177–185Google Scholar
  150. 150.
    Johnson JL, Devel L, Czarny B, George SJ, Jackson CL, Rogakos V, Beau F, Yiotakis A, Newby AC, Dive V (2011) Arterioscler Thromb Vasc Biol 31:528–535Google Scholar
  151. 151.
    Marchant DJ, Bellac CL, Moraes TJ, Wadsworth SJ, Dufour A, Butler GS, Bilawchuk LM, Hendry RG, Robertson AG, Cheung CT, Ng J, Ang L, Luo Z, Heilbron K, Norris MJ, Duan W, Bucyk T, Karpov A, Devel L, Georgiadis D, Hegele RG, Luo H, Granville DJ, Dive V, McManus BM, Overall CM (2014) Nat Med 20:493–502Google Scholar
  152. 152.
    Cursio R, Mari B, Louis K, Rostagno P, Saint-Paul MC, Giudicelli J, Bottero V, Anglard P, Yiotakis A, Dive V, Gugenheim J, Auberger P (2002) FASEB J 16:93–95Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Department of Chemistry, Laboratory of Organic ChemistryUniversity of AthensAthensGreece
  2. 2.CEA-Saclay, Service d’Ingénierie Moléculaire des Protéines Labex LERMIT, CEA-DSV-iBiTecSGif/YvetteFrance

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