Thiazoles in Peptides and Peptidomimetics

  • Jeffrey Y. W. Mak
  • Weijun Xu
  • David P. Fairlie
Chapter
Part of the Topics in Heterocyclic Chemistry book series (TOPICS, volume 48)

Abstract

The natural occurrence of the thiazole ring in chemistry and biology has inspired its widespread use in synthetic peptidomimetics as structural templates, biological probes, and pharmaceuticals. Thiazole can be viewed as a dehydrated cyclized derivative of cysteine, incorporated into peptide sequences through chemical synthesis or ribosomal biosynthesis. Thiazoles are planar heterocycles and valuable synthetic templates with a strong hydrogen bond accepting nitrogen, a sulfur atom with extended lone pair electron orbitals, and an aromatic π-cloud. These properties can influence molecular conformation and direct interactions with proteins, leading to development of thiazole-containing peptidomimetics as protein mimicking scaffolds, modulators of cell surface proteins like G protein-coupled receptors (GPCRs), inhibitors of enzymes, and agonists or antagonists of protein–protein interactions. The thiazole ring is the most common five-membered heterocycle present in pharmaceuticals. This perspective article describes important properties of thiazoles in synthetic peptidomimetics and highlights key examples, including some from the last 5 years.

Keywords

Amino acid Conformation Cyclic peptide Cysteine Drug Heterocycle Peptidomimetic Pharmaceutical Protein structure Thiazole 

Abbreviations

CCK

Cholecystokinin

CRF

Corticotropin-releasing factor

cSRC

Proto-oncogenic (sarcoma) protein tyrosine-protein kinase

FDA

Food and drug administration (USA)

NSAID

Non-steroidal anti-inflammatory drug

SAR

Structure–activity relationships

Notes

Acknowledgments

We acknowledge support from the Australian Research Council (DP130100629, DP150104609, CE140100011) and the National Health and Medical Research Council of Australia (APP1084018). DF is an NHMRC Senior Principal Research Fellow (APP1027369).

References

  1. 1.
    Davyt D, Serra G (2010) Mar Drugs 8:2755CrossRefGoogle Scholar
  2. 2.
    Donia MS, Schmidt EW (2010) Cyanobactins – ubiquitous cyanobacterial ribosomal peptide metabolites. In: Liu H-W, Mander L (eds) Comprehensive natural products II. Elsevier, Oxford, p 539CrossRefGoogle Scholar
  3. 3.
    Jin Z (2013) Nat Prod Rep 30:869CrossRefGoogle Scholar
  4. 4.
    Melby JO, Nard NJ, Mitchell DA (2011) Curr Opin Chem Biol 15:369CrossRefGoogle Scholar
  5. 5.
    Leoni A, Locatelli A, Morigi R, Rambaldi M (2014) Expert Opin Ther Pat 24:201CrossRefGoogle Scholar
  6. 6.
    Dondoni A (2010) Org Biomol Chem 8:3366CrossRefGoogle Scholar
  7. 7.
    Powell RS (1969) In: Kirk-Othmer encyclopedia of chemical technology, 2nd ed, vol 20, p 185Google Scholar
  8. 8.
    Dondoni A, Merino P (1996) Thiazoles. In: Katritzky AR, Rees CW, Scriven EFV (eds) Comprehensive heterocyclic chemistry II. Pergamon, Oxford, 373 pGoogle Scholar
  9. 9.
    Matthews EJ, Kruhlak NL, Benz RD, Contrera JF, Rogers BA, Wolf MA, Richard AM (2008) DSSTox FDA maximum (recommended) daily dose database (FDAMDD): SDF files and documentation, updated version: FDAMDD_v3b_1216_15Feb2008Google Scholar
  10. 10.
    Geyer A, Enck S (2013) Approaches to thiazole dipeptides for the synthesis of thiopeptide antibiotics In: Attanasi OA, Spinelli D (eds) Targets in heterocyclic systems: chemistry and properties, vol 16. Royal Society of Chemistry, p 113Google Scholar
  11. 11.
    Wu Y-J, Yang BV (2011) Five-membered ring systems: with N and S (Se) atoms. In: Gordon WG, John AJ (eds) Progress in heterocyclic chemistry, vol 23. Elsevier, Oxford, p 267Google Scholar
  12. 12.
    Wu Y-J, Yang BV (2012) Five-membered ring systems: with N and S (Se) atoms. In: Gordon WG, John AJ (eds) Progress in heterocyclic chemistry, vol 24. Elsevier, Oxford, p 281Google Scholar
  13. 13.
    Wu Y-J, Yang BV (2013) Five-membered ring systems: with N and S (Se) atoms. In: Gordon WG, John AJ (eds) Progress in heterocyclic chemistry, vol 25. Elsevier, Oxford, p 257Google Scholar
  14. 14.
    Wu Y-J, Yang BV (2014) Five-membered ring systems: with N and S (Se) atoms. In: Gordon WG, John AJ (eds) Progress in heterocyclic chemistry, vol 26. Elsevier, Amsterdam, p 279Google Scholar
  15. 15.
    Wu YJ, Yang BV (2011) Five-membered ring systems: with N and S (Se) atoms. In: Gordon G, John AJ (eds) Progress in heterocyclic chemistry, vol 22. Elsevier, Oxford, p 259Google Scholar
  16. 16.
    Xu Z, Ye T (2011) Thiazoline and thiazole and their derivatives. In: Majumdar KC, Chattopadhyay SK (eds) Heterocycles in natural product synthesis. Wiley-VCH, Weinheim, p 459CrossRefGoogle Scholar
  17. 17.
    Hantzsch A, Weber JH (1887) Chem Ber 20:3118CrossRefGoogle Scholar
  18. 18.
    Snyder NL, Boisvert CJ (2011) Hantzsch synthesis. Wiley, Hoboken, p 591Google Scholar
  19. 19.
    Ambhaikar NB (2013) Thiazoles and benzothiazoles. In: Li JJ (ed) Heterocyclic chemistry in drug discovery. Wiley, Hoboken, p 283Google Scholar
  20. 20.
    Lu J-Y, Riedrich M, Wojtas KP, Arndt H-D (2013) Synthesis 45:1300CrossRefGoogle Scholar
  21. 21.
    Shalaby MA, Grote CW, Rapoport H (1996) J Org Chem 61:9045CrossRefGoogle Scholar
  22. 22.
    Holzapfel CW, Pettit GR (1985) J Org Chem 50:2323CrossRefGoogle Scholar
  23. 23.
    Bredenkamp MW, Holzapfel CW, van Zyl WJ (1990) Synth Commun 20:2235CrossRefGoogle Scholar
  24. 24.
    Aguilar E, Meyers AI (1994) Tetrahedron Lett 35:2473CrossRefGoogle Scholar
  25. 25.
    Butler JD, Coffman KC, Ziebart KT, Toney MD, Kurth MJ (2010) Chem Eur J 16:9002CrossRefGoogle Scholar
  26. 26.
    Nefzi A, Arutyunyan S, Fenwick JE (2010) J Org Chem 75:7939CrossRefGoogle Scholar
  27. 27.
    Cohrt AE, Nielsen TE (2013) ACS Comb Sci 16:71CrossRefGoogle Scholar
  28. 28.
    Murru S, Nefzi A (2014) ACS Comb Sci 16:39CrossRefGoogle Scholar
  29. 29.
    Weiss KM, Wei S, Tsogoeva SB (2011) Org Biomol Chem 9:3457CrossRefGoogle Scholar
  30. 30.
    Cook AH, Heilbron IM, Levy AL (1947) J Chem Soc 1594Google Scholar
  31. 31.
    Cook AH, Heilbron I, Macdonald SF, Mahadevan AP (1949) J Chem Soc 1064Google Scholar
  32. 32.
    Ahmad NM (2005) Cook-Heilbron 5-aminothiazole synthesis. Wiley, Hoboken, p 275Google Scholar
  33. 33.
    Lingaraju GS, Swaroop TR, Vinayaka AC, Kumar KSS, Sadashiva MP, Rangappa KS (2012) Synthesis 44:1373CrossRefGoogle Scholar
  34. 34.
    Gabriel S (1910) Ber Dtsch Chem Ges 43:134CrossRefGoogle Scholar
  35. 35.
    Gabriel S (1910) Ber Dtsch Chem Ges 43:1283CrossRefGoogle Scholar
  36. 36.
    Kiryanov AA, Sampson P, Seed AJ (2001) J Org Chem 66:7925CrossRefGoogle Scholar
  37. 37.
    Di Credico B, Reginato G, Gonsalvi L, Peruzzini M, Rossin A (2011) Tetrahedron 67:267CrossRefGoogle Scholar
  38. 38.
    Nygaard L, Asmussen E, Hoeg JH, Maheshwari RC, Nielsen CH, Petersen IB, Rastrup-Andersen J, Soerensen GO (1971) J Mol Struct 8:225CrossRefGoogle Scholar
  39. 39.
    Beker W, Szarek P, Komorowski L, Lipiński J (2013) J Phys Chem A 117:1596CrossRefGoogle Scholar
  40. 40.
    Metzger JV, Vincent EJ (1979) Properties and reactions of thiazoles. In: Metzger JV (ed) Thiazoles and its derivatives, vol 1, The chemistry of heterocyclic compounds. Wiley, New YorkGoogle Scholar
  41. 41.
    Ioannidis S, Lamb ML, Almeida L, Guan H, Peng B, Bebernitz G, Bell K, Alimzhanov M, Zinda M (2010) Bioorg Med Chem Lett 20:1669CrossRefGoogle Scholar
  42. 42.
    Phan-Tan-Luu R, Surzur JM, Metzger J, Aune JP, Dupuy C (1967) Bull Soc Chim Fr 3274Google Scholar
  43. 43.
    Grandberg II, Kost AN (1959) Zh Obshch Khim 29:1099Google Scholar
  44. 44.
    Acheson RM, Foxton MW, Miller GR (1965) J Chem Soc 3200Google Scholar
  45. 45.
    Reid DH, Skelton FS, Bonthrone W (1964) Tetrahedron Lett 1797Google Scholar
  46. 46.
    Zahradnik R, Koutecky J (1961) Collect Czech Chem Commun 26:156CrossRefGoogle Scholar
  47. 47.
    Metzger J, Koether B (1953) Bull Soc Chim Fr 708Google Scholar
  48. 48.
    Florio S, Troisi L, Capriati V (1998) Tetrahedron Lett 39:7951CrossRefGoogle Scholar
  49. 49.
    Schnürch M, Flasik R, Khan AF, Spina M, Mihovilovic MD, Stanetty P (2006) Eur J Org Chem 2006:3283CrossRefGoogle Scholar
  50. 50.
    Schröter S, Stock C, Bach T (2005) Tetrahedron 61:2245CrossRefGoogle Scholar
  51. 51.
    Schnuerch M, Haemmerle J, Mihovilovic MD, Stanetty P (2010) Synthesis 837Google Scholar
  52. 52.
    Grubb AM, Schmidt MJ, Seed AJ, Sampson P (2012) Synthesis 44:1026CrossRefGoogle Scholar
  53. 53.
    Thompson MJ, Chen B (2009) J Org Chem 74:7084CrossRefGoogle Scholar
  54. 54.
    Dömling A (2005) Chem Rev 106:17CrossRefGoogle Scholar
  55. 55.
    Kazmaier U, Persch A (2010) Org Biomol Chem 8:5442CrossRefGoogle Scholar
  56. 56.
    Just-Baringo X, Albericio F, Alvarez M (2014) Curr Top Med Chem 14:1244CrossRefGoogle Scholar
  57. 57.
    Nefzi A, Fenwick JE (2011) Tetrahedron Lett 52:817CrossRefGoogle Scholar
  58. 58.
    Valdomir G, Padrón JI, Padrón JM, Martín VS, Davyt D (2014) Synthesis 46:2451CrossRefGoogle Scholar
  59. 59.
    Maderna A, Doroski M, Subramanyam C, Porte A, Leverett CA, Vetelino BC, Chen Z, Risley H, Parris K, Pandit J, Varghese AH, Shanker S, Song C, Sukuru SCK, Farley KA, Wagenaar MM, Shapiro MJ, Musto S, Lam M-H, Loganzo F, O’Donnell CJ (2014) J Med Chem 57:10527CrossRefGoogle Scholar
  60. 60.
    Pettit GR, Hogan F, Toms S (2011) J Nat Prod 74:962CrossRefGoogle Scholar
  61. 61.
    Boitano S, Flynn AN, Schulz SM, Hoffman J, Price TJ, Vagner J (2011) J Med Chem 54:1308CrossRefGoogle Scholar
  62. 62.
    Hershko A, Heller H, Eytan E, Kaklij G, Rose IA (1984) Proc Natl Acad Sci 81:7021CrossRefGoogle Scholar
  63. 63.
    Hollebeke J, Van Damme P, Gevaert K (2012) N-terminal acetylation and other functions of Nα-acetyltransferases. Biol Chem 393:291CrossRefGoogle Scholar
  64. 64.
    Bolchi C, Pallavicini M, Bernini SK, Chiodini G, Corsini A, Ferri N, Fumagalli L, Straniero V, Valoti E (2011) Bioorg Med Chem Lett 21:5408CrossRefGoogle Scholar
  65. 65.
    Devine SM, Mulcair MD, Debono CO, Leung EWW, Nissink W, Lim SS, Chandrashekaran IR, Vazirani M, Mohanty B, Simpson JS, Baell JB, Scammells PJ, Norton RS, Scanlon MJ (2015) J Med Chem. doi: 10.1021/jm501402x Google Scholar
  66. 66.
    Reid RC, Yau MK, Singh R, Lim JX, Fairlie DP (2014) J Am Chem Soc 136:11914CrossRefGoogle Scholar
  67. 67.
    Mali SM, Schneider TF, Bandyopadhyay A, Jadhav SV, Werz DB, Gopi HN (2012) Cryst Growth Des 12:5643CrossRefGoogle Scholar
  68. 68.
    Davis MR, Singh EK, Wahyudi H, Alexander LD, Kunicki JB, Nazarova LA, Fairweather KA, Giltrap AM, Jolliffe KA, McAlpine SR (2012) Tetrahedron 68:1029CrossRefGoogle Scholar
  69. 69.
    Legrand B, Mathieu L, Lebrun A, Andriamanarivo S, Lisowski V, Masurier N, Zirah S, Kang YK, Martinez J, Maillard LT (2014) Chem Eur J 20:6713CrossRefGoogle Scholar
  70. 70.
    Mathieu L, Legrand B, Deng C, Vezenkov L, Wenger E, Didierjean C, Amblard M, Averlant-Petit M-C, Masurier N, Lisowski V, Martinez J, Maillard LT (2013) Angew Chem Int Ed 52:6006CrossRefGoogle Scholar
  71. 71.
    Blakeney JS, Reid RC, Le GT, Fairlie DP (2007) Chem Rev 107:2960CrossRefGoogle Scholar
  72. 72.
    Loughlin WA, Tyndall JDA, Glenn MP, Hill TA, Fairlie DP (2010) Chem Rev 110(6):PR32CrossRefGoogle Scholar
  73. 73.
    Cohen F, Koehler MFT, Bergeron P, Elliott LO, Flygare JA, Franklin MC, Gazzard L, Keteltas SF, Lau K, Ly CQ, Tsui V, Fairbrother WJ (2010) Bioorg Med Chem Lett 20:2229CrossRefGoogle Scholar
  74. 74.
    Singh S, Prasad NR, Kapoor K, Chufan EE, Patel BA, Ambudkar SV, Talele TT (2014) ChemBioChem 15:157CrossRefGoogle Scholar
  75. 75.
    Dewal MB, Firestine SM (2011) Curr Med Chem 18:2420CrossRefGoogle Scholar
  76. 76.
    Ngoei KRW, Ng DCH, Gooley PR, Fairlie DP, Stoermer MJ, Bogoyevitch MA (2013) Biochim Biophys Acta 1834:1077CrossRefGoogle Scholar
  77. 77.
    Ojika M, Suzuki Y, Tsukamoto A, Sakagami Y, Fudou R, Yoshimura T, Yamanaka S (1998) J Antibiot 51:275CrossRefGoogle Scholar
  78. 78.
    Iwaki Y, Akita H (2007) Chem Pharm Bull (Tokyo) 55:1610CrossRefGoogle Scholar
  79. 79.
    Bertram A, Pattenden G (2007) Nat Prod Rep 24:18CrossRefGoogle Scholar
  80. 80.
    Walsh CT, Malcolmson SJ, Young TS (2011) ACS Chem Biol 7:429CrossRefGoogle Scholar
  81. 81.
    Jin Z (2011) Nat Prod Rep 28:1143CrossRefGoogle Scholar
  82. 82.
    Bowers A, West N, Taunton J, Schreiber SL, Bradner JE, Williams RM (2008) J Am Chem Soc 130:11219CrossRefGoogle Scholar
  83. 83.
    Diness F, Nielsen DS, Fairlie DP (2011) J Org Chem 76:9845CrossRefGoogle Scholar
  84. 84.
    Taori K, Paul VJ, Luesch H (2008) J Am Chem Soc 130:1806CrossRefGoogle Scholar
  85. 85.
    Taori K, Paul VJ, Luesch H (2008) J Am Chem Soc 130:13506CrossRefGoogle Scholar
  86. 86.
    Ying Y, Taori K, Kim H, Hong J, Luesch H (2008) J Am Chem Soc 130:8455CrossRefGoogle Scholar
  87. 87.
    Foster MP, Concepcion GP, Caraan GB, Ireland CM (1992) J Org Chem 57:6671CrossRefGoogle Scholar
  88. 88.
    Bertram A, Maulucci N, New OM, Mohd Nor SM, Pattenden G (2007) Org Biomol Chem 5:1541CrossRefGoogle Scholar
  89. 89.
    Nielsen DS, Hoang HN, Lohman R-J, Hill TA, Lucke AJ, Craik DJ, Edmonds DJ, Griffith DA, Rotter CJ, Ruggeri RB, Price DA, Liras S, Fairlie DP (2014) Angew Chem Int Ed 53:12059CrossRefGoogle Scholar
  90. 90.
    Nielsen DS, Hoang HN, Lohman R-J, Diness F, Fairlie DP (2012) Org Lett 14:5720CrossRefGoogle Scholar
  91. 91.
    Dalisay DS, Rogers EW, Edison AS, Molinski TF (2009) J Nat Prod 72:732CrossRefGoogle Scholar
  92. 92.
    Singh EK, Ramsey DM, McAlpine SR (2012) Org Lett 14:1198CrossRefGoogle Scholar
  93. 93.
    Wahyudi H, Tantisantisom W, McAlpine SR (2014) Tetrahedron Lett 55:2389CrossRefGoogle Scholar
  94. 94.
    Wahyudi H, Tantisantisom W, Liu X, Ramsey DM, Singh EK, McAlpine SR (2012) J Org Chem 77:10596CrossRefGoogle Scholar
  95. 95.
    Matsuo Y, Kanoh K, Yamori T, Kasai H, Katsuta A, Adachi K, Shin-Ya K, Shizuri Y (2007) J Antibiot 60:251CrossRefGoogle Scholar
  96. 96.
    Donia MS, Hathaway BJ, Sudek S, Haygood MG, Rosovitz MJ, Ravel J, Schmidt EW (2006) Nat Chem Biol 2:729CrossRefGoogle Scholar
  97. 97.
    Koehnke J, Bent A, Houssen WE, Zollman D, Morawitz F, Shirran S, Vendome J, Nneoyiegbe AF, Trembleau L, Botting CH, Smith MC, Jaspars M, Naismith JH (2012) Nat Struct Mol Biol 19:767CrossRefGoogle Scholar
  98. 98.
    Koehnke J, Bent AF, Houssen WE, Mann G, Jaspars M, Naismith JH (2014) Curr Opin Struct Biol 29c:112CrossRefGoogle Scholar
  99. 99.
    Comba P, Dovalil N, Gahan LR, Hanson GR, Westphal M (2014) Dalton Trans 43:1935CrossRefGoogle Scholar
  100. 100.
    van den Brenk AL, Tyndall JDA, Cusack RM, Jones A, Fairlie DP, Gahan LR, Hanson GR (2004) J Inorg Biochem 98:1857CrossRefGoogle Scholar
  101. 101.
    van den Brenk AL, Byriel KA, Fairlie DP, Gahan LR, Hanson GR, Hawkins CJ, Jones A, Kennard CHL, Moubaraki B, Murray KS (1994) Inorg Chem 33:3549CrossRefGoogle Scholar
  102. 102.
    Abbenante G, Fairlie DP, Gahan LR, Hanson GR, Pierens GK, van den Brenk AL (1996) J Am Chem Soc 118:10384CrossRefGoogle Scholar
  103. 103.
    Singh Y, Sokolenko N, Kelso MJ, Gahan LR, Abbenante G, Fairlie DP (2000) J Am Chem Soc 123:333CrossRefGoogle Scholar
  104. 104.
    Sokolenko N, Abbenante G, Scanlon MJ, Jones A, Gahan LR, Hanson GR, Fairlie DP (1999) J Am Chem Soc 121:2603CrossRefGoogle Scholar
  105. 105.
    Just-Baringo X, Albericio F, Alvarez M (2014) Mar Drugs 12:317CrossRefGoogle Scholar
  106. 106.
    Ciufolini MA, Lefranc D (2010) Nat Prod Rep 27:330CrossRefGoogle Scholar
  107. 107.
    Heckmann G, Bach T (2005) Angew Chem 117:1223CrossRefGoogle Scholar
  108. 108.
    Trzasko A, Leeds JA, Praestgaard J, Lamarche MJ, McKenney D (2012) Antimicrob Agents Chemother 56:4459CrossRefGoogle Scholar
  109. 109.
    Nicolaou KC, Zak M, Safina BS, Estrada AA, Lee SH, Nevalainen M (2005) J Am Chem Soc 127:11176CrossRefGoogle Scholar
  110. 110.
    Zhang F, Kelly WL (2015) ACS Chem Biol. doi: 10.1021/cb5007745 Google Scholar
  111. 111.
    Haste NM, Thienphrapa W, Tran DN, Loesgen S, Sun P, Nam SJ, Jensen PR, Fenical W, Sakoulas G, Nizet V, Hensler ME (2012) J Antibiot 65:593CrossRefGoogle Scholar
  112. 112.
    Huber RG, Margreiter MA, Fuchs JE, von Grafenstein S, Tautermann CS, Liedl KR, Fox T (2014) J Chem Inf Model 54:1371CrossRefGoogle Scholar
  113. 113.
    Feher M, Schmidt JM (2003) J Chem Inf Comput Sci 43:218CrossRefGoogle Scholar
  114. 114.
    Li JJ (2013) Heterocyclic chemistry in drug discovery. Wiley, HobokenGoogle Scholar
  115. 115.
    Tokarski JS, Newitt JA, Chang CY, Cheng JD, Wittekind M, Kiefer SE, Kish K, Lee FY, Borzillerri R, Lombardo LJ, Xie D, Zhang Y, Klei HE (2006) Cancer Res 66:5790CrossRefGoogle Scholar
  116. 116.
    Getlik M, Grutter C, Simard JR, Kluter S, Rabiller M, Rode HB, Robubi A, Rauh D (2009) J Med Chem 52:3915CrossRefGoogle Scholar
  117. 117.
    Farenc C, Celie PH, Tensen CP, de Esch IJ, Siegal G (2011) FEBS Lett 585:3593CrossRefGoogle Scholar
  118. 118.
    Hynes J Jr, Wu H, Pitt S, Shen DR, Zhang R, Schieven GL, Gillooly KM, Shuster DJ, Taylor TL, Yang X, McIntyre KW, McKinnon M, Zhang H, Marathe PH, Doweyko AM, Kish K, Kiefer SE, Sack JS, Newitt JA, Barrish JC, Dodd J, Leftheris K (2008) Bioorg Med Chem Lett 18:1762CrossRefGoogle Scholar
  119. 119.
    Simard JR, Grutter C, Pawar V, Aust B, Wolf A, Rabiller M, Wulfert S, Robubi A, Kluter S, Ottmann C, Rauh D (2009) J Am Chem Soc 131:18478CrossRefGoogle Scholar
  120. 120.
    Schonbrunn E, Betzi S, Alam R, Martin MP, Becker A, Han H, Francis R, Chakrasali R, Jakkaraj S, Kazi A, Sebti SM, Cubitt CL, Gebhard AW, Hazlehurst LA, Tash JS, Georg GI (2013) J Med Chem 56:3768CrossRefGoogle Scholar
  121. 121.
    St Charles R, Matthews JH, Zhang E, Tulinsky A (1999) J Med Chem 42:1376CrossRefGoogle Scholar
  122. 122.
    Goodwin KD, Lewis MA, Long EC, Georgiadis MM (2008) Proc Natl Acad Sci U S A 105:5052CrossRefGoogle Scholar
  123. 123.
    Williams NK, Lucet IS, Klinken SP, Ingley E, Rossjohn J (2009) J Biol Chem 284:284CrossRefGoogle Scholar
  124. 124.
    Marcotte DJ, Liu YT, Arduini RM, Hession CA, Miatkowski K, Wildes CP, Cullen PF, Hong V, Hopkins BT, Mertsching E, Jenkins TJ, Romanowski MJ, Baker DP, Silvian LF (2010) Protein Sci 19:429Google Scholar
  125. 125.
    Chang YM, Bai L, Liu S, Yang JC, Kung HJ, Evans CP (2008) Oncogene 27:6365CrossRefGoogle Scholar
  126. 126.
    Du J, Bernasconi P, Clauser KR, Mani DR, Finn SP, Beroukhim R, Burns M, Julian B, Peng XP, Hieronymus H, Maglathlin RL, Lewis TA, Liau LM, Nghiemphu P, Mellinghoff IK, Louis DN, Loda M, Carr SA, Kung AL, Golub TR (2009) Nat Biotechnol 27:77CrossRefGoogle Scholar
  127. 127.
    Yeatman TJ (2004) Nat Rev Cancer 4:470CrossRefGoogle Scholar
  128. 128.
    Cheng N, Brantley DM, Chen J (2002) Cytokine Growth Factor Rev 13:75CrossRefGoogle Scholar
  129. 129.
    Pasquale EB (2008) Cell 133:38CrossRefGoogle Scholar
  130. 130.
    Gong J, Morishita A, Kurokohchi K, Tani J, Kato K, Miyoshi H, Inoue H, Kobayashi M, Liu S, Murota M, Muramatsu A, Izuishi K, Suzuki Y, Yoshida H, Uchida N, Deguchi K, Iwama H, Ishimaru I, Masaki T (2010) Int J Oncol 36:101Google Scholar
  131. 131.
    Ashida S, Nakagawa H, Katagiri T, Furihata M, Iiizumi M, Anazawa Y, Tsunoda T, Takata R, Kasahara K, Miki T, Fujioka T, Shuin T, Nakamura Y (2004) Cancer Res 64:5963CrossRefGoogle Scholar
  132. 132.
    van Doorn R, Dijkman R, Vermeer MH, Out-Luiting JJ, van der Raaij-Helmer EM, Willemze R, Tensen CP (2004) Cancer Res 64:5578CrossRefGoogle Scholar
  133. 133.
    Kumar S, Boehm J, Lee JC (2003) Nat Rev Drug Discov 2:717CrossRefGoogle Scholar
  134. 134.
    Choy EH, Panayi GS (2001) N Engl J Med 344:907CrossRefGoogle Scholar
  135. 135.
    Hall M, Peters G (1996) Adv Cancer Res 68:67CrossRefGoogle Scholar
  136. 136.
    Sonar MV, Wampole ME, Jin Y-Y, Chen C-P, Thakur ML, Wickstrom E (2014) Bioconjug Chem 25:1697CrossRefGoogle Scholar
  137. 137.
    Dalvie DK, Kalgutkar AS, Khojasteh-Bakht SC, Obach RS, O’Donnell JP (2002) Chem Res Toxicol 15:269CrossRefGoogle Scholar
  138. 138.
    Mizutani T, Yoshida K, Kawazoe S (1994) Drug Metab Dispos 22:750Google Scholar
  139. 139.
    Mizutani T, Suzuki K (1996) Toxicol Lett 85:101CrossRefGoogle Scholar
  140. 140.
    Kalgutkar AS, Driscoll J, Zhao SX, Walker GS, Shepard RM, Soglia JR, Atherton J, Yu L, Mutlib AE, Munchhof MJ, Reiter LA, Jones CS, Doty JL, Trevena KA, Shaffer CL, Ripp SL (2007) Chem Res Toxicol 20:1954CrossRefGoogle Scholar
  141. 141.
    Blagg J (2010) Structural alerts for toxicity. In: Abraham DJ, Protella DP (eds) Burger’s medicinal chemistry, drug discovery and development, vol 2. Wiley, Hoboken, p 301Google Scholar
  142. 142.
    Barreiro EJ, Kümmerle AE, Fraga CAM (2011) Chem Rev 111:5215CrossRefGoogle Scholar
  143. 143.
    Hobbs DC, Twomey TM (1977) Drug Metab Dispos 5:75Google Scholar
  144. 144.
    Schmid J, Busch U, Trummlitz G, Prox A, Kaschke S, Wachsmuth H (1995) Xenobiotica 25:1219CrossRefGoogle Scholar
  145. 145.
    Obach RS, Kalgutkar AS, Ryder TF, Walker GS (2008) Chem Res Toxicol 21:1890CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Jeffrey Y. W. Mak
    • 1
  • Weijun Xu
    • 1
  • David P. Fairlie
    • 1
  1. 1.Division of Chemistry and Structural Biology, Institute for Molecular BioscienceThe University of QueenslandBrisbaneAustralia

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