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P-gp Inhibitory Activity from Marine Sponges, Tunicates and Algae

  • Xiao-cong Huang
  • Priyank Kumar
  • Nagaraju Anreddy
  • Xue Xiao
  • Dong-Hua Yang
  • Zhe-Sheng Chen
Chapter

Abstract

The only effective therapy for metastasis in cancer patients is chemotherapy, which all too frequently fails due to innate or acquired multi-drug resistance (MDR). Historically, ATP binding cassette (ABC) transporters, such as P-glycoprotein (P-gp), are recognized as the major culprits responsible for MDR. Over-expressing of P-gp in cancer cells, can lead to premature efflux of clinical chemotherapeutic agents and correlate with poor chemotherapeutic outcome and relapse of some cancers. The most likely strategy to overcome MDR is to search for inhibitors from natural products. With unique and novel chemical structures, marine-derived metabolites are an attractive new resource, to prime the search for new P-gp inhibitors. This chapter summarizes P-gp inhibitory activity in marine natural products (MNPs) and validates that MNPs can deliver new ABC transporter inhibitor scaffolds.

Keywords

ABC transporter P-glycoprotein Inhibitor Multidrug resistance Sponges Tunicates Algae Agosterol A Sipholane triterpenoids Lamellarins Parguerenes 

References

  1. 1.
    Morgan G, Ward R, Barton M (2004) Clin Oncol (R Coll Radiol) 16:549Google Scholar
  2. 2.
    Longley DB, Johnston PG (2005) J Pathol 205:275Google Scholar
  3. 3.
    Szakacs G, Paterson JK, Ludwig JA, Booth-Genthe C, Gottesman MM (2006) Nat Rev Drug Discov 5:219Google Scholar
  4. 4.
    Takano M, Otani Y, Tanda M, Kawami M, Nagai J, Yumoto R (2009) Drug Metab Pharmacokinet 24:418Google Scholar
  5. 5.
    Guo W, Healey JH, Meyers PA, Ladanyi M, Huvos AG, Bertino JR, Gorlick R (1999) Clin Cancer Res 5:621Google Scholar
  6. 6.
    Rodrigues AS, Dinis J, Gromicho M, Martins C, Laires A, Rueff J (2012) Curr Pharm Biotechnol 13:651Google Scholar
  7. 7.
    Dano K (1973) Biochim Biophys Acta 323:466Google Scholar
  8. 8.
    Juliano RL, Ling V (1976) Biochim Biophys Acta 455:152Google Scholar
  9. 9.
    Dean M, Rzhetsky A, Allikmets R (2001) Genome Res 11:1156Google Scholar
  10. 10.
    Leslie EM, Deeley RG, Cole SP (2005) Toxicol Appl Pharmacol 204:216Google Scholar
  11. 11.
    Chan HSL, Haddad G, Thorner PS, Deboer G, Lin YP, Ondrusek N, Yeger H, Ling VN (1991) Engl J Med 325:1608Google Scholar
  12. 12.
    Penson RT, Oliva E, Skates SJ, Glyptis T, Fuller AF, Goodman A, Seiden MV (2004) Gynecol Oncol 93:98Google Scholar
  13. 13.
    Steinbach D, Sell W, Voigt A, Hermann J, Zintl F, Sauerbrey A (2002) Leukemia 16:1443Google Scholar
  14. 14.
    George JDG (1979) JJ marine life. Wiley, New YorkGoogle Scholar
  15. 15.
    Barnes RD (1980) Invertebrate zoology. WB Sauders Company, PhiladelphiaGoogle Scholar
  16. 16.
    Faulkner DJ, Ghiselin MT (1983) Mar Ecol Prog Ser 13:295Google Scholar
  17. 17.
    Coll JC, Bowden BF, Tapiolas DM, Willis RH, Djura P, Streamer M, Trott L (1985) Tetrahedron 41:1085Google Scholar
  18. 18.
    Spitaler M, Utz I, Hilbe W, Hofmann J, Grunicke HH (1998) Biochem Pharmacol 56:861Google Scholar
  19. 19.
    Aoki S, Okano M, Matsui K, Itoh T, Satari R, Akiyama S, Kobayashi M (2001) Tetrahedron 57:8951Google Scholar
  20. 20.
    Tanaka J, Trianto A, Musman M, Issa HH, Ohtani II, Ichiba T, Higa T, Yoshida WY, Scheuer PJ (2002) Tetrahedron 58:6259Google Scholar
  21. 21.
    Sarkadi B, Homolya L, Szakacs G, Varadi A (2006) Physiol Rev 86:1179Google Scholar
  22. 22.
    Deeley RG, Westlake C, Cole SPC (2006) Physiol Rev 86:849Google Scholar
  23. 23.
    Seeger MA, van Veen HW (2009) Biochim Biophys Acta Proteins Proteom 1794:725Google Scholar
  24. 24.
    Aller SG, Yu J, Ward A, Weng Y, Chittaboina S, Zhuo R, Harrell PM, Trinh YT, Zhang Q, Urbatsch IL, Chang G (2009) Science 323:1718Google Scholar
  25. 25.
    Gutmann DA, Ward A, Urbatsch IL, Chang G, van Veen HW (2010) Trends Biochem Sci 35:36Google Scholar
  26. 26.
    Bell DR, Gerlach JH, Kartner N, Buick RN, Ling V (1985) J Clin Oncol 3:311Google Scholar
  27. 27.
    Evers R, Zaman GJ, van Deemter L, Jansen H, Calafat J, Oomen LC, Oude Elferink RP, Borst P, Schinkel AH (1996) J Clin Invest 97:1211Google Scholar
  28. 28.
    Germann UA, Willingham MC, Pastan I, Gottesman MM (1990) Biochemistry 29:2295Google Scholar
  29. 29.
    Wu CP, Calcagno AM, Ambudkar SV (2008) Curr Mol Pharmacol 1:93Google Scholar
  30. 30.
    Shukla S, Wu CP, Ambudkar SV (2008) Expert Opin Drug Metab Toxicol 4:205Google Scholar
  31. 31.
    Chan HS, DeBoer G, Thiessen JJ, Budning A, Kingston JE, O’Brien JM, Koren G, Giesbrecht E, Haddad G, Verjee Z, Hungerford JL, Ling V, Gallie BL (1996) Clin Cancer Res 2:1499Google Scholar
  32. 32.
    Gottesman MM (2002) Annu Rev Med 53:615Google Scholar
  33. 33.
    Tsuruo T, Iida H, Tsukagoshi S, Sakurai Y (1981) Cancer Res 41:1967Google Scholar
  34. 34.
    Benson AB, Koeller JM, Trump DC, Egorin M, Olman E, Witte RS, Davis TE, Tormey DC (1984) Proc Am Assoc Canc Res 25:162Google Scholar
  35. 35.
    Dreyfuss M, Harri E, Hofmann H, Kobel H, Pache W, Tscherter H (1976) Eur J Appl Microbiol Biotechnol 3:125Google Scholar
  36. 36.
    Twentyman PR, Fox NE, White DJG (1987) Br J Cancer 56:55Google Scholar
  37. 37.
    Verweij J, Herweijer H, Oosterom R, Vanderburg MEL, Planting AST, Seynaeve C, Stoter G, Nooter K (1991) Br J Cancer 64:361Google Scholar
  38. 38.
    Bartlett NL, Lum BL, Fisher GA, Brophy NA, Ehsan MN, Halsey J, Sikic BI (1994) J Clin Oncol 12:835Google Scholar
  39. 39.
    Twentyman PR (1992) Biochem Pharmacol 43:109Google Scholar
  40. 40.
    Shepard RL, Cao J, Starling JJ, Dantzig AH (2003) Int J Cancer 103:121Google Scholar
  41. 41.
    Martin C, Berridge G, Mistry P, Higgins C, Charlton P, Callaghan R (1999) Br J Pharmacol 128:403Google Scholar
  42. 42.
    Kruijtzer CMF, Beijnen JH, Rosing H, Huinink WWT, Schot M, Jewell RC, Paul EM, Schellens JHM (2002) J Clin Oncol 20:2943Google Scholar
  43. 43.
    Kuppens IE L, M, Witteveen EO, Jewell RC, Radema SA, Paul EM, Mangum SG, Beijnen JH, Voest EE, Schellens JHM (2007) Clin Cancer Res 13:3276Google Scholar
  44. 44.
    Morschhauser F, Zinzani PL, Burgess M, Sloots L, Bouafia F, Dumontet C (2007) Leuk Lymphoma 48:708Google Scholar
  45. 45.
    Szakacs G, Annereau JP, Lababidi S, Shankavaram U, Arciello A, Bussey KJ, Reinhold W, Guo YP, Kruh GD, Reimers M, Weinstein JN, Gottesman MM (2004) Cancer Cell 6:129Google Scholar
  46. 46.
    Ludwig JA, Szakacs G, Martin SE, Chu BF, Cardarelli C, Sauna ZE, Caplen NJ, Fales HM, Ambudkar SV, Weinstein JN, Gottesman MM (2006) Cancer Res 66:4808Google Scholar
  47. 47.
    Wu CP, Shulkla S, Calcagno AM, Hall MD, Gottesman MM, Ambudkar SV (2007) Mol Cancer Ther 6:3287Google Scholar
  48. 48.
    Turk D, Hall MD, Chu BF, Ludwig JA, Fales HM, Gottesman MM, Szakacs G (2009) Cancer Res 96:8293Google Scholar
  49. 49.
    Tsuruo T, Hamada H, Sato S, Heike Y (1989) Jpn J Cancer Res 80:627Google Scholar
  50. 50.
    Watanabe T, Naito M, Kokubu N, Tsuruo TJ (1997) Natl Cancer Inst 89:512Google Scholar
  51. 51.
    Efferth T, Volm M (1993) Oncology 50:303Google Scholar
  52. 52.
    Mamot C, Drummond DC, Hong K, Kirpotin DB, Park JW (2003) Drug Resist Updates 6:271Google Scholar
  53. 53.
    Kanzaki A, Takebayashi Y, Ren XQ, Miyashita H, Mori S, Akiyama S, Pommier Y (2002) Mol Cancer Ther 1:1327Google Scholar
  54. 54.
    Kobayashi H, Takemura Y, Wang FS, Oka T, Ohnuma T (1999) Int J Cancer 81:944Google Scholar
  55. 55.
    Li L, Xu J, Min T, Huang W (2006) Eur J Pharmacol 536:93Google Scholar
  56. 56.
    Crooke ST, Bennett CF (1996) Annu Rev Pharmacol Toxicol 36:107Google Scholar
  57. 57.
    van Vlerken LE, Duan Z, Seiden MV, Amiji MM (2007) Cancer Res 67:4843Google Scholar
  58. 58.
    Komarov PG, Shtil AA, Buckingham LE, Balasubramanian M, Piraner O, Emanuele RM, Roninson IB, Coon JS (1996) Int J Cancer 68:245Google Scholar
  59. 59.
    Wu CP, Ohnuma S, Ambudkar SV (2011) Curr Pharm Biotechnol 12:609Google Scholar
  60. 60.
    Boumendjel A, Di Pietro A, Dumontet C, Barron D (2002) Med Res Rev 22:512Google Scholar
  61. 61.
    Aoki S, Yoshioka Y, Miyamoto Y, Higuchi K, Setiawan A, Murakami N, Chen ZS, Sumizawa T, Akiyama S, Kobayashi M (1998) Tetrahedron Lett 39:6303Google Scholar
  62. 62.
    Aoki S, Chen ZS, Higasiyama K, Setiawan A, Akiyama S, Kobayashi M (2001) Jpn J Cancer Res 92:886Google Scholar
  63. 63.
    Chen ZS, Aoki S, Komatsu M, Ueda K, Sumizawa T, Furukawa T, Okumura H, Ren XQ, Belinsky MG, Lee K, Kruh GD, Kobayashi M, Akiyama S (2001) Int J Cancer 93:107Google Scholar
  64. 64.
    Jain S, Abraham I, Carvalho P, Kuang YH, Shaala LA, Youssef DT, Avery MA, Chen ZS, El Sayed KA J (2009) Nat Prod 72:1291Google Scholar
  65. 65.
    Abraham I, Jain S, Wu CP, Khanfar MA, Kuang Y, Dai CL, Shi Z, Chen X, Fu L, Ambudkar SV, Sayed KE, Chen ZS (2010) Biochem Pharmacol 80:1497Google Scholar
  66. 66.
    Shi Z, Jain S, Kim IW, Peng XX, Abraham I, Youssef DT, Fu LW, El Sayed K, Ambudkar SV, Chen ZS (2007) Cancer Sci 98:1373Google Scholar
  67. 67.
    Kawakami A, Miyamoto T, Higuchi R, Uchiumi T, Kuwano M, Van Soest RWM (2001) Tetrahedron Lett 42:3335Google Scholar
  68. 68.
    Emura C, Higuchi R, Miyamoto T (2006) Tetrahedron 62:5682Google Scholar
  69. 69.
    Aoki S, Cao LW, Matsui K, Rachmat R, Akiyama S, Kobayashi M (2004) Tetrahedron 60:7053Google Scholar
  70. 70.
    White TC, Marr KA, Bowden RA (1998) Clin Microbiol Rev 11:382Google Scholar
  71. 71.
    Sanglard D (2002) Enferm Infecc Microbiol Clin 20:462Google Scholar
  72. 72.
    Jacob MR, Hossain CF, Mohammed KA, Smillie TJ, Clark AM, Walker LA, Nagle DG (2003) J Nat Prod 66:1618Google Scholar
  73. 73.
    Andersen RJF, DJ, He C-H, Duyne GDV, Clardy J (1985) J Am Chem Soc 107:5492Google Scholar
  74. 74.
    Lindquist N, Fenical W, Vanduyne GD, Clardy JJ (1988) Org Chem 53:4570Google Scholar
  75. 75.
    Carroll AR, Bowden BF, Coll JC (1993) Aust J Chem 46:489Google Scholar
  76. 76.
    Urban S, Capon RJ (1996) Aust J Chem 49:711Google Scholar
  77. 77.
    Reddy MVR, Faulkner DJ, Venkateswarlu Y, Rao MR (1997) Tetrahedron 53:3457Google Scholar
  78. 78.
    Davis RA, Carroll AR, Pierens GK, Quinn RJ (1999) J Nat Prod 62:419Google Scholar
  79. 79.
    Reddy MVR, Rao MR, Rhodes D, Hansen MST, Rubins K, Bushman FD, Venkateswarlu Y, Faulkner DJ (1999) J Med Chem 42:1901Google Scholar
  80. 80.
    Urban S, Butler MS, Capon RJ (1994) Aust J Chem 47:1919Google Scholar
  81. 81.
    Urban S, Hobbs L, Hooper JNA, Capon RJ (1995) Aust J Chem 48:1491Google Scholar
  82. 82.
    Fan H, Peng J, Hamann MT, Hu JF (2008) Chem Rev 108:264Google Scholar
  83. 83.
    Cantrell CL, Groweiss A, Gustafson KR, Boyd MR (1999) Nat Prod Lett 14:39Google Scholar
  84. 84.
    Reddy SM, Srinivasulu M, Satyanarayana N, Kondapi AK, Venkateswarlu Y (2005) Tetrahedron 61:9242Google Scholar
  85. 85.
    Chittchang M, Batsomboon P, Ruchirawat S, Ploypradith P (2009) Chem Med Chem 4:457Google Scholar
  86. 86.
    Thipnate P, Chittchang M, Thasana N, Saparpakorn P, Ploypradith P, Hannongbua S (2011) Monatsh Chem 142:97Google Scholar
  87. 87.
    Baunbaek D, Trinkler N, Ferandin Y, Lozach O, Ploypradith P, Rucirawat S, Ishibashi F, Iwao M, Meijer L (2008) Mar Drugs 6:514Google Scholar
  88. 88.
    Carroll AR, Bowden BF, Coll JC (1993) Aust J Chem 46:489Google Scholar
  89. 89.
    Quesada AR, Garcia Gravalos MD, Fernandez Puentes JL (1996) Br J Cancer 74:677Google Scholar
  90. 90.
    Puentes JLF, Garcia Gravalos D, Rodriguez Quesada A (1997) WO patent 1,997,001,336Google Scholar
  91. 91.
    Plisson F, Huang XC, Zhang H, Khalil Z, Capon RJ (2012) Chem Asian J 7:1616Google Scholar
  92. 92.
    Fan H, Peng JN, Hamann MT, Hu JF (2010) Chem Rev 110:3850Google Scholar
  93. 93.
    Ploypradith P, Petchmanee T, Sahakitpichan P, Litvinas ND, Ruchirawat SJ (2006) Org Chem 71:9440Google Scholar
  94. 94.
    Koehnke J, Bent A, Houssen WE, Zollman D, Morawitz F, Shirran S, Vendome J, Nneoyiegbe AF, Trembleau L, Botting CH, Smith MCM, Jaspars M, Naismith JH (2012) Nat Struct Mol Biol 19:767Google Scholar
  95. 95.
    Ireland CM, Durso AR, Newman RA, Hacker MP (1982) J Org Chem 47:1807Google Scholar
  96. 96.
    Schmitz FJ, Ksebati MB, Chang JS, Wang JL, Hossain MB, Vanderhelm D, Engel MH, Serban A, Silfer JA (1989) J Org Chem 54:3463Google Scholar
  97. 97.
    Degnan BM, Hawkins CJ, Lavin MF, McCaffrey EJ, Parry DL, van den Brenk AL, Watters DJ (1989) J Med Chem 32:1349Google Scholar
  98. 98.
    Mcdonald LA, Ireland CM (1992) J Nat Prod 55:376Google Scholar
  99. 99.
    Rashid MA, Gustafson KR, Cardellina JH, Boyd MR (1995) J Nat Prod 58:594Google Scholar
  100. 100.
    Fu X, Do T, Schmitz FJ, Andrusevich V, Engel MH (1998) J Nat Prod 61:1547Google Scholar
  101. 101.
    Williams AB, Jacobs RS (1993) Cancer Lett 71:97Google Scholar
  102. 102.
    Rinehart KL, Holt TG, Fregeau NL, Stroh JG, Keifer PA, Sun F, Li LH, Martin DG (1990) J Org Chem 55:4512Google Scholar
  103. 103.
    Wright AE, Forleo DA, Gunawardana GP, Gunasekera SP, Koehn FE, Mcconnell OJ (1990) J Org Chem 55:4508Google Scholar
  104. 104.
    Carter NJ, Keam SJ (2007) Drugs 67:2257Google Scholar
  105. 105.
    D’Incalci M, Galmarini CM (2010) Mol Cancer Ther 9:2157Google Scholar
  106. 106.
    Carter NJ, Keam SJ (2010) Drugs 70:355Google Scholar
  107. 107.
    Hurley LH, Zewail-Foote M (2001) Adv Exp Med Biol VI 500:289Google Scholar
  108. 108.
    Bonfanti M, La Valle E, Faro JM F, S, Faircloth G, Caretti G, Mantovani R, D’Incalci M (1999) Anti-Cancer Drug Des 14:179Google Scholar
  109. 109.
    Kanzaki A, Takebayashi Y, Ren XQ, Miyashita H, Mori S, Akiyama S, Pommier Y (2002) Mol Cancer Ther 1:1327Google Scholar
  110. 110.
    Schmitz FJ, Michaud DP, Schmidt PG (1982) J Am Chem Soc 104:6415Google Scholar
  111. 111.
    Suzuki T, Takeda S, Hayama N, Tanaka I, Komiyama K (1989) Chem Lett 10:969Google Scholar
  112. 112.
    Tsukamoto S, Yamashita Y, Yoshida T, Ohta T (2004) Mar Drugs 2:170Google Scholar
  113. 113.
    Ioannou E, Nappo M, Avila C, Vagias C, Roussis VJ (2009) Nat Prod 72:1716Google Scholar
  114. 114.
    Higgs MD, Faulkner DJ (1982) Phytochemistry 21:789Google Scholar
  115. 115.
    Takeda S, Kurosawa E, Komiyama K, Suzuki T (1990) Bull Chem Soc Jpn 63:3066Google Scholar
  116. 116.
    Rochfort SJ, Capon RJ (1996) Aust J Chem 49:19Google Scholar
  117. 117.
    Kurata K, Taniguchi K, Agatsuma Y, Suzuki M (1998) Phytochemistry 47:363Google Scholar
  118. 118.
    Lyakhova EG, Kalinovsky AI, Kolesnikova SA, Vaskovsky VE, Stonik VA (2004) Phytochemistry 65:2527Google Scholar
  119. 119.
    Awad NE (2004) Phytother Res 18:275Google Scholar
  120. 120.
    Huang XC, Sun YL, Salim AA, Chen ZS, Capon RJ (2013) Biochem Pharmacol 85:1257Google Scholar
  121. 121.
    Stratmann K, Moore RE, Bonjouklian R, Deeter JB, Patterson GML, Shaffer S, Smith CD, Smitka TA (1994) J Am Chem Soc 116:9935Google Scholar
  122. 122.
    Smith CD, Zilfou JT, Stratmann K, Patterson GML, Moore RE (1995) Mol Pharmacol 47:241Google Scholar
  123. 123.
    Fairchild CR, Ivy SP, Kaoshan CS, Whangpeng J, Rosen N, Israel MA, Melera PW, Cowan KH, Goldsmith ME (1987) Cancer Res 47:5141Google Scholar
  124. 124.
    Zhang XQ, Smith CD (1996) Mol Pharmacol 49:288Google Scholar
  125. 125.
    Stratmann K, Burgoyne DL, Moore RE, Patterson GML, Smith CD (1994) J Org Chem 59:7219Google Scholar
  126. 126.
    Okuno T, Ohmori K, Nishiyama S, Yamamura S, Nakamura K, Houk KN, Okamoto K (1996) Tetrahedron 52:14723Google Scholar
  127. 127.
    Ohmori K, Okuno T, Nishiyama S, Yamamura S (1996) Tetrahedron Lett 37:3467Google Scholar
  128. 128.
    Kashihara N, To-e S, Nakamura K, Umezawa K, Yamamura S, Nishiyama S (2000) Bioorg Med Chem Lett 10:101Google Scholar
  129. 129.
    Wagner B, Gonzalez GI, Dau METH, Zhu JP (1999) Bioorg Med Chem 7:737Google Scholar
  130. 130.
    O’connell CE, Salvato KA, Meng ZY, Littlefield BA, Schwartz CE (1999) Bioorg Med Chem Lett 9:1541Google Scholar
  131. 131.
    Dinh TQ, Du XH, Smith CD, Armstrong RW (1997) J Org Chem 62:6773Google Scholar
  132. 132.
    Dinh TQ, Smith CD, Du XH, Armstrong RW (1998) J Med Chem 41:981Google Scholar
  133. 133.
    Prinsep MR, Caplan FR, Moore RE, Patterson GML, Smith CD (1992) J Am Chem Soc 114:385Google Scholar
  134. 134.
    Smith CD, Prinsep MR, Caplan FR, Moore RE, Patterson GML (1994) Oncol Res 6:211Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Xiao-cong Huang
    • 1
  • Priyank Kumar
    • 2
  • Nagaraju Anreddy
    • 2
  • Xue Xiao
    • 1
  • Dong-Hua Yang
    • 3
  • Zhe-Sheng Chen
    • 2
  1. 1.Division of Chemistry and Structural Biology, Institute for Molecular BioscienceThe University of QueenslandBrisbaneAustralia
  2. 2.Department of Pharmaceutical Sciences, College of Pharmacy and Health SciencesSt. John’s UniversityNew YorkUSA
  3. 3.Biosample Repository FacilityFox Chase Cancer CenterPhiladelphiaUSA

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