About this Journal Submit a Manuscript Table of Contents
Advances in Pharmacological Sciences
Volume 2010 (2010), Article ID 587306, 13 pages
http://dx.doi.org/10.1155/2010/587306
Review Article

Key Role of Human ABC Transporter ABCG2 in Photodynamic Therapy and Photodynamic Diagnosis

1Omics Science Center, RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku, Yokohama 230-0045, Japan
2Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
3Department of Neurosurgery, Osaka Medical College, Osaka 569-8686, Japan

Received 8 November 2009; Accepted 9 May 2010

Academic Editor: Ryan F. Donnelly

Copyright © 2010 Toshihisa Ishikawa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. L. Lipson and E. J. Baldes, “The photodynamic properties of a particular hematoporphyrin derivative,” Archives of Dermatology, vol. 82, pp. 508–516, 1960.
  2. R. L. Lipson, E. J. Baldes, and A. M. Olsen, “Hematoporphyrin derivative: a new aid for endoscopic detection of malignant disease,” The Journal of Thoracic and Cardiovascular Surgery, vol. 42, pp. 623–629, 1961.
  3. R. L. Lipson, E. J. Baldes, and A. M. Olsen, “Further evaluation of the use of hematoporphyrin derivative as a new aid for the endoscopic detection of malignant disease,” Diseases of the Chest, vol. 46, pp. 676–679, 1964.
  4. R. L. Lipson, E. J. Baldes, and M. J. Gray, “Hematoporphyrin derivative for detection and management of cancer,” Cancer, vol. 20, no. 12, pp. 2255–2257, 1967.
  5. M. J. Gray, R. Lipson, J. V. Maeck, L. Parker, and D. Romeyn, “Use of hematoporphyrin derivative in detection and management of cervical cancer. A preliminary report,” American Journal of Obstetrics and Gynecology, vol. 99, no. 6, pp. 766–771, 1967.
  6. D. R. Sanderson, R. S. Fontana, R. L. Lipson, and E. J. Baldes, “Hematoporphyrin as a diagnostic tool. A preliminary report of new techniques,” Cancer, vol. 30, no. 5, pp. 1368–1372, 1972.
  7. D. E. J. G. J. Dolmans, D. Fukumura, and R. K. Jain, “Photodynamic therapy for cancer,” Nature Reviews Cancer, vol. 3, no. 5, pp. 380–387, 2003. View at Publisher · View at Google Scholar · View at PubMed
  8. T. J. Dougherty, J. E. Kaufman, A. Goldfarb, KR Weishaupt, D. Boyle, and A. Mittleman, “Photoradiation therapy for the treatment of malignant tumors,” Cancer Research, vol. 38, no. 8, pp. 2628–2635, 1978.
  9. W. Stummer, A. Novotny, H. Stepp, C. Goetz, K. Bise, and H. J. Reulen, “Fluorescence-guided resection of glioblastoma multiforme by using 5-aminolevulinic acid-induced porphyrins: a prospective study in 52 consecutive patients,” Journal of Neurosurgery, vol. 93, no. 6, pp. 1003–1013, 2000.
  10. F. W. Floeth and W. Stummer, “The value of metabolic imaging in diagnosis and resection of cerebral gliomas,” Naure Cliical Practice Neurology, vol. 1, no. 2, pp. 62–63, 2005.
  11. J. Shinoda, H. Yano, S.-I. Yoshimura, A. Okumura, Y. Kaku, T. Iwama, and N. Sakai, “Fluorescence-guided resection of glioblastoma multiforme by using high-dose fluorescein sodium. Technical note,” Journal of Neurosurgery, vol. 99, no. 3, pp. 597–603, 2003.
  12. Y. Kajimoto, T. Kuroiwa, S.-I. Miyatake, T. Ichioka, M. Miyashita, H. Tanaka, and M. Tsuji, “Use of 5-aminolevulinic acid in fluorescence-guided resection of meningioma with high risk of recurrence. Case report,” Journal of Neurosurgery, vol. 106, no. 6, pp. 1070–1074, 2007. View at Publisher · View at Google Scholar · View at PubMed
  13. M. Lacroix, D. Abi-Said, and D. Abi-Said, “A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival,” Journal of Neurosurgery, vol. 95, no. 2, pp. 190–198, 2001.
  14. S. J. Hentschel and R. Sawaya, “Optimizing outcomes with maximal surgical resection of malignant gliomas,” Cancer Control, vol. 10, no. 2, pp. 109–114, 2003.
  15. W. Stummer, U. Pichlmeier, T. Meinel, O. D. Wiestler, F. Zanella, and H.-J. Reulen, “Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial,” The Lancet Oncology, vol. 7, no. 5, pp. 392–401, 2006. View at Publisher · View at Google Scholar · View at PubMed
  16. W. Stummer, H. J. Reulen, A. Novotny, H. Stepp, and J. C. Tonn, “Fluorescence-guided resections of malignant gliomas—an overview,” Acta Neurochirurgica. Supplement, vol. 88, pp. 9–12, 2003.
  17. G. O. Latunde-Dada, R. J. Simpson, and A. T. McKie, “Recent advances in mammalian haem transport,” Trends in Biochemical Sciences, vol. 31, no. 3, pp. 182–188, 2006. View at Publisher · View at Google Scholar · View at PubMed
  18. A. S. Tsiftsoglou, A. I. Tsamadou, and L. C. Papadopoulou, “Heme as key regulator of major mammalian cellular functions: molecular, cellular, and pharmacological aspects,” Pharmacology and Therapeutics, vol. 111, no. 2, pp. 327–345, 2006. View at Publisher · View at Google Scholar · View at PubMed
  19. P. Krishnamurthy, T. Xie, and J. D. Schuetz, “The role of transporters in cellular heme and porphyrin homeostasis,” Pharmacology and Therapeutics, vol. 114, no. 3, pp. 345–358, 2007. View at Publisher · View at Google Scholar · View at PubMed
  20. K. Wakabayashi, A. Tamura, H. Saito, Y. Onishi, and T. Ishikawa, “Human ABC transporter ABCG2 in xenobiotic protection and redox biology,” Drug Metabolism Reviews, vol. 38, no. 3, pp. 371–391, 2006. View at Publisher · View at Google Scholar · View at PubMed
  21. R. Dubakiene and M. Kupriene, “Scientific problems of photosensitivity,” Medicina, vol. 42, no. 8, pp. 619–624, 2006.
  22. J. T. Hindmarsh, “The porphyrias, appropriate test selection,” Clinica Chimica Acta, vol. 333, no. 2, pp. 203–207, 2003. View at Publisher · View at Google Scholar
  23. R. A. Norman, “Past and future: porphyria and porphyrins,” Skinmed, vol. 4, no. 5, pp. 287–292, 2005.
  24. J. C. Kennedy and R. H. Pottier, “Endogenous protoporphyrin IX, a clinically useful photosensitizer for photodynamic therapy,” Journal of Photochemistry and Photobiology B, vol. 14, no. 4, pp. 275–292, 1992. View at Publisher · View at Google Scholar
  25. H. Schneckenburger, K. König, K. Kunzi-Rapp, C. Westphal-Frösch, and A. Rück, “Time-resolved in-vivo fluorescence of photosensitizing porphyrins,” Journal of Photochemistry and Photobiology B, vol. 21, no. 2-3, pp. 143–147, 1993. View at Publisher · View at Google Scholar
  26. K. R. Weishaupt, C. J. Gomer, and T. J. Dougherty, “Identification of singlet oxygen as the cytotoxic agent in photo inactivation of a murine tumor,” Cancer Research, vol. 36, no. 7, pp. 2326–2329, 1976.
  27. R. Pottier and T. G. Truscott, “The photochemistry of haematoporphyrin and related systems,” International Journal of Radiation Biology, vol. 50, no. 3, pp. 421–452, 1986.
  28. C. S. Loh, D. Vernon, A. J. MacRobert, J. Bedwell, S. G. Bown, and S. B. Brown, “Endogenous porphyrin distribution induced by 5-aminolaevulinic acid in the tissue layers of the gastrointestinal tract,” Journal of Photochemistry and Photobiology B, vol. 20, no. 1, pp. 47–54, 1993. View at Publisher · View at Google Scholar
  29. F. Iwasa, S. Sassa, and A. Kappas, “δ-Aminolaevulinate synthase in human HepG2 hepatoma cells. Repression by haemin and induction by chemicals,” Biochemical Journal, vol. 262, no. 3, pp. 807–813, 1989.
  30. L. A. Doyle, W. Yang, L. V. Abruzzo, T. Krogmann, Y. Gao, A. K. Rishi, and D. D. Ross, “A multidrug resistance transporter from human MCF-7 breast cancer cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 26, pp. 15665–15670, 1998.
  31. R. Allikmets, L. M. Schriml, A. Hutchinson, V. Romano-Spica, and M. Dean, “A human placenta-specific ATP-binding cassette gene (ABCP) on chromosome 4q22 that is involved in multidrug resistance,” Cancer Research, vol. 58, no. 23, pp. 5337–5339, 1998.
  32. K. Miyake, L. Mickley, and L. Mickley, “Molecular cloning of cDNAs which are highly overexpressed in mitoxantrone-resistant cells: demonstration of homology to ABC transport genes,” Cancer Research, vol. 59, no. 1, pp. 8–13, 1999.
  33. K. Wakabayashi, H. Nakagawa, T. Adachi, I. K II, E. Kobatake, A. Kudo, and T. Ishikawa, “Identification of cysteine residues critically involved in homodimer formation and protein expression of human ATP-binding cassette transporter ABCG2: a new approach using the Flp recombinase system,” Journal of Experimental Therapeutics and Oncology, vol. 5, no. 3, pp. 205–222, 2006.
  34. K. Wakabayashi, H. Nakagawa, A. Tamura, S. Koshiba, K. Hoshijima, M. Komada, and T. Ishikawa, “Intramolecular disulfide bond is a critical check point determining degradative fates of ATP-binding cassette (ABC) transporter ABCG2 protein,” Journal of Biological Chemistry, vol. 282, no. 38, pp. 27841–27846, 2007. View at Publisher · View at Google Scholar · View at PubMed
  35. K. Wakabayashi-Nakao, A. Tamura, T. Furukawa, H. Nakagawa, and T. Ishikawa, “Quality control of human ABCG2 protein in the endoplasmic reticulum: ubiquitination and proteasomal degradation,” Advanced Drug Delivery Reviews, vol. 61, no. 1, pp. 66–72, 2009. View at Publisher · View at Google Scholar · View at PubMed
  36. H. Nakagawa, K. Wakabayashi-Nakao, A. Tamura, Y. Toyoda, S. Koshiba, and T. Ishikawa, “Disruption of N-linked glycosylation enhances ubiquitin-mediated proteasomal degradation of the human ATP-binding cassette transporter ABCG2,” FEBS Journal, vol. 276, no. 24, pp. 7237–7252, 2009. View at Publisher · View at Google Scholar · View at PubMed
  37. T. Ishikawa and H. Nakagawa, “Human ABC transporter ABCG2 in cancer chemotherapy and pharmacogenomics,” Journal of Experimental Therapeutics and Oncology, vol. 8, no. 1, pp. 5–24, 2009.
  38. J. D. Allen and A. H. Schinkel, “Multidrug resistance and pharmacological protection mediated by the breast cancer resistance protein (BCRP/ABCG2),” Molecular Cancer Therapeutics, vol. 1, no. 6, pp. 427–434, 2002.
  39. C. F. Stewart, M. Leggas, and M. Leggas, “Gefitinib enhances the antitumor activity and oral bioavailability of irinotecan in mice,” Cancer Research, vol. 64, no. 20, pp. 7491–7499, 2004. View at Publisher · View at Google Scholar · View at PubMed
  40. J. W. Jonker, M. Buitelaar, and M. Buitelaar, “The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 24, pp. 15649–15654, 2002. View at Publisher · View at Google Scholar · View at PubMed
  41. A. Tamura, M. Watanabe, H. Saito, H. Nakagawa, T. Kamachi, I. Okura, and T. Ishikawa, “Functional validation of the genetic polymorphisms of human ATP-binding cassette (ABC) transporter ABCG2: identification of alleles that are defective in porphyrin transport,” Molecular Pharmacology, vol. 70, no. 1, pp. 287–296, 2006. View at Publisher · View at Google Scholar · View at PubMed
  42. A. Tamura, Y. Onishi, and Y. Onishi, “In vitro evaluation of photosensitivity risk related to genetic polymorphisms of human ABC transporter ABCG2 and inhibition by drugs,” Drug Metabolism and Pharmacokinetics, vol. 22, no. 6, pp. 428–440, 2007. View at Publisher · View at Google Scholar
  43. R. An, Y. Hagiya, A. Tamura, S. Li, H. Saito, D. Tokushima, and T. Ishikawa, “Cellular phototoxicity evoked through the inhibition of human ABC transporter ABCG2 by cyclin-dependent kinase inhibitors in vitro,” Pharmaceutical Research, vol. 26, no. 2, pp. 449–458, 2009. View at Publisher · View at Google Scholar · View at PubMed
  44. Y. Hagiya, T. Adachi, and T. Adachi, “Nrf2-dependent induction of human ABC transporter ABCG2 and heme oxygenase-1 in HepG2 cells by photoactivation of porphyrins: biochemical implications for cancer cell response to photodynamic therapy,” Journal of Experimental Therapeutics and Oncology, vol. 7, no. 2, pp. 153–167, 2008.
  45. T. Nguyen, P. J. Sherratt, P. Nioi, C. S. Yang, and C. B. Pickett, “Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1,” Journal of Biological Chemistry, vol. 280, no. 37, pp. 32485–32492, 2005. View at Publisher · View at Google Scholar · View at PubMed
  46. H. Motohashi and M. Yamamoto, “Nrf2-Keap1 defines a physiologically important stress response mechanism,” Trends in Molecular Medicine, vol. 10, no. 11, pp. 549–557, 2004. View at Publisher · View at Google Scholar · View at PubMed
  47. M. Kobayashi and M. Yamamoto, “Nrf2-Keap1 regulation of cellular defense mechanisms against electrophiles and reactive oxygen species,” Advances in Enzyme Regulation, vol. 46, no. 1, pp. 113–140, 2006. View at Publisher · View at Google Scholar · View at PubMed
  48. T. Adachi, H. Nakagawa, and H. Nakagawa, “Nrf2-dependent and -independent induction of ABC transporters ABCC1, ABCC2, and ABCG2 in HepG2 cells under oxidative stress,” Journal of Experimental Therapeutics and Oncology, vol. 6, no. 4, pp. 335–348, 2007.
  49. T. Yamamoto, T. Suzuki, A. Kobayashi, J. Wakabayashi, J. Maher, H. Motohashi, and M. Yamamoto, “Physiological significance of reactive cysteine residues of Keap1 in determining Nrf2 activity,” Molecular and Cellular Biology, vol. 28, no. 8, pp. 2758–2770, 2008. View at Publisher · View at Google Scholar · View at PubMed
  50. D. Martin, A. I. Rojo, and A. I. Rojo, “Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3-kinase/akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol,” Journal of Biological Chemistry, vol. 279, no. 10, pp. 8919–8929, 2004. View at Publisher · View at Google Scholar · View at PubMed
  51. S. Kocanova, E. Buytaert, J.-Y. Matroule, J. Piette, J. Golab, P. De Witte, and P. Agostinis, “Induction of heme-oxygenase 1 requires the p38MAPK and PI3K pathways and suppresses apoptotic cell death following hypericin-mediated photodynamic therapy,” Apoptosis, vol. 12, no. 4, pp. 731–741, 2007. View at Publisher · View at Google Scholar · View at PubMed
  52. C. K. Andreadi, L. M. Howells, P. A. Atherfold, and M. M. Manson, “Involvement of Nrf2, p38, B-Raf, and nuclear factor-κB, but not phosphatidylinositol 3-kinase, in induction of hemeoxygenase-1 by dietary polyphenols,” Molecular Pharmacology, vol. 69, no. 3, pp. 1033–1040, 2006.
  53. D. A. Bloom and A. K. Jaiswal, “Phosphorylation of Nrf2 at Ser40 by protein kinase C in response to antioxidants leads to the release of Nrf2 from INrf2, but is not required for Nrf2 stabilization/accumulation in the nucleus and transcriptional activation of antioxidant response element-mediated NAD(P)H:quinone oxidoreductase-1 gene expression,” Journal of Biological Chemistry, vol. 278, no. 45, pp. 44675–44682, 2003. View at Publisher · View at Google Scholar · View at PubMed
  54. S. B. Cullinan, D. Zhang, M. Hannink, E. Arvisais, R. J. Kaufman, and J. A. Diehl, “Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival,” Molecular and Cellular Biology, vol. 23, no. 20, pp. 7198–7209, 2003. View at Publisher · View at Google Scholar
  55. S. B. Cullinan and J. A. Diehl, “PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress,” Journal of Biological Chemistry, vol. 279, no. 19, pp. 20108–20117, 2004. View at Publisher · View at Google Scholar · View at PubMed
  56. K. A. Kang, K. H. Lee, and K. H. Lee, “Triphlorethol-A induces heme oxygenase-1 via activation of ERK and NF-E2 related factor 2 transcription factor,” FEBS Letters, vol. 581, no. 10, pp. 2000–2008, 2007. View at Publisher · View at Google Scholar · View at PubMed
  57. K. W. Kang, S. J. Lee, J. W. Park, and S. G. Kim, “Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress,” Molecular Pharmacology, vol. 62, no. 5, pp. 1001–1010, 2002. View at Publisher · View at Google Scholar
  58. K. Igarashi and J. Sun, “The heme-Bach1 pathway in the regulation of oxidative stress response and erythroid differentiation,” Antioxidants and Redox Signaling, vol. 8, no. 1-2, pp. 107–118, 2006. View at Publisher · View at Google Scholar · View at PubMed
  59. T. Oyake, K. Itoh, and K. Itoh, “Bach proteins belong to a novel family of BTB-basic leucine zipper transcription factors that interact with MafK and regulate transcription through the NF-E2 site,” Molecular and Cellular Biology, vol. 16, no. 11, pp. 6083–6095, 1996.
  60. J. Sun, H. Hoshino, and H. Hoshino, “Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene,” The EMBO Journal, vol. 21, no. 19, pp. 5216–5224, 2002. View at Publisher · View at Google Scholar
  61. J. Sun, M. Brand, Y. Zenke, S. Tashiro, M. Groudine, and K. Igarashi, “Heme regulates the dynamic exchange of Bach1 and NF-E2-related factors in the Maf transcription factor network,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 6, pp. 1461–1466, 2004. View at Publisher · View at Google Scholar · View at PubMed
  62. K. J. Hintze, Y. Katoh, K. Igarashi, and E. C. Theil, “Bach1 repression of ferritin and thioredoxin reductase1 is heme-sensitive in cells and in vitro and coordinates expression with heme oxygenase1, β-globin, and NADP(H) quinone (Oxido) reductase1,” Journal of Biological Chemistry, vol. 282, no. 47, pp. 34365–34371, 2007. View at Publisher · View at Google Scholar · View at PubMed
  63. T. Kitamuro, K. Takahashi, and K. Takahashi, “Bach1 functions as a hypoxia-inducible repressor for the heme oxygenase-1 gene in human cells,” Journal of Biological Chemistry, vol. 278, no. 11, pp. 9125–9133, 2003. View at Publisher · View at Google Scholar · View at PubMed
  64. Y. Shan, R. W. Lambrecht, T. Ghaziani, S. E. Donohue, and H. L. Bonkovsky, “Role of Bach-1 in regulation of heme oxygenase-1 in human liver cells: insights from studies with small interfering RNAs,” Journal of Biological Chemistry, vol. 279, no. 50, pp. 51769–51774, 2004. View at Publisher · View at Google Scholar · View at PubMed
  65. Y. Shan, R. W. Lambrecht, S. E. Donohue, and H. L. Bonkovsky, “Role of Bach1 and Nrf2 in up-regulation of the heme oxygenase-1 gene by cobalt protoporphyrin,” The FASEB Journal, vol. 20, no. 14, pp. 2651–2653, 2006. View at Publisher · View at Google Scholar · View at PubMed
  66. K. Ogawa, J. Sun, and J. Sun, “Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1,” The EMBO Journal, vol. 20, no. 11, pp. 2835–2843, 2001. View at Publisher · View at Google Scholar · View at PubMed
  67. H. Suzuki, S. Tashiro, and S. Tashiro, “Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1,” The EMBO Journal, vol. 23, no. 13, pp. 2544–2553, 2004. View at Publisher · View at Google Scholar · View at PubMed
  68. Y. Zenke-Kawasaki, Y. Dohi, and Y. Dohi, “Heme induces ubiquitination and degradation of the transcription factor Bach1,” Molecular and Cellular Biology, vol. 27, no. 19, pp. 6962–6971, 2007. View at Publisher · View at Google Scholar · View at PubMed
  69. J. F. Reichard, G. T. Motz, and A. Puga, “Heme oxygenase-1 induction by NRF2 requires inactivation of the transcriptional repressor BACH1,” Nucleic Acids Research, vol. 35, no. 21, pp. 7074–7086, 2007. View at Publisher · View at Google Scholar · View at PubMed
  70. A. Jozkowicz, H. Was, and J. Dulak, “Heme oxygenase-1 in tumors: is it a false friend?” Antioxidants and Redox Signaling, vol. 9, no. 12, pp. 2099–2117, 2007. View at Publisher · View at Google Scholar · View at PubMed
  71. C. J. Gomer, M. Luna, A. Ferrario, and N. Rucker, “Increased transcription and translation of heme oxygenase in Chinese hamster fibroblasts following photodynamic stress or Photofrin II incubation,” Photochemistry and Photobiology, vol. 53, no. 2, pp. 275–279, 1991.
  72. D. Nowis, M. Legat, and M. Legat, “Heme oxygenase-1 protects tumor cells against photodynamic therapy-mediated cytotoxicity,” Oncogene, vol. 25, no. 24, pp. 3365–3374, 2006. View at Publisher · View at Google Scholar · View at PubMed
  73. F. A. de Jong, M. J. A. de Jonge, J. Verweij, and R. H. J. Mathijssen, “Role of pharmacogenetics in irinotecan therapy,” Cancer Letters, vol. 234, no. 1, pp. 90–106, 2006. View at Publisher · View at Google Scholar · View at PubMed
  74. T. Ishikawa, A. Tamura, H. Saito, K. Wakabayashi, and H. Nakagawa, “Pharmacogenomics of the human ABC transporter ABCG2: from functional evaluation to drug molecular design,” Naturwissenschaften, vol. 92, no. 10, pp. 451–463, 2005. View at Publisher · View at Google Scholar · View at PubMed
  75. G. Bäckström, J. Taipalensuu, H. Melhus, H. Brändström, A.-C. Svensson, P. Artursson, and A. Kindmark, “Genetic variation in the ATP-binding cassette transporter gene ABCG2 (BCRP) in a Swedish population,” European Journal of Pharmaceutical Sciences, vol. 18, no. 5, pp. 359–364, 2003. View at Publisher · View at Google Scholar
  76. T. M. Bosch, L. M. Kjellberg, and L. M. Kjellberg, “Detection of single nucleotide polymorphisms in the ABCG2 gene in a Dutch population,” American Journal of PharmacoGenomics, vol. 5, no. 2, pp. 123–131, 2005. View at Publisher · View at Google Scholar
  77. F. A. de Jong, S. Marsh, R. H. J. Mathijssen, C. King, J. Verweij, A. Sparreboom, and H. L. McLeod, “ABCG2 pharmacogenetics: ethnic differences in allele frequency and assessment of influence on irinotecan disposition,” Clinical Cancer Research, vol. 10, no. 17, pp. 5889–5894, 2004. View at Publisher · View at Google Scholar · View at PubMed
  78. A. Tamura, K. Wakabayashi, and K. Wakabayashi, “Re-evaluation and functional classification of non-synonymous single nucleotide polymorphisms of the human ATP-binding cassette transporter ABCG2,” Cancer Science, vol. 98, no. 2, pp. 231–239, 2007. View at Publisher · View at Google Scholar
  79. Y. Imai, M. Nakane, and M. Nakane, “C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance,” Molecular Cancer Therapeutics, vol. 1, no. 8, pp. 611–616, 2002.
  80. D. Kobayashi, I. Ieiri, and I. Ieiri, “Functional assessment of ABCG2 (BRCP) gene polymorphisms to protein expression in human placenta,” Drug Metabolism and Disposition, vol. 33, no. 1, pp. 94–101, 2005. View at Publisher · View at Google Scholar · View at PubMed
  81. S. Mizuarai, N. Aozasa, and H. Kotani, “Single nucleotide polymorphisms result in impaired membrane localization and reduced atpase activity in multidrug transporter ABCG2,” International Journal of Cancer, vol. 109, no. 2, pp. 238–246, 2004. View at Publisher · View at Google Scholar · View at PubMed
  82. C. P. Zamber, J. K. Lamba, K. Yasuda, J. Farnum, K. Thummel, J. D. Schuetz, and E. G. Schuetz, “Natural allelic variants of breast cancer resistance protein (BCRP) and their relationship to BCRP expression in human intestine,” Pharmacogenetics, vol. 13, no. 1, pp. 19–28, 2003. View at Publisher · View at Google Scholar
  83. K. Morisaki, R. W. Robey, and R. W. Robey, “Single nucleotide polymorphisms modify the transporter activity of ABCG2,” Cancer Chemotherapy and Pharmacology, vol. 56, no. 2, pp. 161–172, 2005. View at Publisher · View at Google Scholar · View at PubMed
  84. C. Kondo, H. Suzuki, and H. Suzuki, “Functional analysis of SNPs variants of BCRP/ABCG2,” Pharmaceutical Research, vol. 21, no. 10, pp. 1895–1903, 2004. View at Publisher · View at Google Scholar
  85. J. Li, G. Cusatis, and G. Cusatis, “Association of variant ABCG2 and the pharmacokinetics of epidermal growth factor receptor tyrosine kinase inhibitors in cancer patients,” Cancer Biology and Therapy, vol. 6, no. 3, pp. 432–438, 2007.
  86. A. Sparreboom, H. Gelderblom, and H. Gelderblom, “Diflomotecan pharmacokinetics in relation to ABCG2 421C>A genotype,” Clinical Pharmacology and Therapeutics, vol. 76, no. 1, pp. 38–44, 2004. View at Publisher · View at Google Scholar · View at PubMed
  87. A. Sparreboom, W. J. Loos, and W. J. Loos, “Effect of ABCG2 genotype on the oral bioavailability of topotecan,” Cancer Biology & Therapy, vol. 4, no. 6, pp. 650–658, 2005.
  88. G. Cusatis, V. Gregorc, and V. Gregorc, “Pharmacogenetics of ABCG2 and adverse reactions to gefitinib,” Journal of the National Cancer Institute, vol. 98, no. 23, pp. 1739–1742, 2006. View at Publisher · View at Google Scholar · View at PubMed
  89. T. Furukawa, K. Wakabayashi, A. Tamura, H. Nakagawa, Y. Morishima, Y. Osawa, and T. Ishikawa, “Major SNP (Q141K) variant of human ABC transporter ABCG2 undergoes lysosomal and proteasomal degradations,” Pharmaceutical Research, vol. 26, no. 2, pp. 469–479, 2009. View at Publisher · View at Google Scholar · View at PubMed
  90. T. Ishikawa, A. Sakurai, Y. Kanamori, et al., “High-speed screening of human ATP-binding cassette transporter function and genetic polymorphisms: new strategies in pharmacogenomics,” Methods in Enzymology, vol. 400, pp. 485–510, 2005. View at Publisher · View at Google Scholar · View at PubMed
  91. M. E. M. Noble, J. A. Endicott, and L. N. Johnson, “Protein kinase inhibitors: insights into drug design from structure,” Science, vol. 303, no. 5665, pp. 1800–1805, 2004. View at Publisher · View at Google Scholar · View at PubMed
  92. J. Dancey and E. A. Sausville, “Issues and progress with protein kinase inhibitors for cancer treatment,” Nature Reviews Drug Discovery, vol. 2, no. 4, pp. 296–313, 2003.
  93. P. Nurse, “Nobel Lecture. Cyclin dependent kinases and cell cycle control,” ChemBioChem, vol. 22, no. 5-6, pp. 487–499, 2002.
  94. P. L. Porter, K. E. Malone, and K. E. Malone, “Expression of cell-cycle regulators p27(Kip1) and cyclin E, alone and in combination, correlate with survival in young breast cancer patients,” Nature Medicine, vol. 3, no. 2, pp. 222–225, 1997. View at Publisher · View at Google Scholar
  95. J. Tsihlias, L. Kapusta, and J. Slingerland, “The prognostic significance of altered cyclin-dependent kinase inhibitors in human cancer,” Annual Review of Medicine, vol. 50, pp. 401–423, 1999. View at Publisher · View at Google Scholar · View at PubMed
  96. H. Saito, H. Hirano, and H. Hirano, “A new strategy of high-speed screening and quantitative structure-activity relationship analysis to evaluate human ATP-binding cassette transporter ABCG2-drug interactions,” Journal of Pharmacology and Experimental Therapeutics, vol. 317, no. 3, pp. 1114–1124, 2006. View at Publisher · View at Google Scholar · View at PubMed
  97. W. Liu, M. R. Baer, and M. R. Baer, “The tyrosine kinase inhibitor imatinib mesylate enhances the efficacy of photodynamic therapy by inhibiting ABCG2,” Clinical Cancer Research, vol. 13, no. 8, pp. 2463–2470, 2007. View at Publisher · View at Google Scholar · View at PubMed
  98. N. Gupta, P. M. Martin, and P. M. Martin, “Down-regulation of BCRP/ABCG2 in colorectal and cervical cancer,” Biochemical and Biophysical Research Communications, vol. 343, no. 2, pp. 571–577, 2006. View at Publisher · View at Google Scholar · View at PubMed