Skip to main content

Advertisement

Log in

Isolation and characterization of PDT-resistant cancer cells

  • Perspective
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Even though the efficacy of photodynamic therapy (PDT) for treating premalignant and malignant lesions has been demonstrated, resistant tumor cells to this therapy occasionally appear. Here, we describe the published methods to isolate resistant cancer cells to PDT and propose new procedures that may be used, as laboratory models allow a better understanding of resistance mechanisms. For this purpose, the treatment conditions, the photosensitizer (PS) or pro-drug, the cell line and the final selection–clonal of total population–must be taken into account. In general, high and repeated treatment doses are used. The resistant cell population characterization may include cell morphology, response to PDT, expression of death proteins or survival related genes and cell proliferation analysis. In addition, in vivo models such as the resistant cell transplantation to mice, allow evaluating tumorigenicity and aggressiveness, leading to the determination of the in vivo resistance. Summarizing, in order to improve clinical results, cellular models can help understand PDT-resistance mechanisms in vivo and in vitro.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

ALA:

δ-Aminolevulinic acid

ALDH1:

Aldehyde dehydrogenase 1

ABC:

ATP-binding cassette

BCC:

Basal cell carcinoma

BCRP:

Breast cancer resistant protein

BPD-MA:

Benzoporphyrin derivative monoacid ring A

CAM:

Cell adhesion molecule

EGFR:

Epidermal growth factor receptor

ERK:

Extracellular signal regulated kinases

HPPH:

2-(1-Hexyloxethyl)-2-devinyl pyropheophorbide-a

IAP:

Inhibitor of apoptosis protein

MAL:

Methyl δ-aminolevulinic acid

MAPK:

Mitogen-activated protein kinase

MDR:

Multidrug resistance

MRP:

Multidrug resistant associated protein

NMSC:

Non-melanoma skin cancer

PHP:

Polyhematoporphyrin

P-gp:

P-glycoprotein

PDT:

Photodynamic therapy

PpIX:

Protoporphyrin IX

PS:

Photosensitizer

PII:

Photofrin II

PPC:

Zn(ii) pyridinium-substituted phthalocyanine

SOD:

Superoxide dismutase

References

  1. C. Holohan, S. Van Schaeybroeck, D. B. Longley, P. G. Johnston, Nat. Rev. Cancer, 2013, 13, 714–726.

    Article  CAS  PubMed  Google Scholar 

  2. D. B. Longley, P. G. Johnston, J. Pathol., 2005, 205, 275–292.

    Article  CAS  PubMed  Google Scholar 

  3. J. P. Gillet, M. Gottesman, Methods Mol. Biol., 2010, 596, 47–76.

    Article  CAS  PubMed  Google Scholar 

  4. S. Al-Dimassi, T. Abou-Antoun, M. El-Sibai, Clin. Transl. Oncol., 2014, 16, 511–516.

    Article  CAS  PubMed  Google Scholar 

  5. E. Maydan, P. K. Nooothet, M. P. Goldman, J. Drugs Dermatol., 2006, 5, 804–806.

    PubMed  Google Scholar 

  6. S. Fiechter, A. Skaria, H. Nievergelt, R. Anex, L. Borradori, L. Parmentier, Dermatology, 2012, 224, 346–351.

    Article  PubMed  Google Scholar 

  7. Y. Gilaberte, L. Milla, N. Salazar, J. Vera-Alvarez, O. Kourani, A. Damian, V. Rivarola, M. J. Roca, J. Espada, S. González, A. Juarranz, J. Invest. Dermatol., 2014, 134, 2428–2437.

    Article  CAS  PubMed  Google Scholar 

  8. F. Bardazzi, C. Loi, M. Magnano, E. C. Burtica, F. Giordano, A. Patrizi, J. Dermatolog. Treat., 2014 10.3109/09546634.2014.915004

    Google Scholar 

  9. A. Juarranz, P. Jaén, F. Sanz-Rodríguez, J. Cuevas, S. González, Clin. Transl. Oncol., 2008, 10, 148–154.

    Article  CAS  PubMed  Google Scholar 

  10. M. G. Bredell, E. Besic, C. Maake, H. Walt, J. Photochem. Photobiol., B, 2010, 101, 185–190.

    Article  CAS  Google Scholar 

  11. P. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B. C. Wilson, J. Golab, CA Cancer J. Clin., 2011, 61, 250–281.

    Article  PubMed  PubMed Central  Google Scholar 

  12. B. Ortiz-Policarpio, H. Lui, Skin Therapy Lett., 2009, 14, 1–3.

    CAS  PubMed  Google Scholar 

  13. M. R. Lackner, T. R. Wilson, J. Settleman, Future Oncol., 2012, 8, 999–1014.

    Article  CAS  PubMed  Google Scholar 

  14. M. Rebucci, C. Michiels, Pharmacology, 2013, 85, 1219–1226.

    CAS  Google Scholar 

  15. R. Rosa, F. Monteleone, N. Zambrano, R. Bianco R, Curr. Med. Chem., 2014, 21, 1595–1606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Q. Wu, Z. Yang, Y. Nie, Y. Shi, D. Fan, Cancer Lett., 2014, 347, 159–166.

    Article  CAS  PubMed  Google Scholar 

  17. A. Marusyk, K. Polyak, Biochim. Biophys. Acta, 2010, 1805, 105–117.

    CAS  PubMed  Google Scholar 

  18. M. Gerlinger, C. Swanton, Br. J. Cancer, 2010, 103, 1139–1143.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. N. A. Saunders, F. Simpson, E. W. Thompson, M. M. Hill, L. Endo-Munoz, G. Leggatt, R. F. Minchin, A. Guminski, EMBO Mol. Med., 2012, 4, 675–684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. M. McDermott, A. Eustace, S. Busschots, L. Breen, J. Crown, M. Clynes, N. O’Donovan, B. Stordal, Front. Oncol., 2014, 4, 40.

    Article  PubMed  PubMed Central  Google Scholar 

  21. R. Ikeda, L. C. Vermeulen, E. Lau, Z. Jiang, S. M. Kavanaugh, K. Yamada, J. M. Kolesar, Oncol. Lett., 2011, 2, 91–94.

    Article  CAS  PubMed  Google Scholar 

  22. K. Q. Zuo, X. P. Zhang, J. Zou, D. Li, Z. W. Lv, J. Int. Med. Res., 2010, 38, 1428–1435.

    Article  CAS  PubMed  Google Scholar 

  23. J. L. Biedler, H. Riehm, Cancer Res., 1970, 30, 1174–1184.

    CAS  PubMed  Google Scholar 

  24. G. M. Hahn, I. van Kersen, Cancer Res., 1988, 48, 1803–1807.

    CAS  PubMed  Google Scholar 

  25. M. C. Luna, C. J. Gomer, Cancer Res., 1991, 51, 4243–4249.

    CAS  PubMed  Google Scholar 

  26. G. Singh, B. C. Wilson, S. M. Sharkey, G. P. Browman, P. Deschamps, Photochem. Photobiol., 1991, 54, 307–312.

    Article  CAS  PubMed  Google Scholar 

  27. A. Casas, C. Perotti, B. Ortel, G. Di Venosa, M. Saccoliti, A. Battle, T. Hasan, Int. J. Oncol., 2006, 29, 397–405.

    CAS  PubMed  Google Scholar 

  28. J. Barretina, G. Caponigro, N. Stransky, K. Venkatesan, A. A. Margolin, S. Kim, C. J. Wilson, J. Lehar, G. V. Kryukov, D. Sonkin, A. Reddy, M. Liu, L. Murray, M. F. Berger, J. E. Monahan, P. Morais, J. Meltzer, A. Korejwa, J. Jane-Valbuena, F. A. Mapa, J. Thibault, E. Bric-Furlong, P. Raman, A. Shipway, I. H. Engels, J. Cheng, G. K. Yu, J. Yu, P. Aspesi Jr., M. de Silva, K. Jagtap, M. D. Jones, L. Wang, C. Hatton, E. Palescandolo, S. Gupta, S. Mohan, C. Sougnez, R. C. Onofrio, T. Liefeld, L. MacConaill, W. Winckler, M. Reich, N. Li, J. P. Mesirov, S. B. Gabriel, G. Getz, K. Ardlie, V. Chan, V. E. Myer, B. L. Weber, J. Porter, M. Warmuth, P. Finan, J. L. Harris, M. Meyerson, T. R. Golub, M. P. Morrissey, W. R. Sellers, R. Schlegel, L. A. Garraway, Nature, 2012, 483, 603–607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. J. P. Gillet, S. Varma, M. M. Gottesman, J. Natl. Cancer Inst., 2013, 105, 452–458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. S. Mayhew, D. Vernon, J. Schofield, J. Griffiths, S. Brown, Photochem. Photobiol., 2001, 73, 39–46.

    Article  CAS  PubMed  Google Scholar 

  31. G. Singh, M. Espiritu, X. Yun Shen, J. G. Hanlon, A. J. Rainbow, Photochem. Photobiol., 2001, 73, 651–656.

    Article  CAS  PubMed  Google Scholar 

  32. T. Tsai, H. Tai Ji, P. Chiang, R. Chou, W. W. Chang, C. Chen, Lasers Surg. Med., 2009, 41, 305–315.

    Article  PubMed  Google Scholar 

  33. L. N. Milla, I. S. Cogno, M. E. Rodríguez, F. Sanz-Rodríguez, A. Zamarrón, Y. Gilaberte, E. Carrasco, V. A. Rivarola, A. Juarranz, J. Cell. Biochem., 2011, 112, 2266–2278.

    Article  CAS  PubMed  Google Scholar 

  34. L. Breen, L. Murphy, J. Keenan, M. Clynes, Toxicol. In vitro, 2008, 22, 1234–1241.

    Article  CAS  PubMed  Google Scholar 

  35. L. Breen, J. Keenan, M. Clynes, Methods Mol. Biol., 2011, 731, 125–133.

    Article  CAS  PubMed  Google Scholar 

  36. S. D. Mertins, Anticancer Drugs, 2014, 25, 353–367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. C. Pincelli, A. Marconi, J. Cell. Physiol., 2010, 225, 310–315.

    Article  CAS  PubMed  Google Scholar 

  38. C. A. La Porta, World J. Stem Cells, 2012, 4, 17–20.

    Article  PubMed  PubMed Central  Google Scholar 

  39. M. Bostad, K. Berg, A. Høgset, E. Skarpen, H. Stenmark, P. K. Selbo, J. Controlled Release, 2013, 168, 317–326.

    Article  CAS  Google Scholar 

  40. J. Morgan, J. D. Jackson, X. Zheng, S. K. Pandey, R. K. Pandey, Mol. Pharm., 2010, 7, 1789–1804.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. C. H. Yu, C. C. Yu, PLoS One, 2014, 9, 1–7.

    Google Scholar 

  42. S. Akiyama, A. Fojo, J. A. Hanover, I. Pastan, M. M. Gottesman, Somatic Cell Mol. Genet., 1985, 11, 117–126.

    Article  CAS  Google Scholar 

  43. L. Y. Yang, J. M. Trujillo, M. J. Siciliano, Y. Kido, Z. H. Siddik, Y. Z. Su, Int. J. Cancer, 1993, 53, 478–485.

    Article  CAS  PubMed  Google Scholar 

  44. W. Sakai, E. M. Swisher, B. Y. Karlan, M. K. Agarwal, J. Higgins, C. Friedman, E. Villegas, C. Jacquemont, D. J. Farrugia, F. J. Couch, N. Urban, T. Taniguchi, Nature, 2008, 451, 1116–1120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. D. Hanahan, R. A. Weinberg, Cell, 2011, 144, 646–674.

    Article  CAS  PubMed  Google Scholar 

  46. G. I. Solyanik, Exp. Oncol., 2010, 32, 181–185.

    CAS  PubMed  Google Scholar 

  47. A. Casas, G. Di Venosa, T. Hasan, A. Batlle, Curr. Med. Chem., 2011, 18, 2486–2515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. L. Milla Sanabria, M. E. Rodríguez, I. S. Cogno, N. B. Rumie Vittar, M. F. Pansa, M. J. Lamberti, V. A. Rivarola, Biochim. Biophys. Acta, 2013, 1835, 86–99.

    PubMed  Google Scholar 

  49. K. Noguchi, K. Katayama, Y. Sugimoto, Pharmagenomics Pers. Med., 2014, 7, 53–64.

    Google Scholar 

  50. R. W. Robey, K. Steadman, O. Polgar, S. E. Bates, Cancer Biol. Ther., 2005, 4, 187–194.

    Article  CAS  PubMed  Google Scholar 

  51. W. Liu, M. R. Baer, M. J. Bowman, P. Pera, X. Zheng, J. Morgan, R. A. Pandey, A. R. Oseroff, Clin. Cancer Res., 2007, 13, 2463–2470.

    Article  CAS  PubMed  Google Scholar 

  52. R. Bianco, T. Troiani, G. Tortora, F. Ciardiello, Endocr. Relat. Cancer, 2005, 12, 159–171.

    Article  CAS  Google Scholar 

  53. R. Roskoski Jr., Pharmacol. Res., 2012, 66, 105–143.

    Article  CAS  PubMed  Google Scholar 

  54. A. Weyergang, P. K. Selbo, K. Berg, Biochim. Biophys. Acta, 2013, 1830, 2659–2670.

    Article  CAS  PubMed  Google Scholar 

  55. H. Ishii, M. Iwatsuki, K. Ieta, D. Ohta, N. Haraguchi, K. Mimori, M. Mori, Cancer Sci., 2008, 99, 1871–1877.

    Article  CAS  PubMed  Google Scholar 

  56. Y. C. Chen, Y. W. Chen, H. S. Hsu, L. M. Tseng, P. I. Huang, K. H. Lu, D. T. Chen, L. K. Tai, M. C. Yung, S. C. Chang, H. H. Ku, S. H. Chiou, W. L. Lo, Biochem. Biophys. Res. Commun., 2009, 385, 307–313.

    Article  CAS  PubMed  Google Scholar 

  57. F. Jiang, Q. Qiu, A. Khanna, N. W. Todd, J. Deepak, L. Xing, H. Wang, Z. Liu, Y. Su, S. A. Stass, R. L. Katz, Mol. Cancer Res., 2009, 7, 330–338.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. M. C. Ortells, W. M. Keyes, Biochem. Soc. Trans., 2014, 42, 663–669.

    Article  CAS  PubMed  Google Scholar 

  59. G. Adhikary, D. Grun, C. Kerr, S. Balasubramanian, E. A. Rorke, M. Vemuri, S. Boucher, J. R. Bickenbach, T. Hornyak, W. Xu, M. L. Fisher, R. L. Eckert, PLoS One, 2013, 8, 1–14.

    Article  CAS  Google Scholar 

  60. J. Kim, W. Lim, S. Kim, S. Jeon, Z. Hui, K. Ni, C. Kim, Y. Im, H. Choi, O. Kim, J. Oral Pathol. Med., 2014, 43, 675–684.

    Article  CAS  PubMed  Google Scholar 

  61. M. F. Wei, M. W. Chen, K. C. Chen, P. J. Lou, S. Y. Lin, S. C. Hung, M. Hsiao, C. J. Yao, M. J. Shieh, Autophagy, 2014, 10, 1179–1192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. K. Adams, A. J. Rainbow, B. C. Wilson, G. Singh, J. Photochem. Photobiol., B, 1999, 49, 136–141.

    Article  CAS  Google Scholar 

  63. Y. C. Lim, J. O. Yoo, D. Park, G. Kang, B. M. Hwang, Y. M. Kim, K. S. Ha, Cancer Sci., 2009, 100, 2431–2436.

    Article  CAS  PubMed  Google Scholar 

  64. S. W. Hoi, H. M. Wong, J. Y. Chan, G. G. Yue, G. M. Tse, B. K. Law, W. P. Fong, K. P. Fung, Phytother. Res., 2012, 26, 734–742.

    Article  CAS  PubMed  Google Scholar 

  65. Y. Ren, R. Wang, Y. Liu, H. Guo, X. Zhou, X. Yuan, C. Liu, J. Tian, H. Yin, Y. Wang, N. Zhang, Biomaterials, 2014, 35, 2462–2470.

    Article  CAS  PubMed  Google Scholar 

  66. P. M. Tang, J. Y. Chan, D. M. Zhang, S. W. Au, W. P. Fong, S. K. Kong, S. K. Tsui, M. M. Waye, T. C. Mak, K. P. Fung, Cancer Biol. Ther., 2007, 6, 504–509.

    Article  CAS  PubMed  Google Scholar 

  67. M. M. Tomayko, C. P. Reynolds, Cancer Chemother. Pharmacol., 1989, 24, 148–154.

    Article  CAS  PubMed  Google Scholar 

  68. A. Casas, G. Di Venosa, S. Vanzulli, C. Perotti, L. Mamome, L. Rodriguez, M. Simian, A. Juarranz, O. Pontiggia, T. Hasan, A. Batlle, Cancer Lett., 2008, 271, 342–351.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. S. M. Sharkey, B. C. Wilson, R. Moorehead, G. Singh, Cancer Res., 1993, 53, 4994–4999.

    CAS  PubMed  Google Scholar 

  70. A. Mukherjee, S. Misra, N. G. Howlett, P. Karmakar, Mutat. Res., 2013, 755, 135–140.

    Article  CAS  PubMed  Google Scholar 

  71. T. Tanaka, S. Toujima, J. Tanaka, Int. J. Oncol., 2012, 41, 1837–1844.

    Article  CAS  PubMed  Google Scholar 

  72. H. H. Evans, M. F. Horng, M. Ricanati, J. T. Deahl, N. L. Oleinick, Photochem. Photobiol., 1997, 66, 690–696.

    Article  CAS  PubMed  Google Scholar 

  73. J. A. Woods, N. J. Traynor, L. Brancaleon, H. Moseley, Photochem. Photobiol., 2004, 79, 105–113.

    Article  CAS  PubMed  Google Scholar 

  74. S. Struski, M. Doco-Fenzy, M. Koehler, I. Chudoba, F. Levy, L. Masson, N. Michel, E. Ulrich, N. Gruson, J. Bénard, G. Potron, P. Cornillet-Lefebvre, Anal. Cell. Pathol., 2003, 25, 115–122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. A. V. Roschke, I. R. Kirsch, Curr. Drug Targets, 2010, 11, 1341–1350.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. S. L. Cooke, C. K. Ng, N. Melnyk, M. J. Garcia, T. Hardcastle, J. Temple, S. Langdon, D. Huntsman, J. D. Brento, Oncogene, 2010, 29, 4905–4913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. G. A. Barron, H. Moseley, J. A. Woods, J. Photochem. Photobiol., B, 2013, 126, 87–96.

    Article  CAS  Google Scholar 

  78. P. A. Martínez-Carpio, M. A. Trelles, Lasers Med. Sci., 2010, 25, 767–771.

    Article  PubMed  Google Scholar 

  79. C. Edmonds, S. Hagan, S. M. Gallagher-Colombo, T. M. Busch, K. A. Cengel, Cancer Biol. Ther., 2012, 13, 1463–1470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. S. A. Rosenzweig, Biochem. Pharmacol., 2012, 83, 1041–1048.

    Article  CAS  PubMed  Google Scholar 

  81. J. Zawacka-Pankau, J. Krachulec, I. Grulkowski, K. P. Bielawski, G. Selivanova, Toxicol. Appl. Pharmacol., 2008, 232, 487–497.

    Article  CAS  PubMed  Google Scholar 

  82. A. Nakanishi, Y. Kitagishi, Y. Ogura, S. Matsuda, Int. J. Oncol., 2014, 44, 1813–1819.

    Article  CAS  PubMed  Google Scholar 

  83. N. Zaffaroni, M. Pennati, G. Colella, Cell. Mol. Life Sci., 2002, 59, 1406–1412.

    Article  CAS  PubMed  Google Scholar 

  84. Á. Ferrario, N. Rucker, S. Wong, M. Luna, C. J. Gomer, Cancer Res., 2007, 67, 4989–4995.

    Article  CAS  PubMed  Google Scholar 

  85. H. Yamamoto, C. Yee Ngan, M. Monden, Cancer Sci., 2008, 99, 1709–1714.

    Article  CAS  PubMed  Google Scholar 

  86. C. J. Gomer, S. W. Ryter, A. Ferrario, N. Rucker, S. Wong, A. M. Fisher, Cancer Res., 1996, 56, 2355–2360.

    CAS  PubMed  Google Scholar 

  87. N. Etminan, C. Peters, D. Lakbir, E. Bünemann, V. Börger, M. C. Sabel, D. Hänggi, H. J. Steiger, W. Stummer, R. V. Sorg, Br. J. Cancer, 2011, 105, 961–969.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. S. Rottenberg, J. Jonkers, Drug Resist. Updat., 2008, 11, 51–60.

    Article  CAS  PubMed  Google Scholar 

  89. K. Politi, W. Pao, J. Clin. Oncol., 2011, 29, 2273–2281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. T. Momma, M. R. Hamblin, H. C. Wu, T. Hasan, Cancer Res., 1998, 58, 5425–5431.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ángeles Juarranz.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zamarrón, A., Lucena, S.R., Salazar, N. et al. Isolation and characterization of PDT-resistant cancer cells. Photochem Photobiol Sci 14, 1378–1389 (2015). https://doi.org/10.1039/c4pp00448e

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c4pp00448e

Navigation