Advertisement

Photo-activated Cancer Therapy: Potential for Treatment of Brain Tumors

Chapter
Part of the Bioanalysis book series (BIOANALYSIS, volume 3)

Abstract

The diffuse and infiltrative nature of high grade gliomas, such as glioblastoma multiforme (GBM), makes complete surgical resection virtually impossible. The propensity of glioma cells to migrate along white matter tracts suggests that a cure is possible only if these migratory cells can be eradicated. Approximately 80% of GBMs recur within 2 cm of the resection margin, suggesting that a reasonable approach for improving the prognosis of GBM patients would be the development of improved local therapies capable of eradicating glioma cells in the brain-adjacent-to-tumor (BAT). An additional complicating factor for the development of successful therapies is the presence of the blood–brain barrier (BBB) which is highly variable throughout the BAT—it is intact in some regions, while leaky in others. This variance in BBB patency has significant implications for the delivery of therapeutic agents. The results of a number of studies have shown that experimental light-based therapeutic modalities such as photochemical internalization (PCI) and photothermal therapy (PTT) may be useful in the treatment of gliomas. This chapter summarizes recent findings illustrating the potential of: (1) PCI for the delivery of therapeutic macromolecules such as chemotherapeutic agents and tumor suppressor genes, and (2) nanoshell-mediated PTT, including nanoparticle delivery approaches via macrophages.

Keywords

Glioma Cell Endocytic Vesicle Photothermal Therapy Endosomal Escape Gold Nanoshells 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Wallner KE, Galicich JH, Krol G, Arbit E, Malkin MG (1989) Patterns of failure following treatment for glioblastoma multiforme and anaplastic astrocytoma. Int J Radiat Oncol Biol Phys 16:1405–9CrossRefGoogle Scholar
  2. 2.
    Brem H, Piantadosi S, Burger PC et al (1995) Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. Lancet 345(8956):1008–12CrossRefGoogle Scholar
  3. 3.
    Johannesen TB, Watne K, Lote K, Norum J, Tvera K, Hirschberg H (1999) Intracavity fractionated balloon brachytherapy in glioblastoma. Acta Neurochir 141:127–33CrossRefGoogle Scholar
  4. 4.
    Boekelheide K, Eveleth J, Tatum A, Winkelman J (1987) Microtubule assembly inhibition by porphyrins and related-compounds. Photochem Photobiol 46:657–661CrossRefGoogle Scholar
  5. 5.
    Dadosh N, Shaklai N (1987) Effect of protoporphyrin-IX on red blood-cell membrane cytoskeleton. J Muscle Res Cell Motil 9:86–92Google Scholar
  6. 6.
    Nelson J, Liaw L, Berns M (1987) Tumor destruction in photodynamic therapy. Photochem Photobiol 46:829–835CrossRefGoogle Scholar
  7. 7.
    Sporn L, Foster T (1992) Photofrin and light induces microtubule depolymerization in cultured human endothelial-cells. Cancer Res 52:3443–3448Google Scholar
  8. 8.
    Chen B, Pogue BW, Luna JM et al (2006) Tumor vascular permeabilization by vascular-targeting photosensitization: effects, mechanism, and therapeutic implications. Clin Cancer Res 12:917–923CrossRefGoogle Scholar
  9. 9.
    Berg K, Selbo PK, Prasmickaite L et al (1999) Photochemical internalization: a novel technology for delivery of macromolecules into cytosol. Cancer Res 59(6):1180–83Google Scholar
  10. 10.
    Dietze A, Peng Q, Selbo PK et al (2005) Enhanced photodynamic destruction of a transplantable fibrosarcoma using photochemical internalization of gelonin. Br J Cancer 92:2004–9CrossRefGoogle Scholar
  11. 11.
    Selbo PK, Kaalhus O, Sivam G, Berg K (2001) 5- aminolevulinic acid-based photochemical internalization of the immunotoxin MOC31-gelonin generates synergistic cytotoxic effects in vitro. Photochem Photobiol 74:303–10CrossRefGoogle Scholar
  12. 12.
    Selbo PK, Sivam G, Fodstad Ø, Sandvig K, Berg K (2000) Photochemical internalization increases the cytotoxic effect of the immunotoxin MOC31 gelonin. Int J Cancer 87:853–9CrossRefGoogle Scholar
  13. 13.
    Prasmickaite L, Høgset A, Selbo PK et al (2002) Photochemical disruption of endocytic vesicles before delivery of drugs: a new strategy for cancer therapy. Br J Cancer 86:652–7CrossRefGoogle Scholar
  14. 14.
    Selbo PK, Weyergang A, Høgset A et al (2010) Photochemical internalization provides time- and space-controlled endolysosomal escape of therapeutic molecules. J Control Release 148(1):2–12CrossRefGoogle Scholar
  15. 15.
    Berg K, Bommer J, Moan J (1989) Evaluation of sulfonated aluminum phthalocyanines for use in photochemotherapy. Cellular uptake studies. Cancer Lett 44:7–15CrossRefGoogle Scholar
  16. 16.
    Maman N, Dhami S, Phillips D, Brault D (1999) Kinetic and equilibrium studies of incorporation of di-sulfonated aluminum phthalocyanine into unilamellar vesicles. Biochim Biophys Acta 1420:168–178CrossRefGoogle Scholar
  17. 17.
    Vykhodtseva N, McDannold N, Hynynen K (2008) Progress and problems in the application of focused ultrasound for blood–brain barrier disruption. Ultrasonics 48:279–96CrossRefGoogle Scholar
  18. 18.
    Hirschberg H, Uzal FA, Chighvinadze D, Zhang MJ, Peng Q, Madsen SJ (2008) Disruption of the blood–brain barrier following ALA-mediated photodynamic therapy. Lasers Surg Med 40:535–41CrossRefGoogle Scholar
  19. 19.
    Hirschberg H, Zhang MJ, Gach HM et al (2009) Targeted delivery of bleomycin to the brain using photo-chemical internalization of Clostridium perfringens epsilon prototoxin. J Neurooncol 95(3):317–29CrossRefGoogle Scholar
  20. 20.
    Murphy LJ, Hachey DL, Oates JA et al (2000) Metabolism of bradykinin in vivo in humans: identification of BK1-5 as a stable plasma peptide metabolite. J Pharmacol Exp Ther 294(1):263–9Google Scholar
  21. 21.
    Worthington R, Mulders M (1975) The effect of Clostridium perfringens epsilon toxin on the blood–brain barrier of mice. Onderstepoort J Vet Res 42:25–31Google Scholar
  22. 22.
    Nagahama M, Sakurai J (1991) Distribution of labeled Clostridium perfringens epsilon toxin in mice. Toxicon 29:211–7CrossRefGoogle Scholar
  23. 23.
    Dorca-Arevalo J, Soler-Jover A, Gibert M et al (2008) Binding of epsilon toxin from Clostridium perfringens in the nervous system. Vet Microbiol 131:14–20CrossRefGoogle Scholar
  24. 24.
    Madsen SJ, Angell-Petersen E, Spetalen S, Carper SW, Ziegler SA, Hirschberg H (2006) Photodynamic therapy of newly implanted glioma cells in the rat brain. Lasers Surg Med 38:540–548CrossRefGoogle Scholar
  25. 25.
    Pron G, Mahrour N, Orlowski S (1999) Internalization of the bleomycin molecules responsible for bleomycin toxicity: a receptor-mediated endocytosis mechanism. Biochem Pharmacol 57:45–56CrossRefGoogle Scholar
  26. 26.
    Berg K, Dietze A, Kaalhus O, Hogset A (2005) Site-specific drug delivery by photochemical internalization enhances the antitumor effect of bleomycin. Clin Cancer Res 11(23):8476–85CrossRefGoogle Scholar
  27. 27.
    Alcantara L, Laguno S et al (2009) Malignant astrocytomas originate from neural stem/progenitor cells in a somatic tumor suppressor mouse model. Cancer Cell 15(1):45–56CrossRefGoogle Scholar
  28. 28.
    Evers P, Lee PP et al (2010) Irradiation of the potential cancer stem cell niches in the adult brain improves progression free survival of patients with malignant gliomas. BMC Cancer 10:384–9CrossRefGoogle Scholar
  29. 29.
    Hogset A, Ovstebo Engesaeter B, Prasmickaite L et al (2002) Light induced adenovirus gene transfer, an efficient and specific gene delivery technology for cancer gene therapy. Cancer Gene Ther 9:365–371CrossRefGoogle Scholar
  30. 30.
    Ndoye A, Dolivet G, Hogset A et al (2006) Eradication of p53-mutated head and neck squamous cell carcinoma xenografts using nonviral p53 gene therapy and photochemical internalization. Mol Ther 13(6):1156–62CrossRefGoogle Scholar
  31. 31.
    Knobbe CB, Merlo A, Reifenberger G (2002) Pten signaling in gliomas. Neuro Oncol 4(3):196–211Google Scholar
  32. 32.
    Cho SK, Kwon YJ (2011) Polyamine/DNA polyplexes with acid-degradable polymeric shell as structurally and functionally virus-mimicking nonviral vectors. J Control Release 150:287–297CrossRefGoogle Scholar
  33. 33.
    Chou CH, Sun CH, Zhou YH, Madsen SJ and Hirschberg H (2011) Enhanced transfection of brain tumor suppressor genes by photochemical internalization. Proceedings SPIE, photonic therapeutics and diagnostics, vol 7883, p 3UGoogle Scholar
  34. 34.
    Hirschberg H, Mathews MB, Shih EC, Madsen SJ, Kwon YJ (2012) Enhanced gene transfection by photochemical internalization of protomine sulfate/DNA complexes. Proceedings SPIE, Photonic therapeutics and diagnostics, vol 8207, p S1Google Scholar
  35. 35.
    Tsuchiya Y, Ishti T, Okahata Y, Sato T (2006) Characterization of protamine as a transfection accelerator for gene delivery. J Bioact Compat Polym 21:519–537CrossRefGoogle Scholar
  36. 36.
    Liu J, Guo S, Li Z, Liu L, Gu J (2009) Synthesis and characterization of stearyl protamine and investigation of their complexes with DNA for gene delivery. Colloids Surf B Biointerfaces 73(1):36–41CrossRefGoogle Scholar
  37. 37.
    Maeda H (2001) The enhanced permeability and retention (EPR) effect in tumor vasculature: the key role of tumor-selective macromolecular drug targeting. Adv Enzyme Regul 41:189–207CrossRefGoogle Scholar
  38. 38.
    Maeda H, Fang J, Inutsuka T, Kitamoto Y (2003) Vascular permeability enhancement in solid tumor: various factors, mechanisms involved and its implications. Int Immunopharmacol 3:319–328CrossRefGoogle Scholar
  39. 39.
    Huang X, Qian W, El-Sayed IH, El-Sayed MA (2007) The potential use of the enhanced nonlinear properties of gold nanospheres in photothermal cancer therapy. Lasers Surg Med 39(9):747–753CrossRefGoogle Scholar
  40. 40.
    Schwartz JA, Shetty AM, Price RE, Stafford RJ, Wang JC, Uthamanthil RK et al (2009) Feasibility study of particle-assisted laser ablation of brain tumors in orthotopic canine model. Cancer Res 69(4):1659–1667CrossRefGoogle Scholar
  41. 41.
    Badie B, Schartner JM (2000) Flow cytometric characterization of tumor associated macrophages in experimental gliomas. Neurosurgery 46:957–61 discussion 61–2Google Scholar
  42. 42.
    Roggendorf W, Strupp S, Paulus W (1996) Distribution and characterization of microglia/macrophages in human brain tumors. Acta Neuropathol 92:288–93CrossRefGoogle Scholar
  43. 43.
    Valable S, Barbier EL, Bernaudin M, Roussel S, Segebarth C, Petit E et al (2008) In vivo MRI tracking of exogenous monocytes/macrophages targeting brain tumors in a rat model of glioma. Neuroimage 40(2):973–983CrossRefGoogle Scholar
  44. 44.
    Choi MR, Stanton-Maxey KJ, Stanley JK et al (2007) A cellular Trojan Horse for delivery of therapeutic nanoparticles into tumors. Nano Lett 7(12):3759–3765ADSCrossRefGoogle Scholar
  45. 45.
    Baek SK, Makkouk AR, Krasieva T, Sun CH, Madsen SJ, Hirschberg H (2011) Photothermal treatment of glioma; an in vitro study of macrophage-mediated delivery of gold nanoshells. J Neurooncol 104(2):439–48CrossRefGoogle Scholar
  46. 46.
    Madsen SJ, Baek SK, Makkouk AK, Krasieva T, Hirschberg H (2012) Macrophages as cell-based delivery systems for nanoshells in photothermal therapy. Ann Biomed Eng 40(2):507–15CrossRefGoogle Scholar
  47. 47.
    Hirschberg H, Samset E, Hole PK, Lote K (2006) Impact of intraoperative MRI on the results of surgery for high grade gliomas. J Min Inv Neurosurg 48:77–84CrossRefGoogle Scholar
  48. 48.
    Stummer W, Pichlmeier U, Meinel T, Wiestler OD, Zanella F, Reulen HJ (2006) Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomized controlled multicentre phase III trial. Lancet Oncol 7:392–401CrossRefGoogle Scholar
  49. 49.
    Madsen SJ, Sun CH, Tromberg BJ, Hirschberg H (2001) Development of a novel balloon applicator for optimizing light delivery in photodynamic therapy. Lasers Surg Med 29:406–10CrossRefGoogle Scholar
  50. 50.
    Madsen SJ, Svaasand LO, Tromberg BJ, Hirschberg H (2001) Characterization of optical and thermal distributions from an intracranial balloon applicator for photodynamic therapy. Proc SPIE 4257:41ADSCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Beckman Laser Institute, University of CaliforniaIrvineUSA

Personalised recommendations