Skip to main content
SpringerLink
Log in

Ligand Liposomes and Boron Neutron Capture Therapy

  • Published:
Journal of Neuro-Oncology Aims and scope Submit manuscript

Abstract

Boron neutron capture therapy (BNCT) has been used both experimentally and clinically for the treatment of gliomas and melanomas, with varying results. However, the therapeutic effects on micro-invasive tumor cells are not clear. The two drugs that have been used clinically, p-boronophenylalanine, (BPA), and the sulfhydryl borane, (BSH), seem to be taken up preferentially in solid tumor areas but it is uncertain whether enough boron is taken up by micro-invasive tumor cells. To increase the selective uptake of boron by such cells, would be to exploit tumor transformation related cellular changes such as over-expression of growth factor receptors. However, the number of receptors varies from small to large and the uptake of large amounts of boron for each receptor interaction is necessary in order to deliver sufficient amounts of boron. Therefore, each targeting moiety must deliver large number of boron atoms. One possible way to meet these requirements would be to use receptor-targeting ligand liposomes, containing large number of boron atoms. This will be the subject of this review and studies of boron containing liposomes, with or without ligand, will be discussed. Two recent examples from the literature are ligand liposomes targeting either folate or epidermal growth factor (EGF) receptors on tumor cells. Other potential receptors on gliomas include PDGFR and EGFRvIII. Besides the appropriate choice of target receptor, it is also important to consider delivery of the ligand liposomes, their pharmacodynamics and pharmacokinetics and cellular processing, subjects that also will be discussed in this review.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Gregoriadis G, Wills EJ, Swain CP, Tavill AS: Drug-carrier potential of liposomes in cancer chemotherapy. Lancet 1: 1313–1316, 1974

    Google Scholar 

  2. Gabizon A, Papahadjopoulos D: Liposome formulations with prolonged circulation time in blood and enhanced uptake by tumors. Proc Natl Acad SciUSA85: 6949–6953, 1998

    Google Scholar 

  3. Papahadjopoulos D, Allen TM, Gabizon A, Mayhew E, Matthay K, Huang SK, Lee KD, Woodle MC, Lasic DD, Redemann C, Martin FJ: Sterically stabilized liposomes: improvements in pharmacokinetics and antitumor therapeutic efficacy. Proc Natl Acad Sci USA 88: 11460–11464, 1991

    Google Scholar 

  4. Allen TM, Hansen C, Martin F, Redemann C, Yau-Young A: Liposomes containing synthetic lipid derivatives of poly(ethylene glycol) show prolonged circulation half-lives in vivo. Biochim Biophys Acta 1066: 29–36, 1991

    Google Scholar 

  5. Gabizon AA: Selective tumor localization and improved therapeutic index of anthracyclines encapsulated in longcirculating liposomes. Cancer Res 52: 891–896, 1992

    Google Scholar 

  6. Klibanov AL, Maruyama K, Torchilin VP, Huang L: Amphipathic polyethylene glycols effectively prolong the circulation time of liposomes. FEBS Lett 268: 235-237, 1990 56

    Google Scholar 

  7. Maruyama K, Yuda T, Okamoto A, Kojima S, Suginaka A, Iwatsuru M: Prolonged circulation time in vivo of large unilamelar liposomes composed of distearoyl phosphatidylcholine and cholesterol containing amphipathic poly(ethylene glycol). Biochim Biophys Acta 1128: 44–49, 1992

    Google Scholar 

  8. Feakes DA, Shelly K, Hawthorne MF: Selective boron delivery to murine tumors by lipophilic species incorporated in the membranes of unilamellar liposomes. Proc Natl Acad Sci USA 92: 1367–1370, 1995

    Google Scholar 

  9. Forssen EA, Coulter DM, Proffitt RT: Selective in vivo localization of daunorubicin small unilamellar vesicles in solid tumors. Cancer Res 52: 3255–3261, 1992

    Google Scholar 

  10. Feakes DA, Shelly K, Knobler CB, Hawthorne MF: Na3[B20H17NH3]: synthesis and liposomal delivery to murine tumors. Proc Natl Acad Sci USA 91(8): 3029–3033, 1994

    Google Scholar 

  11. Hawthorne MF, Shelly K: Liposomes as drug delivery vehicles for boron agents. J Neuro-Oncol 33(1-2): 53–58, 1997

    Google Scholar 

  12. Mehta SC, Lai JC, Lu DR: Liposomal formulations containing sodium mercaptoundecahydrododecaborate (BSH) for boron neutron capture therapy. J Microencapsul 13(3): 269–279, 1996

    Google Scholar 

  13. Moraes AM, Santana MH, Carbonell RG: Preparation and characterization of liposomal systems entrapping the boronated compound o-carboranylpropylamine. J Microencapsul 16(5): 647–664, 1999

    Google Scholar 

  14. Shelly K, Feakes DA, Hawthorne MF, Schmidt PG, Krisch TA, Bauer WF: Model studies directed toward the boron neutron-capture therapy of cancer: boron delivery to murine tumors with liposomes. Proc Natl Acad Sci USA 89(19): 9039–9043, 1992

    Google Scholar 

  15. Yanagie H, Fujii Y, Takahashi T, Tomita T, Fukano Y, Hasumi K, Nariuchi H, Yasuda T, Sekiguchi M, Uchida H: Boron neutron capture therapy using 10B entrapped anti-CEA immunoliposome. Hum Cell 2(3): 290-296, 1989 (in Japanese)

    Google Scholar 

  16. Yanagie H, Tomita T, Kobayashi H, Fujii Y, Takahashi T, Hasumi K, Nariuchi H, Sekiguchi M: Application of bronated anti-CEA immunoliposome to tumour cell growth inhibition in in vitro boron neutron capture therapy model. Br J Cancer 63: 522–526, 1991

    Google Scholar 

  17. Yanagie H, Tomita T, Kobayashi H, Fujii Y, Nonaka Y, Saegusa Y, Hasumi K, Eriguchi M, Kobayashi T, Ono K: Inhibition of human pancreatic cancer growth in nude mice by boron neutron capture therapy. Br J Cancer 75(5): 660–665, 1997

    Google Scholar 

  18. Pan XQ, Wang H, Shukla S, Sekido M, Adams DM, Tjarks W, Barth RF, Lee RJ: Boron-containing folate receptor-targeted liposomes as potential delivery agents for neutron capture therapy. Bioconjug Chem 13(3): 435–442, 2002

    Google Scholar 

  19. Pan XQ, Wang H, Lee RJ: Boron delivery to a murine lung carcinoma using folate receptor-targeted liposomes. Anticancer Res 22(3): 1629–1633, 2002

    Google Scholar 

  20. Bohl Kullberg E, Bergstrand N, Carlsson J, Edwards K, Johnsson M, Sjöberg S, Gedda L: Development of EGFconjugated liposomes for targeted delivery of boronated DNA-binding agents. Bioconj Chem 13(4): 737–743, 2002

    Google Scholar 

  21. Blume G, Cevc G, Crommelin MD, Bakker-Woudenberg IA, Kluft C, Storm G: Specific targeting with poly(ethylene glycol)-modified liposomes: coupling of homing devices to the ends of the polymeric chains combines effective target binding with long circulation times. Biochim Biophys Acta 1149: 180–184, 1993

    Google Scholar 

  22. Barth RF, Yang W, Rotaru JH, Moeschberger ML, Boesel CP, Soloway AH, Joel DD, Nawrocky MM, Ono K, Goodman JH: Boron neutron capture therapy of brain tumors: enhanced survival and cure following blood-brain barrier disruption and intracarotid injection of sodium borocaptate and boronophenylalanine. Int J Radiat Oncol Biol Phys 47: 209–218, 2000

    Google Scholar 

  23. Gregoire V, Sindic C, Gahbauer RA, Wambersie A: Alteration of the blood-brain barrier after irradiation: implication in boron neutron capture therapy. Strahlenther-Onkol 169: 534–542, 1993

    Google Scholar 

  24. Lu DR, Mehta SC, Chen W: Selective boron drug delivery to brain tumors for boron neutron capture therapy. Adv Drug Deliv Rev 26(2-3): 231–247, 1997

    Google Scholar 

  25. Mehta SC, Lu DR: Targeted drug delivery for boron neutron capture therapy. Pharm Res 13(3): 344–351, 1996

    Google Scholar 

  26. Yang W, Barth RF, Leveille R, Adams DM, Ciesielski M, Fenstermaker RA, Capala J: Evaluation of systemically administered radiolabeled epidermal growth factor as a brain tumor targeting agent.J Neuro-Oncol 55(1): 19–28, 2001

    Google Scholar 

  27. Yang W, Barth RF, Adams DM, Ciesielski MJ, Fenstermaker RA, Shukla S, Tjarks W, Caligiuri MA: Convection-enhanced delivery of boronated epidermal growth factor for molecular targeting of EGF receptorpositive gliomas. Cancer Res 62(22): 6552–6558, 2002

    Google Scholar 

  28. Barth RF, Soloway AH, Fairchild RG, Brugger RM: Boron neutron capture therapy for cancer. Realities and prospects. Cancer 70(12): 2995–3007, 1992

    Google Scholar 

  29. Barth RF, Soloway AH, Brugger RM: Boron neutron capture therapy of brain tumors: past history, current status, and future potential. Cancer Invest 14(6): 534–550, 1996

    Google Scholar 

  30. Barth RF, Soloway AH, Goodman JH, Gahbauer RA, Gupta N, Blue TE, Yang W, Tjarks W: Boron neutron capture therapy of brain tumors: an emerging therapeutic modality. Neurosurgery 44(3): 433–450, 1999

    Google Scholar 

  31. Fairchild RG, Bond VP: Current status of 10B-neutron capture therapy: enhancement of tumor dose via beam filtration and dose rate, and the effects of these parameters on minimum boron content: a theoretical evaluation. Int J Radiat Oncol Biol Phys 11: 831–840, 1985

    Google Scholar 

  32. Gabel D, Foster S, Fairchild RG: The Monte Carlo simulation of the biological effect of the 10B(n, alpha)7Li reaction in cells and tissue and its implication for boron neutron capture therapy. Radiat Res 111: 14–25, 1987

    Google Scholar 

  33. Hartman T, Carlsson J: Radiation dose heterogeneity in receptor and antigen mediated boron neutron capture therapy. Radiother Oncol 31: 61–75, 1994

    Google Scholar 

  34. Rassow J, Stecher-Rasmussen F, Voorbraak W, Moss R, Vroegindeweij C, Hideghety K, Sauerwein W: Comparison of quality assurance for performance and safety characteristics of the facility for boron neutron capture therapy 57 in Petten/NL with medical electron accelerators. Radiother Oncol 59: 99–108, 2001

    Google Scholar 

  35. Chanana AD, Capala J, Chadha M, Coderre JA, Diaz AZ, Elowitz EH, Iwai J, Joel DD, Liu HB, Ma R, Pendzick N, Peress NS, Shady MS, Slatkin DN, Tyson GW, Wielopolski L: Boron neutron capture therapy for glioblastoma multiforme: interim results from the phase I/II doseescalation studies. Neurosurgery 44: 1182–1192, 1999

    Google Scholar 

  36. Diaz AZ, Coderre JA, Chanana AD, Ma R: Boron neutron capture therapy for malignant gliomas. Ann Med 32: 81–85, 2000

    Google Scholar 

  37. Tjarks W, Wang J, Chandra S, Ji W, Zhuo J, Lunato AJ, Boyer C, Li Q, Usova EV, Eriksson S, Morrison GH, Cosquer GY: Synthesis and biological evaluation of boronated nucleosides for boron neutron capture therapy (BNCT) of cancer. Nucleosides Nucleotides Nucleic Acids 20: 695–698, 2001

    Google Scholar 

  38. Ceberg CP, Brun A, Kahl SB, Koo MS, Persson BR, Salford LG: A comparative study on the pharmacokinetics and biodistribution of boronated porphyrin (BOPP) and sulfhydryl boron hydride (BSH) in the RG2 rat glioma model. J Neurosurg 83(1): 86–92, 1995

    Google Scholar 

  39. Gedda L, Ghaneolhosseini H, Nilsson P, Nyholm K, Pettersson J, Sjoberg S, Carlsson J: The influence of lipophilicity on binding of boronated DNA-intercalating compounds in human glioma spheroids. Anticancer Drug Des 15: 277–286,2000

    Google Scholar 

  40. Hawthorne MF: New horizons for therapy based on the boron neutron capture reaction. Mol Med Today 4: 174–181, 1998

    Google Scholar 

  41. Sjoberg S, Carlsson J, Ghaneolhosseini H, Gedda L, Hartman T, Malmquist J, Naeslund C, Olsson P, Tjarks W: Chemistry and biology of some low molecular weight boron compounds for boron neutron capture therapy. J Neuro-Oncol 33: 41–52, 1997

    Google Scholar 

  42. Barth RF, Adams DM, Soloway AH, Alam F, Darby MV: Boronated starburst dendrimer-monoclonal antibody immunoconjugates: evaluation as a potential delivery system for neutron capture therapy. Bioconjug Chem 5: 58–66, 1994

    Google Scholar 

  43. Barth RF, Yang W, Adams DM, Rotaru JH, Shukla S, Sekido M, Tjarks W, Fenstermaker RA, Ciesielski M, Nawrocky MM, Coderre JA. Molecular targeting of the epidermal growth factor receptor for neutron capture therapy of gliomas. Cancer Res 62(11): 3159–3166, 2002

    Google Scholar 

  44. Nakanishi A, Guan L, Kane RR, Kasamatsu H, Hawthorne MF: Toward a cancer therapy with boron-rich oligomeric phosphate diesters that target the cell nucleus. Proc Natl Acad Sci USA 96: 238–241, 1999

    Google Scholar 

  45. Setiawan Y, Moore DE, Allen BJ: Selective uptake of boronated low-density lipoprotein in melanoma xenografts achieved by diet supplementation. Br J Cancer 74: 1705–1708, 1996

    Google Scholar 

  46. Gabel D: Present status and perspectives of boron neutron capture therapy. Radiother-Oncol 30: 199–205, 1994

    Google Scholar 

  47. Arteaga CL: The epidermal growth factor receptor: from mutant oncogene in nonhuman cancers to therapeutic target in human neoplasia. J Clin Oncol 19(18 Suppl): 32S–40S, 2001

    Google Scholar 

  48. Capala J, Barth RF, Bendayan M, Lauzon M, Adams DM, Soloway AH, Fenstermaker RA, Carlsson J: Boronated epidermal growth factor as a potential targeting agent for boron neutron capture therapy of brain tumors. Bioconjug Chem 7: 7–15, 1996

    Google Scholar 

  49. Carlsson J, Gedda L, Gronvik C, Hartman T, Lindstrom A, Lindstrom P, Lundqvist H, Lovqvist A, Malmqvist J, Olsson P, Essand M, Ponten J, Sjöberg S, Westermark B: Strategy for boron neutron capture therapy against tumor cells with over-expression of the epidermal growth factorreceptor. Int J Radiat Oncol Biol Phys 30: 105–115, 1994

    Google Scholar 

  50. Gedda L, Olsson P, Pontén J, Carlsson J: Development and in vitro studies of epidermal growth factor-dextran conjugates for boron neutron capture therapy. Bioconjug Chem 7: 584–591, 1996

    Google Scholar 

  51. Olsson P, Gedda L, Goike H, Liu L, Collins VP, Ponten J, Carlsson J: Uptake of a boronated epidermal growth factordextran conjugate in CHO xenografts with and without human EGF-receptor expression. Anticancer Drug Des 13: 279–289, 1998

    Google Scholar 

  52. Guan L, Wims LA, Kane RR, Smuckler MB, Morrison SL, Hawthorne MF: Homogeneous immunoconjugates for boron neutron-capture therapy: design, synthesis, and preliminary characterization. Proc Natl Acad Sci USA 95: 13206–13210, 1998

    Google Scholar 

  53. Liu L, Barth RF, Adams DM, Soloway AH, Reisfeld RA: Bispecific antibodies as targeting agents for boron neutron capture therapy of brain tumors. J Hematother 4: 477–483, 1995

    Google Scholar 

  54. Primus FJ, Pak RH, Richard Dickson KJ, Szalai G, Bolen JL Jr, Kane RR, Hawthorne MF: Bispecific antibody mediated targeting of nido-carboranes to human colon carcinoma cells. Bioconjug Chem 7: 532–535, 1996

    Google Scholar 

  55. Hamel W, Westphal M:Growth factors in gliomas revisited. Acta Neurochir (Wien). 142(2): 113–137, 2000

    Google Scholar 

  56. Mendelsohn J, Baselga J: The EGF receptor family as targets for cancer therapy. Oncogene 19: 6550–6565, 2000

    Google Scholar 

  57. Foulon CF, Reist CJ, Bigner DD, Zalutsky MR: Radioiodination via D-amino acid peptide enhances cellular retention and tumor xenograft targeting of an internalizing antiepidermal growth factor receptor variant III monoclonal antibody. Cancer Res 60: 4453–4460, 2000

    Google Scholar 

  58. Wikstrand CJ, Cokgor I, Sampson JH, Bigner DD: Monoclonal antibody therapy of human gliomas: current status and future approaches. Cancer Metastasis Rev 18: 451–464, 1999

    Google Scholar 

  59. Westphal M, Meima L, Szonyi E, Lofgren J, Meissner H, Hamel W, Nikolics K, Sliwkowski MX: Heregulins and the ErbB-2/3/4 receptors in gliomas. J Neuro-Oncol 35: 335–346, 1997

    Google Scholar 

  60. Hermanson M, Funa K, Koopmann J, Maintz D, Waha A, Westermark B, Heldin CH, Wiestler OD, Louis DN, von Deimling A, Nister M: Association of loss of heterozygosity on chromosome 17p with high plateletderived growth factor alpha receptor expression in human malignant gliomas. Cancer Res 56: 164–171, 1996

    Google Scholar 

  61. Westermark B, Heldin CH, Nister M: Platelet-derived growth factor in human glioma. Glia 15: 257–263, 1995

    Google Scholar 

  62. Akabani G, Cokgor I, Coleman RE, Gonzalez Trotter D, Wong TZ, Friedman HS, Friedman AH, Garcia-Turner A, Herndon JE, DeLong D, McLendon RE, Zhao XG, Pegram CN, Provenzale JM, Bigner DD, Zalutsky MR: Dosimetry and dose-response relationships in newly diagnosed patients with malignant gliomas treated with iodine-131–labeled anti-tenascin monoclonal antibody 81C6 therapy. Int J Radiat Oncol Biol Phys 46: 947–958, 2000

    Google Scholar 

  63. deHerder WW, Lamberts SW: Somatostatin and somatostatin analogues: diagnostic and therapeutic uses. Curr Opin Oncol 14: 53–57, 2002

    Google Scholar 

  64. Cavalla P, Schiffer D: Neuroendocrine tumors in the brain. Ann Oncol12(Suppl 2): S131–S134, 2001

    Google Scholar 

  65. Cervera P, Videau C, Viollet C, Petrucci C, Lacombe J, Winsky-Sommerer R, Csaba Z, Helboe L, Daumas-Duport C, Reubi JC, Epelbaum J: Comparison of somatostatin receptor expression in human gliomas and medulloblastomas. J Neuroendocrinol 14(6): 458–471, 2002

    Google Scholar 

  66. Merlo A, Hausmann O, Wasner M, Steiner P, Otte A, Jermann E, Freitag P, Reubi JC, Muller-Brand J, Gratzl O, Macke HR: Locoregional regulatory peptide receptor targeting with the diffusible somatostatin analogue 90Y-labeled DOTA0–D-Phe1–Tyr3–octreotide (DOTATOC): a pilot study in human gliomas. Clin Cancer Res 5(5): 1025–1033, 1999

    Google Scholar 

  67. Goldenberg DM: The role of radiolabeled antibodies in the treatment of non-Hodgkin's lymphoma: the coming of age of radioimmunotherapy. Crit Rev Oncol Hematol 39(1-2): 195–201, 2001

    Google Scholar 

  68. Goldenberg DM: Targeted therapy of cancer with radiolabeled antibodies. J Nucl Med 43(5): 693–713, 2002

    Google Scholar 

  69. Behr TM, Liersch T, Greiner-Bechert L, Griesinger F, Behe M, Markus PM, Gratz S, Angerstein C, Brittinger G, Becker H, Goldenberg DM, Becker W: Radioimmunotherapy of small-volume disease of metastatic colorectal cancer. Cancer 94: 1373–1381, 2002

    Google Scholar 

  70. Jager D, Jager E, Knuth A: Immune responses to tumour antigens: implications for antigen specific immunotherapy of cancer. J Clin Pathol 54: 669–674, 2001

    Google Scholar 

  71. Savelyeva L, Schwab M: Amplification of oncogenes revisited: from expression profiling to clinical application. Cancer Lett 167: 115–123, 2001

    Google Scholar 

  72. Frantz GD, Pham TQ, Peale FV Jr, Hillan KJ: Detection of novel gene expression in paraffin-embedded tissues by isotopic in situ hybridization in tissue microarrays. J Pathol 195: 87–96, 2001

    Google Scholar 

  73. Hoos A, Cordon-Cardo C: Tissue microarray profiling of cancer specimens and cell lines: opportunities and limitations. Lab Invest 81: 1331–1338, 2001

    Google Scholar 

  74. Maughan NJ, Lewis FA, Smith V: An introduction to arrays. J Pathol 195: 3–6, 2001

    Google Scholar 

  75. Bertram JS: The molecular biology of cancer. Mol Aspects Med 21: 167–223, 2000

    Google Scholar 

  76. Onyango P: Genomics and cancer. Curr Opin Oncol 14: 79–85, 2002

    Google Scholar 

  77. Ahmed NU, Ueda M, Ichihashi M: Increased level of c-erbB-2/neu/HER-2 protein in cutaneous squamous cell carcinoma. Br J Dermatol 136: 908–912, 1997

    Google Scholar 

  78. Molina MA, Saez R, Ramsey EE, Garcia-Barchino MJ, Rojo F, Evans AJ, Albanell J, Keenan EJ, Lluch A, Garcia-Conde J, Baselga J, Clinton GM:NH(2)-terminal truncated HER-2 protein but not full-length receptor is associated with nodal metastasis in human breast cancer. Clin Cancer Res 8: 347–353, 2002

    Google Scholar 

  79. Tewari KS, Kyshtoobayeva AS, Mehta RS, Yu IR, Burger RA, DiSaia PJ, Fruehauf JP: Biomarker conservation in primary and metastatic epithelial ovarian cancer. Gynecol Oncol 78: 130–136, 2000

    Google Scholar 

  80. Wester K, Sjostrom A, de la Torre M, Carlsson J, Malmstrom PU: HER-2-a possible target for therapy of metastatic urinary bladder carcinoma. Acta Oncol 41(3): 282–288, 2002

    Google Scholar 

  81. Lichtner RB, Menrad A, Sommer A, Klar U, Schneider MR: Signaling-inactive epidermal growth factor receptor/ligand complexes in intact carcinoma cells by quinazoline tyrosine kinase inhibitors. Cancer Res 61: 5790–5795, 2001

    Google Scholar 

  82. Adams GP, Schier R, McCall AM, Simmons HH, Horak EM, Alpaugh RK, Marks JD, Weiner LM: High affinity restricts the localization and tumor penetration of single-chain fv antibody molecules. Cancer Res 61: 4750–4755, 2001

    Google Scholar 

  83. . Behe M, Du J, Becker W, Behr T, Angerstein C, Marquez M, Hiltunen J, Nilsson S, Holmberg AR: Biodistribution, blood half-life, and receptor binding of a somatostatin-dextran conjugate. Med Oncol 18: 59–64, 2001

    Google Scholar 

  84. Carlsson J, Blomquist E, Gedda L, Liljegren A, Malmstrom PU, Sjostrom A, Sundin A, Westlin JE, Zhao Q, Tolmachev V, Lundqvist H: Conjugate chemistry and cellular processing of EGF-dextran. Acta Oncol 38: 313–321, 1999

    Google Scholar 

  85. Mattes MJ, Shih LB, Govindan SV, Sharkey RM, Ong GL, Xuan H, Goldenberg DM: The advantage of residualizing radiolabels for targeting B-cell lymphomas with a radiolabeled anti-CD22 monoclonal antibody. Int J Cancer 71: 429–435, 1997

    Google Scholar 

  86. Yasui L, Hughes A, DeSombre E: Relative biological effectiveness of accumulated 125IdU and 125Iestrogen decays in estrogen receptor-expressing MCF-7 human breast cancer cells. Radiat Res 155: 328–334, 2001

    Google Scholar 

  87. Kairemo KJ, Tenhunen M, Jekunen AP: Gene therapy using antisense oligodeoxynucleotides labeled with Augeremitting radionuclides. Cancer Gene Ther 5: 408–412, 1998

    Google Scholar 

  88. Mothersill C, Seymour C: Radiation-induced bystander effects: past history and future directions. Radiat Res 155: 759–767, 2001

    Google Scholar 

  89. Prise KM, Belyakov OV, Newman HC, Patel S, Schettino G, Folkard M, Michael BD: Non-targeted effects of radiation: bystander responses in cell and tissue models. Radiat Prot Dosimetry 99(1-4): 223–226, 2002

    Google Scholar 

  90. Xu L: Boron neutron capture therapy of human gastric cancer by boron-containing immunoliposomes under thermal neutron irradiation. Zhonghua Yi Xue Za Zhi 71(10): 568-571, 1991 (in Chinese) 59

    Google Scholar 

  91. Jain RK: Haemodynamic and transport barriers to the treatment of solid tumours. Int J Radiat Biol 60: 85–100, 1991

    Google Scholar 

  92. Pietras K, Ostman A, Sjoquist M, Buchdunger E, Reed RK, Heldin CH, Rubin K: Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors. Cancer Res 61: 2929–2934, 2001

    Google Scholar 

  93. Harris JM, Martin NE, Modi M:Pegylation: a novel process for modifying pharmacokinetics. Clin Pharmacokinet 40: 539–551, 2001

    Google Scholar 

  94. Lee LS, Conover C, Shi C, Whitlow M, Filpula D: Prolonged circulating lives of single-chain Fv proteins conjugated with polyethylene glycol: a comparison of conjugation chemistries and compounds. Bioconjug Chem 10: 973–981, 1999

    Google Scholar 

  95. Heppeler A, Froidevaux S, E berle AN, Maecke HR: Receptor targeting for tumor localisation and therapy with radiopeptides. Curr Med Chem 7: 971-994, 2000.

    Google Scholar 

  96. Kwekkeboom D, Krenning EP, de Jong M: Peptide receptor imaging and therapy. J Nucl Med 41: 1704–1713, 2000

    Google Scholar 

  97. Virgolini I, Traub T, Novotny C, Leimer M, Fuger B, Li SR, Patri P, Pangerl T, Angelberger P, Raderer M, Andreae F, Kurtaran A, Dudczak R: New trends in peptide receptor radioligands. Q J Nucl Med 45: 153–159, 2001

    Google Scholar 

  98. Adams GP, Schier R: Generating improved single-chain Fv molecules for tumor targeting. J Immunol Meth 231: 249–260, 1999

    Google Scholar 

  99. Maynard J, Georgiou G: Antibody engineering. Annu Rev Biomed Eng 2: 339–376, 2000

    Google Scholar 

  100. Strand SE, Ljungberg M, Tennvall J, Norrgren K, Garkavij M: Radio-immunotherapy dosimetry with special emphasis on SPECT quantification and extracorporeal immuno-adsorption. Med Biol Eng Comput 32: 551–561, 1994

    Google Scholar 

  101. Lundqvist H, Lubberink M, Tolmachev V, Lovqvist A, Sundin A, Beshara S, Bruskin A, Carlsson J, Westlin JE: Positron emission tomography and radioimmunotargeting - general aspects. Acta Oncol 38: 335–341, 1999

    Google Scholar 

  102. Smith DR, Chandra S, Barth RF, Yang W, Joel DD, Coderre JA: Quantitative imaging and microlocalization of boron-10 in brain tumors and infiltrating tumor cells by SIMS ion microscopy: relevance to neutron capture therapy. Cancer Res 61: 8179–8187, 2001

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biomedical Radiation Sciences, Rudbeck Laboratory, Uppsala University, Uppsala, Sweden

    Jörgen Carlsson, Erika Bohl Kullberg, Jacek Capala & Lars Gedda

  2. Department of Organic Chemistry, Uppsala University, Uppsala, Sweden

    Stefan Sjöberg

  3. Department of Physical Chemistry, Uppsala University, Uppsala, Sweden

    Katarina Edwards

Authors
  1. Jörgen Carlsson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Erika Bohl Kullberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jacek Capala
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Sjöberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katarina Edwards
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lars Gedda
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carlsson, J., Bohl Kullberg, E., Capala, J. et al. Ligand Liposomes and Boron Neutron Capture Therapy. J Neurooncol 62, 47–59 (2003). https://doi.org/10.1023/A:1023282818409

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023282818409

Search

Navigation