PDE5 inhibitors enhance tumor permeability and efficacy of chemotherapy in a rat brain tumor model

Brain Research

Volumn 1230, Issue , 2008, Pages 290-302

  Black, Keith L ^a   Yin, Dali ^a   Ong, John M ^a   Hu, Jinwei ^a   Konda, Bindu M ^a   Wang, Xiao ^a   Ko, MinHee K ^a   Bayan, Jennifer Ann ^a   Sacapano, Manuel R ^a   Espinoza, Andreas ^a   Irvin, Dwain K ^a   Shu, Yan ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

Author keywords

Blood brain barrier; Blood brain tumor barrier; Brain tumor; Drug delivery; Drug transport; PDE5 inhibitor

Indexed keywords

BRADYKININ; CYCLIC GMP; DOXORUBICIN; IBERIOTOXIN; PHOSPHODIESTERASE; PHOSPHODIESTERASE 10; PHOSPHODIESTERASE I; PHOSPHODIESTERASE V; PHOSPHODIESTERASE V INHIBITOR; SILDENAFIL; UNCLASSIFIED DRUG; VARDENAFIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BLOOD BRAIN BARRIER; BLOOD BRAIN TUMOR BARRIER; BRAIN CAPILLARY; BRAIN TUMOR; CANCER CHEMOTHERAPY; CANCER SURVIVAL; CAPILLARY PERMEABILITY; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG PENETRATION; DRUG POTENTIATION; DRUG TRANSPORT; GLIOSARCOMA; HUMAN; HUMAN CELL; MONOTHERAPY; NONHUMAN; PERMEABILITY BARRIER; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TREATMENT OUTCOME;

RATTUS;

EID: 54049086905     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2008.06.122     Document Type: Article

References (50)

1. Anhoutte, P.M., Auch-Schwelk, W., Biondi, M.L., Lorenz, R.R., Schini, V.B., Vida, M.J., 1989. Why are converting enzyme inhibitors vasodilators? Br. J. Clin. Pharmacol. 28, 95S-104S.
2. Balmaceda, C., 1998. Advances in brain tumor chemosensitivity. Curr. Opin. Oncol. 10, 194-200.
3. Beavo, J.A., 1995. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 75, 725-748.
4. Bentley, J.K., Beavo, J.A., 1992. Regulation and function of cyclic nucleotides. Curr. Opin. Cell. Biol. 4, 233-240.
5. Black, K.L., 1995. Biochemical opening of the blood-brain barrier. Adv. Drug. Delivery Rev. 15, 37-52.
6. Black, K.L., 1996. The blood-brain barrier. In: Youmans, J.R. (Ed.), Neurological Surgery. W.B. Saunders Co., Philadelphia, pp. 482-490.
7. Black, K.L., Cloughesy, T., Huang, S.C., Gobin, Y.P., Zhou, Y., Grous, J., Nelson, G., Farahani, K., Hoh, C.K., Phelps, M., 1997. Intracarotid infusion of RMP-7, a bradykinin analog, and transport of gallium-68 ethylenediamine tetraacetic acid into human gliomas. J. Neurosurg. 86, 603-609.
8. Brandes, A.A., Fiorentino, M.V., 1996. The role of chemotherapy in recurrent malignant gliomas: an overview. Cancer Invest. 14, 551-559.
9. Broadwell, R.D., Charlton, H.M., Balin, B.J., Salcman, M., 1987. Angioarchitecture of the CNS, pituitary gland, and intracerebral grafts revealed with peroxidase cytochemistry. J. Comp. Neurol. 260, 47-62.
10. Chan, P.H., Fishman, R.A., Caronna, J., Schmidley, J.W., Prioleau, G., Lee, J., 1983. Induction of brain edema following intracerebral injection of arachidonic acid. Ann. Neurol. 13, 625-632.
11. Corbin, J.D., Francis, S.H., 1999. Cyclic GMP phosphodiesterase-5: target of sildenafil. J. Biol. Chem. 274, 13729-13732.
12. Corbin, J.D., Beasley, A., Blount, M.A., Francis, S.H., 2004. Vardenafil: structural basis for higher potency over sildenafil in inhibiting cGMP-specific phosphodiesterase-5 (PDE5). Neurochem. Int. 45, 859-863.
13. Cornford, E.M., Hyman, S., 2005. Localization of brain endothelial luminal and abluminal transporters with immunogold electron microscopy. NeuroRx 2, 27-43.
14. Davis, F.G., Freels, S., Grutsch, J., Barlas, S., Brem, S., 1998. Survival rates in patients with primary malignant brain tumors stratified by patient age and tumor histological type: an analysis based on Surveillance, Epidemiology, and End Results (SEER) data, 1973-1991. J. Neurosurg. 88, 1-10.
15. Erdos, E.G., 1990. Some old and some new ideas on kinin metabolism. J. Cardiovasc. Pharmacol. 15 (Suppl 6), S20-S24.
16. Frank, P.G., Woodman, S.E., Park, D.S., Lisanti, M.P., 2003. Caveolin, caveolae, and endothelial cell function. Arterioscler. Thromb. Vasc. Biol. 23, 1161-1168.
17. Groothuis, D.R., 2000. The blood-brain and blood-tumor barriers: a review of strategies for increasing drug delivery. Neuro. Oncol. 2, 45-59.
18. Hashizume, K., Black, K.L., 2002. Increased endothelial vesicular transport correlates with increased blood-tumor barrier permeability induced by bradykinin and leukotriene C4. J. Neuropathol. Exp. Neurol. 61, 725-735.
19. Hau, P., Fabel, K., Baumgart, U., Rummele, P., Grauer, O., Bock, A., Dietmaier, C., Dietmaier, W., Dietrich, J., Dudel, C., Hubner, F., Jauch, T., Drechsel, E., Kleiter, I., Wismeth, C., Zellner, A., Brawanski, A., Steinbrecher, A., Marienhagen, J., Bogdahn, U., 2004. Pegylated liposomal doxorubicin-efficacy in patients with recurrent high-grade glioma. Cancer 100, 1199-1207.
20. Ignarro, L.J., Byrns, R.E., Wood, K.S., 1987. Endothelium-dependent modulation of cGMP levels and intrinsic smooth muscle tone in isolated bovine intrapulmonary artery and vein. Circ. Res. 60, 82-92.
21. Inamura, T., Black, K.L., 1994. Bradykinin selectively opens blood-tumor barrier in experimental brain tumors. J. Cereb. Blood Flow Metab. 14, 862-870.
22. Inamura, T., Nomura, T., Ikezaki, K., Fukui, M., Pollinger, G., Black, K.L., 1994. Intracarotid histamine infusion increases blood tumour permeability in RG2 glioma. Neurol. Res. 16, 125-128.
23. Liu, Y., Hashizume, K., Chen, Z., Samoto, K., Ningaraj, N., Asotra, K., Black, K.L., 2001. Correlation between bradykinin-induced blood-tumor barrier permeability and B2 receptor expression in experimental brain tumors. Neurol. Res. 23, 379-387.
24. Matsukado, K., Inamura, T., Nakano, S., Fukui, M., Bartus, R.T., Black, K.L., 1996. Enhanced tumor uptake of carboplatin and survival in glioma-bearing rats by intracarotid infusion of bradykinin analog, RMP-7. Neurosurgery 39, 125-133 discussion 133-134.
25. Matsukado, K., Sugita, M., Black, K.L., 1998. Intracarotid low dose bradykinin infusion selectively increases tumor permeability through activation of bradykinin B2 receptors in malignant gliomas. Brain Res. 792, 10-15.
26. Mendel, D.B., Laird, A.D., Xin, X., Louie, S.G., Christensen, J.G., Li, G., Schreck, R.E., Abrams, T.J., Ngai, T.J., Lee, L.B., Murray, L.J., Carver, J., Chan, E., Moss, K.G., Haznedar, J.O., Sukbuntherng, J., Blake, R.A., Sun, L., Tang, C., Miller, T., Shirazian, S., McMahon, G., Cherrington, J.M., 2003. In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship. Clin. Cancer Res. 9, 327-337.
27. Menniti, F.S., Faraci, W.S., Schmidt, C.J., 2006. Phosphodiesterases in the CNS: targets for drug development. Nat. Rev. Drug. Discov. 5, 660-670.
28. Murad, F., 1994. Regulation of cytosolic guanylyl cyclase by nitric oxide: the NO-cyclic GMP signal transduction system. Adv. Pharmacol. 26, 19-33.
29. Nakano, S., Matsukado, K., Black, K.L., 1996. Increased brain tumor microvessel permeability after intracarotid bradykinin infusion is mediated by nitric oxide. Cancer Res. 56, 4027-4031.
30. Neuwelt, E.A., Barnett, P.A., Bigner, D.D., Frenkel, E.P., 1982. Effects of adrenal cortical steroids and osmotic blood-brain barrier opening on methotrexate delivery to gliomas in the rodent: the factor of the blood-brain barrier. Proc. Natl. Acad. Sci. U. S. A. 79, 4420-4423.
31. Ningaraj, N.S., Rao, M., Hashizume, K., Asotra, K., Black, K.L., 2002. Regulation of blood-brain tumor barrier permeability by calcium-activated potassium channels. J. Pharmacol. Exp. Ther. 301, 838-851.
32. Ningaraj, N.S., Rao, M.K., Black, K.L., 2003. Adenosine 5¢-triphosphate-sensitive potassium channel-mediated blood-brain tumor barrier permeability increase in a rat brain tumor model. Cancer Res. 63, 8899-8911.
33. Nishio, S., Ohnishi, A., Fukui, M., Tateishi, J., Kitamura, K., 1983. Peripheral nerve lesions associated with cis-diamminedichloroplatinum (II) treatment - study of a case with yolk sac tumor of the pineal body. Rinsho. Shinkeigaku. 23, 655-660.
34. Nomura, T., Inamura, T., Black, K.L., 1994. Intracarotid infusion of bradykinin selectively increases blood-tumor permeability in 9L and C6 brain tumors. Brain Res. 659, 62-66.
35. Pizard, A., Blaukat, A., Muller-Esterl, W., Alhenc-Gelas, F., Rajerison, R.M., 1999. Bradykinin-induced internalization of the human B2 receptor requires phosphorylation of three serine and two threonine residues at its carboxyl tail. J. Biol. Chem. 274, 12738-12747.
36. Predescu, D., Vogel, S.M., Malik, A.B., 2004. Functional and morphological studies of protein transcytosis in continuous endothelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 287, L895-L901.
37. Rehemtulla, A., Stegman, L.D., Cardozo, S.J., Gupta, S., Hall, D.E., Contag, C.H., Ross, B.D., 2000. Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2, 491-495.
38. Schnitzer, J.E., Oh, P., 1994. Albondin-mediated capillary permeability to albumin. Differential role of receptors in endothelial transcytosis and endocytosis of native and modified albumins. J. Biol. Chem. 269, 6072-6082.
39. Sharma, R., Lovell, H.B., Wiegmann, T.B., Savin, V.J., 1992. Vasoactive substances induce cytoskeletal changes in cultured rat glomerular epithelial cells. J. Am. Soc. Nephrol. 3, 1131-1138.
40. Sheikov, N., McDannold, N., Jolesz, F., Zhang, Y.Z., Tam, K., Hynynen, K., 2006. Brain arterioles show more active vesicular transport of blood-borne tracer molecules than capillaries and venules after focused ultrasound-evoked opening of the blood-brain barrier. Ultrasound Med. Biol. 32, 1399-1409.
41. Smith, P.J., Soues, S., 1994. Multilevel therapeutic targeting by topoisomerase inhibitors. Br. J. Cancer. Suppl. 23, S47-51.
42. Steiniger, S.C., Kreuter, J., Khalansky, A.S., Skidan, I.N., Bobruskin, A.I., Smirnova, Z.S., Severin, S.E., Uhl, R., Kock, M., Geiger, K.D., Gelperina, S.E., 2004. Chemotherapy of glioblastoma in rats using doxorubicin-loaded nanoparticles. Int. J. Cancer 109, 759-767.
43. Stewart, P.A., Hayakawa, K., Farrell, C.L., Del Maestro, R.F., 1987. Quantitative study of microvessel ultrastructure in human peritumoral brain tissue. Evidence for a blood-brain barrier defect. J. Neurosurg. 67, 697-705.
44. Stewart, P.A., Hayakawa, K., Farrell, C.L., 1994. Quantitation of blood-brain barrier ultrastructure. Microsc. Res. Tech. 27, 516-527.
45. Sugita, M., Black, K.L., 1998. Cyclic GMP-specific phosphodiesterase inhibition and intracarotid bradykinin infusion enhances permeability into brain tumors. Cancer. Res. 58, 914-920.
46. Tsuboi, Y., Takahashi, M., Ishikawa, Y., Okada, H., Yamada, T., 1998. Elevated bradykinin and decreased carboxypeptidase R as a cause of hypotension during tryptophan column immunoabsorption therapy. Ther. Apher. 2, 297-299.
47. Voulgaris, S., Partheni, M., Karamouzis, M., Dimopoulos, P., Papadakis, N., Kalofonos, H.P., 2002. Intratumoral doxorubicin in patients with malignant brain gliomas. Am. J. Clin. Oncol. 25, 60-64.
48. Walter, K.A., Tamargo, R.J., Olivi, A., Burger, P.C., Brem, H., 1995. Intratumoral chemotherapy. Neurosurgery 37, 1128-1145.
49. Wolff, J.E., Trilling, T., Molenkamp, G., Egeler, R.M., Jurgens, H., 1999. Chemosensitivity of glioma cells in vitro: a meta analysis. J. Cancer. Res. Clin. Oncol. 125, 481-486.
50. Zhang, R., Wang, Y., Zhang, L., Zhang, Z., Tsang, W., Lu, M., Chopp, M., 2002. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 33, 2675-2680.