Treatment of experimental human breast cancer and lung cancer brain metastases in mice by macitentan, a dual antagonist of endothelin receptors, combined with paclitaxel

Neuro-Oncology

Volumn 18, Issue 4, 2016, Pages 486-496

  Lee, Ho Jeong ^a   Hanibuchi, Masaki ^a   Kim, Sun Jin ^a   Yu, Hyunkyung ^a   Kim, Mark Seungwook ^a   He, Junqin ^a   Langley, Robert R ^a   Lehembre, François ^b   Regenass, Urs ^b   Fidler, Isaiah J ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b ACTELION PHARMACEUTICALS LTD   (Switzerland)

Author keywords

astrocytes; brain metastases; endothelial cells; endothelin; macitentan

Indexed keywords

BCL2 RELATED PROTEIN L1; ENDOTHELIN RECEPTOR; GLUTATHIONE TRANSFERASE A5; MACITENTAN; MITOGEN ACTIVATED PROTEIN KINASE; PACLITAXEL; PEPTIDES AND PROTEINS; PROTEIN KINASE B; TRANSCRIPTION FACTOR TWIST; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; PYRIMIDINE DERIVATIVE; SULFONAMIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN METASTASIS; BREAST CANCER BRAIN METASTASIS; BREAST CANCER CELL LINE; CANCER CELL; CANCER COMBINATION CHEMOTHERAPY; CANCER SURVIVAL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; LUNG CANCER BRAIN METASTASIS; LUNG CANCER CELL LINE; MDA MB 231 CANCER LINE; METASTASIS FREE SURVIVAL; MITOSIS INHIBITION; MOUSE; NONHUMAN; OVERALL SURVIVAL; PC 14 CELL LINE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TUMOR ASSOCIATED ENDOTHELIAL CELL; 3T3 CELL LINE; ANIMAL; BREAST NEOPLASMS; CELL PROLIFERATION; CHEMISTRY; COMBINATION DRUG THERAPY; COMPARATIVE STUDY; DRUG EFFECTS; DRUG SCREENING; ENZYME IMMUNOASSAY; LUNG NEOPLASMS; METABOLISM; NUDE MOUSE; PATHOLOGY; SECONDARY; TUMOR CELL CULTURE;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BREAST NEOPLASMS; CELL PROLIFERATION; DRUG THERAPY, COMBINATION; FEMALE; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MICE; MICE, NUDE; NIH 3T3 CELLS; PACLITAXEL; PYRIMIDINES; RECEPTORS, ENDOTHELIN; SULFONAMIDES; TUMOR CELLS, CULTURED; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84966533797     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/now037     Document Type: Article

References (48)

1. Gavrilovic IT, Posner JB. Brain metastases: epidemiology and pathophysiology. J Neurooncol. 2005;75(1):5-14.
2. Lassman AB, DeAngelis LM. Brain metastases. Neurol Clin. 2003;21(1):1-23.
3. Cruz-Munoz W, Kerbel RS. Preclinical approaches to study the biology and treatment of brain metastases. Semin Cancer Biol. 2011;21(2):123-130.
4. Owonikoko TK, Arbiser J, Zelnak A, et al. Current approaches to the treatment of metastatic brain tumours. Nat Rev Clin Oncol. 2014;11(4):203-222.
5. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res. 2007;13(6):1663-1674.
6. Steeg PS, Camphausen KA, Smith QR. Brain metastases as preventive and therapeutic targets. Nat Rev Cancer. 2011;11(5):352-363.
7. Cairncross JG, Kim JH, Posner JB. Radiation therapy for brain metastases. Ann Neurol. 1980;7(6):529-541.
8. Eichler AF, Loeffler JS. Multidisciplinary management of brain metastases. Oncologist. 2007;12(7):884-898.
9. Clayton AJ, Danson S, Jolly S, et al. Incidence of cerebral metastases in patients treated with trastuzumab for metastatic breast cancer. Br J Cancer. 2004;91(4):639-643.
10. Daryanani D, Plukker JT, de Jong MA, et al. Increased incidence of brain metastases in cutaneous head and neck melanoma. Melanoma Res. 2005;15(2):119-124.
11. Kim SW, Choi HJ, Lee HJ, et al. Role of the endothelin axis in astrocyte- and endothelial cell-mediated chemoprotection of cancer cells. Neuro Oncol. 2014;16(12):585-598.
12. Kedzierski RM, Yanagisawa M. Endothelin system: the double-edged sword in health and disease. Ann Rev Pharmacol Toxicol. 2001;41:851-876.
13. Yanagisawa M, Kurihara H, Kimura S, et al. A novel potent vasoconstrictor peptide produced by vascular endothelial cells. Nature. 1988;332(6163):411-415.
14. Rosano L, Spinella F, Bagnato A. Endothelin-1 in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer. 2013;13(9):637-651.
15. Wulfing P, Diallo R, Kersting C, et al. Expression of endothelin-1, endothelin-A, and endothelin-B receptor in human breast cancer and correlation with long-term follow-up. Clin Cancer Res. 2003;9(11):4125-4131.
16. Wulfing P, Kersting C, Tio J, et al. Endothelin-1-, endothelin-A-, and endothelin-B-receptor expression is correlated with vascular endothelial growth factor expression and angiogenesis in breast cancer. Clin Cancer Res. 2004;10(7):2393-2400.
17. Wulfing P, Tio J, Kersting C, et al. Expression of endothelin-A-receptor predicts unfavourable response to neoadjuvant chemotherapy in locally advanced breast cancer. Br J Cancer. 2004;91(3):434-440.
18. Boldrini L, Gisfredi S, Ursino S, et al. Expression of endothelin-1 is related to poor prognosis in non-small cell lung carcinoma. Eur J Cancer. 2005;41(18):2828-2835.
19. Cruz-Munoz W, Jaramillo ML, Man S, et al. Roles for endothelin receptor B and BCL2A1 in spontaneous CNS metastasis of melanoma. Cancer Res. 2012;72(19):4909-4919.
20. Liu Y, Ye F, Yamada K, et al. Autocrine endothelin-3/endothelin receptor B signaling maintains cellular and molecular properties of glioblastoma stem cells. Mol Cancer Res. 2011;9(12):1668-1685.
21. Zhang M, Olsson Y. Reactions of astrocytes and microglial cells around hematogenous metastases of the human brain. Expression of endothelin-like immunoreactivity in reactive astrocytes and activation of microglial cells. J Neuro Sci. 1995;134:26-32.
22. Yano S, Shinohara H, Herbst RS, et al. Production of experimental malignant pleural effusions is dependent on invasion of the pleura and expression of vascular endothelial growth factor/vascular permeability factor by human lung cancer cells. Am J Pathol. 2000;157(6):1893-1903.
23. Langley RR, Fan D, Guo L, et al. Generation of an immortalized astrocyte cell line from H-2Kb-tsA58 mice to study the role of astrocytes in brain metastasis. Int J Oncol. 2009;35(4):665-672.
24. Langley RR, Ramirez KM, Tsan RZ, et al. Tissue-specific microvascular endothelial cell lines from H-2K(b)-tsA58 mice for studies of angiogenesis and metastasis. Cancer Res. 2003;63(11):2971-2976.
25. Rebhun RB, Langley RR, Yokoi K, Fan D, Gershenwald JE, et al. Targeting receptor tyrosine kinase on lymphatic endothelial cells for the therapy of colon cancer lymph node metastasis. Neoplasia. 2006;8(9):747-757.
26. Kim SJ, Kim JS, Kim SW, et al. Macitentan (ACT-064992), a tissue-targeting endothelin receptor antagonist, enhances therapeutic efficacy of paclitaxel by modulating survival pathways in orthotopic modles of metastatic human ovarian cancer. Neoplasia. 200;13(2):167-179.
27. Weidner N, Semple JP, Welch WR, Folkman J. Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma. N Engl J Med. 1991;324(1):1-8.
28. Kim SJ, Kim JS, Park ES, et al. Astrocytes upregulate survival genes in tumor cells and induce protection from chemotherapy. Neoplasia. 2011;13(2):286-298.
29. Gatfield J, Grandjean CM, Sasse T, Cozel M, Nayler O. Slow receptor dissociation kinetics differentiate macitentan from other endothelin receptor antagonists in pulmonary arterial smooth muscle cells. PloS One. 2012;7(10):1-11.
30. Iglarz M, Binkert C, Morrison K, et al. Pharmacology of macitentan, an orally active tissue-targeting dual endothelin receptor antagonist. J Pharm Exp Ther. 2008;327(3):736-745.
31. Dhillon S. Macitentan: a review of its use in patients with pulmonary arterial hypertension. Drugs. 2014;74(13):1495-1507.
32. Kholdani CA, Fares WH, Trow TK. Macitentan for the treatment of pulmonary arterial hypertension. Vasc Health Risk Manag. 2014;10:665-673.
33. Rosano L, Di Castro V, Spinella F, et al. ZD4054, a specific antagonist of the endothelin-A receptor, inhibits tumor growth and enhances paclitaxel activity in human ovarian carcinoma in vitro and in vivo. Mol Cancer Ther. 2007;6(7):2003-2011.
34. Shichiri M, Kato H, Marumo F, Hirata Y. Endothelin-1 as an autocrine/paracrine apoptosis survival factor for endothelial cells. Hypertension. 1997;30(5):1198-1203.
35. Cifarelli V, Lee S, Kim DH, et al. FOXO1 mediates the autocrine effect of endothelin-1 on endothelial cell survival. Mol Endocrinol. 2012;26(7):1213-1224.
36. Phuphanich S, Carson KA, Grossman SA, et al. Phase I safety study of escalating doses of atrasentan in adults with recurrent malignant glioma. Neuro Oncol. 2008;10(4):617-623.
37. Gilbert MR, Dignam JJ, Armstron TS, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):699-708.
38. de Groot JF, Fuller G, Kumar AJ, et al. Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro Oncol. 2010;12(3):233-242.
39. Robinson ES, Khankin EV, Karumanchi SA, Humphreys BD. Hypertension induced by vascular endothelial growth factor signaling pathway inhibition: mechanisms and potential use as a biomarker. Semin Nephrol. 2010;30(6):591-601.
40. Kappers MH, de Beer VJ, Zhou Z, et al. Sunitinib-induced systemic vasoconstriction in swine is endothelin mediated and does not involve nitric oxide or oxidative stress. Hypertension. 2012;59(1):151-157.
41. Kappers MH, Smedts FM, Horn T, et al. The vascular endothelial growth factor receptor inhibitor sunitinib causes a preeclampsia-like syndrome with activation of the endothelin system. Hypertension. 2011;58(2):295-302.
42. Lockman PR, Mittapalli RK, Taskar KS, et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res. 2010;16(23):5664-5678.
43. Kim SJ, Lee HJ, Kim MS, et al. Macitentan, a dual endothelin receptor antagonist, in combination with temozolomide leads to glioblastoma regression and long-term survival in mice. Clin Cancer Res. 2015;21(20):4630-4641.
44. Lorger M, Felding-Habermann B. Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis. Am J Pathol. 2010;176(6):2958-2971.
45. Kienast Y, von Baumgarten L, Fuhrmann M, et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med. 2010;16(1):116-122.
46. Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007;11(1):69-82.
47. Borovski T, Beke P, van Tellingen O, et al. Therapy-resistant tumor microvascular endothelial cells contribute to treatment failure in glioblastoma multiforme. Oncogene. 2013;32(12):1539-1548.
48. Carbonell WS, Ansorge O, Sibson N, Muschel R. The vascular basement membrane as "soil" in brain metastasis. PloS One. 2009;4(6):e5857.