Profound prevention of experimental brain metastases of breast cancer by temozolomide in an MGMT-Dependent manner

Clinical Cancer Research

Volumn 20, Issue 10, 2014, Pages 2727-2739

  Palmieri, Diane ^a   Duchnowska, Renata ^e   Woditschka, Stephan ^a   Hua, Emily ^a   Qian, Yongzhen ^d   Biernat, Wojciech ^f   Sosinska Mielcarek, Katarzyna ^g   Gril, Brunilde ^a   Stark, Andreas M ^h   Hewitt, Stephen M ^b   Liewehr, David J ^c   Steinberg, Seth M ^c   Jassem, Jacek ^b,f   Steeg, Patricia S ^a  

^a Women's Malignancies Branch   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d SAIC FREDERICK INC   (United States)

^e MILITARY INSTITUTE OF MEDICINE   (Poland)

^f MEDICAL UNIVERSITY OF GDANSK   (Poland)

^g Regional Cancer Center   (Poland)

^h UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; TEMOZOLOMIDE; ALKYLATING AGENT; DACARBAZINE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN METASTASIS; BREAST CANCER; CANCER GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN TISSUE; LONG TERM SURVIVAL; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN NEOPLASMS; BREAST NEOPLASMS; DRUG ADMINISTRATION; DRUG SCREENING; GENETICS; IMMUNOHISTOCHEMISTRY; KAPLAN MEIER METHOD; MCF 7 CELL LINE; METABOLISM; NUDE MOUSE; PATHOLOGY; RNA INTERFERENCE; SECONDARY; TREATMENT OUTCOME; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BRAIN NEOPLASMS; BREAST NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MCF-7 CELLS; MICE; MICE, NUDE; RNA INTERFERENCE; TREATMENT OUTCOME; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84900992935     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-2588     Document Type: Article

References (51)

1. Brufsky A, Mayer M, Rugo H, Kaufman P, Tan-Chiu E, Tripathy D, et al. Central nervous system metastases in patients with Her2-positive metastatic breast cancer: Incidence, treatment, and survival in patients from registHER. Clin Cancer Res 2011;17:4834-43.
2. Bendell J, Domchek S, Burstein H, Harris L, Younger J, Kuter I, et al. Central nervous system metastases in women who receive trastuzumab- based therapy for metastatic breast carcinoma. Cancer 2003;97: 2972-7.
3. Lin N, Claus E, Sohl J, Razzak A, Arnout A, Winer E. Sites of distant recurrence and clinical outcomes in patients with metastatic triplenegative breast cancer. high incidence of central nervous system metastases. Cancer 2008;113:2638-45.
4. Steeg P, Camphausen K, Smith Q. Brain metastases as preventive and therapeutic targets. Nat Rev Cancer 2011;11:352-63.
5. Rosner D, Nemoto T, Lane W. Chemotherapy induces regression of brain metastases in breast carcinoma. Cancer 1986;58:832-9.
6. Boogerd W, Dalesio O, Bais E, van der Sande JJ. Response of brain metastases from breast cancer to systemic chemotherapy. Cancer 1992;69:972-80.
7. Rivera E, Meyers C, Groves M, Valero V, Francis D, Arun B, et al. Phase I study of capecitabine in combination with temozolomide in the treatment of patients with brain metastases of breast cancer. Cancer 2006;107:1348-54.
8. Melisko ME, Kunwar S, Prados M, Berger MS, Park JW. Brain metastases of breast cancer. Expert Rev Anticancer Ther 2005;5:253-68.
9. Walbert T, Gilbert M. The role of chemotherapy in the treatment of patients with brain metastases from solid tumors. Int J Clin Oncol 2009; 14:299-306.
10. Lin N, Carey L, Liu M, Younger J, Come S, Bullitt E, et al. Phase II trial of lapatinib for brain metastases in patients with HER2 breast cancer. J Clin Oncol 2006;24:503.
11. Lin N, Carey L, Liu M, Younger J, Come S, Ewend M, et al. Phase II trial of lapatinib for brain metasetases in patients with human epidermal growth factor receptor 2-positive breast cancer. Clin Cancer Res 2008;26:1993-9.
12. Lockman P, Mittapalli R, Taskar K, Rudraruju V, Gril B, Bohn K, et al. Heterogeneous blood-brain barrier permeability determines drug efficacy in mouse brain metastases of breast cancer. Clin Cancer Res 2010;16:5662-78.
13. Taskar K, Rudraraju V, Mittapali R,Samala R, Thorsheim H, Lockman J, et al. Lapatinib distribution in HER2 overexpressing experimental brain metastases of breast cancer. Pharm Res 2012;29:770-81.
14. Percy D, Ribot E, Chen Y, McFadden C, Simedrea C, Steeg PS, et al. In vivo characterization of changing blood-tumor barrier permeability in a mouse model of breast cancer metastasis: a complementary magnetic resonance imaging approach. Invest Radiol 2011;46: 718-25.
15. Muldoon L, Soussain C, Jahnke K, Johanson C, Siegal T, Smith Q, et al. Chemotherapy delivery issues in central nervous system malignancy: a reality check. J Clin Oncol 2007;25:2295-305.
16. Chamberlain M. Anticancer therapies and CNS relapse: overcoming blood-brain and blood-cerebrospinal fluid barrier impermeability. Expert Rev Neuother 2010;10:547-61.
17. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment, and trojan horses. Clin Cancer Res 2007;13:1663-74.
18. Lin N, Amiri-Kordestani L, Palmieri D, Liewehr D, Steeg P. CNS metastasis: old challenge, new frontiers. Clin Cancer Res 2013;19: 6404-18.
19. Brindley C, Antoni W, Newlands E. Plasma and tissue disposition of mitozolomide in mice. Br J Cancer 1986;53:91.
20. O'Reilly S, Newlands E, Glaser M, Brampton M, Rice-Edwards J, Illingworth R, et al. Temozolomide: a new oral cytotoxic chemotherapeutic agent with promising activity against primary brain tumours. Eur J Cancer 1993;29A:940-2.
21. Newlands E, Blackledge G, Slack J, Rustin G, Smith D, Stuart N, et al. Phase I trial of temozolomide (CCRG81045:M&B39831:NSC362856. Br J Cancer 1992;65:287-91.
22. Newlands E, Stevens M, Wedge S, Wheelhouse R, Brock C. Temozolomide: a review of its discovery, chemical properties, pre-clinical development and clinical trials. Cancer Trt Rev 1997;23:35-61.
23. Trudeau M,Crump M, Charpentier D, Yelle L, Bordeleau L, MatthewsS, et al. Temozolomide in metastatic breast cancer (MBC): a phase II trial of the National Cancer Institute of Canada-Clinical Trials Group (NCIC-CTG). Ann Oncol 2006;17:952-6.
24. Yoneda T, Williams P, Hiraga T, Niewolna M, Nishimura R. A bone seeking clone exhibits different biological properties from the MDAMB- 231 parentalhuman breast cancer cells and a brain-seeking cloe in vivo and in vitro. J Bone Mineral Res 2001;16:1486-95.
25. Palmieri D, Bronder JL, Herring JM, Yoneda T, Weil RJ, Stark AM, et al. Her-2 overexpression increases the metastatic outgrowth of breast cancer cells in the brain. Cancer Res 2007;67:4190-8.
26. Palmieri D, Lockman P, Thomas F, Hua E, Herring J, Hargrave E, et al. Vorinostat inhibits brain metastatic colonization in a model of triplenegative breast cancer. Clin Cancer Res 2009;15:6148-57.
27. Gril B, Palmieri D, Bronder JL, Herring JM, Vega-Valle E, Feigenbaum L, et al. Effect of lapatinib on the outgrowth of metastatic breast cancer cells to the brain. J Natl Cancer Inst 2008;100:1092-103.
28. Nagy P, Friedlander E, Tanner M, Kapanen A, Carraway K, Isola J, et al. Decreased accessibility and lack of activation of ErbB2 in JIMT-1, a herceptin-resistant, MUC4-expressing breast cancer cell line. Cancer Res 2005;65:473-82.
29. Ingold B, Schraml P, Heppner F, Moch H. Homogeneous MGMT immunoreactivity correlates with an unmethylated MGMT promoter status in brain metastases of various solid tumors. PloS ONE 2009;4:e4775.
30. Hirst T, Vesterinen H, Sena E, Egan K, Mcleod M, Whittle I. Systematic review and meta-Analysis of temozolomide in animal models of glioma: was clinical efficacy predicted? Br J Cancer 2013;108:64-71.
31. Donawho C, Luo Y, Luo Y, Penning T, Bauch J, Bouska J, et al. ABT- 888, an orally active Poly (ADP-Ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin Cancer Res 2007;13:2728-37.
32. Heyn C, Ronald J, MacKenzie L, MacDonald I, Chambers A, Rutt B, et al. In vivo magnetic resonance imaging of single cells in mouse brains with optical validation. Magn Reson Med 2006;55:23-9.
33. Koninki K, Barok M, Tanner M, Staff S, Pitkanen J, Hemmila P, et al. Multiple molecular mechanisms underlying trastuzumab and lapatinib resistance in JIMT-1 breast cancer cells. Cancer Lett 2010;294:211-9.
34. Dziadzusko R, Ardizzoni A, Postmus P, Smit E, Price A, Debruyne C, et al. Temozolomide in patients with advanced non-small cell lung cancer with and without brain metastases: a phase II study of the EORTC LUng Cancer Group (08965). Eur J Cancer 2003;39:1271-6.
35. Paul M, Summers Y, Calvert A, Rustin G, Brampton M, Thatcher N, et al. Effect of temozolomide on central nervous system relapse in patients with advanced melanoma. Melanoma Res 2002;12:175-8.
36. Siena S, Crino L, Danova M, DelPrete S, Cascinu S, Salvagni S, et al. Dose-dense temozolomide regimen for the treatment of brain metastases ofmelanoma, breast cancer, or lung cancer notamenable to surgery or radiosurgery:amulticenterphase II study.AnnOncol 2010;21:655-61.
37. Abrey L, Olson J, Raizer J, Mack M, Rodavirch A, Boutros D, et al. A phase II trial of temozolomide for patients with recurrent or progressive brain metastases. J Neurooncol 2001;53:259-65.
38. Larkin J, Hughes S, Beirne D, Patel P, Gibbens I, Bate S, et al.Aphase I/II study of lumustine and temozolomide in aptients with cerebral metastases from malignant melanoma. Br J Cancer 2007;96:44-8.
39. Christodoulou C, Bafaloukos D, Linardou H, Aravantinos G, Bamias A, Carina M, et al. Temozolomide (TMZ) combined with cisplatin (CDDP) in patientswith brain metastses of solid tumors: aHellenic Cooperative Oncology Group (HeCOG) phase II study,. J Neurooncol 2005;71: 61-5.
40. Azambuja Ed, Zardavas D, Lemort M, Rossari J, Moulin C, Buttice A, et al. Phase I trial combining temozolomide plus lapatinib for the treatment of brain metastases in patients with HER2-positive metastatic breast cancer: the LAPTEM trial. Ann Oncol 2013;24:1-5.
41. Verger E, Gil M, Yaya R, Vinolas N, Villa S, Pujol T, et al. Temozolomide and concomitant whole brain radiotherapy in patients with brain metastases: a phase II randomized trial. Int J Rad Oncol Biol Physics 2005;61:185-91.
42. Chua D, Krzakowski M, Chouaid C, Pallotta M, Martinez J, Gottfried M, et al. Whole-brain radiation therapy plus concomitant temozolomide for the treatment of brain metastases from non-small cell lung cancer: a randomized, open-label phase II study. Clin Lung Cancer 2010;11: 176-81.
43. Addeo R, Rosa CD, Faiola V, Leo L, Cennamo G, MOntella L, et al. Phase 2 trial of temozolomide using protracted low-dose and wholebrain radiotherapy for nonsmall cell lung cancer and breast cancer patients with brain metastases. Cancer 2008;113:2524-31.
44. Fitzgerald D, Palmieri D, Hua E, Hargrave E, Herring J, Qian Y, et al. Reactive glia are recruited by highly proliferative brain metastases of breast cancer and promote tumor cell colonization. Clin Exp Metast 2008;25:799-810.
45. Sharp J, Bouffet E, Stempak D, Gammon J, Stephens D, Johnston D, et al. A multi-centre Canadian pilot study of metronomic temozolomide combined with radiotherapy for newly diagnosed paediatric brainstem glioma. Eur J Cancer 2010;46:3271-9.
46. Pouratian N, Gasco J, Sherman J, Shaffrey M, Schiff D. Toxicity and efficacy of protracted low dose temozolomide for the treatment of low grade gliomas. J Neurooncol 2007;82:281-8.
47. Lashkari H, Saso S, Moreno L, Athanasiou T, Zacharoulis S. Using different schedules of temozolomide to treat low-grade gliomas: systematic review of their efficacy and toxicity. J Neurooncol 2011; 105:135-47.
48. Karayan-Tapon L, Quillien V, Guilhot J, Wagner M, Fromont G, Saikali S, et al. Prognostic value of O6-methylguanine-DNA methyltransferase status in glioblastoma patients, assessed by five different methods. J Neurooncol 2010;97:311-22.
49. Christmann M, Nagel G, Horn S, Krahn U, Wiewrodt D, Sommer C, et al. MGMT activity, promoter methylation and immunohistochemistry of pretreatment and recurrent malignant gliomas: a comparative study on astrocytoma and glioblastoma. Int J Cancer 2010; 127:2106-18.
50. Slotman B, Faive-Finn C, Kramer G, Rankin E, Snee M, Hatton M, et al. Prophylactic cranial irradiation in extensive small-cell lung cancer. New Engl J Med 2007;357:664-72.
51. Steeg P. The right trials. Nature 2012;485:S58-9.