Trastuzumab distribution in an in-vivo and in-vitro model of brain metastases of breast cancer

Oncotarget

Volumn 8, Issue 48, 2017, Pages 83734-83744

  Terrell Hall, Tori B ^a   Nounou, Mohamed Ismail ^b,c   El Amrawy, Fatema ^b   Griffith, Jessica I G ^a   Lockman, Paul R ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b Alexandria University Faculty of Pharmacy   (Egypt)

^c UNIVERSITY OF SAINT JOSEPH   (United States)

Author keywords

Blood brain barrier; Drug delivery; Metastasis; Microfluidic device; Permeability

Indexed keywords

DIHYDRORHODAMINE 123; IODINE 125; TRASTUZUMAB;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BLOOD TUMOR BARRIER; BRAIN METASTASIS; BREAST CANCER; CANCER CELL; CANCER MODEL; CANCER SIZE; CELL COMPARTMENTALIZATION; CELL GROWTH; CELL HETEROGENEITY; CELL LINE; CELL STRESS; COCULTURE; CONTROLLED STUDY; CTX TNA2 CELL LINE; DOSE RESPONSE; DRUG BLOOD LEVEL; DRUG DISTRIBUTION; DRUG PENETRATION; DRUG UPTAKE; FEMALE; HEMATOLOGICAL PARAMETERS; HOMOZYGOTE; HUMAN; HUMAN CELL; HUMAN EPIDERMAL GROWTH FACTOR RECEPTOR 2 POSITIVE BREAST CANCER; IN VITRO STUDY; IN VIVO STUDY; MET 1 CELL LINE; METASTATIC BREAST CANCER; MICROFLUIDIC ANALYSIS; MOUSE; NONHUMAN; ONCOLOGICAL PARAMETERS; PERMEABILITY BARRIER; RAT; SHEAR STRESS; TISSUE DISTRIBUTION; UMBILICAL VEIN ENDOTHELIAL CELL;

EID: 85030973110     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.19634     Document Type: Article

References (59)

1. Colzani E, Liljegren A, Johansson AL, Adolfsson J, Hellborg H, Hall PF, Czene K. Prognosis of patients with breast cancer: causes of death and effects of time since diagnosis, age, and tumor characteristics. J Clin Oncol. 2011; 29:4014-4021
2. Zimm S, Wampler GL, Stablein D, Hazra T, Young HF. Intracerebral metastases in solid-tumor patients: natural history and results of treatment. Cancer. 1981; 48:384-394
3. Lin NU. Breast cancer brain metastases: new directions in systemic therapy. Ecancermedicalscience. 2013; 7:307
4. Palmieri D, Smith QR, Lockman PR, Bronder J, Gril B, Chambers AF, Weil RJ, Steeg PS. Brain metastases of breast cancer. Breast Dis. 2006; 26:139-147
5. Yeh RH, Yu JC, Chu CH, Ho CL, Kao HW, Liao GS, Chen HW, Kao WY, Yu CP, Chao TY, Dai MS. Distinct MR imaging features of triple-negative breast cancer with brain metastasis. J Neuroimaging. 2015; 25:474-481
6. Steeg PS, Camphausen KA, Smith QR. Brain metastases as preventive and therapeutic targets. Nat Rev Cancer. 2011; 11:352-363
7. Park YH, Park MJ, Ji SH, Yi SY, Lim DH, Nam DH, Lee JI, Park W, Choi DH, Huh SJ, Ahn JS, Kang WK, Park K, Im YH. Trastuzumab treatment improves brain metastasis outcomes through control and durable prolongation of systemic extracranial disease in HER2-overexpressing breast cancer patients. Br J Cancer. 2009; 100:894-900
8. Sanchez-Munoz A, Plata-Fernandez Y, Fernandez M, Jaen-Morago A, Fernandez-Navarro M, de la Torre-Cabrera C, Ramirez-Tortosa C, Pascual J, Alba E, Sanchez-Rovira P. Tumor histological subtyping determined by hormone receptors and HER2 status defines different pathological complete response and outcome to dose-dense neoadjuvant chemotherapy in breast cancer patients. Clin Transl Oncol. 2013
9. Vaz-Luis I, Ottesen RA, Hughes ME, Marcom PK, Moy B, Rugo HS, Theriault RL, Wilson J, Niland JC, Weeks JC, Lin NU. Impact of hormone receptor status on patterns of recurrence and clinical outcomes among patients with human epidermal growth factor-2-positive breast cancer in the National Comprehensive Cancer Network: a prospective cohort study. Breast Cancer Res. 2012; 14:R129
10. Bendell JC, Domchek SM, Burstein HJ, Harris L, Younger J, Kuter I, Bunnell C, Rue M, Gelman R, Winer E. Central nervous system metastases in women who receive trastuzumab-based therapy for metastatic breast carcinoma. Cancer. 2003; 97:2972-2977
11. Leyland-Jones B. Human epidermal growth factor receptor 2-positive breast cancer and central nervous system metastases. J Clin Oncol. 2009; 27:5278-5286
12. Palmieri D, Bronder JL, Herring JM, Yoneda T, Weil RJ, Stark AM, Kurek R, Vega-Valle E, Feigenbaum L, Halverson D, Vortmeyer AO, Steinberg SM, Aldape K, Steeg PS. Her-2 overexpression increases the metastatic outgrowth of breast cancer cells in the brain. Cancer Res. 2007; 67:4190-4198
13. Clayton AJ, Danson S, Jolly S, Ryder WDJ, Burt PA, Stewart AL, Wilkinson PM, Welch RS, Magee B, Wilson G, Howell A, Wardley AM. Incidence of cerebral metastases in patients treated with trastuzumab for metastatic breast cancer. Br J Cancer. 2004; 91:639-643
14. Witzel I, Oliveira-Ferrer L, Pantel K, Muller V, Wikman H. Breast cancer brain metastases: biology and new clinical perspectives. Breast Cancer Res. 2016; 18:8
15. Brufsky AM, Mayer M, Rugo HS, Kaufman PA, Tan-Chiu E, Tripathy D, Tudor IC, Wang LI, Brammer MG, Shing M, Yood MU, Yardley DA. Central nervous system metastases in patients with HER2-positive metastatic breast cancer: incidence, treatment, and survival in patients from registHER. Clin Cancer Res. 2011; 17:4834-4843
16. Ballabh P, Braun A, Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol Dis. 2004; 16:1-13
17. Cook LJ, Freedman J. (2011). Brain Tumors: Rosen Pub
18. Dauchy S, Miller F, Couraud PO, Weaver RJ, Weksler B, Romero IA, Scherrmann JM, De Waziers I, Decleves X. Expression and transcriptional regulation of ABC transporters and cytochromes P450 in hCMEC/D3 human cerebral microvascular endothelial cells. Biochem Pharmacol. 2009; 77:897-909
19. Abbott NJ, Patabendige AA, Dolman DE, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010; 37:13-25
20. Rip J, Schenk GJ, de Boer AG. Differential receptormediated drug targeting to the diseased brain. Expert Opin Drug Deliv. 2009; 6:227-237
21. Abbott NJ, Friedman A. Overview and introduction: the blood-brain barrier in health and disease. Epilepsia. 2012; 53:1-6
22. van Tellingen O, Yetkin-Arik B, de Gooijer MC, Wesseling P, Wurdinger T, de Vries HE. Overcoming the blood-brain tumor barrier for effective glioblastoma treatment. Drug Resist Updat. 2015; 19:1-12
23. Hawkins BT, Davis TP. The blood-brain barrier/ neurovascular unit in health and disease. Pharmacol Rev. 2005; 57:173-185
24. Liebner S, Fischmann A, Rascher G, Duffner F, Grote EH, Kalbacher H, Wolburg H. Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme. Acta Neuropathol. 2000; 100:323-331
25. Deo AK, Theil FP, Nicolas JM. Confounding parameters in preclinical assessment of blood-brain barrier permeation: an overview with emphasis on species differences and effect of disease states. Mol Pharm. 2013; 10:1581-1595
26. Tate MC, Aghi MK. Biology of angiogenesis and invasion in glioma. Neurotherapeutics. 2009; 6:447-457
27. Puhalla S, Elmquist W, Freyer D, Kleinberg L, Adkins C, Lockman P, McGregor J, Muldoon L, Nesbit G, Peereboom D, Smith Q, Walker S, Neuwelt E. Unsanctifying the sanctuary: challenges and opportunities with brain metastases. Neuro Oncol. 2015; 17:639-651
28. Lin NU, Bellon JR, Winer EP. CNS metastases in breast cancer. J Clin Oncol. 2004; 22:3608-3617
29. Lockman PR, Mittapalli RK, Taskar KS, Rudraraju V, Gril B, Bohn KA, Adkins CE, Roberts A, Thorsheim HR, Gaasch JA, Huang S, Palmieri D, Steeg PS, Smith QR. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res. 2010; 16:5664-5678
30. Villanueva MT. Drug therapy: smuggling trastuzumab into the brain. Nat Rev Clin Oncol. 2013; 10:669-669
31. Yonemori K, Tsuta K, Ono M, Shimizu C, Hirakawa A, Hasegawa T, Hatanaka Y, Narita Y, Shibui S, Fujiwara Y. Disruption of the blood brain barrier by brain metastases of triple-negative and basal-type breast cancer but not HER2/ neu-positive breast cancer. Cancer. 2010; 116:302-308
32. Boskovitz A, Wikstrand CJ, Kuan CT, Zalutsky MR, Reardon DA, Bigner DD. Monoclonal antibodies for brain tumour treatment. Expert Opin Biol Ther. 2004; 4:1453-1471
33. Hoelder S, Clarke PA, Workman P. Discovery of small molecule cancer drugs: successes, challenges and opportunities. Mol Oncol. 2012; 6:155-176
34. Keith KC, Lee Y, Ewend MG, Zagar TM, Anders CK. Activity of trastuzumab-emtansine (Tdm1) in Her2-positive breast cancer brain metastases: a case series. Cancer Treat Commun. 2016; 7:43-46
35. Murthy P, Kidwell KM, Schott AF, Merajver SD, Griggs JJ, Smerage JD, Van Poznak CH, Wicha MS, Hayes DF, Henry NL. Clinical predictors of long-term survival in HER2-positive metastatic breast cancer. Breast Cancer Res Treat. 2016; 155:589-595
36. Olson EM, Najita JS, Sohl J, Arnaout A, Burstein HJ, Winer EP, Lin NU. Clinical outcomes and treatment practice patterns of patients with HER2-positive metastatic breast cancer in the post-trastuzumab era. Breast. 2013; 22:525-531
37. Prabhakarpandian B, Shen MC, Nichols JB, Mills IR, Sidoryk-Wegrzynowicz M, Aschner M, Pant K. SyM-BBB: a microfluidic Blood Brain Barrier model. Lab Chip. 2013; 13:1093-1101
38. Terrell-Hall TB, Ammer AG, Griffith JI, Lockman PR. Permeability across a novel microfluidic blood-tumor barrier model. Fluids Barriers CNS. 2017; 14:3. https://doi. org/10.1186/s12987-017-0050-9
39. Rostami R, Mittal S, Rostami P, Tavassoli F, Jabbari B. Brain metastasis in breast cancer: a comprehensive literature review. J Neurooncol. 2016
40. Dhermain FG, Hau P, Lanfermann H, Jacobs AH, van den Bent MJ. Advanced MRI and PET imaging for assessment of treatment response in patients with gliomas. Lancet Neurol. 2010; 9:906-920
41. Tzeng SY, Green JJ. Therapeutic nanomedicine for brain cancer. Ther Deliv. 2013; 4:687-704
42. Kute T, Lack CM, Willingham M, Bishwokama B, Williams H, Barrett K, Mitchell T, Vaughn JP. Development of Herceptin resistance in breast cancer cells. Cytometry A. 2004; 57:86-93
43. Sendur MA, Uncu D, Zengin N. Longest progressionfree survival with lapatinib and capecitabine combination followed by trastuzumab in HER2-positive brain metastatic breast cancer. Med Oncol. 2014; 31:890
44. Mutlu H, Buyukcelik A. The combination of weekly trastuzumab plus vinorelbine may be preferable regimen in HER-2 positive breast cancer patients with brain metastasis. J Oncol Pharm Pract. 2015; 21:310-312
45. Kodack DP, Chung E, Yamashita H, Incio J, Duyverman AM, Song Y, Farrar CT, Huang Y, Ager E, Kamoun W, Goel S, Snuderl M, Lussiez A, et al. Combined targeting of HER2 and VEGFR2 for effective treatment of HER2-amplified breast cancer brain metastases. Proc Natl Acad Sci U S A. 2012; 109:E3119-3127
46. Askoxylakis V, Ferraro GB, Kodack DP, Badeaux M, Shankaraiah RC, Seano G, Kloepper J, Vardam T, Martin JD, Naxerova K, Bezwada D, Qi X, Selig MK, et al. Preclinical efficacy of ado-trastuzumab emtansine in the brain microenvironment. J Natl Cancer Inst. 2016; 108
47. Pestalozzi BC, Brignoli S. Trastuzumab in CSF. J Clin Oncol. 2000; 18:2349-2351
48. Lampson LA. Monoclonal antibodies in neuro-oncology: getting past the blood-brain barrier. MAbs. 2011; 3:153-160
49. Deeken JF, Loscher W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res. 2007; 13:1663-1674
50. Smith QR, Takasato Y. Kinetics of amino acid transport at the blood-brain barrier studied using an in situ brain perfusion technique. Ann N Y Acad Sci. 1986; 481:186-201
51. Takasato Y, Rapoport SI, Smith QR. An in situ brain perfusion technique to study cerebrovascular transport in the rat. Am J Physiol. 1984; 247:H484-493
52. Neuwelt EA, Minna J, Frenkel E, Barnett PA, McCormick CI. Osmotic blood-brain barrier opening to IgM monoclonal antibody in the rat. Am J Physiol. 1986; 250:R875-883
53. Neuwelt EA, Specht HD, Barnett PA, Dahlborg SA, Miley A, Larson SM, Brown P, Eckerman KF, Hellstrom KE, Hellstrom I. Increased delivery of tumor-specific monoclonal antibodies to brain after osmotic blood-brain barrier modification in patients with melanoma metastatic to the central nervous system. Neurosurgery. 1987; 20:885-895
54. Neuwelt EA, Barnett PA, Hellstrom KE, Hellstrom I, McCormick CI, Ramsey FL. Effect of blood-brain barrier disruption on intact and fragmented monoclonal antibody localization in intracerebral lung carcinoma xenografts. J Nucl Med. 1994; 35:1831-1841
55. Remsen LG, McCormick CI, Roman-Goldstein S, Nilaver G, Weissleder R, Bogdanov A, Hellstrom I, Kroll RA, Neuwelt EA. MR of carcinoma-specific monoclonal antibody conjugated to monocrystalline iron oxide nanoparticles: the potential for noninvasive diagnosis. AJNR Am J Neuroradiol. 1996; 17:411-418
56. Muldoon LL. Effect of antigenic heterogeneity on the efficacy of enhanced delivery of antibody-targeted chemotherapy in a human lung cancer intracerebral xenograft model in rats. Neurosurgery. 2003; 53:1406-1412; discussion 1412-1403
57. Jahnke K, Muldoon LL, Varallyay CG, Lewin SJ, Kraemer DF, Neuwelt EA. Bevacizumab and carboplatin increase survival and asymptomatic tumor volume in a glioma model. Neuro Oncol. 2009; 11:142-150
58. Muldoon LL, Lewin SJ, Dosa E, Kraemer DF, Pagel MA, Doolittle ND, Neuwelt EA. Imaging and therapy with rituximab anti-CD20 immunotherapy in an animal model of central nervous system lymphoma. Clin Cancer Res. 2011; 17:2207-2215
59. Lewis Phillips GD, Nishimura MC, Lacap JA, Kharbanda S, Mai E, Tien J, Malesky K, Williams SP, Marik J, Phillips HS. Trastuzumab uptake and its relation to efficacy in an animal model of HER2-positive breast cancer brain metastasis. Breast Cancer Res Treat. 2017