Suicide HSVtk gene delivery by neurotensin-polyplex nanoparticles via the bloodstream and GCV treatment specifically inhibit the growth of human MDA-MB-231 triple negative breast cancer tumors xenografted in athymic mice

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Castillo Rodríguez, Rosa A ^a   Arango Rodríguez, Martha L ^b   Escobedo, Lourdes ^a   Hernandez Baltazar, Daniel ^a   Gompel, Anne ^c   Forgez, Patricia ^c   Martínez Fong, Daniel ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b Facultad de Medicina Clinica Alemana Universidad del Desarrollo   (Chile)

^c UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GANCICLOVIR; GREEN FLUORESCENT PROTEIN; NANOCARRIER; NANOPARTICLE; NEUROTENSIN; NEUROTENSIN RECEPTOR; POLYPLEX NANOPARTICLE; PROTEIN NTSR1; THYMIDINE KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST ADENOCARCINOMA; CANCER CELL CULTURE; CANCER INHIBITION; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENETIC CODE; HERPES SIMPLEX VIRUS; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MOUSE; NONHUMAN; NUDE MOUSE; PROTEIN CLEAVAGE; REPORTER GENE; SUICIDE GENE THERAPY; TRIPLE NEGATIVE BREAST CANCER; TUMOR XENOGRAFT; ANIMAL; CELL PROLIFERATION; CELL SURVIVAL; DRUG EFFECTS; ENZYMOLOGY; GENE THERAPY; GENE TRANSFER; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; SCANNING ELECTRON MICROSCOPY; SIMPLEXVIRUS; SUICIDE TRANSGENE; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; FEMALE; GANCICLOVIR; GENE TRANSFER TECHNIQUES; GENES, TRANSGENIC, SUICIDE; GENETIC THERAPY; HUMANS; MICE; MICE, NUDE; MICROSCOPY, ELECTRON, SCANNING; NANOPARTICLES; NEUROTENSIN; SIMPLEXVIRUS; THYMIDINE KINASE; TRANSPLANTATION, HETEROLOGOUS; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84901286609     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097151     Document Type: Article

References (68)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, et al. (2011) Global cancer statistics. CA Cancer J Clin 61: 69-90.
2. Chiu SJ, Ueno NT, Lee RJ (2004) Tumor-targeted gene delivery via anti-HER2 antibody (trastuzumab, Herceptin) conjugated polyethylenimine. J Control Release 97: 357-369. (Pubitemid 38759492)
3. Li X, Stuckert P, Bosch I, Marks JD, Marasco WA (2001) Single-chain antibody-mediated gene delivery into ErbB2-positive human breast cancer cells. Cancer Gene Ther 8: 555-565. (Pubitemid 32786558)
4. Huang H, Yu H, Tang G, Wang Q, Li J (2010) Low molecular weight polyethylenimine cross-linked by 2-hydroxypropyl-gamma-cyclodextrin coupled to peptide targeting HER2 as a gene delivery vector. Biomaterials 31: 1830-1838.
5. Eastman A, Tammaro Y, Moldrem A, Andrews V, Huth J, et al. (2013) Outcomes of delays in time to treatment in triple negative breast cancer. Ann Surg Oncol 20: 1880-1885.
6. Bayraktar S, Gluck S (2013) Molecularly targeted therapies for metastatic triplenegative breast cancer. Breast Cancer Res Treat 138: 21-35.
7. Perou CM (2011) Molecular stratification of triple-negative breast cancers. Oncologist 16 Suppl 1: 61-70.
8. Bosch A, Eroles P, Zaragoza R, Vina JR, Lluch A (2010) Triple-negative breast cancer: molecular features, pathogenesis, treatment and current lines of research. Cancer Treat Rev 36: 206-215.
9. Boyle P (2012) Triple-negative breast cancer: epidemiological considerations and recommendations. Ann Oncol 23 Suppl 6: vi7-12.
10. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, et al. (2007) Triplenegative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 13: 4429-4434. (Pubitemid 47219710)
11. Wu Z, Martinez-Fong D, Tredaniel J, Forgez P (2012) Neurotensin and its high affinity receptor 1 as a potential pharmacological target in cancer therapy. Front Endocrinol (Lausanne) 3: 184.
12. Schade B, Lesurf R, Sanguin-Gendreau V, Bui T, Deblois G, et al. (2013) beta-Catenin signaling is a critical event in ErbB2-mediated mammary tumor progression. Cancer Res 73: 4474-4487.
13. Shy BR, Wu CI, Khramtsova GF, Zhang JY, Olopade OI, et al. (2013) Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt/beta-catenin signaling. Cell Rep 4: 1-9.
14. Dupouy S, Mourra N, Doan VK, Gompel A, Alifano M, et al. (2011) The potential use of the neurotensin high affinity receptor 1 as a biomarker for cancer progression and as a component of personalized medicine in selective cancers. Biochimie 93: 1369-1378.
15. Souaze F, Viardot-Foucault V, Roullet N, Toy-Miou-Leong M, Gompel A, et al. (2006) Neurotensin receptor 1 gene activation by the Tcf/beta-catenin pathway is an early event in human colonic adenomas. Carcinogenesis 27: 708-716.
16. Wend P, Runke S, Wend K, Anchondo B, Yesayan M, et al. (2013) WNT10B/beta-catenin signalling induces HMGA2 and proliferation in metastatic triplenegative breast cancer. EMBO Mol Med 5: 264-279.
17. Souaze F, Dupouy S, Viardot-Foucault V, Bruyneel E, Attoub S, et al. (2006) Expression of neurotensin and NT1 receptor in human breast cancer: a potential role in tumor progression. Cancer Res 66: 6243-6249.
18. Somai S, Gompel A, Rostene W, Forgez P (2002) Neurotensin counteracts apoptosis in breast cancer cells. Biochem Biophys Res Commun 295: 482-488. (Pubitemid 34785860)
19. Dupouy S, Viardot-Foucault V, Alifano M, Souaze F, Plu-Bureau G, et al. (2009) The neurotensin receptor-1 pathway contributes to human ductal breast cancer progression. PLoS One 4: e4223.
20. Heakal Y, Kester M (2009) Nanoliposomal short-chain ceramide inhibits agonist-dependent translocation of neurotensin receptor 1 to structured membrane microdomains in breast cancer cells. Mol Cancer Res 7: 724-734.
21. Kao J, Salari K, Bocanegra M, Choi YL, Girard L, et al. (2009) Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PLoS One 4: e6146.
22. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, et al. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10: 515-527. (Pubitemid 44854747)
23. Mendez M, Souaze F, Nagano M, Kelly PA, Rostene W, et al. (1997) High affinity neurotensin receptor mRNA distribution in rat brain and peripheral tissues. Analysis by quantitative RT-PCR. J Mol Neurosci 9: 93-102. (Pubitemid 127499159)
24. Rubio-Zapata HA, Rembao-Bojorquez JD, Arango-Rodriguez ML, Dupouy S, Forgez P, et al. (2009) NT-polyplex: a new tool for therapeutic gene delivery to neuroblastoma tumors. Cancer Gene Ther 16: 573-584.
25. Navarro-Quiroga I, Antonio Gonzalez-Barrios J, Barron-Moreno F, Gonzalez-Bernal V, Martinez-Arguelles DB, et al. (2002) Improved neurotensin-vectormediated gene transfer by the coupling of hemagglutinin HA2 fusogenic peptide and Vp1 SV40 nuclear localization signal. Brain Res Mol Brain Res 105: 86-97. (Pubitemid 35245615)
26. Martinez-Fong D, Bannon MJ, Trudeau LE, Gonzalez-Barrios JA, Arango-Rodriguez ML, et al. (2012) NTS-Polyplex: a potential nanocarrier for neurotrophic therapy of Parkinson's disease. Nanomedicine 8: 1052-1069.
27. Hernandez-Baltazar D, Martinez-Fong D, Trudeau LE (2012) Optimizing NTS-polyplex as a tool for gene transfer to cultured dopamine neurons. PLoS One 7: e51341.
28. Alvarez-Maya I, Navarro-Quiroga I, Meraz-Rios MA, Aceves J, Martinez-Fong D (2001) In vivo gene transfer to dopamine neurons of rat substantia nigra via the high-affinity neurotensin receptor. Mol Med 7: 186-192. (Pubitemid 33701990)
29. Martinez-Fong D, Navarro-Quiroga I, Ochoa I, Alvarez-Maya I, Meraz MA, et al. (1999) Neurotensin-SPDP-poly-L-lysine conjugate: a nonviral vector for targeted gene delivery to neural cells. Brain Res Mol Brain Res 69: 249-262. (Pubitemid 29253817)
30. Arango-Rodriguez ML, Navarro-Quiroga I, Gonzalez-Barrios JA, Martinez-Arguelles DB, Bannon MJ, et al. (2006) Biophysical characteristics of neurotensin polyplex for in vitro and in vivo gene transfection. Biochim Biophys Acta 1760: 1009-1020. (Pubitemid 43870395)
31. Martinez-Fong D, Navarro-Quiroga I (2000) Synthesis of a non-viral vector for gene transfer via the high-affinity neurotensin receptor. Brain Res Brain Res Protoc 6: 13-24.
32. Hernandez-Gutierrez M, Rembao JD, Hernandez-Baltazar D, Castillo-Rodriguez RA, Tellez-Lopez VM, et al. (2013) Safety of the intravenous administration of neurotensin-polyplex nanoparticles in BALB/c mice. Nanomedicine: Nanotechnology, Biology and Medicine.
33. Sakurai H, Kawabata K, Sakurai F, Nakagawa S, Mizuguchi H (2008) Innate immune response induced by gene delivery vectors. Int J Pharm 354: 9-15. (Pubitemid 351400322)
34. Zhu J, Huang X, Yang Y (2009) The TLR9-MyD88 pathway is critical for adaptive immune responses to adeno-associated virus gene therapy vectors in mice. J Clin Invest 119: 2388-2398.
35. Howe SJ, Mansour MR, Schwarzwaelder K, Bartholomae C, Hubank M, et al. (2008) Insertional mutagenesis combined with acquired somatic mutations causes leukemogenesis following gene therapy of SCID-X1 patients. J Clin Invest 118: 3143-3150.
36. Lim KI (2012) Retroviral integration profiles: their determinants and implications for gene therapy. BMB Rep 45: 207-212.
37. Pan JG, Zhou X, Luo R, Han RF (2012) The adeno-associated virus-mediated HSV-TK/GCV suicide system: a potential strategy for the treatment of bladder carcinoma. Med Oncol 29: 1938-1947.
38. Fillat C, Carrio M, Cascante A, Sangro B (2003) Suicide gene therapy mediated by the Herpes Simplex virus thymidine kinase gene/Ganciclovir system: fifteen years of application. Curr Gene Ther 3: 13-26.
39. Tomicic MT, Bey E, Wutzler P, Thust R, Kaina B (2002) Comparative analysis of DNA breakage, chromosomal aberrations and apoptosis induced by the antiherpes purine nucleoside analogues aciclovir, ganciclovir and penciclovir. Mutat Res 505: 1-11.
40. Dachs GU, Hunt MA, Syddall S, Singleton DC, Patterson AV (2009) Bystander or no bystander for gene directed enzyme prodrug therapy. Molecules 14: 4517-4545.
41. Hamel W, Magnelli L, Chiarugi VP, Israel MA (1996) Herpes simplex virus thymidine kinase/ganciclovir-mediated apoptotic death of bystander cells. Cancer Res 56: 2697-2702. (Pubitemid 26175720)
42. Vyas VK, Chintha C, Pandya MR (2013) Biology and medicinal chemistry approaches towards various apoptosis inducers. Anticancer Agents Med Chem 13: 433-455.
43. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63.
44. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on. Nat Protoc 1: 581-585.
45. Hernandez-Baltazar D, Mendoza-Garrido ME, Martinez-Fong D (2013) Activation of GSK-3beta and Caspase-3 Occurs in Nigral Dopamine Neurons during the Development of Apoptosis Activated by a Striatal Injection of 6-Hydroxydopamine. PLoS One 8: e70951.
46. Orozco-Barrios CE, Battaglia-Hsu SF, Arango-Rodriguez ML, Ayala-Davila J, Chery C, et al. (2009) Vitamin B12-impaired metabolism produces apoptosis and Parkinson phenotype in rats expressing the transcobalamin-oleosin chimera in substantia nigra. PLoS One 4: e8268.
47. Tomayko MM, Reynolds CP (1989) Determination of subcutaneous tumor size in athymic (nude) mice. Cancer Chemother Pharmacol 24: 148-154. (Pubitemid 19163397)
48. Gully D, Canton M, Boigegrain R, Jeanjean F, Molimard JC, et al. (1993) Biochemical and pharmacological profile of a potent and selective nonpeptide antagonist of the neurotensin receptor. Proc Natl Acad Sci U S A 90: 65-69. (Pubitemid 23010250)
49. Heuser JE, Anderson RG (1989) Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J Cell Biol 108: 389-400. (Pubitemid 19065841)
50. Lookingbill DP, Spangler N, Helm KF (1993) Cutaneous metastases in patients with metastatic carcinoma: a retrospective study of 4020 patients. J Am Acad Dermatol 29: 228-236. (Pubitemid 23221903)
51. Spencer PS, Helm TN (1987) Skin metastases in cancer patients. Cutis 39: 119-121. (Pubitemid 17011376)
52. Alexis F, Pridgen E, Molnar LK, Farokhzad OC (2008) Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharm 5: 505-515.
53. Merkel OM, Librizzi D, Pfestroff A, Schurrat T, Buyens K, et al. (2009) Stability of siRNA polyplexes from poly(ethylenimine) and poly(ethylenimine)-g- poly(-ethylene glycol) under in vivo conditions: effects on pharmacokinetics and biodistribution measured by Fluorescence Fluctuation Spectroscopy and Single Photon Emission Computed Tomography (SPECT) imaging. J Control Release 138: 148-159.
54. Ward CM, Read ML, Seymour LW (2001) Systemic circulation of poly(Llysine)/DNA vectors is influenced by polycation molecular weight and type of DNA: differential circulation in mice and rats and the implications for human gene therapy. Blood 97: 2221-2229. (Pubitemid 32291466)
55. Huyn ST, Burton JB, Sato M, Carey M, Gambhir SS, et al. (2009) A potent, imaging adenoviral vector driven by the cancer-selective mucin-1 promoter that targets breast cancer metastasis. Clin Cancer Res 15: 3126-3134.
56. McLachlan E, Shao Q, Laird DW (2007) Connexins and gap junctions in mammary gland development and breast cancer progression. J Membr Biol 218: 107-121. (Pubitemid 350132123)
57. McLachlan E, Shao Q, Wang HL, Langlois S, Laird DW (2006) Connexins act as tumor suppressors in three-dimensional mammary cell organoids by regulating differentiation and angiogenesis. Cancer Res 66: 9886-9894. (Pubitemid 44672040)
58. Duarte S, Carle G, Faneca H, de Lima MC, Pierrefite-Carle V (2012) Suicide gene therapy in cancer: where do we stand now? Cancer Lett 324: 160-170.
59. Mesnil M, Yamasaki H (2000) Bystander effect in herpes simplex virusthymidine kinase/ganciclovir cancer gene therapy: role of gap-junctional intercellular communication. Cancer Res 60: 3989-3999. (Pubitemid 30636571)
60. Asklund T, Appelskog IB, Ammerpohl O, Langmoen IA, Dilber MS, et al. (2003) Gap junction-mediated bystander effect in primary cultures of human malignant gliomas with recombinant expression of the HSVtk gene. Exp Cell Res 284: 185-195. (Pubitemid 36329174)
61. Freeman SM, Abboud CN, Whartenby KA, Packman CH, Koeplin DS, et al. (1993) The "bystander effect": tumor regression when a fraction of the tumor mass is genetically modified. Cancer Res 53: 5274-5283. (Pubitemid 23333399)
62. Drake RR, Pitlyk K, McMasters RA, Mercer KE, Young H, et al. (2000) Connexin-independent ganciclovir-mediated killing conferred on bystander effect-resistant cell lines by a herpes simplex virus-thymidine kinase-expressing colon cell line. Mol Ther 2: 515-523.
63. Princen F, Robe P, Lechanteur C, Mesnil M, Rigo JM, et al. (1999) A cell type-specific and gap junction-independent mechanism for the herpes simplex virus-1 thymidine kinase gene/ganciclovir-mediated bystander effect. Clin Cancer Res 5: 3639-3644.
64. Carroll JL, Nielsen LL, Pruett SB, Mathis JM (2001) The role of natural killer cells in adenovirus-mediated p53 gene therapy. Mol Cancer Ther 1: 49-60.
65. Dilber MS, Abedi MR, Bjorkstrand B, Christensson B, Gahrton G, et al. (1996) Suicide gene therapy for plasma cell tumors. Blood 88: 2192-2200. (Pubitemid 26307922)
66. Stover TC, Sharma A, Robertson GP, Kester M (2005) Systemic delivery of liposomal short-chain ceramide limits solid tumor growth in murine models of breast adenocarcinoma. Clin Cancer Res 11: 3465-3474. (Pubitemid 40627901)
67. Reis-Filho JS, Pinheiro C, Lambros MB, Milanezi F, Carvalho S, et al. (2006) EGFR amplification and lack of activating mutations in metaplastic breast carcinomas. J Pathol 209: 445-453. (Pubitemid 44194559)
68. Ferraro DA, Gaborit N, Maron R, Cohen-Dvashi H, Porat Z, et al. (2013) Inhibition of triple-negative breast cancer models by combinations of antibodies to EGFR. Proc Natl Acad Sci U S A 110: 1815-1820.