Efficacy of HER2 retargeted herpes simplex virus as therapy for high-grade glioma in immunocompetent mice

Cancer Gene Therapy

Volumn 19, Issue 11, 2012, Pages 788-795

  Reisoli, E ^a   Gambini, E ^b   Appolloni, I ^a   Gatta, V ^c   Barilari, M ^a   Menotti, L ^c   Malatesta, P ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

HSV; murine model; oncolytic virus; virotherapy

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; GENE THERAPY AGENT; ONCOLYTIC HERPES VIRUS; R LM113; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BAGG ALBINO MOUSE; CANCER STAGING; CANCER SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG SAFETY; EMBRYO; ENCEPHALITIS; GLIOMA; IMMUNOCOMPETENCE; INOCULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; VIRUS RECOMBINANT; VIRUS REPLICATION;

ANIMALS; ANTINEOPLASTIC AGENTS; GENETIC THERAPY; GENETIC VECTORS; GLIOMA; HERPESVIRUS 1, HUMAN; HUMANS; IMMUNOCOMPETENCE; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED BALB C; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; RECEPTOR, ERBB-2; TUMOR CELLS, CULTURED; VIRUS REPLICATION;

ANIMALIA; HUMAN HERPESVIRUS 1; MURINAE; MUS; SIMPLEXVIRUS;

EID: 84867744177     PISSN: 09291903     EISSN: 14765500     Source Type: Journal    
DOI: 10.1038/cgt.2012.62     Document Type: Article

References (42)

1. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10: 459-466.
2. Friedman GK, Pressey JG, Reddy AT, Markert JM, Gillespie GY. Herpes simplex virus oncolytic therapy for pediatric malignancies. Mol Ther 2009; 17: 1125-1135.
3. Campadelli-Fiume G, De Giovanni C, Gatta V, Nanni P, Lollini PL, Menotti L. Rethinking herpes simplex virus: the way to oncolytic agents. Rev Med Virol 2011; 21: 213-226.
4. Menotti L, Campadelli-Fiume G, Nanni P, Lollini PL, De Giovanni C. The Molecular Basis Of Herpesviruses As Oncolytic Agents. Curr Pharm Biotechnol 2011; 13: 1795-1803.
5. Geevarghese SK, Geller DA, de Haan HA, Horer M, Knoll AE, Mescheder A et al. Phase I/II study of oncolytic herpes simplex virus NV1020 in patients with extensively pretreated refractory colorectal cancer metastatic to the liver. Hum Gene Ther 2010; 21: 1119-1128.
6. Harrow S, Papanastassiou V, Harland J, Mabbs R, Petty R, Fraser M et al. HSV1716 injection into the brain adjacent to tumour following surgical resection of high-grade glioma: safety data and long-term survival. Gene Ther 2004; 11: 1648-1658.
7. Hu JC, Coffin RS, Davis CJ, Graham NJ, Groves N, Guest PJ et al. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res 2006; 12: 6737-6747.
8. Kaufman HL, Bines SD. OPTIM trial: a phase III trial of an oncolytic herpes virus encoding GM-CSF for unresectable stage III or IV melanoma. Future Oncol 2010; 6: 941-949.
9. Gambini E, Reisoli E, Appolloni I, Gatta V, Campadelli-Fiume G, Menotti L et al. Replication-competent herpes simplex virus retargeted to HER2 as therapy for high-grade glioma. Mol Ther 2012; 20: 994-1001.
10. Menotti L, Cerretani A, Hengel H, Campadelli-Fiume G. Construction of a fully retargeted herpes simplex virus 1 recombinant capable of entering cells solely via human epidermal growth factor receptor 2. J Virol 2008; 82: 10153-10161.
11. Duhem-Tonnelle V, Bieche I, Vacher S, Loyens A, Maurage CA, Collier F et al. Differential distribution of erbB receptors in human glioblastoma multiforme: expression of erbB3 in CD133-positive putative cancer stem cells. J Neuropathol Exp Neurol 2010; 69: 606-622.
12. Nabika S, Kiya K, Satoh H, Mizoue T, Kondo H, Katagiri M et al. Prognostic significance of expression patterns of EGFR family, p21 and p27 in high-grade astrocytoma. Hiroshima J Med Sci 2010; 59: 65-70.
13. Gulati S, Ytterhus B, Granli US, Gulati M, Lydersen S, Torp SH. Overexpression of c-erbB2 is a negative prognostic factor in anaplastic astrocytomas. Diagn Pathol 2010; 5: 18.
14. Hiesiger EM, Hayes RL, Pierz DM, Budzilovich GN. Prognostic relevance of epidermal growth factor receptor (EGF-R) and c-neu/erbB2 expression in glio-blastomas (GBMs). J Neurooncol 1993; 16: 93-104.
15. Mineo JF, Bordron A, Baroncini M, Maurage CA, Ramirez C, Siminski RM et al. Low HER2-expressing glioblastomas are more often secondary to anaplastic transformation of low-grade glioma. J Neurooncol 2007; 85: 281-287.
16. Press MF, Cordon-Cardo C, Slamon DJ. Expression of the HER-2/neu proto-onco-gene in normal human adult and fetal tissues. Oncogene 1990; 5: 953-962.
17. Lopez C. Resistance to herpes simplex virus type 1 (HSV-1). Curr Top Microbiol Immunol 1981; 92: 15-24.
18. Lopez C. Genetics of natural resistance to herpesvirus infections in mice. Nature 1975; 258: 152-153.
19. Appolloni I, Calzolari F, Tutucci E, Caviglia S, Terrile M, Corte G et al. PDGF-B induces a homogeneous class of oligodendrogliomas from embryonic neural progenitors. Int J Cancer 2009; 124: 2251-2259.
20. Appolloni I, Calzolari F, Corte G, Perris R, Malatesta P. Six3 controls the neural progenitor status in the murine CNS. Cerebral cortex 2008; 18: 553-562.
21. Appolloni I, Calzolari F, Barilari M, Terrile M, Daga A, Malatesta P. Antagonistic modulation of gliomagenesis by Pax6 and Olig2 in PDGF-induced oligoden-droglioma. Int J Cancer 2012; 131: E1078-E1087.
22. Terrile M, Appolloni I, Calzolari F, Perris R, Tutucci E, Malatesta P. PDGF-B-driven gliomagenesis can occur in the absence of the proteoglycan NG2. BMC Cancer 2010; 10: 550.
23. Casalini P, Botta L, Menard S. Role of p53 in HER2-induced proliferation or apoptosis. J Biol Chem 2001; 276: 12449-12453.
24. Lundberg P, Cantin E. A potential role for CXCR3 chemokines in the response to ocular HSV infection. Curr Eye Res 2003; 26: 137-150.
25. Halford WP, Balliet JW, Gebhardt BM. Re-evaluating natural resistance to herpes simplex virus type 1. J Virol 2004; 78: 10086-10095.
26. Lopez C. Resistance to HSV-1 in the mouse is governed by two major, independently segregating, non-H-2 loci. Immunogenetics 1980; 11: 87-92.
27. Calzolari F, Appolloni I, Tutucci E, Caviglia S, Terrile M, Corte G et al. Tumor progression and oncogene addiction in a PDGF-B-induced model of glioma-genesis. Neoplasia (New York, NY) 2008; 10: 1373-1382.
28. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, Holland EC. PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Genes Dev 2001; 15: 1913-1925.
29. Russell SJ, Peng KW, Bell JC. Oncolytic virotherapy. Nat Biotechnol 2012; 30: 658-670.
30. Lasaro MO, Ertl HC. New insights on adenovirus as vaccine vectors. Mol Ther 2009; 17: 1333-1339.
31. Yang Y, Li Q, Ertl HC, Wilson JM. Cellular and humoral immune responses to viral antigens create barriers to lung-directed gene therapy with recombinant ade-noviruses. J Virol 1995; 69: 2004-2015.
32. Todo T, Rabkin SD, Sundaresan P, Wu A, Meehan KR, Herscowitz HB et al. Systemic antitumor immunity in experimental brain tumor therapy using a multimutated, replication-competent herpes simplex virus. Hum Gene Ther 1999; 10: 2741-2755.
33. Kaufman HL, Kim DW, DeRaffele G, Mitcham J, Coffin RS, Kim-Schulze S. Local and distant immunity induced by intralesional vaccination with an oncolytic herpes virus encoding GM-CSF in patients with stage IIIc and IV melanoma. Ann Surg Oncol 2010; 17: 718-730.
34. Hellums EK, Markert JM, Parker JN, He B, Perbal B, Roizman B et al. Increased efficacy of an interleukin-12-secreting herpes simplex virus in a syngeneic intra-cranial murine glioma model. Neuro Oncol 2005; 7: 213-224.
35. Parker JN, Gillespie GY, Love CE, Randall S, Whitley RJ, Markert JM. Engineered herpes simplex virus expressing IL-12 in the treatment of experimental murine brain tumors. Proc Nat Acad Sci USA 2000; 97: 2208-2213.
36. Castro MG, Candolfi M, Kroeger K, King GD, Curtin JF, Yagiz K et al. Gene therapy and targeted toxins for glioma. Curr Gene Ther 2011; 11: 155-180.
37. Curtin JF, Liu N, Candolfi M, Xiong W, Assi H, Yagiz K et al. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med 2009; 6: e10.
38. Ali S, Curtin JF, Zirger JM, Xiong W, King GD, Barcia C et al. Inflammatory and anti-glioma effects of an adenovirus expressing human soluble Fms-like tyrosine kinase 3 ligand (hsFlt3L): treatment with hsFlt3L inhibits intracranial glioma progression. Mol Ther 2004; 10: 1071-1084.
39. Lun X, Chan J, Zhou H, Sun B, Kelly JJ, Stechishin OO et al. Efficacy and safety/toxicity study of recombinant vaccinia virus JX-594 in two immunocompetent animal models of glioma. Mol Ther 2010; 18: 1927-1936.
40. Lun X, Alain T, Zemp FJ, Zhou H, Rahman MM, Hamilton MG et al. Myxoma virus virotherapy for glioma in immunocompetent animal models: optimizing administration routes and synergy with rapamycin. Cancer Res 2010; 70: 598-608.
41. Daga A, Orengo AM, Gangemi RM, Marubbi D, Perera M, Comes A et al. Glioma immunotherapy by IL-21 gene-modified cells or by recombinant IL-21 involves antibody responses. International journal of cancer. Int J Cancer 2007; 121: 1756-1763.
42. Andreansky S, He B, van Cott J, McGhee J, Markert JM, Gillespie GY et al. Treatment of intracranial gliomas in immunocompetent mice using herpes simplex viruses that express murine interleukins. Gene Ther 1998; 5: 121-130.