3,749
Views
16
CrossRef citations to date
0
Altmetric
Review Article

Seek and destroy: targeted adeno-associated viruses for gene delivery to hepatocellular carcinoma

, , &
Pages 289-299 | Received 12 Aug 2016, Accepted 10 Oct 2016, Published online: 06 Feb 2017

References

  • Abdul-Ghani R, Ohana P, Matouk I, et al. (2000). Use of transcriptional regulatory sequences of telomerase (hTER and hTERT) for selective killing of cancer cells. Mol Ther 2:539–44
  • Afione S, Dimattia MA, Halder S, et al. (2015). Identification and mutagenesis of the adeno-associated virus 5 sialic acid binding region. J Virol 89:1660–72
  • Alisky JM, Hughes SM, Sauter SL, et al. (2000). Transduction of murine cerebellar neurons with recombinant FIV and AAV5 vectors. Neuroreport 11:2669–73
  • Amer MH. (2014). Gene therapy for cancer: present status and future perspective. Mol Cell Ther 2:27
  • Arruda VR, Samelson-Jones BJ. (2015). Obstacles and future of gene therapy for hemophilia. Expert Opin Orphan Drugs 3:997–1010
  • Asokan A, Schaffer DV, Samulski RJ. (2012). The AAV vector toolkit: poised at the clinical crossroads. Mol Ther 20:699–708
  • Auricchio A. (2003). Pseudotyped AAV vectors for constitutive and regulated gene expression in the eye. Vision Res 43:913–18
  • Balaji S, King A, Dhamija Y, et al. (2013). Pseudotyped adeno-associated viral vectors for gene transfer in dermal fibroblasts: implications for wound-healing applications. J Surg Res 184:691–8
  • Balakrishnan B, Jayandharan GR. (2014). Basic biology of adeno-associated virus (AAV) vectors used in gene therapy. Curr Gene Ther 14:86–100
  • Barker SD, Dmitriev IP, Nettelbeck DM, et al. (2003). Combined transcriptional and transductional targeting improves the specificity and efficacy of adenoviral gene delivery to ovarian carcinoma. Gene Ther 10:1198–204
  • Bartlett JS, Kleinschmidt J, Boucher RC, Samulski RJ. (1999). Targeted adeno-associated virus vector transduction of nonpermissive cells mediated by a bispecific F(ab′gamma)2 antibody. Nat Biotechnol 17:181–6
  • Bartlett JS, Wilcher R, Samulski RJ. (2000). Infectious entry pathway of adeno-associated virus and adeno-associated virus vectors. J Virol 74:2777–85
  • Boutin S, Monteilhet V, Veron P, et al. (2010). Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther 21:704–12
  • Büning H, Huber A, Zhang L, et al. (2015). Engineering the AAV capsid to optimize vector–host-interactions. Curr Opin Pharmacol 24:94–104
  • Calcedo R, Morizono H, Wang L, et al. (2011). Adeno-associated virus antibody profiles in newborns, children, and adolescents. Clin Vaccine Immunol 18:1586–8
  • Calcedo R, Vandenberghe LH, Gao G, et al. (2009). Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 199:381–90
  • Calcedo R, Wilson JM. (2013). Humoral immune response to AAV. Front Immunol 4:341
  • Casado E, Nettelbeck DM, Gomez-Navarro J, et al. (2001). Transcriptional targeting for ovarian cancer gene therapy. Gynecol Oncol 82:229–37
  • Chang CM, Lo CH, Shih YM, et al. (2010). Treatment of hepatocellular carcinoma with adeno-associated virus encoding interleukin-15 superagonist. Hum Gene Ther 21:611–21
  • Chao H, Liu Y, Rabinowitz J, et al. (2000). Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol Ther 2:619–23
  • Chen CA, Lo CK, Lin BL, et al. (2008). Application of doxorubicin-induced rAAV2-p53 gene delivery in combined chemotherapy and gene therapy for hepatocellular carcinoma. Cancer Biol Ther 7:303–9
  • Cheng AL, Kang YK, Chen Z, et al. (2009). Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomized, double-blind, placebo-controlled trial. Lancet Oncol 10:25–34
  • Cheng B, Ling C, Dai Y, et al. (2012). Development of optimized AAV3 serotype vectors: mechanism of high-efficiency transduction of human liver cancer cells. Gene Ther 19:375–84
  • Coulter JA, Page NL, Worthington J, et al. (2010). Transcriptional regulation of inducible nitric oxide synthase gene therapy: targeting early stage and advanced prostate cancer. J Gene Med 12:755–65
  • Davidoff AM, Gray JT, Ng CY, et al. (2005). Comparison of the ability of adeno-associated viral vectors pseudotyped with serotype 2, 5, and 8 capsid proteins to mediate efficient transduction of the liver in murine and nonhuman primate models. Mol Ther 11:875–88
  • Della Peruta M, Badar A, Rosales C, et al. (2015). Preferential targeting of disseminated liver tumors using a recombinant adeno-associated viral vector. Hum Gene Ther 26:94–103
  • Du B, Qian M, Zhou Z, et al. (2006). In vitro panning of a targeting peptide to hepatocarcinoma from a phage display peptide library. Biochem Biophys Res Commun 342:956–62
  • Du WZ, Yu TX. (2011). Generation of antitumor response against hepatocellular carcinoma by in vitro transduction of dendritic cells with adeno-associated virus expressing α-fetoprotein. Zhonghua Yi Xue Za Zhi 91:2077–80
  • El-Serag HB, Rudolph KL. (2007). Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557–76
  • Ferreira V, Petry H, Salmon F. (2014). Immune responses to AAV-vectors, the Glybera example from bench to bedside. Front Immunol 5:82
  • Figueiredo ML, Sato M, Johnson M, Wu L. (2006). Specific targeting of gene therapy to prostate cancer using a two-step transcriptional amplification system. Future Oncol 2:391–406
  • Flaherty KT, Sun W. (2009). Which questions remain unanswered following the successful development of sorafenib in hepatocellular carcinoma? Nat Clin Pract Oncol 6:64–5
  • Foka P, Pourchet A, Hernandez-Alcoceba R, et al. (2010). Novel tumor-specific promoters for transcriptional targeting of hepatocellular carcinoma by herpes simplex virus vectors. J Gene Med 12:956–67
  • Forner A, Llovet JM, Bruix J. (2012). Hepatocellular carcinoma. Lancet 379:1245–55
  • Forrest AR, Kawaji H, Rehli M, et al. (2014). A promoter-level mammalian expression atlas. Nature 507:462–70
  • Fu X, Rivera A, Tao L, et al. (2012). Construction of an oncolytic herpes simplex virus that precisely targets hepatocellular carcinoma cells. Mol Ther 20:339–46
  • Gao G, Lu Y, Calcedo R, et al. (2006). Biology of AAV serotype vectors in liver-directed gene transfer to nonhuman primates. Mol Ther 13:77–87
  • George LA, Fogarty PF. (2016). Gene therapy for hemophilia: past, present and future. Semin Hematol 53:46–54
  • Girod A, Ried M, Wobus C, et al. (1999). Genetic capsid modifications allow efficient re-targeting of adeno-associated virus type 2. Nat Med 5:1052–6
  • Grifman M, Trepel M, Speece P, et al. (2001). Incorporation of tumor-targeting peptides into recombinant adeno-associated virus capsids. Mol Ther 3:964–75
  • Grimm D, Pandey K, Nakai H, et al. (2006). Liver transduction with recombinant adeno-associated virus is primarily restricted by capsid serotype not vector genotype. J Virol 80:426–39
  • Grimm D, Zhou S, Nakai H, et al. (2003). Preclinical in vivo evaluation of pseudotyped adeno-associated virus vectors for liver gene therapy. Blood 102:2412–9
  • Gu J, Fang B. (2003). Telomerase promoter-driven cancer gene therapy. Cancer Biol Ther 2:S64–70
  • Gurda BL, Dimattia MA, Miller EB, et al. (2013). Capsid antibodies to different adeno-associated virus serotypes bind common regions. J Virol 87:9111–24
  • Hauck B, Chen L, Xiao W. (2003). Generation and characterization of chimeric recombinant AAV vectors. Mol Ther 7:419–25
  • High KA, Aubourg P. (2011). rAAV human trial experience. Methods Mol Biol 807:429–57
  • Hong SY, Lee MH, Kim KS, et al. (2004). Adeno-associated virus mediated endostatin gene therapy in combination with topoisomerase inhibitor effectively controls liver tumor in mouse model. World J Gastroenterol 10:1191–7
  • Iliopoulos D, Satra M, Drakaki A, et al. (2009). Epigenetic regulation of hTERT promoter in hepatocellular carcinomas. Int J Oncol 34:391–9
  • Jiang H, Lillicrap D, Patarroyo-White S, et al. (2006). Multiyear therapeutic benefit of AAV serotypes 2, 6, and 8 delivering factor VIII to hemophilia A mice and dogs. Blood 108:107–15
  • Kandil DH, Cooper K. (2009). Glypican-3: a novel diagnostic marker for hepatocellular carcinoma and more. Adv Anat Pathol 16:125–9
  • Kern A, Schmidt K, Leder C, et al. (2003). Identification of a heparin-binding motif on adeno-associated virus type 2 capsids. J Virol 77:11072–81
  • Kim NW, Piatyszek MA, Prowse KR, et al. (1994). Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011–15
  • Kota J, Chivukula RR, O'donnell KA, et al. (2009). Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137:1005–17
  • Kotterman MA, Schaffer DV. (2014). Engineering adeno-associated viruses for clinical gene therapy. Nat Rev Genet 15:445–51
  • Kwon I, Schaffer DV. (2008). Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm Res 25:489–99
  • Lee K, Yun ST, Kim YG, et al. (2006). Adeno-associated virus-mediated expression of apolipoprotein (a) kringles suppresses hepatocellular carcinoma growth in mice. Hepatology 43:1063–73
  • Li C, Wu S, Albright B, et al. (2016). Development of patient-specific AAV vectors after neutralizing antibody selection for enhanced muscle gene transfer. Mol Ther 24:53–65
  • Li HJ, Everts M, Yamamoto M, et al. (2009). Combined transductional untargeting/retargeting and transcriptional restriction enhances adenovirus gene targeting and therapy for hepatic colorectal cancer tumors. Cancer Res 69:554–64
  • Li X, Zhang J, Gao H, et al. (2005). Transcriptional targeting modalities in breast cancer gene therapy using adenovirus vectors controlled by alpha-lactalbumin promoter. Mol Cancer Ther 4:1850–9
  • Liang CM, Zhong CP, Sun RX, et al. (2007). Local expression of secondary lymphoid tissue chemokine delivered by adeno-associated virus within the tumor bed stimulates strong anti-liver tumor immunity. J Virol 81:9502–11
  • Ling C, Lu Y, Kalsi JK, et al. (2010). Human hepatocyte growth factor receptor is a cellular coreceptor for adeno-associated virus serotype 3. Hum Gene Ther 21:1741–7
  • Lisowski L, Dane AP, Chu K, et al. (2014). Selection and evaluation of clinically relevant AAV variants in a xenograft liver model. Nature 506:382–6
  • Liu Y, Siriwon N, Rohrs JA, Wang P. (2015). Generation of targeted adeno-associated virus (AAV) vectors for human gene therapy. Curr Pharm Des 21:3248–56
  • Liver EAFTSOT, Cancer EOFRATO. (2012). EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56:908–43
  • Llovet JM, Ricci S, Mazzaferro V, et al. (2008). Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 359:378–90
  • Lo A, Lin CT, Wu HC. (2008). Hepatocellular carcinoma cell-specific peptide ligand for targeted drug delivery. Mol Cancer Ther 7:579–89
  • Lo CH, Chang CM, Tang SW, et al. (2010). Differential antitumor effect of interleukin-12 family cytokines on orthotopic hepatocellular carcinoma. J Gene Med 12:423–34
  • Lu B, Makhija SK, Nettelbeck DM, et al. (2005). Evaluation of tumor-specific promoter activities in melanoma. Gene Ther 12:330–8
  • Luo J, Luo Y, Sun J, et al. (2015). Adeno-associated virus-mediated cancer gene therapy: current status. Cancer Lett 356:347–56
  • Luo YQ, Wu MC, Cong WM. (1999). Gene expression of hepatocyte growth factor and its receptor in HCC and nontumorous liver tissues. World J Gastroenterol 5:119–21
  • Ma H, Liu Y, Liu S, et al. (2005a). Recombinant adeno-associated virus-mediated TRAIL gene therapy suppresses liver metastatic tumors. Int J Cancer 116:314–21
  • Ma H, Liu Y, Liu S, et al. (2005b). Oral adeno-associated virus-sTRAIL gene therapy suppresses human hepatocellular carcinoma growth in mice. Hepatology 42:1355–63
  • Ma SH, Chen GG, Yip J, Lai PB. (2010). Therapeutic effect of alpha-fetoprotein promoter-mediated tBid and chemotherapeutic agents on orthotopic liver tumor in mice. Gene Ther 17:905–12
  • Maheshri N, Koerber JT, Kaspar BK, Schaffer DV. (2006). Directed evolution of adeno-associated virus yields enhanced gene delivery vectors. Nat Biotechnol 24:198–204
  • Manno CS, Pierce GF, Arruda VR, et al. (2006). Successful transduction of liver in hemophilia by AAV-factor IX and limitations imposed by the host immune response. Nat Med 12:342–7
  • Masat E, Pavani G, Mingozzi F. (2013). Humoral immunity to AAV vectors in gene therapy: challenges and potential solutions. Discov Med 15:379–89
  • Michelfelder S, Trepel M. (2009). Adeno-associated viral vectors and their redirection to cell-type specific receptors. Adv Genet 67:29–60
  • Michelfelder S, Varadi K, Raupp C, et al. (2011). Peptide ligands incorporated into the threefold spike capsid domain to re-direct gene transduction of AAV8 and AAV9 in vivo. PLoS One 6:e23101
  • Mingozzi F, High KA. (2011). Immune responses to AAV in clinical trials. Curr Gene Ther 11:321–30
  • Mingozzi F, High KA. (2013). Immune responses to AAV vectors: overcoming barriers to successful gene therapy. Blood 122:23–36
  • Münch RC, Janicki H, Völker I, et al. (2013). Displaying high-affinity ligands on adeno-associated viral vectors enables tumor cell-specific and safe gene transfer. Mol Ther 21:109–18
  • Nassar A, Cohen C, Siddiqui MT. (2009). Utility of glypican-3 and survivin in differentiating hepatocellular carcinoma from benign and preneoplastic hepatic lesions and metastatic carcinomas in liver fine-needle aspiration biopsies. Diagn Cytopathol 37:629–35
  • Nicklin SA, Buening H, Dishart KL, et al. (2001). Efficient and selective AAV2-mediated gene transfer directed to human vascular endothelial cells. Mol Ther 4:174–81
  • Niemeyer GP, Herzog RW, Mount J, et al. (2009). Long-term correction of inhibitor-prone hemophilia B dogs treated with liver-directed AAV2-mediated factor IX gene therapy. Blood 113:797–806
  • Opie SR, Warrington KH, Agbandje-Mckenna M, et al. (2003). Identification of amino acid residues in the capsid proteins of adeno-associated virus type 2 that contribute to heparan sulfate proteoglycan binding. J Virol 77:6995–7006
  • Pacak CA, Mah CS, Thattaliyath BD, et al. (2006). Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 99:e3–9
  • Pasini A, Delmonte A, Tesei A, et al. (2015). Targeting chromatin-mediated transcriptional control of gene expression in non-small cell lung cancer therapy: preclinical rationale and clinical results. Drugs 75:1757–71
  • Peng D, Qian C, Sun Y, et al. (2000). Transduction of hepatocellular carcinoma (HCC) using recombinant adeno-associated virus (rAAV): in vitro and in vivo effects of genotoxic agents. J Hepatol 32:975–85
  • Qu L, Wang Y, Gong L, et al. (2013). Suicide gene therapy for hepatocellular carcinoma cells by survivin promoter-driven expression of the herpes simplex virus thymidine kinase gene. Oncol Rep 29:1435–40
  • Reynolds PN, Nicklin SA, Kaliberova L, et al. (2001). Combined transductional and transcriptional targeting improves the specificity of transgene expression in vivo. Nat Biotechnol 19:838–42
  • Ried MU, Girod A, Leike K, et al. (2002). Adeno-associated virus capsids displaying immunoglobulin-binding domains permit antibody-mediated vector retargeting to specific cell surface receptors. J Virol 76:4559–66
  • Robson T, Hirst DG. (2003). Transcriptional targeting in cancer gene therapy. J Biomed Biotechnol 2003:110–37
  • Sallach J, Di Pasquale G, Larcher F, et al. (2014). Tropism-modified AAV vectors overcome barriers to successful cutaneous therapy. Mol Ther 22:929–39
  • Sarkar R, Mucci M, Addya S, et al. (2006). Long-term efficacy of adeno-associated virus serotypes 8 and 9 in hemophilia a dogs and mice. Hum Gene Ther 17:427–39
  • Schlitt HJ, Mornex F, Shaked A, Trotter JF. (2011). Immunosuppression and hepatocellular carcinoma. Liver Transpl 17 Suppl 2:S159–61
  • Sen D. (2014). Improving clinical efficacy of adeno associated vectors by rational capsid bioengineering. J Biomed Sci 21:103
  • Sen D, Balakrishnan B, Gabriel N, et al. (2013). Improved adeno-associated virus (AAV) serotype 1 and 5 vectors for gene therapy. Sci Rep 3:1832
  • Shen Z, Wong OG, Yao RY, et al. (2008a). A novel and effective hepatocyte growth factor kringle 1 domain and p53 cocktail viral gene therapy for the treatment of hepatocellular carcinoma. Cancer Lett 272:268–76
  • Shen Z, Yang ZF, Gao Y, et al. (2008b). The kringle 1 domain of hepatocyte growth factor has antiangiogenic and antitumor cell effects on hepatocellular carcinoma. Cancer Res 68:404–14
  • Sia KC, Huynh H, Chung AY, et al. (2013). Preclinical evaluation of transcriptional targeting strategy for human hepatocellular carcinoma in an orthotopic xenograft mouse model. Mol Cancer Ther 12:1651–64
  • Siegel RL, Miller KD, Jemal A. (2015). Cancer statistics, 2015. CA Cancer J Clin 65:5–29
  • Stachler MD, Bartlett JS. (2006). Mosaic vectors comprised of modified AAV1 capsid proteins for efficient vector purification and targeting to vascular endothelial cells. Gene Ther 13:926–31
  • Stachler MD, Chen I, Ting AY, Bartlett JS. (2008). Site-specific modification of AAV vector particles with biophysical probes and targeting ligands using biotin ligase. Mol Ther 16:1467–73
  • Steel JC, Di Pasquale G, Ramlogan CA, et al. (2013). Oral vaccination with adeno-associated virus vectors expressing the Neu oncogene inhibits the growth of murine breast cancer. Mol Ther 21:680–7
  • Su H, Chang JC, Xu SM, Kan YW. (1996). Selective killing of AFP-positive hepatocellular carcinoma cells by adeno-associated virus transfer of the herpes simplex virus thymidine kinase gene. Hum Gene Ther 7:463–70
  • Su H, Lu R, Chang JC, Kan YW. (1997). Tissue-specific expression of herpes simplex virus thymidine kinase gene delivered by adeno-associated virus inhibits the growth of human hepatocellular carcinoma in athymic mice. Proc Natl Acad Sci USA 94:13891–6
  • Summerford C, Samulski RJ. (1998). Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72:1438–45
  • Torrecilla S, Llovet JM. (2015). New molecular therapies for hepatocellular carcinoma. Clin Res Hepatol Gastroenterol. 39(Suppl 1):S80–S85
  • Tse LV, Moller-Tank S, Asokan A. (2015). Strategies to circumvent humoral immunity to adeno-associated viral vectors. Expert Opin Biol Ther 15:845–55
  • Tse LY, Sun X, Jiang H, et al. (2008). Adeno-associated virus-mediated expression of kallistatin suppresses local and remote hepatocellular carcinomas. J Gene Med 10:508–17
  • Vandenberghe LH, Wilson JM, Gao G. (2009). Tailoring the AAV vector capsid for gene therapy. Gene Ther 16:311–9
  • Vanrell L, Di Scala M, Blanco L, et al. (2011). Development of a liver-specific Tet-on inducible system for AAV vectors and its application in the treatment of liver cancer. Mol Ther 19:1245–53
  • Waehler R, Russell SJ, Curiel DT. (2007). Engineering targeted viral vectors for gene therapy. Nat Rev Genet 8:573–87
  • Waghray A, Murali AR, Menon KN. (2015). Hepatocellular carcinoma: from diagnosis to treatment. World J Hepatol 7:1020–9
  • Wang Y, Huang F, Cai H, et al. (2008). Potent antitumor effect of TRAIL mediated by a novel adeno-associated viral vector targeting to telomerase activity for human hepatocellular carcinoma. J Gene Med 10:518–26
  • Wang Y, Huang F, Cai H, et al. (2010). The efficacy of combination therapy using adeno-associated virus-TRAIL targeting to telomerase activity and cisplatin in a mice model of hepatocellular carcinoma. J Cancer Res Clin Oncol 136:1827–37
  • Weitzman MD, Linden RM. (2011). Adeno-associated virus biology. Methods Mol Biol 807:1–23
  • Wu P, Xiao W, Conlon T, et al. (2000). Mutational analysis of the adeno-associated virus type 2 (AAV2) capsid gene and construction of AAV2 vectors with altered tropism. J Virol 74:8635–47
  • Xie Q, Bu W, Bhatia S, et al. (2002). The atomic structure of adeno-associated virus (AAV-2), a vector for human gene therapy. Proc Natl Acad Sci USA 99:10405–10
  • Xu R, Sun X, Tse LY, et al. (2003). Long-term expression of angiostatin suppresses metastatic liver cancer in mice. Hepatology 37:1451–60
  • Yuan L, Zhao H, Zhang L, Liu X. (2013). The efficacy of combination therapy using adeno-associated virus-mediated co-expression of apoptin and interleukin-24 on hepatocellular carcinoma. Tumor Biol 34:3027–34
  • Zhang Y, Ma H, Zhang J, et al. (2008). AAV-mediated TRAIL gene expression driven by hTERT promoter suppressed human hepatocellular carcinoma growth in mice. Life Sci 82:1154–61
  • Zhang Y, Ren JS, Shi JF, et al. (2015). International trends in primary liver cancer incidence from 1973 to 2007. BMC Cancer 15:94
  • Zincarelli C, Soltys S, Rengo G, Rabinowitz JE. (2008). Analysis of AAV serotypes 1–9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16:1073–80