Asian Pacific Journal of Cancer Prevention

Asian Pacific Journal of Cancer Prevention (아시아태평양암예방학회)
권호 표지
DOI QR코드

DOI QR Code

A New Cancer Cell Detection Method Using an Infectivity-enhanced Adenoviral Vector

  • Uchino, Junji (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Takayama, Koichi (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Nakagaki, Noriaki (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Shuo, Wang (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Hisasue, Junko (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Nakatom, Keita (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Ohta, Keiichi (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Hirano, Ryosuke (Department of Respiratory Medicine, Fukuoka University Faculty of Medicine) ;
  • Tashiro, Naoki (Department of Respiratory Medicine, Fukuoka University Faculty of Medicine) ;
  • Miiru, Izumi (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University) ;
  • Fujita, Masaki (Department of Respiratory Medicine, Fukuoka University Faculty of Medicine) ;
  • Watanabe, Kentaro (Department of Respiratory Medicine, Fukuoka University Faculty of Medicine) ;
  • Nakanishi, Yoichi (Research Institute for Diseases of the Chest, Graduate School of Medical Sciences, Kyushu University)
  • Published : 2012.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

Cytological examination is widely used as a diagnostic tool because of the ease of collecting cells from the involved area. However, the diagnostic yield of cytological examination is unsatisfactory; the reasons include sampling error, poorly prepared samples, small numbers of malignant cells, and low grades of cellular atypia. In this study, we focused on the high infectivity of adenovirus towards epithelial cells and applied the luciferase-expressing adenoviral vector to a new cancer cell detection tool. In addition, adenoviral infectivity was enhanced by modifying viral fiber proteins. The sensitivity of the diagnostic tool was tested using the NCI-H1299 lung cancer cell line, and validated in body fluid samples from cancer patients with a variety of etiology. Results showed that the adenovirus efficiently transfected NCI-H1299 with high sensitivity. Only 10 cancer cells were sufficient for detection of luciferase signals. In body fluid samples, the adenovirus confirmed the diagnosis for malignant and benign cancer, but not in non-epithelial cell derived samples. This study provides proof-of-concept for a more reliable and sensitive diagnostic tool for epithelium-derived cancer.

Keywords

References

  1. Adachi Y, Reynolds P N, Yamamoto M, et al. (2001). A midkine promoter-based conditionally replicative adenovirus for treatment of pediatric solid tumors and bone marrow tumor purging. Cancer Res, 61, 7882-8.
  2. Antunes G, Neville E. (2000). Management of malignant pleural effusions. Thorax, 55, 981-3. https://doi.org/10.1136/thorax.55.12.981
  3. Benlloch S, Galbis-Caravajal J.M, Martin C, et al. (2006). Potential diagnostic value of methylation profile in pleural fluid and serum from cancer patients with pleural effusion. Cancer, 107, 1859-65. https://doi.org/10.1002/cncr.22190
  4. Davidson B. (2004). Malignant effusions: from diagnosis to biology. Diagnostic cytopathology, 31, 246-54. https://doi.org/10.1002/dc.20133
  5. Fiegl M. (2005). The utility of fluorescence in-situ hybridization in the diagnosis of malignant pleural effusion. Curr Opin Pulm Med, 11, 313-8. https://doi.org/10.1097/01.mcp.0000166491.92659.5e
  6. Fishman AP, Fishman JAE, Grippi MA (2008). Malignant Pleural Effuions. In Fishman's pulmonary diseases and disorders (A.P. Fishman ed.). pp. 1506-15. McGraw-Hill Medical, New York
  7. Garcia-Bonafe M, Moragas A. (1996). Differential diagnosis of malignant and reactive cells from serous effusions: image and texture analysis study. Anal Cell Pathol, 12, 85-98.
  8. Hausheer F H, Yarbro J W (1987). Diagnosis and treatment of malignant pleural effusion. Cancer Metastasis Rev, 6, 23-40. https://doi.org/10.1007/BF00047607
  9. He T C, Zhou S, da Costa L T, et al. (1998). A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA, 95, 2509-14. https://doi.org/10.1073/pnas.95.5.2509
  10. Heffner J E, Klein J S (2008). Recent advances in the diagnosis and management of malignant pleural effusions. Mayo Clinic proceedings. Mayo Clinic, 83, 235-50. https://doi.org/10.1016/S0025-6196(11)60848-3
  11. Hemmi S, Geertsen R, Mezzacasa A, Peter I, Dummer R. (1998). The presence of human coxsackievirus and adenovirus receptor is associated with efficient adenovirus-mediated transgene expression in human melanoma cell cultures. Hum Gene Ther, 9, 2363-73. https://doi.org/10.1089/hum.1998.9.16-2363
  12. Henschke C I, Yankelevitz D F, Davis S D (1991). Pleural diseases: multimodality imaging and clinical management. Curr Probl Diagn Radiol, 20, 155-81. https://doi.org/10.1016/0363-0188(91)90020-3
  13. Holloway A J, Diyagama D S, Opeskin K, et al. (2006). A molecular diagnostic test for distinguishing lung adenocarcinoma from malignant mesothelioma using cells collected from pleural effusions. Clin Cancer Res, 12, 5129-35. https://doi.org/10.1158/1078-0432.CCR-06-1027
  14. Kaner R J, Worgall S, Leopold P L, et al. (1999). Modification of the genetic program of human alveolar macrophages by adenovirus vectors in vitro is feasible but inefficient, limited in part by the low level of expression of the coxsackie/ adenovirus receptor. Am J Respir Cell Mol Biol, 20, 361-70. https://doi.org/10.1165/ajrcmb.20.3.3398
  15. Kanerva A, Mikheeva G V, Krasnykh V, et al. (2002). Targeting adenovirus to the serotype 3 receptor increases gene transfer efficiency to ovarian cancer cells. Clin Cancer Res, 8, 275-80.
  16. Kawakami Y, Li H, Lam J.T, et al. (2003). Substitution of the adenovirus serotype 5 knob with a serotype 3 knob enhances multiple steps in virus replication. Cancer Res, 63, 1262-9.
  17. Kuenen-Boumeester V, van Loenen P, de Bruijn E.M. and Henzen-Logmans S.C. (1996). Quality control of immunocytochemical staining of effusions using a standardized method of cell processing. Acta Cytol, 40, 475-9. https://doi.org/10.1159/000333902
  18. Lee J H, Chang J H (2005). Diagnostic utility of serum and pleural fluid carcinoembryonic antigen, neuron-specific enolase, and cytokeratin 19 fragments in patients with effusions from primary lung cancer. Chest, 128, 2298-303. https://doi.org/10.1378/chest.128.4.2298
  19. Lyons M, Onion D, Green N.K, et al (2006). Adenovirus type 5 interactions with human blood cells may compromise systemic delivery. Mol Ther, 14, 118-28. https://doi.org/10.1016/j.ymthe.2006.01.003
  20. Martinez-Moragon E, Aparicio J, Sanchis J, et al. (1998). Malignant pleural effusion: prognostic factors for survival and response to chemical pleurodesis in a series of 120 cases. Respiration, 65, 108-13. https://doi.org/10.1159/000029240
  21. Miller C R, Buchsbaum D J, Reynolds P N, et al (1998). Differential susceptibility of primary and established human glioma cells to adenovirus infection: targeting via the epidermal growth factor receptor achieves fiber receptorindependent gene transfer. Cancer Res, 58, 5738-48.
  22. Motherby H, Kube M, Friedrichs N, et al. (1999). Immunocytochemistry and DNA-image cytometry in diagnostic effusion cytology I. Prevalence of markers in tumour cell positive and negative smears. Anal Cell Pathol, 19, 7-20. https://doi.org/10.1155/1999/459158
  23. Motherby H, Pomjanski N, Kube M, et al. (2002). Diagnostic DNA-flow-vs. -image-cytometry in effusion cytology. Anal Cell Pathol, 24, 5-15. https://doi.org/10.1155/2002/840210
  24. Nalbantoglu J, Larochelle N, Wolf E, et al. (2001). Musclespecific overexpression of the adenovirus primary receptor CAR overcomes low efficiency of gene transfer to mature skeletal muscle. J Virol, 75, 4276-82. https://doi.org/10.1128/JVI.75.9.4276-4282.2001
  25. Nance K V, Shermer R W, Askin F B (1991), Diagnostic efficacy of pleural biopsy as compared with that of pleural fluid examination. Mod Pathol, 4, 320-4.
  26. Northup J.K, Gadre S A, Ge Y, Lockhart L H Velagaleti G V (2007). Do cytogenetic abnormalities precede morphologic abnormalities in a developing malignant condition? Eur J Haematol, 78, 152-6.
  27. Osterheld MC, Liette C, Anca M. (2005). Image cytometry: an aid for cytological diagnosis of pleural effusions. Diagnostic cytopathology, 32, 173-6. https://doi.org/10.1002/dc.20205
  28. Porcel JM, Vives M, Esquerda A, et al. (2004). Use of a panel of tumor markers (carcinoembryonic antigen, cancer antigen 125, carbohydrate antigen 15-3, and cytokeratin 19 fragments) in pleural fluid for the differential diagnosis of benign and malignant effusions. Chest, 126, 1757-63. https://doi.org/10.1378/chest.126.6.1757
  29. Shitrit D, Zingerman B, Shitrit A.B, Shlomi D, Kramer M R (2005). Diagnostic value of CYFRA 21-1, CEA, CA 19-9, CA 15-3, and CA 125 assays in pleural effusions: analysis of 116 cases and review of the literature. Oncologist, 10, 501-7. https://doi.org/10.1634/theoncologist.10-7-501
  30. Sriram K B, Relan V, Clarke B E, et al. (2011). Diagnostic molecular biomarkers for malignant pleural effusions. Future Oncol, 7, 737-52. https://doi.org/10.2217/fon.11.45
  31. Starr R.L. and Sherman M.E. (1991). The value of multiple preparations in the diagnosis of malignant pleural effusions. A cost-benefit analysis. Acta Cytol, 35, 533-7.
  32. Su X Y, Li G D, Liu W P, Xie B, Jiang YH (2011). Cytological differential diagnosis among adenocarcinoma, epithelial mesothelioma, and reactive mesothelial cells in serous effusions by immunocytochemistry. Diagnostic cytopathology, 39, 900-8. https://doi.org/10.1002/dc.21489
  33. Takayama K, Reynolds P N, Short J J, et al (2003). A mosaic adenovirus possessing serotype Ad5 and serotype Ad3 knobs exhibits expanded tropism. Virology, 309, 282-93. https://doi.org/10.1016/S0042-6822(03)00067-9
  34. Westfall D E, Fan X, Marchevsky A M (2010). Evidence-based guidelines to optimize the selection of antibody panels in cytopathology: pleural effusions with malignant epithelioid cells. Diagnostic cytopathology, 38, 9-14.
  35. Woenckhaus M, Grepmeier U, Werner B, et al. (2005). Microsatellite analysis of pleural supernatants could increase sensitivity of pleural fluid cytology. J Mol Diagn, 7, 517-24. https://doi.org/10.1016/S1525-1578(10)60583-1
  36. Zabner J, Freimuth P, Puga A, Fabrega A, Welsh M,J (1997). Lack of high affinity fiber receptor activity explains the resistance of ciliated airway epithelia to adenovirus infection. J Clin Invest, 100, 1144-9. https://doi.org/10.1172/JCI119625