Targeting L1 cell adhesion molecule using lentivirus-mediated short hairpin RNA interference reverses aggressiveness of oral squamous cell carcinoma

Molecular Pharmaceutics

Volumn 7, Issue 6, 2010, Pages 2312-2323

  Hung, Shiao Chen ^a   Wu, I Hui ^a   Hsue, Shui Sang ^b   Liao, Chia Hui ^a   Wang, Hsien Chi ^a,c   Chuang, Pei Hsin ^a   Sung, Shian Ying ^a,d   Hsieh, Chia Ling ^a,d  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b TAIPEI MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d ASIA UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; FIBRONECTIN; LENTIVIRUS VECTOR; NERVE CELL ADHESION MOLECULE L1; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN; VIMENTIN;

ADVANCED CANCER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER INVASION; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; DRUG TARGETING; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; KERATINOCYTE; LYMPH NODE METASTASIS; MALE; MESENCHYME; MOUSE; MOUTH CARCINOMA; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SQUAMOUS CELL CARCINOMA; TUMOR GROWTH;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL CYCLE; CELL PROLIFERATION; DRUG SCREENING ASSAYS, ANTITUMOR; HUMANS; LENTIVIRUS; MICE; MICE, NUDE; MOUTH NEOPLASMS; NEURAL CELL ADHESION MOLECULE L1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED;

EID: 78649974512     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp1002834     Document Type: Article

References (54)

1. Jemal, A.; Siegel, R.; Ward, E.; Hao, Y.; Xu, J.; Thun, M. J. Cancer statistics, 2009 Ca-Cancer J. Clin. 2009, 59 (4) 225-49
2. Parkin, D. M.; Laara, E.; Muir, C. S. Estimates of the worldwide frequency of sixteen major cancers in 1980 Int. J. Cancer 1988, 41 (2) 184-97
3. Hindle, I.; Nally, F. Oral cancer: a comparative study between 1962-67 and 1980-84 in England and Wales Br. Dent. J. 1991, 170 (1) 15-20
4. Warnakulasuriya, S. Global epidemiology of oral and oropharyngeal cancer Oral Oncol. 2009, 45 (4-5) 309-16
5. Khuri, F. R.; Shin, D. M.; Glisson, B. S.; Lippman, S. M.; Hong, W. K. Treatment of patients with recurrent or metastatic squamous cell carcinoma of the head and neck: current status and future directions Semin. Oncol. 2000, 27 (4 Suppl. 8) 25-33
6. Khalili, J. Oral cancer: risk factors, prevention and diagnostic Exp. Oncol. 2008, 30 (4) 259-64
7. Makrilia, N.; Kollias, A.; Manolopoulos, L.; Syrigos, K. Cell adhesion molecules: role and clinical significance in cancer Cancer Invest. 2009, 27 (10) 1023-37
8. Liapis, H.; Flath, A.; Kitazawa, S. Integrin alpha V beta 3 expression by bone-residing breast cancer metastases Diagn. Mol. Pathol. 1996, 5 (2) 127-35
9. Brakebusch, C.; Bouvard, D.; Stanchi, F.; Sakai, T.; Fassler, R. Integrins in invasive growth J. Clin. Invest. 2002, 109 (8) 999-1006
10. Patriarca, C.; Alfano, R. M.; Sonnenberg, A.; Graziani, D.; Cassani, B.; de Melker, A.; Colombo, P.; Languino, L. R.; Fornaro, M.; Warren, W. H.; Coggi, G.; Gould, V. E. Integrin laminin receptor profile of pulmonary squamous cell and adenocarcinomas Hum. Pathol. 1998, 29 (11) 1208-15
11. Fornaro, M.; Tallini, G.; Bofetiado, C. J.; Bosari, S.; Languino, L. R. Down-regulation of beta 1C integrin, an inhibitor of cell proliferation, in prostate carcinoma Am. J. Pathol. 1996, 149 (3) 765-73
12. Yoshida, R.; Kimura, N.; Harada, Y.; Ohuchi, N. The loss of E-cadherin, alpha- and beta-catenin expression is associated with metastasis and poor prognosis in invasive breast cancer Int. J. Oncol. 2001, 18 (3) 513-20
13. Tomita, K.; van Bokhoven, A.; van Leenders, G. J.; Ruijter, E. T.; Jansen, C. F.; Bussemakers, M. J.; Schalken, J. A. Cadherin switching in human prostate cancer progression Cancer Res. 2000, 60 (13) 3650-4
14. Margineanu, E.; Cotrutz, C. E.; Cotrutz, C. Correlation between E-cadherin abnormal expressions in different types of cancer and the process of metastasis Rev. Med.-Chir. Soc. Med. Nat. Iasi 2008, 112 (2) 432-6
15. Gavert, N.; Ben-Shmuel, A.; Raveh, S.; Ben-Ze'ev, A. L1-CAM in cancerous tissues Expert Opin. Biol. Ther. 2008, 8 (11) 1749-57
16. Hortsch, M. Structural and functional evolution of the L1 family: are four adhesion molecules better than one Mol. Cell. Neurosci. 2000, 15 (1) 1-10
17. Lindner, J.; Rathjen, F. G.; Schachner, M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum Nature 1983, 305 (5933) 427-30
18. Maness, P. F.; Schachner, M. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration Nat. Neurosci. 2007, 10 (1) 19-26
19. Haspel, J.; Grumet, M. The L1CAM extracellular region: a multi-domain protein with modular and cooperative binding modes Front. Biosci. 2003, 8 s1210-25
20. Gutwein, P.; Oleszewski, M.; Mechtersheimer, S.; Agmon-Levin, N.; Krauss, K.; Altevogt, P. Role of Src kinases in the ADAM-mediated release of L1 adhesion molecule from human tumor cells J. Biol. Chem. 2000, 275 (20) 15490-7
21. Naus, S.; Richter, M.; Wildeboer, D.; Moss, M.; Schachner, M.; Bartsch, J. W. Ectodomain shedding of the neural recognition molecule CHL1 by the metalloprotease-disintegrin ADAM8 promotes neurite outgrowth and suppresses neuronal cell death J. Biol. Chem. 2004, 279 (16) 16083-90
22. Ebeling, O.; Duczmal, A.; Aigner, S.; Geiger, C.; Schollhammer, S.; Kemshead, J. T.; Moller, P.; Schwartz-Albiez, R.; Altevogt, P. L1 adhesion molecule on human lymphocytes and monocytes: expression and involvement in binding to alpha v beta 3 integrin Eur. J. Immunol. 1996, 26 (10) 2508-16
23. Debiec, H.; Christensen, E. I.; Ronco, P. M. The cell adhesion molecule L1 is developmentally regulated in the renal epithelium and is involved in kidney branching morphogenesis J. Cell Biol. 1998, 143 (7) 2067-79
24. Nolte, C.; Moos, M.; Schachner, M. Immunolocalization of the neural cell adhesion molecule L1 in epithelia of rodents Cell Tissue Res. 1999, 298 (2) 261-73
25. Pancook, J. D.; Reisfeld, R. A.; Varki, N.; Vitiello, A.; Fox, R. I.; Montgomery, A. M. Expression and regulation of the neural cell adhesion molecule L1 on human cells of myelomonocytic and lymphoid origin J. Immunol. 1997, 158 (9) 4413-21
26. Thies, A.; Schachner, M.; Moll, I.; Berger, J.; Schulze, H. J.; Brunner, G.; Schumacher, U. Overexpression of the cell adhesion molecule L1 is associated with metastasis in cutaneous malignant melanoma Eur. J. Cancer 2002, 38 (13) 1708-16
27. Allory, Y.; Matsuoka, Y.; Bazille, C.; Christensen, E. I.; Ronco, P.; Debiec, H. The L1 cell adhesion molecule is induced in renal cancer cells and correlates with metastasis in clear cell carcinomas Clin. Cancer Res. 2005, 11 (3) 1190-7
28. Boo, Y. J.; Park, J. M.; Kim, J.; Chae, Y. S.; Min, B. W.; Um, J. W.; Moon, H. Y. L1 Expression as a Marker for Poor Prognosis, Tumor Progression, and Short Survival in Patients with Colorectal Cancer Ann. Surg. Oncol. 2007, 14 (5) 1703-11
29. Kettunen, E.; Nicholson, A. G.; Nagy, B.; Wikman, H.; Seppanen, J. K.; Stjernvall, T.; Ollikainen, T.; Kinnula, V.; Nordling, S.; Hollmen, J.; Anttila, S.; Knuutila, S. L1CAM, INP10, P-cadherin, tPA and ITGB4 over-expression in malignant pleural mesotheliomas revealed by combined use of cDNA and tissue microarray Carcinogenesis 2005, 26 (1) 17-25
30. Daponte, A.; Kostopoulou, E.; Kollia, P.; Papamichali, R.; Vanakara, P.; Hadjichristodoulou, C.; Nakou, M.; Samara, S.; Koukoulis, G.; Messinis, I. E. L1 (CAM) (CD171) in ovarian serous neoplasms Eur. J. Gynaecol. Oncol. 2008, 29 (1) 26-30
31. Fogel, M.; Gutwein, P.; Mechtersheimer, S.; Riedle, S.; Stoeck, A.; Smirnov, A.; Edler, L.; Ben-Arie, A.; Huszar, M.; Altevogt, P. L1 expression as a predictor of progression and survival in patients with uterine and ovarian carcinomas Lancet 2003, 362 (9387) 869-75
32. Tan, K. D.; Zhu, Y.; Tan, H. K.; Rajasegaran, V.; Aggarwal, A.; Wu, J.; Wu, H. Y.; Hwang, J.; Lim, D. T.; Soo, K. C.; Tan, P. Amplification and overexpression of PPFIA1, a putative 11q13 invasion suppressor gene, in head and neck squamous cell carcinoma Genes, Chromosomes Cancer 2008, 47 (4) 353-62
33. Hsieh, C. L.; Chen, B. F.; Wang, C. C.; Liu, H. H.; Chen, D. S.; Hwang, L. H. Improved gene expression by a modified bicistronic retroviral vector Biochem. Biophys. Res. Commun. 1995, 214 (3) 910-7
34. Hsieh, C. L.; Pang, V. F.; Chen, D. S.; Hwang, L. H. Regression of established mouse leukemia by GM-CSF-transduced tumor vaccine: implications for cytotoxic T lymphocyte responses and tumor burdens Hum. Gene Ther. 1997, 8 (16) 1843-54
35. Hsieh, C. L.; Xie, Z.; Yu, J.; Martin, W. D.; Datta, M. W.; Wu, G. J.; Chung, L. W. Non-invasive bioluminescent detection of prostate cancer growth and metastasis in a bigenic transgenic mouse model Prostate 2007, 67 (7) 685-91
36. Myers, J. N.; Holsinger, F. C.; Jasser, S. A.; Bekele, B. N.; Fidler, I. J. An orthotopic nude mouse model of oral tongue squamous cell carcinoma Clin. Cancer Res. 2002, 8 (1) 293-8
37. Bisanz, K.; Yu, J.; Edlund, M.; Spohn, B.; Hung, M. C.; Chung, L. W.; Hsieh, C. L. Targeting ECM-integrin interaction with liposome-encapsulated small interfering RNAs inhibits the growth of human prostate cancer in a bone xenograft imaging model Mol. Ther. 2005, 12 (4) 634-43
38. Thiery, J. P. Epithelial-mesenchymal transitions in tumour progression Nat. Rev. Cancer 2002, 2 (6) 442-54
39. Beavon, I. R. The E-cadherin-catenin complex in tumour metastasis: structure, function and regulation Eur. J. Cancer 2000, 36 (13 Spec. No.) 1607-20
40. Steinert, P. M.; Roop, D. R. Molecular and cellular biology of intermediate filaments Annu. Rev. Biochem. 1988, 57, 593-625
41. Shook, D.; Keller, R. Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development Mech. Dev. 2003, 120 (11) 1351-83
42. Macfarlane, G. J.; Boyle, P.; Evstifeeva, T. V.; Robertson, C.; Scully, C. Rising trends of oral cancer mortality among males worldwide: the return of an old public health problem Cancer, Causes Control 1994, 5 (3) 259-65
43. Chung, C. H.; Parker, J. S.; Ely, K.; Carter, J.; Yi, Y.; Murphy, B. A.; Ang, K. K.; El-Naggar, A. K.; Zanation, A. M.; Cmelak, A. J.; Levy, S.; Slebos, R. J.; Yarbrough, W. G. Gene expression profiles identify epithelial-to- mesenchymal transition and activation of nuclear factor-kappaB signaling as characteristics of a high-risk head and neck squamous cell carcinoma Cancer Res. 2006, 66 (16) 8210-8
44. Yang, M. H.; Chang, S. Y.; Chiou, S. H.; Liu, C. J.; Chi, C. W.; Chen, P. M.; Teng, S. C.; Wu, K. J. Overexpression of NBS1 induces epithelial- mesenchymal transition and co-expression of NBS1 and Snail predicts metastasis of head and neck cancer Oncogene 2007, 26 (10) 1459-67
45. Shtutman, M.; Levina, E.; Ohouo, P.; Baig, M.; Roninson, I. B. Cell adhesion molecule L1 disrupts E-cadherin-containing adherens junctions and increases scattering and motility of MCF7 breast carcinoma cells Cancer Res. 2006, 66 (23) 11370-80
46. Batlle, E.; Sancho, E.; Franci, C.; Dominguez, D.; Monfar, M.; Baulida, J.; Garcia De Herreros, A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells Nat. Cell Biol. 2000, 2 (2) 84-9
47. Cano, A.; Perez-Moreno, M. A.; Rodrigo, I.; Locascio, A.; Blanco, M. J.; del Barrio, M. G.; Portillo, F.; Nieto, M. A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression Nat. Cell Biol. 2000, 2 (2) 76-83
48. Silletti, S.; Yebra, M.; Perez, B.; Cirulli, V.; McMahon, M.; Montgomery, A. M. Extracellular signal-regulated kinase (ERK)-dependent gene expression contributes to L1 cell adhesion molecule-dependent motility and invasion J. Biol. Chem. 2004, 279 (28) 28880-8
49. Shtutman, M.; Zhurinsky, J.; Simcha, I.; Albanese, C.; D'Amico, M.; Pestell, R.; Ben-Ze'ev, A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (10) 5522-7
50. Yochum, G. S.; Cleland, R.; Goodman, R. H. A genome-wide screen for beta-catenin binding sites identifies a downstream enhancer element that controls c-Myc gene expression Mol. Cell. Biol. 2008, 28 (24) 7368-79
51. Miyamoto, R.; Uzawa, N.; Nagaoka, S.; Hirata, Y.; Amagasa, T. Prognostic significance of cyclin D1 amplification and overexpression in oral squamous cell carcinomas Oral Oncol. 2003, 39 (6) 610-8
52. Eversole, L. R.; Sapp, J. P. c-myc oncoprotein expression in oral precancerous and early cancerous lesions Eur. J. Cancer B Oral Oncol. 1993, 29B (2) 131-5
53. Arlt, M. J.; Novak-Hofer, I.; Gast, D.; Gschwend, V.; Moldenhauer, G.; Grunberg, J.; Honer, M.; Schubiger, P. A.; Altevogt, P.; Kruger, A. Efficient inhibition of intra-peritoneal tumor growth and dissemination of human ovarian carcinoma cells in nude mice by anti-L1-cell adhesion molecule monoclonal antibody treatment Cancer Res. 2006, 66 (2) 936-43
54. Riedle, S.; Kiefel, H.; Gast, D.; Bondong, S.; Wolterink, S.; Gutwein, P.; Altevogt, P. Nuclear translocation and signalling of L1-CAM in human carcinoma cells requires ADAM10 and presenilin/gamma-secretase activity Biochem. J. 2009, 420 (3) 391-402