Aerosol delivery of lentivirus-mediated O-glycosylation mutant osteopontin suppresses lung tumorigenesis in K-ras LA1 mice

Cellular Oncology

Volumn 36, Issue 1, 2013, Pages 15-26

  Minai Tehrani, Arash ^a   Chang, Seung Hee ^a   Kwon, Jung Taek ^a   Hwang, Soon Kyung ^a,f,g   Kim, Ji Eun ^a,b   Shin, Ji Young ^a   Yu, Kyeong Nam ^a   Park, Sung Jin ^a   Jiang, Hu Lin ^a   Kim, Ji Hye ^a,b   Hong, Seong Ho ^a   Kang, Bitna ^a   Kim, Duyeoul ^a   Chae, Chan Hee ^a   Lee, Kee Ho ^d   Beck, George R ^e   Cho, Myung Haing ^a,b,c  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University   (South Korea)

^d Korea Institute of Radiation and Medical Science   (South Korea)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

^g CHINA PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Aerosol delivery; Lung cancer; O glycosylation; Osteopontin

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OSTEOPONTIN;

AEROSOL; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GLYCOSYLATION; HUMAN; LENTIVIRINAE; LUNG CARCINOGENESIS; LUNG NON SMALL CELL CANCER; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 84877039629     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-012-0107-3     Document Type: Article

References (73)

1. A. Jemal, R. Siegel, J.Q. Xu, E. Ward, Cancer Statistics, 2010. CA Cancer J. Clin. 60, 277-300 (2010)
2. R. Govindan, J. Subramanian, D. Morgensztern, B. Goodgame, M.Q. Baggstrom, F. Gao, J. Piccirillo, Distinctive characteristics of Non-small Cell Lung Cancer (NSCLC) in the young a Surveillance, Epidemiology, and End Results (SEER) analysis. J. Thorac. Oncol. 5, 23-28 (2010)
3. C. Gridelli, P. Maione, A. Rossi, The potential role of mTOR inhibitors in non-small cell lung cancer. Oncologist 13, 139-147 (2008)
4. S.V. Fulzele, A. Chatterjee, M.S. Shaik, T. Jackson, M. Singh, Inhalation delivery and anti-tumor activity of celecoxib in human orthotopic non-small cell lung cancer xenograft model. Pharm. Res. 23, 2094-2106 (2006)
5. M. Kohlhaufl, K. Haussinger, F. Stanzel, A. Markus, J. Tritschler, A. Muhlhofer, A. Morresi-Hauf, I. Golly, G. Scheuch, B.H. Jany, H.K. Biesalski, Inhalation of aerosolized vitamin A: reversibility of metaplasia and dysplasia of human respiratory epithelia - a prospective pilot study. Eur. J. Med. Res. 7, 72-78 (2002)
6. L.V. Sequist, D.W. Bell, T.J. Lynch, D.A. Haber, Molecular predictors of response to epidermal growth factor receptor antagonists in non-small-cell lung cancer. J. Clin. Oncol. 25, 587-595 (2007)
7. T.J. Lynch, D.W. Bell, R. Sordella, Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med. 350, 2129-2139 (2004)
8. A. Gautam, C.L. Densmore, B. Xu, J.C. Waldrep, Enhanced gene expression in mouse lung after PEI-DNA aerosol delivery. Mol. Ther. 2, 63-70 (2000)
9. D.E. Zamora-Avila, P. Zapata-Benavides, M.A. Franco-Molina, S. Saavedra-Alonso, L.M. Trejo-Avila, D. Resendez-Perez, J.L. Mendez-Vazquez, J. Isaias-Badillo, C. Rodriguez-Padilla, WT1 gene silencing by aerosol delivery of PEI-RNAi complexes inhibits B16-F10 lung metastases growth. Cancer Gene Ther. 16, 892-899 (2009)
10. A.M. Tehrani, S.K. Hwang, T.H. Kim, C.S. Cho, J. Hua, W.S. Nah, J.T. Kwon, J.S. Kim, S.H. Chang, K.N. Yu, S.J. Park, D.R. Bhandari, K.H. Lee, G.H. An, G.R. Beck, M.H. Cho, Aerosol delivery of Akt controls protein translation in the lungs of dual luciferase reporter mice. Gene Ther. 14, 451-458 (2007)
11. S.K. Hwang, J.T. Kwon, S.J. Park, S.H. Chang, E.S. Lee, Y.S. Chung, G.R. Beck, K.H. Lee, L. Piao, J. Park, M.H. Cho, Lentivirus-mediated carboxyl-terminal modulator protein gene transfection via aerosol in lungs of K-ras null mice. Gene Ther. 14, 1721-1730 (2007)
12. D.C. Look, S.L. Brody, Engineering viral vectors to subvert the airway defense response. Am. J. Respir. Cell Mol. Biol. 20, 1103-1106 (1999)
13. H. Bueler, Adeno associated viral vectors for gene transfer and gene therapy. Biol. Chem. 380, 613-622 (1999)
14. E. Abordo-Adesida, A. Follenzi, C. Barcia, S. Sciascia, M.G. Castro, L. Naldini, P.R. Lowenstein, Stability of lentiviral vector-mediated transgene expression in the brain in the presence of systemic antivector immune responses. Hum. Gene Ther. 16, 741-751 (2005)
15. D.S. Anson, The use of retroviral vectors for gene therapy-what are the risks? A review of retroviral pathogenesis and its relevance to retroviral vector-mediated gene delivery. Genet. Vaccines Ther. 2, 9 (2004)
16. Y. Hu, D. Stout, L. Wu, A dual-targeted lentiviral vector homing in on prostate bone metastases. Mol. Ther. 15, 1906-1908 (2007)
17. K.N. Yu, A. Minai-Tehrani, S.H. Chang, S.K. Hwang, S.H. Hong, J.E. Kim, J.Y. Shin, S.J. Park, J.H. Kim, J.T. Kwon, H.L. Jiang, B. Kang, D. Kim, C.H. Chae, K.H. Lee, T.J. Yoon, G.R. Beck, M.H. Cho, Aerosol delivery of small hairpin osteopontin blocks pulmonary metastasis of breast cancer in mice. PLoS One 5, e15623 (2010)
18. S.R. Rittling, A.F. Chambers, Role of osteopontin in tumour progression. Br. J. Cancer 90, 1877-1881 (2004)
19. P.Y. Wai, P.C. Kuo, Osteopontin: regulation in tumor metastasis. Cancer Metastasis Rev. 27, 103-118 (2008)
20. N.S. Fedarko, A. Jain, A. Karadag, M.R. Van Eman, L.W. Fisher, Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clin. Cancer Res. 7, 4060-4066 (2001)
21. G.F. Weber, G.S. Lett, N.C. Haubein, Osteopontin is a marker for cancer aggressiveness and patient survival. Br. J. Cancer 103, 861-869 (2010)
22. B. Christensen, C.C. Kazanecki, T.E. Petersen, S.R. Rittling, D.T. Denhardt, E.S. Sorensen, Cell type-specific post-translational modifications of mouse osteopontin are associated with different adhesive properties. J. Biol. Chem. 282, 19463-19472 (2007)
23. M.A. Chellaiah, R.S. Biswas, S.R. Rittling, D.T. Denhardt, K.A. Hruska, Rho-dependent Rho kinase activation increases CD44 surface expression and bone resorption in osteoclasts. J. Biol. Chem. 278, 29086-29097 (2003)
24. A. Lopez-Ferrer, C. Barranco, C. de Bolos, Differences in the O-glycosylation patterns between lung squamous cell carcinoma and adenocarcinoma. Am. J. Clin. Pathol. 118, 749-755 (2002)
25. Y. Zhao, Y. Wang, W.G. Zhu, Applications of post-translational modifications of FoxO family proteins in biological functions. J. Mol. Cell Biol. 3, 276-282 (2011)
26. H.E. Miwa, T.A. Gerken, O. Jamison, L.A. Tabak, Isoform-specific O-glycosylation of osteopontin and bone sialoprotein by polypeptide N-acetylgalactosaminyltransferase-1. J. Biol. Chem. 285, 1208-1219 (2010)
27. H.Y. Lee, Y.A. Sub, J.I. Lee, K.A. Hassan, L. Mao, T. Force, B.E. Gilbert, T. Jacks, J.A. Kurie, Inhibition of oncogenic K-ras signaling by aerosolized gene delivery in a mouse model of human lung cancer. Clin. Cancer Res. 8, 2970-2975 (2002)
28. N.E. Mills, C.L. Fishman, W.N. Rom, N. Dubin, D.R. Jacobson, Increased prevalence of K-ras oncogene mutations in lung adenocarcinoma. Cancer Res. 55, 1444-1447 (1995)
29. J. Zhang, F. Takahashi, K. Shimizu, F. Ohshita, Y. Kameda, K. Maeda, K. Nishio, Y. Fukuchi, K. Takahashi, Differential osteopontin expression in lung cancer. Cancer Lett. 171, 215-222 (2001)
30. T. Jacks, L. Johnson, K. Mercer, D. Greenbaum, R.T. Bronson, D. Crowley, D.A. Tuveson, Somatic activation of the K-ras oncogene causes early onset lung cancer in mice. Nature 410, 1111-1116 (2001)
31. S.H. Chang, S.H. Hong, H.L. Jiang, A. Minai-Tehrani, K.N. Yu, J.H. Lee, J.E. Kim, J.Y. Shin, B. Kang, S. Park, K. Han, C.C. Chae, M.H. Cho, GOLGA2/GM130, cis-Golgi matrix protein, is a novel target of anticancer gene therapy. Mol. Ther. (2012). doi: 10.1038/mt.2012.125
32. B.W. Robertson, L. Bonsal, M.A. Chellaiah, Regulation of Erk1/2 activation by osteopontin in PC3 human prostate cancer cells. Mol. Cancer 9, 260 (2010)
33. V. Donati, L. Boldrini, M. Dell'Omodarme, M.C. Prati, P. Faviana, T. Camacci, M. Lucchi, A. Mussi, M. Santoro, F. Basolo, G. Fontanini, Osteopontin expression and prognostic significance in non-small cell lung cancer. Clin. Cancer Res. 11, 6459-6465 (2005)
34. M.A. Bjornsti, P.J. Houghton, The TOR pathway: a target for cancer therapy. Nat. Rev. Cancer 4, 335-348 (2004)
35. A.C. Gingras, S.P. Gygi, B. Raught, R.D. Polakiewicz, R.T. Abraham, M.F. Hoekstra, R. Aebersold, N. Sonenberg, Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev. 13, 1422-1437 (1999)
36. M.A. Lawlor, D.R. Alessi, PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J. Cell Sci. 114, 2903-2910 (2001)
37. M.M. Chaturvedi, B. Sung, V.R. Yadav, R. Kannappan, B.B. Aggarwal, NF-kappa B addiction and its role in cancer: 'one size does not fit all'. Oncogene 30, 1615-1630 (2011)
38. J. Folkman, Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29, 15-18 (2002)
39. R. Cui, F. Takahashi, R. Ohashi, T. Gu, M. Yoshioka, K. Nishio, Y. Ohe, S. Tominaga, Y. Takagi, S. Sasaki, Y. Fukuchi, K. Takahashi, Abrogation of the interaction between osteopontin and alpha v beta 3 integrin reduces tumor growth of human lung cancer cells in mice. Lung Cancer 57, 302-310 (2007)
40. G. Chakraborty, S. Jain, G.C. Kundu, Osteopontin promotes vascular endothelial growth factor-dependent breast tumor growth and angiogenesis via autocrine and paracrine mechanisms. Cancer Res. 68, 152-161 (2008)
41. D. Courter, H.B. Cao, S. Kwok, C. Kong, A. Banh, P.W. Kuo, D.M. Bouley, C. Vice, O.T. Brustugun, N.C. Denko, A.C. Koong, A. Giaccia, Q.T. Le, The RGD domain of human osteopontin promotes tumor growth and metastasis through activation of survival pathways. PLoS One 5, e9633 (2010)
42. V.T. Chang, M. Crispin, A.R. Aricescu, D.J. Harvey, J.E. Nettleship, J.A. Fennelly, C. Yu, K.S. Boles, E.J. Evans, D.I. Stuart, R.A. Dwek, E.Y. Jones, S.J. Davis, R.J. Owens, Glycoprotein structural genomics: solving the glycosylation problem. Structure 15, 267-273 (2007)
43. G. Patsos, C. Robbe-Masselot, A. Klein, V. Hebbe-Viton, R.S. Martin, D. Masselot, M. Graessmann, C. Paraskeva, T. Gallagher, A. Corfield, O-glycan regulation of apoptosis and proliferation in colorectal cancer cell lines. Biochem. Soc. Trans. 35, 1372-1374 (2007)
44. A. Varki, Glycan-based interactions involving vertebrate sialic-acid-recognizing proteins. Nature 446, 1023-1029 (2007)
45. F.A. Saad, E. Salih, M.J. Glimcher, Identification of osteopontin phosphorylation sites involved in bone remodeling and inhibition of pathological calcification. J. Cell. Biochem. 103, 852-856 (2008)
46. L.A. Tabak, K.G. Ten Hagen, D. Tetaert, F.K. Hagen, C. Richet, T.M. Beres, J. Gagnon, M.M. Balys, B. VanWuyckhuyse, G.S. Bedi, P. Degand, Characterization of a UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase that displays glycopeptide N-acetylgalactosaminyltransferase activity. J. Biol. Chem. 274, 27867-27874 (1999)
47. T.A. Gerken, C.L. Perrine, A. Ganguli, P. Wu, C.R. Bertozzi, T.A. Fritz, J. Raman, L.A. Tabak, Glycopeptide-preferring polypeptide GalNAc transferase 10 (ppGalNAc T10), involved in mucin-type O-Glycosylation, has a unique GalNAc-O-Ser/Thr-binding site in its catalytic domain not found in ppGalNAc T1 or T2. J. Biol. Chem. 284, 20387-20397 (2009)
48. K.J. Yarema, M.F. Murrell, A. Levchenko, The systems biology of glycosylation. ChemBioChem 5, 1334-1347 (2004)
49. D. Halter, S. Neumann, S.M. van Dijk, J. Wolthoorn, A.M. De Maziere, O.V. Vieira, P. Mattjus, J. Klumperman, G. van Meer, H. Sprong, Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J. Cell Biol. 179, 101-115 (2007)
50. I. Martinez-Duncker, R. Mollicone, P. Codogno, R. Oriol, The nucleotide-sugar transporter family: a phylogenetic approach. Biochimie 85, 245-260 (2003)
51. J.M. Schulz, K.L. Ross, K. Malmstrom, M. Krieger, J.L. Fridovich-Keil, Mediators of galactose sensitivity in UDP-galactose 4′-epimerase-impaired mammalian cells. J. Biol. Chem. 280, 13493-13502 (2005)
52. H.J. Gabius, S. Andre, H. Kaltner, H.C. Siebert, The sugar code: functional lectinomics. Biochim. Biophys. Acta 1572, 165-177 (2002)
53. M. Mann, O.N. Jensen, Proteomic analysis of post-translational modifications. Nat. Biotechnol. 21, 255-261 (2003)
54. C.C. Kazanecki, D.J. Uzwiak, D.T. Denhardt, Control of osteopontin signaling and function by post-translational phosphorylation and protein folding. J. Cell. Biochem. 102, 912-924 (2007)
55. I. Han, J.E. Kudlow, Reduced O glycosylation of Sp1 is associated with increased proteasome susceptibility. Mol. Cell. Biol. 17, 2550-2558 (1997)
56. Y.H. Lin, H.F. Yang-Yen, The osteopontin-CD44 survival signal involves activation of the phosphatidylinositol 3-kinase/Akt signaling pathway. J. Biol. Chem. 276, 46024-46030 (2001)
57. S.P. Jackson, R. Tjian, O-glycosylation of eukaryotic transcription factors: implications for mechanisms of transcriptional regulation. Cell 55, 125-133 (1988)
58. A. Gasbarri, F. Del Prete, L. Girnita, M.P. Martegani, P.G. Natali, A. Bartolazzi, CD44s adhesive function spontaneous and PMA-inducible CD44 cleavage are regulated at post-translational level in cells of melanocytic lineage. Melanoma Res. 13, 325-337 (2003)
59. R.J. Sola, K. Griebenow, Effects of glycosylation on the stability of protein pharmaceuticals. J. Pharm. Sci. 98, 1223-1245 (2009)
60. A.G. Bader, P.K. Vogt, An essential role for protein synthesis in oncogenic cellular transformation. Oncogene 23, 3145-3150 (2004)
61. M. Gromeier, C. Kaiser, E.Y. Dobrikova, S.S. Bradrick, M. Shveygert, J.T. Herbert, Activation of cap-independent translation by variant eukaryotic initiation factor 4G in vivo. RNA 14, 2170-2182 (2008)
62. A. Iacoangeli, Y. Lin, E.J. Morley, I.A. Muslimov, R. Bianchi, J. Reilly, J. Weedon, R. Diallo, W. Bocker, H. Tiedge, BC200 RNA in invasive and preinvasive breast cancer. Carcinogenesis 25, 2125-2133 (2004)
63. D.R. Gallie, K.S. Browning, eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J. Biol. Chem. 276, 36951-36960 (2001)
64. W.C. Merrick, Cap-dependent and cap-independent translation in eukaryotic systems. Gene 332, 1-11 (2004)
65. R. Zohar, B.Q. Zhu, P. Liu, J. Sodek, C.A. McCulloch, Increased cell death in osteopontin-deficient cardiac fibroblasts occurs by a caspase-3-independent pathway. Am. J. Physiol. Heart Circ. Physiol. 287, H1730-H1739 (2004)
66. A.P.B. Da Silva, A. Pollett, S.R. Rittling, D.T. Denhardt, J. Sodek, R. Zohar, Exacerbated tissue destruction in DSS-induced acute colitis of OPN-null mice is associated with downregulation of TNF-alpha expression and non-programmed cell death. J. Cell. Physiol. 208, 629-639 (2006)
67. K.X. Fan, J.X. Dai, H. Wang, H.F. Wei, Z.G. Cao, S. Hou, W.Z. Qian, H.Q. Wang, B. Li, J. Zhao, H.J. Xu, C.D. Yang, Y. Guo, Treatment of collagen-induced arthritis with an anti-osteopontin monoclonal antibody through promotion of apoptosis of both murine and human activated T cells. Arthritis Rheum. 58, 2041-2052 (2008)
68. Y.J. Guo, J. Zhao, L. Dong, B. Liu, G.B. Wu, D.M. Xu, J.J. Chen, K. Li, X. Tong, J.X. Dai, S. Yao, M.C. Wu, Down-regulation of osteopontin suppresses growth and metastasis of hepatocellular carcinoma via induction of apoptosis. Gastroenterology 135, 956-968 (2008)
69. M. Karin, Nuclear factor-kappa B in cancer development and progression. Nature 441, 431-436 (2006)
70. C. Nakanishi, M. Toi, Nuclear factor-kappa B inhibitors as sensitizers to anticancer drugs. Nat. Rev. Cancer 5, 297-309 (2005)
71. E. Dundar, U. Oner, B.C. Peker, M. Metintas, S. Isiksoy, G. Ak, The significance and relationship between mast cells and tumour angiogenesis in non-small cell lung carcinoma. J. Int. Med. Res. 36, 88-95 (2008)
72. S. Vidal, K. Kovacs, D. Bell, E. Horvath, B.W. Scheithauer, R.V. Lloyd, Cyclooxygenase-2 expression in human pituitary tumors. Cancer 97, 2814-2821 (2003)
73. A.B. Sandler, S.M. Dubinett, COX-2 inhibition and lung cancer. Semin. Oncol. 31, 45-52 (2004)