Mechanism and efficacy of sub-50-nm tenfibgen nanocapsules for cancer cell-directed delivery of anti-CK2 RNAi to primary and metastatic squamous cell carcinoma

Molecular Cancer Therapeutics

Volumn 13, Issue 8, 2014, Pages 2018-2029

  Unger, Gretchen M ^a   Kren, Betsy T ^b,d   Korman, Vicci L ^a   Kimbrough, Tyler G ^b   Vogel, Rachel I ^d   Ondrey, Frank G ^b   Trembley, Janeen H ^c,d,e   Ahmed, Khalil ^b,c,d,e  

^a GeneSegues   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; CASEIN KINASE II; FIBRINOGEN; MESSENGER RNA; NANOCAPSULE; OLIGONUCLEOTIDE; RNA INDUCED SILENCING COMPLEX; TENFIBGEN; UNCLASSIFIED DRUG; ARGONAUTE PROTEIN; EIF2C2 PROTEIN, HUMAN; PEPTIDE FRAGMENT; SMALL INTERFERING RNA; TENASCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CANCER INHIBITION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; FEMALE; HEAD AND NECK SQUAMOUS CELL CARCINOMA; LIPID RAFT; LONG TERM SURVIVAL; METASTASIS; MOUSE; NONHUMAN; PRIMARY TUMOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SPLEEN TUMOR; ANIMAL; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; CARCINOMA, SQUAMOUS CELL; CELL MEMBRANE; CHEMISTRY; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; HEAD AND NECK NEOPLASMS; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PATHOLOGY; SECONDARY; SPLENIC NEOPLASMS; TISSUE DISTRIBUTION;

ANIMALS; ARGONAUTE PROTEINS; BASE SEQUENCE; CARCINOMA, SQUAMOUS CELL; CASEIN KINASE II; FEMALE; GENE KNOCKDOWN TECHNIQUES; HEAD AND NECK NEOPLASMS; HUMANS; MEMBRANE MICRODOMAINS; MICE, INBRED BALB C; MICE, NUDE; NANOCAPSULES; NEOPLASM TRANSPLANTATION; PEPTIDE FRAGMENTS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SPLENIC NEOPLASMS; TENASCIN; TISSUE DISTRIBUTION; TRANSFECTION;

EID: 84905656155     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0166     Document Type: Article

References (50)

1. American Cancer Society. Cancer facts & figures 2014. 2014 [cited 2014 Apr 28]. Atlanta: American Cancer Society; 2014. Available from: http://www.cancer.org/acs/groups/content/@research/documents/webcontent/ acspc-042151.pdf.
2. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer 2011;11:9-22.
3. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011;29:4294-301.
4. Vermorken JB, Guigay J, Mesia R, Trigo JM, Keilholz U, Kerber A, et al. Phase I/II trial of cilengitide with cetuximab, cisplatin and 5-fluorouracil in recurrent and/or metastatic squamous cell cancer of the head and neck: findings of the phase I part. Br J Cancer 2011;104:1691-6.
5. Guerra B, Issinger OG. Protein kinase CK2 in human diseases. Curr Med Chem 2008;15:1870-86.
6. Ruzzene M, Pinna LA. Addiction to protein kinase CK2: a common denominator of diverse cancer cells? Biochim Biophys Acta 2010;1804:499-504.
7. Trembley JH, Wang G, Unger G, Slaton J, Ahmed K. Protein kinase CK2in health and disease: CK2: a key player in cancer biology. Cell Mol Life Sci 2009;66:1858-67.
8. Gapany M, Faust RA, Tawfic S, Davis A, Adams GL, Ahmed K. Association of elevated protein kinase CK2 activity with aggressive behavior of squamous cell carcinoma of the head and neck. Mol Med 1995;1:659-66.
9. Tawfic S, Yu S, Wang H, Faust R, Davis A, Ahmed K. Protein kinase CK2 signal in neoplasia. Histol Histopathol 2001;16:573-82. (Pubitemid 32297655)
10. Trembley JH, Chen Z, Unger G, Slaton J, Kren BT, Van Waes C, et al. Emergence of protein kinase CK2 as a key target in cancer therapy. BioFactors 2010;36:187-95.
11. Guo C, Yu S, Davis AT, Wang H, Green JE, Ahmed K. A potential role of nuclear matrix-associated protein kinase CK2 in protection against drug-induced apoptosis in cancer cells. J Biol Chem 2001;276:5992-9.
12. Ahmed K, Gerber DA, Cochet C. Joining the cell survival squad: an emerging role for protein kinase CK2. Trends Cell Biol 2002;12:226-30. (Pubitemid 34327615)
13. Faust RA, Tawfic S, Davis AT, Bubash LA, Ahmed K. Antisense oligonucleotides against protein kinase CK2-α inhibit growth of squamous cell carcinoma of the head and neck in vitro. Head Neck 2000;22:341-6. (Pubitemid 30413298)
14. Wang H, Davis A, Yu S, Ahmed K. Response of cancer cells to molecular interruption of the CK2 signal. Mol Cell Biochem 2001;227:167-74. (Pubitemid 34048381)
15. Unger GM, Davis AT, Slaton JW, Ahmed K. Protein kinase CK2 as regulator of cell survival: implications for cancer therapy. Curr Cancer Drug Targets 2004;4:77-84. (Pubitemid 38332566)
16. Wang G, Unger G, Ahmad KA, Slaton JW, Ahmed K. Downregulation of CK2 induces apoptosis in cancer cells-a potential approach to cancer therapy. Mol Cell Biochem 2005;274:77-84. (Pubitemid 41001503)
17. Slaton JW, Unger GM, Sloper DT, Davis AT, Ahmed K. Induction of apoptosis by antisense CK2 in human prostate cancer xenograft model. Mol Cancer Res 2004;2:712-21.
18. Trembley JH, Unger GM, Tobolt DK, Korman VL, Wang G, Ahmad KA, et al. Systemic administration of antisense oligonucleotides simultaneously targeting CK2alpha and alpha′ subunits reduces orthotopic xenograft prostate tumors in mice. Mol Cell Biochem 2011;356:21-35.
19. Prudent R, Moucadel V, Lopez-Ramos M, Aci S, Laudet B, Mouawad L, et al. Expanding the chemical diversity of CK2 inhibitors. Mol Cell Biochem 2008;316:71-85.
20. Pagano MA, Bain J, Kazimierczuk Z, Sarno S, Ruzzene M, Di Maira G, et al. The selectivity of inhibitors of protein kinase CK2: an update. Biochem J 2008;415:353-65.
21. Siddiqui-Jain A, Drygin D, Streiner N, Chua P, Pierre F, O'Brien SE, et al. CX-4945, an orally bioavailable selective inhibitor of protein kinase CK2, inhibits prosurvival and angiogenic signaling and exhibits antitumor efficacy. Cancer Res 2010;70:10288-98.
22. Faust RA, Niehans G, Gapany M, Hoistad D, Knapp D, Cherwitz D, et al. Subcellular immunolocalization of protein kinase CK2 in normal and carcinoma cells. Int J Biochem Cell Biol 1999;31:941-9. (Pubitemid 29406120)
23. Brown MS, Diallo OT, Hu M, Ehsanian R, Yang X, Arun P, et al. CK2 modulation of NF-κB, TP53, and the malignant phenotype in head and neck cancer by anti-CK2 oligonucleotides in vitro or in vivo via sub-50-nm nanocapsules. Clin Cancer Res 2010;16:2295-307.
24. Unger G, Trembley J, Kren B, Ahmed K. Nanoparticles in cancer therapy.Schwab M (Ed) Encyclopedia of Cancer: SpringerReference. Jan 31, 2012 ed: Springer-Verlag Berlin Heidelberg, 2009; 2012. p. 1-4.
25. Trembley JH, Unger GM, Korman VL, Tobolt DK, Kazimierczuk Z, Pinna LA, et al. Nanoencapsulated anti-CK2 small molecule drug or siRNA specifically targets malignant cancer but not benign cells. Cancer Lett 2012;315:48-58.
26. Erickson HP, Bourdon MA. Tenascin: an extracellular matrix protein prominent in specialized embryonic tissues and tumors. Annu Rev Cell Biol 1989;5:71-92. (Pubitemid 19286679)
27. Aukhil I, Joshi P, Yan Y, Erickson HP. Cell- and heparin-binding domains of the hexabrachion arm identified by tenascin expression proteins. J Biol Chem 1993;268:2542-53. (Pubitemid 23057877)
28. Yokoyama K, Erickson HP, Ikeda Y, Takada Y. Identification of amino acid sequences in fibrinogen gamma -chain and tenascin C C-terminal domains critical for binding to integrin alpha vbeta 3. J Biol Chem 2000;275:16891-8. (Pubitemid 30398926)
29. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer 2010;10:9-22.
30. Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med 2011;17:867-74.
31. Van Obberghen-Schilling E, Tucker RP, Saupe F, Gasser I, Cseh B, Orend G. Fibronectin and tenascin-C: accomplices in vascular morphogenesis during development and tumor growth. Int J Dev Biol 2011;55:511-25.
32. Schellekens H. Factors influencing the immunogenicity of therapeutic proteins. Nephrol Dial Transplant 2005;20 Suppl 6:vi3-9.
33. Boussif O, Lezoualc'h F, Zanta MA, Mergny MD, Scherman D, Demeneix B, et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci U S A 1995;92:7297-301.
34. Weinberg MS, Villeneuve LM, Ehsani A, Amarzguioui M, Aagaard L, Chen ZX, et al. The antisense strand of small interfering RNAs directs histone methylation and transcriptional gene silencing in human cells. RNA 2006;12:256-62. (Pubitemid 43121930)
35. Kren BT, Unger GM, Sjeklocha L, Trossen AA, Korman V, Diethelm-Okita BM, et al. Nanocapsule-delivered Sleeping Beauty mediates therapeutic Factor VIII expression in liver sinusoidal endothelial cells of hemophilia A mice. J Clin Invest 2009;119:2086-99.
36. Mason M, Spate V, Morris J, Baskett C, Cheng T, Reams C, et al. Determination of iodine in urine, using epithermal instrumental neutron activation analysis (EINAA), at the University of Missouri Research Reactor (MURR). J Radioanal Nucl Chem 1995;195:57-65.
37. Varga CM, Tedford NC, Thomas M, Klibanov AM, Griffith LG, Lauffenburger DA. Quantitative comparison of polyethylenimine formulations and adenoviral vectors in terms of intracellular gene delivery processes. Gene Ther 2005;12:1023-32. (Pubitemid 40946144)
38. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Mol Cell 2004;15:185-97. (Pubitemid 38950966)
39. Ginos M, Page G, Michalowicz B, Patel K, Volker S, Pambuccian S, et al. Identi fication of a gene expression signature associated with recurrent disease in squamous cell carcinoma of the head and neck. Cancer Res 2004;64:55-63. (Pubitemid 38114082)
40. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
41. Trembley JH, Wu J-J, Unger GM, Kren BT, Ahmed K. CK2 suppression of apoptosis and its implication in cancer biology and therapy. In:Pinna LA, editor. Protein kinase CK2. 1st ed. Oxford: John Wiley & Sons, Inc.; 2013. p. 319-43.
42. Sarno S, Papinutto E, Franchin C, Bain J, Elliott M, Meggio F, et al. ATP site-directed inhibitors of protein kinase CK2: an update. Curr Top Med Chem 2011;11:1340-51.
43. Ahmad KA, Wang G, Slaton J, Unger G, Ahmed K. Targeting CK2 for cancer therapy. Anticancer Drugs 2005;16:1037-43. (Pubitemid 41565768)
44. Sioud M. Induction of inflammatory cytokines and interferon responses by double-stranded and single-stranded siRNAs is sequence-dependent and requires endosomal localization. J Mol Biol 2005;348:1079-90. (Pubitemid 40602367)
45. Szebeni J, Moghimi SM. Liposome triggering of innate immune responses: a perspective on benefits and adverse reactions. J Liposome Res 2009;19:85-90.
46. Gagnon KT, Li L, Chu Y, Janowski BA, Corey DR. RNAi factors are present and active in human cell nuclei. Cell Rep 2014;6:211-21.
47. Stalder L, Heusermann W, Sokol L, Trojer D, Wirz J, Hean J, et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J 2013;32:1115-27.
48. Nguyen J, Szoka FC. Nucleic acid delivery: the missing pieces of the puzzle? Acc Chem Res 2012;45:1153-62.
49. Tuxhorn JA, Ayala GE, Smith MJ, Smith VC, Dang TD, Rowley DR. Reactive stroma in human prostate cancer. Clin Cancer Res 2002;8:2912-23.
50. Schroeder A, Heller DA, Winslow MM, Dahlman JE, Pratt GW, Langer R, et al. Treating metastatic cancer with nanotechnology. Nat Rev Cancer 2012;12:39-50.