Journal of Surgical Research
Volume 146, Issue 1 , Pages 16-23 , 1 May 2008

Inhibition of In Vivo Tumor Angiogenesis and Growth Via Systemic Delivery of an Angiopoietin 2-Specific RNA Aptamer

  • Shiva Sarraf-Yazdi, M.D.

      Affiliations

    • Department of Surgery, Duke University Medical Center, Durham, North Carolina
  • ,
  • Jing Mi, M.D., Ph.D.

      Affiliations

    • Department of Surgery, Duke University Medical Center, Durham, North Carolina
  • ,
  • Benjamin J. Moeller, M.D.

      Affiliations

    • Department of Radiation Oncology, Duke University Medical Center, Durham, North Carolina
  • ,
  • Xilin Niu, M.D.

      Affiliations

    • Department of Medicine, Division of Cardiology, Duke University Medical Center, Durham, North Carolina
  • ,
  • Rebekah R. White, M.D.

      Affiliations

    • Department of Surgery, Duke University Medical Center, Durham, North Carolina
  • ,
  • Christopher D. Kontos, M.D.

      Affiliations

    • Department of Medicine, Division of Cardiology, Duke University Medical Center, Durham, North Carolina
  • ,
  • Bruce A. Sullenger, Ph.D.

      Affiliations

    • Department of Surgery, Duke University Medical Center, Durham, North Carolina
  • ,
  • Mark W. Dewhirst, D.V.M., Ph.D.

      Affiliations

    • Department of Radiation Oncology, Duke University Medical Center, Durham, North Carolina
  • ,
  • Bryan M. Clary, M.D.

      Affiliations

    • Department of Surgery, Duke University Medical Center, Durham, North Carolina
    • Corresponding Author InformationTo whom correspondence and reprint requests should be addressed at Department of Surgery, Duke University Medical Center, Box 3247 DUMC, Durham, NC 27710.

Received 10 January 2007

References 

  1. Yancopoulos GD, Davis S, Gale N, et al. Vascular-specific growth factors and blood vessel formation. Nature. 2000;407:242
  2. Dumont DJ, Yamaguchi TP, Conlon RA, et al. Tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene. 1992;7:1471
  3. Sato TN, Tozawa Y, Deutsch U, et al. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature. 1995;376:70
  4. Dumont DJ, Gradwohl G, Fong GH, et al. Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev. 1994;8:1897
  5. Davis S, Aldrich TH, Jones PF, et al. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell. 1996;87:1161
  6. Uemura A, Ogawa M, Hirashima M, et al. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J Clin Invest. 2002;110:1619
  7. Thurston G, Suri C, Smith K, et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science. 1999;286:2511
  8. Suri C, Jones PF, Patan S, et al. Requisite role of angiopoietin-1, a ligand for the Tie2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171
  9. Maisonpierre P, Suri C, Jones P. Angiopoietin-2, a natural antagonist for Tie2 that disrupts n vivo angiogenesis. Science. 1997;277:55
  10. Holash J, Maisonpierre PC, Compton D, et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science. 1999;284:1994
  11. Lobov IB, Brooks PC, Lang RA. Angiopoietin-2 displays the VEGF-dependent modulation of capillary structure and endothelial survival in vivo. Proc Natl Acad Sci. 2002;99:11205
  12. Korff T, Kimmina S, Martiny-Baron G, et al. Blood vessel maturation in a 3-dimensional spheroidal co-culture model: Direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J. 2001;15:447
  13. Visconti RP, Richardson CD, Sato TN. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc Natl Acad Sci. 2002;99:8219
  14. Gale NW, Thurston G, Hackett SF, et al. Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by Angiopoietin-1. Dev Cell. 2002;3:411
  15. Lin P, Polverini P, Dewhirst MW, et al. Inhibition of tumor angiogenesis using a solube receptor establishes a role for Tie2 in pathological vascular growth. J Clin Invest. 1997;100:2072
  16. Stratmann A, Acker T, Burger A, et al. Differential inhibition of tumor angiogenesis by Tie2 and vascular endothelial growth factor receptor-2 dominant-negative receptor mutants. Int J Cancer. 2001;91:273
  17. Hangai M, Moon YS, Kitaya N, et al. Systemically expressed soluble Tie2 inhibits intraocular neovascularization. Hum Gene Ther. 2001;12:1311
  18. Lin P, Buxton JA, Acheson A, et al. Anti-angiogenic gene therapy targeting the endothelium-specific receptor tyrosine kinase Tie2. Proc Natl Acad Sci. 1998;95:8829
  19. Siemeister G, Schirner M, Weindel K. Two independent mechanisms essential for tumor angiogenesis: Inhibition of human melanoma xenograft growth by interfering with either the vascular endothelial growth factor receptor pathway or the Tie-2 pathway. Cancer Res. 1999;59:3185
  20. Hayes AJ, Huang WQ, Yu J, et al. Expression and function of angiopoietin-1 in breast cancer. Br J Cancer. 2000;83:1154
  21. Tanaka S, Mori M, Sakamoto Y, et al. Biologic significance of angiopoietin-2 expression in human hepatocellular carcinoma. J Clin Invest. 1999;103:341
  22. Ahmad SA, Liu W, Jung YD, et al. The effects of angiopoietin-1 and -2 on tumor growth and angiogenesis in human colon cancer. Cancer Res. 2001;61:1255
  23. Zhang L, Yang N, Park JW, et al. Tumor-derived vascular endothelial growth factor up-regulates angiopoietin-2 in host endothelium and destabilizes host vasculature, supporting angiogenesis in ovarian cancer. Cancer Res. 2003;63:3403
  24. White RR, Shan S, Rusconi CP, et al. Inhibition of rat corneal angiogenesis by a nuclease-resistant RNA aptamer specific for angiopoietin-2. Proc Natl Acad Sci. 2003;100:5028
  25. Huang Q, Shan S, Braun RD, et al. Noninvasive visualization of tumors in rodent dorsal skin window chambers: A novel model for evaluating anti-cancer therapies. Nat Biotech. 1999;17:1033
  26. Brody EN, Gold L. Aptamers as therapeutic and diagnostic agents. Rev Mol Biotech. 2000;74:5
  27. Osborne SE, Matsumura I, Ellington AD. Aptamers as therapeutic and diagnostic reagents: Problems and prospects. Curr Opin Chem Biol. 1997;1:5
  28. Huang J, Moore J, Soffer S, et al. Highly specific anti-angiogenic therapy is effective in suppressing growth of experimental Wilms tumors. J Pediatr Surg. 2001;36:357
  29. Kim ES, Serur A, Huang J, et al. Potent VEGF blockade causes regression of coopted vessels in a model of neuroblastoma. Proc Natl Acad Sci. 2002;99:11399
  30. Floege J, Ostendorf T, Janssen U, et al. Novel approach to specific growth factor inhibition in vivo: Antagonism of platelet-derived growth factor in glomerulonephritis by aptamers. Am J Pathol. 1999;154:169
  31. Ostendorf T, Kunter U, Eitner F, et al. VEGF165 mediates glomerular endothelial repair. J Clin Invest. 1999;104:913
  32. Sullenger BA, Gilboa E. Emerging clinical applications of RNA. Nature. 2002;418:252
  33. Hicke BJ, Stephens AW. Escort aptamers: A delivery service for diagnosis and therapy. J Clin Invest. 2002;106:923
  34. White RR, Sullenger BA, Rusconi CP. Developing aptamers into therapeutics. J Clin Invest. 2000;106:929
  35. Pieken WA, Olsen DB, Benseler F, et al. Kinetic characterization of ribonuclease-resistant 2′-modified hammer-head ribozymes. Science. 1991;253:314
  36. Beigelman L, McSwiggen JA, Draper KG, et al. Chemical modification of hammerhead ribozymes (Catalytic activity and nuclease resistance). J Biol Chem. 1995;270:25702
  37. Willis MC, Collins BD, Zhang T, et al. Liposome-anchored vascular endothelial growth factor aptamers. Bioconj Chem. 1998;9:573
  38. Eyetech Study group. Preclinical and phase 1A clinical evaluation of an anti-VEGF pegylated aptamer (EYE001) for the treatment of exudative age-related macular degeneration. Retina. 2002;22:143
  39. Eyetech Study Group. Anti-vascular endothelial growth factor therapy for subfoveal choroidal neovascularization secondary to age-related macular degeneration: Phase II study results. Ophthalmology. 2003;110:979
  40. Li CY, Shan S, Huang Q, Braun RD, et al. Initial stages of tumor cell-induced angiogenesis: Evaluation via skin window chambers in rodent models. J Natl Cancer Inst. 2000;92:143
  41. Oliner J, Min H, Leal J, et al. Suppression of angiogenesis and tumor growth by selective inhibition of angiopoietin-2. Cancer Cell. 2004;6:507
  42. Stoeltzing O, Ahmad SA, Liu W, et al. Angiopoietin-1 inhibits vascular permeability, angiogenesis, and growth of hepatic colon cancer tumors. Cancer Res. 2003;63:3370
  43. Hurwitz H, Fehrenbacher L, Novotny W, et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med. 2004;350:2335

PII: S0022-4804(07)00319-8

doi: 10.1016/j.jss.2007.04.028

Journal of Surgical Research
Volume 146, Issue 1 , Pages 16-23 , 1 May 2008