The angiogenic response to PLL-g-PEG-mediated HIF-1α plasmid DNA delivery in healthy and diabetic rats

Biomaterials

Volumn 34, Issue 16, 2013, Pages 4173-4182

  Thiersch, Markus ^a,b   Rimann, Markus ^a,d   Panagiotopoulou, Vasiliki ^a,e   Öztürk, Ece ^a   Biedermann, Thomas ^c   Textor, Marcus ^a   Lühmann, Tessa C ^a,f   Hall, Heike ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^d ZURICH UNIVERSITY OF APPLIED SCIENCES   (Switzerland)

^e ZÜHLKE ENGINEERING AG   (Switzerland)

^f UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Angiogenesis; DNA delivery; HIF 1 ; PLL g PEG; Wound healing

Indexed keywords

ANGIOGENESIS; DNA DELIVERY; HYPOXIA-INDUCIBLE TRANSCRIPTION FACTORS; NORMOXIC CONDITIONS; PLL-G-PEG; SMOOTH MUSCLE CELLS; TRANSIENT GENE EXPRESSIONS; WOUND HEALING;

BIOMATERIALS; BIOMOLECULES; BLOOD VESSELS; ENDOTHELIAL CELLS; FUNCTIONAL POLYMERS; GENE ENCODING; GENE THERAPY; GENE TRANSFER; HEALTH RISKS; PEPTIDES; RATS; TRANSCRIPTION FACTORS;

DRUG THERAPY;

CD31 ANTIGEN; FIBRIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MACROGOL; PLASMID DNA; POLYLYSINE; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COVALENT BOND; DEGRADATION; GENE EXPRESSION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRECURSOR; PRIORITY JOURNAL; RAT; SMOOTH MUSCLE FIBER; WOUND HEALING;

AMINO ACID SEQUENCE; ANIMALS; CAPILLARIES; CERCOPITHECUS AETHIOPS; COS CELLS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DNA; FIBRIN; GENE EXPRESSION REGULATION; GENE TRANSFER TECHNIQUES; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MOLECULAR SEQUENCE DATA; NEOVASCULARIZATION, PHYSIOLOGIC; PLASMIDS; POLYETHYLENE GLYCOLS; POLYLYSINE; RATS; RATS, SPRAGUE-DAWLEY; VASCULAR ENDOTHELIAL GROWTH FACTOR A; WOUND HEALING;

RATTUS;

EID: 84874990812     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2013.02.021     Document Type: Article

References (48)

1. Gurtner G.C., Werner S., Barrandon Y., Longaker M.T. Wound repair and regeneration. Nature 2008, 453:314-321.
2. Blakytny R., Jude E.B., Martin Gibson J., Boulton A.J., Ferguson M.W. Lack of insulin-like growth factor 1 (IGF1) in the basal keratinocyte layer of diabetic skin and diabetic foot ulcers. J Pathol 2000, 190:589-594.
3. Whitney J.D. Wound care: the challenges ahead. Rehabil Nurs 2005, 30:78-79.
4. Gary Sibbald R., Woo K.Y. The biology of chronic foot ulcers in persons with diabetes. Diabetes Metab Res Rev 2008, 24(Suppl. 1):S25-S30.
5. Kuehn B.M. Chronic wound care guidelines issued. JAMA 2007, 297:938-939.
6. Chandler L.A., Gu D.L., Ma C., Gonzalez A.M., Doukas J., Nguyen T., et al. Matrix-enabled gene transfer for cutaneous wound repair. Wound Repair Regen 2000, 8:473-479.
7. Eriksson E., Velander P. Gene transfer in wound healing. Br J Surg 2004, 91:1093-1094.
8. Keswani S.G., Katz A.B., Lim F.Y., Zoltick P., Radu A., Alaee D., et al. Adenoviral mediated gene transfer of PDGF-B enhances wound healing in type I and type II diabetic wounds. Wound Repair Regen 2004, 12:497-504.
9. Tal J. Adeno-associated virus-based vectors in gene therapy. J Biomed Sci 2000, 7:279-291.
10. Ramsay E., Hadgraft J., Birchall J., Gumbleton M. Examination of the biophysical interaction between plasmid DNA and the polycations, polylysine and polyornithine, as a basis for their differential gene transfection in-vitro. Int J Pharm 2000, 210:97-107.
11. Halama A., Kulinski M., Librowski T., Lochynski S. Polymer-based non-viral gene delivery as a concept for the treatment of cancer. Pharmacol Rep 2009, 61:993-999.
12. von Erlach T., Zwicker S., Pidhatika B., Konradi R., Textor M., Hall H., et al. Formation and characterization of DNA-polymer-condensates based on poly(2-methyl-2-oxazoline) grafted poly(l-lysine) for non-viral delivery of therapeutic DNA. Biomaterials 2011, 32:5291-5303.
13. Zaitsev S., Cartier R., Vyborov O., Sukhorukov G., Paulke B.R., Haberland A., et al. Polyelectrolyte nanoparticles mediate vascular gene delivery. Pharm Res 2004, 21:1656-1661.
14. Lee H., Jeong J.H., Park T.G. PEG grafted polylysine with fusogenic peptide for gene delivery: high transfection efficiency with low cytotoxicity. J Control Release 2002, 79:283-291.
15. Choi Y.H., Liu F., Kim J.S., Choi Y.K., Park J.S., Kim S.W. Polyethylene glycol-grafted poly-l-lysine as polymeric gene carrier. J Control Release 1998, 54:39-48.
16. Luhmann T., Rimann M., Bittermann A.G., Hall H. Cellular uptake and intracellular pathways of PLL-g-PEG-DNA nanoparticles. Bioconjug Chem 2008, 19:1907-1916.
17. Rimann M., Luhmann T., Textor M., Guerino B., Ogier J., Hall H. Characterization of PLL-g-PEG-DNA nanoparticles for the delivery of therapeutic DNA. Bioconjug Chem 2008, 19:548-557.
18. Weidemann A., Johnson R.S. Biology of HIF-1alpha. Cell Death Differ 2008, 15:621-627.
19. Bruick R.K., McKnight S.L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001, 294:1337-1340.
20. 2-regulated prolyl hydroxylation. Science 2001, 292:468-472.
21. Masson N., Willam C., Maxwell P.H., Pugh C.W., Ratcliffe P.J. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J 2001, 20:5197-5206.
22. Huang L.E., Gu J., Schau M., Bunn H.F. Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci U S A 1998, 95:7987-7992.
23. Mahon P.C., Hirota K., Semenza G.L. FIH-1: a novel protein that interacts with HIF-1alpha and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev 2001, 15:2675-2686.
24. Trentin D., Hubbell J., Hall H. Non-viral gene delivery for local and controlled DNA release. J Control Release 2005, 102:263-275.
25. Currie L.J., Sharpe J.R., Martin R. The use of fibrin glue in skin grafts and tissue-engineered skin replacements: a review. Plast Reconstr Surg 2001, 108:1713-1726.
26. Montano I., Schiestl C., Schneider J., Pontiggia L., Luginbuhl J., Biedermann T., et al. Formation of human capillaries in vitro: the engineering of prevascularized matrices. Tissue Eng Part A 2010, 16:269-282.
27. Mogford J.E., Tawil B., Jia S., Mustoe T.A. Fibrin sealant combined with fibroblasts and platelet-derived growth factor enhance wound healing in excisional wounds. Wound Repair Regen 2009, 17:405-410.
28. Catelas I., Dwyer J.F., Helgerson S. Controlled release of bioactive transforming growth factor beta-1 from fibrin gels in vitro. Tissue Eng Part C Methods 2008, 14:119-128.
29. Pasche S., Textor M., Meagher L., Spencer N.D., Griesser H.J. Relationship between interfacial forces measured by colloid-probe atomic force microscopy and protein resistance of poly(ethylene glycol)-grafted poly(L-lysine) adlayers on niobia surfaces. Langmuir 2005, 21:6508-6520.
30. Thangarajah H., Yao D., Chang E.I., Shi Y., Jazayeri L., Vial I.N., et al. The molecular basis for impaired hypoxia-induced VEGF expression in diabetic tissues. Proc Natl Acad Sci U S A 2009, 106:13505-13510.
31. Wood S.H., Clements D.N., McEwan N.A., Nuttall T., Carter S.D. Reference genes for canine skin when using quantitative real-time PCR. Vet Immunol Immunopathol 2008, 126:392-395.
32. Park T.G., Jeong J.H., Kim S.W. Current status of polymeric gene delivery systems. Adv Drug Deliver Rev 2006, 58:467-486.
33. Trentin D., Hall H., Wechsler S., Hubbell J.A. Peptide-matrix-mediated gene transfer of an oxygen-insensitive hypoxia-inducible factor-1alpha variant for local induction of angiogenesis. Proc Natl Acad Sci U S A 2006, 103:2506-2511.
34. Hao X., Silva E.A., Mansson-Broberg A., Grinnemo K.H., Siddiqui A.J., Dellgren G., et al. Angiogenic effects of sequential release of VEGF-A165 and PDGF-BB with alginate hydrogels after myocardial infarction. Cardiovasc Res 2007, 75:178-185.
35. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 2003, 161:1163-1177.
36. Hendel R.C., Henry T.D., Rocha-Singh K., Isner J.M., Kereiakes D.J., Giordano F.J., et al. Effect of intracoronary recombinant human vascular endothelial growth factor on myocardial perfusion: evidence for a dose-dependent effect. Circulation 2000, 101:118-121.
37. Botusan I.R., Sunkari V.G., Savu O., Catrina A.I., Grunler J., Lindberg S., et al. Stabilization of HIF-1alpha is critical to improve wound healing in diabetic mice. Proc Natl Acad Sci U S A 2008, 105:19426-19431.
38. Albina J.E., Mastrofrancesco B., Vessella J.A., Louis C.A., Henry W.L., Reichner J.S. HIF-1 expression in healing wounds: HIF-1alpha induction in primary inflammatory cells by TNF-alpha. Am J Physiol Cell Physiol 2001, 281:C1971-C1977.
39. Stoeltzing O., McCarty M.F., Wey J.S., Fan F., Liu W., Belcheva A., et al. Role of hypoxia-inducible factor 1alpha in gastric cancer cell growth, angiogenesis, and vessel maturation. J Natl Cancer Inst 2004, 96:946-956.
40. Walsh M., Tangney M., O'Neill M.J., Larkin J.O., Soden D.M., McKenna S.L., et al. Evaluation of cellular uptake and gene transfer efficiency of pegylated poly-l-lysine compacted DNA: implications for cancer gene therapy. Mol Pharm 2006, 3:644-653.
41. Kwon A.H., Qiu Z., Hashimoto M., Yamamoto K., Kimura T. Effects of medicinal mushroom (Sparassis crispa) on wound healing in streptozotocin-induced diabetic rats. Am J Surg 2009, 197:503-509.
42. Mace K.A., Yu D.H., Paydar K.Z., Boudreau N., Young D.M. Sustained expression of Hif-1alpha in the diabetic environment promotes angiogenesis and cutaneous wound repair. Wound Repair Regen 2007, 15:636-645.
43. Catrina S.B., Okamoto K., Pereira T., Brismar K., Poellinger L. Hyperglycemia regulates hypoxia-inducible factor-1alpha protein stability and function. Diabetes 2004, 53:3226-3232.
44. Thangarajah H., Vial I.N., Grogan R.H., Yao D., Shi Y., Januszyk M., et al. HIF-1alpha dysfunction in diabetes. Cell Cycle 2010, 9:75-79.
45. Ilan N., Madri J.A. PECAM-1: old friend, new partners. Curr Opin Cell Biol 2003, 15:515-524.
46. Skalli O., Pelte M.F., Peclet M.C., Gabbiani G., Gugliotta P., Bussolati G., et al. Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 1989, 37:315-321.
47. Drew A.F., Liu H., Davidson J.M., Daugherty C.C., Degen J.L. Wound-healing defects in mice lacking fibrinogen. Blood 2001, 97:3691-3698.
48. Alfranca A. VEGF therapy: a timely retreat. Cardiovasc Res 2009, 83:611-612.