Compacted DNA nanoparticle gene transfer of GDNF to the rat striatum enhances the survival of grafted fetal dopamine neurons

Cell Transplantation

Volumn 18, Issue 10-11, 2009, Pages 1183-1196

  Yurek, David M ^a   Flectcher, Anita M ^a   Kowalczyk, Tomasz H ^b   Padegimas, Linas ^b   Cooper, Mark J ^b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b Copernicus Therapeutics Inc ^*  (United States)

Author keywords

DNA nanoparticles; Gene transfer; Glial cell line derived neurotrophic factor (GDNF); Parkinson's disease

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LYSINE; MACROGOL; NANOPARTICLE; PLASMID DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; CELL COUNT; CELL SURVIVAL; CELL SUSPENSION; CONTROLLED STUDY; CORPUS STRIATUM; DENERVATION; DOPAMINERGIC NERVE CELL; FOREFOOT; FORELIMB; GENETIC TRANSFECTION; MALE; MESENCEPHALON; MOTOR ACTIVITY; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEREOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN TISSUE TRANSPLANTATION; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DNA; DOPAMINE; FETAL TISSUE TRANSPLANTATION; GENE TRANSFER TECHNIQUES; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; MALE; MESENCEPHALON; MOTOR ACTIVITY; NANOPARTICLES; NEURONS; PARKINSON DISEASE; PLASMIDS; POLYETHYLENE GLYCOLS; POLYLYSINE; RATS; RATS, SPRAGUE-DAWLEY; ROTAROD PERFORMANCE TEST;

ANIMALIA; RATTUS;

EID: 75149113700     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368909X12483162196881     Document Type: Article

References (55)

1. Ahn, Y. H.; Bensadoun, J. C.; Aebischer, P.; Zurn, A. D.; Seiger, A.; Bjorklund, A.; Lindvall, O.; Wahlberg, L.; Brundin, P.; Kaminski Schierle, G. S. Increased fiber outgrowth from xeno-transplanted human embryonic do paminergic neurons with co-implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor. Brain Res. Bull. 66(2): 135-142; 2005.
2. Annett, L. E. Functional studies of neural grafts in parkinsonian primates. In: Dunnett, S. B.; Bjorklund, A., eds. Functional neural transplantation. New York: Raven Press; 1994:71-102.
3. Apostolides, C.; Sanford, E.; Hong, M.; Mendez, I. Glial cell line-derived neurotrophic factor improves intrastriatal graft survival of stored dopaminergic cells. Neuroscience 83(2):363-372; 1998.
4. Bankiewicz, K.; Mandel, R. J.; Sofroniew, M. V. Trophism, transplantation, and animal models of Parkinson's disease. Exp. Neurol. 124(1):140-149; 1993.
5. Baumgartner, B. J.; Shine, H. D. Permanent rescue of lesioned neonatal motoneurons and enhanced axonal regeneration by adenovirus-mediated expression of glial cell-line-derived neurotrophic factor. J. Neurosci. Res. 54(6): 766-777; 1998.
6. Baumgartner, B. J.; Shine, H. D. Targeted transduction of CNS neurons with adenoviral vectors carrying neurotrophic factor genes confers neuroprotection that exceeds the transduced population. J. Neurosci. 17(17):6504-6511; 1997.
7. Bharali, D. J.; Klejbor, I.; Stachowiak, E. K.; Dutta, P.; Roy, I.; Kaur, N.; Bergey, E. J.; Prasad, P. N.; Stachowiak, M. K. Organically modified silica nanoparticles: A nonviral vector for in vivo gene delivery and expression in the brain. Proc. Natl. Acad. Sci. USA 102(32):11539-11544; 2005.
8. Brundin, P.; Duan, W. M.; Sauer, H. Functional effects of mesencephalic dopamine neurons and adrenal chromaffin cells grafted to the rat striatum. In: Dunnett, S. B.; Bjorklund, A., eds. Functional neural transplantation. New York: Raven Press; 1994:9-46.
9. Brundin, P.; Karlsson, J.; Emgard, M.; Schierle, G. S.; Hansson, O.; Petersen, A.; Castilho, R. F. Improving the survival of grafted dopaminergic neurons: A review over current approaches. Cell Transplant. 9(2):179-195; 2000.
10. Chen, X.; Kube, D. M.; Cooper, M. J.; Davis, P. B. Cell surface nucleolin serves as receptor for DNA nanoparticles composed of pegylated polylysine and DNA. Mol. Ther. 16(2):333-342; 2008.
11. Duan, W.-M.; Widner, H.; Brundin, P. Temporal pattern of host responses against intrastriatal grafts of syngeneic, allogeneic or xenogeneic embryonic neuronal tissue in rats. Exp. Brain Res. 104:227-242; 1995.
12. Elsworth, J. D.; Redmond, Jr., D. E.; Leranth, C.; Bjugstad, K. B.; Sladek, Jr., J. R.; Collier, T. J.; Foti, S. B.; Samulski, R. J.; Vives, K. P.; Roth, R. H. AAV2-mediated gene transfer of GDNF to the striatum of MPTP monkeys enhances the survival and outgrowth of co-implanted fetal dopamine neurons. Exp. Neurol. 211(1):252-258; 2008.
13. Farjo, R.; Skaggs, J.; Quiambao, A. B.; Cooper, M. J.; Naash, M. I. Efficient non-viral ocular gene transfer with compacted DNA nanoparticles. PLoS ONE 1:e38; 2006.
14. Fink, T. L.; Klepcyk, P. J.; Oette, S. M.; Gedeon, C. R.; Hyatt, S. L.; Kowalczyk, T. H.; Moen, R. C.; Cooper, M. J. Plasmid size up to 20 kbp does not limit effective in vivo lung gene transfer using compacted DNA nanoparticles. Gene Ther. 13(13):1048-1051; 2006.
15. Freed, C. R.; Greene, P. E.; Breeze, R. E.; Tsai, W. Y.; DuMouchel, W.; Kao, R.; Dillon, S.; Winfield, H.; Culver, S.; Trojanowski, J. Q.; Eidelberg, D.; Fahn, S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344(10):710-719; 2001.
16. Georgievska, B.; Carlsson, T.; Lacar, B.; Winkler, C.; Kirik, D. Dissociation between short-term increased graft survival and long-term functional improvements in Parkinsonian rats overexpressing glial cell line-derived neurotrophic factor. Eur. J. Neurosci. 20(11):3121-3130; 2004.
17. Gill, D. R.; Smyth, S. E.; Goddard, C. A.; Pringle, I. A.; Higgins, C. F.; Colledge, W. H.; Hyde, S. C. Increased persistence of lung gene expression using plasmids containing the ubiquitin C or elongation factor 1alpha promoter. Gene Ther. 8(20):1539-1546; 2001.
18. Konstan, M. W.; Davis, P. B.; Wagener, J. S.; Hilliard, K. A.; Stern, R. C.; Milgram, L. J.; Kowalczyk, T. H.; Hyatt, S. L.; Fink, T. L.; Gedeon, C. R.; Oette, S. M.; Payne, J. M.; Muhammad, O.; Ziady, A. G.; Moen, R. C.; Cooper, M. J. Compacted DNA nanoparticles administered to the nasal mucosa of cystic fibrosis subjects are safe and demonstrate partial to complete cystic fibrosis transmembrane regulator reconstitution. Hum. Gene Ther. 15(12):1255-1269; 2004.
19. Kordower, J. H.; Chu, Y.; Hauser, R. A.; Freeman, T. B.; Olanow, C. W. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat. Med. 14(5):504-506; 2008.
20. Lai, S. K.; Hida, K.; Man, S. T.; Chen, C.; Machamer, C.; Schroer, T. A.; Hanes, J. Privileged delivery of polymer nanoparticles to the perinuclear region of live cells via a non-clathrin, non-degradative pathway. Biomaterials 28(18):2876-2884; 2007.
21. Leone, P.; Janson, C. G.; Bilaniuk, L.; Wang, Z.; Sorgi, F.; Huang, L.; Matalon, R.; Kaul, R.; Zeng, Z.; Freese, A.; McPhee, S. W.; Mee, E.; During, M. J. Aspartoacylase gene transfer to the mammalian central nervous system with therapeutic implications for Canavan disease. Ann. Neurol. 48(1):27-38; 2000.
22. Li, J. Y.; Englund, E.; Holton, J. L.; Soulet, D.; Hagell, P.; Lees, A. J.; Lashley, T.; Quinn, N. P.; Rehncrona, S.; Bjorklund, A.; Widner, H.; Revesz, T.; Lindvall, O.; Brundin, P. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat. Med. 14(5):501-503; 2008.
23. Lindvall, O.; Hagell, P. Cell therapy and transplantation in Parkinson's disease. Clin. Chem. Lab. Med. 39(4):356-361; 2001.
24. Liu, G.; Li, D.; Pasumarthy, M. K.; Kowalczyk, T. H.; Gedeon, C. R.; Hyatt, S. L.; Payne, J. M.; Miller, T. J.; Brunovskis, P.; Fink, T. L.; Muhammad, O.; Moen, R. C.; Hanson, R. W.; Cooper, M. J. Nanoparticles of compacted DNA transfect postmitotic cells. J. Biol. Chem. 278(35):32578-32586; 2003.
25. Lowenstein, P. R.; Mandel, R. J.; Xiong, W. D.; Kroeger, K.; Castro, M. G. Immune responses to adenovirus and adeno-associated vectors used for gene therapy of brain diseases: The role of immunological synapses in understanding the cell biology of neuroimmune interactions. Curr. Gene Ther. 7(5):347-360; 2007.
26. Mendez, I.; Vinuela, A.; Astradsson, A.; Mukhida, K.; Hallett, P.; Robertson, H.; Tierney, T.; Holness, R.; Dagher, A.; Trojanowski, J. Q.; Isacson, O. Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat. Med. 14(5):507-509; 2008.
27. Mouton, P. R. Principles and practices of unbiased stereology. Baltimore, MD: The Johns Hopkins University Press; 2002.
28. National Research Council. Guide for the care and use of laboratory animals. Washington, DC: National Academy Press; 1997.
29. Nimesh, S.; Goyal, A.; Pawar, V.; Jayaraman, S.; Kumar, P.; Chandra, R.; Singh, Y.; Gupta, K. C. Polyethylenimine nanoparticles as efficient transfecting agents for mammalian cells. J. Control. Release 110(2):457-468; 2006.
30. Oh, S.; Pluhar, G. E.; McNeil, E. A.; Kroeger, K. M.; Liu, C.; Castro, M. G.; Lowenstein, P. R.; Freese, A.; Ohlfest, J. R. Efficacy of nonviral gene transfer in the canine brain. J. Neurosurg. 107(1):136-144; 2007.
31. Olanow, C. W.; Kordower, J. H.; Freeman, T. B. Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci. 19(3):102-109; 1996.
32. Piccini, P.; Brooks, D. J.; Bjorklund, A.; Gunn, R. N.; Grasby, P. M.; Rimoldi, O.; Brundin, P.; Hagell, P.; Rehncrona, S.; Widner, H.; Lindvall, O. Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Nat. Neurosci. 2(12):1137-1140; 1999.
33. Plank, C.; Mechtler, K.; Szoka, Jr., F. C.; Wagner, E. Activation of the complement system by synthetic DNA complexes: A potential barrier for intravenous gene delivery. Hum. Gene Ther. 7(12):1437-1446; 1996.
34. Plank, C.; Mechtler, K.; Wagner, E.; Szoka, F. C. Complement activation by polylysine-DNA complexes. In: Grigoriadis, G.; McCormack, B., ed. Targeting of drugs: Strategies for oligonucleotide and gene delivery in therapy. New York: Plenum Publishing Corp.; 1996:125-130.
35. Redmond, Jr., D. E. Cellular replacement therapy for Parkinson's disease - where we are today? Neuroscientist 8(5):457-488; 2002.
36. Rosenblad, C.; Martinez-Serrano, A.; Bjorklund, A. Glial cell line-derived neurotrophic factor increases survival, growth and function of intrastriatal fetal nigral dopaminergic grafts. Neuroscience 75(4):979-985; 1996.
37. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular cloning: A laboratory manual, 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989.
38. Sautter, J.; Tseng, J. L.; Braguglia, D.; Aebischer, P.; Spenger, C.; Seiler, R. W.; Widmer, H. R.; Zurn, A. D. Implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor improve survival, growth, and function of fetal dopaminergic grafts. Exp. Neurol. 149(1):230-236; 1998.
39. Schallert, T.; Tillerson, J. L. Intervention strategies for degeneration of dopamine neurons in parkinsonism: Optimizing behavioral assessment of outcome. In: Emerich, D.; Dean, 3rd, R. L.; Sanberg, P. R., ed. Innovative models of CNS disease: From molecule to therapy. Clifton, NJ: Humana Press; 2000:131-151.
40. Schmitz, C.; Hof, P. R. Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J. Chem. Neuroanat. 20(1):93-114; 2000.
41. Sinclair, S. R.; Svendsen, C. N.; Torres, E. M.; Martin, D.; Fawcett, J. W.; Dunnett, S. B. GDNF enhances dopaminergic cell survival and fibre outgrowth in embryonic nigral grafts. Neuroreport 7(15-17):2547-2552; 1996.
42. Sortwell, C. E.; Camargo, M. D.; Pitzer, M. R.; Gyawali, S.; Collier, T. J. Diminished survival of mesencephalic dopamine neurons grafted into aged hosts occurs during the immediate postgrafting interval. Exp. Neurol. 169(1):23-29; 2001.
43. Sortwell, C. E.; Pitzer, M. R.; Collier, T. J. Time course of apoptotic cell death within mesencephalic cell suspension grafts: Implications for improving grafted dopamine neuron survival. Exp. Neurol. 165(2):268-277; 2000.
44. Sullivan, A. M.; Pohl, J.; Blunt, S. B. Growth/differentiation factor 5 and glial cell line-derived neurotrophic factor enhance survival and function of dopaminergic grafts in a rat model of Parkinson's disease. Eur. J. Neurosci. 10(12):3681-3688; 1998.
45. Thomas, C. E.; Ehrhardt, A.; Kay, M. A. Progress and problems with the use of viral vectors for gene therapy. Nat. Rev. Genet. 4(5):346-358; 2003.
46. Thorne, R. G.; Nicholson, C. In vivo diffusion analysis with quantum dots and dextrans predicts the width of brain extracellular space. Proc. Natl. Acad. Sci. USA 103(14):5567-5572; 2006.
47. Watson, Jr., R. E.; Wiegand, S. J.; Clough, R. W.; Hoffman, G. E. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 7(1):155-159; 1986.
48. Wilby, M. J.; Sinclair, S. R.; Muir, E. M.; Zietlow, R.; Adcock, K. H.; Horellou, P.; Rogers, J. H.; Dunnett, S. B.; Fawcett, J. W. A glial cell line-derived neurotrophic factor-secreting clone of the Schwann cell line SCTM41 enhances survival and fiber outgrowth from embryonic nigral neurons grafted to the striatum and to the lesioned substantia nigra. J. Neurosci. 19(6):2301-2312; 1999.
49. Yurek, D. M. Glial cell line-derived neurotrophic factor improves survival of dopaminergic neurons in transplants of fetal ventral mesencephalic tissue. Exp. Neurol. 153(2):195-202; 1998.
50. Yurek, D. M.; Fletcher-Turner, A. Differential expression of GDNF, BDNF, and NT-3 in the aging nigrostriatal system following a neurotoxic lesion. Brain Res. 891(1-2):228-235; 2001.
51. Yurek, D. M.; Fletcher, A. M.; Smith, G. M.; Seroogy, K. B.; Ziady, A. G.; Molter, J.; Kowalczyk, T. H.; Padegimas, L.; Cooper, M. J. Long-term transgene expression in the central nervous system using DNA nanoparticles. Mol. Ther. 17(4):641-650; 2009.
52. Yurek, D. M.; Seroogy, K. B. Neurotrophic factor protection of dopaminergic neurons. In: Mocchetti, I., ed. Neurobiology of the neurotrophins. New York: Sulburger & Graham Publishing; 2001:355-397.
53. Yurek, D. M.; Sladek, Jr., J. R. Dopamine cell replacement: Parkinson's disease. Ann. Rev. Neurosci. 13:415-440; 1990.
54. Ziady, A. G.; Gedeon, C. R.; Miller, T.; Quan, W.; Payne, J. M.; Hyatt, S. L.; Fink, T. L.; Muhammad, O.; Oette, S.; Kowalczyk, T.; Pasumarthy, M. K.; Moen, R. C.; Cooper, M. J.; Davis, P. B. Transfection of airway epithelium by stable PEGylated poly-L-lysine DNA nanoparticles in vivo. Mol. Ther. 8(6):936-947; 2003.
55. Ziady, A. G.; Gedeon, C. R.; Muhammad, O.; Stillwell, V.; Oette, S. M.; Fink, T. L.; Quan, W.; Kowalczyk, T. H.; Hyatt, S. L.; Payne, J.; Peischl, A.; Seng, J. E.; Moen, R. C.; Cooper, M. J.; Davis, P. B. Minimal toxicity of stabilized compacted DNA nanoparticles in the murine lung. Mol. Ther. 8(6):948-956; 2003.