Effective delivery of Pep-1-cargo protein into ischemic neurons and long-term neuroprotection of Pep-1-SOD1 against ischemic injury in the gerbil hippocampus

Neurochemistry International

Volumn 52, Issue 4-5, 2008, Pages 659-668

  Cho, Jun Hwi ^a   Hwang, In Koo ^b   Yoo, Ki Yeon ^c   Kim, So Young ^c   Kim, Dae Won ^c   Kwon, Young Guen ^d   Choi, Soo Young ^c   Won, Moo Ho ^c  

^a Kangwon National University   (South Korea)

^b Seoul National University   (South Korea)

^c Hallym University   (South Korea)

^d Yonsei University   (South Korea)

Author keywords

Hippocampus; Ischemic damage; Long lasting neuroprotection; Pep 1 GFP; Pep 1 SOD1; Protein delivery; Pyramidal neurons

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GREEN FLUORESCENT PROTEIN; PROTEIN PEP 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN ISCHEMIA; CONTROLLED STUDY; GERBIL; HIPPOCAMPUS; HISTOCHEMISTRY; LOCOMOTION; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; REPERFUSION INJURY;

ANIMALS; BRAIN; BRAIN ISCHEMIA; CELL DEATH; CYSTEAMINE; DRUG DELIVERY SYSTEMS; GERBILLINAE; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; ISCHEMIC ATTACK, TRANSIENT; MALE; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; PEPTIDES; SUPEROXIDE DISMUTASE;

ANIMALIA; GERBILLINAE;

EID: 38349191031     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2007.08.013     Document Type: Article

References (56)

1. Adibhatla R.M., and Hatcher J.F. Citicoline decreases phospholipase A2 stimulation and hydroxyl radical generation in transient cerebral ischemia. J. Neurosci. Res. 73 (2003) 308-315
2. Allen J.W., Knoblach S.M., and Faden A.I. Combined mechanical trauma and metabolic impairment in vitro induces NMDA receptor-dependent neuronal cell death and caspase-3-dependent apoptosis. FASEB J. 13 (1999) 1875-1882
3. Beauchamp C., and Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 44 (1971) 276-287
4. Bémeur C., Ste-Marie L., and Montgomery J. Increased oxidative stress during hyperglycemic cerebral ischemia. Neurochem. Int. 50 (2007) 890-904
5. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
6. Braida D., Pozzi M., and Sala M. CP 55, 940 protect against ischemia-induced electroencephalic flattening and hyperlocomotion in Mongolian gerbils. Neurosci. Lett. 296 (2000) 69-72
7. Carney J.M. Acute tryptophan pretreatment protects against behavioral changes caused by cerebral ischemia. Neurosci. Lett. 66 (1986) 127-130
8. 2+ and ATP. Neurochem. Int. 50 (2007) 148-158
9. Clemens J.A. Cerebral ischemia: gene activation, neuronal injury, and the protective role of antioxidants. Free Radic. Biol. Med. 28 (2000) 1526-1531
10. De Angelis D.A., Miesenbock G., Zemelman B.V., and Rothman J.E. PRIM: proximity imaging of green fluorescent protein-tagged polypeptides. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 12312-12316
11. Deshayes S., Heitz A., Morris M.C., Charnet P., Divita G., and Heitz F. Insight into the mechanism of internalization of the cell-penetrating carrier peptide Pep-1 through conformational analysis. Biochemistry 43 (2004) 1449-1457
12. Egleton R.D., and Davis T.P. Bioavailability and transport of peptides and peptide drugs into the brain. Peptides 18 (1997) 1431-1439
13. Elliott G., and O'Hare P. Intercellular trafficking and protein delivery by a herpesvirus structural protein. Cell 88 (1997) 223-233
14. Eum W.S., Kim D.W., Hwang I.K., Yoo K.Y., Kang T.C., Jang S.H., Choi H.S., Choi S.H., Kim Y.H., Kim S.Y., Kwon H.Y., Kang J.H., Kwon O.S., Cho S.W., Lee K.S., Park J., Won M.H., and Choi S.Y. In vivo protein transduction: biologically active intact pep-1-superoxide dismutase fusion protein efficiently protects against ischemic insult. Free Radic. Biol. Med. 37 (2004) 1656-1669
15. Futaki S., Suzuki T., Ohashi W., Yagami T., Tanaka S., Ueda K., and Sugiura Y. Arginine-rich peptides. An abundant source of membrane-permeable peptides having potential as carriers for intracellular protein delivery. J. Biol. Chem. 276 (2001) 5836-5840
16. Han K., Jeon M.-J., Kim K.-A., Park J., and Choi S.Y. Efficient intracellular delivery of GFP by homeodomains of Drosophila Fushi-tarazu and Engrailed proteins. Mol. Cells 10 (2000) 728-732
17. Henriques S.T., and Castanho M.A. Consequences of nonlytic membrane perturbation to the translocation of the cell penetrating peptide pep-1 in lipidic vesicles. Biochemistry 43 (2004) 9716-9724
18. Henriques S.T., Costa J., and Castanho M.A. Translocation of beta-galactosidase mediated by the cell-penetrating peptide pep-1 into lipid vesicles and human HeLa cells is driven by membrane electrostatic potential. Biochemistry 44 (2005) 10189-10198
19. Henriques S.T., Costa J., and Castanho M.A. Re-evaluating the role of strongly charged sequences in amphipathic cellpenetrating peptides: a fluorescence study using Pep-1. FEBS Lett. 579 (2005) 4498-4502
20. Himeda T., Tounai H., Hayakawa N., and Araki T. Postischemic Alterations of BDNF, NGF, HSP 70 and Ubiquitin Immunoreactivity in the Gerbil Hippocampus: Pharmacological Approach. Cell. Mol. Neurobiol. 27 (2007) 229-250
21. Hwang I.K., Yoo K.Y., Park S.K., An S.J., Lee J.Y., Choi S.Y., Kang J.H., Kwon Y.G., Kang T.C., and Won M.H. Expression and changes of endogenous insulin-like growth factor-1 in neurons and glia in the gerbil hippocampus and dentate gyrus after ischemic insult. Neurochem. Int. 45 (2004) 149-156
22. Hwang I.K., Eum W.S., Yoo K.Y., Cho J.H., Kim D.W., Choi S.H., Kang T.C., Kwon O.S., Kang J.H., Choi S.Y., and Won M.H. Copper chaperone for Cu,Zn-SOD supplement potentiates the Cu, Zn-SOD function of neuroprotective effects against ischemic neuronal damage in the gerbil hippocampus. Free Radic. Biol. Med. 39 (2005) 392-402
23. Hwang I.K., Yoo K.Y., Kim D.W., Kang T.C., Choi S.Y., Kwon Y.G., Han B.H., Kim J.S., and Won M.H. Na+/Ca2+ exchanger 1 alters in pyramidal cells and expresses in astrocytes of the gerbil hippocampal CA1 region after ischemia. Brain Res. 1086 (2006) 181-190
24. Iqbal S., Baziany A., Gordon S., Wright S., Hussain M., Miyashita H., Shuaib A., and Hasan Rajput A. Neuroprotective effect of tiagabine in transient forebrain global ischemia: an in vivo microdialysis, behavioral, and histological study. Brain Res. 946 (2002) 162-170
25. Janać B., Radenović L., Selaković V., and Prolić Z. Time course of motor behavior changes in Mongolian gerbils submitted to different durations of cerebral ischemia. Behav. Brain Res. 175 (2006) 362-373
26. Jin L.H., Bahn J.H., Eum W.S., Kwon H.Y., Jang S.H., Han K.H., Kang T.C., Won M.H., Kang J.H., Cho S.W., Park J., and Choi S.Y. Transduction of human catalase mediated by an HIV-1 TAT protein basic domain and arginine-rich peptides into mammalian cells. Free Radic. Biol. Med. 31 (2001) 1509-1519
27. Karasawa Y., Araki H., and Otomo S. Changes in locomotor activity and passive avoidance task performance induced by cerebral ischemia in Mongolian gerbils. Stroke 25 (1994) 645-650
28. Khan S.H., Wright S.L., Banigesh A., Miyashita H., Todd K., Hemmings S.J., Wishart T., and Shuaib A. Antiischemic effects of topiramate in a transient global forebrain ischemia model: a neurochemical, histological, and behavioral evaluation. Neurochem. Res. 28 (2003) 1235-1239
29. Kim D.H., Li H., Yoo K.Y., Lee B.H., Hwang I.K., and Won M.H. Effects of fluoxetine on ischemic cells and expressions in BDNF and some antioxidants in the gerbil hippocampal CA1 region induced by transient ischemia. Exp. Neurol. 204 (2007) 748-758
30. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239 (1982) 57-69
31. Kirino T., and Sano K. Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropathol. (Berl.) 62 (1984) 201-208
32. Lipton P. Ischemic cell death in brain neurons. Physiol. Rev. 79 (1999) 1431-1568
33. Lo E.H., Moskowitz M.A., and Jacobs T.P. Exciting, radical, suicidal: how brain cells die after stroke. Stroke 36 (2005) 189-192
34. Mahajan N.P., Linder K., Berry G., Gordon G.W., Heim R., and Herman B. Bcl-2 and Bax interactions in mitochondria probed with green fluorescent protein and fluorescence resonance energy transfer. Nat. Biotechnol. 16 (1998) 547-552
35. Marinova Z., Vukojević V., Surcheva S., Yakovleva T., Cebers G., Pasikova N., Usynin I., Hugonin L., Fang W., Hallberg M., Hirschberg D., Bergman T., Langel U., Hauser K.F., Pramanik A., Aldrich J.V., Graslund A., Terenius L., and Bakalkin G. Translocation of dynorphin neuropeptides across the plasma membrane. A putative mechanism of signal transmission. J. Biol. Chem. 280 (2005) 26360-26370
36. McCord J.M., and Fridovich I. Superoxide dismutase: an enzymic function for erythrocuprein (hemocuprein). J. Biol. Chem. 244 (1969) 6049-6055
37. Mi Z., Mai J., Lu X., and Robbins P.D. Characterization of a class of cationic peptides able to facilitate efficient protein transduction in vitro and in vivo. Mol. Ther. 2 (2000) 339-347
38. Morris M.C., Depollier J., Mery J., Heitz F., and Divita G. A peptide carrier for the delivery of biologically active proteins into mammalian cells. Nat. Biotechnol. 19 (2001) 1173-1176
39. Park J., Ryu J., Jin L.H., Bahn J.H., Kim J.A., Yoon C.S., Kim D.W., Han K.H., Eum W.S., Kwon H.Y., Kang T.C., Won M.H., Kang J.H., Cho S.W., and Choi S.Y. 9-Polylysine protein transduction domain: enhanced penetration efficiency of superoxide dismutase into mammalian cells and skin. Mol. Cells 13 (2002) 202-208
40. Peters K.G., Rao P.S., Bell B.S., and Kindman L.A. Green fluorescent fusion proteins: powerful tools for monitoring protein expression in live zebrafish embryos. Dev. Biol. 171 (1995) 252-257
41. Pinheiro A.C., Gomez R.S., Massensini A.R., Cordeiro M.N., Richardson M., Romano-Silva M.A., Prado M.A., De Marco L., and Gomez M.V. Neuroprotective effect on brain injury by neurotoxins from the spider Phoneutria nigriventer. Neurochem. Int. 49 (2006) 543-547
42. Pooga M., Kut C., Kihlmark M., Hallbrink M., Fernaeus S., Raid R., Land T., Hallberg E., Bartfai T., and Langel U. Cellular translocation of proteins by transportan. FASEB J. 15 (2001) 1451-1453
43. Schwarze S.R., Ho A., Vocero-Akbani A., and Dowdy S.F. In vivo protein transduction: delivery of a biologically active protein into the mouse. Science 285 (1999) 1569-1572
44. Siesjo B.K., and Bengtsson F. Calcium fluxes, calcium antagonists, and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J. Cereb. Blood Flow Metab. 9 (1989) 127-140
45. Tomomura M., Rice D.S., Morgan J.I., and Yuzaki M. Purification of Purkinje cells by fluorescence-activated cell sorting from transgenic mice that express green fluorescent protein. Eur. J. Neurosci. 14 (2001) 57-63
46. Van de Waterbeemd H., Camenisch G., Folkers G., Chretien J.R., and Raevsky O.A. Estimation of blood-brain barrier crossing of drugs using molecular size and shape, and H-bonding descriptors. J. Drug Target 6 (1998) 151-165
47. Van den Pol A.N., and Ghosh P.K. Selective neuronal expression of green fluorescent protein with cytomegalovirus promoter reveals entire neuronal arbor in transgenic mice. J. Neurosci. 18 (1998) 10640-10651
48. Wang Y.Q., Guo X., Qiu M.H., Feng X.Y., and Sun F.Y. VEGF overexpression enhances striatal neurogenesis in brain of adult rat after a transient middle cerebral artery occlusion. J. Neurosci. Res. 85 (2007) 73-82
49. Weller K., Lauber S., Lerch M., Renaud A., Merkle H.P., and Zerbe O. Biophysical and biological studies of end-group-modified derivatives of Pep-1. Biochemistry 44 (2005) 15799-15811
50. Yang M., Hasegawa S., Jiang P., Wang X., Tan Y., Chishima T., Shimada H., Moossa A.R., and Hoffman R.M. Widespread skeletal metastatic potential of human lung cancer revealed by green fluorescent protein expression. Cancer Res. 58 (1998) 4217-4221
51. Yang M., Reynoso J., Jiang P., Li L., Moossa A.R., and Hoffman R.M. Transgenic nude mouse with ubiquitous green fluorescent protein expression as a host for human tumors. Cancer Res. 64 (2004) 8651-8656
52. Yeh E., Gustafson K., and Boulianne G.L. Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 7036-7040
53. Zernicka-Goetz M., Pines J., Ryan K., Siemering K.R., Haseloff J., Evans M.J., and Gurdon J.B. An indelible lineage marker for Xenopus using a mutated green fluorescent protein. Development 122 (1996) 3719-3724
54. Zhang G., Gurtu V., and Kain S.R. An enhanced green fluorescent protein allows sensitive detection of gene transfer in mammalian cells. Biochem. Biophys. Res. Commun. 227 (1996) 707-711
55. Zhang X., Baader S.L., Bian F., Muller W., and Oberdick J. High level Purkinje cell specific expression of green fluorescent protein in transgenic mice. Histochem. Cell. Biol. 115 (2001) 455-464
56. Zhu Y., Hoell P., Ahlemeyer B., Sure U., Bertalanffy H., and Krieglstein J. Implication of PTEN in production of reactive oxygen species and neuronal death in in vitro models of stroke and Parkinson's disease. Neurochem. Int. 50 (2007) 507-516