Electroosmotic push-pull perfusion: Description and application to qualitative analysis of the hydrolysis of exogenous galanin in organotypic hippocampal slice cultures

ACS Chemical Neuroscience

Volumn 4, Issue 5, 2013, Pages 838-848

  Rupert, Amy E ^a   Ou, Y ^a   Sandberg, M ^b   Weber, S G ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Ectopeptidase; electroosmosis; galanin; hippocampus; hydrolysis; neuropeptide

Indexed keywords

AMINOPEPTIDASE; GALANIN; GALANIN RECEPTOR; PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ELECTRIC FIELD; ELECTRIC POTENTIAL; ELECTROOSMOSIS; ELECTROPORATION; ENZYME ACTIVITY; FINITE ELEMENT ANALYSIS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HYDROLYSIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; RAT; ZETA POTENTIAL;

AMINOPEPTIDASES; ANIMALS; ELECTRIC STIMULATION; ELECTROOSMOSIS; EXTRACELLULAR SPACE; GALANIN; HIPPOCAMPUS; HYDROLYSIS; ORGAN CULTURE TECHNIQUES; PERFUSION; RATS; RATS, SPRAGUE-DAWLEY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 84877826641     PISSN: None     EISSN: 19487193     Source Type: Journal    
DOI: 10.1021/cn400082d     Document Type: Article

References (66)

1. Zini, S., Roisin, M., Armengaud, C., and Ben-Ari, Y. (1993) Effect of potassium channel modulators on the release of glutamate induced by ischemic-like conditions in rat hippocampal slices Neurosci. Lett. 153, 202-205
2. Elliott-Hunt, C., Marsh, B., Bacon, A., Pope, R., Vanderplank, P., and Wynick, D. (2004) Galanin acts as a neuroprotective factor to the hippocampus Proc. Natl. Acad. Sci. U.S.A. 101, 5105-5110
3. Elliott-Hunt, C., Pope, R., Vanderplank, P., and Wynick, D. (2007) Activation of the galanin receptor 2 (GalR2) protects the hippocampus from neuronal damag J. Neurochem. 100, 780-789
4. Lipton, P. (1999) Ischemic cell death in brain neurons Physiol. Rev. 79, 1431-1568
5. Shen, P.-J., Yuan, C.-G., Ma, J., Chen, S., Yao, M., Turnley, A., and Gundlach, A. (2005) Galanin in neuro(glio)genesis: expression of galanin and receptors by progenitor cells in vivo and in vitro and effects of galanin on neurosphere proliferation Neuropeptides. 39, 201-205
6. Melander, T., Hoekfelt, T., Roekaeus, A., Cuello, A., Oertel, W., Verhofstad, A., and Goldstein, M. (1986) Coexistence of galanin-like immunoreactivity with catecholamines, 5-hydroxytryptamine, GABA and neuropeptides in the rat CNS J. Neurosci. 6, 3640-3654
7. Skofitsch, G. and Jacobowitz, D. (1985) Immunohistochemical mapping of galanin-like neurons in the rat central nervous system Peptides 6, 509-546
8. Abbosh, C., Lawkowski, A., Zaben, M., and Gray, W. (2011) GalR2/3 mediates proliferative and trophic effects of galanin on postnatal hippocampal precursors J. Neurochem. 117, 426-436
9. Bunnett, N. W. (1987) The role of neuropeptides in regulating airway function. Postsecretory metabolism of peptides Am. Rev. Respir. Dis. 136, S27-S34
10. Land, T., Langel, U., and Bartfai, T. (1991) Hypothalamic degradation of galanin(1-29) and galanin(1-16): identification and characterization of the peptidolytic products Brain Res. 558, 245-250
11. Hallberg, M. and Nyberg, F. (2003) Neuropeptide conversion to bioactive fragments-an important pathway in neuromodulation Curr. Protein Pept. Sci. 4, 31-44
12. Fisone, G., Langel, U., Carlquist, M., Bergman, T., Consolo, S., Hoekfelt, T., Unden, A., Andell, S., and Bartfai, T. (1989) Galanin receptor and its ligands in the rat hippocampus Eur. J. Biochem. 181, 269-276
13. Lang, R., Gundlach, A., and Kofler, B. (2007) The galanin peptide family: receptor pharmacology, pleiotropic biological actions, and implications in health and disease Pharmacol. Ther. 115, 177-207
14. Stoppini, L., Buchs, P., and Muller, D. (1991) A simple method for organotypic cultures of nervous tissue J. Neurosci. Methods 37, 173-182
15. Noraberg, J. (2004) Organotypic brain slice cultures: An efficient and reliable method for neurotoxicological screening and mechanistic studies ATLA, Altern. Lab. Anim. 32, 329-337
16. Lindroos, M. M., Soini, S. L., Kukko-Lukjanov, T. K., Korpi, E. R., Lovinger, D., and Holopainen, I. E. (2005) Maturation of cultured hippocampal slices results in increased excitability in granule cells Int. J. Dev. Neurosci. 23, 65-73
17. Poulsen, F., Blaabjerg, M., Montero, M., and Zimmer, J. (2005) Glutamate receptor antagonists and growth factors modulate dentate granule cell neurogenesis in organotypic, rat hippocampal slice cultures Brain Res. 1051, 35-49
18. Holopainen, I. (2005) Organotypic hippocampal slice cultures: A model system to study basic cellular and molecular mechanisms of neuronal cell death, neuroprotection, and synaptic plasticity Neurochem. Res. 30, 1521-1528
19. Lushnikova, I., Skibo, G., Muller, D., and Nikonenko, I. (2011) Excitatory synaptic activity is associated with a rapid structural plasticity of inhibitory synapses on hippocampal CA1 pyramidal cells Neuropharmacology 60, 757-764
20. Won, R., Lee, K. H.., and Lee, B. H. (2011) Coenzyme Q10 protects neurons against neurotoxicity in hippocampal slice culture NeuroReport. 22, 721-726
21. Takahashi, M., Liou, S.-Y., and Kunihara, M. (1995) Ca2+- and Cl - dependent, NMDA receptor-mediated neuronal death induced by depolarization in rat hippocampal organotypic cultures Brain Res. 675, 249-256
22. Ziemka-Nalecz, M., Stanaszek, L., and Zalewska, T. (2013) Oxygen-glucose deprivation promotes gliogenesis and microglia activation in organotypic hippocampal slice culture: Involvement of metalloproteinases Acta Neurobiol. Exp. (Wars) 73, 130-142
23. Vornov, J., Park, J., and Thomas, A. (1998) Regional vulnerability to endogenous and exogenous oxidative stress in organotypic hippocampal culture Exp. Neurol. 149, 109-122
24. Simao, F., Zamin Laurenqq, L., Frozza, R., Nassif, M., Horn Ana, P., and Salbego Christianne, G. (2009) Protective profile of oxcarbazepine against oxygen-glucose deprivation in organotypic hippocampal slice culture could involve PI3K cell signaling pathway Neurol. Res. 31, 1044-1048
25. Holopainen, I., Kukko-Lukjanov, T., and Lopez-Picon, F. (2005) Neuroprotection against kainic acid excitotoxicity by specific glutamate receptor antagonists in cultured organotypic hippocampal slices Trends Neurochem. Res. 145-164
26. Nakagami, Y., Saito, H., and Matsuki, N. (1997) Basic fibroblast growth factor and brain-derived neurotrophic factor promote survival and neuronal circuit formation in organotypic hippocampal culture Jpn. J. Pharmacol. 75, 319-326
27. Andersen, L., Morris, R., Amaral, D., Bliss, T., and O'Keefe, J. The Hippocampus Book; Oxford University Press: New York, 2007.
28. Butler, T., Self, R., Smith, K., Sharrett-Field, L., Berry, J., Littleton, J., Pauly, J., Mulholland, P., and Prendergast, M. (2010) Selective vulnerability of hippocampal cornu ammonis 1 pyramidal cells to excitotoxic insult is associated with the expression of polyamine-sensitive N-methyl - asparate-type glutamate receptors Neuroscience 165, 525-534
29. Tasker, R. C., Coyle, J. T., and Vornov, J. J. (1992) The regional vulnerability to hypoglycemia-induced neurotoxicity in organotypic hippocampal culture: protection by early tetrodotoxin or delayed MK-801 J. Neurosci. 12, 4298-4308
30. Wang, X., Michaelis, M. L., and Michaelis, E. K. (2010) Functional genomics of brain aging and Alzheimer's disease: focus on selective neuronal vulnerability Curr. Genomics 11, 618-633
31. Sawada, M. and Sawamoto, K. (2013) Mechanisms of neurogenesis in the normal and injured adult brain Keio J. Med. 62, 13-28
32. Liu, J., Solway, K., Messing, R. O., and Sharp, F. R. (1998) Increased neurogenesis in the dentate gyrus after transient global ischemia in gerbils J. Neurosci. 18, 7768-77678
33. Andren, P. E. and Caprioli, R. M. (1995) In vivo metabolism of substance P in rat striatum utilizing microdialysis/liquid chromatography/micro- electrospray mass spectrometry J. Mass Spectrom. 30, 817-824
34. Eriksson, U., Andren, P. E., Caprioli, R. M., and Nyberg, F. (1996) Reversed-phase high-performance liquid chromatography combined with tandem mass spectrometry in studies of a substance P-converting enzyme from human cerebrospinal fluid J. Chromatogr., A 743, 213-220
35. Nydahl, K. S., Pierson, J., Nyberg, F., Caprioli, R. M., and Andren, P. E. (2003) In vivo processing of LVV-hemorphin-7 in rat brain and blood utilizing microdialysis combined with electrospray mass spectrometry Rapid Commun. Mass Spectrom. 17, 838-844
36. Sanderson, K., Andren, P. E., Caprioli, R. M., and Nyberg, F. (1996) In vitro metabolism of LVV-hemorphin-7 in human plasma studied by reversed-phase high-performance liquid chromatography and micro-electrospray mass spectrometry J. Chromatogr., A 743, 207-212
37. Guy, Y., Faraji, A. H., Gavigan, C. A., Strein, T. G., and Weber, S. G. (2012) Iontophoresis from a micropipet into a porous medium depends on the zeta-potential of the medium Anal. Chem. 84, 2179-2187
38. Xu, H., Guy, Y., Hamsher, A., Shi, G., Sandberg, M., and Weber, S. (2010) Electroosmotic sampling. Application to determination of ectopeptidase activity in organotypic hippocampal slice cultures Anal. Chem. 82, 6377-6383
39. Hamsher, A. E. (2010) Development of electroosmotic sampling for the identification and quantification of neuropeptides and their metabolites in the extracellular space of the hippocampus. In Monitoring Molecules in Neuroscience 2010 (Westerink, B., Clinkers, R., Smolders, I., Sarre, S., and Michotte, Y., Ed.), Vrije Universiteit Brussel: Brussels, Belgium and Fonds Wetenschappelijk Onderzoek: Vlaanderen.
40. Kottegoda, S., Shaik, I., and Shippy Scott, A. (2002) Demonstration of low flow push-pull perfusion J. Neurosci. Methods 121, 93-101
41. Slaney, T. R., Nie, J., Hershey, N. D., Thwar, P. K., Linderman, J., Burns, M. A., and Kennedy, R. T. (2011) Push-pull perfusion sampling with segmented flow for high temporal and spatial resolution in vivo chemical monitoring Anal. Chem. 83, 5207-5213
42. Faraji, A., Cui, J., Guy, Y., Li, L., Gavigan, C., Strein, T., and Weber, S. (2011) Synthesis and characterization of a hydrogel with controllable electroosmosis: a potential brain tissue surrogate for electrokinetic transport Langmuir 27, 13635-13642
43. Nolkrantz, K., Farre, C., Brederlau, A., Karlsson, R., Brennan, C., Eriksson, P., Weber, S., Sandberg, M., and Orwar, O. (2001) Electroporation of single cells and tissues with an electrolyte-filled capillary Anal. Chem. 73, 4469-4477
44. Hlushkou, D., Seidel-Morgenstern, A., and Tallarek, U. (2005) Numerical analysis of electroosmotic flow in dense regular and random arrays of impermeable, nonconducting spheres Langmuir 21, 6097-6112
45. Scales, N. and Tait, R. N. (2006) Modeling electroosmotic and pressure-driven flows in porous microfluidic devices: Zeta potential and porosity changes near the channel walls J. Chem. Phys. 125, 094714
46. Shen, L. and Chen, Z. (2007) Critical review of the impact of tortuosity on diffusion Chem. Eng. Sci. 62, 3748-3755
47. Nicholson, C. (2001) Diffusion and related transport mechanisms in brain tissue Rep. Prog. Phys. 64, 815-844
48. Hrabe, J., Hrabetova, S., and Segeth, K. (2004) A model of effective diffusion and tortuosity in the extracellular space of the brain Biophys. J. 87, 1606-1617
49. Guy, Y., Sandberg, M., and Weber, S. (2008) Determination of ζ-potential in rat organotypic hippocampal cultures Biophys. J. 94, 4561-4569
50. Rupert, A. E., Ou, Y., Sandberg, M., and Weber, S. G. (2013) Assessment of tissue viability following electroosmotic push-pull perfusion from organotypic hippocampal slice cultures. ACS Chem. Neurosci. DOI: 10.1021/cn4000814.
51. Sykova, E. and Vargova, L. (2008) Extrasynaptic transmission and the diffusion parameters of the extracellular space Neurochem. Int. 52, 5-13
52. Ritchie, J. C., Davis, T. P., and Nemeroff, C. B. (2003) Action of three ectopeptidases on corticotropin-releasing factor: metabolism and functional aspects Neuropsychopharmacology 28, 22-33
53. Wachsmuth, E. D. and Donner, P. (1976) Conclusions about aminopeptidase in tissue sections from studies of amino acid naphthylamide hydrolysis Histochemistry 47, 271-283
54. Krishnamoorthy, M. and Achary, A. (2013) Exploration of Sitagliptin as a potential inhibitor for the M1 Alanine aminopeptidase enzyme in Plasmodium falciparum using computational docking Bioinformation 9, 293-298
55. Hersh, L. B., Aboukhair, N., and Watson, S. (1987) Immunohistochemical localization of aminopeptidase M in rat brain and periphery: relationship of enzyme localization and enkephalin metabolism Peptides 8, 523-532
56. Fricker, L. D. (1988) Carboxypeptidase E Annu. Rev. Physiol. 50, 309-321
57. Supattapone, S., Fricker, L. D., and Snyder, S. H. (1984) Purification and characterization of a membrane-bound enkephalin-forming carboxypeptidase, "enkephalin convertase" J. Neurochem. 42, 1017-1023
58. MacCumber, M. W., Snyder, S. H., and Ross, C. A. (1990) Carboxypeptidase E (enkephalin convertase): mRNA distribution in rat brain by in situ hybridization J. Neurosci. 10, 2850-2860
59. Lynch, D. R., Strittmatter, S. M., Venable, J. C., and Snyder, S. H. (1986) Enkephalin convertase: localization to specific neuronal pathways J. Neurosci. 6, 1662-1675
60. Prajapati, S. C. and Chauhan, S. S. (2011) Dipeptidyl peptidase III: a multifaceted oligopeptide N-end cutter FEBS J. 278, 3256-3276
61. Kottegoda, S., Pulido, J., Thongkhao-on, K., and Shippy, S. (2007) Demonstration and use of nanoliter sampling of in vivo rat vitreous and vitreoretinal interface Mol. Vision 13, 2073-2082
62. Piyankarage, S. C., Featherstone, D. E., and Shippy, S. A. (2012) Nanoliter hemolymph sampling and analysis of individual adult Drosophila melanogaster Anal. Chem. 84, 4460-4466
63. Pritchett, J., Pulido, J., and Shippy, S. (2008) Measurement of region-specific nitrate levels of the posterior chamber of the rat eye using low-flow push-pull perfusion Anal. Chem. 80, 5342-5349
64. Patterson, E. E., 2nd, Pritchett, J. S., and Shippy, S. A. (2009) High temporal resolution coupling of low-flow push-pull perfusion to capillary electrophoresis for ascorbate analysis at the rat vitreoretinal interface Analyst 134, 401-406
65. Hamsher, A., Xu, H., Guy, Y., Sandberg, M., and Weber, S. (2010) Minimizing tissue damage in electroosmotic sampling Anal. Chem. 82, 6370-6376
66. Jaquins-Gerstl, A., Shu, Z., Zhang, J., Liu, Y., Weber, S. G., and Michael, A. C. (2011) Effect of dexamethasone on gliosis, ischemia, and dopamine extraction during microdialysis sampling in brain tissue Anal. Chem. 83, 7662-7667