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Activation of VIP/PACAP type 2 receptor by the peptide histidine isoleucine in astrocytes influences GLAST-mediated glutamate uptake.

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Goursaud, Stéphanie [UCL] Maloteaux, Jean-Marie [UCL] Hermans, Emmanuel [UCL]

Considering the putative neuroprotective role of the vasoactive intestinal peptide (VIP) and the pituitary adenylyl cyclase-activating polypeptide (PACAP), we investigated the acute modulation of glial glutamate uptake by the structurally related peptide histidine isoleucine (PHI). Using cultures of cortical astrocytes, we demonstrated that a 6 min treatment with 1 mumol/L PHI strongly increased the d-[(3)H]-aspartate uptake velocity from 24.3 +/- 1.9 to 46.8 +/- 3.5 nmol/mg prot/min. This effect was found to reflect an increase in the activity of the GLAST, the predominant functional glutamate transporter in these cultures. The combination of protein kinase A and C inhibitors was effective in blocking the effect of PHI and the use of peptide antagonists contributed to demonstrate the implication of the VIP/PACAP type 2 receptor (VPAC(2)). Accordingly, G-protein activation measures and gene reporter assays revealed the expression of functional PHI-sensitive receptors in cultured astrocytes. Biotinylation/immunoblotting studies indicated that PHI significantly increased the cell surface expression of the GLAST (by 34.24 +/- 8.74 and 43.00 +/- 6.36%, when considering the 72 and 55 kDa immunoreactive proteins, respectively). Such cross-talk between PHI and glutamate transmission systems in glial cells opens attractive perspectives in neuropharmacology.

Document type Article de périodique (Journal article) – Article de recherche – Comparative Study, Journal Article, Research Support, Non-U.S. Gov't
Access type Accès restreint
Publication date 2008
Language Anglais
Journal information "Journal of Neurochemistry" - Vol. 105, no. 4, p. 1165-1175 (2008)
Peer reviewed yes
Publisher Wiley-Blackwell Publishing Ltd. ((United Kingdom) Oxford)
issn 0022-3042
e-issn 1471-4159
Publication status Publié
Affiliations UCL - MD/FSIO - Département de physiologie et pharmacologie
UCL - (SLuc) Centre de référence pour l'épilepsie réfractaire
UCL - (SLuc) Service de neurologie
UCL - MD/NOPS - Département de neurologie et de psychiatrie
MESH Subject Swine ; Receptors, Vasoactive Intestinal Peptide, Type II - agonists - genetics - metabolism ; Rats, Wistar ; Rats ; Peptide PHI - pharmacology - physiology ; Humans ; Glutamic Acid - metabolism ; Cells, Cultured ; Biological Transport - drug effects - physiology ; Astrocytes - drug effects - metabolism ; Animals ; Amino Acid Transport System X-AG - genetics - metabolism
Links
  1. Arriza J. L., J. Neurosci., 14, 5559 (1994)
  2. Beart P M, O'Shea R D, Transporters for L-glutamate: An update on their molecular pharmacology and pathological involvement : Roles and regulation of EAATs, 10.1038/sj.bjp.0706949
  3. Beckman M. L., J. Neurosci., 19, 1 (1999)
  4. Bonde C., Sarup A., Schousboe A., Gegelashvili G., Zimmer J., Noraberg J., Neurotoxic and neuroprotective effects of the glutamate transporter inhibitor dl-threo-beta-benzyloxyaspartate (dl-TBOA) during physiological and ischemia-like conditions, 10.1016/s0197-0186(03)00024-x
  5. Brenneman Douglas E., Neuroprotection: A comparative view of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide, 10.1016/j.peptides.2007.04.002
  6. Brenneman D. E., Ann. NY Acad. Sci., 805, 280 (1996)
  7. Brenneman D. E., Ann. NY Acad. Sci., 921, 109 (2000)
  8. Brenneman Douglas E, Phillips Terry M, Hauser Janet, Hill Joanna M, Spong Catherine Y, Gozes Illana, Complex array of cytokines released by vasoactive intestinal peptide, 10.1016/s0143-4179(03)00022-2
  9. Brown David R., Neuronal Release of Vasoactive Intestinal Peptide Is Important to Astrocytic Protection of Neurons from Glutamate Toxicity, 10.1006/mcne.2000.0840
  10. Conradt M., J. Neurochem., 68, 1244 (1997)
  11. Conradt Marcus, Storck Thorsten, Stoffel Wilhelm, Localization of N-Glycosylation Sites and Functional Role of the Carbohydrate Units of GLAST-1, a Cloned Rat Brain l-glutamate/l-aspartate Transporter, 10.1111/j.1432-1033.1995.tb20514.x
  12. Danbolt Niels C, Glutamate uptake, 10.1016/s0301-0082(00)00067-8
  13. Dejda A., Pharmacol. Rep., 57, 307 (2005)
  14. Dickinson Tracey, Fleetwood-Walker Susan M., VIP and PACAP: very important in pain?, 10.1016/s0165-6147(99)01340-1
  15. Duan S., J. Neurosci., 19, 10193 (1999)
  16. Figiel M., J. Neurosci., 20, 3596 (2000)
  17. Fukushima H., J. Dent. Res., 84, 329 (2005)
  18. González Marco I, Marı́a López-Colomé Ana, Ortega Arturo, Sodium-dependent glutamate transport in Müller glial cells: regulation by phorbol esters, 10.1016/s0006-8993(99)01438-9
  19. Grimaldi Maurizio, Cavallaro Sebastiano, Functional and molecular diversity of PACAP/VIP receptors in cortical neurons and type I astrocytes : PACAP/VIP receptors in neurons and astrocytes, 10.1046/j.1460-9568.1999.00693.x
  20. GUILLET B, VELLY L, CANOLLE B, MASMEJEAN F, NIEOULLON A, PISANO P, Differential regulation by protein kinases of activity and cell surface expression of glutamate transporters in neuron-enriched cultures, 10.1016/j.neuint.2004.10.006
  21. Harmar A. J., Pharmacol. Rev., 50, 265 (1998)
  22. Hazell A. S., J. Neurochem., 68, 2216 (1997)
  23. Kanai Yoshikatsu, Hediger Matthias A., Primary structure and functional characterization of a high-affinity glutamate transporter, 10.1038/360467a0
  24. Kimmich G. A., J. Membr. Biol., 182, 17 (2001)
  25. Kosugi Tatsuro, Kawahara Koichi, Reversed Actrocytic GLT-1 during Ischemia is Crucial to Excitotoxic Death of Neurons, but Contributes to the Survival of Astrocytes themselves, 10.1007/s11064-006-9099-6
  26. Lievens J.-C., Bernal F., Forni C., Mahy N., Kerkerian-Le Goff L., Characterization of striatal lesions produced by glutamate uptake alteration: Cell death, reactive gliosis, and changes in GLT1 and GADD45 mRNA expression, 10.1002/(sici)1098-1136(20000201)29:3<222::aid-glia4>3.0.co;2-0
  27. MacKenzie C. J., Mechanisms of Phospholipase C Activation by the Vasoactive Intestinal Polypeptide/Pituitary Adenylate Cyclase-Activating Polypeptide Type 2 Receptor, 10.1210/en.142.3.1209
  28. Nanmoku T, Stimulation of catecholamine biosynthesis via the PKC pathway by prolactin-releasing peptide in PC12 rat pheochromocytoma cells, 10.1677/joe.1.05919
  29. Pilzer Inbar, Gozes Illana, VIP provides cellular protection through a specific splice variant of the PACAP receptor: A new neuroprotection target, 10.1016/j.peptides.2006.06.007
  30. Pines Gilia, Danbolt Niels C., Bjørås Magnar, Zhang Yumin, Bendahan Annie, Eide Lars, Koepsell Hermann, Storm-Mathisen Jon, Seeberg Erling, Kanner Baruch I., Cloning and expression of a rat brain L-glutamate transporter, 10.1038/360464a0
  31. Rangon C.-M., VPAC2 Receptors Mediate Vasoactive Intestinal Peptide-Induced Neuroprotection against Neonatal Excitotoxic Brain Lesions in Mice, 10.1124/jpet.105.086405
  32. Robinson Michael B., Regulated trafficking of neurotransmitter transporters: common notes but different melodies : Trafficking of neurotransmitter transporters, 10.1046/j.0022-3042.2001.00698.x
  33. Rossi David J., Oshima Takeo, Attwell David, Glutamate release in severe brain ischaemia is mainly by reversed uptake, 10.1038/35002090
  34. Rothstein Jeffrey D., Martin Lee J., Kuncl Ralph W., Decreased Glutamate Transport by the Brain and Spinal Cord in Amyotrophic Lateral Sclerosis, 10.1056/nejm199205283262204
  35. Sassone-Corsi P, Visvader J, Ferland L, Mellon P L, Verma I M, Induction of proto-oncogene fos transcription through the adenylate cyclase pathway: characterization of a cAMP-responsive element., 10.1101/gad.2.12a.1529
  36. Schlüter Karen, Figiel Maciej, Rozyczka Joanna, Engele Jürgen, CNS region-specific regulation of glial glutamate transporter expression : Glial glutamate transporter expression, 10.1046/j.1460-9568.2002.02130.x
  37. Sherwood N. M., The Origin and Function of the Pituitary Adenylate Cyclase-Activating Polypeptide (PACAP)/Glucagon Superfamily, 10.1210/er.21.6.619
  38. Storck T., Schulte S., Hofmann K., Stoffel W., Structure, expression, and functional analysis of a Na(+)-dependent glutamate/aspartate transporter from rat brain., 10.1073/pnas.89.22.10955
  39. Susarla Bala T. S., Seal Rebecca P., Zelenaia Olga, Watson Deborah J., Wolfe John H., Amara Susan G., Robinson Michael B., Differential regulation of GLAST immunoreactivity and activity by protein kinase C: evidence for modification of amino and carboxyl termini : PKC-dependent regulation of GLAST, 10.1111/j.1471-4159.2004.02791.x
  40. Swanson R. A., J. Neurosci., 17, 932 (1997)
  41. Tatemoto K., Mutt V., Isolation and characterization of the intestinal peptide porcine PHI (PHI-27), a new member of the glucagon--secretin family., 10.1073/pnas.78.11.6603
  42. Trotti Davide, Aoki Masashi, Pasinelli Piera, Berger Urs V., Danbolt Niels C., Brown Robert H., Hediger Matthias A., Amyotrophic Lateral Sclerosis-linked Glutamate Transporter Mutant Has Impaired Glutamate Clearance Capacity, 10.1074/jbc.m003779200
  43. Tse D. L.-Y., Identification of a Potential Receptor for Both Peptide Histidine Isoleucine and Peptide Histidine Valine, 10.1210/en.143.4.1327
  44. Tsuda T., J. Biochem. (Tokyo), 102, 1579 (1987)
  45. Vaudry D., Pharmacol. Rev., 52, 269 (2000)
  46. Vermeiren Céline, Najimi Mustapha, Maloteaux Jean-Marie, Hermans Emmanuel, Molecular and functional characterisation of glutamate transporters in rat cortical astrocytes exposed to a defined combination of growth factors during in vitro differentiation, 10.1016/j.neuint.2004.08.004
  47. Vermeiren Céline, Najimi Mustapha, Vanhoutte Nicolas, Tilleux Sébastien, De Hemptinne Isabelle, Maloteaux Jean-Marie, Hermans Emmanuel, Acute up-regulation of glutamate uptake mediated by mGluR5a in reactive astrocytes : mGluR5a-mediated activation of astroglial GLT-1, 10.1111/j.1471-4159.2005.03216.x
  48. Zanassi Patrizia, Paolillo Mayra, Feliciello Antonio, Avvedimento Enrico V., Gallo Vittorio, Schinelli Sergio, cAMP-dependent Protein Kinase Induces cAMP-response Element-binding Protein Phosphorylation via an Intracellular Calcium Release/ERK-dependent Pathway in Striatal Neurons, 10.1074/jbc.m007631200
Bibliographic reference Goursaud, Stéphanie ; Maloteaux, Jean-Marie ; Hermans, Emmanuel. Activation of VIP/PACAP type 2 receptor by the peptide histidine isoleucine in astrocytes influences GLAST-mediated glutamate uptake.. In: Journal of Neurochemistry, Vol. 105, no. 4, p. 1165-1175 (2008)
Permanent URL http://hdl.handle.net/2078.1/11252