Neurokinins robustly activate the majority of septohippocampal cholinergic neurons

European Journal of Neuroscience

Volumn 27, Issue 1, 2008, Pages 114-122

  Morozova, Elena ^a   Wu, Min ^a   Dumalska, Iryna ^a   Alreja, Meenakshi ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Acetylcholine; Hippocampus; Medial septum; Rat; Tachykinins

Indexed keywords

HEMOKININ 1; NEUROKININ; TACHYKININ DERIVATIVE; TACHYKININ RECEPTOR; TACHYKININ RECEPTOR 1; TACHYKININ RECEPTOR 2; TACHYKININ RECEPTOR 3; TACHYKININ RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; HIPPOCAMPUS; MALE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

ACETYLCHOLINE; ANIMALS; ANIMALS, NEWBORN; DOSE-RESPONSE RELATIONSHIP, DRUG; HIPPOCAMPUS; MALE; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TACHYKININ; SEPTUM OF BRAIN; TACHYKININS;

EID: 37749039070     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2007.05993.x     Document Type: Article

References (48)

1. Alreja, M. Liu, W. (1996) Noradrenaline induces IPSCs in rat medial septal/diagonal band neurons: involvement of septohippocampal GABAergic neurons. J. Physiol., 494, 201 215.
2. Alreja, M., Wu, M., Liu, W., Atkins, J.B., Leranth, C. Shanabrough, M. (2000) Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J. Neurosci., 20, 8103 8110.
3. Arendt, T., Brückner, M.K., Bigl, V. Marcova, L. (1995) Dendritic reorganisation in the basal forebrain under degenerative conditions and its defects in Alzheimer's disease. II. Ageing, Korsakoff's disease, Parkinson's disease, and Alzheimer's disease. J. Comp. Neurol., 351, 189 222.
4. Beaujouan, J.C., Torrens, Y., Saffroy, M. Glowinski, J. (1986) Quantitative autoradiographic analysis of the distribution of binding sites for [125I]Bolton Hunter derivatives of eledoisin and substance P in the rat brain. Neuroscience, 18, 857 875.
5. Bellucci, F., Carini, F., Catalani, C., Cucchi, P., Lecci, A., Meini, S., Patacchini, R., Quartara, L., Ricci, R., Tramontana, M., Giuliani, S. Maggi, C.A. (2002) Pharmacological profile of the novel mammalian tachykinin, hemokinin 1. Br. J. Pharmacol., 135, 266 274.
6. Chen, L.W., Wei, L.C., Liu, H.L., Qiu, Y. Chan, Y.S. (2001) Cholinergic neurons expressing substance P receptor (NK(1)) in the basal forebrain of the rat: a double immunocytochemical study. Brain Res., 904, 161 166.
7. Chen, L.W., Yung, K.K. Chan, Y.S. (2004) Neurokinin peptides and neurokinin receptors as potential therapeutic intervention targets of basal ganglia in the prevention and treatment of Parkinson's disease. Curr. Drug Targets, 5, 197 206.
8. Deal, M.J., Hagan, R.M., Ireland, S.J., Jordan, C.C., McElroy, A.B., Porter, B., Ross, B.C., Stephens-Smith, M. Ward, P. (1992) Conformationally constrained tachykinin analogues: potent and highly selective neurokinin NK-2 receptor agonists. J. Med. Chem., 35, 4195 4204.
9. Desvignes, C., Rouquier, L., Souilhac, J., Mons, G., Rodier, D., Soubrié, P. Steinberg, R. (2003) Control by tachykinin NK(2) receptors of CRF(1) receptor-mediated activation of hippocampal acetylcholine release in the rat and guinea-pig. Neuropeptides, 37, 89 97.
10. Duffy, R.A., Hedrick, J.A., Randolph, G., Morgan, C.A., Cohen-Williams, M.E., Vassileva, G., Lachowicz, J.E., Laverty, M., Maguire, M., Shan, L.S., Gustafson, E. Varty, G.B. (2003) Centrally administered hemokinin-1 (HK-1), a neurokinin NK1 receptor agonist, produces substance P-like behavioral effects in mice and gerbils. Neuropharmacology, 45, 242 250.
11. Furuta, T., Koyano, K., Tomioka, R., Yanagawa, Y. Kaneko, T. (2004) GABAergic basal forebrain neurons that express receptor for neurokinin B and send axons to the cerebral cortex. J. Comp. Neurol., 473, 43 58.
12. Geraghty, D.P. Maguire, C.M. (2002) Reduced [125I]-Bolton Hunter substance P binding (NK1 receptors) in the basal forebrain nuclei of aged rats. Clin. Exp. Pharmacol. Physiol., 29, 1112 1115.
13. Gerfen, C. (1991) Substance P (neurokinin-1) receptor mRNA is selectively expressed in cholinergic neurons in the striatum and basal forebrain. Brain Res., 556, 165 170.
14. Griebel, G. (1999) Is there a future for neuropeptide receptor ligands in the treatment of anxiety disorders? Pharmacol. Ther., 82, 1 61.
15. Härtig, W., Seeger, J., Naumann, T., Brauer, K. Brückner, G. (1998) Selective in vivo fluorescence labelling of cholinergic neurons containing p75 (NTR) in the rat basal forebrain. Brain Res., 808, 155 165.
16. Kasai, H. (1993) Cytosolic Ca2+ gradients, Ca2+ binding proteins and synaptic plasticity. Neurosci. Res., 16, 1 7.
17. Kramer, M.S., Cutler, N., Feighner, J., Shrivastava, R., Carman, J., Sramek, J.J., Reines, S.A., Liu, G., Snavely, D., Wyatt-Knowles, E., Hale, J.J., Mills, S.G., MacCoss, M., Swain, C.J., Harrison, T., Hill, R.G., Hefti, F., Scolnick, E.M., Cascieri, M.A., Chicchi, G.G., Sadowski, S., Williams, A.R., Hewson, L., Smith, D., Carlson, E.J., Hargreaves, R.J. Rupniak, N.M. (1998) Distinct mechanism for antidepressant activity by blockade of central substance P receptors. Science, 281, 1640 1645.
18. Kurtz, M.M., Wang, R., Clements, M.K., Cascieri, M.A., Austin, C.P., Cunningham, B.R., Chicchi, G.G. Liu, Q. (2002) Identification, localization and receptor characterization of novel mammalian substance P-like peptides. Gene, 296, 205 212.
19. Lamour, Y., Dutar, P. Jobert, A. (1984) Septo-hippocampal and other medial septum-diagonal band neurons: electrophysiological and pharmacological properties. Brain Res., 309, 227 239.
20. Lamour, Y., Senut, M., Dutar, P. Bassant, M. (1988) Neuropeptides and septo-hippocampal neurons: electrophysiological effects and distributions of immunoreactivity. Peptides, 9, 1351 1359.
21. Li, Y.W. Guyenet, P.G. (1997) Effect of substance P on C1 and other bulbospinal cells of the RVLM in neonatal rats. Am. J. Physiol., 273, R805 R813.
22. Lucas, L.R., Hurley, D.L., Krause, J.E. Harlan, R.E. (1992) Localization of the tachykinin neurokinin B precursor peptide in rat brain by immunocytochemistry and in situ hybridization. Neuroscience, 51, 317 345.
23. Mantyh, P.W., Hunt, S.P. Maggio, J.E. (1984) Substance P receptors: localization by light microscopic autoradiography in rat brain using [3H]SP as the radioligand. Brain Res., 307, 147 165.
24. Marco, N., Thirion, A., Mons, G., Bougault, I., Le Fur, G., Soubrié, P. Steinberg, R. (1998) Activation of dopaminergic and cholinergic neurotransmission by tachykinin NK3 receptor stimulation: an in vivo microdialysis approach in guinea pig. Neuropeptides, 32, 481 488.
25. Maubach, K.A. Jones, R.S. (1997) Electrophysiological characterisation of tachykinin receptors in the rat nucleus of the solitary tract and dorsal motor nucleus of the vagus in vitro. Br. J. Pharmacol., 122, 1151 1159.
26. Merchenthaler, I., Maderdrut, J.L., O'Harte, F. Conlon, J.M. (1992) Localization of neurokinin B in the central nervous system of the rat. Peptides, 13, 815 829.
27. Mufson, E.J., Bothwell, M. Kordower, J.H. (1989) Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: a quantitative analysis across subregions of the basal forebrain. Exp. Neurol., 105, 221 232.
28. Ogier, R. Raggenbass, M. (2003) Action of tachykinins in the rat hippocampus: modulation of inhibitory synaptic transmission. Eur. J. Neurosci., 17, 2639 2647.
29. Page, N.M. (2004) Hemokinins and endokinins. Cell Mol. Life Sci., 61, 1652 1663.
30. Pennefather, J.N., Lecci, A., Candenas, M.L., Patak, E., Pinto, F.M. Maggi, C.A. (2004) Tachykinins and tachykinin receptors: a growing family. Life Sci., 74, 1445 1463.
31. Peterson, G.M. Shurlow, C.L. (1992) Morphological evidence for a substance P projection from medial septum to hippocampus. Peptides, 13, 509 517.
32. Ptak, K., Konrad, M., Di Pasquale, E., Tell, F., Hilaire, G. Monteau, R. (2000) Cellular and synaptic effect of substance P on neonatal phrenic motoneurons. Eur. J. Neurosci., 12, 126 138.
33. Regehr, W.G., Connor, J.A. Tank, D.W. (1989) Optical imaging of calcium accumulation in hippocampal pyramidal cells during synaptic activation. Nature, 341, 533 536.
34. Saffroy, M., Torrens, Y., Glowinski, J. Beaujouan, J.C. (2003) Autoradiographic distribution of tachykinin NK2 binding sites in the rat brain: comparison with NK1 and NK3 binding sites. Neuroscience, 116, 761 773.
35. Shughrue, P.J., Lane, M.V. Merchenthaler, I. (1996) In situ hybridization analysis of the distribution of neurokinin-3 mRNA in the rat central nervous system. J. Comp. Neurol., 372, 395 414.
36. Stacey, A.E., Woodhall, G.L. Jones, R.S. (2002) Neurokinin-receptor- mediated depolarization of cortical neurons elicits an increase in glutamate release at excitatory synapses. Eur. J. Neurosci., 16, 1896 1906.
37. Steinberg, R., Marco, N., Voutsinos, B., Bensaid, M., Rodier, D., Souilhac, J., Alonso, R., Oury-Donat, F., Le Fur, G. Soubrie, P. (1998) Expression and presence of septal neurokinin-2 receptors controlling hippocampal acetylcholine release during sensory stimulation in rat. Eur. J. Neurosci., 10, 2337 2345.
38. Steinberg, R., Alonso, R., Griebel, G., Bert, L., Jung, M., Oury-Donat, F., Poncelet, M., Gueudet, C., Desvignes, C., Le Fur, G. Soubrié, P. (2001) Selective blockade of neurokinin-2 receptors produces antidepressant-like effects associated with reduced corticotropin-releasing factor function. J. Pharmacol. Exp. Ther., 299, 449 458.
39. Sutin, E.L. Jacobowitz, D.M. (1990) Localization of substance P mRNA in cholinergic cells of the rat laterodorsal tegmental nucleus: in situ hybridization histochemistry and immunocytochemistry. Cell Mol. Neurobiol., 10, 19 31.
40. Tsien, R.Y. (1980) New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry, 19, 2396 2404.
41. Whitehouse, P.J., Price, D.L., Struble, R.G., Clark, A.W., Coyle, J.T. Delon, M.R. (1982) Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science, 215, 1237 1239.
42. Wu, M., Shanabrough, M., Leranth, C. Alreja, M. (2000) Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: implications for learning and memory. J. Neurosci., 20, 3900 3908.
43. Wu, M., Hajszan, T., Leranth, C. Alreja, M. (2003a) Nicotine recruits a local glutamatergic circuit to excite septohippocampal GABAergic neurons. Eur. J. Neurosci., 18, 1155 1168.
44. Wu, M., Newton, S.S., Atkins, J.B., Xu, C., Duman, R.S. Alreja, M. (2003b) Acetylcholinesterase inhibitors activate septohippocampal GABAergic neurons via muscarinic but not nicotinic receptors. J. Pharmacol. Exp. Ther., 307, 535 543.
45. Wu, M., Hajszan, T., Xu, C., Leranth, C. Alreja, M. (2004a) Group I metabotropic glutamate receptor activation produces a direct excitation of identified septohippocampal cholinergic neurons. J. Neurophysiol., 92, 1216 1225.
46. Wu, M., Zaborszky, L., Hajszan, T., van den Pol, A.N. Alreja, M. (2004b) Hypocretin/orexin innervation and excitation of identified septohippocampal cholinergic neurons. J. Neurosci., 24, 3527 3536.
47. Xu, C., Datta, S., Wu, M. Alreja, M. (2004) Hippocampal theta rhythm is reduced by suppression of the H-current in septohippocampal GABAergic neurons. Eur. J. Neurosci., 19, 2299 2309.
48. Zhang, Y., Lu, L., Furlonger, C., Wu, G.E. Paige, C.J. (2000) Hemokinin is a hematopoietic-specific tachykinin that regulates B lymphopoiesis. Nat. Immunol., 1, 392 397.