Fusion of diphtheria toxin and urotensin II produces a neurotoxin selective for cholinergic neurons in the rat mesopontine tegmentum

Journal of Neurochemistry

Volumn 102, Issue 1, 2007, Pages 112-120

  Clark, S D ^a   Alderson, H L ^b   Winn, P ^b   Latimer, M P ^b   Nothacker, H P ^c   Civelli, O ^c  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF ST ANDREWS   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetylcholine; Fusion toxin; Laterodorsal tegmental nucleus; Pedunculopontine tegmental nucleus

Indexed keywords

CALCIUM; CARRIER PROTEIN; CHOLINE; DIPHTHERIA TOXIN; HYBRID PROTEIN; NEUROTOXIN; RECEPTOR PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE; UNCLASSIFIED DRUG; UROTENSIN II; UROTENSIN II RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOASSAY; BRAIN FUNCTION; CALCIUM MOBILIZATION; CELL LOSS; CHO CELL; CHOLINERGIC NERVE; CONTROLLED STUDY; DEPLETION; IN VITRO STUDY; IN VIVO STUDY; MALE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; TEGMENTUM; WILD TYPE;

ANIMALS; CELL SURVIVAL; CHO CELLS; CRICETINAE; CRICETULUS; DIPHTHERIA TOXIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; MALE; NADPH DEHYDROGENASE; NEURONS; NEUROTOXICITY SYNDROMES; NEUROTOXINS; PARASYMPATHETIC NERVOUS SYSTEM; PLASMIDS; PONS; RATS; TEGMENTUM MESENCEPHALI; UROTENSINS;

MAMMALIA; RATTUS;

EID: 34250197937     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.04529.x     Document Type: Article

References (45)

1. Alderson H. Winn P (2005) The pedunculopontine and reinforcement, in The Basal Ganglia VIII Bolam J., Ingham C. A. Magill P. J., eds Springer Science and Business Media, New York.
2. Alderson H. L., Latimer M. P., Blaha C. D., Phillips A. G. Winn P. (2004) An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioned rats. Neuroscience 125, 349 358.
3. Benoliel R., Eliav E., Mannes A. J., Caudle R. M., Leeman S. Iadarola M. J. (1999) Actions of intrathecal diphtheria toxin- substance P fusion protein on models of persistent pain. Pain 79, 243 253.
4. Blanke S. R., Huang K., Wilson B. A., Papini E., Covacci A. Collier R. J. (1994) Active-site mutations of the diphtheria toxin catalytic domain: role of histidine-21 in nicotinamide adenine dinucleotide binding and ADP-ribosylation of elongation factor 2. Biochemistry 33, 5155 5161.
5. Book A. A., Wiley R. G. Schweitzer J. B. (1994) 192 IgG-saporin: I. Specific lethality for cholinergic neurons in the basal forebrain of the rat. J. Neuropathol. Exp. Neurol. 53, 95 102.
6. Chiron M. F., Fryling C. M. FitzGerald D. J. (1994) Cleavage of pseudomonas exotoxin and diphtheria toxin by a furin-like enzyme prepared from beef liver. J. Biol. Chem. 269, 18 167 18 176.
7. Choe S., Bennett M. J., Fujii G., Curmi P. M., Kantardjieff K. A., Collier R. J. Eisenberg D. (1992) The crystal structure of diphtheria toxin. Nature 357, 216 222.
8. Chudasama Y., Dalley J. W., Nathwani F., Bouger P. Robbins T. W. (2004) Cholinergic modulation of visual attention and working memory: dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learn Mem. 11, 78 86.
9. Clark S. D., Nothacker H. P., Wang Z., Saito Y., Leslie F. M. Civelli O. (2001) The urotensin II receptor is expressed in the cholinergic mesopontine tegmentum of the rat. Brain Res. 923, 120 127.
10. Clark S. D., Nothacker H. P., Blaha C. D., Tyler C. J., Duangdao D. M., Grupke S. L., Helton D. R., Leonard C. S. Civelli O. (2005) Urotensin II acts as a modulator of mesopontine cholinergic neurons. Brain Res. 1059, 139 148.
11. Datta S. Siwek D. F. (2002) Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J. Neurosci. Res. 70, 611 621.
12. Falnes P. O., Wiedlocha A., Rapak A. Olsnes S. (1995) Farnesylation of CaaX-tagged diphtheria toxin A-fragment as a measure of transfer to the cytosol. Biochemistry 34, 11 152 11 159.
13. Fisher C. E., Sutherland J. A., Krause J. E., Murphy J. R., Leeman S. E. vanderSpek J. C. (1996) Genetic construction and properties of a diphtheria toxin-related substance P fusion protein: in vitro destruction of cells bearing substance P receptors. Proc. Natl Acad. Sci. U. S. A. 93, 7341 7345.
14. Frankel A. E., Kreitman R. J. Sausville E. A. (2000) Targeted toxins. Clin Cancer Res 6, 326 334.
15. Garcia-Rill E. Skinner R. D. (1987) The mesencephalic locomotor region. I. Activation of a medullary projection site. Brain Res. 411, 1 12.
16. Giebing G., Tolle M., Jurgensen J. et al. (2005) Arrestin-independent internalization and recycling of the urotensin receptor contribute to long-lasting urotensin II-mediated vasoconstriction. Circ. Res. 97, 707 715.
17. Hanin I. (1990) AF64A-induced cholinergic hypofunction, in Progress in Brain Research, Vol. 84. (Aquilonius S.-M. Gillberg P.-G., eds pp. 289 299. Elsevier Science Publishers, Amsterdam.
18. Hirsch E. C., Graybiel A. M., Duyckaerts C. Javoy-Agid F. (1987) Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc. Natl Acad. Sci. U. S. A. 84, 5976 5980.
19. Huitron-Resendiz S., Kristensen M. P., Sanchez-Alavez M. et al. (2005) Urotensin II modulates rapid eye movement sleep through activation of brainstem cholinergic neurons. J. Neurosci. 25, 5465 5474.
20. Inglis W. L., Dunbar J. S. Winn P. (1993) Barbiturate anaesthesia reduces the neurotoxic effects of quinolinate but not ibotenate in the rat pedunculopontine tegmental nucleus. Neurosci Lett 156, 78 82.
21. Inglis W. L., Olmstead M. C. Robbins T. W. (2001) Selective deficits in attentional performance on the 5-choice serial reaction time task following pedunculopontine tegmental nucleus lesions. Behav. Brain Res. 123, 117 131.
22. Itoh H., McMaster D. Lederis K. (1988) Functional receptors for fish neuropeptide urotensin II in major rat arteries. Eur. J. Pharmacol. 149, 61 66.
23. Jellinger K. (1988) The pedunculopontine nucleus in Parkinson's disease, progressive supranuclear palsy and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 51, 540 543.
24. Knusel B. Hefti F. (1988) Development of cholinergic pedunculopontine neurons in vitro: comparison with cholinergic septal cells and response to nerve growth factor, ciliary neuronotrophic factor, and retinoic acid. J. Neurosci. Res. 21, 365 375.
25. Lanca A. J., Adamson K. L., Coen K. M., Chow B. L. Corrigall W. A. (2000) The pedunculopontine tegmental nucleus and the role of cholinergic neurons in nicotine self-administration in the rat: a correlative neuroanatomical and behavioral study. Neuroscience 96, 735 742.
26. McGaughy J., Kaiser T. Sarter M. (1996) Behavioral vigilance following infusions of 192 IgG-saporin into the basal forebrain: selectivity of the behavioral impairment and relation to cortical AChE-positive fiber density. Behav. Neurosci. 110, 247 265.
27. McGaughy J., Everitt B. J., Robbins T. W. Sarter M. (2000) The role of cortical cholinergic afferent projections in cognition: impact of new selective immunotoxins. Behav. Brain. Res. 115, 251 263.
28. Mena-Segovia J., Bolam J. P. Magill P. J. (2004) Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Trends Neurosci. 27, 585 588.
29. Nothacker H. P., Wang Z., McNeill A. M., Saito Y., Merten S., O'Dowd B., Duckles S. P. Civelli O. (1999) Identification of the natural ligand of an orphan G-protein-coupled receptor involved in the regulation of vasoconstriction. Nat. Cell Biol. 1, 383 385.
30. Oakman S. A., Faris P. L., Kerr P. E., Cozzari C. Hartman B. K. (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J. Neurosci. 15, 5859 5869.
31. Oh K. J., Zhan H., Cui C., Hideg K., Collier R. J. Hubbell W. L. (1996) Organization of diphtheria toxin T domain in bilayers: a site-directed spin labeling study. Science 273, 810 812.
32. Olmstead M. C., Munn E. M., Franklin K. B. Wise R. A. (1998) Effects of pedunculopontine tegmental nucleus lesions on responding for intravenous heroin under different schedules of reinforcement. J. Neurosci. 18, 5035 5044.
33. Pearson D., Shively J. E., Clark B. R., Geschwind I. I., Barkley M., Nishioka R. S. Bern H. A. (1980) Urotensin II: a somatostatin-like peptide in the caudal neurosecretory system of fishes. Proc. Natl Acad. Sci. U. S. A. 77, 5021 5024.
34. Rodriguez M., Mantolan-Sarmiento B. Gonzalez-Hernandez T. (1998) Effects of ethylcholine mustard azirinium ion (AF64A) on the choline acetyltransferase and nitric oxide synthase activities in mesopontine cholinergic neurons of the rat. Neuroscience 82, 853 866.
35. Simpson J. C., Smith D. C., Roberts L. M. Lord J. M. (1998) Expression of mutant dynamin protects cells against diphtheria toxin but not against ricin. Exp. Cell. Res. 239, 293 300.
36. Takahashi K., Totsune K., Murakami O. Shibahara S. (2001) Expression of urotensin II and urotensin II receptor mRNAs in various human tumor cell lines and secretion of urotensin II-like immunoreactivity by SW-13 adrenocortical carcinoma cells. Peptides 22, 1175 1179.
37. Takakusaki K., Shiroyama T., Yamamoto T. Kitai S. T. (1996) Cholinergic and noncholinergic tegmental pedunculopontine projection neurons in rats revealed by intracellular labeling. J. Comp. Neurol. 371, 345 361.
38. Takakusaki K., Shiroyama T. Kitai S. T. (1997) Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79, 1089 1109.
39. Torres E. M., Perry T. A., Blockland A., Wilkinson L. S., Wiley R. G., Lappi D. A. Dunnet S. B. (1994) Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 63, 95 122.
40. Vincent S. R. Kimura H. (1992) Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46, 755 784.
41. Vincent S. R., Satoh K., Armstrong D. M. Fibiger H. C. (1983) NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci. Lett. 43, 31 36.
42. Wiley R. G., Oeltmann T. N. Lappi D. A. (1991) Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor. Brain Res. 562, 149 153.
43. Winn P. (1991) Excitotoxins as tools for producing brain lesions, in Methods in Neurosciences vol. 7: Lesions and Transplantation, Vol. 7 (Conn P., ed pp. 16 27. Academic Press, San Diego.
44. Winn P. (1998) Frontal syndrome as a consequence of lesions in the pedunculopontine tegmental nucleus: a short theoretical review. Brain Res Bull 47, 551 563.
45. Woolf N. J. (1991) Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37, 475 524.