The coexistence of VGluT2 and neurotensin or leu-enkephalin in the medullary dorsal horn: A confocal and electron microscopic immunohistochemical study in the rat

Neuroscience Letters

Volumn 584, Issue , 2014, Pages 390-394

  Liu, Tao ^a,b   Li, Jinlian ^a   Liu, Hui ^b   Wang, Xin ^c   Fan, Feiyan ^b   Zhang, Pengxing ^b   Tu, Yanyang ^b,c   Zhang, Yongsheng ^b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Enkephalin; Fluorescent immunohistochemistry; Medullary dorsal horn; Neurotensin; Rat; The second vesicular glutamate transporter

Indexed keywords

ENKEPHALIN; GLUTAMIC ACID; LEUCINE ENKEPHALIN; NEUROTENSIN; VESICULAR GLUTAMATE TRANSPORTER 2; SLC17A6 PROTEIN, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITE; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNEURON; NERVE CELL; NERVE ENDING; NONHUMAN; RAT; SPINAL CORD DORSAL HORN; ANIMAL; CONFOCAL MICROSCOPY; MEDULLA OBLONGATA; METABOLISM; POSTERIOR HORN CELL; SYNAPTOSOME; WISTAR RAT;

ANIMALS; ENKEPHALIN, LEUCINE; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; NEUROTENSIN; POSTERIOR HORN CELLS; PRESYNAPTIC TERMINALS; RATS, WISTAR; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84911888116     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2014.11.008     Document Type: Article

References (37)

1. Mason P. Medullary circuits for nociceptive modulation. Curr. Opin. Neurobiol. 2012, 22:640-645.
2. Leite-Almeida H., Valle-Fernandes A., Almeida A. Brain projection from the medullary dorsal reticular nucleus: an anterograde and retrograde tracing study in the rat. Neuroscience 2006, 140:577-595.
3. Difiglia M., Aronin N., Leeman S.E. Ultrastructural localization of immunoreactive neurotensin in the monkey superficial dorsal horn. J. Comp. Neurol. 1984, 225:1-12.
4. Kadiri N., Rodeau J.L., Schlichter R., Hugel S. Neurotensin inhibits background K+ channels and facilitates glutamatergic transmission in rat spinal cord dorsal horn. Eur. J. Neurosci. 2011, 34:1230-1240.
5. Marvizón J.C., Chen W., Murphy N. Enkephalins, dynorphins, and beta-endorphin in the rat dorsal horn: an immunofluorescence colocalization study. J. Comp. Neurol. 2009, 517:51-68.
6. St-Gelais F., Jomphe C., Trudeau L.E. The role of neurotensin in central nervous system pathophysiology: what is the evidence?. J. Psychiatry Neurosci. 2006, 31:229-245.
7. Ribeiro-da-Silva A., Pioro E.P., Cuello A.C. Substance P- and enkephalin-like immunoreactivities are colocalized in certain neurons of the substantia gelatinosa of the rat spinal cord: an ultrastructural double-labeling study. J. Neurosci. 1991, 11:1068-1080.
8. Fukushima T., Tsuda M., Kofuji T., Hori Y. Physiological properties of enkephalin-containing neurons in the spinal dorsal horn visualized by expression of green fluorescent protein in BAC transgenic mice. BMC Neurosci. 2011, 12:36.
9. Gupta K., Vats I.D., Gupta Y.K., Saleem K., Pasha S. Lack of tolerance and morphine-induced cross-tolerance to the analgesia of chimeric peptide of Met-enkephalin and FMRFa. Peptides 2008, 29:2266-2275.
10. Kleczkowska P., Lipkowski A.W. Neurotensin and neurotensin receptors: characteristic, structure-activity relationship and pain modulation-a review. Eur. J. Pharmacol. 2013, 716:54-60.
11. Mustain W.C., Rychahou P.G., Evers B.M. The role of neurotensin in physiologic and pathologic processes. Curr. Opin. Endocrinol. Diabetes Obes. 2011, 18:75-82.
12. Takamori S. VGLUTs: 'exciting' times for glutamatergic research?. Neurosci. Res. 2006, 55:343-351.
13. Herzog E., Bellenchi G.C., Gras C., Bernard V., Ravassard P., Bedet C., Gasnier B., Giros B., El Mestikawy S. The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci. 2001, 21:RC181.
14. Anne C., Gasnier B. Vesicular neurotransmitter transporters: mechanistic aspects. Curr. Top Membr. 2014, 73:149-174.
15. Kaneko T., Fujiyama F. Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci. Res. 2002, 42:243-250.
16. Kaneko T., Fujiyama F., Hioki H. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J. Comp. Neurol. 2002, 444:39-62.
17. Li J.L., Fujiyama F., Kaneko T., Mizuno N. Expression of vesicular glutamate transporters VGluT1 and VGluT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat. J. Comp. Neurol. 2003, 457:236-249.
18. Li J.L., Xiong K.H., Dong Y.L., Fujiyama F., Kaneko T., Mizuno N. Vesicular glutamate transporters VGluT1 and VGluT2, in the trigeminal ganglion neurons of the rat, with special reference to coexpression. J. Comp. Neurol. 2003, 463:212-220.
19. Takamori S., Rhee J.S., Rosenmund C., Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 2000, 407:189-194.
20. Todd A.J., Hughes D.I., Polgar E., Nagy G.G., Mackie M., Ottersen O.P., Maxwell D.J. The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur. J. Neurosci. 2003, 17:13-27.
21. Olszewski J. On the anatomical and functional organization of the spinal trigeminal nucleus. J. Comp. Neurol. 1995, 92:401-413.
22. Waite P.M.E. Trigeminal sensory system. The rat nervous system 2004, 817-851. Elsevier, Amsterdam. 3rd ed. G. Paxinos (Ed.).
23. Zhang X., Nicholas A.P., Hökfelt T. Ultrastructural studies on peptides in the dorsal horn of the rat spinal cord-II. Co-existence of galanin with other peptides in local neurons. Neuroscience 1995, 64:875-891.
24. Huang J., Chen J., Wang W., Wang W., Koshimizu Y., Wei Y.Y., Kaneko T., Li Y.Q., Wu S.X. Neurochemical properties of enkephalinergic neurons in lumbar spinal dorsal horn revealed by preproenkephalin-green fluorescent protein transgenic mice. J. Neuronchem. 2010, 113:1555-1564.
25. Katoh S., Hisano S., Kawano H., Kagotani Y., Daikoku S. Light- and electron-microscopic evidence of costoring of immunoreactive enkephalins and substance P in dorsal horn neurons of rat. Cell Tissue Res. 1988, 253:297-303.
26. Tiong S.Y., Polgár E., van Kralingen J.C., Watanabe M., Todd A.J. Galanin-immunoreactivity identifies a distinct population of inhibitory interneurons in laminae I-III of the rat spinal cord. Mol. Pain 2011, 7:36.
27. Polgár E., Durrieux C., Hughes D.I., Todd A.J. A quantitative study of inhibitory interneurons in laminae I-III of the mouse spinal dorsal horn. PLoS One 2013, 8:e78309.
28. Leah J., Menetrey D., de Pommery J. Neuropeptides in long ascending spinal tract cells in the rat: evidence for parallel processing of ascending information. Neuroscience 1988, 24:195-207.
29. Todd A.J., Russell G., Spike R.C. Immunocytochemical evidence that GABA and neurotensin exist in different neurons in laminae II and III of rat spinal dorsal horn. Neuroscience 1992, 47:685-691.
30. Todd A.J., Spike R.C., Price R.F., Neilson M. Immunocytochemical evidence that neurotensin is present in glutamatergic neurons in the superficial dorsal horn of the rat. J. Neurosci. 1994, 14:774-784.
31. Song B., Marvizón J.C. Dorsal horn neurons firing at high frequency but not primary afferents, release opioid peptides that produce micro-opioid receptor internalization in the rat spinal cord. J. Neurosci. 2003, 23:9171-9184.
32. Weihe E., Nohr D., Hartschuh W. Immunohistochemical evidence for a co-transmitter role of opioid peptides in primary sensory neurons. Prog. Brain Res. 1988, 74:189-199.
33. Todd A.J., Spike R.C., Russell G., Johnston H.M. Immunohistochemical evidence that Met-enkephalin and GABA coexist in some neurons in rat dorsal horn. Brain Res. 1992, 584:149-156.
34. Yasaka T., Tiong S.Y., Hughes D.I., Riddell J.S., Todd A.J. Populations of inhibitory and excitatory interneurons in lamina II of the adult rat spinal dorsal horn revealed by a combined electrophysiological and anatomical approach. Pain 2010, 151:475-488.
35. Santos S.F., Rebelo S., Derkach V.A., Safronov B.V. Excitatory interneurons dominate sensory processing in the spinal substantia gelatinosa of rat. J. Physiol. 2007, 581:241-254.
36. Bannatyne B.A., Edgley S.A., Hammar I., Jankowska E., Maxwell D.J. Differential projections of excitatory and inhibitory dorsal horn interneurons relaying information from group II muscle afferents in the cat spinal cord. J. Neurosci. 2006, 26:2871-2880.
37. Todd A.J., Spike R.C. The localization of classical transmitters and neuropeptides within neurons in laminae I-III of the mammalian spinal dorsal horn. Prog. Neurobiol. 1993, 41:609-645.