Immunolocalization of ecto-nucleoside triphosphate diphosphohydrolase 3 in rat brain: Implications for modulation of multiple homeostatic systems including feeding and sleep-wake behaviors

Neuroscience

Volumn 137, Issue 4, 2006, Pages 1331-1346

  Belcher, S M ^a   Zsarnovszky, A ^a,b   Crawford, P A ^a   Hemani, H ^a   Spurling, L ^a   Kirley, T L ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF VETERINARY MEDICINE   (Hungary)

Author keywords

CD39L3; Immunohistochemistry; NTPDase3; Nucleoside triphosphate diphosphohydrolase; Orexin hypocretin co localization; Purinergic signaling

Indexed keywords

NUCLEOSIDE TRIPHOSPHATE; OREXIN A; PHOSPHATASE; PROTEIN NTPDASE3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; FEMALE; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; LATERAL HYPOTHALAMUS; NONHUMAN; NORADRENERGIC NERVE; NUCLEOTIDE SEQUENCE; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SLEEP WAKING CYCLE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CLONING, MOLECULAR; FEEDING BEHAVIOR; FEMALE; HOMEOSTASIS; MOLECULAR SEQUENCE DATA; NERVE FIBERS; OVARIECTOMY; PEPTIDE FRAGMENTS; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; PYROPHOSPHATASES; RATS; SLEEP; WAKEFULNESS;

EID: 31144457368     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2005.08.086     Document Type: Article

References (56)

1. A. Banjac, N. Nedeljkovic, A. Horvat, D. Kanazir, G. Nikezic Ontogenetic profile of ecto-ATPase activity in rat hippocampal and caudate nucleus synaptic plasma membrane fractions Physiol Res 50 2001 411 417
2. F. Bigonnesse, S.A. Levesque, F. Kukulski, J. Lecka, S.C. Robson, M.J. Fernandes, J. Sevigny Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-8 Biochemistry 43 2004 5511 5519
3. N. Braun, S. Fengler, C. Ebeling, J. Servos, H. Zimmermann Sequencing, functional expression and characterization of rat NTPDase6, a nucleoside diphosphatase and novel member of the ecto-nucleoside triphosphate diphosphohydrolase family Biochem J 351 2000 639 647
4. N. Braun, J. Sevigny, S.C. Robson, K. Enjyoji, O. Guckelberger, K. Hammer, F. Di Virgilio, H. Zimmermann Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain Eur J Neurosci 12 2000 4357 4366
5. N. Braun, J. Sevigny, S.K. Mishra, S.C. Robson, S.W. Barth, R. Gerstberger, K. Hammer, H. Zimmermann Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain Eur J Neurosci 17 2003 1355 1364
6. N. Braun, J. Sevigny, S.C. Robson, K. Hammer, M. Hanani, H. Zimmermann Association of the ecto-ATPase NTPDase2 with glial cells of the peripheral nervous system Glia 45 2004 124 132
7. G. Burnstock Noradrenaline and ATP cotransmitters and neuromodulators J Physiol Pharmacol 46 1995 365 384
8. B.P. Chadwick, A.M. Frischauf The CD39-like gene family Identification of three new human members (CD39L2, CD39L3, and CD39L4), their murine homologues, and a member of the gene family from Drosophila melanogaster Genomics 50 1998 357 367
9. D.A. Hager, R.R. Burgess Elution of proteins from sodium dodecyl sulfate-polyacrylamide gels, removal of sodium dodecyl sulfate, and renaturation of enzymatic activity results with sigma subunit of Escherichia coli RNA polymerase, wheat germ DNA topoisomerase, and other enzymes Anal Biochem 109 1980 76 86
10. G.R. Hayes, A.M. Williams, J.J. Lucas, C.A. Enns Structure of human transferrin receptor oligosaccharides conservation of site-specific processing Biochemistry 36 1997 5276 5284
11. A. Helenius, M. Aebi Intracellular functions of N-linked glycans Science 291 2001 2364 2369
12. C.A. Hicks-Berger, B.P. Chadwick, A.-M. Frischauf, T.L. Kirley Expression and characterization of soluble and membrane-bound human nucleoside triphosphate diphosphohydrolase 6 (CD39L2) J Biol Chem 275 2000 34041 34045
13. V.V. Ivanenkov, J. Meller, T.L. Kirley Characterization of disulfide bonds in human nucleoside triphosphate diphosphohydrolase 3 (NTPDase3) Implications for NTPDase structural modeling Biochemistry 44 2005 8998 9012
14. R.L. Jakab, J.K. Wong, S.M. Belcher Estrogen receptor beta immunoreactivity in differentiating cells of the developing rat cerebellum J Comp Neurol 430 2001 396 409
15. S.P. Kalra, M.G. Dube, S. Pu, B. Xu, T.L. Horvath, P.S. Kalra Interacting appetite-regulating pathways in the hypothalamic regulation of body weight Endocr Rev 20 1999 68 100
16. K.A. Keay, R. Bandler Periaqueductal gray chapter 10 G. Paxinos The rat nervous system 2004 Academic Press San Diego 244 253
17. B.F. King, A. Townsend-Nicholson, G. Burnstock Metabotropic receptors for ATP and UTP exploring the correspondence between native and recombinant nucleotide receptors Trends Pharmacol Sci 19 1998 506 514
18. T.L. Kirley, F. Yang, V.V. Ivanenkov Site-directed mutagenesis of human nucleoside triphosphate diphosphohydrolase 3 The importance of conserved glycine residues and the identification of additional conserved protein motifs in eNTPDases Arch Biochem Biophys 395 2001 94 102
19. F. Kukulski, M. Komoszynski Purification and characterization of NTPDase1 (ecto-apyrase) and NTPDase2 (ecto-ATPase) from porcine brain cortex synaptosomes Eur J Biochem 270 2003 3447 3454
20. F. Kukulski, J. Sevigny, M. Komoszynski Comparative hydrolysis of extracellular adenine nucleotides and adenosine in synaptic membranes from porcine brain cortex, hippocampus, cerebellum and medulla oblongata Brain Res 1030 2004 49 56
21. E.G. Lavoie, F. Kukulski, S.A. Levesque, J. Lecka, J. Sevigny Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-3 Biochem Pharmacol 67 2004 1917 1926
22. R.J. Liu, A.N. van den Pol, G.K. Aghajanian Hypocretins (orexins) regulate serotonin neurons in the dorsal raphe nucleus by excitatory direct and inhibitory indirect actions J Neurosci 22 2002 9453 9464
23. F. Maley, R.B. Trimble, A.L. Tarentino, T.H. Plummer Jr Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases Anal Biochem 180 1989 195 204
24. C.R. Maliszewski, G.J. Delespesse, M.A. Schoenborn, R.J. Armitage, W.C. Fanslow, T. Nakajima, E. Baker, G.R. Sutherland, K. Poindexter, C. Birks, A. Alpert, D. Friend, S.D. Gimpel, R.B.I. Gayle The CD39 lymphoid cell activation antigen. Molecular cloning and structural characterization J Immunol 153 1994 3574 3583
25. J. Mateo, T.K. Harden, J.L. Boyer Functional expression of a cDNA encoding a human ecto-ATPase Br J Pharmacol 128 1999 396 402
26. I. Matsuzaki, T. Sakurai, K. Kunii, T. Nakamura, M. Yanagisawa, K. Goto Involvement of the serotonergic system in orexin-induced behavioral alterations in rats Regul Pept 104 2002 119 123
27. J.J. Mulero, G. Yeung, S.T. Nelken, J.M. Bright, D.W. McGowan, J.E. Ford Biochemical characterization of CD39L4 Biochemistry 39 2000 12924 12928
28. D.M. Murphy, V.V. Ivanenkov, T.L. Kirley Identification of cysteine residues responsible for oxidative cross-linking and chemical inhibition of human nucleoside triphosphate diphosphohydrolase 3 J Biol Chem 277 2002 6162 6169
29. D.M. Murphy, T.L. Kirley Asparagine 81, an invariant glycosylation site near apyrase conserved region 1, is essential for full enzymatic activity of ecto nucleoside triphosphate diphosphohydrolase 3 Arch Biochem Biophys 413 2003 107 115
30. T. Nambu, T. Sakurai, K. Mizukami, Y. Hosoya, M. Yanagisawa, K. Goto Distribution of orexin neurons in the adult rat brain Brain Res 827 1999 243 260
31. N. Nedeljkovic, A. Banjac, A. Horvat, M. Stojiljkovic, G. Nikezic Ecto-ATPase and ecto-ATP-diphosphohydrolase are co-localized in rat hippocampal and caudate nucleus synaptic plasma membranes Physiol Res 52 2003 797 804
32. N. Nedeljkovic, V. Djordjevic, A. Horvat, G. Nikezic, D.T. Kanazir Effect of steroid hormone deprivation on the expression of ecto-ATPase in distinct brain regions of female rats Physiol Res 49 2000 419 426
33. R.A. North Molecular physiology of P2X receptors Physiol Rev 82 2002 1013 1067
34. J.G. Paez, J.A. Recio, A. Rouzaut, V. Notario Identity between the PCPH proto-oncogene and the CD39L4 (ENTPD5) ectonucleoside triphosphate diphosphohydrolase gene Int J Oncol 19 2001 1249 1254
35. G. Paxinos, C. Watson The rat brain in stereotaxic coordinates 1998 Academic Press San Diego
36. C. Peyron, D.K. Tighe, A.N. van den Pol, L. de Lecea, H.C. Heller, J.G. Sutcliffe, T.S. Kilduff Neurons containing hypocretin (orexin) project to multiple neuronal systems J Neurosci 18 1998 9996 10015
37. D.J. Pinsky, M.J. Broekman, J.J. Peschon, K.L. Stocking, T. Fujita, R. Ramasamy, E.S. Connolly Jr, J. Huang, S. Kiss, Y. Zhang, T.F. Choudhri, R.A. McTaggart, H. Liao, J.H. Drosopoulos, V.L. Price, A.J. Marcus, C.R. Maliszewski Elucidation of the thromboregulatory role of CD39/ectoapyrase in the ischemic brain J Clin Invest 109 2002 1031 1040
38. B. Rucker, D. Pochmann, C.R. Furstenau, M.S. Carneiro-Ramos, A.M. Battastini, M.L. Barreto-Chaves, J.J. Sarkis Effects of steroid hormones on synaptosomal ectonucleotidase activities from hippocampus and cortex of adult female rats Gen Comp Endocrinol 140 2005 94 100
39. K. Sakai, S. Crochet Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake-sleep states Neuroscience 104 2001 1141 1155
40. J.D. Shi, T. Kukar, C.Y. Wang, Q.Z. Li, P.E. Cruz, A. Davoodi-Semiromi, P. Yang, Y. Gu, W. Lian, D.H. Wu, J.X. She Molecular cloning and characterization of a novel mammalian endo-apyrase (LALP1) J Biol Chem 276 2001 17474 17478
41. T.M. Smith, T.L. Kirley Cloning, sequencing, and expression of a human brain ecto-apyrase related to both the ecto-ATPases and CD39 ecto-apyrases Biochim Biophys Acta 1386 1998 65 78
42. T.M. Smith, T.L. Kirley Glycosylation is essential for functional expression of a human brain ecto-apyrase Biochemistry 38 1999 1509 1516
43. T.M. Smith, T.L. Kirley Site-directed mutagenesis of a human brain ecto-apyrase evidence that the E-type ATPases are related to the actin/heat shock 70/sugar kinase superfamily Biochemistry 38 1999 321 328
44. T.M. Smith, S.A. Lewis Carl, T.L. Kirley Mutagenesis of two conserved tryptophan residues of the E-type ATPases Inactivation and conversion of an ecto-apyrase to an ecto-NTPase Biochemistry 38 1999 5849 5857
45. J.G. Sutcliffe, L. de Lecea The hypocretins excitatory neuromodulatory peptides for multiple homeostatic systems, including sleep and feeding J Neurosci Res 62 2000 161 168
46. A.L. Tarentino, C.M. Gomez, T.H.J. Plummer Deglycosylation of asparagine-linked glycans by peptide -glycosidase F Biochemistry 24 1985 4665 4671
47. M.J. Treuheit, P.L. Vaghy, T.L. Kirley The Mg2+-ATPase of rabbit skeletal muscle transverse tubules is a 67 kDa glycoprotein J Biol Chem 267 1992 11777 11782
48. S. Vlajkovic, P. Thorne, J. Sevigny, S. Robson, G. Housley Distribution of ectonucleoside triphosphate diphosphohydrolases 1 and 2 in rat cochlea Hear Res 170 2002 127
49. S.M. Vlajkovic, P.R. Thorne, J. Sevigny, S.C. Robson, G.D. Housley NTPDase1 and NTPDase2 immunolocalization in mouse cochlea implications for regulation of p2 receptor signaling J Histochem Cytochem 50 2002 1435 1442
50. M. Wakamori, M. Sorimachi Properties of native P2X receptors in large multipolar neurons dissociated from rat hypothalamic arcuate nucleus Brain Res 1005 2004 51 59
51. T.-F. Wang, G. Guidotti Golgi localization and functional expression of human uridine diphosphatase J Biol Chem 273 1998 11392 11399
52. T.-F. Wang, G. Guidotti Widespread expression of ecto-apyrase (CD39) in the central nervous system Brain Res 790 1998 318 322
53. Z. Xiang, X. Bo, I. Oglesby, A. Ford, G. Burnstock Localization of ATP-gated P2X2 receptor immunoreactivity in the rat hypothalamus Brain Res 813 1998 390 397
54. G. Yeung, J.J. Mulero, D.W. McGowan, S.S. Bajwa, J.E. Ford CD39L2, a gene encoding a human nucleoside diphosphatase, predominantly expressed in the heart Biochemistry 39 2000 12916 12923
55. H. Zimmermann, A.R. Beaudoin, M. Bollen, J.W. Goding, G. Guidotti, T.L. Kirley, S.C. Robson, K. Sano Proposed nomenclature for two novel nucleotide hydrolyzing enzyme families expressed on the cell surface L. Vanduffel Ecto-ATPases and related ectonucleotidases. Proceedings of the Second International Workshop on Ecto-ATPases and Related Ectonucleotidases, Diepenbeek, Belgium 1999 Shaker Publishing BV Maastricht, The Netherlands 1 9
56. A. Zsarnovszky, S.M. Belcher Identification of a developmental gradient of estrogen receptor expression and cellular localization in the developing and adult female rat primary somatosensory cortex Brain Res Dev Brain Res 129 2001 39 46