Tanycyte pyroglutamyl peptidase II contributes to regulation of the hypothalamic-pituitary-thyroid axis through glial-axonal associations in the median eminence

Endocrinology

Volumn 150, Issue 5, 2009, Pages 2283-2291

  Sanchez, Edith ^a   Vargas, Miguel Angel ^b   Singru, Praful S ^a   Pascual, Isel ^c   Romero, Fidelia ^b   Fekete, Csaba ^a,d   Charli, Jean Louis ^b   Lechan, Ronald M ^a,e  

^a TUFTS MEDICAL CENTER   (United States)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UNIVERSITY OF HAVANA   (Cuba)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 OXOPROLYL PEPTIDASE; PROTIRELIN; AMINOPEPTIDASE; DRUG DERIVATIVE; MESSENGER RNA; PRO THYROTROPIN RELEASING HORMONE; PRO-THYROTROPIN RELEASING HORMONE; PROTEIN PRECURSOR; PYROGLUTAMIC ACID; PYROGLUTAMYL PEPTIDASE II; PYROGLUTAMYL-PEPTIDASE II; THYROTROPIN; THYROXINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; HORMONE RELEASE; HYPOPHYSIS THYROID SYSTEM; IN SITU HYBRIDIZATION; MALE; MEDIAN EMINENCE; NONHUMAN; PRIORITY JOURNAL; RAT; TANYCYTE; THYROTROPIN BLOOD LEVEL; ANIMAL; BIOLOGICAL MODEL; BLOOD; CELL COMMUNICATION; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLIA; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INNERVATION; METABOLISM; NERVE FIBER; PHYSIOLOGY; SPRAGUE DAWLEY RAT; THYROID GLAND; TISSUE DISTRIBUTION;

AMINOPEPTIDASES; ANIMALS; AXONS; CELL COMMUNICATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MEDIAN EMINENCE; MODELS, BIOLOGICAL; NEUROGLIA; PROTEIN PRECURSORS; PYRROLIDONECARBOXYLIC ACID; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; THYROID GLAND; THYROTROPIN; THYROTROPIN-RELEASING HORMONE; THYROXINE; TISSUE DISTRIBUTION;

EID: 66449101268     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1643     Document Type: Article

References (56)

1. Charli JL, Vargas MA, CisnerosM, de Gortari P, BaezaMA, Jasso P, Bourdais J, Perez L, Uribe RM, Joseph-Bravo P 1998 TRH inactivation in the extracellular compartment: role of pyroglutamyl peptidase II. Neurobiology 6:45-57
2. Vargas M, Mendez M, Cisneros M, Joseph-Bravo P, Charli JL 1987 Regional distribution of the membrane-bound pyroglutamate amino peptidase-degrad- ing thyrotropin-releasing hormone in rat brain. Neurosci Lett 79:311-314
3. Heuer H, Schafer MK, O'Donnell D, Walker P, Bauer K 2000 Expression of thyrotropin-releasing hormone receptor 2 (TRH-R2) in the central nervous system of rats. J Comp Neurol 428:319-336
4. Schmitmeier S, Thole H, Bader A, Bauer K 2002 Purification and characterization of the thyrotropin-releasing hormone (TRH)-degrading serum enzyme and its identification as a product of liver origin. Eur JBiochem 269:1278-1286
5. Grosvenor CE, MenaF 1980 Evidence that thyrotropin-releasing hormone and a hypothalamic prolactin-releasing factor may function in the release of pro- lactin in the lactating rat. Endocrinology 107:863-868
6. Haisenleder DJ, Ortolano GA, Dalkin AC, Yasin M, Marshall JC 1992 Differential actions of thyrotropin (TSH)-releasing hormone pulses in the expression of prolactin and TSH subunit messenger ribonucleic acid in rat pituitary cells in vitro. Endocrinology 130:2917-2923
7. Lechan RM, Fekete C 2006 The TRH neuron: a hypothalamic integrator of energy metabolism. Prog Brain Res 153:209-235
8. Segerson TP, Kauer J, Wolfe HC, Mobtaker H, Wu P, Jackson IM, Lechan RM 1987 Thyroid hormone regulates TRH biosynthesis in the paraventricular nucleus of the rat hypothalamus. Science 238:78 -80
9. Rondeel JM, de Greef WJ, Klootwijk W, Visser TJ 1992 Effects of hypothy- roidism on hypothalamic release of thyrotropin-releasing hormone in rats. Endocrinology 130:651-656
10. Dahl GE, Evans NP, Thrun LA, Karsch FJ 1994 A central negative feedback action of thyroid hormones on thyrotropin-releasing hormone secretion. Endocrinology 135:2392-2397
11. Schomburg L, Bauer K 1995 Thyroid hormones rapidly and stringently regulate the messenger RNA levels of the thyrotropin-releasing hormone (TRH) receptorandtheTRH-degradingectoenzyme. Endocrinology136:3480-3485
12. Blake NG, Johnson MR, Eckland DJ, Foster OJ, Lightman SL 1992 Effect of food deprivation and altered thyroid status on the hypothalamic-pituitary- thyroid axis in the rat. JEndocrinol 133:183-188
13. Ponce G, Charli JL, Pasten JA, Aceves C, Joseph-Bravo P 1988 Tissue-specific regulation of pyroglutamate aminopeptidase II activity by thyroid hormones. Neuroendocrinology 48:211-213
14. Heuer H, Ehrchen J, Bauer K, Schafer MK 1998 Region-specific expression of thyrotrophin-releasing hormone-degrading ectoenzyme in the rat central nervous system and pituitary gland. Eur J Neurosci 10:1465-1478
15. Lechan RM, Qi Y, Berrodin TJ, Davis KD, Schwartz HL, Strait KA, Oppenheimer JH, Lazar MA 1993 Immunocytochemical delineation of thyroid hormone receptor /32-like immunoreactivity in the rat central nervous system. Endocrinology 132:2461-2469
16. Heuer H, Maier MK, Iden S, Mittag J, Friesema EC, Visser TJ, Bauer K 2005 Themonocarboxylatetransporter8linkedtohumanpsychomotorretardation is highly expressed in thyroid hormone-sensitive neuron populations. Endocrinology146:1701-1706
17. Nakao N, Takagi T, Iigo M, Tsukamoto T, Yasuo S, Masuda T, Yanagisawa T, Ebihara S, Yoshimura T 2006 Possible involvement of organic anion transporting polypeptide 1c1 in the photoperiodic response of gonads in birds. Endocrinology 147:1067-1073
18. Tu HM, Kim SW, Salvatore D, Bartha T, Legradi G, Larsen PR, Lechan RM 1997 Regional distribution of type 2 thyroxine deiodinase messenger ribonu- cleic acid in rat hypothalamus and pituitary and its regulation by thyroid hormone. Endocrinology 138:3359-3368
19. Guadafio-Ferraz A, Escaimez MJ, Rausell E, Bernal J 1999 Expression of type 2 iodothyronine deiodinase in hypothyroid rat brain indicates an important role of thyroid hormone in the development of specific primary sensory systems. J Neurosci 19:3430 -3439
20. Fekete C, Freitas BC, Zeold A, Wittmann G, Kadar A, Liposits Z, Christoffolete MA, Singru P, Lechan RM, Bianco AC, Gereben B 2007 Expression patterns of WSB-1 and USP-33 underlie cell-specific posttranslational control of type 2 deio- dinase in the rat brain. Endocrinology 148:4865-4874
21. de Gortari P, Romero F, Cisneros M, Joseph-Bravo P 2005 Acute administration of alcohol modulates pyroglutamyl amino peptidase II activity and mRNA levels in rat limbic regions. Neurochem Int 46:347-356
22. Sanchez E, Singru PS, Fekete C, Lechan RM 2008 Induction of type 2 iodo- thyronine deiodinase in the mediobasal hypothalamus by bacterial lipopoly- saccharide: role of corticosterone. Endocrinology 149:2484-2493
23. Paxinos G, Watson C 1986 The rat brain in stereotaxic coordinates. 2nd ed. New York: Academic Press
24. Lechan RM, Segerson TP 1989 Pro-TRH gene expression and precursor pep- tides in rat brain. Observations by hybridization analysis and immunocyto- chemistry. Ann NY Acad Sci 553:29-59
25. Osborn M, Debus E, Weber K 1984 Monoclonal antibodies specific for vimentin. Eur JCell Biol 34:137-143
26. Vargas MA, Cisneros M, Joseph-Bravo P, Charli JL 2000 Regulation of ad- enohypophyseal pyroglutamyl aminopeptidase II activity by thyrotropin-re- leasing hormone and phorbol esters. Endocrine 13:267-272
27. Bauer K, Nowak P 1979 Characterization of a thyroliberin-degrading serum enzyme catalyzing the hydrolysis of thyroliberin at the pyroglutamyl-histidine bond. Eur J Biochem 99:239-246
28. Pascual I, Gil-Parrado S, Cisneros M, Joseph-Bravo P, Diaz J, Possani LD, Charli JL, Chavez M 2004 Purification of a specific inhibitor of pyroglutamyl aminopeptidase II from the marine annelide Hermodice carunculata: in vivo effects in rodent brain. Int JBiochem Cell Biol 36:138-152
29. Arancibia S, Tapia-Arancibia L, Astier H, Assenmacher I 1989 Physiological evidence for a1-adrenergic facilitatory control of the cold-induced TRH release in the rat, obtained by push-pull cannulation of the median eminence. Neurosci Lett 100:169-174
30. Charli JL, Mendez M, Joseph-Bravo P, Wilk S 1987 Specific inhibitors of pyroglutamyl peptidase I and prolyl endopeptidase do not change the in vitro release of TRH or its content in rodent brain. Neuropeptides 9:373-378
31. CharliJL, MendezM, VargasMA, CisnerosM, AssaiM, Joseph-BravoP, Wilk S 1989 Pyroglutamyl peptidase II inhibition specifically increases recovery of TRH released from rat brain slices. Neuropeptides 14:191-196
32. Joseph-Bravo P, Charli JL, Palacios JM, Kordon C 1979 Effect of neurotrans- mitters on the in vitro release of immunoreactive thyrotropin-releasing hormone from rat mediobasal hypothalamus. Endocrinology 104:801-806
33. Koller KJ, Wolff RS, Warden MK, Zoeller RT 1987 Thyroid hormones regulate levels of thyrotropin-releasing-hormone mRNA in the paraventricular nucleus. Proc Natl Acad Sci USA 84:7329-7333
34. Perello M, Friedman T, Paez-Espinosa V, Shen X, Stuart RC, Nillni EA 2006 Thyroidhormonesselectivelyregulatetheposttranslationalprocessingofpro- thyrotropin-releasing hormone in the paraventricular nucleus of the hypothal- amus. Endocrinology 147:2705-2716
35. Barrett P, Ebling FJ, Schuhler S, Wilson D, Ross AW, Warner A, Jethwa P, Boelen A, Visser TJ, Ozanne DM, Archer ZA, Mercer JG, Morgan PJ 2007 Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 148:3608 -3617
36. BauerK, CarmelietP, SchulzM, BaesM, DenefC1990 Regulationandcellular localization of the membrane-bound thyrotropin-releasing hormone-degrad- ingenzymeinprimaryculturesofneuronal, glial, andadenohypophysealcells. Endocrinology 127:1224-1233
37. CruzR, Vargas MA, UribeRM, PascualI, LazcanoI, Yiotakis A, MatziariM, Joseph-Bravo P, Charli JL 2008 Anterior pituitary pyroglutamyl peptidase II activity controls TRH-induced prolactin release. Peptides 29:1953-1964
38. CruzC, CharliJL, VargasMA, Joseph-BravoP1991 Neuronallocalizationof pyroglutamate aminopeptidase II in primary cultures of fetal mouse brain. JNeurochem 56:1594-1601
39. KamedaY, AraiY, NishimakiT2003 Ultrastructurallocalizationofvimentin immunoreactivity and gene expression in tanycytes and their alterations in hamsters kept under different photoperiods. Cell Tissue Res 314:251-262
40. Lin J, Wilk S 1998 Quantitation and regulation of pyroglutamyl peptidase II messenger RNA levels in rat tissues and GH3 cells. Neuroendocrinology 67: 197-208
41. CruzR, Chavez-GutierrezL, Joseph-Bravo P, CharliJL2004 3, 3', 5'-Triiodo- L-thyronine reduces efficiency of mRNA knockdown by antisense oligode- oxynucleotides: a study with pyroglutamyl aminopeptidase II in adenohy- pophysis. Oligonucleotides 14:176-190
42. Emerson CH, Wu CF 1987 Thyroid status influences rat serum but not brain TRHpyroglutamylaminopeptidaseactivities.Endocrinology120:1215-1217
43. Kakucska I, Rand W, Lechan RM 1992 Thyrotropin-releasing hormone gene expression in the hypothalamic paraventricular nucleus is dependent upon feedback regulation by both triiodothyronine and thyroxine. Endocrinology 130:2845-2850
44. Bauer K 1976 Regulation of degradation of thyrotropin releasing hormone by thyroid hormones. Nature 259:591-593
45. SuenCS, WilkS1989 Regulationofthyrotropinreleasinghormonedegrading enzymes in rat brain and pituitary by L-3, 5, 3 '-triiodothyronine. J Neurochem 52:884-888
46. Akmayev IG, Popov AP 1977 Morphological aspects of the hypothalamic- hypophyseal system. VII. The tanycytes: their relation to the hypophyseal adrenocorticotrophic function. An ultrastructural study. Cell Tissue Res 180: 263-282
47. Rodriguez EM, Gonzalez CB, Delannoy L 1979 Cellular organization of the lateral and postinfundibular regions of the median eminence in the rat. Cell Tissue Res 201:377-408
48. Peruzzo B, Pastor FE, Blazquez JL, Schobitz K, Pelaez B, Amat P, Rodriguez EM2000 Asecondlook atthebarriersofthemedialbasalhypothalamus. Exp Brain Res 132:10-26
49. Flament-Durand J, Brion JP 1985 Tanycytes: morphology and functions. A review. Int Rev Cytol 96:121-155
50. Schauder B, Schomburg L, Kohrle J, Bauer K 1994 Cloning of a cDNA en- codinganectoenzymethatdegradesthyrotropin-releasinghormone. ProcNatl Acad Sci USA 91:9534-9538
51. Schomburg L, Turwitt S, Prescher G, Lohmann D, Horsthemke B, Bauer K 1999 Human TRH-degrading ectoenzyme cDNA cloning, functional expression, genomic structure and chromosomal assignment. Eur J Biochem 265: 415-422
52. Chavez-Gutierrez L, Bourdais J, Aranda G, Vargas MA, Matta-Camacho E, Ducancel F, Segovia L, Joseph-Bravo P, Charli JL 2005 A truncated isoform ofpyroglutamylaminopeptidaseIIproducedbyexonextensionhasdominant- negative activity. J Neurochem 92:807-817
53. WuTJ, Pierotti AR, Jakubowski M, Sheward WJ, GlucksmanMJ, SmithAI, King JC, Fink G, Roberts JL 1997 Endopeptidase EC 3.4.24.15 presence in the rat median eminence and hypophysial portal blood and its modulation of the luteinizing hormone surge. J Neuroendocrinol 9:813-822
54. Vandenbulcke F, Ciofi P, Beauvillain JC 1994 Detection of neutral endopep- tidase (NEP, enkephalinase, E.C. 3.4.24.11) in relation to dopaminergic and gonadoliberinergic nerve endings in the median eminence of the male rat: a double labeling ultrastructural study. J Neuroendocrinol 6:655-664
55. Vandenbulcke F, Ciofi P, Beauvillain JC 1994 Concomitant variation in im- munoreactivity for enkephalins and neutral endopeptidase in the median eminence of the lactating rat. Neurosci Lett 175:53-57
56. Charli JL, Pascual I, Cruz R, Vargas MA 2006 Post-secretory inactivation of peptides in the hypothalamic-adenohypophyseal axis. Focus on pyro- glutamyl peptidase II, the thyrotropin releasing hormone inactivating ec- toenzyme. In: Joseph-Bravo P, ed. Molecular endocrinology. Kerala, India: Research Signpost