Tuberoinfundibular peptide of 39 residues modulates the mouse hypothalamic-pituitary-adrenal axis via paraventricular glutamatergic neurons

Journal of Comparative Neurology

Volumn 518, Issue 21, 2010, Pages 4375-4394

  Dimitrov, Eugene ^a   Usdin, Ted Björn ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Neuroendocrine; Neuropeptide; Parathyroid hormone 2 receptor; Paraventricular nucleus; Presynaptic facilitation; Stress

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; CORTICOSTERONE; FLUOROGOLD; MESSENGER RNA; NEUROPEPTIDE; PARATHYROID HORMONE RECEPTOR 2; PROLACTIN; TUBEROINFUNDIBULAR PEPTIDE OF 39; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL LABELING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; FLUORESCENCE IN SITU HYBRIDIZATION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROLACTIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION;

ANIMALS; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; GLUTAMIC ACID; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; NEUROPEPTIDES; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY-ADRENAL SYSTEM; RECEPTOR, PARATHYROID HORMONE, TYPE 2; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 77957798256     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22462     Document Type: Article

References (79)

1. Alon T, Zhou L, Perez CA, Garfield AS, Friedman JM, Heisler LK. 2009. Transgenic mice expressing green fluorescent protein under the control of the corticotropin-releasing hormone promoter. Endocrinology 150:5626-5632.
2. Ben-Barak Y, Russell JT, Whitnall M, Ozato K, Gainer H. 1984. Phylogenetic cross-reactivities of monoclonal antibodies produced against rat neurophysin. Cell Mol Neurobiol 4:339-349.
3. Bjorklund A, Nobin A. 1973. Fluorescence histochemical and microspectrofluorometric mapping of dopamine and nor-adrenaline cell groups in the rat diencephalon. Brain Res 51:193-205.
4. Boudaba C, Szabo K, Tasker JG. 1996. Physiological mapping of local inhibitory inputs to the hypothalamic paraventricular nucleus. J Neurosci 16:7151-7160.
5. Bregonzio C, Navarro CE, Donoso AO. 1998. NMDA receptor antagonists block stress-induced prolactin release in female rats at estrus. Eur J Pharmacol 350:259-265.
6. Brown EM, Segre GV, Goldring SR. 1996. Serpentine receptors for parathyroid hormone, calcitonin and extracellular calcium ions. Baillieres Clin Endocrinol Metab 10:123-161.
7. Burstein R, Cliffer KD, Giesler GJ Jr. 1990. Cells of origin of the spinohypothalamic tract in the rat. J Comp Neurol 291:329-344.
8. Chagnaud JL, Campistron G, Geffard M. 1989. Monoclonal antibody directed against glutaraldehyde conjugated glutamate and immunocytochemical applications in the rat brain. Brain Res 481:175-180.
9. Charmandari E, Tsigos C, Chrousos G. 2005. Endocrinology of the stress response. Annu Rev Physiol 67:259-284.
10. Christian HC, Chapman LP, Morris JF. 2007. Thyrotrophin-releasing hormone, vasoactive intestinal peptide, prolactin releasing peptide and dopamine regulation of prolactin secretion by different lactotroph morphological subtypes in the rat. J Neuroendocrinol 19:605-613.
11. Cole RL, Sawchenko PE. 2002. Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 22:959-969.
12. 3H]D-aspartate autoradiography. Neuroscience 101:637-655.
13. Daftary SS, Boudaba C, Szabo K, Tasker JG. 1998. Noradrenergic excitation of magnocellular neurons in the rat hypothalamic paraventricular nucleus via intranuclear glutamatergic circuits. J Neurosci 18:10619-10628.
14. Dobolyi A, Palkovits M, Bodnar I, Usdin TB. 2003a. Neurons containing tuberoinfundibular peptide of 39 residues project to limbic, endocrine, auditory and spinal areas in rat. Neuroscience 122:1093-1105.
15. Dobolyi A, Palkovits M, Usdin TB. 2003b. Expression and distribution of tuberoinfundibular peptide of 39 residues in the rat central nervous system. J Comp Neurol 455:547-566.
16. Dobolyi A, Irwin S, Wang J, Usdin TB. 2006. The distribution and neurochemistry of the parathyroid hormone 2 receptor in the rat hypothalamus. Neurochem Res 31:227-236.
17. Faber CA, Dobolyi A, Sleeman M, Usdin TB. 2007. Distribution of tuberoinfundibular peptide of 39 residues and its receptor, parathyroid hormone 2 receptor, in the mouse brain. J Comp Neurol 502:563-583.
18. Fegley DB, Holmes A, Riordan T, Faber CA, Weiss JR, Ma S, Batkai S, Pacher P, Dobolyi A, Murphy A, Sleeman MW, Usdin TB. 2008. Increased fear- and stress-related anxiety- like behavior in mice lacking tuberoinfundibular peptide of 39 residues. Genes Brain Behav 7:933-942.
19. Ferguson AV, Latchford KJ, Samson WK. 2008. The paraventricular nucleus of the hypothalamus-a potential target for integrative treatment of autonomic dysfunction. Expert Opin Ther Targets 12:717-727.
20. Fjeldheim AK, Hovring PI, Loseth OP, Johansen PW, Glover JC, Matre V, Olstad OK, Reppe S, Gordeladze JO, Walaas SI, Gautvik KM. 2005. Thyrotrophin-releasing hormone receptor 1 and prothyrotrophin-releasing hormone mRNA expression in the central nervous system are regulated by suckling in lactating rats. Eur J Endocrinol 152:791-803.
21. Franklin KBJ, Paxinos G, editors. 2008. The mouse brain in stereotaxic coordinates, 3rd ed. New York: Academic Press.
22. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH. 2001. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
23. Goldstein J, Perello M, Nillni EA. 2007. Preprothyrotropin-releasing hormone 178-199 affects tyrosine hydroxylase biosynthesis in hypothalamic neurons: a possible role for pituitary prolactin regulation. J Mol Neurosci 31:69-82.
24. Herman JP, Prewitt CM, Cullinan WE. 1996. Neuronal circuit regulation of the hypothalamo-pituitary-adrenocortical stress axis. Crit Rev Neurobiol 10:371-394.
25. Herman JP, Tasker JG, Ziegler DR, Cullinan WE. 2002. Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol Biochem Behav 71:457-468.
26. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE. 2003. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151-180.
27. Hopman AH, Ramaekers FC, Speel EJ. 1998. Rapid synthesis of biotin-, digoxigenin-, trinitrophenyl-, and fluorochrome-labeled tyramides and their application for In situ hybridization using CARD amplification. J Histochem Cytochem 46:771-777.
28. Hsu DT, Price JL. 2009. Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 512:825-848.
29. Justice NJ, Yuan ZF, Sawchenko PE, Vale W. 2008. Type 1 corticotropin-releasing factor receptor expression reported in BAC transgenic mice: implications for reconciling ligand-receptor mismatch in the central corticotropin-releasing factor system. J Comp Neurol 511:479-496.
30. Kapoor R, Chapman IM, Willoughby JO. 1993. Alpha 2 and beta adrenoceptors in the mediobasal hypothalamus and alpha 2 adrenoceptors in the preoptic-anterior hypothalamus stimulate prolactin secretion in the conscious male rat. J Neuroendocrinol 5:189-193.
31. Kawaguchi Y, Shindou T. 1998. Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. J Neurosci 18:6963-6976.
32. Kawano H, Daikoku S. 1987. Functional topography of the rat hypothalamic dopamine neuron systems: retrograde tracing and immunohistochemical study. J Comp Neurol 265:242-253.
33. Kiss JZ, Palkovits M, Zaborszky L, Tribollet E, Szabo D, Makara GB. 1983. Quantitative histological studies on the hypothalamic paraventricular nucleus in rats. II. Number of local and certain afferent nerve terminals. Brain Res 265: 11-20.
34. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf KR, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168-176.
35. Lin W, McKinney K, Liu L, Lakhlani S, Jennes L. 2003. Distribution of vesicular glutamate transporter-2 messenger ribonucleic Acid and protein in the septum-hypothalamus of the rat. Endocrinology 144:662-670.
36. Liposits Z. 1993. Ultrastructure of hypothalamic paraventricular neurons. Crit Rev Neurobiol 7:89-162.
37. Liu P, Jenkins NA, Copeland NG. 2003. A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13:476-484.
38. Meites J. 1977. Neuroendocrine control of prolactin in experimental animals. Clin Endocrinol 6(Suppl):9S-18S.
39. Merchenthaler I, Lennard DE. 1991. The hypophysiotropic neurotensin-immunoreactive neuronal system of the rat brain. Endocrinology 129:2875-2880.
40. Mezey E, Kiss JZ. 1985. Vasoactive intestinal peptide-containing neurons in the paraventricular nucleus may participate in regulating prolactin secretion. Proc Natl Acad Sci USA 82:245-247.
41. Moga MM, Weis RP, Moore RY. 1995. Efferent projections of the paraventricular thalamic nucleus in the rat. J Comp Neurol 359:221-238.
42. Myers RD. 1966. Injection of solutions into cerebral tissue: relation between volume and diffusion. Physiology and Behavior 1:171-174.
43. Nagy GM, Bodnar I, Banky Z, Halasz B. 2005. Control of prolactin secretion by excitatory amino acids. Endocrine 28: 303-308.
44. Nillni EA, Sevarino KA, Jackson IM. 1993. Identification of the thyrotropin-releasing hormone-prohormone and its post-translational processing in a transfected AtT20 tumoral cell line. Endocrinology 132:1260-1270.
45. O'Gorman S, Dagenais NA, Qian M, Marchuk Y. 1997. Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc Natl Acad Sci USA 94: 14602-14607.
46. Palkovits M, Baffi JS, Pacak K. 1999. The role of ascending neuronal pathways in stress-induced release of noradrenaline in the hypothalamic paraventricular nucleus of rats. J Neuroendocrinol 11:529-539.
47. Pohl CR, Lee LR, Smith MS. 1989. Qualitative changes in luteinizing hormone and prolactin responses to N-methylaspartic acid during lactation in the rat. Endocrinology 124:1905-1911.
48. Rasband WS. 1997-2009. Image J. Bethesda, MD: U.S. National Institutes of Health.
49. Rittenhouse PA, Levy AD, Li Q, Bethea CL, Van de Kar LD. 1993. Neurons in the hypothalamic paraventricular nucleus mediate the serotonergic stimulation of prolactin secretion via 5-HT1c/2 receptors. Endocrinology 133:661-667.
50. Roland BL, Sawchenko PE. 1993. Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol 332:123-143.
51. Sawchenko PE. 1987a. Adrenalectomy-induced enhancement of CRF and vasopressin immunoreactivity in parvocellular neurosecretory neurons: anatomic, peptide, and steroid specificity. J Neurosci 7:1093-1106.
52. Sawchenko PE. 1987b. Evidence for differential regulation of corticotropin-releasing factor and vasopressin immunoreactivities in parvocellular neurosecretory and autonomic-related projections of the paraventricular nucleus. Brain Res 437:253-263.
53. Sawchenko PE, Swanson LW. 1982. The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat. Brain Res 257:275-325.
54. Sawchenko PE, Swanson LW. 1985. Localization, colocalization, and plasticity of corticotropin-releasing factor immunoreactivity in rat brain. Fed Proc 44:221-227.
55. Sawchenko PE, Swanson LW, Grzanna R, Howe PR, Bloom SR, Polak JM. 1985. Colocalization of neuropeptide Y immuno-reactivity in brainstem catecholaminergic neurons that project to the paraventricular nucleus of the hypothalamus. J Comp Neurol 241:138-153.
56. Semenenko FM, Cuello AC, Goldstein M, Lee KY, Sidebottom E. 1986. A monoclonal antibody against tyrosine hydroxylase: application in light and electron microscopy. J Histochem Cytochem 34:817-821.
57. Smith DW, Day TA. 1994. c-fos Expression in hypothalamic neurosecretory and brainstem catecholamine cells following noxious somatic stimuli. Neuroscience 58:765-775.
58. Sugimura Y, Murase T, Ishizaki S, Tachikawa K, Arima H, Miura Y, Usdin TB, Oiso Y. 2003. Centrally administered tuberoinfundibular peptide of 39 residues inhibits arginine vasopressin release in conscious rats. Endocrinology 144: 2791-2796.
59. Swanson LW, Sawchenko PE. 1983. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6:269-324.
60. Toth ZE, Mezey E. 2007. Simultaneous visualization of multiple antigens with tyramide signal amplification using antibodies from the same species. J Histochem Cytochem 55: 545-554.
61. Usdin TB. 2000. The PTH2 receptor and TIP39: a new peptide-receptor system. Trends Pharmacol Sci 21:128-130.
62. Usdin TB, Hoare SR, Wang T, Mezey E, Kowalak JA. 1999. TIP39: a new neuropeptide and PTH2-receptor agonist from hypothalamus. Nat Neurosci 2:941-943.
63. Usdin TB, Paciga M, Riordan T, Kuo J, Parmelee A, Petukova G, Camerini-Otero RD, Mezey E. 2008. Tuberoinfundibular peptide of 39 residues is required for germ cell development. Endocrinology 149:4292-4300.
64. Vale W, Vaughan J, Yamamoto G, Bruhn T, Douglas C, Dalton D, Rivier C, Rivier J. 1983. Assay of corticotropin releasing factor. Methods Enzymol 103:565-577.
65. Van de Kar LD, Blair ML. 1999. Forebrain pathways mediating stress-induced hormone secretion. Front Neuroendocrinol 20:1-48.
66. van den Pol AN, Trombley PQ. 1993. Glutamate neurons in hypothalamus regulate excitatory transmission. J Neurosci 13:2829-2836.
67. van den Pol AN, Wuarin JP, Dudek FE. 1990. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 250:1276-1278.
68. Van der Krans A. 1983. Labeling of neurons following intravenous injections of fluorescent tracers in mice. J Neurosci Methods 9:95-103.
69. +/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22:142-155.
70. Wang J, Palkovits M, Usdin TB, Dobolyi A. 2006a. Afferent connections of the subparafascicular area in rat. Neuroscience 138:197-220.
71. Wang J, Palkovits M, Usdin TB, Dobolyi A. 2006b. Forebrain projections of tuberoinfundibular peptide of 39 residues (TIP39)-containing subparafascicular neurons. Neuroscience 138:1245-1263.
72. Wang T, Palkovits M, Rusnak M, Mezey E, Usdin TB. 2000. Distribution of parathyroid hormone-2 receptor-like immunoreactivity and messenger RNA in the rat nervous system. Neuroscience 100:629-649.
73. Ward HL, Small CJ, Murphy KG, Kennedy AR, Ghatei MA, Bloom SR. 2001. The actions of tuberoinfundibular peptide on the hypothalamo-pituitary axes. Endocrinology 142: 3451-3456.
74. Wittmann G, Lechan RM, Liposits Z, Fekete C. 2005. Glutamatergic innervation of corticotropin-releasing hormone- and thyrotropin-releasing hormone-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. Brain Res 1039:53-62.
75. Wu P, Jackson IM. 1988. Post-translational processing of thyrotropin-releasing hormone precursor in rat brain: identification of 3 novel peptides derived from proTRH. Brain Res 456:22-28.
76. Xu X, Roby KD, Callaway EM. 2006. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499:144-160.
77. Zhang BJ, Kusano K, Zerfas P, Iacangelo A, Young WS 3rd, Gainer H. 2002. Targeting of green fluorescent protein to secretory granules in oxytocin magnocellular neurons and its secretion from neurohypophysial nerve terminals in transgenic mice. Endocrinology 143:1036-1046.
78. Ziegler DR, Herman JP. 2000. Local integration of glutamate signaling in the hypothalamic paraventricular region: regulation of glucocorticoid stress responses. Endocrinology 141:4801-4804.
79. Ziegler DR, Cullinan WE, Herman JP. 2002. Distribution of vesicular glutamate transporter mRNA in rat hypothalamus. J Comp Neurol 448:217-229.