A secretagogin locus of the mammalian hypothalamus controls stress hormone release

EMBO Journal

Volumn 34, Issue 1, 2015, Pages 36-54

  Romanov, Roman A ^a   Alpár, Alán ^a,d   Zhang, Ming Dong ^a   Zeisel, Amit ^a   Calas, André ^b   Landry, Marc ^b   Fuszard, Matthew ^c   Shirran, Sally L ^c   Schnell, Robert ^a   Dobolyi, Árpád ^d   Oláh, Márk ^d   Spence, Lauren ^e   Mulder, Jan ^a,f   Martens, Henrik ^g   Palkovits, Miklõs ^d   Uhlen, Mathias ^f   Sitte, Harald H ^h   Botting, Catherine H ^c   Wagner, Ludwig ^h   Linnarsson, Sten ^a   Hökfelt, Tomas ^a   Harkany, Tibor ^a,i   more..

^a KAROLINSKA INSTITUTE   (Sweden)

^b University of Bordeaux   (France)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

^d SEMMELWEIS UNIVERSITY   (Hungary)

^e UNIVERSITY OF ABERDEEN   (United Kingdom)

^f SCIENCE FOR LIFE LABORATORY   (Sweden)

^g SYNAPTIC SYSTEMS GMBH   (Germany)

^h MEDICAL UNIVERSITY OF VIENNA   (Austria)

ⁱ Medical University of Vienna   (Austria)

Author keywords

acute stress; Ca2+ sensor; HPA axis; vesicular release

Indexed keywords

CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; NEURONAL CALCIUM SENSOR; SECRETAGOGIN; STRESS HORMONE; TRANSCRIPTOME; SCGN PROTEIN, MOUSE;

ACUTE STRESS; ADULT; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL POPULATION; CELL VACUOLE; CONTROLLED STUDY; EXOCYTOSIS; HORMONE RELEASE; HUMAN; HUMAN CELL; HYPOPHYSIS; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IN VITRO STUDY; IN VIVO STUDY; MEDIAN EMINENCE; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; RNA ANALYSIS; RNA INTERFERENCE; ANIMAL; CYTOLOGY; GENETICS; MALE; NERVE CELL; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SECRETION (PROCESS);

MAMMALIA;

ANIMALS; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; MALE; MICE; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; PITUITARY GLAND; RNA INTERFERENCE; SECRETAGOGINS; STRESS, PHYSIOLOGICAL; TRANSCRIPTOME;

EID: 84920440440     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488977     Document Type: Article

References (110)

1. Aguilera G, Kiss A, Liu Y, Kamitakahara A, (2007) Negative regulation of corticotropin releasing factor expression and limitation of stress response. Stress 10: 153-161
2. 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
3. Alonso G, Szafarczyk A, Assenmacher I, (1986) Immunoreactivity of hypothalamo-neurohypophysial neurons which secrete corticotropin-releasing hormone (CRH) and vasopressin (Vp): immunocytochemical evidence for a correlation with their functional state in colchicine-treated rats. Exp Brain Res 61: 497-505
4. Andressen C, Blumcke I, Celio MR, (1993) Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271: 181-208
5. Arai R, Jacobowitz DM, Deura S, (1993) Immunohistochemical localization of calretinin-, calbindin-D28k- and parvalbumin-containing cells in the hypothalamic paraventricular and supraoptic nuclei of the rat. Brain Res 618: 323-327
6. Armario A, (2006) The hypothalamic-pituitary-adrenal axis: what can it tell us about stressors? CNS Neurol Disord Drug Targets 5: 485-501
7. Bargmann W, (1969) The neurosecretory diencephalon-hypophyseal system and its synaptic connections. J Neurovisc Relat 31 (Suppl 9): 64-77
8. Barna I, Koenig JI, (1992) Effects of mediobasal hypothalamic lesion on immunoreactive ACTH/beta-endorphin levels in cerebrospinal fluid, in discrete brain regions, in plasma, and in pituitary of the rat. Brain Res 593: 69-76
9. Bauer MC, O'Connell DJ, Maj M, Wagner L, Cahill DJ, Linse S, (2011) Identification of a high-affinity network of secretagogin-binding proteins involved in vesicle secretion. Mol BioSyst 7: 2196-2204
10. Baxter JD, Forsham PH, (1972) Tissue effects of glucocorticoids. Am J Med 53: 573-589
11. Birkenkamp-Demtroder K, Wagner L, Brandt SF, Bording AL, Gartner W, Scherubl H, Heine B, Christiansen P, Orntoft TF, (2005) Secretagogin is a novel marker for neuroendocrine differentiation. Neuroendocrinology 82: 121-138
12. Brose N, Petrenko AG, Sudhof TC, Jahn R, (1992) Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256: 1021-1025
13. Cam GR, Bassett JR, (1983) The plasma levels of ACTH following exposure to stress or nicotine. Arch Int Pharmacodyn Ther 264: 154-167
14. Carafoli E, Santella L, Branca D, Brini M, (2001) Generation, control, and processing of cellular calcium signals. Crit Rev Biochem Mol Biol 36: 107-260
15. Cazalis M, Dayanithi G, Nordmann JJ, (1985) The role of patterned burst and interburst interval on the excitation-coupling mechanism in the isolated rat neural lobe. J Physiol 369: 45-60
16. Ceccatelli S, Cintra A, Hokfelt T, Fuxe K, Wikstrom AC, Gustafsson JA, (1989) Coexistence of glucocorticoid receptor-like immunoreactivity with neuropeptides in the hypothalamic paraventricular nucleus. Exp Brain Res 78: 33-42
17. Clapham DE, (2007) Calcium signaling. Cell 131: 1047-1058
18. Cortes R, Ceccatelli S, Schalling M, Hokfelt T, (1990) Differential effects of intracerebroventricular colchicine administration on the expression of mRNAs for neuropeptides and neurotransmitter enzymes, with special emphasis on galanin: an in situ hybridization study. Synapse 6: 369-391
19. Dayanithi G, Forostyak O, Ueta Y, Verkhratsky A, Toescu EC, (2012) Segregation of calcium signalling mechanisms in magnocellular neurones and terminals. Cell Calcium 51: 293-299
20. Dierickx K, Vandesande F, (1979) Immunocytochemical localization of somatostatin-containing neurons in the rat hypothalamus. Cell Tissue Res 201: 349-359
21. Donner KM, Hiltunen TP, Janne OA, Sane T, Kontula K, (2013) Generalized glucocorticoid resistance caused by a novel two-nucleotide deletion in the hormone-binding domain of the glucocorticoid receptor gene NR3C1. Eur J Endocrinol 168: K9-K18
22. Dutton A, Dyball RE, (1979) Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol 290: 433-440
23. Everitt BJ, Meister B, Hokfelt T, Melander T, Terenius L, Rokaeus A, Theodorsson-Norheim E, Dockray G, Edwardson J, Cuello C, (1986) The hypothalamic arcuate nucleus-median eminence complex: immunohistochemistry of transmitters, peptides and DARPP-32 with special reference to coexistence in dopamine neurons. Brain Res 396: 97-155
24. Fuxe K, Wikstrom AC, Okret S, Agnati LF, Harfstrand A, Yu ZY, Granholm L, Zoli M, Vale W, Gustafsson JA, (1985) Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor. Endocrinology 117: 1803-1812
25. Gainer H, Yamashita M, Fields RL, House SB, Rusnak M, (2002) The magnocellular neuronal phenotype: cell-specific gene expression in the hypothalamo-neurohypophysial system. Prog Brain Res 139: 1-14
26. Guillemin R, (1978) Peptides in the brain: the new endocrinology of the neuron. Science 202: 390-402
27. Haam J, Popescu IR, Morton LA, Halmos KC, Teruyama R, Ueta Y, Tasker JG, (2012) GABA is excitatory in adult vasopressinergic neuroendocrine cells. J Neurosci 32: 572-582
28. Hallbeck M, Blomqvist A, Hermanson O, (1996) Ca2+/calmodulin-dependent kinase II immunoreactivity in the rat hypothalamus. NeuroReport 7: 1957-1960
29. Harris GW, (1972) Humours and hormones. J Endocrinol 53: 2-23
30. Hata Y, Slaughter CA, Sudhof TC, (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366: 347-351
31. Herman JP, Schafer MK, Thompson RC, Watson SJ, (1992) Rapid regulation of corticotropin-releasing hormone gene transcription in vivo. Mol Endocrinol 6: 1061-1069
32. Hirokawa N, Takemura R, (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6: 201-214
33. Horvath TL, Gao XB, (2005) Input organization and plasticity of hypocretin neurons: possible clues to obesity's association with insomnia. Cell Metab 1: 279-286
34. Hrabovszky E, Wittmann G, Turi GF, Liposits Z, Fekete C, (2005) Hypophysiotropic thyrotropin-releasing hormone and corticotropin-releasing hormone neurons of the rat contain vesicular glutamate transporter-2. Endocrinology 146: 341-347
35. Islam S, Kjallquist U, Moliner A, Zajac P, Fan JB, Lonnerberg P, Linnarsson S, (2011) Characterization of the single-cell transcriptional landscape by highly multiplex RNA-seq. Genome Res 21: 1160-1167
36. Islam S, Zeisel A, Joost S, La MG, Zajac P, Kasper M, Lonnerberg P, Linnarsson S, (2014) Quantitative single-cell RNA-seq with unique molecular identifiers. Nat Methods 11: 163-166
37. Keegan CE, Herman JP, Karolyi IJ, O'Shea KS, Camper SA, Seasholtz AF, (1994) Differential expression of corticotropin-releasing hormone in developing mouse embryos and adult brain. Endocrinology 134: 2547-2555
38. Keimpema E, Barabas K, Morozov YM, Tortoriello G, Torii M, Cameron G, Yanagawa Y, Watanabe M, Mackie K, Harkany T, (2010) Differential subcellular recruitment of monoacylglycerol lipase generates spatial specificity of 2-arachidonoyl glycerol signaling during axonal pathfinding. J Neurosci 30: 13992-14007
39. Kiss JZ, Palkovits M, Zaborszky L, Tribollet E, Szabo D, Makara GB, (1983) Quantitative histological studies on the hypothalamic paraventricular nucleus in rats: I. Number of cells and synaptic boutons. Brain Res 262: 217-224
40. Kiss JZ, Cassell MD, Palkovits M, (1984) Analysis of the ACTH/beta-End/alpha-MSH-immunoreactive afferent input to the hypothalamic paraventricular nucleus of rat. Brain Res 324: 91-99
41. Kiss JZ, Martos J, Palkovits M, (1991) Hypothalamic paraventricular nucleus: a quantitative analysis of cytoarchitectonic subdivisions in the rat. J Comp Neurol 313: 563-573
42. Kiss A, Palkovits M, Aguilera G, (1996) Neural regulation of corticotropin releasing hormone (CRH) and CRH receptor mRNA in the hypothalamic paraventricular nucleus in the rat. J Neuroendocrinol 8: 103-112
43. Kita T, Chihara K, Abe H, Minamitani N, Kaji H, Kodama H, Chiba T, Fujita T, Yanaihara N, (1986) Regional distribution of gastrin-releasing peptide- and somatostatin-like immunoreactivity in the rabbit hypothalamus. Brain Res 398: 18-22
44. de Kloet ER, Joels M, Holsboer F, (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463-475
45. Kodama T, Guerrero S, Shin M, Moghadam S, Faulstich M, du Lac S, (2012) Neuronal classification and marker gene identification via single-cell expression profiling of brainstem vestibular neurons subserving cerebellar learning. J Neurosci 32: 7819-7831
46. Korte SM, (2001) Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev 25: 117-142
47. Kovacs KJ, Sawchenko PE, (1996) Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons. J Neurosci 16: 262-273
48. Lee S, Han TH, Sonner PM, Stern JE, Ryu PD, Lee SY, (2008) Molecular characterization of T-type Ca(2+) channels responsible for low threshold spikes in hypothalamic paraventricular nucleus neurons. Neuroscience 155: 1195-1203
49. Lee SK, Lee S, Shin SY, Ryu PD, Lee SY, (2012) Single cell analysis of voltage-gated potassium channels that determines neuronal types of rat hypothalamic paraventricular nucleus neurons. Neuroscience 205: 49-62
50. Léránth C, Antoni FA, Palkovits M, (1983) Ultrastructural demonstration of ovine CRF-like immunoreactivity (oCRF-LI) in the rat hypothalamus: processes of magnocellular neurons establish membrane specializations with parvocellular neurons containing oCRF-LI. Regul Pept 6: 179-188
51. Linden M, Lind SB, Mayrhofer C, Segersten U, Wester K, Lyutvinskiy Y, Zubarev R, Malmstrom PU, Pettersson U, (2012) Proteomic analysis of urinary biomarker candidates for nonmuscle invasive bladder cancer. Proteomics 12: 135-144
52. Lovatt D, Ruble BK, Lee J, Dueck H, Kim TK, Fisher S, Francis C, Spaethling JM, Wolf JA, Grady MS, Ulyanova AV, Yeldell SB, Griepenburg JC, Buckley PT, Kim J, Sul JY, Dmochowski IJ, Eberwine J, (2014) Transcriptome in vivo analysis (TIVA) of spatially defined single cells in live tissue. Nat Methods 11: 190-196
53. Luther JA, Tasker JG, (2000) Voltage-gated currents distinguish parvocellular from magnocellular neurones in the rat hypothalamic paraventricular nucleus. J Physiol 523 (Pt 1): 193-209
54. Luther JA, Daftary SS, Boudaba C, Gould GC, Halmos KC, Tasker JG, (2002) Neurosecretory and non-neurosecretory parvocellular neurones of the hypothalamic paraventricular nucleus express distinct electrophysiological properties. J Neuroendocrinol 14: 929-932
55. Maejima Y, Sedbazar U, Suyama S, Kohno D, Onaka T, Takano E, Yoshida N, Koike M, Uchiyama Y, Fujiwara K, Yashiro T, Horvath TL, Dietrich MO, Tanaka S, Dezaki K, Oh I, Hashimoto K, Shimizu H, Nakata M, Mori M, et al, (2009) Nesfatin-1-regulated oxytocinergic signaling in the paraventricular nucleus causes anorexia through a leptin-independent melanocortin pathway. Cell Metab 10: 355-365
56. Maj M, Milenkovic I, Bauer J, Berggard T, Veit M, Ilhan-Mutlu A, Wagner L, Tretter V, (2012) Novel insights into the distribution and functional aspects of the calcium binding protein secretagogin from studies on rat brain and primary neuronal cell culture. Front Mol Neurosci 5: 84
57. Makara GB, Stark E, Karteszi M, Palkovits M, Rappay G, (1981) Effects of paraventricular lesions on stimulated ACTH release and CRF in stalk-median eminence of the rat. Am J Physiol 240: E441-E446
58. Makino S, Hashimoto K, Gold PW, (2002) Multiple feedback mechanisms activating corticotropin-releasing hormone system in the brain during stress. Pharmacol Biochem Behav 73: 147-158
59. McEwen BS, (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87: 873-904
60. Meister B, Hokfelt T, Geffard M, Oertel W, (1988) Glutamic acid decarboxylase- and gamma-aminobutyric acid-like immunoreactivities in corticotropin-releasing factor-containing parvocellular neurons of the hypothalamic paraventricular nucleus. Neuroendocrinology 48: 516-526
61. Meister B, Villar MJ, Ceccatelli S, Hokfelt T, (1990) Localization of chemical messengers in magnocellular neurons of the hypothalamic supraoptic and paraventricular nuclei: an immunohistochemical study using experimental manipulations. Neuroscience 37: 603-633
62. Mulder J, Zilberter M, Spence L, Tortoriello G, Uhlen M, Yanagawa Y, Aujard F, Hokfelt T, Harkany T, (2009) Secretagogin is a Ca2+-binding protein specifying subpopulations of telencephalic neurons. Proc Natl Acad Sci U S A 106: 22492-22497
63. Naveilhan P, Hassani H, Lucas G, Blakeman KH, Hao JX, Xu XJ, Wiesenfeld-Hallin Z, Thoren P, Ernfors P, (2001) Reduced antinociception and plasma extravasation in mice lacking a neuropeptide Y receptor. Nature 409: 513-517
64. Ohtori S, Takahashi K, Chiba T, Takahashi Y, Yamagata M, Sameda H, Moriya H, (2000) Fos expression in the rat brain and spinal cord evoked by noxious stimulation to low back muscle and skin. Spine (Phila Pa 1976) 25: 2425-2430
65. Pacak K, Palkovits M, Kvetnansky R, Yadid G, Kopin IJ, Goldstein DS, (1995) Effects of various stressors on in vivo norepinephrine release in the hypothalamic paraventricular nucleus and on the pituitary-adrenocortical axis. Ann N Y Acad Sci 771: 115-130
66. Palkovits M, (1984) Neuropeptides in the hypothalamo-hypophyseal system: lateral retrochiasmatic area as a common gate for neuronal fibers towards the median eminence. Peptides 5 (Suppl 1): 35-39
67. Palkovits M, (1987) Anatomy of neural pathways affecting CRH secretion. Ann N Y Acad Sci 512: 139-148
68. Pang ZP, Sudhof TC, (2010) Cell biology of Ca2+-triggered exocytosis. Curr Opin Cell Biol 22: 496-505
69. Paxinos G, Franklin KBJ, (2001) The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press
70. Pelletier G, (1991) Anatomy of the hypothalamic-pituitary axis. Methods Achiev Exp Pathol 14: 1-22
71. Petersen OH, Michalak M, Verkhratsky A, (2005) Calcium signalling: past, present and future. Cell Calcium 38: 161-169
72. Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, Friedman JM, Horvath TL, (2004) Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304: 110-115
73. Rivier C, Vale W, (1983) Influence of the frequency of ovine corticotropin-releasing factor administration on adrenocorticotropin and corticosterone secretion in the rat. Endocrinology 113: 1422-1426
74. Rogstam A, Linse S, Lindqvist A, James P, Wagner L, Berggard T, (2007) Binding of calcium ions and SNAP-25 to the hexa EF-hand protein secretagogin. Biochem J 401: 353-363
75. van Rossum EF, Voorhoeve PG, te Velde SJ, Koper JW, Delemarre-van de Waal HA, Kemper HC, Lamberts SW, (2004) The ER22/23EK polymorphism in the glucocorticoid receptor gene is associated with a beneficial body composition and muscle strength in young adults. J Clin Endocrinol Metab 89: 4004-4009
76. Sanchez F, Alonso JR, Arevalo R, Carretero J, Vazquez R, Aijon J, (1992) Calbindin D-28K- and parvalbumin-reacting neurons in the hypothalamic magnocellular neurosecretory nuclei of the rat. Brain Res Bull 28: 39-46
77. Sapolsky RM, Krey LC, McEwen BS, (1986) The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr Rev 7: 284-301
78. Sawchenko PE, Imaki T, Potter E, Kovacs K, Imaki J, Vale W, (1993) The functional neuroanatomy of corticotropin-releasing factor. Ciba Found Symp 172: 5-21
79. Schally AV, (1978) Aspects of hypothalamic regulation of the pituitary gland. Science 202: 18-28
80. Schluter OM, Basu J, Sudhof TC, Rosenmund C, (2006) Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity. J Neurosci 26: 1239-1246
81. Schwaller B, (2009) The continuing disappearance of "pure" Ca2+ buffers. Cell Mol Life Sci 66: 275-300
82. Selye H, Fortier C, (1949) Adaptive reactions to stress. Res Publ Assoc Res Nerv Ment Dis 29: 3-18
83. Shapiro E, Biezuner T, Linnarsson S, (2013) Single-cell sequencing-based technologies will revolutionize whole-organism science. Nat Rev Genet 14: 618-630
84. Shi TJ, Xiang Q, Zhang MD, Tortoriello G, Hammarberg H, Mulder J, Fried K, Wagner L, Josephson A, Uhlen M, Harkany T, Hokfelt T, (2012) Secretagogin is expressed in sensory CGRP neurons and in spinal cord of mouse and complements other calcium-binding proteins, with a note on rat and human. Mol Pain 8: 80
85. Simmons DM, Swanson LW, (2009) Comparison of the spatial distribution of seven types of neuroendocrine neurons in the rat paraventricular nucleus: toward a global 3D model. J Comp Neurol 516: 423-441
86. Sollner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE, (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362: 318-324
87. Spiess J, Rivier J, Rivier C, Vale W, (1981) Primary structure of corticotropin-releasing factor from ovine hypothalamus. Proc Natl Acad Sci U S A 78: 6517-6521
88. Stern JE, (2001) Electrophysiological and morphological properties of pre-autonomic neurones in the rat hypothalamic paraventricular nucleus. J Physiol 537: 161-177
89. Sudhof TC, (2004) The synaptic vesicle cycle. Annu Rev Neurosci 27: 509-547
90. Sudhof TC, Rothman JE, (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477
91. Sutton RB, Fasshauer D, Jahn R, Brunger AT, (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353
92. Swanson LW, Sawchenko PE, (1980) Paraventricular nucleus: a site for the integration of neuroendocrine and autonomic mechanisms. Neuroendocrinology 31: 410-417
93. Swanson LW, Sawchenko PE, (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 6: 269-324
94. Swanson LW, Sawchenko PE, Lind RW, (1986) Regulation of multiple peptides in CRF parvocellular neurosecretory neurons: implications for the stress response. Prog Brain Res 68: 169-190
95. Swanson LW, Simmons DM, (1989) Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J Comp Neurol 285: 413-435
96. Swanson LW, (1991) Biochemical switching in hypothalamic circuits mediating responses to stress. Prog Brain Res 87: 181-200
97. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, et al, (2006) Molecular anatomy of a trafficking organelle. Cell 127: 831-846
98. Tang F, Barbacioru C, Wang Y, Nordman E, Lee C, Xu N, Wang X, Bodeau J, Tuch BB, Siddiqui A, Lao K, Surani MA, (2009) mRNA-Seq whole-transcriptome analysis of a single cell. Nat Methods 6: 377-382
99. Tasker JG, Herman JP, (2011) Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic-pituitary-adrenal axis. Stress 14: 398-406
100. Tobin V, Leng G, Ludwig M, (2012a) The involvement of actin, calcium channels and exocytosis proteins in somato-dendritic oxytocin and vasopressin release. Front Physiol 3: 261
101. Tobin V, Schwab Y, Lelos N, Onaka T, Pittman QJ, Ludwig M, (2012b) Expression of exocytosis proteins in rat supraoptic nucleus neurones. J Neuroendocrinol 24: 629-641
102. Tortoriello G, Morris CV, Alpar A, Fuzik J, Shirran SL, Calvigioni D, Keimpema E, Botting CH, Reinecke K, Herdegen T, Courtney M, Hurd YL, Harkany T, (2014) Miswiring the brain: Delta9-tetrahydrocannabinol disrupts cortical development by inducing an SCG10/stathmin-2 degradation pathway. EMBO J 33: 668-685
103. Tsafrir D, Tsafrir I, Ein-Dor L, Zuk O, Notterman DA, Domany E, (2005) Sorting points into neighborhoods (SPIN): data analysis and visualization by ordering distance matrices. Bioinformatics 21: 2301-2308
104. Vale W, Spiess J, Rivier C, Rivier J, (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213: 1394-1397
105. Vogt MC, Paeger L, Hess S, Steculorum SM, Awazawa M, Hampel B, Neupert S, Nicholls HT, Mauer J, Hausen AC, Predel R, Kloppenburg P, Horvath TL, Bruning JC, (2014) Neonatal insulin action impairs hypothalamic neurocircuit formation in response to maternal high-fat feeding. Cell 156: 495-509
106. Wagner L, Oliyarnyk O, Gartner W, Nowotny P, Groeger M, Kaserer K, Waldhausl W, Pasternack MS, (2000) Cloning and expression of secretagogin, a novel neuroendocrine- and pancreatic islet of Langerhans-specific Ca2+-binding protein. J Biol Chem 275: 24740-24751
107. Wamsteeker Cusulin JI, Fuzesi T, Watts AG, Bains JS, (2013) Characterization of corticotropin-releasing hormone neurons in the paraventricular nucleus of the hypothalamus of Crh-IRES-Cre mutant mice. PLoS ONE 8: e64943
108. Wickner W, Schekman R, (2008) Membrane fusion. Nat Struct Mol Biol 15: 658-664
109. Wynn PC, Aguilera G, Morell J, Catt KJ, (1983) Properties and regulation of high-affinity pituitary receptors for corticotropin-releasing factor. Biochem Biophys Res Commun 110: 602-608
110. Yamamori E, Asai M, Yoshida M, Takano K, Itoi K, Oiso Y, Iwasaki Y, (2004) Calcium/calmodulin kinase IV pathway is involved in the transcriptional regulation of the corticotropin-releasing hormone gene promoter in neuronal cells. J Mol Endocrinol 33: 639-649