Identification of STAT3 and STAT5 proteins in the rat suprachiasmatic nucleus and the Day/Night difference in astrocytic STAT3 phosphorylation in response to lipopolysaccharide

Journal of Neuroscience Research

Volumn 94, Issue 1, 2016, Pages 99-108

  Moravcová, Simona ^a   Červená, Kateřina ^a   Pačesová, Dominika ^a   Bendová, Zdeňka ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Circadian clock; Lipopolysaccharide; Rat; STAT proteins; Suprachiasmatic nucleus

Indexed keywords

LIPOPOLYSACCHARIDE; STAT3 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; STAT5 PROTEIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CIRCADIAN RHYTHM; CONTROLLED STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SUPRACHIASMATIC NUCLEUS; ANALYSIS OF VARIANCE; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PHOSPHORYLATION; TIME FACTOR; WISTAR RAT;

ANALYSIS OF VARIANCE; ANIMALS; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; LIPOPOLYSACCHARIDES; MALE; PHOSPHORYLATION; RATS; RATS, WISTAR; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; SUPRACHIASMATIC NUCLEUS; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 84945272105     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23673     Document Type: Article

References (65)

1. Bendová Z, Sládek M, Svobodová I. 2012. The expression of NR2B subunit of NMDA receptor in the suprachiasmatic nucleus of Wistar rats and its role in glutamate-induced CREB and ERK1/2 phosphorylation. Neurochem Int 61:43-47.
2. Bennett E, McGuinness L, Gevers EF, Thomas GB, Robinson IC, Davey HW, Luckman SM. 2005. Hypothalamic STAT proteins: regulation of somatostatin neurones by growth hormone via STAT5b. J Neuroendocrinol 17:186-194.
3. Beynon AL, Coogan AN. 2010. Diurnal, age, and immune regulation of interleukin-1β and interleukin-1 type 1 receptor in the mouse suprachiasmatic nucleus. Chronobiol Int 27:1546-1563.
4. Bhattacharya A, Vavra V, Svobodova I, Bendová Z, Vereb G, Zemkova H. 2013. Potentiation of inhibitory synaptic transmission by extracellular ATP in rat suprachiasmatic nuclei. J Neurosci 33:8035-8044.
5. Bozek K, Relógio A, Kielbasa SM, Heine M, Dame C, Kramer A, Herzel H. 2009. Regulation of clock-controlled genes in mammals. PLoS One 4:e4882.
6. 2+ axis controls circuit-level encoding of circadian time in the suprachiasmatic nucleus. Neuron 78:714-728.
7. Buntin JD, Buntin L. 2014. Increased STAT5 signaling in the ring dove brain in response to prolactin administration and spontaneous elevations in prolactin during the breeding cycle. Gen Comp Endocrinol 200:1-9.
8. Butcher GQ, Lee B, Cheng HY, Obrietan K. 2005. Light stimulates MSK1 activation in the suprachiasmatic nucleus via a PACAP-ERK/MAP kinase-dependent mechanism. J Neurosci 25:5305-5313.
9. Cao R, Lee B, Cho HY, Saklayen S, Obrietan K. 2008. Photic regulation of the mTOR signaling pathway in the suprachiasmatic circadian clock. Mol Cell Neurosci 38:312-324.
10. Cermakian N, Lange T, Golombek D, Sarkar D, Nakao A, Shibata S, Mazzoccoli G. 2013. Crosstalk between the circadian clock circuitry and the immune system. Chronobiol Int 30:870-888.
11. Chao HW, Lai YT, Lu YL, Lin CL, Mai W, Huang YS. 2012. NMDAR signaling facilitates the IPO5-mediated nuclear import of CPEB3. Nucleic Acids Res 40:8484-8498.
12. Chatterjee-Kishore M1, van den Akker F, Stark GR 2000. Association of STATs with relatives and friends. Trends Cell Biol 10:106-111.
13. Curtis AM, Bellet MM, Sassone-Corsi P, O'Neill LA. 2014. Circadian clock proteins and immunity. Immunity 40:178-186.
14. Dopp JM, Mackenzie-Graham A, Otero GC, Merrill JE. 1997. Differential expression, cytokine modulation, and specific functions of type-1 and type-2 tumor necrosis factor receptors in rat glia. J Neuroimmunol 75:104-112.
15. Duhart JM, Leone MJ, Paladino N, Evans JA, Castanon-Cervantes O, Davidson AJ, Golombek DA. 2013. Suprachiasmatic astrocytes modulate the circadian clock in response to TNF-α. J Immunol 191:4656-4664.
16. Ernst MB, Wunderlich CM, Hess S, Paehler M, Mesaros A, Koralov SB, Kleinridders A, Husch A, Münzberg H, Hampel B, Alber J, Kloppenburg P, Brüning JC, Wunderlich FT. 2009. Enhanced Stat3 activation in POMC neurons provokes negative feedback inhibition of leptin and insulin signaling in obesity. J Neurosci 29:11582-11593.
17. Franklin AE, Engeland CG, Kavaliers M, Ossenkopp KP. 2007. The rate of behavioral tolerance development to repeated lipopolysaccharide treatments depends upon the time of injection during the light-dark cycle: a multivariable examination of locomotor activity. Behav Brain Res 180:161-173.
18. Frontini A, Bertolotti P, Tonello C, Valerio A, Nisoli E, Cinti S, Giordano A. 2008. Leptin-dependent STAT3 phosphorylation in postnatal mouse hypothalamus. Brain Res 1215:105-115.
19. Gautron L, Lafon P, Chaigniau M, Tramu G, Layé S. 2002. Spatiotemporal analysis of signal transducer and activator of transcription 3 activation in rat brain astrocytes and pituitary following peripheral immune challenge. Neuroscience 112:717-729.
20. Girardet C, Lebrun B, Cabirol-Pol MJ, Tardivel C, François-Bellan AM, Becquet D, Bosler O. 2013. Brain-derived neurotrophic factor/TrkB signaling regulates daily astroglial plasticity in the suprachiasmatic nucleus: electron-microscopic evidence in mouse. Glia 61:1172-1177.
21. Golombek DA, Rosenstein RE. 2010. Physiology of circadian entrainment. Physiol Rev 90:1063-1102.
22. Grosbellet E, Gourmelen S, Pévet P, Criscuolo F, Challet E. 2015. Leptin normalizes photic synchronization in male ob/ob mice, via indirect effects on the suprachiasmatic nucleus. Endocrinology 156:1080-1090.
23. Guerrero-Vargas NN, Salgado-Delgado R, Basualdo Mdel C, García J, Guzmán-Ruiz M, Carrero JC, Escobar C, Buijs RM. 2014. Reciprocal interaction between the suprachiasmatic nucleus and the immune system tunes down the inflammatory response to lipopolysaccharide. J Neuroimmunol 273:22-30.
24. Guido ME, de Guido L, Goguen D, Robertson HA, Rusak B. 1999. Differential effects of glutamatergic blockade on circadian and photic regulation of gene expression in the hamster suprachiasmatic nucleus. Brain Res Mol Brain Res 67:247-257.
25. Guo D, Dunbar JD, Yang CH, Pfeffer LM, Donner DB. 1998. Induction of Jak/STAT signaling by activation of the type 1 TNF receptor. J Immunol 160:2742-2750.
26. Gupta S, Mishra K, Surolia A, Banerjee K. 2011. Suppressor of cytokine signalling-6 promotes neurite outgrowth via JAK2/STAT5-mediated signalling pathway, involving negative feedback inhibition. PLoS One 6:e26674.
27. He F, Ge W, Martinowich K, Becker-Catania S, Coskun V, Zhu W, Wu H, Castro D, Guillemot F, Fan G, de Vellis J, Sun YE. 2005. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. Nat Neurosci 8:616-625.
28. He JC, Gomes I, Nguyen T, Jayaram G, et al. 2005. A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis. J Biol Chem 280:33426-33434.
29. Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, Korsak RA, Takeda K, Akira S, Sofroniew MV. 2008. STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28:7231-7243.
30. Howard JK, Cave BJ, Oksanen LJ, Tzameli I, Bjørbaek C, Flier JS. 2004. Enhanced leptin sensitivity and attenuation of diet-induced obesity in mice with haploinsufficiency of Socs3. Nat Med 10:734-738.
31. Jakubcakova V, Oster H, Tamanini F, Cadenas C, Leitges M, van der Horst GT, Eichele G. 2007. Light entrainment of the mammalian circadian clock by a PRKCA-dependent posttranslational mechanism. Neuron 54:831-843.
32. Kim YI, Choi HJ, Colwell CS. 2006. Brain-derived neurotrophic factor regulation of N-methyl-D-aspartate receptor-mediated synaptic currents in suprachiasmatic nucleus neurons. J Neurosci Res 84:1512-1520.
33. Kiu H, Nicholson SE. 2012. Biology and significance of the JAK/STAT signalling pathways. Growth Factors 30:88-106.
34. Leone MJ, Marpegán L, Bekinschtein TA, Costas MA, Golombek DA. 2006. Suprachiasmatic astrocytes as an interface for immune-circadian signalling. J Neurosci Res 84:1521-1527.
35. Ma FY, Anderson GM, Gunn TD, Goffin V, Grattan DR, Bunn SJ. 2005. Prolactin specifically activates signal transducer and activator of transcription 5b in neuroendocrine dopaminergic neurons. Endocrinology 146:5112-5119.
36. Markham K, Schuurmans C, Weiss S. 2007. STAT5A/B activity is required in the developing forebrain and spinal cord. Mol Cell Neurosci 35:272-282.
37. Marpegán L, Bekinschtein TA, Costas MA, Golombek DA. 2005. Circadian responses to endotoxin treatment in mice. J Neuroimmunol 160:102-109.
38. Marpegán L, Leone MJ, Katz ME, Sobrero PM, Bekinstein TA, Golombek DA. 2009. Diurnal variation in endotoxin-induced mortality in mice: correlation with proinflammatory factors. Chronobiol Int 26:1430-1442.
39. Moore RY. 2013. The suprachiasmatic nucleus and the circadian timing system. Prog Mol Biol Transl Sci 119:1-28.
40. Nakano Y, Furube E, Morita S, Wanaka A, Nakashima T, Miyata S. 2015. Astrocytic TLR4 expression and LPS-induced nuclear translocation of STAT3 in the sensory circumventricular organs of adult mouse brain. J Neuroimmunol 278:144-158.
41. Nicolas CS, Peineau S, Amici M, Csaba Z, Fafouri A, Javalet C, Collett VJ, Hildebrandt L, Seaton G, Choi SL, Sim SE, Bradley C, Lee K, Zhuo M, Kaang BK, Gressens P, Dournaud P, Fitzjohn SM, Bortolotto ZA, Cho K, Collingridge GL. 2012. The Jak/STAT pathway is involved in synaptic plasticity. Neuron 73:374-390.
42. O'Callaghan JP, Kelly KA, VanGilder RL, Sofroniew MV, Miller DB. 2014. Early activation of STAT3 regulates reactive astrogliosis induced by diverse forms of neurotoxicity. PLoS One 9:e102003.
43. Okada K, Yano M, Doki Y, Azama T, Iwanaga H, Miki H, Nakayama M, Miyata H, Takiguchi S, Fujiwara Y, Yasuda T, Ishida N, Monden M. 2008. Injection of LPS causes transient suppression of biological clock genes in rats. J Surg Res 145:5-12.
44. Pačesová D, Volfová B, Červená K, Hejnová L, Novotný J, Bendová Z. 2015. Acute morphine affects the rat circadian clock via rhythms of phosphorylated ERK1/2 and GSK3β kinases and Per1 expression in the rat suprachiasmatic nucleus. Br J Pharmacol 172:3638-3649.
45. Paladino N, Mul Fedele ML, Duhart JM, Marpegán L, Golombek DA. 2014. Modulation of mammalian circadian rhythms by tumor necrosis factor-α. Chronobiol Int 31:668-679.
46. Pellegrino MJ, Habecker BA. 2013. STAT3 integrates cytokine and neurotrophin signals to promote sympathetic axon regeneration. Mol Cell Neurosci 56:272-282.
47. Peng SC, Lai YT, Huang HY, Huang HD, Huang YS. 2010. A novel role of CPEB3 in regulating EGFR gene transcription via association with Stat5b in neurons. Nucleic Acids Res 38:7446-7457.
48. Pincheira R, Castro AF, Ozes ON, Idumalla PS, Donner DB. 2008. Type 1 TNF receptor forms a complex with and uses Jak2 and c-Src to selectively engage signaling pathways that regulate transcription factor activity. J Immunol 181:1288-1298.
49. Pircher TJ, Petersen H, Gustafsson JA, Haldosén LA. 1999. Extracellular signal-regulated kinase (ERK) interacts with signal transducer and activator of transcription (STAT) 5a. Mol Endocrinol 13:555-565.
50. Ptitsyn AA, Gimble JM. 2007. Analysis of circadian pattern reveals tissue-specific alternative transcription in leptin signaling pathway. BMC Bioinformatics 8(Suppl 7):S15.
51. Rajan P. 2011. STATus and context within the mammalian nervous system. Mol Med 17:965-973.
52. Sadki A, Bentivoglio M, Kristensson K, Nygård M. 2007. Suppressors, receptors, and effects of cytokines on the aging mouse biological clock. Neurobiol Aging 28:296-305.
53. Sarafian TA, Montes C, Imura T, Qi J, Coppola G, Geschwind DH, Sofroniew MV. 2010. Disruption of astrocyte STAT3 signaling decreases mitochondrial function and increases oxidative stress in vitro. PLoS One 5:e9532.
54. Sasaki A, Yasukawa H, Suzuki A, Kamizono S, Syoda T, Kinjyo I, Sasaki M, Johnston JA, Yoshimura A. 1999. Cytokine-inducible SH2 protein-3 (CIS3/SOCS3) inhibits Janus tyrosine kinase by binding through the N-terminal kinase inhibitory region as well as SH2 domain. Genes Cells 4:339-351.
55. Timofeeva OA, Tarasova NI. 2012. Alternative ways of modulating JAK-STAT pathway: looking beyond phosphorylation. JAKSTAT 1:274-284.
56. Wang Z, Bunting KD. 2013. STAT5 in hematopoietic stem cell biology and transplantation. JAKSTAT 2:e27159.
57. Washburn KB, Neary JT. 2006. P2 purinergic receptors signal to STAT3 in astrocytes: difference in STAT3 responses to P2Y and P2X receptor activation. Neuroscience 142:411-423.
58. Watson CJ, Burdon TG. 1996. Prolactin signal transduction mechanisms in the mammary gland: the role of the Jak/Stat pathway. Rev Reprod 1:1-5.
59. Wierenga AT, Vogelzang I, Eggen BJ, Vellenga E. 2003. Erythropoietin-induced serine 727 phosphorylation of STAT3 in erythroid cells is mediated by a MEK-, ERK-, and MSK1-dependent pathway. Exp Hematol 31:398-405.
60. Wunderlich CM, Hövelmeyer N, Wunderlich FT. 2013. Mechanisms of chronic JAK-STAT3-SOCS3 signaling in obesity. JAKSTAT 2:e23878.
61. Wyszomierski SL, Rosen JM. 2001. Cooperative effects of STAT5 (signal transducer and activator of transcription 5) and C/EBPbeta (CCAAT/enhancer-binding protein-beta) on beta-casein gene transcription are mediated by the glucocorticoid receptor. Mol Endocrinol 15:228-240.
62. Xiong A, Yang Z, Shen Y, Zhou J, Shen Q. 2014. Transcription factor STAT3 as a novel molecular target for cancer prevention. Cancers 6:926-957.
63. Yang J, Stark GR. 2008. Roles of unphosphorylated STATs in signaling. Cell Res 18:443-451.
64. Yokogami K, Wakisaka S, Avruch J, Reeves SA. 2000. Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR. Curr Biol 10:47-50.
65. Yoshimura A, Naka T, Kubo M. 2007. SOCS proteins, cytokine signaling, and immune regulation. Nat Rev Immunol 7:454-465.