Suppressor of cytokine Signalling-6 promotes neurite outgrowth via JAK2/STAT5-Mediated signalling pathway, involving negative feedback inhibition

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Gupta, Sakshi ^a   Mishra, Kanchan ^a   Surolia, Avadhesha ^a,b   Banerjee, Kakoli ^a  

^a NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

^b INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE 2; MESSENGER RNA; SMALL INTERFERING RNA; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; STAT5 PROTEIN; STAT5A PROTEIN; STAT5B PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; SUPPRESSOR OF CYTOKINE SIGNALING 6; UNCLASSIFIED DRUG; JAK2 PROTEIN, RAT; SOCS6 PROTEIN, RAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOINFORMATICS; CELL LEVEL; CELL STIMULATION; CELL STRAIN; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSFECTION; INHIBITION KINETICS; INTRACELLULAR SIGNALING; NEGATIVE FEEDBACK; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NEURAL STEM CELL; NONHUMAN; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; RAT; RNA INTERFERENCE; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; DRUG EFFECT; FEEDBACK SYSTEM; FEMALE; GENETICS; IMMUNOBLOTTING; MALE; METABOLISM; NEURITE; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FEEDBACK, PHYSIOLOGICAL; FEMALE; GENE EXPRESSION; IMMUNOBLOTTING; INSULIN-LIKE GROWTH FACTOR I; JANUS KINASE 2; MALE; NEURAL STEM CELLS; NEURITES; PC12 CELLS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 81255195795     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026674     Document Type: Article

References (62)

1. da Silva JS, Dotti CG, (2002) Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat Rev Neurosci 3: 694-704.
2. Goldshmit Y, Galea MP, Wise G, Bartlett PF, Turnley AM, (2004) Axonal regeneration and lack of astrocytic gliosis in EphA4-deficient mice. J Neurosci 24: 10064-10073.
3. Goldshmit Y, Greenhalgh CJ, Turnley AM, (2004) Suppressor of cytokine signalling-2 and epidermal growth factor regulate neurite outgrowth of cortical neurons. Eur J Neurosci 20: 2260-22660.
4. Goldshmit Y, Walters CE, Scott HJ, Greenhalgh CJ, Turnley AM, (2004) SOCS2 induces neurite outgrowth by regulation of epidermal growth factor receptor activation. J Biol Chem 279: 16349-16355.
5. Krebs DL, Hilton DJ, (2000) SOCS: physiological suppressors of cytokine signalling. J Cell Sci 113: 2813-2819.
6. Wormald S, Hilton DJ, (2004) Inhibitors of cytokine signal transduction. J Biol Chem 279: 821-824.
7. Hansen JA, Lindberg K, Hilton DJ, Nielsen JH, Billestrup N, (1999) Mechanism of inhibition of growth hormone receptor signalling by suppressor of cytokine signalling proteins. Mol Endocrinol 13: 1832-1843.
8. Ram PA, Waxman DJ, (1999) SOCS/CIS protein inhibition of growth hormone-stimulated STAT5 signalling by multiple mechanisms. J Biol Chem 274: 35553-35561.
9. Polizzotto MN, Bartlett PF, Turnley AM, (2000) Expression of "suppressor of cytokine signalling" (SOCS) genes in the developing and adult mouse nervous system. J Comp Neurol 423: 348-358.
10. Turnley AM, Starr R, Bartlett PF, (2001) SOCS1 regulates interferon-gamma mediated sensory neuron survival. Neuroreport 12: 3443-3445.
11. Scott HJ, Stebbing MJ, Walters CE, McLenachan S, Ransome MI, et al. (2006) Differential effects of SOCS2 on neuronal differentiation and morphology. Brain Res 1067: 138-145.
12. Turnley AM, Faux CH, Rietze RL, Coonan JR, Bartlett PF, (2002) Suppressor of cytokine signalling 2 regulates neuronal differentiation by inhibiting growth hormone signalling. Nat Neurosci 5: 1155-1162.
13. Cao F, Hata R, Zhu P, Ma YJ, Tanaka J, et al. (2006) Over-expression of SOCS3 inhibits astrogliogenesis and promotes maintenance of neural stem cells. J Neurochem 98: 459-470.
14. Zhu P, Hata R, Cao F, Gu F, Hanakawa Y, et al. (2008) Ramified microglial cells promote astrogliogenesis and maintenance of neural stem cells through activation of Stat3 function. FASEB J 22: 3866-3877.
15. Yadav A, Kalita A, Dhillon S, Banerjee K, (2005) JAK/STAT3 pathway is involved in survival of neurons in response to insulin-like growth factor and negatively regulated by suppressor of cytokine signalling-3. J Biol Chem 280: 31830-31840.
16. Drago J, Murphy M, Carroll SM, Harvey RP, Bartlett PF, (1991) Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc Natl Acad Sci U S A 88: 2199-2203.
17. Bondy CA, (1991) Transient IGF-I gene expression during the maturation of functionally related central projection neurons. J Neurosci 11: 3442-3455.
18. Liu JL, Grinberg A, Westphal H, Sauer B, Accili D, et al. (1998) Insulin-like growth factor-I affects perinatal lethality and postnatal development in a gene dosage-dependent manner: manipulation using the Cre/loxP system in transgenic mice. Mol Endocrinol 12: 1452-1462.
19. Ye P, Xing Y, Dai Z, D'Ercole AJ, (1996) In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-I increases proliferation of granule cell progenitors. Brain Res Dev Brain Res 95: 44-54.
20. Liu X, Mameza MG, Lee YS, Eseonu CI, Yu CR, et al. (2008) Suppressors of cytokine-signalling proteins induce insulin resistance in the retina and promote survival of retinal cells. Diabetes 57: 1651-1658.
21. Masuhara M, Sakamoto H, Matsumoto A, Suzuki R, Yasukawa H, et al. (1997) Cloning and characterization of novel CIS family genes. Biochem Biophys Res Commun 239: 439-446.
22. Nicholson SE, Willson TA, Farley A, Starr R, Zhang JG, et al. (1999) Mutational analyses of the SOCS proteins suggest a dual domain requirement but distinct mechanisms for inhibition of LIF and IL-6 signal transduction. EMBO J 18: 375-385.
23. Howard JK, Flier JS, (2006) Attenuation of leptin and insulin signalling by SOCS proteins. Trends Endocrinol Metab 17: 365-371.
24. Krebs DL, Uren RT, Metcalf D, Rakar S, Zhang JG, et al. (2002) SOCS-6 binds to insulin receptor substrate 4, and mice lacking the SOCS-6 gene exhibit mild growth retardation. Mol Cell Biol 22: 4567-4578.
25. Li L, Gronning LM, Anderson PO, Li S, Edvardsen K, et al. (2004) Insulin induces SOCS-6 expression and its binding to the p85 monomer of phosphoinositide 3-kinase, resulting in improvement in glucose metabolism. J Biol Chem 279: 34107-34114.
26. Mooney RA, Senn J, Cameron S, Inamdar N, Boivin LM, et al. (2001) Suppressors of cytokine signalling-1 and-6 associate with and inhibit the insulin receptor. A potential mechanism for cytokine-mediated insulin resistance. J Biol Chem 276: 25889-25893.
27. Bayle J, Lopez S, Iwai K, Dubreuil P, De Sepulveda P, (2006) The E3 ubiquitin ligase HOIL-1 induces the polyubiquitination and degradation of SOCS6 associated proteins. FEBS Lett 580: 2609-2614.
28. Hwang MN, Ha TH, Park J, Shim J, Lee H, et al. (2007) Increased SOCS6 stability with PMA requires its N-terminal region and the Erk pathway via Pkcdelta activation. Biochem Biophys Res Commun 354: 184-189.
29. Balasubramaniyan V, Timmer N, Kust B, Boddeke E, Copray S, (2004) Transient expression of Olig1 initiates the differentiation of neural stem cells into oligodendrocyte progenitor cells. Stem Cells 22: 878-882.
30. Shanley DK, Sullivan AM, (2006) Alterations in cellular phenotypes differentiating from embryonic rat brain neurosphere cultures by immunoselection of neuronal progenitors. Brain Res 1067: 85-94.
31. Vaudry D, Stork PJ, Lazarovici P, Eiden LE, (2002) Signalling pathways for PC12 cell differentiation: making the right connections. Science 296: 1648-1649.
32. Wang LH, Kirken RA, Erwin RA, Yu CR, Farrar WL, (1999) JAK3, STAT, and MAPK signalling pathways as novel molecular targets for the tyrphostin AG-490 regulation of IL-2-mediated T cell response. J Immunol 162: 3897-3904.
33. Nakasato M, Shirakura Y, Ooga M, Iwatsuki M, Ito M, et al. (2006) Involvement of the STAT5 signalling pathway in the regulation of mouse preimplantation development. Biol Reprod 75: 508-517.
34. Yasukawa H, Misawa H, Sakamoto H, Masuhara M, Sasaki A, et al. (1999) The JAK-binding protein JAB inhibits Janus tyrosine kinase activity through binding in the activation loop. EMBO J 18: 1309-1320.
35. Brooker GJ, Kalloniatis M, Russo VC, Murphy M, Werther GA, et al. (2000) Endogenous IGF-1 regulates the neuronal differentiation of adult stem cells. J Neurosci Res 59: 332-341.
36. Arsenijevic Y, Weiss S, Schneider B, Aebischer P, (2001) Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci 21: 7194-7202.
37. Ning H, Lin G, Fandel T, Banie L, Lue TF, et al. (2008) Insulin growth factor signalling mediates neuron-like differentiation of adipose-tissue-derived stem cells. Differentiation 76: 488-494.
38. Greene LA, Tischler AS, (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73: 2424-2428.
39. Turnley AM, (2005) Role of SOCS2 in growth hormone actions. Trends Endocrinol Metab 16: 53-58.
40. Nikolic M, Dudek H, Kwon YT, Ramos YF, Tsai LH, (1996) The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev 10: 816-825.
41. Lai RH, Hsiao YW, Wang MJ, Lin HY, Wu CW, et al. (2010) SOCS6, down-regulated in gastric cancer, inhibits cell proliferation and colony formation. Cancer Lett 288: 75-85.
42. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, et al. (1997) Regulation of gliogenesis in the central nervous system by the JAK-STAT signalling pathway. Science 278: 477-483.
43. Narita M, Miyatake M, Shibasaki M, Shindo K, Nakamura A, et al. (2006) Direct evidence of astrocytic modulation in the development of rewarding effects induced by drugs of abuse. Neuropsychopharmacology 31: 2476-2488.
44. O'Sullivan LA, Liongue C, Lewis RS, Stephenson SE, Ward AC, (2007) Cytokine receptor signalling through the Jak-Stat-Socs pathway in disease. Mol Immunol 44: 2497-2506.
45. Murray PJ, (2007) The JAK-STAT signalling pathway: input and output integration. J Immunol 178: 2623-2629.
46. Croker BA, Kiu H, Nicholson SE, (2008) SOCS regulation of the JAK/STAT signalling pathway. Semin Cell Dev Biol 19: 414-422.
47. Lee CK, Raz R, Gimeno R, Gertner R, Wistinghausen B, et al. (2002) STAT3 is a negative regulator of granulopoiesis but is not required for G-CSF-dependent differentiation. Immunity 17: 63-72.
48. Hwang MN, Kim KS, Choi YW, Jou I, Yoon S, (2007) PMA activates Stat3 in the Jak/Stat pathway and induces SOCS5 in rat brain astrocytes. Mol Cells 23: 94-99.
49. 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.
50. Zhu J, Cote-Sierra J, Guo L, Paul WE, (2003) Stat5 Activation Plays a Critical Role in Th2 Differentiation. Immunity 19: 739-748.
51. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui ALF, et al. (1999) STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J 18: 4754-4765.
52. Kyba M, Perlingeiro RC, Hoover RR, Lu CW, Pierce J, et al. (2003) Enhanced hematopoietic differentiation of embryonic stem cells conditionally expressing Stat5. Proc Natl Acad Sci U S A 100 (Suppl 1): 11904-10.
53. Byts N, Samoylenko A, Fasshauer T, Ivanisevic M, Hennighausen L, et al. (2008) Essential role for Stat5 in the neurotrophic but not in the neuroprotective effect of erythropoietin. Cell Death and Differentiation 15: 783-792.
54. Lee J-Y, Muenzberg H, Gavrilova O, Reed JA, Berryman D, et al. (2008) Loss of Cytokine-STAT5 Signaling in the CNS and Pituitary Gland Alters Energy Balance and Leads to Obesity. PLoS ONE 3 (2): e1639.
55. Zong CS, Chan J, Levy DE, Horvath C, Sadowski HB, et al. (2000) Mechanism of STAT3 activation by insulin-like growth factor I receptor. J Biol Chem 275: 15099-15105.
56. Himpe E, Kooijman R, (2009) Insulin-like growth factor-I receptor signal transduction and the Janus Kinase/Signal Transducer and Activator of Transcription (JAK-STAT) pathway. Biofactors 35: 76-81.
57. Dey BR, Spence SL, Nissley P, Furlanetto RW, (1998) Interaction of human suppressor of cytokine signalling (SOCS)-2 with the insulin-like growth factor-I receptor. J Biol Chem 273: 24095-24101.
58. Dey BR, Furlanetto RW, Nissley P, (2000) Suppressor of cytokine signalling (SOCS)-3 protein interacts with the insulin-like growth factor-I receptor. Biochem Biophys Res Commun 278: 38-43.
59. Garcia-Segura LM, Rodriguez JR, Torres-Aleman I, (1997) Localization of the insulin-like growth factor I receptor in the cerebellum and hypothalamus of adult rats: an electron microscopic study. J Neurocytology 26: 479-490.
60. Sehat B, Tofigh A, Lin Y, Trocmé E, Liljedahl U, et al. (2010) SUMOylation Mediates the Nuclear Translocation and Signaling of the IGF-1 receptor. Sci Signal 3: ra10.
61. Naka T, Narazaki M, Hirata M, Matsumoto T, Minamoto S, et al. (1997) Structure and function of a new STAT-induced STAT inhibitor. Nature 387: 924-929.
62. Piessevaux J, Lavens D, Montoye T, Wauman J, Catteeuw D, et al. (2006) Functional cross-modulation between SOCS proteins can stimulate cytokine signalling. J Biol Chem 281: 32953-32966.