Potential Role of JAK-STAT Signaling Pathway in the Neurogenic-to-Gliogenic Shift in Down Syndrome Brain

Neural Plasticity

Volumn 2016, Issue , 2016, Pages

  Lee, Han Chung ^a,b   Tan, Kai Leng ^a   Cheah, Pike See ^a   Ling, King Hwa ^a,b  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^b Faculty of Science   (Malaysia)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; JANUS KINASE; STAT PROTEIN;

BRAIN DEVELOPMENT; COGNITION; DOWN SYNDROME; GAIN OF FUNCTION MUTATION; GLIOGENESIS; HUMAN; LOSS OF FUNCTION MUTATION; MACROGLIA; NERVE CELL DIFFERENTIATION; NEUROEPITHELIUM CELL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; DISEASE MODEL; EMBRYOLOGY; GENETICS; GLIA; METABOLISM; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT;

ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DOWN SYNDROME; HUMANS; JANUS KINASES; MICE; NEUROGENESIS; NEUROGLIA; NEURONS; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84962678654     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2016/7434191     Document Type: Review

References (86)

1. J. Busciglio, G. Capone, J. P. O'Byran, and K. J. Gardiner, "Down syndrome: genes, model systems, and progress towards pharmacotherapies and clinical trials for cognitive deficits," Cytogenetic and Genome Research, vol. 141, no. 4, pp. 260-271, 2013.
2. C. Finesilver, "A new age for childhood diseases. Down syndrome," RN, vol. 65, no. 11, pp. 43-49, 2002.
3. F. K. Wiseman, K. A. Alford, V. L. J. Tybulewicz, and E. M. C. Fisher, "Down syndrome-recent progress and future prospects," Human Molecular Genetics, vol. 18, no. 1, pp. R75-R83, 2009.
4. M. Marin-Padilla, "Pyramidal cell abnormalities in the motor cortex of a child with Down's syndrome. A Golgi study," The Journal of Comparative Neurology, vol. 167, no. 1,pp. 63-81, 1976.
5. L. E. Becker, D. L. Armstrong, and F. Chan, "Dendritic atrophy in children with Down's syndrome," Annals of Neurology, vol. 20, no. 4, pp. 520-526, 1986.
6. I. Ferrer and F. Gullotta, "Down's syndrome and Alzheimer's disease: dendritic spine counts in the hippocampus," Acta Neuropathologica, vol. 79, no. 6, pp. 680-685, 1990.
7. K. E. Wisniewski, "Down syndrome children often have brain with maturation delay, retardation of growth, and cortical dysgenesis," American Journal of Medical Genetics, vol. 7, Supplement, pp. 274-281, 1990.
8. E. H. Aylward, R. Habbak, A. C. Warren et al., "Cerebellar volume in adults with down syndrome," Archives of Neurology, vol. 54, no. 2, pp. 209-212, 1997.
9. W. E. Kaufmann and H. W. Moser, "Dendritic anomalies in disorders associated with mental retardation," Cerebral Cortex, vol. 10, no. 10, pp. 981-991, 2000.
10. W. R. Kates, B. S. Folley, D. C. Lanham, G. T. Capone, andW. E. Kaufmann, "Cerebral growth in Fragile X syndrome: review and comparison with Down syndrome," Microscopy Research and Technique, vol. 57, no. 3, pp. 159-167, 2002.
11. L. Chakrabarti, Z. Galdzicki, and T. F. Haydar, "Defects in embryonic neurogenesis and initial synapse formation in the forebrain of the Ts65Dn mousemodel of Down syndrome," The Journal of Neuroscience, vol. 27, no. 43, pp. 11483-11495, 2007.
12. S. Guidi, E. Ciani, P. Bonasoni, D. Santini, and R. Bartesaghi, "Widespread proliferation impairment and hypocellularity in the cerebellum of fetuses with down syndrome," Brain Pathology, vol. 21, no. 4, pp. 361-373, 2011.
13. S. Guidi, P. Bonasoni, C. Ceccarelli et al., "Neurogenesis impairment and increased cell death reduce total neuron number in the hippocampal region of fetuses with Down syndrome," Brain Pathology, vol. 18, no. 2, pp. 180-197, 2008.
14. A. Contestabile, T. Fila, C. Ceccarelli et al., "Cell cycle alteration and decreased cell proliferation in the hippocampal dentate gyrus and in the neocortical germinal matrix of fetuses with down syndrome and in Ts65Dn mice," Hippocampus, vol. 17, no. 8, pp. 665-678, 2007.
15. E. M. Ullian, S. K. Sapperstein, K. S. Christopherson, and B. A. Barres, "Control of synapse number by glia," Science, vol. 291, no. 5504, pp. 657-661, 2001.
16. A. J. Barker and E. M. Ullian, "Astrocytes and synaptic plasticity," The Neuroscientist, vol. 16, no. 1, pp. 40-50, 2010.
17. M. Sidoryk-Wegrzynowicz, E. Lee, N. Mingwei, and M. Aschner, "Disruption of astrocytic glutamine turnover bymanganese is mediated by the protein kinase C pathway," Glia, vol. 59, no. 11, pp. 1732-1743, 2011.
18. J. A. Briggs, J. Sun, J. Shepherd et al., "Integration-free induced pluripotent stem cells model genetic and neural developmental features of down syndrome etiology," STEM CELLS, vol. 31, no. 3, pp. 467-478, 2013.
19. G. Zdaniuk, T. Wierzba-Bobrowicz, G. M. Szpak, and T. Stpien, "Astroglia disturbances during development of the central nervous system in fetuses with Down's syndrome," Folia Neuropathologica, vol. 49, no. 2, pp. 109-114, 2011.
20. C. A. Hewitt, K.-H. Ling, T. D. Merson et al., "Gene network disruptions and neurogenesis defects in the adult Ts1Cjemouse model of down syndrome," PLoS ONE, vol. 5, no. 7, Article ID e11561, 2010.
21. C.Chen, P. Jiang, H. Xue et al., "Role of astroglia inDown's syndrome revealed by patient-derived human-induced pluripotent stem cells," Nature Communications, vol. 5, article 4430, 2014.
22. A. Bonni, Y. Sun, M. Nadal-Vicens et al., "Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway," Science, vol. 278, no. 5337, pp. 477-483, 1997.
23. D. M. Wilcock, "Neuroinflammation in the aging down syndrome brain; lessons fromAlzheimer's disease," Current Gerontology and Geriatrics Research, vol. 2012, Article ID 170276, 10 pages, 2012.
24. K. Shuai and B. Liu, "Regulation of JAK-STAT signalling in the immune system," Nature Reviews Immunology, vol. 3, no. 11, pp. 900-911, 2003.
25. C. S.Nicolas, M. Amici, Z. A. Bortolotto et al., "The role of JAKSTAT signaling within the CNS," JAK-STAT, vol. 2, no. 1,Article ID e22925, 2013.
26. T. Kisseleva, S. Bhattacharya, J. Braunstein, and C.W. Schindler, "Signaling through the JAK/STAT pathway, recent advances and future challenges," Gene, vol. 285, no. 1-2, pp. 1-24, 2002.
27. K. D. Liu, S. L. Gaffen, and M. A. Goldsmith, "JAK/STAT signaling by cytokine receptors," Current Opinion in Immunology, vol. 10, no. 3, pp. 271-278, 1998.
28. P.Dell'Albani,R.Santangelo, L. Torrisi,V.G.Nicoletti, andA.M. G. Stella, "Role of the JAK/STAT signal transduction pathway in the regulation of gene expression in CNS," Neurochemical Research, vol. 28, no. 1, pp. 53-64, 2003.
29. C. Schindler, D. E. Levy, and T. Decker, "JAK-STAT signaling: from interferons to cytokines," The Journal of Biological Chemistry, vol. 282, no. 28, pp. 20059-20063, 2007.
30. S. Hong and M.-R. Song, "STAT3 but not STAT1 is required for astrocyte differentiation," PLoS ONE, vol. 9, no. 1,Article ID e86851, 2014.
31. C. De-Fraja, L. Conti, L. Magrassi, S. Govoni, and E. Cattaneo, "Members of the JAK/STAT proteins are expressed and regulated during development in themammalian forebrain," Journal of Neuroscience Research, vol. 54, no. 3, pp. 320-330, 1998.
32. Y. H. Kim, J.-I. Chung, H. G.Woo et al., "Differential regulation of proliferation and differentiation in neural precursor cells by the Jak pathway," STEM CELLS, vol. 28, no. 10, pp. 1816-1828, 2010.
33. C. De-Fraja, L. Conti, S. Govoni, F. Battaini, and E. Cattaneo, "STAT signalling in the mature and aging brain," International Journal of DevelopmentalNeuroscience, vol. 18, no. 4-5, pp. 439-446, 2000.
34. T. Shimazaki, "Regulatory mechanisms underlying the neurogenesis-to-gliogenesis switch by neural stem cells," in Cortical Development, R. Kageyama and T. Yamamori, Eds., pp. 63-87, Springer, Tokyo, Japan, 2013.
35. K. Nakashima, M. Yanagisawa, H. Arakawa et al., "Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300," Science, vol. 284, no. 5413, pp. 479-482, 1999.
36. J. S.Rawlings, K.M. Rosler, andD. A. Harrison, "The JAK/STAT signaling pathway," Journal of Cell Science, vol. 117, part 8, pp. 1281-1283, 2004.
37. Y. Zheng, H. Qin, S. J. Frank et al., "ACK2-dependent mechanism for activation of the JAK-STAT signaling pathway," Blood, vol. 118, no. 1, pp. 156-166, 2011.
38. D. J.Gough,D.E.Levy, R.W. Johnstone, andC. J.Clarke, "IFN signaling-does it mean JAK-STAT" Cytokine and Growth Factor Reviews, vol. 19, no. 5-6, pp. 383-394, 2008.
39. O. Hermanson, K. Jepsen, and M. G. Rosenfeld, "N-CoR controls differentiation of neural stem cells into astrocytes," Nature, vol. 419, no. 6910, pp. 934-939, 2002.
40. Y. Hirabayashi, N. Suzki, M. Tsuboi et al., "Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition," Neuron, vol. 63, no. 5, pp. 600-613, 2009.
41. M. Namihira, J. Kohyama, K. Semi et al., "Committed neuronal precursors confer astrocytic potential on residual neural precursor cells," Developmental Cell, vol. 16, no. 2, pp. 245-255, 2009.
42. G. Fan, K. Martinowich, M. H. Chin et al., "DNA methylation controls the timing of astrogliogenesis through regulation of JAK-STAT signaling," Development, vol. 132, no. 15, pp. 3345-3356, 2005.
43. D.M.Hallam, N. L. Capps, A. L. Travelstead, G. J. Brewer, and L. E.Maroun, "Evidence for an interferon-related inflammatory reaction in the trisomy 16 mouse brain leading to caspase-1-mediated neuronal apoptosis," Journal of Neuroimmunology, vol. 110, no. 1-2, pp. 66-75, 2000.
44. K.-H. Ling,C.A.Hewitt, K.-L.Tan et al., "Functional transcriptome analysis of the postnatal brain of the Ts1Cje mouse model for Down syndrome reveals global disruption of interferonrelatedmolecular networks,"BMC Genomics, vol. 15, article 624, 2014.
45. X. Sturgeon, T. Le, M. M. Ahmed, and K. J. Gardiner, "Pathways to cognitive deficits in Down syndrome," Progress in Brain Research, vol. 197, pp. 73-100, 2012.
46. K. Amano, H. Sago, C. Uchikawa et al., "Dosage-dependent over-expression of genes in the trisomic region of Ts1Cje mouse model forDown syndrome," HumanMolecular Genetics, vol. 13, no. 13, pp. 1333-1340, 2004.
47. K.-H. Ling,C.A.Hewitt, K.-L.Tan et al., "Functional transcriptome analysis of the postnatal brain of the Ts1Cje mouse model for Down syndrome reveals global disruption of interferonrelated molecular networks," BMC Genomics, vol. 15, no. 1, article 624, 2014.
48. F.Guedj, J. L. A. Pennings,H.C.Wick, andD.W. Bianchi, "Analysis of adult cerebral cortex and hippocampus transcriptomes reveals unique molecular changes in the Ts1Cje mouse model of down syndrome," Brain Pathology, vol. 25, no. 1, pp. 11-23, 2015.
49. R. Ferrando-Miguel, K.-S. Shim, M. S. Cheon, M. Gimona, M. Furuse, and G. Lubec, "Overexpression of interferon/receptor chain in fetal Down syndrome brain," Neuroembryology and Aging, vol. 2, no. 4, pp. 147-155, 2003.
50. L. E. Maroun, "Interferon action and chromosome 21 trisomy (Down syndrome): 15 years later," Journal ofTheoretical Biology, vol. 181, no. 1, pp. 41-46, 1996.
51. D. M. Wilcock and W. S. T. Griffin, "Down's syndrome, neuroinflammation, and Alzheimer neuropathogenesis," Journal of Neuroinflammation, vol. 10, article 84, 2013.
52. G. R. Stark and J. E.Darnell, "The JAK-STAT pathway at twenty," Immunity, vol. 36, no. 4, pp. 503-514, 2012.
53. F. He, W. Ge, K.Martinowich et al., "A positive autoregulatory loop of Jak-STAT signaling controls the onset of astrogliogenesis," Nature Neuroscience, vol. 8, no. 5, pp. 616-625, 2005.
54. J.Walter, H.-P. Hartung, andM. Dihne, "Interferon gamma and sonic hedgehog signaling are required to dysregulate murine neural stem/precursor cells," PLoS ONE, vol. 7, no. 8,Article ID e43338, 2012.
55. S. Dedoni, M. C. Olianas, A. Ingianni, and P. Onali, "Type i interferons impair BDNF-induced cell signaling and neurotrophic activity in differentiated human SH-SY5Y neuroblastoma cells and mouse primary cortical neurons," Journal of Neurochemistry, vol. 122, no. 1, pp. 58-71, 2012.
56. H. Hasle, I. Haunstrup Clemmensen, andM.Mikkelsen, "Risks of leukaemia and solid tumours in individuals with Down's syndrome," The Lancet, vol. 355, no. 9199, pp. 165-169, 2000.
57. K. Patja, E. Pukkala, R. Sund, M. Iivanainen, and M. Kaski, "Cancer incidence of persons with Down syndrome in Finland: a population-based study," International Journal of Cancer, vol. 118, no. 7, pp. 1769-1772, 2006.
58. E. Flex, V. Petrangeli, L. Stella et al., "Somatically acquired JAK1 mutations in adult acute lymphoblastic leukemia," The Journal of Experimental Medicine, vol. 205, no. 4, pp. 751-758, 2008.
59. S. Breit, M. Stanulla, T. Flohr et al., "Activating NOTCH1 mutations predict favorable early treatment response and longterm outcome in childhood precursor T-cell lymphoblastic leukemia," Blood, vol. 108, no. 4, pp. 1151-1157, 2006.
60. T. Hornakova, S. Chiaretti, M. M. Lemaire et al., "ALLassociated JAK1 mutations confer hypersensitivity to the antiproliferative effect of type I interferon," Blood, vol. 115, no. 16, pp. 3287-3295, 2010.
61. A. Laurence, M. Pesu, O. Silvennoinen, and J. O'Shea, "JAK kinases in health and disease: an update," The Open Rheumatology Journal, vol. 6, no. 2, pp. 232-244, 2012.
62. R. Zhao, S. Xing, Z. Li et al., "Identification of an acquired JAK2 mutation in polycythemia vera," The Journal of Biological Chemistry, vol. 280, no. 24, pp. 22788-22792, 2005.
63. C. James, V. Ugo, J.-P. Le Couedic et al., "A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera," Nature, vol. 434, no. 7037, pp. 1144-1148, 2005.
64. R. L. Levine, M. Wadleigh, J. Cools et al., "Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, andmyeloidmetaplasia withmyelofibrosis," Cancer Cell, vol. 7, no. 4, pp. 387-397, 2005.
65. M. B. Hookham, J. Elliott, Y. Suessmuth et al., "The myeloproliferative disorder-associated JAK2 V617F mutant escapes negative regulation by suppressor of cytokine signaling 3," Blood, vol. 109, no. 11, pp. 4924-4929, 2007.
66. D. Bercovich, I. Ganmore, L. M. Scott et al., "Mutations of JAK2 in acute lymphoblastic leukaemias associatedwithDown's syndrome," The Lancet, vol. 372, no. 9648, pp. 1484-1492, 2008.
67. L. Kearney, D. G. De Castro, J. Yeung et al., "Specific JAK2 mutation (JAK2R683) and multiple gene deletions in Down syndrome acute lymphoblastic leukemia," Blood, vol. 113, no. 3, pp. 646-648, 2009.
68. S.Malinge, R. Ben-Abdelali, C. Settegrana et al., "Novel activating JAK2mutation in a patient withDown syndrome andB-cell precursor acute lymphoblastic leukemia," Blood, vol. 109, no. 5, pp. 2202-2204, 2007.
69. S. Malinge, C. Ragu, V. Della-Valle et al., "Activating mutations in human acute megakaryoblastic leukemia," Blood, vol. 112, no. 10, pp. 4220-4226, 2008.
70. D. K. Walters, T. Mercher, T.-L. Gu et al., "Activating alleles of JAK3 in acute megakaryoblastic leukemia," Cancer Cell, vol. 10, no. 1, pp. 65-75, 2006.
71. T. Sato, T. Toki, R. Kanezaki et al., "Functional analysis of JAK3 mutations in transient myeloproliferative disorder and acute megakaryoblastic leukaemia accompanying Down syndrome," British Journal ofHaematology, vol. 141, no. 5, pp. 681-688, 2008.
72. R. C. Harvey, C. G. Mullighan, I.-M. Chen et al., "Rearrangement of CRLF2 is associated with mutation of JAK kinases, alteration of IKZF1, Hispanic/Latino ethnicity, and a poor outcome in pediatric B-progenitor acute lymphoblastic leukemia," Blood, vol. 115, no. 26, pp. 5312-5321, 2010.
73. A. Yoda, Y. Yoda, S. Chiaretti et al., "Functional screening identifies CRLF2 in precursor B-cell acute lymphoblastic leukemia," Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 1, pp. 252-257, 2010.
74. J. Mäkelä, R. Koivuniemi, L. Korhonen, and D. Lindholm, "Interferon-produced by microglia and the neuropeptide PACAP have opposite effects on the viability of neural progenitor cells," PLoS ONE, vol. 5, no. 6,Article ID e11091, 2010.
75. L. E.Maroun, T. N. Heffernan, and D. M. Hallam, "Partial IFN-/and IFN-receptor knockout trisomy 16 mouse fetuses show improved growth and cultured neuron viability," Journal of Interferon & Cytokine Research, vol. 20, no. 2, pp. 197-203, 2000.
76. D. M. Hallam and L. E. Maroun, "Anti-gamma interferon can prevent the premature death of trisomy 16 mouse cortical neurons in culture," Neuroscience Letters, vol. 252, no. 1, pp. 17-20, 1998.
77. J. M. Taylor, M. R. Minter, A. G. Newman, M. Zhang, P. A. Adlard, and P. J. Crack, "Type-1 interferon signaling mediates neuro-inflammatory events in models of Alzheimer's disease," Neurobiology of Aging, vol. 35, no. 5, pp. 1012-1023, 2014.
78. L. E. Maroun, "Anti-interferon immunoglobulins can improve the trisomy 16 mouse phenotype," Teratology, vol. 51, no. 5, pp. 329-335, 1995.
79. M. Furqan, N. Mukhi, B. Lee, and D. Liu, "Dysregulation of JAK-STAT pathway in hematological malignancies and JAK inhibitors for clinical application," Biomarker Research, vol. 1, no. 1, p. 5, 2013.
80. N. A. de Weerd and T. Nguyen, "The interferons and their receptors-distribution and regulation," Immunology and Cell Biology, vol. 90, no. 5, pp. 483-491, 2012.
81. R. N. Veedu and J. Wengel, "Locked nucleic acids: promising nucleic acid analogs for therapeutic applications," Chemistry and Biodiversity, vol. 7, no. 3, pp. 536-542, 2010.
82. M. Sen and J. R. Grandis, "Nucleic acid-based approaches to STAT inhibition," JAK-STAT, vol. 1, no. 4, pp. 285-291, 2014.
83. B. Vester and J. Wengel, "LNA (locked nucleic acid): highaffinity targeting of complementary RNA and DNA," Biochemistry, vol. 43, no. 42, pp. 13233-13241, 2004.
84. H. Kaur, B. R. Babu, and S. Maiti, "Perspective on chemistry and therapeutic applications of locked nucleic acid (LNA)," Chemical Reviews, vol. 107, no. 11, pp. 4672-4697, 2007.
85. W. Jeong, A. Rapisarda, S. R. Park et al., "Pilot trial of EZN-2968, an antisense oligonucleotide inhibitor of hypoxia-inducible factor-1 (HIF-1), in patients with refractory solid tumors," Cancer Chemotherapy and Pharmacology, vol. 73,no. 2, pp. 343-348, 2014.
86. J. Zhao, Q. Lin, K. J. Kim et al., "Ngn1 inhibits astrogliogenesis through induction of miR-9 during neuronal fate specification," eLife, vol. 4, Article IDe06885, 2015.