Deletion of N-myc downstream-regulated gene 2 attenuates reactive astrogliosis and inflammatory response in a mouse model of cortical stab injury

Journal of Neurochemistry

Volumn 130, Issue 3, 2014, Pages 374-387

  Takarada Iemata, Mika ^a,b   Kezuka, Dai ^a,b   Takeichi, Toshiaki ^c   Ikawa, Masahito ^d   Hattori, Tsuyoshi ^a,b   Kitao, Yasuko ^a,b   Hori, Osamu ^a,b  

^a KANAZAWA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c KANAZAWA MEDICAL UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

Author keywords

brain injury; inflammation; interleukin 6; neuronal death; reactive astrogliosis

Indexed keywords

CYTOPLASM PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 6; N MYC DOWNSTREAM REGULATED GENE 2 PROTEIN; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; ATTENUATION; BIOACCUMULATION; BRAIN INJURY; CELL MIGRATION; CELL PROLIFERATION; CHEMICAL ANALYSIS; CONTROLLED STUDY; CORTICAL STAB INJURY; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; MACROGLIA; MALE; MICROGLIA; MOUSE; N MYC DOWNSTREAM REGULATED GENE 2; NERVE CELL NECROSIS; NERVOUS SYSTEM INFLAMMATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACTIVATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

ADENOVIRIDAE; MUS;

BRAIN INJURY; INFLAMMATION; INTERLEUKIN-6; NEURONAL DEATH; REACTIVE ASTROGLIOSIS;

ANIMALS; ASTROCYTES; BRAIN INJURIES; CELL DEATH; CELLS, CULTURED; CEREBRAL CORTEX; COLFORSIN; DEPENDOVIRUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE DELETION; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOSIS; HEAD INJURIES, PENETRATING; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; WOUNDS, STAB;

EID: 84904614117     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12729     Document Type: Article

References (48)

1. Araque A., Parpura V., Sanzgiri R. P., and, Haydon P. G., (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22, 208-215.
2. Auguste K. I., Jin S., Uchida K., Yan D., Manley G. T., Papadopoulos M. C., and, Verkman A. S., (2007) Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J. 21, 108-116.
3. Bi F., Huang C., Tong J., et al,. (2013) Reactive astrocytes secrete lcn2 to promote neuron death. Proc. Natl Acad. Sci. USA 110, 4069-4074.
4. Boulkroun S., Fay M., Zennaro M. C., Escoubet B., Jaisser F., Blot-Chabaud M., Farman N., and, Courtois-Coutry N., (2002) Characterization of rat NDRG2 (N-Myc downstream regulated gene 2), a novel early mineralocorticoid-specific induced gene. J. Biol. Chem. 277, 31506-31515.
5. Brambilla R., Bracchi-Ricard V., Hu W. H., Frydel B., Bramwell A., Karmally S., Green E. J., and, Bethea J. R., (2005) Inhibition of astroglial nuclear factor kappaB reduces inflammation and improves functional recovery after spinal cord injury. J. Exp. Med. 202, 145-156.
6. Buffo A., Rite I., Tripathi P., Lepier A., Colak D., Horn A. P., Mori T., and, Götz M., (2008) Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc. Natl Acad. Sci. USA 105, 3581-3586.
7. Deng Y., Yao L., Chau L., et al,. (2003) N-Myc downstream-regulated gene 2 (NDRG2) inhibits glioblastoma cell proliferation. Int. J. Cancer 106, 342-347.
8. Foletta V. C., Prior M. J., Stupka N., Carey K., Segal D. H., Jones S., Swinton C., Martin S., Cameron-Smith D., and, Walder K. R., (2009) NDRG2, a novel regulator of myoblast proliferation, is regulated by anabolic and catabolic factors. J. Physiol. 1, 1619-1634.
9. Gadea A., Schinelli S., and, Gallo V., (2008) Endothelin-1 regulates astrocyte proliferation and reactive gliosis via a JNK/c-Jun signaling pathway. J. Neurosci. 28, 2394-2408.
10. Hashida K., Kitao Y., Sudo H., Awa Y., Maeda S., Mori K., Takahashi R., Iinuma M., and, Hori O., (2012) ATF6alpha promotes astroglial activation and neuronal survival in a chronic mouse model of Parkinson's disease. PLoS ONE 7, e47950.
11. Herrmann J. E., Imura T., Song B., Qi J., Ao Y., Nguyen T. K., Korsak R. A., Takeda K., Akira S., and, Sofroniew M. V., (2008) STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J. Neurosci. 28, 7231-7243.
12. Huang C., Han X., Li X., et al,. (2012) Critical role of connexin 43 in secondary expansion of traumatic spinal cord injury. J. Neurosci. 32, 3333-3338.
13. Hwang J., Kim Y., Kang H. B., et al,. (2011) Crystal structure of the human N-Myc downstream-regulated gene 2 protein provides insight into its role as a tumor suppressor. J. Biol. Chem. 286, 12450-12460.
14. Iadecola C., and, Nedergaard M., (2007) Glial regulation of the cerebral microvasculature. Nat. Neurosci. 10, 1369-1376.
15. Jeschke J., Van Neste L., Glöckner S. C., et al,. (2012) Biomarkers for detection and prognosis of breast cancer identified by a functional hypermethylome screen. Epigenetics 7, 701-709.
16. Kim A., Kim M. J., Yang Y., Kim J. W., Yeom Y. I., and, Lim J. S., (2009a) Suppression of NF-kappaB activity by NDRG2 expression attenuates the invasive potential of highly malignant tumor cells. Carcinogenesis 30, 927-936.
17. Kim Y. J., Yoon S. Y., Kim J. T., Choi S. C., Lim J. S., Kim J. H., Song E. Y., Lee H. G., Choi I., and, Kim J. W., (2009b) NDRG2 suppresses cell proliferation through down-regulation of AP-1 activity in human colon carcinoma cells. Int. J. Cancer 124, 7-15.
18. Kuwabara K., Matsumoto M., Ikeda J., et al,. (1996) Purification and characterization of a novel stress protein, the150-kDa oxygen-regulated protein (ORP150), from cultured rat astrocytes and its expression in ischemic mouse brain. J. Biol. Chem. 271, 5025-5032.
19. Li Y., Shen L., Cai L., Wang Q., Hou W., Wang F., Zeng Y., Zhao G., Yao L., and, Xiong L., (2011) Spatial-temporal expression of NDRG2 in rat brain after focal cerebral ischemia and reperfusion. Brain Res. 1382, 252-258.
20. Lusis E. A., Watson M. A., Chicoine M. R., Lyman M., Roerig P., Reifenberger G., Gutmann D. H., and, Perry A., (2005) Integrative genomic analysis identifies NDRG2 as a candidate tumor suppressor gene frequently inactivated in clinically aggressive meningioma. Cancer Res. 65, 7121-7126.
21. Mitchelmore C., Büchmann-Møller S., Rask L., West M. J., Troncoso J. C., and, Jensen N. A., (2004) NDRG2: a novel Alzheimer's disease associated protein. Neurobiol. Dis. 16, 48-58.
22. Murakami M., and, Hirano T., (2012) The pathological and physiological roles of IL-6 amplifier activation. Int. J. Biol. Sci. 8, 1267-1280.
23. Murray J. T., Campbell D. G., Morrice N., et al,. (2004) Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem. J. 384, 477-488.
24. Naudé P. J., Nyakas C., Eiden L. E., Ait-Ali D., van der Heide R., Engelborghs S., Luiten P. G., De Deyn P. P., den Boer J. A., and, Eisel U. L., (2012) Lipocalin 2: novel component of proinflammatory signaling in Alzheimer's disease. FASEB J. 26, 2811-2823.
25. Nichols N. R., (2003) Ndrg2, a novel gene regulated by adrenal steroids and antidepressants, is highly expressed in astrocytes. Ann. N. Y. Acad. Sci. 1007, 349-356.
26. Okada S., Nakamura M., Katoh H., et al,. (2006) Conditional ablation of Stat3 orSocs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat. Med. 12, 829-834.
27. Okuda T., Kokame K., and, Miyata T., (2008) Differential expression patterns of NDRG family proteins in the central nervous system. J. Histochem. Cytochem. 56, 175-182.
28. Park C., Cho I. H., Kim D., Jo E. K., Choi S. Y., Oh S. B., Park K., Kim J. S., and, Lee S. J., (2008) Toll-like receptor 2 contributes to glial cell activation and heme oxygenase-1 expression in traumatic brain injury. Neurosci. Lett. 431, 123-128.
29. Penkowa M., Giralt M., Carrasco J., Hadberg H., and, Hidalgo J., (2000) Impaired inflammatory response and increased oxidative stress and neurodegeneration after brain injury in interleukin-6-deficient mice. Glia 32, 271-285.
30. Qu X., Zhai Y., Wei H., Zhang C., Xing G., Yu Y., and, He F., (2002) Characterization and expression of three novel differentiation-related genes belong to the human NDRG gene family. Mol. Cell. Biochem. 229, 35-44.
31. Robel S., Bardehle S., Lepier A., Brakebusch C., and, Götz M., (2011a) Genetic deletion of cdc42 reveals a crucial role for astrocyte recruitment to the injury site in vitro and in vivo. J. Neurosci. 31, 12471-12482.
32. Robel S., Berninger B., and, Götz M., (2011b) The stem cell potential of glia: lessons from reactive gliosis. Nat. Rev. Neurosci. 12, 88-104.
33. Sasaki K., and, Miyazaki J., (1997) A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the cre transgene transmission. Biochem. Biophys. Res. Commun. 237, 318-324.
34. Schachtrup C., Ryu J. K., Helmrick M. J., Vagena E., Galanakis D. K., Degen J. L., Margolis R. U., and, Akassoglou K., (2010) Fibrinogen triggers astrocyte scar formation by promoting the availability of active TGF-beta after vascular damage. J. Neurosci. 30, 5843-5854.
35. Schummers J., Yu H., and, Sur M., (2008) Tuned responses of astrocytes and their influence on hemodynamic signals in the visual cortex. Science 320, 1638-1643.
36. Shimada I. S., LeComte M. D., Granger J. C., Quinlan N. J., and, Spees J. L., (2012) Self-renewal and differentiation of reactive astrocyte-derived neural stem/progenitor cells isolated from the cortical peri-infarct area after stroke. J. Neurosci. 32, 7926-7940.
37. Silver J., and, Miller J. H., (2004) Regeneration beyond the glial scar. Nat. Rev. Neurosci. 5, 146-156.
38. Sofroniew M. V., (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638-647.
39. Sofroniew M. V., and, Vinters H. V., (2010) Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
40. Sung B., Lim G., and, Mao J., (2003) Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats. J. Neurosci. 23, 2899-2910.
41. Takahashi K., Yamada M., Ohata H., Momose K., Higuchi T., Honda K., and, Yamada M., (2005a) Expression of Ndrg2 in the rat frontal cortex after antidepressant and electroconvulsive treatment. Int. J. Neuropsychopharmacol. 8, 381-389.
42. Takahashi K., Yamada M., Ohata H., Honda K., and, Yamada M., (2005b) Ndrg2 promotes neurite outgrowth of NGF-differentiated PC12 cells. Neurosci. Lett. 388, 157-162.
43. Takeichi T., Takarada-Iemata M., Hashida K., et al,. (2011) The effect of Ndrg2 expression on astroglial activation. Neurochem. Int. 59, 21-27.
44. van der Weerd L., Tariq Akbar M., Aron Badin R., Valentim L. M., Thomas D. L., Wells D. J., Latchman D. S., Gadian D. G., Lythgoe M. F., and, de Belleroche J. S., (2010) Overexpression of heat shock protein 27 reduces cortical damage after cerebral ischemia. J. Cereb. Blood Flow Metab. 30, 849-856.
45. Widestrand A., Faijerson J., Wilhelmsson U., Smith P. L., Li L., Sihlbom C., Eriksson P. S., and, Pekny M., (2007) Increased neurogenesis and astrogenesis from neural progenitor cells grafted in the hippocampus of GFAP-/- Vim-/- mice. Stem Cells 25, 2619-2627.
46. Zamanian J. L., Xu L., Foo L. C., Nouri N., Zhou L., Giffard R. G., and, Barres B. A., (2012) Genomic analysis of reactive astrogliosis. J. Neurosci. 32, 6391-6410.
47. Zhang S. J., Buchthal B., Lau D., Hayer S., Dick O., Schwaninger M., Veltkamp R., Zou M., Weiss U., and, Bading H., (2011) A signaling cascade of nuclear calcium-CREB-ATF3 activated by synaptic NMDA receptors defines a gene repression module that protects against extrasynaptic NMDA receptor-induced neuronal cell death and ischemic brain damage. J. Neurosci. 31, 4978-4990.
48. Zhu H., Zhao J., Zhou W., et al,. (2012) Ndrg2 regulates vertebral specification in differentiating somites. Dev. Biol. 369, 308-318.