NDRG2 as a marker protein for brain astrocytes

Cell and Tissue Research

Volumn 357, Issue 1, 2014, Pages 31-41

  Flügge, Gabriele ^a,b   Araya Callis, Carolina ^a   Garea Rodriguez, Enrique ^a,b   Stadelmann Nessler, Christine ^b   Fuchs, Eberhard ^a,b  

^a GERMAN PRIMATE CENTER   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Astrocyte; GFAP; NDRG2; Reactive astrocyte; S100

Indexed keywords

AQUAPORIN 4; CELL PROTEIN; CHONDROITIN SULFATE PROTEOGLYCAN 4; GLIAL FIBRILLARY ACIDIC PROTEIN; N MYC DOWNREGULATED GENE 2 PROTEIN; NESTIN; PROTEOCHONDROITIN SULFATE; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; NDR2 PROTEIN, MOUSE; NDRG2 PROTEIN, RAT; NERVE PROTEIN; PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTONOMIC NERVOUS SYSTEM; BRAIN DAMAGE; BRAIN REGION; CALLITHRIX; CAUDATE NUCLEUS; CELL LABELING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSOL; FEMALE; GABAERGIC SYSTEM; GLUTAMATERGIC NERVE CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MICROSCOPY; MOUSE; MUELLER CELL; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SCANDENTIA; WHITE MATTER; ANIMAL; BRAIN; C57BL MOUSE; GENETICS; HUMAN; METABOLISM; WISTAR RAT;

MAMMALIA; MARMOSETS; RATTUS; TUPAIIDAE;

ANIMALS; ASTROCYTES; BIOLOGICAL MARKERS; BRAIN; CALLITHRIX; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; PROTEINS; RATS; RATS, WISTAR; TUPAIA;

EID: 84904717229     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1837-5     Document Type: Article

References (54)

1. Adami C, Sorci G, Blasi E, Agneletti AL, Bistoni F, Donato R (2001) S100B expression in and effects on microglia. Glia 33:131-142 (Pubitemid 32160976)
2. Annett LE, Rogers DC, Hernandez TD, Dunnett SB (1992) Behavioural analysis of unilateral monoamine depletion in the marmoset. Brain 115:825-856
3. Annett LE, Torres EM, Ridley RM, Baker HF, Dunnett SB (1995) A comparison of the behavioural effects of embryonic nigral grafts in the caudate nucleus and in the putamen ofmarmosets with unilateral 6-OHDA lesions. Exp Brain Res 103:355-371
4. Araque A, Parpura V, Sanzgiri RP, Haydon PG (1999) Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208-215 (Pubitemid 29202082)
5. Araya-Callís C, Hiemke C, Abumaria N, Flugge G (2012) Chronic psychosocial stress and citalopram modulate the expression of the glial proteins GFAP and NDRG2 in the hippocampus. Psychopharmacology (Berl) 224:209-222
6. Banasr M, Chowdhury GM, Terwilliger R, Newton SS, Duman RS, Behar KL, Sanacora G (2010) Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol Psychiatry 15:501-511
7. Bellamy TC (2006) Interactions between Purkinje neurones and Bergmann glia. Cerebellum 5:116-126
8. Bramanti V, Tomassoni D, Avitabile M, Amenta F, Avola R (2010) Biomarkers of glial cell proliferation and differentiation in culture. Front Biosci (Schol Ed) 2:558-570
9. Bringmann A, Grosche A, Pannicke T, Reichenbach A (2013) GABA and glutamate uptake and metabolism in retinal glial (Müller) cells. Front Endocrinol (Lausanne) 4:48. doi:10.3389/fendo.2013.00048
10. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192 (Pubitemid 34033496)
11. Czéh B, Fuchs E, Flügge G (2013) Altered glial plasticity in animal models for mood disorders. Curr Drug Targets 14:1249-1261
12. Deng Y, Yao L, Chau L, Ng SS, Peng Y, Liu X, Au WS, Wang J, Li F, Ji S, Han H, Nie X, Li Q, Kung HF, Leung SY, Lin MC (2003) N-Myc downstream-regulated gene 2 (NDRG2) inhibits glioblastoma cell proliferation. Int J Cancer 106:342-347 (Pubitemid 36870394)
13. Foletta VC, Prior MJ, Stupka N, Carey K, Segal DH, Jones S, Swinton C, Martin S, Cameron-Smith D, Walder KR (2009) NDRG2, a novel regulator of myoblast proliferation, is regulated by anabolic and catabolic factors. J Physiol 587(Pt7):1619-1634
14. Fuchs E, Corbach-Söhle S (2010) Tree shrews. In: Hubrecht R, Kirkwood J (eds) The UFAW handbook on the care and management of laboratory animals and other research animals. Wiley-Blackwell, Chichester, pp 262-275
15. Haydon PG (2001) Glia: listening and talking to the synapse. Nat Rev Neurosci 2:185-193
16. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009-1031 (Pubitemid 44033387)
17. Hendrickson A, Troilo D, Possin D, Springer A (2006) Development of the neural retina and its vasculature in the marmoset Callithrix jacchus. J Comp Neurol 497:270-286 (Pubitemid 43825431)
18. Hu XL, Liu XP, Deng YC, Lin SX, Wu L, Zhang J, Wang LF, Wang XB, Li X, Shen L, Zhang YQ, Yao LB (2006) Expression analysis of the NDRG2 gene inmouse embryonic and adult tissues. Cell Tissue Res 325:67-76 (Pubitemid 44124299)
19. Hwang J, Kim Y, Kang HB, Jaroszewski L, Deacon AM, Lee H, Choi WC, Kim KJ, Kim CH, Kang BS, Lee JO, Oh TK, Kim JW, Wilson IA, Kim MH (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
20. Kim YJ, Yoon SY, Kim JT, Choi SC, Lim JS, Kim JH, Song EY, Lee HG, Choi I, Kim JW (2009) NDRG2 suppresses cell proliferation through down-regulation of AP-1 activity in human colon carcinoma cells. Int J Cancer 124:7-15
21. Kim WR, Kim JY, Moon Y, Kim HJ, Kim H, Sun W (2012) Regional difference of reactive astrogliosis following traumatic brain injury revealed by hGFAP-GFP transgenic mice. Neurosci Lett 513:155-159
22. Lavialle M, Aumann G, Anlauf E, Prols F, Arpin M, Derouiche A (2011) Structural plasticity of perisynaptic astrocyte processes involves ezrin and metabotropic glutamate receptors. Proc Natl Acad Sci USA 108:12915-12919
23. Lepekhin EA, Eliasson C, Berthold CH, Berezin V, Bock E, Pekny M (2001) Intermediate filaments regulate astrocyte motility. J Neurochem 79:617-625 (Pubitemid 33029935)
24. Lewis GP, Fisher SK (2003) Up-regulation of glial fibrillary acidic protein in response to retinal injury: its potential role in glial remodeling and a comparison to vimentin expression. Int Rev Cytol 230:263-290 (Pubitemid 37517867)
25. Li Y, Yang J, Li S, Zhang J, Zheng J, Hou W, Zhao H, Guo Y, Liu X, Dou K, Situ Z, Yao L (2011) N-myc downstream-regulated gene 2, a novel estrogen-targeted gene, is involved in the regulation of Na+/K+-ATPase. J Biol Chem 286:32289-32299
26. Messing A, Brenner M (2003) GFAP: functional implications gleaned from studies of genetically engineered mice. Glia 43:87-90 (Pubitemid 36781701)
27. Miguel-Hidalgo JJ, Waltzer R, Whittom AA, Austin MC, Rajkowska G, Stockmeier CA (2010) Glial and glutamatergic markers in depression, alcoholism, and their comorbidity. J Affect Disord 127:230-240
28. Mitura A, Liebert F, Schlumbohm C, Fuchs E (2012) Improving the energy and nutrient supply for common marmoset monkeys fed under long-term laboratory conditions. J Med Primatol 41:82-88
29. Muller MB, Lucassen PJ, Yassouridis A, Hoogendijk WJ, Holsboer F, Swaab DF (2001) Neither major depression nor glucocorticoid treatment affects the cellular integrity of the human hippocampus. Eur J Neurosci 14:1603-1612 (Pubitemid 35478029)
30. Nichols NR (2003) Ndrg2, a novel gene regulated by adrenal steroids and antidepressants, is highly expressed in astrocytes. Ann NY Acad Sci 1007:349-356
31. Okuda T, Kondoh H (1999) Identification of new genes ndr2 and ndr3 which are related to Ndr1/RTP/Drg1 but show distinct tissue specificity and response to N-myc. Biochem Biophys Res Commun 266: 208-215 (Pubitemid 30028793)
32. Okuda T, Kokame K, Miyata T (2008) Differential expression patterns of NDRG family proteins in the central nervous system. J Histochem Cytochem 56:175-182 (Pubitemid 351170969)
33. Paxinos G, Franklin K (2008) Themouse brain in stereotaxic coordinates, 3rd edn. Academic, San Diego
34. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic, San Diego
35. Pekny M, Pekna M (2004) Astrocyte intermediate filaments in CNS pathologies and regeneration. J Pathol 204:428-437 (Pubitemid 39468154)
36. Pellerin L, Magistretti PJ (1997) Glutamate uptake stimulates Na+, K+ -ATPase activity in astrocytes via activation of a distinct subunit highly sensitive to ouabain. J Neurochem 69: 2132-2137 (Pubitemid 27452761)
37. Raponi E, Agenes F, Delphin C, Assard N, Baudier J, Legraverend C, Deloulme JC (2007) S100B expression defines a state in which GFAP-expressing cells lose their neural stem cell potential and acquire a more mature developmental stage. Glia 55:165-177 (Pubitemid 46036463)
38. Reichenbach A, Derouiche A, Kirchhoff F (2010) Morphology and dynamics of perisynaptic glia. Brain Res Rev 63:11-25
39. Ribic A, Flügge G, Schlumbohm C, Mätz-Rensing K, Walter L, Fuchs E (2011) Activity-dependent regulation of MHC class I expression in the developing primary visual cortex of the common marmoset monkey. Behav Brain Funct 7:1. doi:10.1186/1744-9081-7-1
40. Rickmann M, Wolff JR (1995a) Modifications of S100-protein immunoreactivity in rat brain induced by tissue preparation. Histochem Cell Biol 103:135-145
41. Rickmann M, Wolff JR (1995b) S100 protein expression in subpopulations of neurons of rat brain. Neuroscience 67:977-991
42. Singh S, Metz I, Amor S, van der Valk P, Stadelmann C, Brück W (2013) Microglial nodules in early multiple sclerosis white matter are associated with degenerating axons. Acta Neuropathol 125:595-608
43. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647
44. Sosunov AA, Guilfoyle E, Wu X, McKhann GM, Goldman JE (2013) Phenotypic conversions of "protoplasmic" to "reactive" astrocytes in Alexander disease. J Neurosci 33:7439-7450
45. Stephan H, Baron G, Schwerdtfeger WK (1980) The brain of the common marmoset (Callithrix jacchus). A stereotaxic atlas, Springer, Berlin
46. Stockmeier CA, Mahajan GJ, Konick LC, Overholser JC, Jurjus GJ, Meltzer HY, Uylings HB, Friedman L, Rajkowska G (2004) Cellular changes in the post mortem hippocampus in major depression. Biol Psychiatry 56:640-650 (Pubitemid 39446845)
47. Takahashi K, Yamada M, Ohata H, Honda K, Yamada M (2005) Ndrg2 promotes neurite outgrowth of NGF-differentiated PC12 cells. Neurosci Lett 388:157-162 (Pubitemid 41208212)
48. Takeichi T, Takarada-Iemata M, Hashida K, Sudo H, Okuda T, Kokame K, Hatano T, Takanashi M, Funabe S, Hattori N, Kitamura O, Kitao Y, Hori O (2011) The effect of Ndrg2 expression on astroglial activation. Neurochem Int 59:21-27
49. Tigges J, Shanta TR (1969) A stereotaxic brain atlas of the tree shrew (Tupaia glis). Williams and Wilkins, Baltimore
50. Wachter B, Schürger S, Rolinger J, von Ameln-Mayerhofer A, Berg D, Wagner HJ, Kueppers E (2010) Effect of 6-hydroxydopamine (6-OHDA) on proliferation of glial cells in the rat cortex and striatum: evidence for de-differentiation of resident astrocytes. Cell Tissue Res 342:147-160
51. Wanner IB, Anderson MA, Song B, Levine J, Fernandez A, Gray-Thompson Z, Ao Y, Sofroniew MV (2013) Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury. J Neurosci 33:12870-12886
52. Wielpütz MO, Lee IH, Dinudom A, Boulkroun S, Farman N, Cook DI, Korbmacher C, Rauh R (2007) NDRG2 stimulates amiloridesensitive Na+ currents in Xenopus laevis oocytes and fisher rat thyroid cells. J Biol Chem 282:28264-28273 (Pubitemid 47529528)
53. Zhang J, Li F, Liu X, Shen L, Liu J, Su J, Zhang W, Deng Y, Wang L, Liu N, Han W, Zhang J, Ji S, Yang A, Han H, Yao L (2006) The repression of human differentiation-related geneNDRG2 expression by Myc via Miz-1-dependent interaction with the NDRG2 core promoter. J Biol Chem 281:39159-39168 (Pubitemid 46041876)
54. Zhu H, Zhao J, Zhou W, Li H, Zhou R, Zhang L, Zhao H, Cao J, Zhu X, Hu H, Ma G, He L, Yao Z, Yao L, Guo X (2012) Ndrg2 regulates vertebral specification in differentiating somites. Dev Biol 369:308-318