Induction of clusterin Expression by Neuronal Cell Death in Zebrafish

Yun-Mi Jeong; Tae-Eun Jin; Jung-Hwa Choi; Mi-Sun Lee; Hyun-Taek Kim; Kyu-Seok Hwang; Doo-Sang Park; Hyun-Woo Oh; Joong-Kook Choi; Vladimir Korzh; Melitta Schachner; Kwan-Hee You; Cheol-Hee Kim

doi:10.1016/j.jgg.2014.08.007

Volume 41 Issue 11

Nov. 2014

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Article Navigation > Journal of Genetics and Genomics > 2014 > 41(11): 583-589

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Induction of clusterin Expression by Neuronal Cell Death in Zebrafish

doi: 10.1016/j.jgg.2014.08.007

a
Department of Biology, Chungnam National University, Daejeon 305-764, Republic of Korea
b
Korea Research Institute of Bioscience and Biotechnology, Daejeon 305-333, Republic of Korea
c
Department of Biochemistry, College of Medicine, Chungbuk National University, Cheongju 361–763, Republic of Korea
d
Institute of Molecular and Cell Biology, Agency for Science, Technology and Research, Singapore
e
Keck Center for Collaborative Neuroscience and Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ 08854-8082, USA
f
Center for Neuroscience, Shantou University Medical College, Shantou 515041, China

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Corresponding author: E-mail address: Schachner@biology.rutgers.edu (Melitta Schachner); E-mail address: khyou@cnu.ac.kr (Kwan-Hee You); E-mail address: zebrakim@cnu.ac.kr (Cheol-Hee Kim)
Received Date: 2014-05-26
Accepted Date: 2014-08-30
Rev Recd Date: 2014-08-18

Available Online: 2014-09-30

Publish Date: 2014-11-20

Abstract

Abstract

Clusterin, a protein associated with multiple functions, is expressed in a wide variety of mammalian tissues. Although clusterin is known to be involved in neurodegenerative diseases, ageing, and tumorigenesis, a detailed analysis of the consequences of gain- or loss-of-function approaches has yet to be performed to understand the underlying mechanisms of clusterin functions. Since clusterin levels change in neurological diseases, it is likely that clusterin contributes to cell death and degeneration in general. Zebrafish was investigated as a model system to study human diseases. During development, zebrafish clusterin was expressed in the notochord and nervous system. Embryonic overexpression of clusterin by mRNA microinjection did not affect axis formation, whereas its knock-down by anti-sense morpholino treatment resulted in neuronal cell death. To analyze the function of clusterin in neurodegeneration, a transgenic zebrafish was investigated, in which nitroreductase expression is regulated under the control of a neuron-specific huC promoter which is active between the stages of early neuronal precursors and mature neurons. Nitroreductase turns metronidazole into a cytotoxic agent that induces cell death within 12 h. After metronidazole treatment, transgenic zebrafish showed neuron-specific cell death. Interestingly, we also observed a dramatic induction of clusterin expression in the brain and spinal cord in these fish, suggesting a direct or indirect role of clusterin in neuronal cell death and thus, more generally, in neurodegeneration.
- Clusterin,
- Neuronal cell death,
- Neurodegeneration,
- Zebrafish

These authors contributed equally to this work.

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References(39)

References

[1]	Aronow, B.J., Lund, S.D., Brown, T.L. et al. Apolipoprotein J expression at fluid-tissue interfaces: potential role in barrier cytoprotection Proc. Natl. Acad. Sci. USA, 90 (1993),pp. 725-729
[2]	Awatramani, R., Soriano, P., Rodriguez, C. et al. Cryptic boundaries in roof plate and choroid plexus identified by intersectional gene activation Nat. Genet., 35 (2003),pp. 70-75
[3]	Bettuzzi, S. Chapter 1: Introduction Adv. Cancer Res., 104 (2009),pp. 1-8
[4]	Blaschuk, O., Burdzy, K., Fritz, I.B. Purification and characterization of a cell-aggregating factor (Clusterin), the major glycoprotein in ram rete testis fluid J. Biol. Chem., 258 (1983),pp. 7714-7720
[5]	Charnay, Y., Imhof, A., Vallet, P.G. et al. Clusterin expression during fetal and postnatal CNS development in mouse Neuroscience, 155 (2008),pp. 714-724
[6]	Charnay, Y., Imhof, A., Vallet, P.G. et al. Clusterin in neurodegenerative diseases: molecular perspectives and clinical relevance Brain Res. Bull., 88 (2012),pp. 434-443
[7]	Chung, A.Y., Kim, P.S., Kim, S. et al. Generation of demyelination models by targeted ablation of oligodendrocytes in the zebrafish CNS Mol. Cells, 36 (2013),pp. 82-87
[8]	Curado, S., Anderson, R.M., Jungblut, B. et al. Conditional targeted cell ablation in zebrafish: a new tool for regeneration studies Dev. Dyn., 236 (2007),pp. 1025-1035
[9]	Davison, J.M., Akitake, C.M., Goll, M.G. et al. Transactivation from Gal4-VP16 transgenic insertions for tissue-specific cell labeling and ablation in zebrafish Dev. Biol., 304 (2007),pp. 811-824
[10]	Del Bigio, M.R. Ependymal cells: biology and pathology Acta Neuropathol., 119 (2010),pp. 55-73
[11]	de Silva, H.V., Stuart, W.D., Park, Y.B. et al. Purification and characterization of apolipoprotein J J. Biol. Chem., 265 (1990),pp. 14292-14297
[12]	Guo, S. Linking genes to brain, behavior and neurological diseases: what can we learn from zebrafish? Genes Brain Behav., 3 (2004),pp. 63-74
[13]	Hunter, N.L., Dymecki, S.M. Molecularly and temporally separable lineages form the hindbrain roof plate and contribute differentially to the choroid plexus Development, 134 (2007),pp. 3449-3460
[14]	Humphreys, D., Hochgrebe, T.T., Easterbrook-Smith, S.B. et al. Effects of clusterin overexpression on TNFalpha- and TGFbeta-mediated death of L929 cells Biochemistry, 36 (1997),pp. 15233-15243
[15]	Jiao, S., Dai, W., Lu, L. et al. The conserved clusterin gene is expressed in the developing choroid plexus under the regulation of notch but not IGF signaling in zebrafish Endocrinology, 152 (2011),pp. 1860-1871
[16]	Jones, S.E., Jomary, C. Clusterin Int. J. Biochem. Cell Biol., 34 (2002),pp. 427-431
[17]	Kimmel, C.B., Ballard, W.W., Kimmel, S.R. et al. Stages of embryonic development of zebrafish Dev. Dyn., 203 (1995),pp. 253-310
[18]	Kimura, Y., Satou, C., Higashijima, S. V2a and V2b neurons are generated by the final divisions of pair-producing progenitors in the zebrafish spinal cord Development, 18 (2008),pp. 3001-3005
[19]	Kim, C.H., Ueshima, E., Muraoka, O. et al. Zebrafish elav/HuC homologue as a very early neuronal marker Neurosci. Lett., 216 (1996),pp. 109-112
[20]	Lee, S., Hong, S.W., Min, B.H. et al. Essential role of clusterin in pancreas regeneration Dev. Dyn., 240 (2011),pp. 605-615
[21]	Leskov, K.S., Klokov, D.Y., Li, J. et al. Synthesis and functional analyses of nuclear clusterin, a cell death protein J. Biol. Chem., 278 (2003),pp. 11590-11600
[22]	Michel, D., Chatelain, G., North, S. et al. Biochem. J., 328 (1997),pp. 45-50
[23]	Moro, E., Vettori, A., Porazzi, P. et al. Generation and application of signaling pathway reporter lines in zebrafish Mol. Genet. Genomics, 288 (2013),pp. 231-242
[24]	Nuutinen, T., Suuronen, T., Kauppinen, A. et al. Clusterin: a forgotten player in Alzheimer's disease Brain Res. Rev., 61 (2009),pp. 89-104
[25]	Peng, J., Zhang, J., Meng, A. The tiny zebrafish keep swimming fast in the developmental biology pond J. Genet. Genomics, 39 (2012),pp. 419-420
[26]	Přikrylová Vranová, H., Mareš, J., Nevrlý, M. et al. CSF markers of neurodegeneration in Parkinson's disease J. Neural. Transm., 117 (2010),pp. 1177-1181
[27]	Reddy, K.B., Jin, G., Karode, M.C. et al. Transforming growth factor beta (TGF beta)-induced nuclear localization of apolipoprotein J/clusterin in epithelial cells Biochemistry, 35 (1996),pp. 6157-6163
[28]	Rizzi, F., Coletta, M., Bettuzzi, S. Chapter 2: Clusterin (CLU): from one gene and two transcripts to many proteins Adv. Cancer Res., 104 (2009),pp. 9-23
[29]	Rizzi, F., Bettuzzi, S. The clusterin paradigm in prostate and breast carcinogenesis Endocr. Relat. Cancer, 17 (2010),pp. R1-R17
[30]	Sasaki, T., Kishi, S. Molecular and chemical genetic approaches to developmental origins of aging and disease in zebrafish Biochim. Biophys. Acta, 1832 (2013),pp. 1362-1370
[31]	Sensibar, J.A., Sutkowski, D.M., Raffo, A. et al. Prevention of cell death induced by tumor necrosis factor alpha in LNCaP cells by overexpression of sulfated glycoprotein-2 (clusterin) Cancer Res., 55 (1995),pp. 2431-2437
[32]	Sihlbom, C., Davidsson, P., Sjögren, M. et al. Structural and quantitative comparison of cerebrospinal fluid glycoproteins in Alzheimer's disease patients and healthy individuals Neurochem. Res., 33 (2008),pp. 1332-1340
[33]	Tang, M., Li, J., Liu, B. et al. Clusterin expression and human testicular seminoma Med. Hypotheses, 81 (2013),pp. 635-637
[34]	Thomas-Salgar, S., Millis, A.J. Clusterin expression in differentiating smooth muscle cells J. Biol. Chem., 269 (1994),pp. 17879-17885
[35]	Trougakos, I.P., Gonos, E.S. Clusterin/apolipoprotein J in human aging and cancer Int. J. Biochem. Cell Biol., 34 (2002),pp. 1430-1448
[36]	Trougakos, I.P., Lourda, M., Agiostratidou, G. et al. Differential effects of clusterin/apolipoprotein J on cellular growth and survival Free Radic. Biol. Med., 38 (2005),pp. 436-449
[37]	Xi, Y., Noble, S., Ekker, M. Modeling neurodegeneration in zebrafish Curr. Neurol. Neurosci. Rep., 11 (2011),pp. 274-282
[38]	Zellweger, T., Miyake, H., July, L.V. et al. Chemosensitization of human renal cell cancer using antisense oligonucleotides targeting the antiapoptotic gene clusterin Neoplasia, 3 (2001),pp. 360-367
[39]	Zhang, Q., Beltran, W.A., Mao, Z. et al. Invest. Ophthalmol. Vis. Sci., 44 (2003),pp. 4542-4549