Molecules and Cells

  • 제44권4호
  • /
  • Pages.233-244
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  • 2021
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  • 1016-8478(pISSN)
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  • 0219-1032(eISSN)
한국분자세포생물학회 (Korean Society for Molecular and Cellular Biology)
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Kapd Is Essential for Specification of the Dopaminergic Neurogenesis in Zebrafish Embryos

  • Jung, Jangham (Department of Life Science, BK21 Plus Program, Graduate School, Chungnam National University) ;
  • Kim, Eunhee (Department of Biological Sciences, College of Bioscience and Biotechnology, Chungnam National University) ;
  • Rhee, Myungchull (Department of Life Science, BK21 Plus Program, Graduate School, Chungnam National University)
  • 투고 : 2021.01.07
  • 심사 : 2021.02.22
  • 발행 : 2021.04.30
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초록

To define novel networks of Parkinson's disease (PD) pathogenesis, the substantia nigra pars compacta of A53T mice, where a death-promoting protein, FAS-associated factor 1 was ectopically expressed for 2 weeks in the 2-, 4-, 6-, and 8-month-old mice, and was subjected to transcriptomic analysis. Compendia of expression profiles and a hierarchical clustering heat map of differentially expressed genes associated with PD were bioinformatically generated. Transcripts level of a particular gene was fluctuated by 20, 60, and 0.75 fold in the 4-, 6-, and 8-month-old mice compared to the 2 months old. Because the gene contained Kelch domain, it was named as Kapd (Kelch-containing protein associated with PD). Biological functions of Kapd were systematically investigated in the zebrafish embryos. First, transcripts of a zebrafish homologue of Kapd, kapd were found in the floor plate of the neural tube at 10 h post fertilization (hpf), and restricted to the tegmentum, hypothalamus, and cerebellum at 24 hpf. Second, knockdown of kapd caused developmental defects of DA progenitors in the midbrain neural keel and midbrain-hindbrain boundary at 10 hpf. Third, overexpression of kapd increased transcripts level of the dopaminergic immature neuron marker, shha in the prethalamus at 16.5 hpf. Finally, developmental consequences of kapd knockdown reduced transcripts level of the markers for the immature and mature DA neurons, nkx2.2, olig2, otx2b, and th in the ventral diencephalon of the midbrain at 18 hpf. It is thus most probable that Kapd play a key role in the specification of the DA neuronal precursors in zebrafish embryos.

키워드

과제정보

This research was funded by the National Research Foundation of Korea Government Grant (NRF-2020R1A2C101409911). I would like to thank Dr. Boksuk Kim for his invaluable support in the experiments of FAF1 overexpression at the SNpc of A53T mice.

참고문헌

  1. Al Oustah, A., Danesin, C., Khouri-Farah, N., Farreny, M.A., Escalas, N., Cochard, P., Glise, B., and Soula, C. (2014). Dynamics of sonic hedgehog signaling in the ventral spinal cord are controlled by intrinsic changes in source cells requiring sulfatase 1. Development 141, 1392-1403. https://doi.org/10.1242/dev.101717
  2. Arenas, E. (2014). Wnt signaling in midbrain dopaminergic neuron development and regenerative medicine for Parkinson's disease. J. Mol. Cell Biol. 6, 42-53. https://doi.org/10.1093/jmcb/mju001
  3. Bai, C.B., Auerbach, W., Lee, J.S., Stephen, D., and Joyner, A.L. (2002). Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 129, 4753-4761. https://doi.org/10.1242/dev.129.20.4753
  4. Barth, K.A. and Wilson, S.W. (1995). Expression of zebrafish nk2.2 is influenced by sonic hedgehog/vertebrate hedgehog-1 and demarcates a zone of neuronal differentiation in the embryonic forebrain. Development 121, 1755-1768. https://doi.org/10.1242/dev.121.6.1755
  5. Bomont, P., Cavalier, L., Blondeau, F., Hamida, C.B., Belal, S., Tazir, M., Demir, E., Topaloglu, H., Korinthenberg, R., Landrieu, P., et al. (2000). The gene encoding gigaxonin, a new member of the cytoskeletal BTB/kelch repeat family, is mutated in giant axonal neuropathy. Nat. Genet. 26, 370-374. https://doi.org/10.1038/81701
  6. Borodovsky, N., Ponomaryov, T., Frenkel, S., and Levkowitz, G. (2009). Neural protein Olig2 acts upstream of the transcriptional regulator Sim1 to specify diencephalic dopaminergic neurons. Dev. Dyn. 238, 826-834. https://doi.org/10.1002/dvdy.21894
  7. Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T.M., Rubenstein, J.L.R., and Ericson, J. (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398, 622-627. https://doi.org/10.1038/19315
  8. Chin, K.T., Xu, H.T., Ching, Y.P., and Jin, D.Y. (2007). Differential subcellular localization and activity of kelch repeat proteins KLHDC1 and KLHDC2. Mol. Cell. Biochem. 296, 109-119. https://doi.org/10.1007/s11010-006-9304-6
  9. Ciruna, B., Jenny, A., Lee, D., Mlodzik, M., and Schier, A.F. (2006). Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439, 220-224. https://doi.org/10.1038/nature04375
  10. Clarke, J. (2009). Role of polarized cell divisions in zebrafish neural tube formation. Curr. Opin. Neurobiol. 19, 134-138. https://doi.org/10.1016/j.conb.2009.04.010
  11. Del Giacco, L., Pistocchi, A., Cotelli, F., Fortunato, A.E., and Sordino, P. (2008). A peek inside the neurosecretory brain through Orthopedia lenses. Dev. Dyn. 237, 2295-2303. https://doi.org/10.1002/dvdy.21668
  12. Dhanoa, B.S., Cogliati, T., Satish, A.G., Bruford, E.A., and Friedman, J.S. (2013). Update on the Kelch-like (KLHL) gene family. Hum. Genomics 7, 1-7. https://doi.org/10.1186/1479-7364-7-1
  13. Di Fonzo, A., Dekker, M.C.J., Montagna, P., Baruzzi, A., Yonova, E.H., Guedes, L.C., Szczerbinska, A., Zhao, T., DubbelHulsman, L.O.M., de Graaff, E., et al. (2009). FBXO7 mutations cause autosomal recessive, early-onset parkinsonian-pyramidal syndrome. Neurology 72, 240-245. https://doi.org/10.1212/01.wnl.0000338144.10967.2b
  14. Duncan, R.N., Panahi, S., Piotrowski, T., and Dorsky, R.I. (2015). Identification of Wnt genes expressed in neural progenitor zones during zebrafish brain development. PLoS One 10, e0145810. https://doi.org/10.1371/journal.pone.0145810
  15. Ertzer, R., Muller, F., Hadzhiev, Y., Rathnam, S., Fischer, N., Rastegar, S., and Strahle, U. (2007). Cooperation of sonic hedgehog enhancers in midline expression. Dev. Biol. 301, 578-589. https://doi.org/10.1016/j.ydbio.2006.11.004
  16. Fearnley, J.M. and Lees, A.J. (1991). Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114, 2283-2301. https://doi.org/10.1093/brain/114.5.2283
  17. Filippi, A., Mahler, J., Schweitzer, J., and Driever, W. (2010). Expression of the paralogous tyrosine hydroxylase encoding genes th1 and th2 reveals the full complement of dopaminergic and noradrenergic neurons in zebrafish larval and juvenile brain. J. Comp. Neurol. 518, 423-438. https://doi.org/10.1002/cne.22213
  18. Forno, L.S. (1969). Concentric hyalin intraneuronal inclusions of Lewy type in the brains of elderly persons (50 incidental cases): relationship to parkinsonism. J. Am. Geriatr. Soc. 17, 557-575. https://doi.org/10.1111/j.1532-5415.1969.tb01316.x
  19. Galvin, J.E., Lee, V.M.Y., and Trojanowski, J.Q. (2001). Synucleinopathies: clinical and pathological implications. Arch. Neurol. 58, 186-190. https://doi.org/10.1001/archneur.58.2.186
  20. Gao, K., Deng, X., Zheng, W., Song, Z., Zhu, A., Xiu, X., and Deng, H. (2013). Genetic analysis of the FBXO42 gene in Chinese Han patients with Parkinson's disease. BMC Neurol. 13, 125. https://doi.org/10.1186/1471-2377-13-125
  21. Giasson, B.I., Jakes, R., Goedert, M., Duda, J.E., Leight, S., Trojanowski, J.Q., and Lee, V.M. (2000). A panel of epitope-specific antibodies detects protein domains distributed throughout human α-synuclein in lewy bodies of Parkinson's disease. J. Neurosci. Res. 59, 528-533. https://doi.org/10.1002/(SICI)1097-4547(20000215)59:4<528::AID-JNR8>3.0.CO;2-0
  22. Glinka, A., Wu, W., Delius, H., Monaghan, A.P., Blumenstock, C., and Niehrs, C. (1998). Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction. Nature 391, 357-362. https://doi.org/10.1038/34848
  23. Golbe, L.I., Di Iorio, G., Bonavita, V., Miller, D.C., and Duvoisin, R.C. (1990). A large kindred with autosomal dominant Parkinson's disease. Ann. Neurol. 27, 276-282. https://doi.org/10.1002/ana.410270309
  24. Guner, B. and Karlstrom, R.O. (2007). Cloning of zebrafish nkx6. 2 and a comprehensive analysis of the conserved transcriptional response to Hedgehog/Gli signaling in the zebrafish neural tube. Gene Expr. Patterns 7, 596-605. https://doi.org/10.1016/j.modgep.2007.01.002
  25. Hassler, R. (1938). Zur Pathologie der Paralysis agitans und des postenzephalitischen Parkinsonismus. J. Psychol. Neurol. 48, 387-476. German.
  26. Hegarty, S.V., Sullivan, A.M., and O'keeffe, G.W. (2013). Midbrain dopaminergic neurons: a review of the molecular circuitry that regulates their development. Dev. Biol. 379, 123-138. https://doi.org/10.1016/j.ydbio.2013.04.014
  27. Hill-Burns, E.M., Ross, O.A., Wissemann, W.T., Soto-Ortolaza, A.I., Zareparsi, S., Siuda, J., Lynch, T., Wszolek, Z.K., Silburn, P.A., Ritz, B., et al. (2016). Identification of genetic modifiers of age-at-onset for familial Parkinson's disease. Hum. Mol. Genet. 25, 3849-3862. https://doi.org/10.1093/hmg/ddw206
  28. Holzschuh, J., Hauptmann, G., and Driever, W. (2003). Genetic analysis of the roles of Hh, FGF8, and nodal signaling during catecholaminergic system development in the zebrafish brain. J. Neurosci. 23, 5507-5519. https://doi.org/10.1523/jneurosci.23-13-05507.2003
  29. Jacobs, F.M., van Erp, S., van der Linden, A.J., von Oerthel, L., Burbach, J.P.H., and Smidt, M.P. (2009). Pitx3 potentiates Nurr1 in dopamine neuron terminal differentiation through release of SMRT-mediated repression. Development 136, 531-540. https://doi.org/10.1242/dev.029769
  30. Jessell, T.M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29. https://doi.org/10.1038/35049541
  31. Jung, J., Choi, I., Ro, H., Huh, T.L., Choe, J., and Rhee, M. (2020). march5 Governs the convergence and extension movement for organization of the telencephalon and diencephalon in zebrafish embryos. Mol. Cells 43, 76. https://doi.org/10.14348/molcells.2019.0210
  32. Kanehisa, M. and Sato, Y. (2020). KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci. 29, 28-35. https://doi.org/10.1002/pro.3711
  33. Klein, C. and Westenberger, A. (2012). Genetics of Parkinson's disease. Cold Spring Harb. Perspect. Med. 2, a008888. https://doi.org/10.1101/cshperspect.a008888
  34. Laale, H.W. (1977). The biology and use of zebrafish, Brachydanio rerio in fisheries research. A literature review. J. Fish Biol. 10, 121-173. https://doi.org/10.1111/j.1095-8649.1977.tb04049.x
  35. Lewis, J.L., Bonner, J., Modrell, M., Ragland, J.W., Moon, R.T., Dorsky, R.I., and Raible, D.W. (2004). Reiterated Wnt signaling during zebrafish neural crest development. Development 131, 1299-1308. https://doi.org/10.1242/dev.01007
  36. Liem, K.F., Jr., Tremml, G., Roelink, H., and Jessell, T.M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82, 969-979. https://doi.org/10.1016/0092-8674(95)90276-7
  37. Mesman, S., von Oerthel, L., and Smidt, M.P. (2014). Mesodiencephalic dopaminergic neuronal differentiation does not involve GLI2A-mediated SHH-signaling and is under the direct influence of canonical WNT signaling. PLoS One 9, e97926. https://doi.org/10.1371/journal.pone.0097926
  38. Moury, J.D. and Jacobson, A.G. (1990). The origins of neural crest cells in the axolotl. Dev. Biol. 141, 243-253. https://doi.org/10.1016/0012-1606(90)90380-2
  39. Nguyen, V.H., Schmid, B., Trout, J., Connors, S.A., Ekker, M., and Mullins, M.C. (1998). Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirlpathway of genes. Dev. Biol. 199, 93-110. https://doi.org/10.1006/dbio.1998.8927
  40. Okumura, F., Fujiki, Y., Oki, N., Osaki, K., Nishikimi, A., Fukui, Y., Nakatsukasa, K., and Kamura, T. (2020). Cul5-type ubiquitin ligase KLHDC1 contributes to the elimination of truncated SELENOS produced by failed UGA/Sec decoding. iScience 23, 100970. https://doi.org/10.1016/j.isci.2020.100970
  41. Park, H.C., Mehta, A., Richardson, J.S., and Appel, B. (2002). olig2 is required for zebrafish primary motor neuron and oligodendrocyte development. Dev. Biol. 248, 356-368. https://doi.org/10.1006/dbio.2002.0738
  42. Polymeropoulos, M.H., Higgins, J.J., Golbe, L.I., Johnson, W.G., Ide, S.E., Di Iorio, G., Sanges, G., Stenroos, E., Pho, L.T., Schaffer, A.A., et al. (1996). Mapping of a gene for Parkinson's disease to chromosome 4q21-q23. Science 274, 1197-1199. https://doi.org/10.1126/science.274.5290.1197
  43. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., et al. (1997). Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047. https://doi.org/10.1126/science.276.5321.2045
  44. Russek-Blum, N., Gutnick, A., Nabel-Rosen, H., Blechman, J., Staudt, N., Dorsky, R.I., Houart, C., and Levkowitz, G. (2008). Dopaminergic neuronal cluster size is determined during early forebrain patterning. Development 135, 3401-3413. https://doi.org/10.1242/dev.024232
  45. Ryu, S.W., Chae, S.K., Lee, K.J., and Kim, E. (1999). Identification and characterization of human Fas associated factor 1, hFAF1. Biochem. Biophys. Res. Commun. 262, 388-394. https://doi.org/10.1006/bbrc.1999.1217
  46. Sherman, B.T. and Lempicki, R.A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44. https://doi.org/10.1038/nprot.2008.211
  47. Simeone, A., Di Salvio, M., Di Giovannantonio, L.G., Acampora, D., Omodei, D., and Tomasetti, C. (2011). The role of otx2 in adult mesencephalic-diencephalic dopaminergic neurons. Mol. Neurobiol. 43, 107-113. https://doi.org/10.1007/s12035-010-8148-y
  48. Smeets, W.J.A.J. and Reiner, A. (1994). Catecholamines in the CNS of vertebrates: current concepts of evolution and functional significance. In Phylogeny and Development of Catecholamine Systems in the CNS of Vertebrates, W.J.A.J. Smeets and A. Reiner, eds. (Cambridge: Cambridge University Press), pp. 463-481.
  49. Stigloher, C., Ninkovic, J., Laplante, M., Geling, A., Tannhauser, B., Topp, S., Kikuta, H., Becker, T.S., Houart, C., and Bally-Cuif, L. (2006). Segregation of telencephalic and eye-field identities inside the zebrafish forebrain territory is controlled by Rx3. Development 133, 2925-2935. https://doi.org/10.1242/dev.02450
  50. Sul, J.W., Park, M.Y., Shin, J.H., Kim, Y.R., Yoo, S.E., Kong, Y.Y., Kwon, K.S., Lee, Y.H., and Kim, E. (2013). Accumulation of the parkin substrate, FAF1, plays a key role in the dopaminergic neurodegeneration. Hum. Mol. Genet. 22, 1558-1573. https://doi.org/10.1093/hmg/ddt006
  51. TeSlaa, J.J., Keller, A.N., Nyholm, M.K., and Grinblat, Y. (2013). Zebrafish Zic2a and Zic2b regulate neural crest and craniofacial development. Dev. Biol. 380, 73-86. https://doi.org/10.1016/j.ydbio.2013.04.033
  52. Tofaris, G.K. and Spillantini, M.G. (2007). Physiological and pathological properties of α-synuclein. Cell. Mol. Life Sci. 64, 2194-2201. https://doi.org/10.1007/s00018-007-7217-5
  53. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111. https://doi.org/10.1093/bioinformatics/btp120
  54. Villanueva, S., Glavic, A., Ruiz, P., and Mayor, R. (2002). Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction. Dev. Biol. 241, 289-301. https://doi.org/10.1006/dbio.2001.0485
  55. Wakabayashi, K., Tanji, K., Mori, F., and Takahashi, H. (2007). The Lewy body in Parkinson's disease: molecules implicated in the formation and degradation of α-synuclein aggregates. Neuropathology 27, 494-506. https://doi.org/10.1111/j.1440-1789.2007.00803.x
  56. Werner, A., Iwasaki, S., McGourty, C.A., Medina-Ruiz, S., Teerikorpi, N., Fedrigo, I., Ingolia, N.T., and Rape, M. (2015). Cell-fate determination by ubiquitin-dependent regulation of translation. Nature 525, 523-527. https://doi.org/10.1038/nature14978
  57. Yu, C., Kim, B.S., and Kim, E. (2016). FAF1 mediates regulated necrosis through PARP1 activation upon oxidative stress leading to dopaminergic neurodegeneration. Cell Death Differ. 23, 1873-1885. https://doi.org/10.1038/cdd.2016.99