Omi/HtrA2 is relevant to the selective vulnerability of striatal neurons in Huntington's disease

European Journal of Neuroscience

Volumn 28, Issue 1, 2008, Pages 30-40

  Inagaki, Reina ^a   Tagawa, Kazuhiko ^a   Qi, Mei Ling ^a   Enokido, Yasushi ^a   Ito, Hikaru ^a   Tamura, Takuya ^a   Shimizu, Shigeomi ^a   Oyanagi, Kityomitsu ^b   Arai, Nobutaka ^b   Kanazawa, Ichiro ^c   Wanker, Erich E ^d   Okazawa, Hitoshi ^a,b,e  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Cell death; Huntingtin; Huntington's disease; Mitochondria; Omi HtrA2; Polyglutamine

Indexed keywords

ADENOVIRUS VECTOR; ATAXIN 1; HUNTINGTIN; SERINE PROTEINASE OMI; HD PROTEIN, HUMAN; HUNTINGTON PROTEIN, MOUSE; MITOCHONDRIAL PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; SERINE PROTEINASE; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; HUMAN; HUNTINGTON CHOREA; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TRANSGENIC MOUSE; ANIMAL; CELL CULTURE; CYTOLOGY; GENETICS; HOMEOSTASIS; METABOLISM; MICROARRAY ANALYSIS; PATHOLOGY; WISTAR RAT;

ANIMALS; CELL DEATH; CELLS, CULTURED; CORPUS STRIATUM; HOMEOSTASIS; HUMANS; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; MICROARRAY ANALYSIS; MITOCHONDRIAL PROTEINS; NERVE TISSUE PROTEINS; NEURONS; NUCLEAR PROTEINS; RATS; RATS, WISTAR; RNA, SMALL INTERFERING; SERINE ENDOPEPTIDASES;

EID: 54049152861     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06323.x     Document Type: Article

References (32)

1. Bass, S., Gu, Q. & Christen, A. (1996) Multicopy suppressors of Pre mutant Escherichia coli include two HtrA (DegP) proteases homologs (HhoAB), DksA, and a truncated RlpA. J. Bacteriol., 178, 1154-1161.
2. Chao, J.-R., Parganas, E., Boyd, K., Hong, C.Y., Opferman, J.T. &Ihle, J.N. (2008) Hax1-mediated processing of HtrA2 by Parl allows survival of lymphocytes and neurons. Nature, 452, 98-102.
3. Clausen, T., Southan, C. & Ehrmann, M. (2002) The HtrA family of proteases: implication for protein composition and cell fate. Mol. Cell, 10, 443-455.
4. Colin, E., Regulier, E., Perrin, V., Durr, A., Brice, A., Aebischer, P., Deglon, N., Humbert, S. & Saudou, F. (2005) Akt is altered in an animal model of Huntington's disease and in patients. Eur. J. Neurosci., 21, 1478-1488.
5. Gupta, S., Singh, R., Datta, P., Zhang, Z., Orr, C., Lu, Z., Dubois, G., Zervos, A.S., Meisler, M.H., Srinivasula, S.M., Fernaddes-Alnemri, T. & Alnemri, E.S. (2004) The C-terminal tail of presenilin regulates Omi/HtrA2 protease activity. J. Biol. Chem, 279, 45844-45854.
6. Hegde, R., Srinivasula, S.M., Zhang, Z., Wassel, R., Mukattash, R., Cilenti, L., Dubois, G., Lazebnik, Y., Zervos, A.S., Fernandes-Alnemri, T. & Alnemri, E.S. (2002) Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem., 277, 432-438.
7. Hoshino, M., Tagawa, K., Okuda, T., Murata, M., Oyanagi, K., Arai, N., Mizutani, T., Kanazawa, I., Wanker, E.E. & Okazawa, H. (2003) Histone deacetylase activity is retained in primary neurons expressing mutant huntingtin protein. J. Neurochem., 87, 257-267.
8. Hoshino, M., Tagawa, K., Okuda, T. & Okazawa, H. (2004) Transcriptional repression by polyglutamine disease is not directly linked to the presence of inclusion bodies. Biochem. Biophys. Res. Commun., 313, 110-116.
9. Hoshino, M., Qi, M.L., Yoshimura, N., Miyashita, T., Tagawa, K., Wada, Y.-i., Enokido, Y., Marubuchi, S., Harjes, P., Arai, N., Oyanagi, K., Blandino, G., Sudol, M., Rich, T., Kanazawa, I., Wanker, E.E., Saitoe, M. &Okazawa, H. (2006) Transcriptional repression induces a slowly progressive atypical neuronal death associated with changes of YAP isoforms and p73. J. Cell Biol., 172, 589-604.
10. Humbert, S., Bryson, E.A., Cordelieres, F.P., Connors, N.C., Datta, S.R., Finkbeiner, S., Greenberg, M.E. & Saudou, F. (2002) The IGF-1/Akt pathway is neuroprotective in Huntington's disease and involves Huntingtin phosphorylation by Akt. Dev. Cell, 2, 831-837.
11. Jones, J.M., Albin, R.L., Feldman, E.L., Simin, K., Schuster, T.G., Dunnick, W.A., Collins, J.T., Chrisp, C.E., Taylor, B.A. & Meisler, M.H. (1993) mnd2: a new mouse model of inherited motor neuron disease. Genomics, 16, 669-677.
12. Jones, J.M., Datta, P., Srinivasa, S.M., Jl, W., Gupta, S., Zhang, Z., Davies, E., Hajnoczky, G., Saunders, T.L., van Keuren, M.L., Fernandes-Alnemri, T., Meisler, M.H. & Alnemri, E.S. (2003) Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice. Nature, 425, 721-727.
13. Li, H., Li, S.H., Johnston, H., Shelbourne, P.F. & Li, X.J. (2000) Amino- terminal fragments of mutant huntingtin show selective accumulation in striatal neurons and synaptic toxicity. Nat. Genet., 25, 385-389.
14. Li, W., Srinivasula, S.M., Chain, J., Li, P., Wu, J.W., Zhang, Z., Alnemri, E.S. & Shi, Y. (2002) Structural insights into the pro-apoptotic function of mitochondrial serine protease HtrA2/Omi. Nat. Struct. Biol., 9, 436-441.
15. Martins, L.M., Iaccarino, I., Tenev, T., Gschmeissner, S., Totty, N.F., Lemoine, N.R., Savopoulos, J., Gray, C.W., Creasy, C.L., Dingwall, C. & Downward, J. (2002) The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a Reaper-like motif. J. Biol. Chem., 277, 439-444.
16. Martins, L.M., Morrison, A., Klupsch, K., Fedele, V., Moisoi, N., Teismann, P., Abuin, A., Grau, E., Geppert, M., Livi, G.P., Creasy, C.L., Martin, A., Hargreaves, I., Heals, S.J., Okada, H., Brandner, S., Schulz, J.B., Mak, T. & Downward, J. (2004) Neuroprotective role of the reaper-related serine protease HtrA2/Omi revealed by targeted deletion in mice. Mol. Cell. Biol., 24, 9848-9862.
17. Migheli, A., Atzori, C., Piva, R., Tortarolo, M., Girelli, M., Schiffer, D. & Bendotti,C. (1999) Lack of apoptosis in mice with ALS. Nat. Med., 5,966-967. Okazawa, H., Rich, T., Chang, A., Lin, X., Waragai, M., Kajikawa, M., Enokido, Y., Komuo, A., Kato, S., Shibata, M., Hatanaka, H., Mouradian, M.M., Sudol, M. & Kanazawa, I. (2002) Interaction between mutant ataxin-1 and PQBP-1 affects transcription and cell death. Neuron, 34, 701-713.
18. Pardo, P., Colin, E., Regulier, E., Aebischer, P., Deglon, N., Humbert, S. & Saudou, F. (2006) Inhibition of calcineurin by FK506 protects against polyglutamine-huntingtin toxicity through an increase of huntingtin phos- phorylation at S421. J. Neurosci., 26, 1635-1645.
19. Qi, Y., Hoshino, M., Wada, Y., Marubuchi, S., Yoshimura, N., Kanazawa, I., Shinomiya, K. & Okazawa, H. (2005) PQBP-1 is expressed predominantly in the central nervous system during development. Eur. J. Neurosci., 22, 1277-1286.
20. Rathke-Hartlieb, S., Schlomann, U., Heimann, P., Meisler, M.H., Jockusch, H. & Bartsch, J.W. (2002) Progressive loss of striatal neurons causes motor dysfunction in MND2 mutant mice and is not prevented by bcl-2. Exp. Neurol., 175, 87-97.
21. Sittler, A., Lurz, R., Lueder, G., Priller, J., Lehrach, H., Hayer-Hartl, M.K., Hartl, F.U. &Wanker, E.E. (2001) Geldanamycin activates a heat shock response and inhibits huntingtin aggregation in a cell culture model of Huntington's disease. Hum. Mol. Genet., 10, 1307-1315.
22. Spiess, C., Beil, A. & Ehrmann, M. (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell, 97, 339-347.
23. Strauss, K.M., Martins, L.M., Plun-Favreau, H., Marx, F.P., Kautzmann, S., Berg, D., Gasser, T., Wszolek, Z., Miiller, T., Bornemann, A., Wolburg, H., Downward, J., Riess, O., Schulz, J.B. & Kruger, R. (2005) Loss of function mutations in the gene encoding Omi/HtrA2 in Parkinson's disease. Hum. Mol. Genet., 14, 2099-2111.
24. Suzuki, Y., Imai, Y., Nakayama, H., Takahashi, K., Takio, K. & Takahashi, R. (2001) A serine protease, HtrA2 is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell, 8, 613-621.
25. Tagawa, K., Hoshino, M., Okuda, T., Ueda, H., Hayashi, H., Engemann, S., Okado, H., Ichikawa, M., Wanker, E.E. & Okazawa, H. (2004) Distinct aggregation and cell death patterns among different types of primary neurons induced by mutant huntingtin protein. J. Neurochem., 89, 974-0987.
26. Tagawa, K., Marubuchi, S., Qi, M.-L., Enokido, Y., Tamura, T., Inagaki, R., Murata, M., Kanazawa, I., Wanker, E.E. & Okazawa, H. (2007) The induction levels of hsp70 differentiate the vulnerabilities to mutant huntingtin among neuronal subtypes. J. Neurosci., 27, 868-880.
27. Tsujimoto, Y., Nakagawa, T. & Shimizu, S. (2006) Mitochondrial membrane potential permeability transition and cell death. Biochem. Biophys. Acta., 1757, 1297-1300.
28. Turmaine, M., Raza, A., Mahal, A., Mangiarini, L., Bates, G.P. & Davies, S.W. (2000) Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease. Proc. Natl Acad. Sci. USA, 97, 8093-8097.
29. Verhagen, A.M., Silke, J., Ekert, P.G., Pakusch, M., Kaufmann, H., Connolly, L.M., Day, C.L., Tikoo, A., Burke, R., Wrobel, C., Moritz, R.L., Simpson,
30. R.J. & Vaux, D.L. (2002) HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem., 277, 445-454.
31. Waragai, M., Claas-Hinrich, L., Takeuchi, S., Imafuku, I., Udagawa, Y., Kanazawa, I., Kawabata, M., Mouradian, M.M. & Okazawa, H. (1999) PQBP-1, a novel polyglutamine tract-binding protein, inhibits transcription activation by Brn-2 and affects cell survival. Hum. Mol. Genet., 8, 97-987.
32. Warby, S.C., Chan, E.Y., Metzler, M., Gan, L., Singaraja, R.R., Crocker, S.F., Robertson, H.A. & Hayden, M.R. (2005) Huntingtin phosphorylation on serine 421 is significantly reduced in the striatum and by polyglutamine expansion in vivo. Hum. Mol. Genet., 14, 1569-1577.