Caspase-9 activation revealed by semaphorin 7A cleavage is independent of apoptosis in the aged olfactory bulb

Journal of Neuroscience

Volumn 29, Issue 36, 2009, Pages 11385-11392

  Ohsawa, Shizue ^a   Hamada, Shun ^c   Asou, Hiroaki ^d   Kuida, Keiuke ^e   Uchiyama, Yasuo ^f   Yoshida, Hiroki ^g   Miura, Masayuki ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c FUKUOKA WOMEN'S UNIVERSITY   (Japan)

^d TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^e VERTEX PHARMACEUTICALS   (United States)

^f JUNTENDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g SAGA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 9; PROCASPASE 3; SEMAPHORIN; SEMAPHORIN 7A; UNCLASSIFIED DRUG;

AGE DISTRIBUTION; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN MATURATION; CELL ACTIVATION; CELL COUNT; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL NECROSIS; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DETERMINATION; PROTEIN EXPRESSION;

AGING; ANIMALS; ANTIGENS, CD; APOPTOSIS; CASPASE 9; ENZYME ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OLFACTORY BULB; SEMAPHORINS; SUBSTRATE SPECIFICITY;

EID: 70349149472     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4780-08.2009     Document Type: Article

References (41)

1. Bartzokis G (2004) Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer's disease. Neurobiol Aging 25:5-18; author reply 49-62.
2. Cain WS, Stevens JC (1989) Uniformity of olfactory loss in aging. Ann N Y Acad Sci 561:29-38.
3. Doty RL, Shaman P, Applebaum SL, Giberson R, Siksorski L, Rosenberg L (1984) Smell identification ability: changes with age. Science 226:1441-1443. (Pubitemid 15161278)
4. D'Sa C, Klocke BJ, Cecconi F, Lindsten T, Thompson CB, Korsmeyer SJ, Flavell RA, Roth KA (2003) Caspase regulation of genotoxin-induced neural precursor cell death. J Neurosci Res 74:435-445. (Pubitemid 37362820)
5. D'Sa-Eipper C, Leonard JR, Putcha G, Zheng TS, Flavell RA, Rakic P, Kuida K, Roth KA (2001) DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3. Development 128:137-146. (Pubitemid 32097941)
6. Fujita E, Egashira J, Urase K, Kuida K, Momoi T (2001) Caspase-9 processing by caspase-3 via a feedback amplification loop in vivo. Cell Death Differ 8:335-344. (Pubitemid 32409604)
7. Galvan V, Gorostiza OF, Banwait S, Ataie M, Logvinova AV, Sitaraman S, Carlson E, Sagi SA, Chevallier N, Jin K, Greenberg DA, Bredesen DE (2006) Reversal of Alzheimer's-like pathology and behavior in human APP transgenic mice by mutation of Asp664. Proc Natl Acad Sci U S A 103:7130-7135.
8. Inoue H, Tsukita K, Iwasato T, Suzuki Y, Tomioka M, Tateno M, Nagao M, Kawata A, Saido TC, Miura M, Misawa H, Itohara S, Takahashi R (2003) The crucial role of caspase-9 in the disease progression of a transgenic ALS mouse model. EMBO J 22:6665-6674. (Pubitemid 38009612)
9. Jacobson MD, Weil M, Raff MC (1997) Programmed cell death in animal development. Cell 88:347-354. (Pubitemid 27131376)
10. Kanuka H, Hisahara S, Sawamoto K, Shoji S, Okano H, Miura M (1999) Proapoptotic activity of Caenorhabditis elegans CED-4 protein in Drosophila: implicated mechanisms for caspase activation. Proc Natl Acad Sci U S A 96:145-150.
11. Kempermann G, Wiskott L, Gage FH (2004) Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186-191.
12. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K, Uchiyama Y (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172:454-469. (Pubitemid 351282032)
13. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, Flavell RA (1996) Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372. (Pubitemid 26408520)
14. Kumar S (2004) Migrate, differentiate, proliferate, or die: pleiotropic functions of an apical "apoptotic caspase." Sci STKE 2004:pe49.
15. Kumar S (2007) Caspase function in programmed cell death. Cell Death Differ 14:32-43. (Pubitemid 44911892)
16. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN (2006) Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating Drosophila sensory neuron dendrite pruning. Neuron 51:283-290.
17. Kuranaga E, Miura M (2007) Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 17:135-144. (Pubitemid 46341825)
18. Kuranaga E, Kanuka H, Tonoki A, Takemoto K, Tomioka T, Kobayashi M, Hayashi S, Miura M (2006) Drosophila IKK-related kinase regulates nonapoptotic function of caspases via degradation of IAPs. Cell 126:583-596.
19. Lu DC, Rabizadeh S, Chandra S, Shayya RF, Ellerby LM, Ye X, Salvesen GS, Koo EH, Bredesen DE (2000) A second cytotoxic proteolytic peptide derived from amyloid beta-protein precursor. Nat Med 6:397-404. (Pubitemid 30208156)
20. Lüthi AU, Martin SJ (2007) The CASBAH: a searchable database of caspase substrates. Cell Death Differ 14:641-650.
21. Maruyama T, Matsuura M, Suzuki K, Yamamoto N (2008) Cooperative activity of multiple upper layer proteins for thalamocortical axon growth. Dev Neurobiol 68:317-331. (Pubitemid 351263622)
22. Mine T, Harada K, Matsumoto T, Yamana H, Shirouzu K, Itoh K, Yamada A (2000) CDw108 expression during T-cell development. Tissue Antigens 55:429-436.
23. Mirich JM, Williams NC, Berlau DJ, Brunjes PC (2002) Comparative study of aging in the mouse olfactory bulb. J Comp Neurol 454:361-372. (Pubitemid 35416797)
24. Miura M, Yuan J (1996) Mechanisms of programmed cell death in Caenorhabditis elegans and vertebrates. Curr Top Dev Biol 32:139-174.
25. Nakanishi K, Maruyama M, Shibata T, Morishima N (2001) Identification of a caspase-9 substrate and detection of its cleavage in programmed cell death during mouse development. J Biol Chem 276:41237-41244. (Pubitemid 37373281)
26. Ohsawa S, Hamada S, Kakinuma Y, Yagi T, Miura M (2005) Novel function of neuronal PAS domain protein 1 in erythropoietin expression in neuronal cells. J Neurosci Res 79:451-458. (Pubitemid 40283344)
27. Ohsawa S, Hamada S, Yoshida H, Miura M (2008a) Caspase-mediated changes in histone H1 in early apoptosis: prolonged caspase activation in developing olfactory sensory neurons. Cell Death Differ 15:1429-1439.
28. Ohsawa S, Watanabe T, Katada T, Nishina H, Miura M (2008b) Novel antibody to human BASP1 labels apoptotic cells post-caspase activation. Biochem Biophys Res Commun 371:639-643.
29. Pasterkamp RJ, Peschon JJ, Spriggs MK, Kolodkin AL (2003) Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424:398-405.
30. Pasterkamp RJ, Kolk SM, Hellemons AJ, Kolodkin AL (2007) Expression patterns of semaphorin7A and plexinC1 during rat neural development suggest roles in axon guidance and neuronal migration. BMC Dev Biol 7:98.
31. Seki T, Arai Y (1991) Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat Embryol (Berl) 184:395-401.
32. Seki T, Arai Y (1993) Highly polysialylated neural cell adhesion molecule (NCAM-H) is expressed by newly generated granule cells in the dentate gyrus of the adult rat. J Neurosci 13:2351-2358. (Pubitemid 23151752)
33. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ (1999) Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 144:281-292.
34. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES (1998) Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell 1:949-957.
35. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J, Lee RA, Robbins PD, Fernandes-Alnemri T, Shi Y, Alnemri ES (2001) A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410:112-116. (Pubitemid 32225846)
36. Suzuki K, Okuno T, Yamamoto M, Pasterkamp RJ, Takegahara N, Takamatsu H, Kitao T, Takagi J, Rennert PD, Kolodkin AL, Kumanogoh A, Kikutani H (2007) Semaphorin 7A initiates T-cell-mediated inflammatory responses through alpha1beta1 integrin. Nature 446:680-684. (Pubitemid 46606878)
37. Suzuki Y, Nakabayashi Y, Takahashi R (2001) Ubiquitin-protein ligase activity of X-linked inhibitor of apoptosis protein promotes proteasomal degradation of caspase-3 and enhances its anti-apoptotic effect in Fas-induced cell death. Proc Natl Acad Sci U S A 98:8662-8667. (Pubitemid 32678084)
38. Takemoto K, Nagai T, Miyawaki A, Miura M (2003) Spatio-temporal activation of caspase revealed by indicator that is insensitive to environmental effects. J Cell Biol 160:235-243. (Pubitemid 36254957)
39. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, Houtzager VM, Nordstrom PA, Roy S, Vaillancourt JP, Chapman KT, Nicholson DW (1997) A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 272:17907-17911. (Pubitemid 27306365)
40. Williams DW, Kondo S, Krzyzanowska A, Hiromi Y, Truman JW (2006) Local caspase activity directs engulfment of dendrites during pruning. Nat Neurosci 9:1234-1236. (Pubitemid 44454262)
41. Yoshida H, Kong YY, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, Mak TW (1998) Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739-750. (Pubitemid 28436006)