Contribution of serine racemase/d-serine pathway to neuronal apoptosis

Aging Cell

Volumn 11, Issue 4, 2012, Pages 588-598

  Esposito, Simona ^a   Pristerà, Andrea ^a   Maresca, Giovanna ^a   Cavallaro, Sebastiano ^b   Felsani, Armando ^a   Florenzano, Fulvio ^c   Manni, Luigi ^d   Ciotti, Maria T ^a   Pollegioni, Loredano ^e   Borsello, Tiziana ^f   Canu, Nadia ^a,g  

^a CNR   (Italy)

^b INSTITUTE OF NEUROLOGICAL SCIENCES   (Italy)

^c EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^d INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

^e UNIVERSITY OF INSUBRIA   (Italy)

^f MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^g UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Apoptosis; C Jun N terminal Kinase; Cerebellar granule neurons; d serine; Neuronal death; NMDA receptor; Proteasome; Serine racemase

Indexed keywords

DEXTRO SERINE; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; RACEMASE; RNA; SERINE RACEMASE; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL DEATH; CEREBELLAR GRANULE NEURON; DOWN REGULATION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; APOPTOSIS; CELL AGING; CEREBELLUM; JNK MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; PROTEASOME ENDOPEPTIDASE COMPLEX; RACEMASES AND EPIMERASES; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, MESSENGER; RNA, SMALL INTERFERING; SERINE; SIGNAL TRANSDUCTION; STEREOISOMERISM;

EID: 84864001287     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2012.00822.x     Document Type: Article

References (41)

1. Amadoro G, Serafino AL, Barbato C, Ciotti MT, Sacco A, Calissano P, Canu N (2004) Role of N-terminal tau domain integrity on the survival of cerebellar granule neurons. Cell Death Differ. 11, 217-230.
2. Bhave SV, Hoffman PL (1997) Ethanol promotes apoptosis in cerebellar granule cells by inhibiting the trophic effect of NMDA. J. Neurochem. 68, 578-586.
3. Borsello T, Clarke PG, Hirt L, Vercelli A, Repici M, Schorderet DF, Bogousslavsky J, Bonny C (2003) A peptide inhibitor of c-Jun N-terminal kinase protects against excitotoxicity and cerebral ischemia. Nat. Med. 9, 1180-1186.
4. Burgoyne RD, Cambray-Deakin MA (1988) The cellular neurobiology of neuronal development: the cerebellar granule cell. Brain Res. 472, 77-101.
5. Butts BD, Hudson HR, Linseman DA, Le SS, Ryan KR, Bouchard RJ, Heidenreich KA (2005) Proteasome inhibition elicits a biphasic effect on neuronal apoptosis via differential regulation of pro-survival and pro-apoptotic transcription factors. Mol. Cell. Neurosci. 30, 279-289.
6. Canu N, Barbato C, Ciotti MT, Serafino A, Dus L, Calissano P (2000) Proteasome involvement and accumulation of ubiquitinated proteins in cerebellar granule neurons undergoing apoptosis. J. Neurosci. 20, 589-599.
7. Canu N, Tufi R, Serafino AL, Amadoro G, Ciotti MT, Calissano P (2005) Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J. Neurochem. 92, 1228-1242.
8. De Miranda J, Panizzutti R, Foltyn VN, Wolosker H (2002) Cofactors of serine racemase that physiologically stimulate the synthesis of the N-methyl-D-aspartate (NMDA) receptor coagonist D-serine". PNAS 99, 14542-14547.
9. D'Mello SR (1998) Molecular regulation of neuronal apoptosis. Curr. Top. Dev. Biol. 39, 187-213.
10. D'Mello SR, Galli C, Ciotti T, Calissano P (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. PNAS 90, 10989-10993.
11. Dumin E, Bendikov I, Foltyn VN, Misumi Y, Ikehara Y, Kartvelishvily E, Wolosker H (2006) Modulation of D-serine levels via ubiquitin-dependent proteasomal degradation of serine racemase. J. Biol. Chem. 281, 20291-20302.
12. Foltyn VN, Bendikov I, De Miranda J, Panizzutti R, Dumin E, Shleper M, Li P, Toney MD, Kartvelishvily E, Wolosker H (2005) Serine racemase modulates intracellular D-serine levels through an alpha, beta-elimination activity. J. Biol. Chem. 280, 1754-1763.
13. Gallo V, Kingsbury A, Balázs R, Jørgensen OS (1987) The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. J. Neurosci. 7, 2203-2213.
14. Gamblin TC, Chen F, Abraha A, Miller R, Fu Y, Garcia-Sierra F, Lagalwar S, Berry RW, Binder LI, Cryns VL (2003) Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. PNAS 100, 10032-10037.
15. Hardingham GE (2006) Pro-survival signalling from the NMDAR. Biochem. Soc. Trans. 34, part 5, 936-938.
16. Harris C, Maroney AC, Johnson EM Jr (2002) Identification of JNK dependent and independent components of cerebellar granule neuron apoptosis. J. Neurochem. 83, 992-1001.
17. Hetman M, Kharebava G (2006) Survival signaling pathways activated by NMDARs. Curr. Top. Med. Chem. 6, 787-799.
18. Johnson JW, Ascher P (1990) Voltage-dependent block by intracellular Mg2+ of N-methyl-D-aspartate-activated channels. Biophys. J. 57, 1085-1090.
19. Kartvelishvily E, Shleper M, Balan L, Dumin E, Wolosker H (2006) Neuron-derived D-serine release provides a novel means to activate N-methyl-D-aspartate receptors. J. Biol. Chem. 281, 14151-14162.
20. Kim PM, Aizawa H, Kim PS, Huang AS, Wickramasinghe SR, Kashani AH, Barrow RK, Huganir RL, Ghosh A, Snyder SH (2005) Serine racemase: activation by glutamate neurotransmission via glutamate receptor interacting protein and mediation of neuronal migration. PNAS 102, 2105-2110.
21. Labrie V, Roder JC (2010) The involvement of the NMDA receptor D-serine/glycine site in the pathophysiology and treatment of schizophrenia. Neurosci. Biobehav. Rev. 34, 351-372.
22. Mellor JR, Merlo D, Jones A, Wisden W, Randall AD (1998) Mouse cerebellar granule cell differentiation: electrical activity regulates the GABA receptor alpha 6 subunit gene. J. Neurosci. 18, 2822-2833.
23. Monti B, Contestabile A (2000) Blockade of the NMDA receptor increases developmental apoptotic elimination of granule neurons and activates caspases in the rat cerebellum. Eur. J. Neurosci. 12, 3117-3123.
24. Mothet JP, Parent AT, Wolosker H, Brady RO Jr, Linden DJ, Ferris CD, Rogawski MA, Snyder SH (2000) D-serine is an endogenous ligand for the glycine site of the N-methyl-D-aspartate receptor. PNAS 297, 4926-4931.
25. Nardi N, Avidan G, Daily D, Zilkha-Falb R, Barzilai A (1997) Biochemical and temporal analysis of events associated with apoptosis induced by lowering the extracellular potassium concentration in mouse cerebellar granule neurons. J. Neurochem. 68, 750-759.
26. Pollegioni L, Sacchi S (2010) Metabolism of the neuromodulator D-serine. Cell. Mol. Life Sci. 67, 2387-2404.
27. Ryder EF, Cepko CL (1994) Migration patterns of clonally related granule cells and their progenitors in the developing chick cerebellum. Neuron 12, 1011-1028.
28. Sasabe J, Chiba T, Yamada M, Okamoto K, Nishimoto I, Matsuoka M, Aiso S (2007) D-serine is a key determinant of glutamate toxicity in amyotrophic lateral sclerosis. EMBO J. 26, 4149-4159.
29. Shao Z, Kamboj A, Anderson CM (2009) Functional and immunocytochemical characterization of D-serine transporters in cortical and astrocytes cultures. J. Neurosci. Res. 87, 2520-2530.
30. Shoji K, Mariotto S, Ciampa AR, Suzuki H (2006) Mutual regulation between serine and nitric oxide metabolism in human glioblastoma cells. Neurosci. Lett. 394, 163-167.
31. Sikka P, Walker R, Cockayne R, Wood MJ, Harrison PJ, Burnet PW (2010) D-Serine metabolism in C6 glioma cells: involvement of alanine-serine-cysteine transporter (ASCT2) and serine racemase (SR) but not D-amino acid oxidase (DAO). J. Neurosci. Res. 88, 1829-1840.
32. Stevens ER, Esguerra M, Kim PM, Newman EA, Snyder SH, Zahs KR, Miller RF (2003) D-Serine and serine racemase are present in the vertebrate retina and contribute to the physiological activation of NMDA receptors. PNAS 100, 6789-6794.
33. Tay AS, Hu LF, Lu M, Wong PT, Bian JS (2010) Hydrogen sulfide protects neurons against hypoxic injury via stimulation of ATP-sensitive potassium channel/protein kinase C/extracellular signal-regulated kinase/heat shock protein 90 pathway. Neuroscience 167, 277-286.
34. Turpin FR, Potier B, Dulong JR, Sinet PM, Alliot J, Oliet SH, Dutar P, Epelbaum J, Mothet JP, Billard JM (2011) Reduced serine racemase expression contributes to age-related deficits in hippocampal cognitive function. Neurobiol Aging. 32, 1495-1504.
35. Verrall L, Burnet PW, Betts JF, Harrison PJ (2010) The neurobiology of D-amino acid oxidase and its involvement in schizophrenia. Mol. Psychiatry. 15, 122-137.
36. Villalba M, Bockaert J, Journot L (1997) Concomitant induction of apoptosis and necrosis in cerebellar granule cells following serum and potassium withdrawal. NeuroReport 8, 981-985.
37. Wu S, Barger SW (2004) Induction of serine racemase by inflammatory stimuli is dependent on AP-1. Ann. N. Y. Acad. Sci. 1035, 133-146.
38. Xifro X, Malagelada C, Miñano A, Rodríguez-Alvarez J (2005) Brief exposure to NMDA produces long-term protection of cerebellar granule cells from apoptosis. Eur. J. Neurosci. 21, 827-840.
39. Yuan Z, Gong S, Luo J, Zheng Z, Song B, Ma S, Guo J, Hu C, Thiel G, Vinson C, Hu CD, Wang Y, Li M (2009) Opposing roles for ATF2 and c-Fos in c-Jun-mediated neuronal apoptosis. Mol. Cell. Biol. 29, 2431-2442.
40. Zhang FX, Rubin R, Rooney TA (1998) N-Methyl-D-aspartate inhibits apoptosis through activation of phosphatidylinositol 3-kinase in cerebellar granule neurons. A role for insulin receptor substrate-1 in the neurotrophic action of N-methyl-D-aspartate and its inhibition by ethanol. J. Biol. Chem. 273, 26596-26602.
41. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D (1998) Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J. Virol. 172, 9873-9880.