Synaptic activity bidirectionally regulates a novel sequence-specific S-Q phosphoproteome in neurons

Journal of Neurochemistry

Volumn 128, Issue 6, 2014, Pages 841-851

  Siddoway, Benjamin ^a   Hou, Hailong ^a   Yang, Hongtian ^a   Petralia, Ronald ^b   Xia, Houhui ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

L type calcium channels; Phosphoproteomics; phosphorylation; SQ motif; synaptic activity

Indexed keywords

ATM PROTEIN; BICUCULLINE; CALCIUM CHANNEL L TYPE; GLUTAMINE; N METHYL DEXTRO ASPARTIC ACID; SERINE; THREONINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL VIABILITY; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; EMBRYO; ENZYME RELEASE; FEMALE; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; RAT; SYNAPSE; TRANSLATION INITIATION; UPREGULATION;

ATAXIA TELANGIECTASIA;

L-TYPE CALCIUM CHANNELS; PHOSPHOPROTEOMICS; PHOSPHORYLATION; SQ MOTIF; SYNAPTIC ACTIVITY;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; CEREBRAL CORTEX; ENZYME INHIBITORS; FEMALE; MALE; NEURONS; ORGAN CULTURE TECHNIQUES; PHOSPHOPROTEINS; PHOSPHORYLATION; PREGNANCY; PRIMARY CELL CULTURE; PROTEOME; PROTEOMICS; RATS; SODIUM CHANNEL BLOCKERS; SYNAPSES; TETRODOTOXIN;

EID: 84895927173     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12487     Document Type: Article

References (34)

1. Abraham R. T., (2004) PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways. DNA Repair 3, 883-887.
2. Ascoli G. A., Gasparini S., Medinilla V., and, Migliore M., (2010) Local control of postinhibitory rebound spiking in CA1 pyramidal neuron dendrites. J. Neurosci. 30, 6434-6442.
3. Barlow C., Hirotsune S., Paylor R., et al,. (1996) Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159-171.
4. Baumgartel K., and, Mansuy I. M., (2012) Neural functions of calcineurin in synaptic plasticity and memory. Learn Mem. 19, 375-384.
5. Boehrs J. K., He J., Halaby M. J., and, Yang D. Q., (2007) Constitutive expression and cytoplasmic compartmentalization of ATM protein in differentiated human neuron-like SH-SY5Y cells. J. Neurochem. 100, 337-345.
6. Borghesani P. R., Alt F. W., Bottaro A., et al,. (2000) Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc. Natl Acad. Sci. USA 97, 3336-3341.
7. Daniel J. A., Pellegrini M., Lee B. S., et al,. (2012) Loss of ATM kinase activity leads to embryonic lethality in mice. J. Cell Biol. 198, 295-304.
8. Deisseroth K., Mermelstein P. G., Xia H., and, Tsien R. W., (2003) Signaling from synapse to nucleus: the logic behind the mechanisms. Curr. Opin. Neurobiol. 13, 354-365.
9. Ditch S., and, Paull T. T., (2012) The ATM protein kinase and cellular redox signaling: beyond the DNA damage response. Trends Biochem. Sci. 37, 15-22.
10. Ehlers M. D., (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6, 231-242.
11. Fu A. K., Hung K. W., Fu W. Y., Shen C., Chen Y., Xia J., Lai K. O., and, Ip N. Y., (2011) APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat. Neurosci. 14, 181-189.
12. van Gorp A. G., van der Vos K. E., Brenkman A. B., et al,. (2009) AGC kinases regulate phosphorylation and activation of eukaryotic translation initiation factor 4B. Oncogene 28, 95-106.
13. Hoeffer C. A., and, Klann E., (2010) mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci. 33, 67-75.
14. Hou Q., Gilbert J., and, Man H. Y., (2011) Homeostatic regulation of AMPA receptor trafficking and degradation by light-controlled single-synaptic activation. Neuron 72, 806-818.
15. Jaworski J., and, Sheng M., (2006) The growing role of mTOR in neuronal development and plasticity. Mol. Neurobiol. 34, 205-219.
16. Kilkenny C., Browne W. J., Cuthill I. C., Emerson M., and, Altman D. G., (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8, e1000412.
17. Kulkarni A., and, Das K. C., (2008) Differential roles of ATR and ATM in p53, Chk1, and histone H2AX phosphorylation in response to hyperoxia: ATR-dependent ATM activation. Am. J. Physiol. 294, L998-L1006.
18. Li J., Han Y. R., Plummer M. R., and, Herrup K., (2009) Cytoplasmic ATM in neurons modulates synaptic function. Curr. Biol. 19, 2091-2096.
19. Lim D. S., Kirsch D. G., Canman C. E., Ahn J. H., Ziv Y., Newman L. S., Darnell R. B., Shiloh Y., and, Kastan M. B., (1998) ATM binds to beta-adaptin in cytoplasmic vesicles. Proc. Natl Acad. Sci. USA 95, 10146-10151.
20. Lisman J., Schulman H., and, Cline H., (2002) The molecular basis of CaMKII function in synaptic and behavioural memory. Nat. Rev. 3, 175-190.
21. Liu Y., Formisano L., Savtchouk I., Takayasu Y., Szabo G., Zukin R. S., and, Liu S. J., (2010) A single fear-inducing stimulus induces a transcription-dependent switch in synaptic AMPAR phenotype. Nat. Neurosci. 13, 223-231.
22. Malenka R. C., and, Nicoll R. A,. (1999) Long-term potentiation-a decade of progress? Science 285, 1870-1874.
23. Matsuoka S., Ballif B. A., Smogorzewska A,. et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166.
24. Petralia R. S., Wang Y. X., Hua F., Yi Z., Zhou A., Ge L., Stephenson F. A., and, Wenthold R. J., (2010) Organization of NMDA receptors at extrasynaptic locations. Neuroscience 167, 68-87.
25. Sarkaria J. N., Tibbetts R. S., Busby E. C., Kennedy A. P., Hill D. E., and, Abraham R. T., (1998) Inhibition of phosphoinositide 3-kinase related kinases by the radiosensitizing agent wortmannin. Cancer Res. 58, 4375-4382.
26. Shiloh Y., (2003) ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3, 155-168.
27. Stark D. T., and, Bazan N. G., (2011) Synaptic and extrasynaptic NMDA receptors differentially modulate neuronal cyclooxygenase-2 function, lipid peroxidation, and neuroprotection. J. Neurosci. 31, 13710-13721.
28. Stokes M. P., Rush J., Macneill J., et al,. (2007) Profiling of UV-induced ATM/ATR signaling pathways. Proc. Natl Acad. Sci. USA 104, 19855-19860.
29. Tian B., Yang Q., and, Mao Z., (2009) Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death. Nat. Cell Biol. 11, 211-218.
30. Wayman G. A., Lee Y. S., Tokumitsu H., Silva A. J., and, Soderling T. R., (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59, 914-931.
31. Wei F. Y., Tomizawa K., Ohshima T., et al,. (2005) Control of cyclin-dependent kinase 5 (Cdk5) activity by glutamatergic regulation of p35 stability. J. Neurochem. 93, 502-512.
32. Xu Y., Ashley T., Brainerd E. E., Bronson R. T., Meyn M. S., and, Baltimore D., (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10, 2411-2422.
33. Yamamoto K., Wang Y., Jiang W., Liu X., Dubois R. L., Lin C. S., Ludwig T., Bakkenist C. J., and, Zha S., (2012) Kinase-dead ATM protein causes genomic instability and early embryonic lethality in mice. J. Cell Biol. 198, 305-313.
34. Zucker R. S., (1999) Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 9, 305-313.