Structural basis for the interaction of unstructured neuron specific substrates neuromodulin and neurogranin with calmodulin

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Kumar, Veerendra ^a   Chichili, Vishnu Priyanka Reddy ^a   Zhong, Ling ^c   Tang, Xuhua ^a   Velazquez Campoy, Adrian ^d,e   Sheu, Fwu Shan ^a   Seetharaman, J ^b   Gerges, Nashaat Z ^c   Sivaraman, J ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d UNIVERSITY OF ZARAGOZA   (Spain)

^e FUNDACIÓN ARAID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CALMODULIN; NEUROGRANIN; NEUROMODULIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; METABOLISM; MOLECULAR GENETICS; NERVE CELL; NUCLEAR MAGNETIC RESONANCE; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN UNFOLDING; RAT; SEQUENCE ALIGNMENT; SYNAPTIC TRANSMISSION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CALMODULIN; GAP-43 PROTEIN; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUROGRANIN; NEURONS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; RATS; SEQUENCE ALIGNMENT; SYNAPTIC TRANSMISSION;

EID: 84875147681     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep01392     Document Type: Article

References (52)

1. Andreasen, T. J., Luetje, C. W., Heideman, W. & Storm, D. R. Purification of a novel calmodulin binding protein from bovine cerebral cortex membranes. Biochemistry 22, 4615-8 (1983). (Pubitemid 13016989)
2. Neuner-Jehle, M.,Denizot, J. P.&Mallet, J. Neurogranin is locally concentrated in rat cortical and hippocampal neurons. Brain research 733, 149-54 (1996). (Pubitemid 26300971)
3. Clayton, D. F., George, J. M., Mello, C. V. & Siepka, S. M. Conservation and expression of IQ-domain-containing calpacitin gene products (neuromodulin/GAP-43, neurogranin/RC3) in the adult and developing oscine song control system. Developmental neurobiology 69, 124-40 (2009).
4. Xia, Z. & Storm, D. R. The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6, 267-76 (2005). (Pubitemid 40469981)
5. Shen, Y.,Mani, S., Donovan, S. L., Schwob, J. E. &Meiri, K. F. Growth-associated protein-43 is required for commissural axon guidance in the developing vertebrate nervous system. J Neurosci 22, 239-47 (2002). (Pubitemid 34033501)
6. Denny, J. B. Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr Neuropharmacol 4, 293-304 (2006). (Pubitemid 44524465)
7. Nelson, R. B. & Routtenberg, A. Characterization of protein F1 (47 kDa, 4.5 pI): a kinase C substrate directly related to neural plasticity. Exp Neurol 89, 213-24 (1985). (Pubitemid 15059519)
8. Hulo, S., Alberi, S., Laux, T., Muller, D. & Caroni, P. A point mutant of GAP-43 induces enhanced short-term and long-term hippocampal plasticity. Eur J Neurosci 15, 1976-82 (2002). (Pubitemid 35471887)
9. Routtenberg, A., Cantallops, I., Zaffuto, S., Serrano, P. & Namgung, U. Enhanced learning after genetic overexpression of a brain growth protein. Proc Natl Acad Sci USA 97, 7657-62 (2000). (Pubitemid 30431519)
10. Holahan, M. & Routtenberg, A. The protein kinase C phosphorylation site on GAP-43 differentially regulates information storage. Hippocampus 18, 1099-102 (2008).
11. Bernal, J., Rodriguez-Pena, A., Iniguez, M. A., Ibarrola, N. &Munoz, A. Influence of thyroid hormone on brain gene expression. Acta medica Austriaca 19 Suppl 1, 32-5 (1992).
12. Husson, M. et al. Triiodothyronine administration reverses vitamin A deficiencyrelated hypo-expression of retinoic acid and triiodothyronine nuclear receptors and of neurogranin in rat brain. The British journal of nutrition 90, 191-8 (2003). (Pubitemid 36903417)
13. Alvarez-Bolado, G., Rodriguez-Sanchez, P., Tejero-Diez, P., Fairen, A. & Diez-Guerra, F. J. Neurogranin in the development of the rat telencephalon. Neuroscience 73, 565-80 (1996). (Pubitemid 26168809)
14. Pak, J. H. et al. Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: a study with knockout mice. Proceedings of the National Academy of Sciences of the United States of America 97, 11232-7 (2000).
15. Dominguez-Gonzalez, I., Vazquez-Cuesta, S. N., Algaba, A. & Diez-Guerra, F. J. Neurogranin binds to phosphatidic acid and associates to cellular membranes. The Biochemical journal 404, 31-43 (2007). (Pubitemid 46788082)
16. Diez-Guerra, F. J. Neurogranin, a link between calcium/calmodulin and protein kinase C signaling in synaptic plasticity. IUBMB Life 62, 597-606 (2010).
17. Zhabotinsky, A. M., Camp, R. N., Epstein, I. R. & Lisman, J. E. Role of the neurogranin concentrated in spines in the induction of long-term potentiation. Journal of Neuroscience 26, 7337-47 (2006). (Pubitemid 44315201)
18. Zhong, L. & Gerges, N. Z. Neurogranin and synaptic plasticity balance. Commun Integr Biol 3, 340-2 (2010).
19. Zhong, L., Cherry, T., Bies, C. E., Florence, M. A. & Gerges, N. Z. Neurogranin enhances synaptic strength through its interaction with calmodulin. The EMBO journal 28, 3027-39 (2009).
20. Ran, X., Miao, H. H., Sheu, F. S. & Yang, D. Structural and dynamic characterization of a neuron-specific protein kinase C substrate, neurogranin. Biochemistry 42, 5143-50 (2003). (Pubitemid 36532069)
21. Chapman, E. R., Au, D., Alexander, K. A., Nicolson, T. A. & Storm, D. R. Characterization of the calmodulin binding domain of neuromodulin. Functional significance of serine 41 and phenylalanine 42. J Biol Chem 266, 207-13 (1991). (Pubitemid 21906110)
22. Alexander, K. A., Wakim, B. T., Doyle, G. S., Walsh, K. A. & Storm, D. R. Identification and characterization of the calmodulin-binding domain of neuromodulin, a neurospecific calmodulin-binding protein. The Journal of biological chemistry 263, 7544-9 (1988).
23. Prichard, L., Deloulme, J. C. & Storm,D. R. Interactions between neurogranin and calmodulin in vivo. J Biol Chem 274, 7689-94 (1999).
24. Huang, K. P., Huang, F. L. & Chen, H. C. Characterization of a 7.5-kDa protein kinase C substrate (RC3 protein, neurogranin) from rat brain. Archives of biochemistry and biophysics 305, 570-80 (1993). (Pubitemid 23282948)
25. Uversky, V. N. Natively unfolded proteins: a point where biology waits for physics. Protein science : a publication of the Protein Society 11, 739-56 (2002). (Pubitemid 34241284)
26. Rehm, T., Huber, R. & Holak, T. A. Application of NMR in structural proteomics: screening for proteins amenable to structural analysis. Structure 10, 1613-8 (2002). (Pubitemid 35447976)
27. Permyakov, S. E., Millett, I. S., Doniach, S., Permyakov, E. A. & Uversky, V. N. Natively unfolded C-terminal domain of caldesmon remains substantially unstructured after the effective binding to calmodulin. Proteins 53, 855-62 (2003). (Pubitemid 37490438)
28. Kleerekoper, Q. K. & Putkey, J. A. PEP-19, an intrinsically disordered regulator of calmodulin signaling. The Journal of biological chemistry 284, 7455-64 (2009).
29. De Guzman, R. N., Martinez-Yamout, M. A., Dyson, H. J. & Wright, P. E. Interaction of the TAZ1 domain of the CREB-binding protein with the activation domain of CITED2: regulation by competition between intrinsically unstructured ligands for non-identical binding sites. The Journal of biological chemistry 279, 3042-9 (2004). (Pubitemid 38114297)
30. Ye, Q., Li, X., Wong, A., Wei, Q. & Jia, Z. Structure of calmodulin bound to a calcineurin peptide: a new way of making an old binding mode. Biochemistry 45, 738-45 (2006). (Pubitemid 43122238)
31. Osawa, M. et al. A novel target recognition revealed by calmodulin in complex with Ca21-calmodulin-dependent kinase kinase. Nat Struct Biol 6, 819-24 (1999). (Pubitemid 29415172)
32. Lo,D. C., McAllister, A. K.&Katz, L. C. Neuronal transfection in brain slices using particle-mediated gene transfer. Neuron 13, 1263-8 (1994).
33. Gerendasy, D. Homeostatic tuning of Ca21 signal transduction by members of the calpacitin protein family. Journal of neuroscience research 58, 107-19 (1999). (Pubitemid 29463697)
34. Han, N. L. et al. Proteomics analysis of the expression of neurogranin in murine neuroblastoma (Neuro-2a) cells reveals its involvement for cell differentiation. Int J Biol Sci 3, 263-73 (2007).
35. Meiri, K. F., Hammang, J. P., Dent, E.W. & Baetge, E. E. Mutagenesis of ser41 to ala inhibits the association of GAP-43 with the membrane skeleton of GAP-43-deficient PC12B cells: effects on cell adhesion and the composition of neurite cytoskeleton and membrane. Journal of neurobiology 29, 213-32 (1996).
36. Pfuhl, M., Al-Sarayreh, S. & El-Mezgueldi, M. The calponin regulatory region is intrinsically unstructured: novel insight into actin-calponin and calmodulincalponin interfaces using NMR spectroscopy. Biophysical journal 100, 1718-28 (2011).
37. Houdusse, A. et al. Crystal structure of apo-calmodulin bound to the first two IQ motifs of myosin V reveals essential recognition features. Proceedings of the National Academy of Sciences of the United States of America 103, 19326-31 (2006). (Pubitemid 46026031)
38. Kingston, R. L., Baase, W. A.&Gay, L. S. Characterization of nucleocapsid binding by the measles virus and mumps virus phosphoproteins. J Virol 78, 8630-40 (2004). (Pubitemid 39025129)
39. Ellis, R. J. Macromolecular crowding: obvious but underappreciated. Trends in biochemical sciences 26, 597-604 (2001). (Pubitemid 32925190)
40. Rivas, G., Ferrone, F. &Herzfeld, J. Life in a crowded world. EMBO reports 5, 23-7 (2004). (Pubitemid 38228522)
41. Dedmon, M.M., Patel, C. N., Young, G. B. & Pielak, G. J. FlgM gains structure in living cells. Proceedings of the National Academy of Sciences of the United States of America 99, 12681-4 (2002).
42. le Maire, M., Ghazi, A., Moller, J. V. & Aggerbeck, L. P. The use of gel chromatography for the determination of sizes and relative molecular masses of proteins. Interpretation of calibration curves in terms of gel-pore-size distribution. The Biochemical journal 243, 399-404 (1987). (Pubitemid 17072839)
43. Hendrickson, W. A., Horton, J. R. & LeMaster, D. M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J 9, 1665-72 (1990).
44. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Macromolecular Crystallography, Pt A 276, 307-326 (1997). (Pubitemid 27085611)
45. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr A 64, 112-22 (2008).
46. Cowtan, K. The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62, 1002-11 (2006). (Pubitemid 44337374)
47. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-32 (2004). (Pubitemid 41742764)
48. Vagin, A. A. et al. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use. Acta Crystallogr D Biol Crystallogr 60, 2184-95 (2004). (Pubitemid 41742770)
49. Laskowski, R. A., Macarthur, M. W., Moss, D. S. & Thornton, J. M. Procheck-a Program to Check the Stereochemical Quality of Protein Structures. Journal of Applied Crystallography 26, 283-291 (1993).
50. DeLano,W. L. & Lam, J.W. PyMOL: A communications tool for computational models. Abstracts of Papers of the American Chemical Society 230, U1371-U1372 (2005).
51. Gahwiler, B. H., Capogna, M., Debanne, D., McKinney, R. A. & Thompson, S.M. Organotypic slice cultures: a technique has come of age. Trends in Neurosciences 20, 471-7 (1997). (Pubitemid 27421710)
52. Zhong, L., Kaleka, K. S. & Gerges, N. Z. Neurogranin phosphorylation fine-tunes long-term potentiation. The European journal of neuroscience 33, 244-50 (2011).