Lobe specific Ca2+-calmodulin nano-domain in neuronal spines: A single molecule level analysis

PLoS Computational Biology

Volumn 6, Issue 11, 2010, Pages

  Kubota, Yoshihisa ^a   Waxham, M Neal ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM COMPOUNDS; CAMS; CHEMICAL ACTIVATION; ENZYMES; INTELLIGENT SYSTEMS; MOLECULES; MONTE CARLO METHODS; NANOTECHNOLOGY; NEURONS; TRANSCRIPTION;

CA 2+; DOWNSTREAM TARGET; INJECTION RATES; LONG TERM DEPRESSION; LONG-TERM POTENTIATIONS; N-TERMINALS; NANODOMAIN; SECOND MESSENGER; SINGLE MOLECULE LEVEL; SYNAPTIC PLASTICITY;

CALMODULIN;

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL; CALCIUM ION; CALMODULIN; CALCIUM;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; CALCIUM BINDING; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MONTE CARLO METHOD; NERVE CELL PLASTICITY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPINAL CORD NERVE CELL; ALGORITHM; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; DENDRITIC SPINE; HIPPOCAMPAL CA1 REGION; METABOLISM; PHYSIOLOGY; PYRAMIDAL NERVE CELL; RAT;

ALGORITHMS; ANIMALS; CA1 REGION, HIPPOCAMPAL; CALCIUM; CALMODULIN; DENDRITIC SPINES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MONTE CARLO METHOD; PYRAMIDAL CELLS; RATS;

EID: 78649642698     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000987     Document Type: Article

References (70)

1. Xia Z, Storm DR (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6: 267-276.
2. Malenka RC, Kauer JA, Perkel DJ, Mauk MD, Kelly PT, et al. (1989) An essential role for postsynaptic calmodulin and protein kinase activity in longterm potentiation. Nature 340: 554-557.
3. Malinow R, Schulman H, Tsien RW (1989) Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245: 862-866.
4. Otmakhov N, Griffith LC, Lisman JE (1997) Postsynaptic inhibitors of calcium/ calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. J Neurosci 17: 5357-5365.
5. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, et al. (1995) Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc Natl Acad Sci U S A 92: 11175-11179.
6. Pettit DL, Perlman S, Malinow R (1994) Potentiated transmission and prevention of further LTP by increased CaMKII activity in postsynaptic hippocampal slice neurons. Science 266: 1881-1885.
7. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369: 486-488.
8. Kubota Y, Putkey JA, Shouval HZ, Waxham MN (2008) IQ-motif proteins influence intracellular free Ca2+ in hippocampal neurons through their interactions with calmodulin. J Neurophysiol 99: 264-276.
9. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15: 303-308.
10. Singec I, Knoth R, Ditter M, Volk B, Frotscher M (2004) Neurogranin is expressed by principal cells but not interneurons in the rodent and monkey neocortex and hippocampus. J Comp Neurol 479: 30-42.
11. Guadano-Ferraz A, Vinuela A, Oeding G, Bernal J, Rausell E (2005) RC3/ neurogranin is expressed in pyramidal neurons of motor and somatosensory cortex in normal and denervated monkeys. J Comp Neurol 493: 554-570.
12. Klee CB, Vanaman TC (1982) Calmodulin. Adv Protein Chem 35: 213-321.
13. Linse S, Helmersson A, Forsen S (1991) Calcium binding to calmodulin and its globular domains. J Biol Chem 266: 8050-8054.
14. 2+. Biophys J 34: 559-569.
15. 2+ binding sites of calmodulin. J Biol Chem 271: 761-767.
16. Smith GD, Dai L, Miura RM, Sherman A (2001) Asymptotic Analysis of Buffered Calcium Diffusion Near a Point Source. SIAM J Appl Math 61: 1816-1838.
17. Quintana AR, Wang D, Forbes JE, Waxham MN (2005) Kinetics of calmodulin binding to calcineurin. Biochem Biophys Res Commun 334: 674-680.
18. Gaertner TR, Kolodziej SJ, Wang D, Kobayashi R, Koomen JM, et al. (2004) Comparative analyses of the three-dimensional structures and enzymatic properties of alpha, beta, gamma and delta isoforms of Ca2+-calmodulindependent protein kinase II. J Biol Chem 279: 12484-12494.
19. Byrne MJ, Putkey JA, Waxham MN, Kubota Y (2009) Dissecting cooperative calmodulin binding to CaM kinase II: a detailed stochastic model. J Comput Neurosci 27: 621-638.
20. Sabatini BL, Oertner TG, Svoboda K (2002) The life cycle of Ca(2+) ions in dendritic spines. Neuron 33: 439-452.
21. Svoboda K, Tank DW, Denk W (1996) Direct measurement of coupling between dendritic spines and shafts. Science 272: 716-719.
22. Maravall M, Mainen ZF, Sabatini BL, Svoboda K (2000) Estimating intracellular calcium concentrations and buffering without wavelength ratioing. Biophys J 78: 2655-2667.
23. Majewska A, Brown E, Ross J, Yuste R (2000) Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J Neurosci 20: 1722-1734.
24. Majewska A, Tashiro A, Yuste R (2000) Regulation of spine calcium dynamics by rapid spine motility. J Neurosci 20: 8262-8268.
25. Higley MJ, Sabatini BL (2008) Calcium signaling in dendrites and spines: practical and functional considerations. Neuron 59: 902-913.
26. Byrne MJ, Waxham MN, Kubota Y (2010) Cellular dynamic simulator: an event driven molecular simulation environment for cellular physiology. Neuroinformatics 8: 63-82.
27. Kerr RA, Bartol TM, Kaminsky B, Dittrich M, Chang JC, et al. (2008) Fast Monte Carlo Simulation Methods for Biological Reaction-Diffusion Systems in Solution and on Surfaces. SIAM J Sci Comput 30: 3126.
28. Illian J (2008) Statistical analysis and modelling of spatial point patterns. Chichester, West Sussex, Eng.; Hoboken NJ: John Wiley. 534 p.
29. Shaevitz JW, Block SM, Schnitzer MJ (2005) Statistical kinetics of macromolecular dynamics. Biophys J 89: 2277-2285.
30. Kubota Y, Putkey JA, Waxham MN (2007) Neurogranin controls the spatiotemporal pattern of postsynaptic Ca2+/CaM signaling. Biophys J 93: 3848-3859.
31. Allbritton NL, Meyer T, Stryer L (1992) Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258: 1812-1815.
32. Berezhkovskii AM, Barzykin AV, Zitserman VY (2009) Escape from cavity through narrow tunnel. J Chem Phys 130: 245104.
33. Schuss Z, Singer A, Holcman D (2007) The narrow escape problem for diffusion in cellular microdomains. Proc Natl Acad Sci U S A 104: 16098-16103.
34. Scheuss V, Yasuda R, Sobczyk A, Svoboda K (2006) Nonlinear [Ca2+] signaling in dendrites and spines caused by activity-dependent depression of Ca2+ extrusion. J Neurosci 26: 8183-8194.
35. Keller DX, Franks KM, Bartol TM, Jr., Sejnowski TJ (2008) Calmodulin activation by calcium transients in the postsynaptic density of dendritic spines. PLoS One 3: e2045.
36. Wakabayashi M, Hirano A, Sugawara M, Uchino S, Nakajima-Iijima S (2001) A single-channel method for evaluation of very magnitudes of Ca2+ ion fluxes through epsilon4/zeta1 N-methyl-D-aspartate receptor channels in bilayer lipid membranes. J Pharm Biomed Anal 24: 453-460.
37. Burnashev N, Zhou Z, Neher E, Sakmann B (1995) Fractional calcium currents through recombinant GluR channels of the NMDA, AMPA and kainite receptor subtypes. J Physiol 485 (Pt 2): 403-418.
38. Pina-Crespo JC, Gibb AJ (2002) Subtypes of NMDA receptors in new-born rat hippocampal granule cells. J Physiol 541: 41-64.
39. Kim SA, Heinze KG, Waxham MN, Schwille P (2004) Intracellular calmodulin availability accessed with two-photon cross-correlation. Proc Natl Acad Sci U S A 101: 105-110.
40. Diggle P (2003) Statistical analysis of spatial point patterns. London New York: Arnold; Distributed by Oxford University Press. viii, 159 p.
41. Kiskowski MA, Hancock JF, Kenworthy AK (2009) On the use of Ripley's K-function and its derivatives to analyze domain size. Biophys J 97: 1095-1103.
42. Nimchinsky EA, Yasuda R, Oertner TG, Svoboda K (2004) The Number of Glutamate Receptors Opened by Synaptic Stimulation in Single Hippocampal Spines. J Neurosci 24: 2054-2064.
43. Kalantzis G, Kubota Y, Shouval HZ (2009) Evaluating statistical methods used to estimate the number of postsynaptic receptors. J Neurosci Methods 178: 393-401.
44. Forest A, Swulius MT, Tse JK, Bradshaw JM, Gaertner T, et al. (2008) Role of the N- and C-lobes of calmodulin in the activation of Ca(2+)/calmodulindependent protein kinase II. Biochemistry 47: 10587-10599.
45. Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458: 299-304.
46. Huang KP, Huang FL, Jager T, Li J, Reymann KG, et al. (2004) Neurogranin/ RC3 enhances long-term potentiation and learning by promoting calciummediated signaling. J Neurosci 24: 10660-10669.
47. Krucker T, Siggins GR, McNamara RK, Lindsley KA, Dao A, et al. (2002) Targeted disruption of RC3 reveals a calmodulin-based mechanism for regulating metaplasticity in the hippocampus. J Neurosci 22: 5525-5535.
48. Gaertner TR, Putkey JA, Waxham MN (2004) RC3/Neurogranin and Ca2+/ calmodulin-dependent protein kinase II produce opposing effects on the affinity of calmodulin for calcium. J Biol Chem 279: 39374-39382.
49. Dominguez-Gonzalez I, Vazquez-Cuesta SN, Algaba A, Diez-Guerra FJ (2007) Neurogranin binds to phosphatidic acid and associates to cellular membranes. Biochem J 404: 31-43.
50. Smith GD (1996) Analytical steady-state solution to the rapid buffering approximation near an open Ca2+ channel. Biophys J 71: 3064-3072.
51. Parekh AB (2008) Ca2+ microdomains near plasma membrane Ca2+ channels: impact on cell function. J Physiol 586: 3043-3054.
52. Di Leva F, Domi T, Fedrizzi L, Lim D, Carafoli E (2008) The plasma membrane Ca2+ ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476: 65-74.
53. Cooney JR, Hurlburt JL, Selig DK, Harris KM, Fiala JC (2002) Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J Neurosci 22: 2215-2224.
54. Holbro N, Grunditz A, Oertner TG (2009) Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses. Proc Natl Acad Sci U S A 106: 15055-15060.
55. Stefan MI, Edelstein SJ, Le Novere N (2008) An allosteric model of calmodulin explains differential activation of PP2B and CaMKII. Proc Natl Acad Sci U S A 105: 10768-10773.
56. Bloodgood BL, Sabatini BL (2007) Nonlinear regulation of unitary synaptic signals by CaV(2.3) voltage-sensitive calcium channels located in dendritic spines. Neuron 53: 249-260.
57. Lorincz A, Rozsa B, Katona G, Vizi ES, Tamas G (2007) Differential distribution of NCX1 contributes to spine-dendrite compartmentalization in CA1 pyramidal cells. Proc Natl Acad Sci U S A 104: 1033-1038.
58. Li XF, Kiedrowski L, Tremblay F, Fernandez FR, Perizzolo M, et al. (2006) Importance of K+-dependent Na+/Ca2+-exchanger 2, NCKX2, in motor learning and memory. J Biol Chem 281: 6273-6282.
59. Jeon D, Yang YM, Jeong MJ, Philipson KD, Rhim H, et al. (2003) Enhanced learning and memory in mice lacking Na+/Ca2+ exchanger 2. Neuron 38: 965-976.
60. Sgambato-Faure V, Xiong Y, Berke JD, Hyman SE, Strehler EE (2006) The Homer-1 protein Ania-3 interacts with the plasma membrane calcium pump. Biochem Biophys Res Commun 343: 630-637.
61. Kip SN, Gray NW, Burette A, Canbay A, Weinberg RJ, et al. (2006) Changes in the expression of plasma membrane calcium extrusion systems during the maturation of hippocampal neurons. Hippocampus 16: 20-34.
62. Minelli A, Castaldo P, Gobbi P, Salucci S, Magi S, et al. (2007) Cellular and subcellular localization of Na+-Ca2+ exchanger protein isoforms, NCX1, NCX2, and NCX3 in cerebral cortex and hippocampus of adult rat. Cell Calcium 41: 221-234.
63. Zador A, Koch C, Brown TH (1990) Biophysical model of a Hebbian synapse. Proc Natl Acad Sci U S A 87: 6718-6722.
64. Guerini D, Coletto L, Carafoli E (2005) Exporting calcium from cells. Cell Calcium 38: 281-289.
65. Byrne MJ, Waxham MN, Kubota Y. Cellular Dynamic Simulator: An Event Driven Molecular Simulation Environment for Cellular Physiology. Neuroinformatics.
66. Andrews SS, Bray D (2004) Stochastic simulation of chemical reactions with spatial resolution and single molecule detail. Phys Biol 1: 137-151.
67. van Zon JS, ten Wolde PR (2005) Simulating biochemical networks at the particle level and in time and space: Green's function reaction dynamics. Phys Rev Lett 94: 128103.
68. Ridgway D, Broderick G, Lopez-Campistrous A, Ru'aini M, Winter P, et al. (2008) Coarse-grained molecular simulation of diffusion and reaction kinetics in a crowded virtual cytoplasm. Biophys J 94: 3748-3759.
69. Lightstone FC, Schwegler E, Allesch M, Gygi F, Galli G (2005) A first-principles molecular dynamics study of calcium in water. Chemphyschem 6: 1745-1749.
70. Harris KM, Stevens JK (1989) Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9: 2982-2997.