Nonlinear gap junctions enable long-distance propagation of pulsating calcium waves in astrocyte networks

PLoS Computational Biology

Volumn 6, Issue 8, 2010, Pages

  Goldberg, Mati ^a   de Pittà, Maurizio ^a   Volman, Vladislav ^b,c   Berry, Hugues ^d   Ben Jacob, Eshel ^a,b  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d INRIA RHÔNE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CELLS; CYTOLOGY; DYNAMICS; ENCODING (SYMBOLS); MODULATION; SIGNAL ENCODING; SIGNALING; WAVE PROPAGATION;

BRAIN FUNCTIONS; BRAIN SCIENCE; CA 2+; CALCIUM WAVES; CELL-CELL COMMUNICATIONS; CORTEXES; GAP-JUNCTIONS; GLIAL CELLS; INTRACELLULAR SIGNALING; LONG-DISTANCE PROPAGATION;

NEURONS;

AMPLITUDE MODULATION; ARTICLE; ASTROCYTE; BACK PROPAGATION; BRAIN FUNCTION; CALCIUM SIGNALING; CELL COMMUNICATION; CELL PROLIFERATION; COMPUTER MODEL; CONTROLLED STUDY; FREQUENCY MODULATION; GAP JUNCTION; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; MOLECULAR MODEL; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NERVE CONDUCTION; NERVE FIBER REGENERATION; NONLINEAR SYSTEM; PREDICTION; PULSATILE FLOW; SIGMOID SINUS; STOICHIOMETRY;

EID: 78049432843     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000909     Document Type: Article

References (75)

1. Herculano-Houzel S (2009) The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci 3: 1-11.
2. Allen NJ, Barres BA (2009) Glia - more than just brain glue. Nature 457: 675-677.
3. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640.
4. Santello M, Volterra A (2009) Synaptic modulation by astrocytes via Ca2+ - dependent glutamate release. Neuroscience 158: 253-259.
5. Bezzi P, Volterra A (2001) A neuron-glia signalling network in the active brain. Curr Opin Neurobiol 11: 387-394.
6. Agulhon C, Petravicz J, McMullen AB, Sweger EJ, Minton SK, et al. (2008) What is the role of astrocyte calcium in neurophysiology? Neuron 59: 932-946.
7. Codazzi F, Teruel MN, Meyer T (2001) Control of astrocyte Ca2+ oscillations and waves by oscillating translocation and activation of protein kinase C. Curr Biol 11: 1089-1097.
8. Zonta M, Carmignoto G (2002) Calcium oscillations encoding neuron-toastrocyte communication. J Physiol Paris 96: 193-198.
9. Grosche J, Matyash V, Möller T, Verkhratsky A, Reichenbach A, et al. (1999) Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nature 2: 139-143.
10. Pasti L, Volterra A, Pozzan T, Carmignoto G (1997) Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J Neurosci 17: 7817-7830.
11. Dani JW, Chernjavsky A, Smith SJ (1992) Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron 8: 429-440.
12. Cornell-Bell AH, Finkbeiner SM, Cooper MS, Smith SJ (1990) Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247: 470-473.
13. Charles AC (1998) Intercellular calcium waves in glia. Glia 24(1): 39-49.
14. Scemes E, Giaume C (2006) Astrocyte calcium waves: What they are and what they do. Glia 54: 716-725.
15. Sul JY, Orosz G, Givens Rs, Haydon PG (2004) Astrocytic connectivity in the hippocampus. Neuron Glia Biol 1: 3-11.
16. Tian GF, Takano T, Lin JHC, Wang X, Bekar L, et al. (2006) Imaging of cortical astrocytes using 2-photon laser scanning microscopy in the intact mouse brain. Adv Drug Deliv Rev 58: 773-787.
17. Hirase H, Qian L, Barthó P, Buzsáki G (2004) Calcium dynamics of cortical astrocytic networks in vivo. PLoS Biol 2: 0494-0496.
18. Newman EA, Zahs KR (1997) Calcium waves in retinal glial cells. Science 275: 844-847.
19. Carmignoto G (2000) Reciprocal communication systems between astrocytes and neurones. Prog Neurobiol 62: 561-581.
20. Berridge MJ (1997) The AM and FM of calcium signaling. Nature 389: 759-760.
21. Camacho P, Leichleiter JD (1993) Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. Science 260: 226-229.
22. Schipke CG, Heidenmann A, Skupin A, Peters O, Falcke M, et al. (2008) Temperature and nitric oxide control spontaneous calcium transients in astrocytes. Cell Calcium 43: 285-295.
23. Giaume C, Venance L (1998) Intracellular calcium signaling and gap junctional communication in astrocytes. Glia 24: 50-64.
24. Guthrie PB, Knappenberger J, Segal M, Bennett MVL, Charles AC, et al. (1999) ATP released from astrocytes mediates glial calcium waves. J Neurosci 19: 520-528.
25. Charles AC, Dirksen ER, Merrill JE, Sanderson MJ (1991) Intercellular signalling in glial cells: calcium waves and oscillations in response to mechanical stimulation and glutamate. Neuron 6: 983-992.
26. Finkbeiner SM (1993) Glial calcium. Glia 9: 83-104.
27. Kettenmann H, Schipke CG (2004) Calcium signaling in glia. In: Hatton GI, Parpura V, eds. Glial-neuronal signaling Kluwer Academic Publisher. pp 297-322.
28. Venance L, Stella N, Glowinski J, Giaume C (1997) Mechanism involved in initiation and propagation of receptor-induced intercellular calcium signaling in cultured rat astrocytes. J Neurosci 17: 1981-1992.
29. Sneyd J, Wetton BTR, Charles AC, Sanderson MJ (1995) Intercellular calcium waves mediated by diffusion of inositol trisphosphate: a two-dimensional model. Am J Physiol 268: C1537-C1545.
30. Falcke M (2004) Reading the patterns in living cells - the physics of Ca2+ signaling. Adv Phys 53: 255-440.
31. Harootunian AT, Kao JPY, Paranjape S, Tsien RY (1991) Generation of calcium oscillations in fibroblasts by positive feedback between calcium and IP3. Science 251: 75-78.
32. Höfer T, Venance L, Giaume C (2002) Control and plasticity of intercellular calcium waves in astrocytes: a modeling approach. J Neurosci 22: 4850-4859.
33. De Pittà M, Goldberg M, Volman V, Berry H, Ben-Jacob E (2009) Glutamatedependent intracellular calcium and IP3 oscillating and pulsating dynamics in astrocytes. J Biol Phys 35: 383-411.
34. Li Y, Rinzel J (1994) Equations for InsP3 receptor-mediated [Ca2+ ]i oscillations derived from a detailed kinetic model: A Hodgkin-Huxley like formalism. J Theor Biol 166: 461-473.
35. Harris AL (2001) Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34: 325-472.
36. Nagy JI, Rash JE (2000) Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res Rev 32: 29-44.
37. Lampe PD, Tenbroek EM, Burt JM, Kurata WE, Johnson RG, et al. (2000) Phosphorylation of connexin43 on serine368 by protein kinase C regulates gap junctional communication. J Cell Biol 149: 1503-1512.
38. Kwak B, Hermans MMP, DeJonge H, Lohmann S, Jongsma HJ, et al. (1995) Differential regulation of distinct types of gap junction channels by similar phosphorylating conditions. Molec Biol Cell 6: 1707-1719.
39. Müller T, Möller T, Neuhaus J, Kettenmann H (1996) Electrical coupling among Bergmann glial cells and its modulation by glutamate receptor activation. Glia 17: 274-284.
40. Scemes E (2001) Components of astrocytic intercellular calcium signaling. Mol Neurobiol 22: 167-179.
41. Sanderson MJ, Charles AC, Boitano S, Dirksen ER (1994) Mechanisms and function of intercellular calcium signaling. Mol Cell Endocrinol 98: 173-187.
42. Christ GJ, Brink PR, Ramanan SV (1994) Dynamic gap junctional communication: a delimiting model for tissue responses. Biophys J 67: 1335-1344.
43. Henriquez AP, Vogel R, Muller-Borer BJ, Henriquez CS, Weingart R, et al. (2001) Influence of dynamic gap junction resistance on impulse propagation in ventricular myocardium: A computer simulation study. Biophys J 81: 2112-2121.
44. Klein CT, Seelig FF (1995) Turing structures in a system with regulated gapjunctions. Biosystems 35: 15-23.
45. Irvine RF, Letcher AJ, Heslop JP, Berridge MJ (1986) The inositol tris/ tetrakisphopshate pathway- demonstration of Ins(1,4,5)P3 3-kinase activity in animal tissues. Nature 320: 631-634.
46. Hegger R, Kantz H, Schreiber T (1999) Practical implementation of nonlinear time series methods: The TISEAN package. Chaos 9: 413-435.
47. De Pittà M, Volman V, Levine H, Pioggia G, De Rossi D, et al. (2008) Coexistence of amplitude and frequency modulations in intracellular calcium dynamics. Phys Rev E 77: 030903(R).
48. De Pittà M, Volman V, Levine H, Ben-Jacob E (2009) Multimodal encoding in a simplified model of intracellular calcium signaling. Cogn Proc 10: 55-70.
49. Kimelberg HK (2004) The problem of astrocyte identity. Neurochem Int 45: 191-202.
50. Nimmerjahn A (2009) Astrocytes going live: advances and challenges. J Physiol 587: 1639-1647.
51. Haas B, Schipke CG, Peters O, Söhl G, Willecke K, et al. (2006) Activitydependent ATP-waves in the mouse neocortex are independent from astrocytic calcium waves. Cereb. Cortex 16: 237-246.
52. Edwards JR, Gibson WG (2010) A model for Ca2+ waves in networks of glial cells incorporating both intercellular and extracellular communication pathways. J Theor Biol 263: 45-58.
53. Young KW, Nash MS, Challiss JRA, Nahorski SR (2003) Role of Ca2+ feedback on single cell inositol 1,4,5-trisphosphate oscillations mediated by G-proteincoupled receptors. J Biol Chem 278: 20753-20760.
54. Nash MS, Young KW, Challiss JRA, Nahorski SR (2001) Intracellular signalling receptor-specific messenger oscillations. Nature 413: 381-382.
55. Hirose K, Kadowaki S, Tanabe M, Takeshima H, Lino M (1999) Spatiotemporal dynamics of inositol 1,4,5-trisphosphate that underlies complex Ca2+ mobilization. Science 284: 1527-1530.
56. Verboomen H, Wuytack F, De Smedt H, Himpens B, Casteels R (1992) Functional difference between SERCA2a and SERCA2b Ca2+ pumps and their modulation by phospholamban. Biochem J 286: 591-596.
57. Lytton J, Weslin M, Burk SE, Schull GE, MacLennan DH (1992) Functional comparison between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J Biol Chem 267: 14483-14489.
58. Papp S, Dziak E, Michalak M, Opas M (2003) Is all of the endoplasmic reticulum created equal? The effects of the heterogeneous distribution of endoplasmic reticulum Ca2+ -handling proteins. J Cell Biol 160: 475-479.
59. Baker HL, Errington RJ, Davies SC, Campbell AK (2002) A mathematical model predicts that calreticulin interacts with the endoplasmic reticulum Ca2+ - ATPase. Biophys J 82: 582-590.
60. Rebecchi MJ, Pentyala SN (2000) Structure, function, and control of phosphoinositide-specific phospholipase C. Physiol Rev 80: 1291-1335.
61. Lechleiter JLM, Camacho P (1998) Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142: 963-973.
62. Henriquez AP, Vogel R, Müller-Borer BJ, Henriquez CS, Weingart R, et al. (2001) Influence of dynamic gap junction resistance on impulse propagation in ventricular myocardium: a computer simulation study. Biophys J 81: 2112-2121.
63. Banach K, Weingart R (1996) Connexin43 gap junctions exhibit asymmetrical gating properties. Pflugers Arch 431: 775-785.
64. Sim SS, Kim JW, Rhee SG (1990) Regulation of D-myo-inositol 1,4,5- trisphosphate 3-kinase by cAMP-dependent protein kinase and protein kinase C. J Biol Chem 265: 10367-10372.
65. Enkvist MO, McCarthy KD (1992) Activation of protein kinase C blocks astroglial gap junction communication and inhibits the spread of calcium waves. J Neurochem 59: 519-526.
66. Rouach N, Avignone E, Meme W, Koulakoff A, Venance L, et al. (2002) Gap junctions and connexin expression in the normal and pathological central nervous system. Biol Cell 94: 457-475.
67. Dokukina IV, Gracheva ME, Grachev EA, Gunton JD (2008) Role of network connectivity in intercellular calcium signaling. Physica D 237: 745-754.
68. Volman V, Perc M (2010) Fast random rewiring and strong connectivity impair subthreshold signal detection in excitable networks. New J Phys 12: 043013.
69. Houades V, Rouach N, Ezan P, Kirchhoff F, Koulakoff A, et al. (2006) Shapes of astrocyte networks in the juvenile brain. Neuron Glia Biol 2: 3-14.
70. Walz W (2000) Controversy surrounding the existence of discrete functional classes of astrocytes in adult gray matter. Glia 31: 95-103.
71. Dreher Z, Tout S, Stone J (1994) Interactions of living astrocytes in vitro: Evidence of the development of contact spacing. Glia 11: 56-63.
72. Chan-Ling T, Stone J (1991) Factors determining the morphology and distribution of astrocytes in the cat retina: A contact-spacing model of astrocyte interaction. J Comp Neurol 303: 387-399.
73. Fellin T, Gonzalo MG, Gobbo S, Carmignoto G, Haydon PG (2006) Astrocytic glutamate is not necessary for the generation of epileptiform neuronal activity in hippocampal slices. J Neurosci 26: 9312-9322.
74. Aguado F, Espinosa-Parrilla JF, Carmona MA, Soriano E (2002) Neuronal activity regulates correlated network properties of spontaneous calcium transients in astrocytes in situ. J Neurosci 22: 9430-9444.
75. Communi D, Vanweyenberg V, Erneux C (1995) Molecular study and regulation of D-myo-inositol 1,4,5-trisphopshate 3-kinase. Cell Signal 7: 643-650.