Microtubule ionic conduction and its implications for higher cognitive functions

Journal of Integrative Neuroscience

Volumn 9, Issue 2, 2010, Pages 103-122

  Craddock, Travis J A ^a   Tuszynski, Jack A ^a,b   Priel, Avner ^a,c   Freedman, Holly ^d  

^a UNIVERSITY OF ALBERTA   (Canada)

^b CROSS CANCER INSTITUTE   (Canada)

^c Israel Institute for Advanced Research   (Israel)

^d UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

cognitive function; Cytoskeleton; ionic conduction

Indexed keywords

TUBULIN;

ACTIN FILAMENT; BRAIN FUNCTION; CARBOXY TERMINAL SEQUENCE; COGNITION; CONSCIOUSNESS; CYTOSKELETON; ELECTRIC ACTIVITY; ELECTROCHEMICAL ANALYSIS; ELECTROENCEPHALOGRAM; HUMAN; INTRACELLULAR SIGNALING; ION TRANSPORT; LEARNING; MEMORY; MICROTUBULE ASSEMBLY; NERVE CELL MEMBRANE; NERVE CELL NETWORK; NERVE CONDUCTION; NEUROTRANSMISSION; REVIEW; SIGNAL TRANSDUCTION; STATIC ELECTRICITY;

ANIMALS; BRAIN; CYTOSKELETON; HUMANS; IONS; MICROTUBULES; NEURONS; SIGNAL TRANSDUCTION;

EID: 77954189509     PISSN: 02196352     EISSN: None     Source Type: Journal    
DOI: 10.1142/S0219635210002421     Document Type: Review

References (100)

1. Gundersen GG, Cook TA, Microtubules and signal transduction, Curr Opin Cell Biol 11:81-94, 1999.
2. Glanz J, Cook LM, Cell biology: Force-carrying web pervades living cell, Science 276:678-679, 1997.
3. Manitois AJ, Chen CS, Ingber DE, Demonstration of mechanical connections between integrins, cytoskeletal laments, and nucleoplasm that stabilize nuclear structure, Proc Natl Acad Sci USA 90:1807-1816, 2003.
4. Woolf NJ, Priel A, Tuszynski JA, Nanoneurosciene: Novel Biolmolecular Contributions to Mind, Springer, New York, 2009.
5. Priel A, Tuszynski JA, Woolf NJ, Neural cytoskeleton capabilities for learning and memory, J Biol Phys 36:3-21, 2009.
6. Tuszynski JA, Priel A, Brown JA, Cantiello HF, Dixon JM, Electronic and ionic conductivities of microtubules and actin filaments, their consequences for cell signaling and applications to bioelectronics, in Lyshevski SE (ed.), CRC Nano and Molecular Electronics Handbook, Taylor and Francis, London, 2007.
7. Priel A, Ramos AJ, Tuszynski JA, Cantiello HF, A biopolymer transistor: Electrical amplification by microtubules, Biophys J 90:4639-4643, 2006.
8. Conde C, Caceres A, Microtubule assembly, organization and dynamics in axons and dendrites, Nat Rev Neurosci 10:319-322, 2009.
9. Meyer DK, Olenik C, Hoffmann F, Barth H, Leemhuis J, Brunig I, Aktories K, Norenberg W, Regulation of somatodendritic GABAA receptor channels in rat hippocampal neurons: Evidence for a role of the small GTPase Rac1, J Neurosci 20:6743-6751, 2000.
10. Mironov SL, Richter DW, Cytoskeleton mediates inhibition of the fast Na+ current in respiratory brainstem neurons during hypoxia, Eur J Neurosci 11:1831-1834, 2008.
11. Furukawa KY,Wang PJ, YaoW, FuW, Mattson MP, Itoyama Y, Onodera H, D'Souza PH, Poorkaj PH, Bird TD, Schellenberg GD, Alteration in calcium channel properties is responsible for the neurotoxic action of a familial frontotemporal dementia tau mutation, J Neurochem 87:427-436, 2003.
12. Furukawa K, Mattson MP, Taxol stabilizes [Ca2+]i and protects hippocampal neurons against excitotoxicity, Brain Res 689:141-146, 1995.
13. Johnson BD, Byerly L, Ca2+ channel Ca2+-dependent inactivation in a mammalian central neuron involves the cytoskeleton, Pfluegers Archiv 429:14-21, 1994.
14. Johnson BD, Byerly L, A cytoskeletal mechanism for calcium channel metabolic dependence and inactivation by intracellular calcium, Neuron 10:797, 1993.
15. Woolf NJ, Microtubules in the cerebral cortex: Role in memory and consciousness, in Tuszynski JA (ed.), The Emerging Physics of Consciousness, Springer, New York, 2006.
16. OConnell C, OMalley A, Regan CM, Transient, learning-induced ultrastructural change in spatially-clustered dentate granule cells of the adult rat hippocampus, Neurosci 76:5562, 1997.
17. Mileusnic R, Lancashire CL, Rose SP, Recalling an aversive experience by day-old chicks is not dependent on somatic protein synthesis, Learn Mem 12:615-619, 2005.
18. Nakayama T, Sawada T, Involvement of microtubule integrity in memory impairment caused by colchicine, Pharmacol Biochem Behav 71:119-138, 2002.
19. Bensimon G, Chermat R, Microtubule disruption and cognitive defects: Effect of colchicine on learning behavior in rats, Pharmacol Biochem Behav 38:141-145, 1991.
20. Di Patre PL, Oh JD, Simmons JM, Butcher LL, Intrambrial colchicine produces transient impairment of radial-arm maze performance correlated with morphologic abnormalities of septohippocampal neurons expressing cholinergic markers and nerve growth factor receptor, Brain Res 523:316-320, 1990.
21. Yamaguchi S, Fujii-Taira I, Murakami A, Hirose N, Aoki N, Izawa E, Fujimoto Y, Takano T, Matsushima T, Homma KJ, Up-regulation of microtubule-associated protein 2 accompanying the filial imprinting of domestic chicks (Gallus gallus domesticus), Brain Res Bull 76:282-288, 2008.
22. Dehmelt L, Halpain S, The MAP2/Tau family of microtubule-associated proteins, Genome Biol 6:204, 2004.
23. Matus A, Microtubule-associated proteins and the determination of neuronal form, J Physiol (Paris) 84:134-137, 1990.
24. Liu HX, Zhang JJ, Zheng P, Zhang Y, Altered expression of MAP-2, GAP-43, and synaptophysin in the hippocampus of rats with chronic cerebral hypoperfusion correlates with cognitive impairment, Brain Res Mol Brain Res 139:169-177, 2005.
25. Shimada A, Tsuzuki M, Keino H, Satoh M, Chiba Y, Saitoh Y, Hosokawa M, Apical vulnerability to dendritic retraction in prefrontal neurones of ageing SAMP10 mouse: A model of cerebral degeneration, Neuropathol Appl Neurobiol 32:1-14, 2006.
26. Woolf NJ, Zinnerman MD, Johnson GV, Hippocampal microtubule-associated protein-2 alterations with contextual memory, Brain Res 821:241-249, 1999.
27. Woolf NJ, A structural basis for memory storage in mammals, Prog Neurobiol 55:5977, 1998.
28. Woolf NJ, Young SL, Johnson GV, Fanselow MS, Pavlovian conditioning alters cortical microtubule-associated protein-2, NeuroReport 5:1045-1048, 1994.
29. Nelson TJ, Backlund PS Jr, Alkon DL, Hippocampal proteinprotein interactions in spatial memory, Hippocampus 14:46-57, 2004.
30. Cavallaro S, DAgata V, Manickam P, Dufour F, Alkon DL, Memory-specific temporal profiles of gene expression in the hippocampus, Proc Natl Acad Sci USA 99:16279-16284, 2002. (Pubitemid 35462786)
31. Boekhoorn K, Terwel D, Biemans B, Borghgraef P, Wiegert O, Ramakers GJ, de Vos K, Krugers H, Tomiyama T, Mori H, Joels M, van Leuven F, Lucassen PJ, Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy, J Neurosci 26:3514-3523, 2006.
32. Pennanen L, Wolfer DP, Nitsch RM, Götz J, Impaired spatial reference memory and increased exploratory behavior in P301L tau transgenic mice, Genes Brain Behav 5:369-379, 2006.
33. Mershin A, Pavlopoulos E, Fitch O, Braden BC, Nanopoulos DV, Skoulakis EM, Learning and memory decits upon TAU accumulation in Drosophila mushroom body neurons, Learn Mem 11:277-287, 2004.
34. Minati L, Edginton T, Bruzzone MG, Giaccone G, Reviews: Current concepts in Alzheimer's Disease: A multidisciplinary review, Am J Alzheimers Dis Other Demen 24:95-121, 2009.
35. Colbran RJ, Brown AM, Calcium/calmodulin-dependent protein kinase II and synaptic plasticity, Curr Opin Neurobiol 14:318-327, 2004.
36. Lisman J, Schulman H, Cline H, The molecular basis of CaMKII function in synaptic and behavioural memory, Nat Rev Neurosci 3:175-190, 2002.
37. Fukunaga K, Muller D, Miyamoto E, CaM kinase II in long-term potentiation, Neurochem Int 28:343-358, 1996.
38. Roberts LA, Large CH, Higgins MJ, Stone TW, OShaughnessy CT, Morris BJ, Increased expression of dendritic mRNA following the induction of long-term potentiation, Mol Brain Res 56:38-44, 1998.
39. Wandosell F, Serrano L, Hernández MA, Avila J, Phosphorylation of tubulin by a calmodulin-dependent protein kinase, J Biol Chem 261:10332-10339, 1986.
40. Van der Zee EA, Douma BR, Bohus B, Luiten PG, Passive avoidance training induces enhanced levels of immunoreactivity for muscarinic acetylcholine receptor and coexpressed PKC gamma and MAP-2 in rat cortical neurons, Cereb Cortex 4:376-390, 1994.
41. Khuchua Z, Wozniak DF, Bardgett ME, Yue Z, McDonald M, Boero J, Hartman RE, Sims H, Strauss AW, Deletion of the N-terminus of murine map2 by gene targeting disrupts hippocampal ca1 neuron architecture and alters contextual memory, Neurosci 119:101-111, 2003.
42. Kerssens C, Alkire M, Memory formation during general anesthesia, in Mashour G (ed.), Consciousness, Awareness and Anesthesia, Cambridge University Press, New York, 2010.
43. Edelman GM, Naturalizing consciousness: A theoretical framework, Proc Natl Acad Sci USA 100:5520-5524, 2003.
44. Pan JZ, Xi J, Tobias JW, Eckenhoff MF, Eckenhoff RG, Halothane binding proteome in human brain cortex, J Proteome Res 6:582-592, 2007.
45. Pan JZ, Xi J, Eckenhoff MF, Eckenhoff RG, Inhaled anesthetics elicit region-specific changes in protein expression in mammalian brain, Proteomics 8:2983-2992, 2008.
46. Futterer CD, Maurer MH, Schmitt A, Feldmann RE Jr, Kuschinsky W, Waschke KF, Alterations in rat brain proteins after desflurane anesthesia, Anesthesiology 100:302-308, 2004.
47. Kalenka A, Hinkelbein J, Feldmann RE, Jr, KuschinskyW,Waschke KF, Maurer MH, The effects of sevoflurane anesthesia on rat brain proteins: A proteomic time-course analysis, Anesth Analg 104:1129-1135, 2007.
48. Akk G, Covey DF, Evers AS, Steinbach JH, Zorumski CF, Mennerick S, Mechanisms of neurosteroid interactions with GABA(A) receptors, Pharmacol Ther 116:35-37, 2007.
49. Mennerick S, He Y, Jiang X, Manion BD, Wang M, Shute A, Benz A, Evers AS, Covey DF, Zorumski CF, Selective antagonism of 5?-reduced neurosteroid effects at GABA(A) receptors, Mol Pharmacol 65:1191-1197, 2004.
50. Allison AC, Nunn JF, Effects of general anaesthetics on microtubules: A possible mechanism of anaesthesia, Lancet 292:1326-1329, 1968.
51. Hameroff S, Nip A, Porter M, Tuszynski J, Conduction pathways in microtubules, biological quantum computation, and consciousness, Biosystems 64:149-168, 2002. (Pubitemid 34033606)
52. Hameroff S, Marcer P, Quantum computation in brain microtubules? The Penrose- Hameroff 'Orch OR' model of consciousness [and discussion], Phil Trans R Soc Lond A 356:1869-1896, 1998.
53. Rosa LP, Faber J, Quantum models of the mind: Are they compatible with environmental decoherence?, Phys Rev E 70:031902, 2004.
54. Hagan S, Hameroff SR, Tuszynski JA, Quantum computation in brain microtubules: Decoherence and biological feasibility, Phys Rev E 65:061901, 2002.
55. Tegmark M, Importance of quantum decoherence in brain processes, Phys Rev E 61:4194-4206, 2000.
56. Vassilev PM, Dronzine RT, Vassileva MP, Georgiev GA, Parallel arrays of microtubules in electric and magnetic fields, Biosci Rep 2:1025-1029, 1982.
57. Kirson ED, Gurvich Z, Schneiderman R, Dekel E, Itzhaki A, Wasserman Y, Schatzberger R, Palti Y, Disruption of cancer cell replication by alternating electric fields, Cancer Res 64:3288-3295, 2004.
58. Goddard G, Whittier JE, Biomolecules as nanomaterials: Interface characterization for sensor development, Proc SPIE Int Soc Opt Eng 6172:43-54, 2006.
59. Fritzsche W, Köhler JM, Böhm KJ, Unger E, Wagner T, Kirsch R, Mertig M, Pompe W, Wiring of metallized microtubules by electron beam-induced structuring, Nanotechnol 10:331-335, 1999.
60. Fritzsche W, Böhm KJ, Unger E, Köhler JM, Making electrical contact to single molecules, Nanotechnol 9:177-183, 1998.
61. Umnov M, Palusinski OA, Deymier PA, Guzman R, Hoying J, Barnaby H, Yang Y, Raghavan S, Experimental evaluation of electrical conductivity of microtubules, J Materials Sci 42:373-378, 2007.
62. Minoura I, Muto E, Dielectric measurement of individual microtubules using the electroorientation method, Biophys J 90:3739-3748, 2006.
63. Li H, DeRosier D, Nicholson W, Nogales E, Downing K, Microtubule structure at 8 resolution, Structure 10:1317-1328, 2002.
64. Sept D, Baker NA, McCammon JA, The physical basis of microtubule structure and stability, Prot Sci 12:2257-2261, 2003.
65. Song YH, Mandelkow E, Recombinant kinesin motor domain binds to b-tubulin and decorates microtubules with a B surface lattice, Proc Natl Acad Sci USA 99:1671-1675, 1993.
66. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, Electrostatics of nanosystems: Application to microtubules and the ribosome, Proc Natl Acad Sci USA 98:10037-10041, 2001.
67. Dixon JM, Chelminiak P, Tuszynski JA, Surface conductance in seamless microtubules, Physica A 387:4183-4194, 2008.
68. Priel A, Tuszynski JA, A nonlinear cable-like model of amplified ionic wave propagation along microtubules, Europhys Lett 83:68004, 2008.
69. Priel A, Tuszynski JA, Woolf NJ, Transitions in microtubule C-termini conformations as a possible dendritic signaling phenomenon, Eur Biophys J 35:40-52, 2005.
70. Priel A, Tuszynski JA, Cantiello HF, Electrodynamic signaling by the dendritic cytoskeleton: Toward an intracellular information processing model, Electromagn Biol Med 24:221-231, 2005.
71. Chelminiak PW, Tuszynski JA, Dixon JM, Effects of C-termini distribution on ionic transport along microtubules, Interdiscip Sci Comput Life Sci 1:108-112, 2009.
72. Satarïc MV, Ilïc DI, Ralevic̈, Tuszynski JA, A nonlinear model of ionic wave propagation along microtubules, Eur Biophys J 38:637-647, 2009.
73. Freedman H, Rezania V, Priel A, Carpenter E, Noskov SY, Tuszynski JA, Model of ionic currents through microtubule nanopores and the lumen, Phys Rev E, in press (Accepted Tuesday Feb 23, 2010).
74. Diaz JF, Barasoain I, Andreu JM, Fast kinetics of taxol binding to microtubules, J Biol Chem 278:8407-8419, 2003.
75. Pal D, Mahapatra P, Manna T, Chakrabarti P, Bhattacharyya B, Banerjee A, Basu G, Roy S, Conformational properties of α-tubulin tail peptide: Implications for tail-body interaction, Biochem 40:15512-15519, 2001.
76. Szasz J, Yaffe MB, Elzinga M, Blank GS, Sternlicht H, Microtubule assembly is dependent on a cluster of basic residues in α-tubulin, Biochem 12:4572-4582, 1986.
77. Dehmelt L, Smart FM, Ozer RS, Halpain S, The role of microtubule- associated protein 2c in the reorganization of microtubules and lamellipodia during neurite initiation, J Neurosci 23:9479-9490, 2003.
78. Challacombe JF, Snow DM, Letourneau PC, Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue, J Neurosci 17:3085-3095, 1997.
79. Tuszynski J, Portet S, Dixon J, Luxford C, Cantiello H, Ionic wave propagation along actin filaments, Biophys J 86:1890-1903, 2004.
80. Mitchison TJ, Compare and contrast actin filaments and microtubules,Mol Biol Cell 3:1309-1315, 1992.
81. Lin EC, Cantiello HF, A novel method to study the electrodynamic behavior of actin filaments: Evidence for cable-like properties of actin, Biophys J 65:1371-1378, 1993.
82. Cantiello HF, Patenaude C, Zaner K, Osmotically induced electrical signals from actin filaments, Biophys J 59:1284-1289, 1991.
83. Morales M, Fifkova E, Distribution of MAP 2 in dendritic spines and its colocalization with actin, Cell Tissue Res 256:447-456, 1989.
84. Rodriguez OC, Schaefer AW, Mandato CA, Forscher P, Bement WM, Waterman- Storer CM, Conserved microtubule-actin interactions in cell movement and morphogenesis, Nature Cell Biol 5:599-609, 2003.
85. Passafaro M, Sala C, Niethammer M, Sheng M, Microtubule binding by CRIPT and its potential role in the synaptic clustering of PSD-95, Nature Neurosci 2:1063-1069, 1999.
86. Kube-Granderath E, Schliwa M, Unusual tubulins for unusual cells, Protist 149:123-126, 1998.
87. Luduena RF, Banerjee A, The isotypes of tubulin: Distribution and functional significance, in Fojo T (ed.), The Role of Microtubules in Cell Biology, Neurobiology, and Oncology, Humana Press, 2008.
88. Gordon R, The Hierarchical Genome and Differentiation Waves, World Scientific, Singapore, 1999.
89. Sackett DL, Structure and function in the tubulin dimer and the role of the acidic carboxyl terminus, Subcell Biochem 24:255-302, 1995.
90. Tuszynski JA, Carpenter EJ, Huzil, JT, Malinski W, Luchko T, Luduena RF, The evolution of the structure of tubulin and its potential consequences for the role and function of microtubules in cells and embryos, Int J Dev Biol 50:341-358, 2006.
91. Duan J, Gorovsky MA, Both carboxy-terminal tails of α- and β-tubulin are essential, but either one will suffice, Curr Biol 12:313-316, 2002.
92. Luduena RF, Multiple forms of tubulin: Different gene products and covalent modifications, Int Rev Cytol 178:207-275, 1997.
93. Sarkar T, Manna T, Bhattacharyya S, Mahapatra P, Poddar A, Roy S, Pena J, Solana R, Tarazona R, Bhattacharyya B, Role of the carboxy-termini of tubulin on its chaperone-like activity, Proteins 44:262-269, 2001.
94. Makrides V, Shen TE, Rajinder B, Smith BL, Thimm J, Lal R, Feinstein SC, Microtubule-dependent oligomerization of tau: Implications for physiological tau function and tauopathies, J Biol Chem 278:33298-33304, 2003.
95. Luduena RF, The post-translational modifications of tubulin, in Fojo T (ed.), The Role of Microtubules in Cell Biology, Neurobiology, and Oncology, Humana Press, 2008.
96. Redeker V, Rossier J, Frankfurter A, Posttranslationalmodifications of the C-terminus of α-tubulin in adult rat brain: β4 is glutamylated at two residues, Biochem 37:14838-14844, 1998.
97. MacRae TH, Tubulin post-translational modifications - enzymes and their mechanisms of action, Eur J Biochem 244:265-278, 1997.
98. Stracke R, Boehm KJ,Wollweber L, Unger E, Tuszynski JA, Analysis of the migration behavior of single microtubules in electric fields, Biochem Biophys Res Com 293:602-609, 2002.
99. Behrens S, Wu J, Habicht W, Unger E, Silver nanoparticle and nanowire formation by microtubule templates, Chem Mater 16:3085-3090, 2004.
100. Saubermann AJ, Gallagher ML, Mechanisms of general anesthesia: Failure of pentobarbital and halothane to depolymerize microlubules in mouse optic nerve, Anesthesiology 38:25-29, 1973.