A hierarchical coherent-gene-group model for brain development

Genes, Brain and Behavior

Volumn 12, Issue 2, 2013, Pages 147-165

  Tsigelny, I F ^a,b,c   Kouznetsova, V L ^a,b   Baitaluk, M ^a   Changeux, J P ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d INSTITUT PASTEUR   (France)

Author keywords

Autism spectrum disorder; Brain development; Coherent gene groups; Cortex; Hierarchical coherent gene group model; Hierarchical transcription factor network; Informational entropy; Neurogenesis; Neurotransmission; Schizophrenia; Self organizing maps; Signaling pathway; Synaptic epigenesis; Synaptogenesis

Indexed keywords

TRANSCRIPTION FACTOR;

ARTICLE; AUTISM; BRAIN DEVELOPMENT; DRUG DESIGN; GENE EXPRESSION; GENETIC PREDISPOSITION; GENETIC TRANSCRIPTION; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PERINATAL PERIOD; PRENATAL PERIOD; PRIORITY JOURNAL; SCHIZOPHRENIA; SYNAPTOGENESIS;

ANIMALS; BRAIN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GENES; MODELS, GENETIC; MODELS, STATISTICAL; NEUROGENESIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

RATTUS;

EID: 84874217621     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12005     Document Type: Article

References (114)

1. Avasarala, J.R., Chittur, S.V., George, A.D. & Tine, J.A. (2008) Microarray analysis in B cells among siblings with/without MS-role for transcription factor TCF2. BMC Med Genomics 1, 2.
2. Ayoub, A.E., Oh, S., Xie, Y., Leng, J., Cotney, J., Dominguez, M.D., Noonan, J.P. & Rakic, P. (2011) Transcriptional programs in transient embryonic zones of the cerebral cortex defined by high-resolution mRNA-sequencing. Proc Natl Acad Sci U S A 108, 14950-14955.
3. Baitaluk, M. & Ponomarenko, J. (2010) Semantic integration of data on transcriptional regulation. Bioinformatics 26, 1651-1661.
4. Baitaluk, M., Qian, X., Godbole, S., Raval, A., Ray, A. & Gupta, A. (2006a) PathSys: integrating molecular interaction graphs for systems biology. BMC Bioinformatics 7, 55.
5. Baitaluk, M., Sedova, M., Ray, A. & Gupta, A. (2006b) BiologicalNetworks: visualization and analysis tool for systems biology. Nucleic Acids Res 34, W466-W471.
6. Baitaluk, M., Kozhenkov, S., Dubinina, Y. & Ponomarenko, J. (2012) IntegromeDB: an integral system and biological search engine. BMC Genomics 13, 35.
7. Bandeira, F., Lent, R. & Herculano-Houzel, S. (2009) Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc Natl Acad Sci U S A 106, 14108-14113.
8. Bayès, A., van de Lagemaat, L.N., Collins, M.O., Croning, M.D., Whittle, I.R., Choudhary, J.S. & Grant, S.G. (2011) Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat Neurosci 14, 19-21.
9. Ben-David, E. & Shifman, S. (2012) Networks of neuronal genes affected by common and rare variants in Autism Spectrum Disorders. PLoS Genet 8: e1002556.
10. Benoit, P. & Changeux, J.-P. (1975) Consequences of tenotomy on the evolution of multiinnervation in developing rat soleus muscle. Brain Res 99, 354-358.
11. Benoit, P. & Changeux, J.-P. (1978) Consequences of blocking the nerve with a local anaesthetic on the evolution of multiinnervation at the regenerating neuromuscular junction of the rat. Brain Res 149, 89-96.
12. Britten, R.J. & Davidson, E.H. (1969) Gene regulation for higher cells: a theory. Science 165, 349-357.
13. Brunet, A., Datta, S.R. & Greenberg, M.E. (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11, 297-305.
14. Brzózka, M.M., Radyushkin, K., Wichert, S.P., Ehrenreich, H. & Rossner, M.J. (2006) Cognitive and sensorimotor gating impairments in transgenic mice overexpressing the schizophrenia susceptibility geneTcf4 in the brain. J Neurosci 26, 12003-120013.
15. Buckingham, M. & Relaix, F. (2007) The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu Rev Cell Dev Biol 23, 645-673.
16. Castro-Caldas, A., Petersson, K.M., Reis, A., Stone-Elander, S. & Ingvar, M. (1998) The illiterate brain. Learning to read and write during childhood influences the functional organization of the adult brain. Brain (Pt 6), 1053-1063.
17. Chang, L.W., Fontaine, B.R., Stormo, G.D. & Nagarajan, R. (2007) PAP: A comprehensive workbench for mammalian transcriptional regulatory sequence analysis. Nucleic Acids Res 35, W238-W244.
18. Changeux, J.-P. (1973) Cholinergic receptors in electrophorus. Neurosci Res Program Bull 11, 246-252.
19. Changeux, J-P. (1983) L'homme neuronal. Fayard Paris. (English edition: Changeux, J-P. Neuronal Man: The Biology of Mind. Pantheon Books, New York.
20. Changeux, J.-P. (2004) The Physiology of Truth: Neuroscience and Human Knowledge (Mind/Brain/Behavior Initiative). Belknap Press of Harvard University Press, Boston.
21. Changeux, J.-P. (2012) The Good, the True, and the Beautiful: A Neuronal Approach. Yale University Press, New Haven.
22. Changeux, J.-P. & Danchin, A. (1976) Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature 264, 705-712.
23. Changeux, J.-P., Courrège, P. & Danchin, A. (1973) A theory of the epigenesis of neuronal networks by selective stabilization of synapses. Proc Natl Acad Sci U S A 70, 2974-2978.
24. Dai, M., Wam, P., Boyd, A.D., Kostov, G., Athey, B., Jones, E.G., Bunney, W.E., Myers, R.M., Speed, T.P., Akil, H., Watson, S.J. & Meng, F. (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 32, e175.
25. Davidson, E.H. (2010) Emerging properties of animal gene regulatory networks. Nature 468, 911-920.
26. Davies, E. (2005) Machine Vision: Theory, Algorithms and Practicalities. Elsevier Inc., Morgan Kaufmann Publishers, San Francisco.
27. Dehaene, S. & Changeux, J.-P. (2011) Experimental and theoretical approaches to conscious processing. Neuron 70, 200-227.
28. Dehaene, S., Pegado, F., Braga, L.W., Ventura, P., Nunes Filho, G., Jobert, A., Dehaene-Lambertz, G., Kolinsky, R., Morais, J. & Cohen, L. (2010) How learning to read changes the cortical networks for vision and language. Science 330, 1359-1364.
29. Driever, W. & Nüsslein-Volhard, C. (1998) A gradient of bicoid protein in Drosophila embryos. Cell 54, 83-93.
30. Ebersberger, I., Metzler, D., Schwarz, C. & Pääbo, S. (2002) Genomewide comparison of DNA sequences between humans and chimpanzees. Am J Hum Genet 70, 1490-1497.
31. Eichler, G.S., Huang, S. & Ingber, D.E. (2003) Gene Expression Dynamics Inspector (GEDI): for integrative analysis of expression profiles. Bioinformatics 19, 2321-2322.
32. Ey, E., Leblond, C.S. & Bourgeron, T. (2011) Behavioral profiles of mouse models for autism spectrum disorders. Autism Res 4, 5-16.
33. de Felipe, J. (2010) From the connectome to the synaptome: an epic love story. Science 330, 198-201.
34. Fessele, S., Maier, H., Zischek, C., Nelson, P.J. & Werner, T. (2002) Regulatory context is a crucial part of gene function. Trends Genet 18, 60-63.
35. Flavell, S.W., Cowan, C.W., Kim, T.K., Gree, P.L., Lin, Y., Paradis, S., Griffith, E.C., Hu, L.S., Chen, C. & Greenberg, M.E. (2006) Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311, 1008-1012.
36. Fu, X., Giavalisco, P., Liu, X., Catchpole, G., Fu, N., Ning, Z.B., Guo, S., Yan, Z., Somel, M., Pääbo, S., Zeng, R., Willmitzer, L. & Khaitovich, P. (2011) Rapid metabolic evolution in human prefrontal cortex. Proc Natl Acad Sci U S A 108, 6181-6186.
37. Furtak, S.C., Moyer, J.R. & Brown, T.H. (2007) Morphology and ontogeny of rat perirhinal cortical neurons. J Comp Neurol 505, 493-510.
38. Girirajan, S., Campbell, C.D. & Eichler, E.E. (2011) Human copy number variation and complex genetic disease. Annu Rev Genet 45, 203-226.
39. Greene, M.E., Mundschau, G., Wechsle, J., McDevitt, M., Gamis, A., Karp, J., Gurbuxani, S., Arceci, R. & Crispino, J.D. (2003) Mutations in GATA1 in both transient myeloproliferative disorder and acute megakaryoblastic leukemia of Down syndrome. Blood Cells Mol Dis 31, 351-356.
40. Gulyás, B. & Halldin, C. (2012) New PET radiopharmaceuticals beyond FDG for brain tumor imaging. Q J Nucl Med Mol Imaging 56, 173-190.
41. Guo, Y., Eichler, G.S., Feng, Y., Ingber, D.E. & Huang, S. (2006) Towards a holistic, yet gene-centered analysis of gene expression profiles: a case study of human lung cancers. J Biomed Biotechnol 2006, 1-11.
42. Halfon, M.S., Grad, Y., Church, G.M. & Michelson, A.M. (2002) Computation-based discovery of related transcriptional regulatory modules and motifs using an experimentally validated combinatorial model. Genome Res 12, 1019-1028.
43. Insel, T.R. (2010) Rethinking schizophrenia. Nature 468, 187-193.
44. Jacob, F. & Monod, J. (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3, 318-356.
45. Jamain, S., Radyushkin, K., Hammerschmidt, K., Granon, S., Boretius, S., Varoqueaux, F., Ramanantsoa, N., Gallego, J., Ronnenberg, A., Winter, D., Frahm, J., Fischer, J., Bourgeron, T., Ehrenreich, H. & Brose, N. (2008) Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci U S A 105, 1710-1715.
46. Jaźwińska, A., Badakov, R. & Keating, M.T. (2007) Activin-betaA signaling is required for zebrafish fin regeneration. Curr Biol 17: 1390-1395.
47. Jiang, J. & Levine, M. (1993) Binding affinities and cooperative interactions with bHLH activators delimit threshold responses to the dorsal gradient morphogen. Cell 72, 741-752.
48. Jiang, Z., Tang, H., Ventura, M., Cardone, M.F., Marques-Bonet, T., She, X., Pevzne, P.A. & Eichler, E.E. (2007) Ancestral reconstruction of segmental duplications reveals punctuated cores of human genome evolution. Nat Genet 39, 1361-1368.
49. Johnson, M.H. (2011) Developmental Cognitive Neuroscience, 3rd edn. Wiley-Blackwell, Hoboken, New Jersey, USA, pp. 308.
50. Kang, H.Y., Kawasawa, Y.I., Cheng, F. et al. (2011) Spacio-temporal transcriptome of the human brain. Nature 478, 483-489.
51. Kapur, J.N., Sahoo, P.K. & Wong, A.C. (1985) A new method for gray-level picture thresholding using the entropy of the histogram. Comput Vision Graph 29, 273-285.
52. Karlsgodt, K.H., Sun, D., Jimenez, A.M., Lutkenhoff, E.S., Willhite, R., van Erp, T.G. & Cannon, T.D. (2008) Developmental disruptions in neural connectivity in the pathophysiology of schizophrenia. Dev Psychopathol 20, 1297-1327.
53. Karlsgodt, K.H., Jacobson, S.C., Seal, M. & Fusar-Poli, P. (2012) The relationship of developmental changes in white matter to the onset of psychosis. Curr Pharm Des 18, 422-433.
54. Kerszberg, M. & Changeux, J.-P. (1994a) A model for reading morphogenetic gradients: autocatalysis and competition at the gene level. Proc Natl Acad Sci U S A 91, 5823-5827.
55. Kerszberg, M. & Changeux, J.-P. (1994b) Partners make patterns in morphogenesis. Curr Biol 4, 1046-1047.
56. Kerszberg, M. & Changeux, J.-P. (1998) A simple molecular model of neurulation. Bioessays 20, 758-770.
57. Kirov, G., Pocklington, A.J., Holmans, P. et al. (2012) De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Mol Psychiatry 17, 142-153.
58. Kohonen, T. (2000) Self-Organized Maps, 3 edn. Springler, Berlin.
59. Konopka, G., Friedrich, T., Davis-Turak, J., Winden, K., Oldham, M.C., Gao, F., Chen, L., Wang, G.-Z., Luo, R., Preuss, T.M. & Geschwind, D.H. (2012) Human-specific transcriptional networks in the brain. Neuron 75, 601-617.
60. Kouznetsova, V.L. & Rakov, M.A. (1987) Self-Organization in Technical Systems. Naukova Dumka, Kiev (in Russian).
61. Kouznetsova, V.L., Tsigelny, I.F., Nagle, M.A. & Nigam, S.K. (2011) Elucidation of common pharmacophores from analysis of targeted metabolites transported by the multispecific drug transporter-Organic anion transporter1 (Oat1). Bioorg Med Chem 19, 3320-3340.
62. Kozhenkov, S., Dubinina, Y., Sedova, M., Gupta, A., Ponomarenko, J. & Baitaluk, M. (2010) BiologicalNetworks 2.0-an integrative view of genome biology data. BMC Bioinformatics 11, 610.
63. Kwon, E., Wang, W. & Tsai, L.-H. (2011) Validation of schizophrenia-associated genes CSMD1, C10orf26, CACNA1C and TCF4 as miR-137 targets. Mol Psychiatry 20, 1-2.
64. Lagercrantz, H. (2009) The birth of consciousness. Early Hum Dev 85 (Suppl. 10), S57-S58.
65. Lagercrantz, H. (2012) Are cardiorespiratory complications a question of epigenetics? Proc Natl Acad Sci U S A 109, 2192-2193.
66. Lagercrantz, H., Nilsson, E., Redham, I. & Hjemdahl, P. (1986) Plasma catecholamines following nursing procedures in a neonatal ward. Early Hum Dev 14, 61-65.
67. Lagercrantz, H., Pequignot, J., Pequignot, J.M. & Peyrin, L. (1992) The first breaths of air stimulate noradrenaline turnover in the brain of the newborn rat. Acta Physiol Scand 144, 433-438.
68. Lagercrantz, H., Hanson, M.A., Ment, L.R. & Peebles, D.M. (2010) The newborn brain, 2 edn. Cambridge University Press, Cambridge.
69. Larson, E.B., Akkentli, F., Edwards, S., Graham, D.L., Simmons, D.L., Alibhai, I.N., Nestler, E.J. & Self, D.W. (2010) Striatal regulation of ΔFosB, FosB, and cFos during cocaine self-administration and withdrawal. J Neurochem 115, 112-122.
70. Le Bras, B., Barallobre, M.J., Homman-Ludiye, J., Ny, A., Wyns, S., Tammela, T., Haiko, P., Karkkainen, M.J., Yuan, L., Muriel, M.P., Chatzopoulou, E., Bréant, C., Zalc, B., Carmeliet, P., Alitalo, K., Eichmann, A. & Thomas, J.L. (2006) VEGF-C is a trophic factor for neural progenitors in the vertebrate embryonic brain. Nat Neurosci 9, 340-348.
71. Li, E. & Davidson, E.H. (2009) Building developmental gene regulatory networks. Birth Defects Res C Embryo Today 87, 123-130.
72. Li, L., Li, Q., Rohlin, L., Kim, U.M., Salmon, K., Rejtar, T., Gunsalus, R.P., Karger, B.L. & Ferry, J.G. (2007) Quantitative proteomic and microarray analysis of the archaeon Methanosarcina acetivorans grown with acetate versus methanol. J Proteome Res 6, 759-771.
73. Liu, X., Bushnell, D.A., Wang, D., Calero, G. & Kornberg, R.D. (2010) Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science 327, 206-209.
74. Liu, X., Somel, M., Tang, L., Yan, Z., Jiang, X., Guo, S., Yuan, Y., He, L., Oleksiak, A., Zhang, Y., Li, N., Hu, Y., Chen, W., Qiu, Z., Pääbo, S. & Khaitovich, P. (2012) Extension of cortical synaptic development distinguishes humans from chimpanzees and macaques. Genome Res 22, 611-622.
75. Luo, L. & O'Leary, D.D. (2005) Axon retraction and degeneration in development and disease. Annu Rev Neurosci 28, 127-156.
76. Mannervik, M., Nibu, Y., Zhang, H. & Levine, M. (1999) Transcriptional coregulators in development. Science 284, 606-609.
77. Monod, J. & Jacob, F. (1961) Teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harb Symp Quant Biol 26, 389-401.
78. Narayan, S., Tang, B., Head, S.R., Gilmartin, T.J., Sutcliffe, J.G., Dean, B. & Thomas, E.A. (2008) Molecular profiles of schizophrenia in the CNS at different stages of illness. Brain Res 1239, 235-248.
79. van Neerven, S., Kampmann, E. & Mey, J. (2008) RAR/RXR and PPAR/RXR signaling in neurological and psychiatric diseases. Prog Neurobiol 85, 433-451.
80. Noll, M. (1993) Evolution and role of Pax genes. Curr Opin Genet Dev 3, 595-605.
81. Pennypacker, K.R. (1995) AP-1 transcription factor complexes in CNS disorders and development. J Fla Med Assoc 82, 551-554.
82. Petanjek, Z., Judaš, M., Šimic, G., Rasin, M.R., Uylings, H.B., Rakic, P. & Kostovic, I. (2011) Extraordinary neoteny of synaptic spines in the human prefrontal cortex. Proc Natl Acad Sci U S A 108, 13281-13286.
83. Prieto, C. & De Las Rivas, J. (2006) APID: Agile Protein Interaction DataAnalyzer. Nucleic Acids Res 34, W298-W302.
84. Pugliese, L., Catani, M., Ameis, S., Dell'Acqua, F., Thiebaut de Schotten, M., Murphy, C., Robertson, D., Deeley, Q., Daly, E. & Murphy, D.G. (2009) The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study. Neuroimage 47, 427-434.
85. Purves, D. & Lichtman, J.W. (1980) Elimination of synapses in the developing nervous system. Science 210, 153-157.
86. Qiu, P., Qin, L., Sorrentino, R.P., Greene, J.R., Wang, L. & Partridge, N.C. (2003) Comparative promoter analysis and its application in analysis of PTH-regulated gene expression. J Mol Biol 326, 1327-3136.
87. Rakic, P. (2006) A century of progress in corticoneurogenesis: from silver impregnation to genetic engineering. Cereb Cortex 16 (Suppl. 1), i3-i17.
88. Rice, D. & Barone, S. (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108, 511-533.
89. Ripke, S., Sanders, A.R., Kendler, K.S., Levinson, D.F., Sklar, P., Holmans, P.A. et al. (2011) Genome-wide association study identifies five new schizophrenia loci. Nat Genet 43, 969-976.
90. Saeed, A.I., Bhagabati, N.K., Braisted, J.C., Liang, W., Sharov, V., Howe, E.A., Li, J., Thiagarajan, M., White, J.A. & Quackenbush, J. (2006) TM4 microarray software suite. Methods Enzymol 411, 134-193.
91. Sarkar, S., Kalia, V., Haining, W.N., Konieczny, B.T., Subramaniam, S. & Ahmed, R. (2008) Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J Exp Med 205, 625-640.
92. Schmeisser, M.J., Ey, E., Wegener, S. et al. (2012) Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature 486, 256-260.
93. Sebat, J., Levy, D.L. & McCarthy, S.E. (2009) Rare structural variants in schizophrenia: one disorder, multiple mutations; one mutation, multiple disorders. Trends Genet 25, 528-535.
94. Segal, E., Shapira, M., Regev, A., Pe'er, D., Botstein, D., Koller, D. & Friedman, N. (2003) Module networks: identifying regulatory modules and their condition specific regulators from gene expression data. Nat Genet 34, 166-176.
95. Shannon, C.E. (1948) A mathematical theory of communication. AT&T Tech J (Bell Syst Tech J) 27, 379-423 623-656.
96. Shibata, K., Ishimura, A. & Maéno, M. (1998) GATA-1 inhibits the formation of notochord and neural tissue in Xenopus embryo. Biochem Biophys Res Commun 252, 241-248.
97. Sieniutycz, S. & Jeżowski, J. (2009) Energy Optimization in Process Systems E-book. Elsevier, Boston.
98. Somel, M., Franz, H., Yan, Z., Lorenc, A., Guo, S., Giger, T., Kelso, J., Nickel, B., Dannemann, M., Bahn, S., Webster, M.J., Weickert, C.S., Lachmann, M., Pääbo, S. & Khaitovich, P. (2009) Transcriptional neoteny in the human brain. Proc Natl Acad Sci U S A 106, 5743-5748.
99. Somel, M., Guo, S., Fu, N., Yan, Z., Hu, H.Y., Xu, Y., Yuan, Y., Ning, Z., Hu, Y., Menzel, C., Hu, H., Lachmann, M., Zeng, R., Chen, W. & Khaitovich, P. (2010) MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain. Genome Res 20, 1207-1218.
100. Stead, J.D., Neal, C., Meng, F., Wang, Y., Evans, S., Vazquez, D.M., Watson, S.J. & Akil, H. (2006) Transcriptional profiling of the developing rat brain reveals that the most dramatic regional differentiation in gene expression occurs postpartum. J Neurosci 26, 345-353.
101. Stretavan, D.W., Shatz, C.J. & Stryker, M.P. (1988) Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin. Nature 336, 468-471.
102. Thayer, M.J., Tapscott, S.J., Davis, R.L., Wright, W.E., Lassar, A.B. & Weintraub, H. (1989) Positive autoregulation of the myogenic determination gene MyoD1. Cell 58, 241-248.
103. Torkamani, A., Dean, B., Schork, N.J. & Thomas, E.A. (2010) Coexpression network analysis of neural tissue reveals perturbations in developmental processes in schizophrenia. Genome Res 20, 403-412.
104. Tsallis, C. (1988) Possible generalization of Boltzmann-Gibbs statistics. J Stat Phys 52, 479-487.
105. Tsigelny, I., Burton, D.W., Sharikov, Y., Hastings, R.H. & Deftos, L.J. (2005a) Coherent expression chromosome cluster analysis reveals differential regulatory functions of amino-terminal and distal parathyroid hormone-related protein domains in prostate carcinoma. J Biomed Biotechnol 4, 353-363.
106. Tsigelny, I., Hotchko, M., Yuan, J.X. & Keller, S.H. (2005b) Identification of molecular determinants that modulate trafficking of DeltaF508 CFTR, the mutant ABC transporter associated with cystic fibrosis. Cell Biochem Biophys 42, 41-53.
107. Tsigelny, I.F., Kouznetsova, V.L., Sweeney, D.E., Wu, W., Bush, K.T. & Nigam, S.K. (2008) Analysis of metagene portraits reveals distinct transitions during kidney organogenesis. Sci Signal 1, ra16.
108. Tsigelny, I.F., Kovalskyy, D., Kouznetsova, V.L., Balinskyi, O., Sharikov, Y., Bhatnagar, V. & Nigam, S.K. (2011) Conformational changes of the multispecific transporter organic anion transporter 1 (OAT1/SLC22A6) suggests a molecular mechanism for initial stages of drug and metabolite transport. Cell Biochem Biophys 61, 251-259.
109. Ueno, M., Tomita, S., Ueki, M., Iwanaga, Y., Huang, C.-I., Onodera, M., Maekava, N., Gonzalez, F.J. & Sakamoto, H. (2006) Two pathways of apoptosis are simultaneously induced in the embryonal brains of neural cell-specific HIF-1α-deficient mice. Histochem Cell Biol 125, 535-544.
110. Walther, C. & Gruss P. (1991) Pax-6, a murine paired box gene, is expressed in the developing CNS. Development 113, 1435-1449.
111. Wei, K., Chen, J., Akrami, K., Galbraith, G.C., Lopez, I.A. & Chen, F. (2007) Neural crest cell deficiency of c-myc causes skull and hearing defects. Genesis 45, 382-390.
112. Wolpert, L. (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25, 1-47.
113. Yamada, K., Matsuzaki, S., Hattori, T., Kuwahara, R., Taniguchi, M., Hashimoto, H., Shintani, N., Baba, A., Kumamoto, N., Yamada, K., Yoshikawa, T., Katayama, T. & Tohyama, M. (2010) Increased stathmin1 expression in the dentate gyrus of mice causes abnormal axonal arborizations. PLoS One 5, e8596.
114. Yu, Y., Platoshyn, O., Safrina, O., Tsigelny, I., Yuan, J.X. & Keller, S.H. (2007) Cystic fibrosis transmembrane conductance regulator (CFTR) functionality is dependent on coatomer protein I (COPI). Biol Cell 99, 433-444.