RAB GTPases and RAB-interacting proteins and their role in the control of cognitive functions

Neuroscience and Biobehavioral Reviews

Volumn 46, Issue P2, 2014, Pages 302-314

  D'Adamo, Patrizia ^a,b   Masetti, Michela ^a   Bianchi, Veronica ^a,b   Morè, Lorenzo ^a   Mignogna, Maria Lidia ^a,b   Giannandrea, Maila ^a,c   Gatti, Silvia ^c  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

Brain development; G proteins; GDI1; GTPase; Intellectual disability; RAB

Indexed keywords

CALCIUM; CELL PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EXCITATORY AMINO ACID TRANSPORTER 1; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE; PROTEIN KINASE CIOTA; PURINERGIC P2X3 RECEPTOR; RAB PROTEIN; RAB11 PROTEIN; RAB15 PROTEIN; RAB17 PROTEIN; RAB21 PROTEIN; RAB22B PROTEIN; RAB27B PROTEIN; RAB33A PROTEIN; RAB39B PROTEIN; RAB3B PROTEIN; RAB3C PROTEIN; RAB7 PROTEIN; RAB8 PROTEIN; RAB9B PROTEIN; RGS4 PROTEIN; SOMATOSTATIN RECEPTOR 3; SYNAPSIN; UNCLASSIFIED DRUG; AGENTS AFFECTING WATER, MOLECULE OR ION TRANSPORT; NERVE PROTEIN; PROTEIN BINDING;

ASTROCYTE; AUTISM; CALCIUM TRANSPORT; CELL MIGRATION; COGNITION; DOWN REGULATION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME LOCALIZATION; ENZYME REGULATION; EXOCYTOSIS; GENE; GENETIC ASSOCIATION; GLIA CELL; GOLGI COMPLEX; HUMAN; INTERNALIZATION; LEARNING; MEMORY; MORPHOGENESIS; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAB11FIP5 GENE; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TRANS GOLGI NETWORK; ANIMAL; CENTRAL NERVOUS SYSTEM; COGNITIVE DEFECT; DISEASE MODEL; GENETICS; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; NEUROLOGIC DISEASE; PHYSIOLOGY;

ANIMALS; CENTRAL NERVOUS SYSTEM; COGNITION; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; HUMANS; MEMBRANE TRANSPORT MODULATORS; NERVE TISSUE PROTEINS; NERVOUS SYSTEM DISEASES; NEUROGLIA; NEURONS; PROTEIN BINDING; RAB GTP-BINDING PROTEINS;

EID: 84909965921     PISSN: 01497634     EISSN: 18737528     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2013.12.009     Document Type: Review

References (146)

1. Abderrahmani A., Plaisance V., Lovis P., Regazzi R. Mechanisms controlling the expression of the components of the exocytotic apparatus under physiological and pathological conditions. Biochem Soc Trans 2006, 34:696-700.
2. Aligianis I.A., Johnson C.A., Gissen P., Chen D., Hampshire D., Hoffmann K., Maina E.N., Morgan N.V., Tee L., Morton J., Ainsworth J.R., Horn D., Rosser E., Cole T.R., Stolte-Dijkstra I., Fieggen K., Clayton-Smith J., Megarbane A., Shield J.P., Newbury-Ecob R., Dobyns W.B., Graham J.M., Kjaer K.W., Warburg M., Bond J., Trembath R.C., Harris L.W., Takai Y., Mundlos S., Tannahill D., Woods C.G., Maher E.R. Mutations of the catalytic subunit of RAB3GAP cause Warburg Micro syndrome. Nature genetics 2005, 37:221-223.
3. Allan B.B., Moyer B.D., Balch W.E. Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science 2000, 289:444-448.
4. Anitei M., Cowan A.E., Pfeiffer S.E., Bansal R. Role for Rab3a in oligodendrocyte morphological differentiation. J Neurosci Res 2009, 87:342-352.
5. Barnekow A., Thyrock A., Kessler D. Chapter 5: rab proteins and their interaction partners. Int Rev Cell Mol Biol 2009, 274:235-274.
6. Barr F., Lambright D.G. Rab GEFs and GAPs. Curr Opin Cell Biol 2010, 22:461-470.
7. Bastin G., Heximer S.P. Rab Family Proteins Regulate the Endosomal Trafficking and Function of RGS4. J Biol Chem 2013, 288:21836-21849.
8. BasuRay S., Mukherjee S., Romero E.G., Seaman M.N., Wandinger-Ness A. Rab7 mutants associated with Charcot-Marie-Tooth disease cause delayed growth factor receptor transport and altered endosomal and nuclear signaling. J Biol Chem 2013, 288:1135-1149.
9. Bem D., Yoshimura S., Nunes-Bastos R., Bond F.C., Kurian M.A., Rahman F., Handley M.T., Hadzhiev Y., Masood I., Straatman-Iwanowska A.A., Cullinane A.R., McNeill A., Pasha S.S., Kirby G.A., Foster K., Ahmed Z., Morton J.E., Williams D., Graham J.M., Dobyns W.B., Burglen L., Ainsworth J.R., Gissen P., Muller F., Maher E.R., Barr F.A., Aligianis I.A. Loss-of-function mutations in RAB18 cause Warburg micro syndrome. American journal of human genetics 2011, 88:499-507.
10. Bespalov A., Klein C., Behl B., Gross G., Schoemaker H. Development of disease-modifying treatment of schizophrenia. Handb Exp Pharmacol 2012, 419-442.
11. Bianchi V., Farisello P., Baldelli P., Meskenaite V., Milanese M., Vecellio M., Muhlemann S., Lipp H.P., Bonanno G., Benfenati F., Toniolo D., D'Adamo P. Cognitive impairment in Gdi1-deficient mice is associated with altered synaptic vesicle pools and short-term synaptic plasticity, and can be corrected by appropriate learning training. Hum Mol Genet 2009, 18:105-117.
12. Bianchi V., Gambino F., Muzio L., Toniolo D., Humeau Y., D'Adamo P. Forebrain deletion of alphaGDI in adult mice worsens the pre-synaptic deficit at cortico-lateral amygdala synaptic connections. PLoS One 2012, 7:e29763.
13. Bienvenu T., des Portes V., Saint Martin A., McDonell N., Billuart P., Carrie A., Vinet M.C., Couvert P., Toniolo D., Ropers H.H., Moraine C., van Bokhoven H., Fryns J.P., Kahn A., Beldjord C., Chelly J. Non-specific X-linked semidominant mental retardation by mutations in a Rab GDP-dissociation inhibitor. Hum Mol Genet 1998, 7:1311-1315.
14. Borck G., Wunram H., Steiert A., Volk A.E., Korber F., Roters S., Herkenrath P., Wollnik B., Morris-Rosendahl D.J., Kubisch C. A homozygous RAB3GAP2 mutation causes Warburg Micro syndrome. Hum Genet 2011, 129:45-50.
15. Brown T.C., Correia S.S., Petrok C.N., Esteban J.A. Functional compartmentalization of endosomal trafficking for the synaptic delivery of AMPA receptors during long-term potentiation. J Neurosci 2007, 27:13311-13315.
16. Brown T.C., Tran I.C., Backos D.S., Esteban J.A. NMDA receptor-dependent activation of the small GTPase Rab5 drives the removal of synaptic AMPA receptors during hippocampal LTD. Neuron 2005, 45:81-94.
17. Bucci C., Parton R.G., Mather I.H., Stunnenberg H., Simons K., Hoflack B., Zerial M. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992, 70:715-728.
18. Burgo A., Proux-Gillardeaux V., Sotirakis E., Bun P., Casano A., Verraes A., Liem R.K., Formstecher E., Coppey-Moisan M., Galli T. A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev Cell 2012, 23:166-180.
19. Calakos N., Schoch S., Sudhof T.C., Malenka R.C. Multiple roles for the active zone protein RIM1alpha in late stages of neurotransmitter release. Neuron 2004, 42:889-896.
20. Castillo P.E., Janz R., Sudhof T.C., Tzounopoulos T., Malenka R.C., Nicoll R.A. Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature 1997, 388:590-593.
21. Castillo P.E., Schoch S., Schmitz F., Sudhof T.C., Malenka R.C. RIM1alpha is required for presynaptic long-term potentiation. Nature 2002, 415:327-330.
22. Chaufty J., Sullivan S.E., Ho A. Intracellular amyloid precursor protein sorting and amyloid-beta secretion are regulated by Src-mediated phosphorylation of Mint2. J Neurosci 2012, 32:9613-9625.
23. Chen R.H., Wislet-Gendebien S., Samuel F., Visanji N.P., Zhang G., Marsilio D., Langman T., Fraser P.E., Tandon A. alpha-Synuclein membrane association is regulated by the Rab3a recycling machinery and presynaptic activity. J Biol Chem 2013, 288:7438-7449.
24. Chen W., Feng Y., Chen D., Wandinger-Ness A. Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 1998, 9:3241-3257.
25. Chen X.Q., Wang B., Wu C., Pan J., Yuan B., Su Y.Y., Jiang X.Y., Zhang X., Bao L. Endosome-mediated retrograde axonal transport of P2X3 receptor signals in primary sensory neurons. Cell Res 2012, 22:677-696.
26. Cherfils J., Zeghouf M. Regulation of small GTPases by GEFs. GAPs, and GDIs. Physiol Rev 2013, 93:269-309.
27. Chevaleyre V., Heifets B.D., Kaeser P.S., Sudhof T.C., Castillo P.E. Endocannabinoid-mediated long-term plasticity requires cAMP/PKA signaling and RIM1alpha. Neuron 2007, 54:801-812.
28. Chi Z.L., Akahori M., Obazawa M., Minami M., Noda T., Nakaya N., Tomarev S., Kawase K., Yamamoto T., Noda S., Sasaoka M., Shimazaki A., Takada Y., Iwata T. Overexpression of optineurin E50K disrupts Rab8 interaction and leads to a progressive retinal degeneration in mice. Hum Mol Genet 2010, 19:2606-2615.
29. Chiurazzi P., Schwartz C.E., Gecz J., Neri G. XLMR genes: update 2007. Eur J Hum Genet 2008, 16:422-434.
30. Choudhury A., Dominguez M., Puri V., Sharma D.K., Narita K., Wheatley C.L., Marks D.L., Pagano R.E. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J Clin Invest 2002, 109:1541-1550.
31. Cogli L., Progida C., Thomas C.L., Spencer-Dene B., Donno C., Schiavo G., Bucci C. Charcot-Marie-Tooth type 2B disease-causing RAB7A mutant proteins show altered interaction with the neuronal intermediate filament peripherin. Acta Neuropathol 2013, 125:257-272.
32. Cooper A.A., Gitler A.D., Cashikar A., Haynes C.M., Hill K.J., Bhullar B., Liu K., Xu K., Strathearn K.E., Liu F., Cao S., Caldwell K.A., Caldwell G.A., Marsischky G., Kolodner R.D., Labaer J., Rochet J.C., Bonini N.M., Lindquist S. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 2006, 313:324-328.
33. Corbeel L., Freson K. Rab proteins and Rab-associated proteins: major actors in the mechanism of protein-trafficking disorders. Eur J Pediatr 2008, 167:723-729.
34. D'Adamo P., Menegon A., Lo Nigro C., Grasso M., Gulisano M., Tamanini F., Bienvenu T., Gedeon A.K., Oostra B., Wu S.K., Tandon A., Valtorta F., Balch W.E., Chelly J., Toniolo D. Mutations in GDI1 are responsible for X-linked non-specific mental retardation. Nature genetics 1998, 19:134-139.
35. D'Adamo P., Welzl H., Papadimitriou S., Raffaele di Barletta M., Tiveron C., Tatangelo L., Pozzi L., Chapman P.F., Knevett S.G., Ramsay M.F., Valtorta F., Leoni C., Menegon A., Wolfer D.P., Lipp H.P., Toniolo D. Deletion of the mental retardation gene Gdi1 impairs associative memory and alters social behavior in mice. Hum Mol Genet 2002, 11:2567-2580.
36. D'Adamo P., Wolfer D.P., Kopp C., Tobler I., Toniolo D., Lipp H.P. Mice deficient for the synaptic vesicle protein Rab3a show impaired spatial reversal learning and increased explorative activity but none of the behavioral changes shown by mice deficient for the Rab3a regulator Gdi1. Eur J Neurosci 2004, 19:1895-1905.
37. Dalfo E., Gomez-Isla T., Rosa J.L., Nieto Bodelon M., Cuadrado Tejedor M., Barrachina M., Ambrosio S., Ferrer I. Abnormal alpha-synuclein interactions with Rab proteins in alpha-synuclein A30P transgenic mice. J Neuropathol Exp Neurol 2004, 63:302-313.
38. Darchen F., Goud B. Multiple aspects of Rab protein action in the secretory pathway: focus on Rab3 and Rab6. Biochimie 2000, 82:375-384.
39. Deinhardt K., Salinas S., Verastegui C., Watson R., Worth D., Hanrahan S., Bucci C., Schiavo G. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron 2006, 52:293-305.
40. Dejgaard S.Y., Murshid A., Erman A., Kizilay O., Verbich D., Lodge R., Dejgaard K., Ly-Hartig T.B., Pepperkok R., Simpson J.C., Presley J.F. Rab18 and Rab43 have key roles in ER-Golgi trafficking. J Cell Sci 2008, 121:2768-2781.
41. del Toro D., Alberch J., Lazaro-Dieguez F., Martin-Ibanez R., Xifro X., Egea G., Canals J.M. Mutant huntingtin impairs post-Golgi trafficking to lysosomes by delocalizing optineurin/Rab8 complex from the Golgi apparatus. Mol Biol Cell 2009, 20:1478-1492.
42. Deretic D., Huber L.A., Ransom N., Mancini M., Simons K., Papermaster D.S. rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J Cell Sci 1995, 108(Pt 1):215-224.
43. Dulubova I., Lou X., Lu J., Huryeva I., Alam A., Schneggenburger R., Sudhof T.C., Rizo J. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity?. Embo J 2005, 24:2839-2850.
44. Eggenschwiler J.T., Bulgakov O.V., Qin J., Li T., Anderson K.V. Mouse Rab23 regulates hedgehog signaling from smoothened to Gli proteins. Dev Biol 2006, 290:1-12.
45. Eggenschwiler J.T., Espinoza E., Anderson K.V. Rab23 is an essential negative regulator of the mouse Sonic hedgehog signalling pathway. Nature 2001, 412:194-198.
46. Elfrink H.L., Zwart R., Cavanillas M.L., Schindler A.J., Baas F., Scheper W. Rab6 is a modulator of the unfolded protein response: implications for Alzheimer's disease. J Alzheimers Dis 2012, 28:917-929.
47. Elias M. Patterns and processes in the evolution of the eukaryotic endomembrane system. Mol Membr Biol 2010, 27:469-489.
48. Esseltine J.L., Ribeiro F.M., Ferguson S.S. Rab8 modulates metabotropic glutamate receptor subtype 1 intracellular trafficking and signaling in a protein kinase C-dependent manner. J Neurosci 2012, 32:16933-16942.
49. Fischer von Mollard G., Mignery G.A., Baumert M., Perin M.S., Hanson T.J., Burger P.M., Jahn R., Sudhof T.C. rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc Natl Acad Sci U S A 1990, 87:1988-1992.
50. Fischer von Mollard G., Stahl B., Li C., Sudhof T.C., Jahn R. Rab proteins in regulated exocytosis. Trends Biochem Sci 1994, 19:164-168.
51. Fischer von Mollard G., Stahl B., Walch-Solimena C., Takei K., Daniels L., Khoklatchev A., De Camilli P., Sudhof T.C., Jahn R. Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur J Cell Biol 1994, 65:319-326.
52. Frasa M.A., Koessmeier K.T., Ahmadian M.R., Braga V.M. Illuminating the functional and structural repertoire of human TBC/RABGAPs. Nat Rev Mol Cell Biol 2012, 13:67-73.
53. Fukuda M. Regulation of secretory vesicle traffic by Rab small GTPases. Cell Mol Life Sci 2008, 65:2801-2813.
54. Fukuda M. How can mammalian Rab small GTPases be comprehensively analyzed?.: Development of new tools to comprehensively analyze mammalian Rabs in membrane traffic. Histol Histopathol 2010, 25:1473-1480.
55. Fukuda M. TBC proteins: GAPs for mammalian small GTPase Rab?. Biosci Rep 2011, 31:159-168.
56. Fukuda M. Rab27 effectors, pleiotropic regulators in secretory pathways. Traffic 2013, 14:949-963.
57. Ganley I.G., Carroll K., Bittova L., Pfeffer S. Rab9 GTPase regulates late endosome size and requires effector interaction for its stability. Mol Biol Cell 2004, 15:5420-5430.
58. Geppert M., Bolshakov V.Y., Siegelbaum S.A., Takei K., De Camilli P., Hammer R.E., Sudhof T.C. The role of Rab3A in neurotransmitter release. Nature 1994, 369:493-497.
59. Geppert M., Goda Y., Stevens C.F., Sudhof T.C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 1997, 387:810-814.
60. Gerges N.Z., Backos D.S., Esteban J.A. Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J Biol Chem 2004, 279:43870-43878.
61. Gerges N.Z., Brown T.C., Correia S.S., Esteban J.A. Analysis of Rab protein function in neurotransmitter receptor trafficking at hippocampal synapses. Methods Enzymol 2005, 403:153-166.
62. Giannandrea M., Bianchi V., Mignogna M.L., Sirri A., Carrabino S., D'Elia E., Vecellio M., Russo S., Cogliati F., Larizza L., Ropers H.H., Tzschach A., Kalscheuer V., Oehl-Jaschkowitz B., Skinner C., Schwartz C.E., Gecz J., Van Esch H., Raynaud M., Chelly J., de Brouwer A.P., Toniolo D., D'Adamo P. Mutations in the small GTPase gene RAB39B are responsible for X-linked mental retardation associated with autism, epilepsy, and macrocephaly. American journal of human genetics 2010, 86:185-195.
63. Ginsberg S.D., Mufson E.J., Alldred M.J., Counts S.E., Wuu J., Nixon R.A., Che S. Upregulation of select rab GTPases in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease. J Chem Neuroanat 2011, 42:102-110.
64. Giovedi S., Darchen F., Valtorta F., Greengard P., Benfenati F. Synapsin is a novel Rab3 effector protein on small synaptic vesicles. II. Functional effects of the Rab3A-synapsin I interaction. J Biol Chem 2004, 279:43769-43779.
65. Gitler A.D., Bevis B.J., Shorter J., Strathearn K.E., Hamamichi S., Su L.J., Caldwell K.A., Caldwell G.A., Rochet J.C., McCaffery J.M., Barlowe C., Lindquist S. The Parkinson's disease protein alpha-synuclein disrupts cellular Rab homeostasis. Proc Natl Acad Sci U S A 2008, 105:145-150.
66. Gonzalez L., Scheller R.H. Regulation of membrane trafficking: structural insights from a Rab/effector complex. Cell 1999, 96:755-758.
67. Gutierrez M.G., Munafo D.B., Beron W., Colombo M.I. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 2004, 117:2687-2697.
68. Handley M.T., Morris-Rosendahl D.J., Brown S., Macdonald F., Hardy C., Bem D., Carpanini S.M., Borck G., Martorell L., Izzi C., Faravelli F., Accorsi P., Pinelli L., Basel-Vanagaite L., Peretz G., Abdel-Salam G.M., Zaki M.S., Jansen A., Mowat D., Glass I., Stewart H., Mancini G., Lederer D., Roscioli T., Giuliano F., Plomp A.S., Rolfs A., Graham J.M., Seemanova E., Poo P., Garcia-Cazorla A., Edery P., Jackson I.J., Maher E.R., Aligianis I.A. Mutation spectrum in RAB3GAP1, RAB3GAP2, and RAB18 and genotype-phenotype correlations in warburg micro syndrome and Martsolf syndrome. Hum. Mutat. 2013, 34:686-696.
69. Harris K.P., Littleton J.T. Vesicle trafficking: a Rab family profile. Curr. Biol. 2011, 21:R841-R843.
70. Hensbroek R.A., Kamal A., Baars A.M., Verhage M., Spruijt B.M. Spatial, contextual and working memory are not affected by the absence of mossy fiber long-term potentiation and depression. Behav. Brain Res. 2003, 138:215-223.
71. Hernandez-Hernandez O., Guiraud-Dogan C., Sicot G., Huguet A., Luilier S., Steidl E., Saenger S., Marciniak E., Obriot H., Chevarin C., Nicole A., Revillod L., Charizanis K., Lee K.Y., Suzuki Y., Kimura T., Matsuura T., Cisneros B., Swanson M.S., Trovero F., Buisson B., Bizot J.C., Hamon M., Humez S., Bassez G., Metzger F., Buee L., Munnich A., Sergeant N., Gourdon G., Gomes-Pereira M. Myotonic dystrophy CTG expansion affects synaptic vesicle proteins, neurotransmission and mouse behaviour. Brain 2013, 136:957-970.
72. Houlden H., King R.H., Muddle J.R., Warner T.T., Reilly M.M., Orrell R.W., Ginsberg L. A novel RAB7 mutation associated with ulcero-mutilating neuropathy. Ann Neurol 2004, 56:586-590.
73. Huber L.A., Dupree P., Dotti C.G. A deficiency of the small GTPase rab8 inhibits membrane traffic in developing neurons. Mol Cell Biol 1995, 15:918-924.
74. Huber L.A., Pimplikar S., Parton R.G., Virta H., Zerial M., Simons K. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane. J. Cell Biol. 1993, 123:35-45.
75. Huerta P.T., Sun L.D., Wilson M.A., Tonegawa S. Formation of temporal memory requires NMDA receptors within CA1 pyramidal neurons. Neuron 2000, 25:473-480.
76. Ishizaki H., Miyoshi J., Kamiya H., Togawa A., Tanaka M., Sasaki T., Endo K., Mizoguchi A., Ozawa S., Takai Y. Role of rab GDP dissociation inhibitor alpha in regulating plasticity of hippocampal neurotransmission. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:11587-11592.
77. Itzen A., Goody R.S. GTPases involved in vesicular trafficking: structures and mechanisms. Semin. Cell Dev. Biol. 2011, 22:48-56.
78. Jenkins D., Baynam G., De Catte L., Elcioglu N., Gabbett M.T., Hudgins L., Hurst J.A., Jehee F.S., Oley C., Wilkie A.O. Carpenter syndrome: extended RAB23 mutation spectrum and analysis of nonsense-mediated mRNA decay. Hum Mutat 2011, 32:E2069-2078.
79. Kapfhamer D., Valladares O., Sun Y., Nolan P.M., Rux J.J., Arnold S.E., Veasey S.C., Bucan M. Mutations in Rab3a alter circadian period and homeostatic response to sleep loss in the mouse. Nat. Genet. 2002, 32:290-295.
80. Kenna K.P., McLaughlin R.L., Byrne S., Elamin M., Heverin M., Kenny E.M., Cormican P., Morris D.W., Donaghy C.G., Bradley D.G., Hardiman O. Delineating the genetic heterogeneity of ALS using targeted high-throughput sequencing. J Med Genet 2013, 50:776-783.
81. Kennedy M.J., Ehlers M.D. Organelles and trafficking machinery for postsynaptic plasticity. Annu. Rev. Neurosci. 2006, 29:325-362.
82. Khvotchev M.V., Ren M., Takamori S., Jahn R., Sudhof T.C. Divergent functions of neuronal Rab11b in Ca2+-regulated versus constitutive exocytosis. J Neurosci 2003, 23:10531-10539.
83. Klin A., Lin D.J., Gorrindo P., Ramsay G., Jones W. Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature 2009, 459:257-261.
84. Lai C., Xie C., Shim H., Chandran J., Howell B.W., Cai H. Regulation of endosomal motility and degradation by amyotrophic lateral sclerosis 2/alsin. Mol Brain 2009, 2:23.
85. Li C., Fan Y., Lan T.H., Lambert N.A., Wu G. Rab26 modulates the cell surface transport of alpha2-adrenergic receptors from the Golgi. J Biol Chem 2012, 287:42784-42794.
86. Li X., Sapp E., Chase K., Comer-Tierney L.A., Masso N., Alexander J., Reeves P., Kegel K.B., Valencia A., Esteves M., Aronin N., Difiglia M. Disruption of Rab11 activity in a knock-in mouse model of Huntington's disease. Neurobiol Dis 2009, 36:374-383.
87. Li X., Valencia A., McClory H., Sapp E., Kegel K.B., Difiglia M. Deficient Rab11 activity underlies glucose hypometabolism in primary neurons of Huntington's disease mice. Biochem Biophys Res Commun 2012, 421:727-730.
88. Lisik M.Z., Sieron A.L. X-linked mental retardation. Med. Sci. Monit. 2008, 14:RA221-RA229.
89. Liu S., Storrie B. Are Rab proteins the link between Golgi organization and membrane trafficking?. Cell. Mol. Life Sci. 2012, 69:4093-4106.
90. Lombardi D., Soldati T., Riederer M.A., Goda Y., Zerial M., Pfeffer S.R. Rab9 functions in transport between late endosomes and the trans Golgi network. Embo J 1993, 12:677-682.
91. Luiro K., Yliannala K., Ahtiainen L., Maunu H., Jarvela I., Kyttala A., Jalanko A. Interconnections of CLN3. Hook1 and Rab proteins link Batten disease to defects in the endocytic pathway. Hum Mol Genet 2004, 13:3017-3027.
92. Ma X., Fei E., Fu C., Ren H., Wang G. Dysbindin-1, a schizophrenia-related protein, facilitates neurite outgrowth by promoting the transcriptional activity of p53. Mol. Psychiatry 2011, 16:1105-1116.
93. MacLeod D.A., Rhinn H., Kuwahara T., Zolin A., Di Paolo G., McCabe B.D., Marder K.S., Honig L.S., Clark L.N., Small S.A., Abeliovich A. RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron 2013, 77:425-439.
94. Madani R., Kozlov S., Akhmedov A., Cinelli P., Kinter J., Lipp H.P., Sonderegger P., Wolfer D.P. Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol. Cell. Neurosci. 2003, 23:473-494.
95. Madison D.L., Kruger W.H., Kim T., Pfeiffer S.E. Differential expression of rab3 isoforms in oligodendrocytes and astrocytes. J. Neurosci. Res. 1996, 45:258-268.
96. Maier S., Reiterer V., Ruggiero A.M., Rothstein J.D., Thomas S., Dahm R., Sitte H.H., Farhan H. GTRAP 3-18 serves as a negative regulator of Rab1 in protein transport and neuronal differentiation. J. Cell. Mol. Med. 2009, 13:114-124.
97. Martelli A.M., Baldini G., Tabellini G., Koticha D., Bareggi R. Rab3A and Rab3D control the total granule number and the fraction of granules docked at the plasma membrane in PC12 cells. Traffic 2000, 1:976-986.
98. Meggouh F., Bienfait H.M., Weterman M.A., de Visser M., Baas F. Charcot-Marie-Tooth disease due to a de novo mutation of the RAB7 gene. Neurology 2006, 67:1476-1478.
99. Mellman I. Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 1996, 12:575-625.
100. Menasche G., Pastural E., Feldmann J., Certain S., Ersoy F., Dupuis S., Wulffraat N., Bianchi D., Fischer A., Le Deist F., de Saint Basile G. Mutations in RAB27A cause Griscelli syndrome associated with haemophagocytic syndrome. Nature genetics 2000, 25:173-176.
101. Mohrmann K., Gerez L., Oorschot V., Klumperman J., van der Sluijs P. Rab4 function in membrane recycling from early endosomes depends on a membrane to cytoplasm cycle. J Biol Chem 2002, 277:32029-32035.
102. More L., Gravius A., Pietraszek M., Belozertseva I., Malyshkin A., Shekunova E., Barberi C., Schaefer D., Schmidt W.J., Danysz W. Comparison of the mGluR1 antagonist A-841720 in rat models of pain and cognition. Behav. Pharmacol. 2007, 18:273-281.
103. Mori Y., Matsui T., Fukuda M. Rabex-5 protein regulates dendritic localization of small GTPase Rab17 and neurite morphogenesis in hippocampal neurons. J. Biol. Chem. 2013, 288:9835-9847.
104. Mori Y., Matsui T., Furutani Y., Yoshihara Y., Fukuda M. Small GTPase Rab17 regulates dendritic morphogenesis and postsynaptic development of hippocampal neurons. J. Biol. Chem. 2012, 287:8963-8973.
105. Moritz O.L., Tam B.M., Hurd L.L., Peranen J., Deretic D., Papermaster D.S. Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol Biol Cell 2001, 12:2341-2351.
106. Morton A.J., Faull R.L., Edwardson J.M. Abnormalities in the synaptic vesicle fusion machinery in Huntington's disease. Brain Res Bull 2001, 56:111-117.
107. Nakada-Tsukui K., Saito-Nakano Y., Ali V., Nozaki T. A retromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol. Biol. Cell 2005, 16:5294-5303.
108. Nakazawa H., Sada T., Toriyama M., Tago K., Sugiura T., Fukuda M., Inagaki N. Rab33a mediates anterograde vesicular transport for membrane exocytosis and axon outgrowth. J. Neurosci. 2012, 32:12712-12725.
109. Ng E.L., Tang B.L. Rab GTPases and their roles in brain neurons and glia. Brain Res. Rev. 2008, 58:236-246.
110. Pavlos N.J., Gronborg M., Riedel D., Chua J.J., Boyken J., Kloepper T.H., Urlaub H., Rizzoli S.O., Jahn R. Quantitative analysis of synaptic vesicle Rabs uncovers distinct yet overlapping roles for Rab3a and Rab27b in Ca2+-triggered exocytosis. J. Neurosci. 2010, 30:13441-13453.
111. Pavlos N.J., Jahn R. Distinct yet overlapping roles of Rab GTPases on synaptic vesicles. Small GTPases 2011, 2:77-81.
112. Pavlowsky A., Chelly J., Billuart P. Emerging major synaptic signaling pathways involved in intellectual disability. Mol. Psychiatry 2012, 17:682-693.
113. Pereira-Leal J.B., Seabra M.C. Evolution of the Rab family of small GTP-binding proteins. J. Mol. Biol. 2001, 313:889-901.
114. Pfeffer S.R. Rab GTPase regulation of membrane identity. Curr. Opin. Cell Biol. 2013, 25:414-419.
115. Pham T.V., Hartomo T.B., Lee M.J., Hasegawa D., Ishida T., Kawasaki K., Kosaka Y., Yamamoto T., Morikawa S., Yamamoto N., Kubokawa I., Mori T., Yanai T., Hayakawa A., Takeshima Y., Iijima K., Matsuo M., Nishio H., Nishimura N. Rab15 alternative splicing is altered in spheres of neuroblastoma cells. Oncol. Rep. 2012, 27:2045-2049.
116. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
117. Potokar M., Lacovich V., Chowdhury H.H., Kreft M., Zorec R. Rab4 and Rab5 GTPase are required for directional mobility of endocytic vesicles in astrocytes. Glia 2012, 60:594-604.
118. Quadrato G., Di Giovanni S. Gatekeeper between quiescence and differentiation: p53 in axonal outgrowth and neurogenesis. Int. Rev. Neurobiol. 2012, 105:71-89.
119. Ragozzino M.E., Unick K.E., Gold P.E. Hippocampal acetylcholine release during memory testing in rats: augmentation by glucose. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:4693-4698.
120. Roohi J., Tegay D.H., Pomeroy J.C., Burkett S., Stone G., Stanyon R., Hatchwell E. A de novo apparently balanced translocation [46,XY,t(2;9)(p13;p24)] interrupting RAB11FIP5 identifies a potential candidate gene for autism spectrum disorder. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2008, 147B:411-417.
121. Ropers H.H. Genetics of intellectual disability. Curr. Opin. Genet. Dev. 2008, 18:241-250.
122. Sanderson D.J., Good M.A., Seeburg P.H., Sprengel R., Rawlins J.N., Bannerman D.M. The role of the GluR-A (GluR1) AMPA receptor subunit in learning and memory. Prog. Brain Res. 2008, 169:159-178.
123. Sasidharan N., Sumakovic M., Hannemann M., Hegermann J., Liewald J.F., Olendrowitz C., Koenig S., Grant B.D., Rizzoli S.O., Gottschalk A., Eimer S. RAB-5 and RAB-10 cooperate to regulate neuropeptide release in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:18944-18949.
124. Schluter O.M., Khvotchev M., Jahn R., Sudhof T.C. Localization versus function of Rab3 proteins. Evidence for a common regulatory role in controlling fusion. J. Biol. Chem. 2002, 277:40919-40929.
125. Schluter O.M., Schmitz F., Jahn R., Rosenmund C., Sudhof T.C. A complete genetic analysis of neuronal Rab3 function. J. Neurosci. 2004, 24:6629-6637.
126. Schluter O.M., Schnell E., Verhage M., Tzonopoulos T., Nicoll R.A., Janz R., Malenka R.C., Geppert M., Sudhof T.C. Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J. Neurosci. 1999, 19:5834-5846.
127. Schoch S., Castillo P.E., Jo T., Mukherjee K., Geppert M., Wang Y., Schmitz F., Malenka R.C., Sudhof T.C. RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 2002, 415:321-326.
128. Seaman M.N., Harbour M.E., Tattersall D., Read E., Bright N. Membrane recruitment of the cargo-selective retromer subcomplex is catalysed by the small GTPase Rab7 and inhibited by the Rab-GAP TBC1D5. J. Cell Sci. 2009, 122:2371-2382.
129. Shirane M., Nakayama K.I. Protrudin induces neurite formation by directional membrane trafficking. Science 2006, 314:818-821.
130. Shupliakov O., Brodin L. Recent insights into the building and cycling of synaptic vesicles. Exp. Cell Res. 2010, 316:1344-1350.
131. Stenmark H. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 2009, 10:513-525.
132. Strick D.J., Elferink L.A. Rab15 effector protein: a novel protein for receptor recycling from the endocytic recycling compartment. Mol. Biol. Cell 2005, 16:5699-5709.
133. Teber I., Nagano F., Kremerskothen J., Bilbilis K., Goud B., Barnekow A. Rab6 interacts with the mint3 adaptor protein. Biol. Chem. 2005, 386:671-677.
134. Tisdale E.J., Artalejo C.R. Src-dependent aprotein kinase C iota/lambda (aPKCiota/lambda) tyrosine phosphorylation is required for aPKCiota/lambda association with Rab2 and glyceraldehyde-3-phosphate dehydrogenase on pre-Golgi intermediates. J. Biol. Chem. 2006, 281:8436-8442.
135. Torisu H., Iwaki A., Takeshita K., Hiwatashi A., Sanefuji M., Fukumaki Y., Hara T. Clinical and genetic characterization of a 2-year-old boy with complete PLP1 deletion. Brain Dev. 2012, 34:852-856.
136. Touchot N., Chardin P., Tavitian A. Four additional members of the ras gene superfamily isolated by an oligonucleotide strategy: molecular cloning of YPT-related cDNAs from a rat brain library. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:8210-8214.
137. Tower-Gilchrist C., Lee E., Sztul E. Endosomal trafficking of the G protein-coupled receptor somatostatin receptor 3. Biochem. Biophys. Res. Commun. 2011, 413:555-560.
138. Tremml P., Lipp H.P., Muller U., Ricceri L., Wolfer D.P. Neurobehavioral development, adult openfield exploration and swimming navigation learning in mice with a modified beta-amyloid precursor protein gene. Behav. Brain Res. 1998, 95:65-76.
139. Tsetsenis T., Younts T.J., Chiu C.Q., Kaeser P.S., Castillo P.E., Sudhof T.C. Rab3B protein is required for long-term depression of hippocampal inhibitory synapses and for normal reversal learning. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14300-14305.
140. Turner L.A., Hale C.A., Borkowski J.G. Influence of intelligence on memory development. Am. J. Ment. Retard. 1996, 100:468-480.
141. van Vlijmen T., Vleugel M., Evers M., Mohammed S., Wulf P.S., Heck A.J., Hoogenraad C.C., van der Sluijs P. A unique residue in rab3c determines the interaction with novel binding protein Zwint-1. FEBS Lett. 2008, 582:2838-2842.
142. Vissers L.E., de Ligt J., Gilissen C., Janssen I., Steehouwer M., de Vries P., van Lier B., Arts P., Wieskamp N., del Rosario M., van Bon B.W., Hoischen A., de Vries B.B., Brunner H.G., Veltman J.A. A de novo paradigm for mental retardation. Nat. Genet. 2010, 42:1109-1112.
143. Yamaguchi K., Tanaka M., Mizoguchi A., Hirata Y., Ishizaki H., Kaneko K., Miyoshi J., Takai Y. A GDP/GTP exchange protein for the Rab3 small G protein family up-regulates a postdocking step of synaptic exocytosis in central synapses. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:14536-14541.
144. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2001, 2:107-117.
145. Zhang K., Fishel Ben Kenan R., Osakada Y., Xu W., Sinit R.S., Chen L., Zhao X., Chen J.Y., Cui B., Wu C. Defective axonal transport of Rab7 GTPase results in dysregulated trophic signaling. J. Neurosci. 2013, 33:7451-7462.
146. Zhao S., Torii S., Yokota-Hashimoto H., Takeuchi T., Izumi T. Involvement of Rab27b in the regulated secretion of pituitary hormones. Endocrinology 2002, 143:1817-1824.