Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development

Kunwar AJ, Rickmann M, Backofen B, Browski SM, Rosenbusch J, Schoening S, Fleischmann T, Krieglstein K, Fischer von Mollard G (2011)
Proceedings of the National Academy of Sciences 108(6): 2575-2580.

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DOI
Autor*in
Kunwar, Ajaya J.; Rickmann, Michael; Backofen, Bianca; Browski, Sascha M.UniBi; Rosenbusch, Joachim; Schoening, Susanne; Fleischmann, Thomas; Krieglstein, Kerstin; Fischer von Mollard, GabrieleUniBi
Einrichtung
Centrum für Biotechnologie > Institut für Biochemie und Biotechnik
Fakultät für Chemie > Biochemie III
Centrum für Biotechnologie > Arbeitsgruppe G. Fischer von Mollard
Abstract / Bemerkung
Fusion between membranes is mediated by specific SNARE complexes. Here we report that fibroblasts survive the absence of the trans-Golgi network/early endosomal SNARE vti1a and the late endosomal SNARE vti1b with intact organelle morphology and minor trafficking defects. Because vti1a and vti1b are the only members of their SNARE subclass and the yeast homolog Vti1p is essential for cell survival, these data suggest that more distantly related SNAREs acquired the ability to function in endosomal traffic during evolution. However, absence of vti1a and vti1b resulted in perinatal lethality. Major axon tracts were missing, reduced in size, or misrouted in Vti1a(-/-) Vti1b(-/-) embryos. Progressive neurodegeneration was observed in most Vti1a(-/-) Vti1b(-/-) peripheral ganglia. Neurons were reduced by more than 95% in Vti1a(-/-) Vti1b(-/-) dorsal root and geniculate ganglia at embryonic day 18.5. These data suggest that special demands for endosomal membrane traffic could not be met in Vti1a(-/-) Vti1b(-/-) neurons. Vti1a(-/-) and Vti1b(-/-) single deficient mice were viable without these neuronal defects, indicating that they can substitute for each other in these processes.
Stichworte
endosome; neurite outgrowth; neuronal survival
Erscheinungsjahr
2011
Zeitschriftentitel
Proceedings of the National Academy of Sciences
Band
108
Ausgabe
6
Seite(n)
2575-2580
ISSN
0027-8424
eISSN
1091-6490
Page URI
https://pub.uni-bielefeld.de/record/2093998

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Kunwar AJ, Rickmann M, Backofen B, et al. Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proceedings of the National Academy of Sciences. 2011;108(6):2575-2580.
Kunwar, A. J., Rickmann, M., Backofen, B., Browski, S. M., Rosenbusch, J., Schoening, S., Fleischmann, T., et al. (2011). Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proceedings of the National Academy of Sciences, 108(6), 2575-2580. https://doi.org/10.1073/pnas.1013891108
Kunwar, Ajaya J., Rickmann, Michael, Backofen, Bianca, Browski, Sascha M., Rosenbusch, Joachim, Schoening, Susanne, Fleischmann, Thomas, Krieglstein, Kerstin, and Fischer von Mollard, Gabriele. 2011. “Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development”. Proceedings of the National Academy of Sciences 108 (6): 2575-2580.
Kunwar, A. J., Rickmann, M., Backofen, B., Browski, S. M., Rosenbusch, J., Schoening, S., Fleischmann, T., Krieglstein, K., and Fischer von Mollard, G. (2011). Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proceedings of the National Academy of Sciences 108, 2575-2580.
Kunwar, A.J., et al., 2011. Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proceedings of the National Academy of Sciences, 108(6), p 2575-2580.
A.J. Kunwar, et al., “Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development”, Proceedings of the National Academy of Sciences, vol. 108, 2011, pp. 2575-2580.
Kunwar, A.J., Rickmann, M., Backofen, B., Browski, S.M., Rosenbusch, J., Schoening, S., Fleischmann, T., Krieglstein, K., Fischer von Mollard, G.: Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proceedings of the National Academy of Sciences. 108, 2575-2580 (2011).
Kunwar, Ajaya J., Rickmann, Michael, Backofen, Bianca, Browski, Sascha M., Rosenbusch, Joachim, Schoening, Susanne, Fleischmann, Thomas, Krieglstein, Kerstin, and Fischer von Mollard, Gabriele. “Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development”. Proceedings of the National Academy of Sciences 108.6 (2011): 2575-2580.

23 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Thalamocortical Afferents Innervate the Cortical Subplate much Earlier in Development in Primate than in Rodent.
Alzu'bi A, Homman-Ludiye J, Bourne JA, Clowry GJ., Cereb Cortex 29(4), 2019
PMID: 30668846
Cumulative evidence for relationships between multiple variants in the VTI1A and TCF7L2 genes and cancer incidence.
Zhang M, Tang M, Fang Y, Cui H, Chen S, Li J, Xiong H, Lu J, Gu D, Zhang B., Int J Cancer 142(3), 2018
PMID: 28949031
Conserved Oligomeric Golgi and Neuronal Vesicular Trafficking.
Climer LK, Hendrix RD, Lupashin VV., Handb Exp Pharmacol 245(), 2018
PMID: 29063274
Endosomal and Phagosomal SNAREs.
Dingjan I, Linders PTA, Verboogen DRJ, Revelo NH, Ter Beest M, van den Bogaart G., Physiol Rev 98(3), 2018
PMID: 29790818
Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi.
Emperador-Melero J, Huson V, van Weering J, Bollmann C, Fischer von Mollard G, Toonen RF, Verhage M., Nat Commun 9(1), 2018
PMID: 30143604
Integrated Proteomics and Lipidomics Investigation of the Mechanism Underlying the Neuroprotective Effect of N-benzylhexadecanamide.
Zhou Y, Wang H, Guo F, Si N, Brantner A, Yang J, Han L, Wei X, Zhao H, Bian B., Molecules 23(11), 2018
PMID: 30424008
Somato-Dendritic Regulation of Raphe Serotonin Neurons; A Key to Antidepressant Action.
Quentin E, Belmer A, Maroteaux L., Front Neurosci 12(), 2018
PMID: 30618598
Selective molecular impairment of spontaneous neurotransmission modulates synaptic efficacy.
Crawford DC, Ramirez DM, Trauterman B, Monteggia LM, Kavalali ET., Nat Commun 8(), 2017
PMID: 28186166
A population study of binocular function.
Bosten JM, Goodbourn PT, Lawrance-Owen AJ, Bargary G, Hogg RE, Mollon JD., Vision Res 110(pt a), 2015
PMID: 25771401
Molecular underpinnings of synaptic vesicle pool heterogeneity.
Crawford DC, Kavalali ET., Traffic 16(4), 2015
PMID: 25620674
Defects in the COG complex and COG-related trafficking regulators affect neuronal Golgi function.
Climer LK, Dobretsov M, Lupashin V., Front Neurosci 9(), 2015
PMID: 26578865
The SNARE protein vti1a functions in dense-core vesicle biogenesis.
Walter AM, Kurps J, de Wit H, Schöning S, Toft-Bertelsen TL, Lauks J, Ziomkiewicz I, Weiss AN, Schulz A, Fischer von Mollard G, Verhage M, Sørensen JB., EMBO J 33(15), 2014
PMID: 24902738
Trans-ethnic genome-wide association study of colorectal cancer identifies a new susceptibility locus in VTI1A.
Wang H, Burnett T, Kono S, Haiman CA, Iwasaki M, Wilkens LR, Loo LW, Van Den Berg D, Kolonel LN, Henderson BE, Keku TO, Sandler RS, Signorello LB, Blot WJ, Newcomb PA, Pande M, Amos CI, West DW, Bézieau S, Berndt SI, Zanke BW, Hsu L, Genetics and Epidemiology of Colorectal Cancer Consortium (GECCO), Lindor NM, Haile RW, Hopper JL, Jenkins MA, Gallinger S, Casey G, Colon Cancer Family Registry (CCFR), Stenzel SL, Schumacher FR, Peters U, Gruber SB, Colorectal Transdisciplinary Study (CORECT), Tsugane S, Stram DO, Le Marchand L., Nat Commun 5(), 2014
PMID: 25105248
Molecular characterization and functional significance of the Vti family of SNARE proteins in tick salivary glands.
Villarreal AM, Adamson SW, Browning RE, Budachetri K, Sajid MS, Karim S., Insect Biochem Mol Biol 43(5), 2013
PMID: 23499931
Monocytes and macrophages as biomarkers for the diagnosis of megalencephalic leukoencephalopathy with subcortical cysts.
Petrini S, Minnone G, Coccetti M, Frank C, Aiello C, Cutarelli A, Ambrosini E, Lanciotti A, Brignone MS, D'Oria V, Strippoli R, De Benedetti F, Bertini E, Bracci-Laudiero L., Mol Cell Neurosci 56(), 2013
PMID: 23851226
The 8-oxoguanine DNA glycosylase 1 (ogg1) decreases the vulnerability of the developing brain to DNA damage.
Gu A, Ji G, Yan L, Zhou Y., DNA Repair (Amst) 12(12), 2013
PMID: 24075420
Transforming growth factor beta receptor 1 is increased following abstinence from cocaine self-administration, but not cocaine sensitization.
Gancarz-Kausch AM, Schroeder GL, Panganiban C, Adank D, Humby MS, Kausch MA, Clark SD, Dietz DM., PLoS One 8(12), 2013
PMID: 24386286
Vti1a identifies a vesicle pool that preferentially recycles at rest and maintains spontaneous neurotransmission.
Ramirez DM, Khvotchev M, Trauterman B, Kavalali ET., Neuron 73(1), 2012
PMID: 22243751
Absence of TI-VAMP/Vamp7 leads to increased anxiety in mice.
Danglot L, Zylbersztejn K, Petkovic M, Gauberti M, Meziane H, Combe R, Champy MF, Birling MC, Pavlovic G, Bizot JC, Trovero F, Della Ragione F, Proux-Gillardeaux V, Sorg T, Vivien D, D'Esposito M, Galli T., J Neurosci 32(6), 2012
PMID: 22323709
Ablation of vacuole protein sorting 18 (Vps18) gene leads to neurodegeneration and impaired neuronal migration by disrupting multiple vesicle transport pathways to lysosomes.
Peng C, Ye J, Yan S, Kong S, Shen Y, Li C, Li Q, Zheng Y, Deng K, Xu T, Tao W., J Biol Chem 287(39), 2012
PMID: 22854957
Targeting host syntaxin-5 preferentially blocks Leishmania parasitophorous vacuole development in infected cells and limits experimental Leishmania infections.
Canton J, Kima PE., Am J Pathol 181(4), 2012
PMID: 22885104
Genome-wide association analysis identifies new lung cancer susceptibility loci in never-smoking women in Asia.
Lan Q, Hsiung CA, Matsuo K, Hong YC, Seow A, Wang Z, Hosgood HD, Chen K, Wang JC, Chatterjee N, Hu W, Wong MP, Zheng W, Caporaso N, Park JY, Chen CJ, Kim YH, Kim YT, Landi MT, Shen H, Lawrence C, Burdett L, Yeager M, Yuenger J, Jacobs KB, Chang IS, Mitsudomi T, Kim HN, Chang GC, Bassig BA, Tucker M, Wei F, Yin Z, Wu C, An SJ, Qian B, Lee VH, Lu D, Liu J, Jeon HS, Hsiao CF, Sung JS, Kim JH, Gao YT, Tsai YH, Jung YJ, Guo H, Hu Z, Hutchinson A, Wang WC, Klein R, Chung CC, Oh IJ, Chen KY, Berndt SI, He X, Wu W, Chang J, Zhang XC, Huang MS, Zheng H, Wang J, Zhao X, Li Y, Choi JE, Su WC, Park KH, Sung SW, Shu XO, Chen YM, Liu L, Kang CH, Hu L, Chen CH, Pao W, Kim YC, Yang TY, Xu J, Guan P, Tan W, Su J, Wang CL, Li H, Sihoe AD, Zhao Z, Chen Y, Choi YY, Hung JY, Kim JS, Yoon HI, Cai Q, Lin CC, Park IK, Xu P, Dong J, Kim C, He Q, Perng RP, Kohno T, Kweon SS, Chen CY, Vermeulen R, Wu J, Lim WY, Chen KC, Chow WH, Ji BT, Chan JK, Chu M, Li YJ, Yokota J, Li J, Chen H, Xiang YB, Yu CJ, Kunitoh H, Wu G, Jin L, Lo YL, Shiraishi K, Chen YH, Lin HC, Wu T, Wu YL, Yang PC, Zhou B, Shin MH, Fraumeni JF, Lin D, Chanock SJ, Rothman N., Nat Genet 44(12), 2012
PMID: 23143601
Both pre- and postsynaptic activity of Nsf prevents degeneration of hair-cell synapses.
Mo W, Nicolson T., PLoS One 6(11), 2011
PMID: 22073277

46 References

Daten bereitgestellt von Europe PubMed Central.

Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth.
Martinez-Arca S, Alberts P, Zahraoui A, Louvard D, Galli T., J. Cell Biol. 149(4), 2000
PMID: 10811829
Severe peripheral sensory neuron loss and modest motor neuron reduction in mice with combined deficiency of brain-derived neurotrophic factor, neurotrophin 3 and neurotrophin 4/5.
Liu X, Jaenisch R., Dev. Dyn. 218(1), 2000
PMID: 10822262
Syntaxin 13 is a developmentally regulated SNARE involved in neurite outgrowth and endosomal trafficking.
Hirling H, Steiner P, Chaperon C, Marsault R, Regazzi R, Catsicas S., Eur. J. Neurosci. 12(6), 2000
PMID: 10886332
The SNARE Vti1a-beta is localized to small synaptic vesicles and participates in a novel SNARE complex.
Antonin W, Riedel D, von Mollard GF., J. Neurosci. 20(15), 2000
PMID: 10908612
A SNARE complex mediating fusion of late endosomes defines conserved properties of SNARE structure and function.
Antonin W, Holroyd C, Fasshauer D, Pabst S, Von Mollard GF, Jahn R., EMBO J. 19(23), 2000
PMID: 11101518
Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform.
Mallard F, Tang BL, Galli T, Tenza D, Saint-Pol A, Yue X, Antony C, Hong W, Goud B, Johannes L., J. Cell Biol. 156(4), 2002
PMID: 11839770
The SNAREs vti1a and vti1b have distinct localization and SNARE complex partners.
Kreykenbohm V, Wenzel D, Antonin W, Atlachkine V, von Mollard GF., Eur. J. Cell Biol. 81(5), 2002
PMID: 12067063
Deletion of the SNARE vti1b in mice results in the loss of a single SNARE partner, syntaxin 8.
Atlashkin V, Kreykenbohm V, Eskelinen EL, Wenzel D, Fayyazi A, Fischer von Mollard G., Mol. Cell. Biol. 23(15), 2003
PMID: 12861006
A dual mechanism controlling the localization and function of exocytic v-SNAREs.
Martinez-Arca S, Rudge R, Vacca M, Raposo G, Camonis J, Proux-Gillardeaux V, Daviet L, Formstecher E, Hamburger A, Filippini F, D'Esposito M, Galli T., Proc. Natl. Acad. Sci. U.S.A. 100(15), 2003
PMID: 12853575
Cross talk between tetanus neurotoxin-insensitive vesicle-associated membrane protein-mediated transport and L1-mediated adhesion.
Alberts P, Rudge R, Hinners I, Muzerelle A, Martinez-Arca S, Irinopoulou T, Marthiens V, Tooze S, Rathjen F, Gaspar P, Galli T., Mol. Biol. Cell 14(10), 2003
PMID: 14517330
Characterization of the in vitro retrograde transport of MPR46.
Medigeshi GR, Schu P., Traffic 4(11), 2003
PMID: 14617361
The mechanisms of vesicle budding and fusion.
Bonifacino JS, Glick BS., Cell 116(2), 2004
PMID: 14744428
Retinal axon guidance: novel mechanisms for steering.
van Horck FP, Weinl C, Holt CE., Curr. Opin. Neurobiol. 14(1), 2004
PMID: 15018939
Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis.
Rao SK, Huynh C, Proux-Gillardeaux V, Galli T, Andrews NW., J. Biol. Chem. 279(19), 2004
PMID: 14993220
Combinatorial SNARE complexes with VAMP7 or VAMP8 define different late endocytic fusion events.
Pryor PR, Mullock BM, Bright NA, Lindsay MR, Gray SR, Richardson SC, Stewart A, James DE, Piper RC, Luzio JP., EMBO Rep. 5(6), 2004
PMID: 15133481
Complementary roles of BDNF and NT-3 in vestibular and auditory development.
Ernfors P, Van De Water T, Loring J, Jaenisch R., Neuron 14(6), 1995
PMID: 7605630
Neither type of mannose 6-phosphate receptor is sufficient for targeting of lysosomal enzymes along intracellular routes.
Kasper D, Dittmer F, von Figura K, Pohlmann R., J. Cell Biol. 134(3), 1996
PMID: 8707842
Timing of neuronal death in trkA, trkB and trkC mutant embryos reveals developmental changes in sensory neuron dependence on Trk signalling.
Pinon LG, Minichiello L, Klein R, Davies AM., Development 122(10), 1996
PMID: 8898237
The yeast v-SNARE Vti1p mediates two vesicle transport pathways through interactions with the t-SNAREs Sed5p and Pep12p.
von Mollard GF, Nothwehr SF, Stevens TH., J. Cell Biol. 137(7), 1997
PMID: 9199167
Absence of sensory neurons before target innervation in brain-derived neurotrophic factor-, neurotrophin 3-, and TrkC-deficient embryonic mice.
Liebl DJ, Tessarollo L, Palko ME, Parada LF., J. Neurosci. 17(23), 1997
PMID: 9364058
Amphiphysin I antisense oligonucleotides inhibit neurite outgrowth in cultured hippocampal neurons.
Mundigl O, Ochoa GC, David C, Slepnev VI, Kabanov A, De Camilli P., J. Neurosci. 18(1), 1998
PMID: 9412489
A human homolog can functionally replace the yeast vesicle-associated SNARE Vti1p in two vesicle transport pathways.
Fischer von Mollard G, Stevens TH., J. Biol. Chem. 273(5), 1998
PMID: 9446565
Three novel proteins of the syntaxin/SNAP-25 family.
Steegmaier M, Yang B, Yoo JS, Huang B, Shen M, Yu S, Luo Y, Scheller RH., J. Biol. Chem. 273(51), 1998
PMID: 9852078
The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole.
Fischer von Mollard G, Stevens TH., Mol. Biol. Cell 10(6), 1999
PMID: 10359592
Pincher-mediated macroendocytosis underlies retrograde signaling by neurotrophin receptors.
Valdez G, Akmentin W, Philippidou P, Kuruvilla R, Ginty DD, Halegoua S., J. Neurosci. 25(21), 2005
PMID: 15917464
Functions and mechanisms of retrograde neurotrophin signalling.
Zweifel LS, Kuruvilla R, Ginty DD., Nat. Rev. Neurosci. 6(8), 2005
PMID: 16062170
Gene silencing reveals a specific function of hVps34 phosphatidylinositol 3-kinase in late versus early endosomes.
Johnson EE, Overmeyer JH, Gunning WT, Maltese WA., J. Cell. Sci. 119(Pt 7), 2006
PMID: 16522686
A role for synaptotagmin VII-regulated exocytosis of lysosomes in neurite outgrowth from primary sympathetic neurons.
Arantes RM, Andrews NW., J. Neurosci. 26(17), 2006
PMID: 16641243
Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression.
Holt M, Varoqueaux F, Wiederhold K, Takamori S, Urlaub H, Fasshauer D, Jahn R., J. Biol. Chem. 281(25), 2006
PMID: 16621800
SNAREs--engines for membrane fusion.
Jahn R, Scheller RH., Nat. Rev. Mol. Cell Biol. 7(9), 2006
PMID: 16912714
Commissure formation in the mammalian forebrain.
Lindwall C, Fothergill T, Richards LJ., Curr. Opin. Neurobiol. 17(1), 2007
PMID: 17275286
Syntaxin 16 and syntaxin 5 are required for efficient retrograde transport of several exogenous and endogenous cargo proteins.
Amessou M, Fradagrada A, Falguieres T, Lord JM, Smith DC, Roberts LM, Lamaze C, Johannes L., J. Cell. Sci. 120(Pt 8), 2007
PMID: 17389686
An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system.
Kloepper TH, Kienle CN, Fasshauer D., Mol. Biol. Cell 18(9), 2007
PMID: 17596510
The retromer complex influences Wnt secretion by recycling wntless from endosomes to the trans-Golgi network.
Belenkaya TY, Wu Y, Tang X, Zhou B, Cheng L, Sharma YV, Yan D, Selva EM, Lin X., Dev. Cell 14(1), 2007
PMID: 18160348
A syntaxin 10-SNARE complex distinguishes two distinct transport routes from endosomes to the trans-Golgi in human cells.
Ganley IG, Espinosa E, Pfeffer SR., J. Cell Biol. 180(1), 2008
PMID: 18195106
Syntaxin 16 is enriched in neuronal dendrites and may have a role in neurite outgrowth.
Chua CE, Tang BL., Mol. Membr. Biol. 25(1), 2008
PMID: 17852734
Syntaxin 6 regulates nerve growth factor-dependent neurite outgrowth.
Kabayama H, Tokushige N, Takeuchi M, Mikoshiba K., Neurosci. Lett. 436(3), 2008
PMID: 18406529
New insights into the mechanisms of macroautophagy in mammalian cells.
Eskelinen EL., Int Rev Cell Mol Biol 266(), 2008
PMID: 18544495
SNAREing the basis of multicellularity: consequences of protein family expansion during evolution.
Kloepper TH, Kienle CN, Fasshauer D., Mol. Biol. Evol. 25(9), 2008
PMID: 18621745
Identification of a developmentally regulated pathway of membrane retrieval in neuronal growth cones.
Bonanomi D, Fornasiero EF, Valdez G, Halegoua S, Benfenati F, Menegon A, Valtorta F., J. Cell. Sci. 121(Pt 22), 2008
PMID: 18940911
Endocytosis and intracellular trafficking of ErbBs.
Sorkin A, Goh LK., Exp. Cell Res. 315(4), 2009
PMID: 19278030
Plasma membrane expansion: a neuron's Herculean task.
Pfenninger KH., Nat. Rev. Neurosci. 10(4), 2009
PMID: 19259102
Roles of endosomal trafficking in neurite outgrowth and guidance.
Sann S, Wang Z, Brown H, Jin Y., Trends Cell Biol. 19(7), 2009
PMID: 19540123
Combinational soluble N-ethylmaleimide-sensitive factor attachment protein receptor proteins VAMP8 and Vti1b mediate fusion of antimicrobial and canonical autophagosomes with lysosomes.
Furuta N, Fujita N, Noda T, Yoshimori T, Amano A., Mol. Biol. Cell 21(6), 2010
PMID: 20089838
Loss of SNAP29 impairs endocytic recycling and cell motility.
Rapaport D, Lugassy Y, Sprecher E, Horowitz M., PLoS ONE 5(3), 2010
PMID: 20305790
Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis.
Gupton SL, Gertler FB., Dev. Cell 18(5), 2010
PMID: 20493807
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