Cell type-specific transcriptomics of hypothalamic energy-sensing neuron responses to weight-loss

eLife

Volumn 4, Issue September 2015, 2015, Pages

  Henry, Fredrick E ^a   Sugino, Ken ^a   Tozer, Adam ^b   Branco, Tiago ^b   Sternson, Scott M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; G PROTEIN COUPLED RECEPTOR KINASE 6; NEUROPEPTIDE; OSTEOGENIN; PARVOVIRUS VECTOR; PROOPIOMELANOCORTIN; SYNAPTOTAGMIN; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 7; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; X BOX BINDING PROTEIN 1; AGRP PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARCUATE NUCLEUS; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; E BOX ELEMENT; ENDOPLASMIC RETICULUM STRESS; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IN SITU HYBRIDIZATION; FOOD DEPRIVATION; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; OLIGODENDROGLIA; POLYMERASE CHAIN REACTION; PROTEIN LOCALIZATION; RNA SEQUENCE; TRANSCRIPTOMICS; UPREGULATION; WEIGHT GAIN; WEIGHT REDUCTION; WHOLE CELL PATCH CLAMP; YOUNG ADULT; ANIMAL; CHEMISTRY; CYTOLOGY; HYPOTHALAMUS; PHYSIOLOGY; SENSORY NERVE CELL;

AGOUTI-RELATED PROTEIN; ANIMALS; GENE EXPRESSION PROFILING; HYPOTHALAMUS; MICE; PRO-OPIOMELANOCORTIN; SENSORY RECEPTOR CELLS; WEIGHT LOSS;

EID: 84943784819     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.09800     Document Type: Article

References (85)

1. Accili D, Seigneur EM, Panicker LM, Ren H, Chen C, Simonds WF. 2013. FoxO1 target Gpr17 activates AgRP neurons to regulate food intake. NCBI Gene Expression Omnibus GSE45858. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE45858.
2. Allison MB, Patterson CM, Krashes MJ, Lowell BB, Myers MG Jr, Olson DP. 2015. TRAP-seq defines markers for novel populations of hypothalamic and brainstem LepRb neurons. Molecular Metabolism 4:299-309. doi: 10.1016/j.molmet.2015.01.012.
3. Anders S, Pyl PT, Huber W. 2015. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31:166-169. doi: 10.1093/bioinformatics/btu638.
4. Aponte Y, Atasoy D, Sternson SM. 2011. AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nature Neuroscience 14:351-355. doi: 10.1038/nn.2739.
5. Atasoy D, Aponte Y, Su HH, Sternson SM. 2008. A FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. The Journal of Neuroscience 28:7025-7030. doi: 10.1523/JNEUROSCI.1954-08.2008.
6. Atasoy D, Betley JN, Su HH, Sternson SM. 2012. Deconstruction of a neural circuit for hunger. Nature 488:172-177. doi: 10.1038/nature11270.
7. Bandyopadhyay U, Cotney J, Nagy M, Oh S, Leng J, Mahajan M, Mane S, Fenton WA, Noonan JP, Horwich AL. 2013. RNA-Seq profiling of spinal cord motor neurons from a presymptomatic SOD1 ALS mouse. PLOS ONE 8:e53575. doi: 10.1371/journal.pone.0053575.
8. Banks AS, Davis SM, Bates SH, Myers MG Jr. 2000. Activation of downstream signals by the long form of the leptin receptor. The Journal of Biological Chemistry 275:14563-14572. doi: 10.1074/jbc.275.19.14563.
9. Bartos JA, Ulrich JD, Li H, Beazely MA, Chen Y, Macdonald JF, Hell JW. 2010. Postsynaptic clustering and activation of Pyk2 by PSD-95. The Journal of Neuroscience 30:449-463. doi: 10.1523/JNEUROSCI.4992-08.2010.
10. Baskin DG, Breininger JF, Schwartz MW. 1999. Leptin receptor mRNA identifies a subpopulation of neuropeptide Y neurons activated by fasting in rat hypothalamus. Diabetes 48:828-833. doi: 10.2337/diabetes.48.4.828.
11. Benosman S, Ravanan P, Correa RG, Hou YC, Yu M, Gulen MF, Li X, Thomas J, Cuddy M, Matsuzawa Y, Sano R, Diaz P, Matsuzawa S, Reed JC. 2013. Interleukin-1 receptor-associated kinase-2 (IRAK2) is a critical mediator of endoplasmic reticulum (ER) stress signaling. PLOS ONE 8:e64256. doi: 10.1371/journal.pone.0064256.
12. Betley JN, Xu S, Cao ZF, Gong R, Magnus CJ, Yu Y, Sternson SM. 2015. Neurons for hunger and thirst transmit a negative-valence teaching signal. Nature 521:180-185. doi: 10.1038/nature14416.
13. Boda B, Alberi S, Nikonenko I, Node-Langlois R, Jourdain P, Moosmayer M, Parisi-Jourdain L, Muller D. 2004. The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. The Journal of Neuroscience 24:10816-10825. doi: 10.1523/JNEUROSCI.2931-04.2004.
14. Bouret SG, Draper SJ, Simerly RB. 2004. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304:108-110. doi: 10.1126/science.1095004.
15. Broberger C, Johansen J, Johansson C, Schalling M, Hokfelt T. 1998. The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-treated mice. Proceedings of the National Academy of Sciences of USA 95:15043-15048. doi: 10.1073/pnas.95.25.15043.
16. Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G. 2004. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proceedings of the National Academy of Sciences of USA 101:11707-11712. doi: 10.1073/pnas.0306880101.
17. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, Christopherson KS, Xing Y, Lubischer JL, Krieg PA, Krupenko SA, Thompson WJ, Barres BA. 2008. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. The Journal of Neuroscience 28:264-278. doi: 10.1523/JNEUROSCI.4178-07.2008.
18. Cahoy JD, Emery B, Xing Y, Kaushal A. 2007. A Transcriptome Database for Astrocytes, Neurons, and Oligodendrocytes. NCBI Gene Expression Omnibus GSE9566. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE9566.
19. Cao P, Maximov A, Sudhof TC. 2011. Activity-dependent IGF-1 exocytosis is controlled by the Ca(2+)-sensor synaptotagmin-10. Cell 145:300-311. doi: 10.1016/j.cell.2011.03.034.
20. Chacon PJ, del Marco A, Arevalo A, Dominguez-Gimenez P, Garcia-Segura LM, Rodriguez-Tebar A. 2015. Cerebellin 4, a synaptic protein, enhances inhibitory activity and resistance of neurons to amyloid-beta toxicity. Neurobiology of Aging 36:1057-1071. doi: 10.1016/j.neurobiolaging.2014.11.006.
21. Chen Y, Zhang Y, Yin Y, Gao G, Li S, Jiang Y, Gu X, Luo J. 2005. SPD-a web-based secreted protein database. Nucleic Acids Research 33:D169-D173. doi: 10.1093/nar/gki093.
22. Colombrita C, Zennaro E, Fallini C, Weber M, Sommacal A, Buratti E, Silani V, Ratti A. 2009. TDP-43 is recruited to stress granules in conditions of oxidative insult. Journal of Neurochemistry 111:1051-1061. doi: 10.1111/j.1471-4159.2009.06383.x.
23. Dalal J, Roh JH, Maloney SE, Akuffo A, Shah S, Yuan H, Wamsley B, Jones WB, de Guzman Strong C, Gray PA, Holtzman DM, Heintz N, Dougherty JD. 2013. Translational profiling of hypocretin neurons identifies candidate molecules for sleep regulation. Genes & Development 27:565-578. doi: 10.1101/gad.207654.112.
24. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29:15-21. doi: 10.1093/bioinformatics/bts635.
25. Duong HA, Robles MS, Knutti D, Weitz CJ. 2011. A molecular mechanism for circadian clock negative feedback. Science 332:1436-1439. doi: 10.1126/science.1196766.
26. Ekstrand MI, Nectow AR, Knight ZA, Latcha KN, Pomeranz LE, Friedman JM. 2014. Molecular profiling of neurons based on connectivity. Cell 157:1230-1242. doi: 10.1016/j.cell.2014.03.059.
27. Francis JS, Dragunow M, During MJ. 2004. Over expression of ATF-3 protects rat hippocampal neurons from in vivo injection of kainic acid. Molecular Brain Research 124:199-203. doi: 10.1016/j.molbrainres.2003.10.027.
28. Gautron L, Elmquist Joel K, Williams Kevin W. 2015. Neural control of energy balance: translating circuits to therapies. Cell 161:133-145. doi: 10.1016/j.cell.2015.02.023.
29. Guarnieri DJ, Brayton CE, Richards SM, Maldonado-Aviles J, Trinko JR, Nelson J, Taylor JR, Gourley SL, DiLeone RJ. 2012. Gene profiling reveals a role for stress hormones in the molecular and behavioral response to food restriction. Biological Psychiatry 71:358-365. doi: 10.1016/j.biopsych.2011.06.028.
30. Hahn T, Breininger J, Baskin D, Schwartz M. 1998. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nature Neuroscience 1:271-272. doi: 10.1038/1082.
31. Hart SN, Therneau TM, Zhang Y, Poland GA, Kocher JP. 2013. Calculating sample size estimates for RNA sequencing data. Journal of Computational Biology 20:970-978. doi: 10.1089/cmb.2012.0283.
32. He L, Kim SO, Kwon O, Jeong SJ, Kim MS, Lee HG, Osada H, Jung M, Ahn JS, Kim BY. 2009. ATM blocks tunicamycin-induced endoplasmic reticulum stress. FEBS Letters 583:903-908. doi: 10.1016/j.febslet.2009.02.002.
33. Heiman M, Schaefer A, Gong S, Peterson JD, Day M, Ramsey KE, Suarez-Farinas M, Schwarz C, Stephan DA, Surmeier DJ, Greengard P, Heintz N. 2008. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135:738-748. doi: 10.1016/j.cell.2008.10.028.
34. Hempel CM, Sugino K, Nelson SB. 2007. A manual method for the purification of fluorescently labeled neurons from the mammalian brain. Nature Protocols 2:2924-2929. doi: 10.1038/nprot.2007.416.
35. Izumi S, Saito A, Kanemoto S, Kawasaki N, Asada R, Iwamoto H, Oki M, Miyagi H, Ochi M, Imaizumi K. 2012. The endoplasmic reticulum stress transducer BBF2H7 suppresses apoptosis by activating the ATF5-MCL1 pathway in growth plate cartilage. The Journal of Biological Chemistry 287:36190-36200. doi: 10.1074/jbc.M112.373746.
36. Jovanovic Z, Tung YC, Lam BY, O’Rahilly S, Yeo GS. 2010. Identification of the global transcriptomic response of the hypothalamic arcuate nucleus to fasting and leptin. Journal of Neuroendocrinology 22:915-925. doi: 10.1111/j.1365-2826.2010.02026.x.
37. Kalashnikova E, Lorca RA, Kaur I, Barisone GA, Li B, Ishimaru T, Trimmer JS, Mohapatra DP, Diaz E. 2010. SynDIG1: an activity-regulated, AMPA- receptor-interacting transmembrane protein that regulates excitatory synapse development. Neuron 65:80-93. doi: 10.1016/j.neuron.2009.12.021.
38. Kitahara H, Masumoto J, Parker AL, Maruta F, Kubo N, Shimizu A, Akita N, Miwa S, Kobayashi N, Nakayama J, Miyagawa S. 2011. COP35, a cholangiocarcinoma-binding oligopeptide, interacts with the clathrin heavy chain accompanied by GRP78. Molecular Cancer Research 9:688-701. doi: 10.1158/1541-7786.MCR-10-0470.
39. Kitamura T, Feng Y, Kitamura YI, Chua SC Jr, Xu AW, Barsh GS, Rossetti L, Accili D. 2006. Forkhead protein FoxO1 mediates Agrp-dependent effects of leptin on food intake. Nature Medicine 12:534-540. doi: 10.1038/nm1392.
40. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T, Igarashi K, Yamamoto M. 2004. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Molecular and Cellular Biology 24:7130-7139. doi: 10.1128/MCB.24.16.7130-7139.2004.
41. Krashes MJ, Koda S, Ye C, Rogan SC, Adams AC, Cusher DS, Maratos-Flier E, Roth BL, Lowell BB. 2011. Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. The Journal of Clinical Investigation 121:1424-1428. doi: 10.1172/JCI46229.
42. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods 9:357-359. doi: 10.1038/nmeth.1923.
43. Law CW, Chen Y, Shi W, Smyth GK. 2014. voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biology 15:R29. doi: 10.1186/gb-2014-15-2-r29.
44. Lee AH, Iwakoshi NN, Glimcher LH. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Molecular and Cellular Biology 23:7448-7459. doi: 10.1128/MCB.23.21.7448-7459.2003.
45. Lee S, Lee TA, Lee E, Kang S, Park A, Kim SW, Park HJ, Yoon JH, Ha SJ, Park T, Lee JS, Cheon JH, Park B. 2015. Identification of a subnuclear body involved in sequence-specific cytokine RNA processing. Nature Communications 6:5791. doi: 10.1038/ncomms6791.
46. LeSauter J, Lambert CM, Robotham MR, Model Z, Silver R, Weaver DR. 2012. Antibodies for assessing circadian clock proteins in the rodent suprachiasmatic nucleus. PLOS ONE 7:e35938. doi: 10.1371/journal.pone.0035938.
47. Li JY, Kuick R, Thompson RC, Misek DE, Lai YM, Liu YQ, Chai BX, Hanash SM, Gantz I. 2005. Arcuate nucleus transcriptome profiling identifies ankyrin repeat and suppressor of cytokine signalling box-containing protein 4 as a gene regulated by fasting in central nervous system feeding circuits. Journal of Neuroendocrinology 17:394-404. doi: 10.1111/j.1365-2826.2005.01317.x.
48. Liu T, Kong D, Shah BP, Ye C, Koda S, Saunders A, Ding JB, Yang Z, Sabatini BL, Lowell BB. 2012. Fasting activation of AgRP neurons requires NMDA receptors and involves spinogenesis and increased excitatory tone. Neuron 73:511-522. doi: 10.1016/j.neuron.2011.11.027.
49. Lovero KL, Blankenship SM, Shi Y, Nicoll RA. 2013. SynDIG1 promotes excitatory synaptogenesis independent of AMPA receptor trafficking and biophysical regulation. PLOS ONE 8:e66171. doi: 10.1371/journal.pone.0066171.
50. Luquet S, Perez FA, Hnasko TS, Palmiter RD. 2005. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310:683-685. doi: 10.1126/science.1115524.
51. Maddalo D, Neeb A, Jehle K, Schmitz K, Muhle-Goll C, Shatkina L, Walther TV, Bruchmann A, Gopal SM, Wenzel W, Ulrich AS, Cato AC. 2012. A peptidic unconjugated GRP78/BiP ligand modulates the unfolded protein response and induces prostate cancer cell death. PLOS ONE 7:e45690. doi: 10.1371/journal.pone.0045690.
52. Miller MN, Okaty BW, Kato S, Nelson SB. 2011. Activity-dependent changes in the firing properties of neocortical fast-spiking interneurons in the absence of large changes in gene expression. Developmental Neurobiology 71:62-70. doi: 10.1002/dneu.20811.
53. Okaty BW, Sugino K, Nelson SB. 2011. A quantitative comparison of cell-type-specific microarray gene expression profiling methods in the mouse brain. PLOS ONE 6:e16493. doi: 10.1371/journal.pone.0016493.
54. Ozcan L, Ergin AS, Lu A, Chung J, Sarkar S, Nie D, Myers MG Jr, Ozcan U. 2009. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metabolism 9:35-51. doi: 10.1016/j.cmet.2008.12.004.
55. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, Davenport AP, McGrath JC, Peters JA, Southan C, Spedding M, Yu W, Harmar AJ, Nc I. 2014. The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucleic Acids Research 42:D1098-D1106. doi: 10.1093/nar/gkt1143.
56. Qiu J, Fang Y, Ronnekleiv OK, Kelly MJ. 2010. Leptin excites proopiomelanocortin neurons via activation of TRPC channels. The Journal of Neuroscience 30:1560-1565. doi: 10.1523/JNEUROSCI.4816-09.2010.
57. Ren H, Orozco IJ, Su Y, Suyama S, Gutierrez-Juarez R, Horvath TL, Wardlaw SL, Plum L, Arancio O, Accili D. 2012. FoxO1 target Gpr17 activates AgRP neurons to regulate food intake. Cell 149:1314-1326. doi: 10.1016/j.cell.2012.04.032.
58. Rey G, Cesbron F, Rougemont J, Reinke H, Brunner M, Naef F. 2011. Genome-wide and phase-specific DNAbinding rhythms of BMAL1 control circadian output functions in mouse liver. PLOS Biology 9:e1000595. doi: 10.1371/journal.pbio.1000595.
59. Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. 2015. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Research 43:e47. doi: 10.1093/nar/gkv007.
60. Robinson MD, Oshlack A. 2010. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology 11:R25. doi: 10.1186/gb-2010-11-3-r25.
61. Roepke TA, Qiu J, Smith AW, Ronnekleiv OK, Kelly MJ. 2011. Fasting and 17beta-estradiol differentially modulate the M-current in neuropeptide Y neurons. The Journal of Neuroscience 31:11825-11835. doi: 10.1523/JNEUROSCI.1395-11.2011.
62. Sacco F, Perfetto L, Castagnoli L, Cesareni G. 2012. The human phosphatase interactome: an intricate family portrait. FEBS Letters 586:2732-2739. doi: 10.1016/j.febslet.2012.05.008.
63. Samali A, Fitzgerald U, Deegan S, Gupta S. 2010. Methods for monitoring endoplasmic reticulum stress and the unfolded protein response. International Journal of Cell Biology 2010:830307. doi: 10.1155/2010/830307.
64. Sandoval-Guzman T, Gongrich C, Moliner A, Guo T, Wu H, Broberger C, Ibanez CF. 2012. Neuroendocrine control of female reproductive function by the activin receptor ALK7. FASEB Journal 26:4966-4976. doi: 10.1096/fj.11-199059.
65. Sasaki K, Oomura Y, Suzuki K, Muto T, Hanai K, Tooyama I, Kimura H, Yanaihara N. 1991. Effects of fibroblast growth factors and platelet-derived growth factor on food intake in rats. Brain Research Bulletin 27:327-332. doi: 10.1016/0361-9230(91)90120-9.
66. Sato T, Sako Y, Sho M, Momohara M, Suico MA, Shuto T, Nishitoh H, Okiyoneda T, Kokame K, Kaneko M, Taura M, Miyata M, Chosa K, Koga T, Morino-Koga S, Wada I, Kai H. 2012. STT3B-dependent posttranslational N-glycosylation as a surveillance system for secretory protein. Molecular Cell 47:99-110. doi: 10.1016/j.molcel.2012.04.015.
67. Schioth HB. 2006. G protein-coupled receptors in regulation of body weight. CNS & Neurological Disorders Drug Targets 5:241-249. doi: 10.2174/187152706777452263.
68. Schwartz MW, Seeley RJ, Woods SC, Weigle DS, Campfield LA, Burn P, Baskin DG. 1997. Leptin increases hypothalamic pro-opiomelanocortin mRNA expression in the rostral arcuate nucleus. Diabetes 46:2119-2123. doi: 10.2337/diab.46.12.2119.
69. Seeburg DP, Feliu-Mojer M, Gaiottino J, Pak DT, Sheng M. 2008. Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 58:571-583. doi: 10.1016/j.neuron.2008.03.021.
70. Sugino K, Hempel CM, Miller MN, Hattox AM, Shapiro P, Wu C, Huang ZJ, Nelson SB. 2006. Molecular taxonomy of major neuronal classes in the adult mouse forebrain. Nature Neuroscience 9:99-107. doi: 10.1038/nn1618.
71. Sugino K, Hempel CM, Okaty BW, Arnson HA, Kato S, Dani VS, Nelson SB. 2014. Cell-type-specific repression by methyl-CpG-binding protein 2 is biased toward long genes. The Journal of Neuroscience 34:12877-12883. doi: 10.1523/JNEUROSCI.2674-14.2014.
72. Takahashi KA, Cone RD. 2005. Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons. Endocrinology 146:1043-1047. doi: 10.1210/en.2004-1397.
73. Tan K, Knight ZA, Friedman JM. 2014. Ablation of AgRP neurons impairs adaption to restricted feeding. Molecular Metabolism 3:694-704. doi: 10.1016/j.molmet.2014.07.002.
74. Tinkum KL, White LS, Marpegan L, Herzog E, Piwnica-Worms D, Piwnica-Worms H. 2013. Forkhead box O1 (FOXO1) protein, but not p53, contributes to robust induction of p21 expression in fasted mice. The Journal of Biological Chemistry 288:27999-28008. doi: 10.1074/jbc.M113.494328.
75. Uhlenbrock K, Gassenhuber H, Kostenis E. 2002. Sphingosine 1-phosphate is a ligand of the human gpr3, gpr6 and gpr12 family of constitutively active G protein-coupled receptors. Cellular Signalling 14:941-953. doi: 10.1016/S0898-6568(02)00041-4.
76. van den Pol AN, Yao Y, Fu LY, Foo K, Huang H, Coppari R, Lowell BB, Broberger C. 2009. Neuromedin B and gastrin-releasing peptide excite arcuate nucleus neuropeptide Y neurons in a novel transgenic mouse expressing strong Renilla green fluorescent protein in NPY neurons. The Journal of Neuroscience 29:4622-4639. doi: 10.1523/JNEUROSCI.3249-08.2009.
77. vander Klaauw Agatha A, Farooqi IS. 2015. The hunger genes: pathways to obesity. Cell 161:119-132. doi: 10.1016/j.cell.2015.03.008.
78. Williams KW, Liu T, Kong X, Fukuda M, Deng Y, Berglund ED, Deng Z, Gao Y, Liu T, Sohn JW, Jia L, Fujikawa T, Kohno D, Scott MM, Lee S, Lee CE, Sun K, Chang Y, Scherer PE, Elmquist JK. 2014. Xbp1s in Pomc neurons connects ER stress with energy balance and glucose homeostasis. Cell Metabolism 20:471-482. doi: 10.1016/j.cmet.2014.06.002.
79. Xu T, Bajjalieh SM. 2001. SV2 modulates the size of the readily releasable pool of secretory vesicles. Nature Cell Biology 3:691-698. doi: 10.1038/35087000.
80. Yamamoto K, Sato T, Matsui T, Sato M, Okada T, Yoshida H, Harada A, Mori K. 2007. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Developmental Cell 13:365-376. doi: 10.1016/j.devcel.2007.07.018.
81. Yan J, Wang H, Liu Y, Shao C. 2008. Analysis of gene regulatory networks in the mammalian circadian rhythm. PLOS Computational Biology 4:e1000193. doi: 10.1371/journal.pcbi.1000193.
82. Yang Y, Atasoy D, Su HH, Sternson SM. 2011. Hunger states switch a flip-flop memory circuit via a synaptic AMPKdependent positive feedback loop. Cell 146:992-1003. doi: 10.1016/j.cell.2011.07.039.
83. Zeisel A, Munoz-Manchado AB, Codeluppi S, Lonnerberg P, La Manno G, Jureus A, Marques S, Munguba H, He L, Betsholtz C, Rolny C, Castelo-Branco G, Hjerling-Leffler J, Linnarsson S. 2015. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347:1138-1142. doi: 10.1126/science.aaa1934.
84. Zhang Y, Chen K, Sloan SA, Bennett ML, Scholze AR, O’Keeffe S, Phatnani HP, Guarnieri P, Caneda C, Ruderisch N, Deng S, Liddelow SA, Zhang C, Daneman R, Maniatis T, Barres BA, Wu JQ. 2014a. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. The Journal of Neuroscience 34:11929-11947. doi: 10.1523/JNEUROSCI.1860-14.2014.
85. Zhang Y, Chen K, Sloan SA, Scholze AR, Caneda C, Ruderisch N, Deng S, Daneman R, Barres BA, Wu JQ. 2014b. An RNA-Seq transcriptome and splicing database of neurons, glia, and vascular cells of the cerebral cortex. NCBI Gene Expression Omnibus GSE52564. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE52564.