Olfactory sensory neurons transiently express multiple olfactory receptors during development

Molecular Systems Biology

Volumn 11, Issue 12, 2015, Pages

  Tan, Longzhi ^a   Li, Qian ^b   Xie, X Sunney ^a  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

immature and mature olfactory sensory neurons; odorant receptor; olfactory system; single cell RNA Seq; trace amine associated receptor (TAAR)

Indexed keywords

BETA TUBULIN; COLLAPSIN RESPONSE MEDIATOR PROTEIN; COMPLEMENTARY DNA; CYCLIC NUCLEOTIDE GATED CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL ALPHA 2; DIHYDROPYRIMIDINASE LIKE 3 PROTEIN; DIHYDROPYRIMIDINASE LIKE 5 PROTEIN; GNAS PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN 8; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT 13; HISTONE DEACETYLASE 2; HOMEOBOX PROTEIN LHX2; HOMEODOMAIN PROTEIN; NEUROMODULIN; OLFACTORY MARKER PROTEIN; STATHMIN; STATHMIN 1; STATHMIN 2; STOMATIN LIKE 3; TRANSCRIPTION FACTOR EMX2; TRANSCRIPTOME; TUBULIN BETA 3; UNCLASSIFIED DRUG; OLFACTORY RECEPTOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CHROMOSOME 2; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE NUMBER; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; OLFACTORY EPITHELIUM; OLFACTORY RECEPTOR; OLFACTORY SENSORY NERVE CELL; OLFACTORY SYSTEM; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION; RNA DEGRADATION; RNA SEQUENCE; SENSORY NERVE CELL; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; TRANSCRIPTOMICS; UPREGULATION; ANIMAL; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; OLFACTORY RECEPTOR NEURON; PROCEDURES;

ANIMALS; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; OLFACTORY RECEPTOR NEURONS; RECEPTORS, ODORANT; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS;

EID: 84956600040     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.15252/msb.20156639     Document Type: Article

References (46)

1. Armelin-Correa LM, Gutiyama LM, Brandt DY, Malnic B, (2014) Nuclear compartmentalization of odorant receptor genes. Proc Natl Acad Sci USA 111: 2782-2787
2. Belluscio L, Gold GH, Nemes A, Axel R, (1998) Mice deficient in G(olf) are anosmic. Neuron 20: 69-81
3. Bonigk W, Bradley J, Muller F, Sesti F, Boekhoff I, Ronnett GV, Kaupp UB, Frings S, (1999) The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits. J Neurosci 19: 5332-5347
4. Buck L, Axel R, (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65: 175-187
5. Calof AL, Chikaraishi DM, (1989) Analysis of neurogenesis in a mammalian neuroepithelium: proliferation and differentiation of an olfactory neuron precursor in vitro. Neuron 3: 115-127
6. Cau E, Gradwohl G, Fode C, Guillemot F, (1997) Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124: 1611-1621
7. Chapman AR, He Z, Lu S, Yong J, Tan L, Tang F, Xie XS, (2015) Single cell transcriptome amplification with MALBAC. PLoS ONE 10: e0120889
8. Clowney EJ, LeGros MA, Mosley CP, Clowney FG, Markenskoff-Papadimitriou EC, Myllys M, Barnea G, Larabell CA, Lomvardas S, (2012) Nuclear Aggregation of Olfactory Receptor Genes Governs Their Monogenic Expression. Cell 151: 724-737
9. Dalton RP, Lyons DB, Lomvardas S, (2013) Co-opting the unfolded protein response to elicit olfactory receptor feedback. Cell 155: 321-332
10. Dulac C, Axel R, (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83: 195-206
11. Feinstein P, Bozza T, Rodriguez I, Vassalli A, Mombaerts P, (2004) Axon guidance of mouse olfactory sensory neurons by odorant receptors and the beta2 adrenergic receptor. Cell 117: 833-846
12. Fleischmann A, Abdus-Saboor I, Sayed A, Shykind B, (2013) Functional interrogation of an odorant receptor locus reveals multiple axes of transcriptional regulation. PLoS Biol 11: e1001568
13. Hirota J, Mombaerts P, (2004) The LIM-homeodomain protein Lhx2 is required for complete development of mouse olfactory sensory neurons. Proc Natl Acad Sci USA 101: 8751-8755
14. Ibarra-Soria X, Levitin MO, Saraiva LR, Logan DW, (2014) The olfactory transcriptomes of mice. PLoS Genet 10: e1004593
15. Kobayakawa K, Hayashi R, Morita K, Miyamichi K, Oka Y, Tsuboi A, Sakano H, (2002) Stomatin-related olfactory protein, SRO, specifically expressed in the murine olfactory sensory neurons. J Neurosci 22: 5931-5937
16. Li J, Ishii T, Feinstein P, Mombaerts P, (2004) Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428: 393-399
17. Li Q, Korzan WJ, Ferrero DM, Chang RB, Roy DS, Buchi M, Lemon JK, Kaur AW, Stowers L, Fendt M, Liberles SD, (2013) Synchronous evolution of an odor biosynthesis pathway and behavioral response. Curr Biol 23: 11-20
18. Liberles SD, Buck LB, (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442: 645-650
19. Lyons DB, Allen WE, Goh T, Tsai L, Barnea G, Lomvardas S, (2013) An epigenetic trap stabilizes singular olfactory receptor expression. Cell 154: 325-336
20. Ma L, Wu Y, Qiu Q, Scheerer H, Moran A, Yu CR, (2014) A developmental switch of axon targeting in the continuously regenerating mouse olfactory system. Science 344: 194-197
21. MacDonald JL, Gin CS, Roskams AJ, (2005) Stage-specific induction of DNA methyltransferases in olfactory receptor neuron development. Dev Biol 288: 461-473
22. Magklara A, Yen A, Colquitt BM, Clowney EJ, Allen W, Markenscoff-Papadimitriou E, Evans ZA, Kheradpour P, Mountoufaris G, Carey C, Barnea G, Kellis M, Lomvardas S, (2011) An Epigenetic Signature for Monoallelic Olfactory Receptor Expression. Cell 145: 555-570
23. Maier DL, Mani S, Donovan SL, Soppet D, Tessarollo L, McCasland JS, Meiri KF, (1999) Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice. Proc Natl Acad Sci USA 96: 9397-9402
24. Malnic B, Hirono J, Sato T, Buck LB, (1999) Combinatorial receptor codes for odors. Cell 96: 713-723
25. Marcucci F, Zou DJ, Firestein S, (2009) Sequential onset of presynaptic molecules during olfactory sensory neuron maturation. J Comp Neurol 516: 187-198
26. Markenscoff-Papadimitriou E, Allen WE, Colquitt BM, Goh T, Murphy KK, Monahan K, Mosley CP, Ahituv N, Lomvardas S, (2014) Enhancer interaction networks as a means for singular olfactory receptor expression. Cell 159: 543-557
27. McIntyre JC, Titlow WB, McClintock TS, (2010) Axon growth and guidance genes identify nascent, immature, and mature olfactory sensory neurons. J Neurosci Res 88: 3243-3256
28. Mombaerts P, (2004) Odorant receptor gene choice in olfactory sensory neurons: the one receptor-one neuron hypothesis revisited. Curr Opin Neurobiol 14: 31-36
29. Monti-Graziadei GA, Margolis FL, Harding JW, Graziadei PP, (1977) Immunocytochemistry of the olfactory marker protein. J Histochem Cytochem 25: 1311-1316
30. Mori K, Sakano H, (2011) How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 34: 467-499
31. Nedelec S, Foucher I, Brunet I, Bouillot C, Prochiantz A, Trembleau A, (2004) Emx2 homeodomain transcription factor interacts with eukaryotic translation initiation factor 4E (eIF4E) in the axons of olfactory sensory neurons. Proc Natl Acad Sci USA 101: 10815-10820
32. Picelli S, Faridani OR, Bjorklund AK, Winberg G, Sagasser S, Sandberg R, (2014) Full-length RNA-seq from single cells using Smart-seq2. Nat Protoc 9: 171-181
33. Roskams AJ, Cai X, Ronnett GV, (1998) Expression of neuron-specific beta-III tubulin during olfactory neurogenesis in the embryonic and adult rat. Neuroscience 83: 191-200
34. Sathyanesan A, Feijoo AA, Mehta ST, Nimarko AF, Lin W, (2013) Expression profile of G-protein betagamma subunit gene transcripts in the mouse olfactory sensory epithelia. Front Cell Neurosci 7: 84
35. Serizawa S, Miyamichi K, Nakatani H, Suzuki M, Saito M, Yoshihara Y, Sakano H, (2003) Negative feedback regulation ensures the one receptor-one olfactory neuron rule in mouse. Science 302: 2088-2094
36. Serizawa S, Miyamichi K, Sakano H, (2004) One neuron-one receptor rule in the mouse olfactory system. Trends Genet 20: 648-653
37. Shykind BM, (2005) Regulation of odorant receptors: one allele at a time. Hum Mol Genet 14: R33-R39
38. Shykind BM, Rohani SC, O'Donnell S, Nemes A, Mendelsohn M, Sun Y, Axel R, Barnea G, (2004) Gene switching and the stability of odorant receptor gene choice. Cell 117: 801-815
39. Strittmatter SM, Fankhauser C, Huang PL, Mashimo H, Fishman MC, (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80: 445-452
40. Tan LZ, Zong CH, Xie XS, (2013) Rare event of histone demethylation can initiate singular gene expression of olfactory receptors. Proc Natl Acad Sci USA 110: 21148-21152
41. Tian H, Ma M, (2008) Activity plays a role in eliminating olfactory sensory neurons expressing multiple odorant receptors in the mouse septal organ. Mol Cell Neurosci 38: 484-488
42. Tietjen I, Rihel JM, Cao Y, Koentges G, Zakhary L, Dulac C, (2003) Single-cell transcriptional analysis of neuronal progenitors. Neuron 38: 161-175
43. Tsai L, Barnea G, (2014) A critical period defined by axon-targeting mechanisms in the murine olfactory bulb. Science 344: 197-200
44. Verhaagen J, Oestreicher AB, Gispen WH, Margolis FL, (1989) The expression of the growth associated protein B50/GAP43 in the olfactory system of neonatal and adult rats. J Neurosci 9: 683-691
45. Wu AR, Neff NF, Kalisky T, Dalerba P, Treutlein B, Rothenberg ME, Mburu FM, Mantalas GL, Sim S, Clarke MF, Quake SR, (2014) Quantitative assessment of single-cell RNA-sequencing methods. Nat Methods 11: 41-46
46. Zou DJ, Chesler AT, Le Pichon CE, Kuznetsov A, Pei X, Hwang EL, Firestein S, (2007) Absence of adenylyl cyclase 3 perturbs peripheral olfactory projections in mice. J Neurosci 27: 6675-6683