G protein-coupled odorant receptors underlie mechanosensitivity in mammalian olfactory sensory neurons

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 2, 2015, Pages 590-595

  Connelly, Timothy ^a   Yu, Yiqun ^a   Grosmaitre, Xavier ^a,b   Wang, Jue ^a   Santarelli, Lindsey C ^a   Savigner, Agnes ^a   Qiao, Xin ^a   Wang, Zhenshan ^c,d   Storm, Daniel R ^d   Ma, Minghong ^a   Carlson, John R ^e  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITÉ DE BOURGOGNE   (France)

^c HEBEI UNIVERSITY   (China)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e YALE UNIVERSITY   (United States)

Author keywords

G protein coupled receptors; Heterologous expression; Mechanical sensors; Mechanotransduction; Odorant receptors

Indexed keywords

G PROTEIN COUPLED ODORANT RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; OLFACTORY RECEPTOR; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HETEROLOGOUS EXPRESSION; HOST CELL; INTERNAL RIBOSOME ENTRY SITE; ION CURRENT; LOSS OF FUNCTION MUTATION; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; 129 MOUSE; ANIMAL; C57BL MOUSE; CALCIUM SIGNALING; DBA MOUSE; GENETICS; HEK293 CELL LINE; HUMAN; KNOCKOUT MOUSE; MECHANORECEPTOR; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SITE DIRECTED MUTAGENESIS; TRANSGENIC MOUSE;

MAMMALIA;

ANIMALS; CALCIUM SIGNALING; HEK293 CELLS; HUMANS; MECHANORECEPTORS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTAGENESIS, SITE-DIRECTED; OLFACTORY RECEPTOR NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, ODORANT; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84920973881     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1418515112     Document Type: Article

References (45)

1. Delmas P, Coste B (2013) Mechano-gated ion channels in sensory systems. Cell 155(2): 278-284.
2. Eijkelkamp N, Quick K, Wood JN (2013) Transient receptor potential channels and mechanosensation. Annu Rev Neurosci 36:519-546.
3. Storch U, Mederos y Schnitzler M, Gudermann T (2012) G protein-mediated stretch reception. Am J Physiol Heart Circ Physiol 302(6):H1241-H1249.
4. Grosmaitre X, Santarelli LC, Tan J, Luo M, Ma M (2007) Dual functions of mammalian olfactory sensory neurons as odor detectors and mechanical sensors. Nat Neurosci 10(3):348-354.
5. Kleinfeld D, Deschênes M, Wang F, Moore JD (2014) More than a rhythm of life: breathing as a binder of orofacial sensation. Nat Neurosci 17(5):647-651.
6. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 65(1):175-187.
7. Zhang X, Zhang X, Firestein S (2007) Comparative genomics of odorant and pheromone receptor genes in rodents. Genomics 89(4):441-450.
8. Su CY, Menuz K, Carlson JR (2009) Olfactory perception: receptors, cells, and circuits. Cell 139(1):45-59.
9. Mori K, Sakano H (2011) How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 34:467-499.
10. Wong ST, et al. (2000) Disruption of the type III adenylyl cyclase gene leads to peripheral and behavioral anosmia in transgenic mice. Neuron 27(3):487-497.
11. Chen X, Xia Z, Storm DR (2012) Stimulation of electro-olfactogram responses in the main olfactory epithelia by airflow depends on the type 3 adenylyl cyclase. J Neurosci 32(45):15769-15778.
12. Scheer A, Fanelli F, Costa T, De Benedetti PG, Cotecchia S (1996) Constitutively active mutants of the alpha 1B-adrenergic receptor: role of highly conserved polar amino acids in receptor activation. EMBO J 15(14):3566-3578.
13. Kobilka BK, Deupi X (2007) Conformational complexity of G-protein-coupled receptors. Trends Pharmacol Sci 28(8):397-406.
14. Sakmar TP, Franke RR, Khorana HG (1989) Glutamic acid-113 serves as the retinylidene Schiff base counterion in bovine rhodopsin. Proc Natl Acad Sci USA 86(21):8309-8313.
15. Imai T, Suzuki M, Sakano H (2006) Odorant receptor-derived cAMP signals direct axonal targeting. Science 314(5799):657-661.
16. Connelly T, Savigner A, Ma M (2013) Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors. J Neurophysiol 110(1):55-62.
17. Savigner A, et al. (2009) Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin. J Neurophysiol 101(6):2898-2906.
18. Oka Y, et al. (2006) Odorant receptor map in the mouse olfactory bulb: in vivo sensitivity and specificity of receptor-defined glomeruli. Neuron 52(5):857-869.
19. Vassalli A, Rothman A, Feinstein P, Zapotocky M, Mombaerts P (2002) Minigenes impart odorant receptor-specific axon guidance in the olfactory bulb. Neuron 35(4):681-696.
20. Grosmaitre X, et al. (2009) SR1, a mouse odorant receptor with an unusually broad response profile. J Neurosci 29(46):14545-14552.
21. Bozza T, Feinstein P, Zheng C, Mombaerts P (2002) Odorant receptor expression defines functional units in the mouse olfactory system. J Neurosci 22(8):3033-3043.
22. Tian H, Ma M (2004) Molecular organization of the olfactory septal organ. J Neurosci 24(38):8383-8390.
23. Fuss SH, Zhu Y, Mombaerts P (2013) Odorant receptor gene choice and axonalwiring in mice with deletion mutations in the odorant receptor gene SR1.Mol Cell Neurosci 56:212-224.
24. 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(6):833-846.
25. Omura M, Grosmaitre X, Ma M, Mombaerts P (2014) The β2-adrenergic receptor as a surrogate odorant receptor in mouse olfactory sensory neurons. Mol Cell Neurosci 58:1-10.
26. Mederos y Schnitzler M, et al. (2008) Gq-coupled receptors as mechanosensors mediating myogenic vasoconstriction. EMBO J 27(23):3092-3103.
27. Zou Y, et al. (2004) Mechanical stress activates angiotensin II type 1 receptor without the involvement of angiotensin II. Nat Cell Biol 6(6):499-506.
28. Potter SM, et al. (2001) Structure and emergence of specific olfactory glomeruli in the mouse. J Neurosci 21(24):9713-9723.
29. Saito H, Chi Q, Zhuang H, Matsunami H, Mainland JD (2009) Odor coding by a Mammalian receptor repertoire. Sci Signal 2(60):ra9.
30. Saito H, Kubota M, Roberts RW, Chi Q, Matsunami H (2004) RTP family members induce functional expression of mammalian odorant receptors. Cell 119(5):679-691.
31. Zhuang H, Matsunami H (2007) Synergism of accessory factors in functional expression of mammalian odorant receptors. J Biol Chem 282(20):15284-15293.
32. Reisert J (2010) Origin of basal activity in mammalian olfactory receptor neurons. J Gen Physiol 136(5):529-540.
33. Carey RM, Verhagen JV, Wesson DW, Pírez N, Wachowiak M (2009) Temporal structure of receptor neuron input to the olfactory bulb imaged in behaving rats. J Neurophysiol 101(2):1073-1088.
34. Buonviso N, Amat C, Litaudon P (2006) Respiratory modulation of olfactory neurons in the rodent brain. Chem Senses 31(2):145-154.
35. Schaefer AT, Margrie TW (2007) Spatiotemporal representations in the olfactory system. Trends Neurosci 30(3):92-100.
36. Wachowiak M (2011) All in a sniff: olfaction as a model for active sensing. Neuron 71(6):962-973.
37. Uchida N, Kepecs A, Mainen ZF (2006) Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat Rev Neurosci 7(6):485-491.
38. Smear M, Shusterman R, O'Connor R, Bozza T, Rinberg D (2011) Perception of sniff phase in mouse olfaction. Nature 479(7373):397-400.
39. Onoda N, Mori K (1980) Depth distribution of temporal firing patterns in olfactory bulb related to air-intake cycles. J Neurophysiol 44(1):29-39.
40. Phillips ME, Sachdev RN, Willhite DC, Shepherd GM (2012) Respiration drives network activity and modulates synaptic and circuit processing of lateral inhibition in the olfactory bulb. J Neurosci 32(1):85-98.
41. Ito J, et al. (2014) Whisker barrel cortex delta oscillations and gamma power in the awake mouse are linked to respiration. Nat Commun 5:3572.
42. Ma M, Chen WR, Shepherd GM (1999) Electrophysiological characterization of rat and mouse olfactory receptor neurons from an intact epithelial preparation. J Neurosci Methods 92(1-2):31-40.
43. Grosmaitre X, Vassalli A, Mombaerts P, Shepherd GM, Ma M (2006) Odorant responses of olfactory sensory neurons expressing the odorant receptor MOR23: A patch clamp analysis in gene-targeted mice. Proc Natl Acad Sci USA 103(6):1970-1975.
44. Zhuang H, Matsunami H (2008) Evaluating cell-surface expression and measuring activation of mammalian odorant receptors in heterologous cells. Nat Protoc 3(9):1402-1413.
45. Jiang J, Zhao K (2008) Quantifying mechanical stimuli in rat and human nose models during breathing. Chem Senses 33:S106.