Evolutionary origins of taste buds: phylogenetic analysis of purinergic neurotransmission in epithelial chemosensors

Open Biology - Tập 3 Số 3 - Trang 130015 - 2013
Masato Kirino1, Jason Parnes2, Anne Hansen2, Sadao Kiyohara1, Thomas E. Finger2
1Department of Chemistry and Bioscience, Graduate School of Science and Engineering, Kagoshima University, Kagoshima, Japan
2Department of Cell and Developmental Biology, Rocky Mountain Taste and Smell Center, University of Colorado School of Medicine, MS 8108, Room L18-11118, RC-1, 12801 E. 17th Avenue, Aurora, CO 80045, USA

Tóm tắt

Taste buds are gustatory endorgans which use an uncommon purinergic signalling system to transmit information to afferent gustatory nerve fibres. In mammals, ATP is a crucial neurotransmitter released by the taste cells to activate the afferent nerve fibres. Taste buds in mammals display a characteristic, highly specific ecto-ATPase (NTPDase2) activity, suggesting a role in inactivation of the neurotransmitter. The purpose of this study was to test whether the presence of markers of purinergic signalling characterize taste buds in anamniote vertebrates and to test whether similar purinergic systems are employed by other exteroceptive chemosensory systems. The species examined include several teleosts, elasmobranchs, lampreys and hagfish, the last of which lacks vertebrate-type taste buds. For comparison, Schreiner organs of hagfish and solitary chemosensory cells (SCCs) of teleosts, both of which are epidermal chemosensory end organs, were also examined because they might be evolutionarily related to taste buds. Ecto-ATPase activity was evident in elongate cells in all fish taste buds, including teleosts, elasmobranchs and lampreys. Neither SCCs nor Schreiner organs show specific ecto-ATPase activity, suggesting that purinergic signalling is not crucial in those systems as it is for taste buds. These findings suggest that the taste system did not originate from SCCs but arose independently in early vertebrates.

Từ khóa


Tài liệu tham khảo

Finger TE, 2009, Evolutionary neuroscience, 1, 460

10.1016/j.ydbio.2007.07.042

Whitear M, 1992, Chemoreception in fishes, 2, 103, 10.1007/978-94-011-2332-7_6

10.1002/(SICI)1096-9861(19980309)392:2<135::AID-CNE1>3.0.CO;2-3

10.1002/(SICI)1096-9861(19960909)373:1<129::AID-CNE11>3.0.CO;2-F

10.1002/cne.903310310

10.1007/978-94-011-5834-3_32

10.1159/000113337

10.1126/science.1118435

10.1152/jn.00414.2010

10.1038/sj.emboj.7601526

10.1073/pnas.0611280104

10.1002/cne.20954

10.1007/s11302-012-9309-4

Reutter K, 1993, Mechanisms of taste transduction, 29

Finger TE, 2000, Neurobiology of taste and smell, 2, 287

10.1093/chemse/bjh110

10.1083/jcb.201003144

Murray RG, 1973, The ultrastructure of sensory organs, 1

10.1038/nature05401

10.1002/1096-9861(20000911)425:1<139::AID-CNE12>3.0.CO;2-#

10.1002/cne.10963

10.1113/jphysiol.2008.151233

10.1093/chemse/bjm083

10.2331/suisan.53.1943

10.1007/978-3-642-67008-4

10.1007/978-94-007-1060-3_3

10.1002/cne.903530304

10.1002/(SICI)1096-9861(19980309)392:2<199::AID-CNE4>3.0.CO;2-Y

10.1016/j.neuroscience.2005.11.058

10.1177/40.12.1453008

10.1177/002215540205000412

10.1111/j.1748-1716.2009.01957.x

10.1177/31.2.6339606

10.1016/j.acthis.2011.03.006

10.1093/chemse/10.4.549

10.1002/cne.21844

10.1002/cne.900860204

10.1007/BF00604982

10.1016/0014-4827(67)90388-6

10.1177/17.11.724

10.1679/aohc.47.31

10.1097/00001756-199904060-00037

10.1152/physrev.00015.2002

10.1016/j.pneurobio.2005.03.001

10.1186/1471-2202-8-64

10.1007/s00418-008-0455-2

10.1073/pnas.1531172100

10.1111/j.1463-6409.1979.tb00619.x

10.1073/pnas.0913844107

10.1006/mpev.2001.1045

10.1242/dev.074716

10.1038/ncomms1355

10.1073/pnas.042617699

10.1186/1471-2202-8-49

10.1073/pnas.0911934107

10.1073/pnas.0606189103

10.1152/ajpgi.00073.2006

10.3410/B3-20

10.1002/cne.22589

10.1002/ddr.1097

10.1152/physrev.00043.2006

10.1007/s00424-009-0703-x

10.1113/jphysiol.2011.207829

10.1111/j.1469-7793.1997.503bb.x

10.1113/jphysiol.2009.180083

10.1002/cne.902350105

10.1523/JNEUROSCI.1570-10.2010

10.1523/JNEUROSCI.2351-09.2009

10.1038/nn796

10.1523/JNEUROSCI.5230-07.2008

10.1002/jez.b.21188

10.1073/pnas.92.6.1916

10.1006/dbio.1995.1143

10.1046/j.1463-6395.2002.00120.x

10.1046/j.1463-6395.1999.80220005.x