Gene expression profiles and neural activities of Kenyon cell subtypes in the honeybee brain: identification of novel ‘middle-type’ Kenyon cells

Kaneko, Kumi; Suenami, Shota; Kubo, Takeo

doi:10.1186/s40851-016-0051-6

Table 1 Summary of genes expressed in a brain area-preferential manner in the honeybee brain

From: Gene expression profiles and neural activities of Kenyon cell subtypes in the honeybee brain: identification of novel ‘middle-type’ Kenyon cells

Name	Function of the product	Worker brain area where preferentially expressed	Expression in queen and drone brains^a	References
Calcium-signaling
IP ₃ R	Inositol 1, 4, 5 (IP₃)-trisphosphate receptor	lKC	W=Q=D	[24, 35, 36]
CaMKII	C²⁺/calmodulin-dependent protein kinase II	lKC	W=Q=D	[35, 36]
PKC	Protein kinase C	whole MB	N.A.	[35]
IP ₃ P	IP₃ phosphatase	lKC	N.A.	[28]
IP ₃ K	IP₃ kinase (Type A and B)	whole brain (/Type A, 96h > 48h > 0-1h), and OL (/Type B, 0-1h > 48h = 96h)^b	N.A.	[47]
Cac	Calcium channel	MB > central brain	N.A.	[36]
Ryr	Ryanodine receptor	lKC	N.A.	[32, 36]
Reticulocalbin	Calcium-binding protein in the endoplasmic reticulum	lKC	N.A.	[32]
PLCe	Phospholipase C epsilon	whole MB	N.A.	[29]
Ecdysteroid/JH-signaling
Mblk-1/E93	Ecdysone-regulated gene/ transcription factor	lKC	W=Q=D	[25]
E74	Ecdysone-regulated gene/ transcription factor	sKC	N.A.	[37]
HR38	Hormone receptor-like 38 (orphan receptor)	sKC, IIKC (F > N)	F>N=Q	[38]
E75	Ecdysone-regulated gene/ transcription factor	whole MB	N.A.	[30]
BR-C	Ecdysone-regulated gene/ transcription factor	lKC	N.A.	[30]
USP	Ultraspiracle (cofactor that binds EcR)	incKC (=lKC, constitutive) and icKC (=sKC, 1d > F), and part of AL	N.A.	[38, 64]
EcR	Ecdysone receptor	sKC	N=F=Q	[39]
JHDK	JH diol kinase (enzyme that inactivates JH)	sKC and lKCs (but not mKC), IIKC^c	N.A.	[33]
Other signaling
RJP-3	Major royal jelly protein-3	‘A defined population of KCs’	N.A.	[40]
PKA	Catalytic subunit of cAMP-dependent protein kinase	lKC and sKC (entire inside of MB calyces)	N.A.	[36, 41]
For (PKG)	cGMP-dependent protein kinase	sKC and OL lamina (F > N, preF > N)	N.A.	[45]
Mahya	Secretory protein with a follistatin-like domain	‘small cell-body KCs’ and AL (28d > 7d > NE)	W=Q=D	[46]
MESK2	Protein implicated in Ras/MAPK-signaling	transverse zone in ventral OL	W=Q=D	[31]
mKast	mKC-preferential arrestin-related protein	mKC (but not lKC or sKC) and OL^d	N.A.	[23]
sgg	Protein kinase, GSK 3-β	MB > central brain	N.A.	[36]
Neurotransmitters and their biosynthetic enzymes, receptors or transporters
Dop1	Dopamine D1 receptor	whole brain (NE > 15d)^e	N.A.	[43, 92]
Tyr1	Tyramine receptor	whole brain	N.A.	[93]
EAAT ^f	Glutamate transporter	icKC (=sKC) and OL (NE = 1h > 24h = F)	N.A.	[94]
Dop2	Dopamine D2 receptor	‘small-cell bodied KC’ (=sKC; constitutive), ‘(large-cell bodied KC (=1KC; F>NE=N) ‘outer small-cell bodied KC	W=D [i.e., older D > NE D, (large-cell bodied KC)]	[42, 43]
OA1	Octopamine (OA) receptor	whole brain	N.A.	[95]
Apisα2	Nicotinic acetylcholine receptor α2-subunit	ocKC (=II KC), incKC (=lKC), a part of OL, AL and DL	N.A.	[49]
Apisα7-1	Nicotinic acetylcholine receptor α7−1-subunit	a part of ocKC (=II KC), incKC (=lKC), a part of OL, AL and DL	N.A.	[49]
Apisα7-2 (GB17254)	Nicotinic acetylcholine receptor α7−2-subunit	ocKC (=IIKC), inner chiasma, a part of OL, AL and DL	N.A.	[49]
5-HT ₇	Serotonin (5-HT) receptor 7	whole brain	N.A.	[96]
Trp	Tachykinin-related peptide (neuromodulator)	sKC, lKC (but not mKC), IIKC, and some neurons in OL, AL and SOG	W=Q=D	[44]
Gad	Glutamic acid decarboxylase (GABA synthetic enzyme)	OL and AL (but not MB)	N.A.	[48]
Dop3	Dopamine D3 receptor	whole brain	N.A.	[97]
GB12077	Muscarinic acetylcholine receptor	MB > central brain	N.A.	[36]
Morphology of neurons
Futsch	Microtubule-associated protein	OL monopolar cell	W=Q=D	[31]
Tau	Microtubule-associated protein (22C10 antigen)	OL monopolar cell	W=Q=D	[31]
Syt14	Synaptotagmin 14	lKC	N.A.	[29]
Dlg5	Disc large 5	lKC	N.A.	[29]
ncRNAs
Ks-1	Function unknown	sKC, IIKC and some large somata neurons	W=Q=D (sKC, IIKC), D>W (between MB and OL)	[26]
Nb-1	Function unknown	subpopulation of octopamine-positive neurons (N > F)	N>F>Q	[27]
mir-276	miRNA	sKC, IIKC and OL	N=F=D>Q (sKC, IIKC),	[75]
mir-276	miRNA	sKC, IIKC and OL	N=F=D=Q (OL)	[75]

Note that, in most studies, in situ hybridization was used for gene expression analysis, while northern blotting [47], transcriptome analysis [36] and reverse transcription-polymerase chain reaction [43] were also used in some studies
Original Table from reference [20] was modified (a column for ‘Expression in queen and drone brains’ was newly added), updated (18 genes were newly added) and used
Abbreviations: MB mushroom body, OL optic lobe, AL antennal lobe, DL dorsal lobe, lKC class-I large-type KC, mKC, class-I middle-type KC, sKC class-I small-type KC, II KC class-II KC, ocKC outer compact KC, incKC inner non-compact KC, icKC inner compact KC. Terminologically, incKC = lKC, icKC = sKC, and ocKC = II KC, respectively
^aInformation for gene expression in queen and drones are shown, when they are available. W; worker, Q; queen, D; drone, NE D; newly emerged drone. N.A.; not analyzed. = means similar expression levels. < and > means higher expression in right than in left and vise versa, respectively
^bInformation for age/labor-dependent change in gene expression are shown in parenthesis in italic, when they are available. NE, newly emerged worker; N, nurse bee; F, forager; preF, precocious forager. 0-1h, 1d (24h), 48h, 96h, 7d, 15d and 28d indicate 0-1h-, 1d (24h)-, 48h-, 96h-, 7day, 15day-, and 28day-old worker, respectively. = means similar expression levels. < and > means higher expression in right than in left and vise versa, respectively
^cMore detailed information for restricted expression patterns are shown in parenthesis, when they are available
^dNote that, in all cases except mKast, Mblk-1, CaMKII, JHDK, Trp, Syt14 and Dlg5, mKCs were not discriminated from lKCs (incKCs) or sKCs (icKCs)
^eGenes for some major neurotransmitter receptors are also listed in this Table as references, though they show rather uniform expression in the whole brain; i.e., Dop1, Tyr1, OA1, Dop3 and 5-HT ₇
^fThe terms ‘Am’ are omitted from gene names, which were used in the original papers, because only Apis mellifera genes are listed in this Table

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