Skip to main content

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 brainsa 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), IIKCc 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 OLd 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]
N=F=D=Q (OL)
  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. cMore detailed information for restricted expression patterns are shown in parenthesis, when they are available
  7. 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)
  8. 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
  9. 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