Research Progress of Effect of Royal Jelly on Honeybee Learning and Memory
Queen and worker are two castes and have completely different jobs in a honeybee colony. The differences in phenotype and function of this two casts are related to their food royal jelly. Royal jelly from young workers serves as an important food source for lifetime of queens and less than three days old of worker larvae, which also plays a critical role in the healthy development of honeybee colony. However, the effects of royal jelly on the cognitive and behavioral ability of honeybees has not yet been elucidated. Therefore, this paper summarizes the research progress on learning and memory of honeybee itself owing to the royal jelly, in order to provide certain theoretical ideas for the future investigation on honeybee’s cognitive behavior.
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蜂王浆是5~14日幼龄工蜂咽下腺和上颚腺分泌的一种专门用于饲喂蜂王与3日龄内幼虫的黄色乳状物质[1-2]，对蜂王和工蜂个体发育和生殖具有重要影响。据报道，蜂王浆的主要功能包括：(1) 作为供给蜂王与蜜蜂幼虫的重要食物营养来源[3-5]；(2) 对蜜蜂蜂王与工蜂级型分化起关键作用，调控个体生长与发育[6-12]；(3) 可影响蜜蜂的认知行为能力[13-15]。蜂王与工蜂同是来自二倍体的受精卵，经级型分化最终发育成蜂王与工蜂，并在蜂群中承担截然不同的工作。工蜂因拥有良好的认知能力使之能顺利完成复杂的外界采集活动[16-21]，而蜂王认知能力如何目前尚不完全清楚。一般来说，工蜂在羽化出房21 d后才出巢采集，蜂王则通常在羽化出房后第5~13天即达到性成熟并完成婚飞[22-23]，能在如此短时间内完成婚飞并顺利返回蜂群从事产卵工作，说明蜂王具有很强的认知能力。有研究对西方蜜蜂蜂王的学习记忆能力进行了测试，发现5日龄蜂王的学习能力远高于同日龄工蜂，且与20日龄工蜂相当，15日龄蜂王在学习训练时的伸吻率甚至超过95%，可见，蜂王具有超强的学习记忆能力[15]。由于蜂王终生食用蜂王浆，而工蜂仅在幼虫期前3 d食用蜂王浆，后期食用蜂蜜和花粉，蜂王与工蜂的学习能力差异可能与蜂王浆密切相关。基于此，本文结合有关蜂王浆的最新研究，从蜂王浆影响蜜蜂认知行为的角度出发，综述了蜂王浆影响蜜蜂学习记忆能力的研究进展。
1. 蜂王浆的成分
1.1 蜂王浆成分及王浆主蛋白
蜂王浆成分复杂，主要含有60%~70%的水分、12%~15%的蛋白质、10%~16%的糖、3%~6%的脂肪以及0.8%~3.0%的维生素、盐和自由氨基酸[24-25]。进一步分析发现：蜂王浆中含有20种有机酸，其中10-羟基-2-癸烯酸(10-hydroxy-2-decenoic acid，10-HDA)和癸二酸(1,10-decanedioic acid)占有机酸总含量的80%~90%[26]。10-HDA是蜂王浆的独有物质，癸二酸具有抗真菌、抗氧化和抗炎活性，二者均可作为蜂王浆质量评价的标准。蜂王浆中含有多种蛋白质，其中近82%~90%属于王浆主蛋白(major royal jelly proteins，MRJPs)家族，且约48%的蛋白成分属于水溶性蛋白[27-29]。MRJPs家族已鉴定出9种成分，分别为MRJP-1~MJRP-9[29-31]。
1.2 东方蜜蜂与西方蜜蜂的蜂王浆成分比较
在蜂王浆产量方面，东方蜜蜂(Apis cerana)产浆量仅(3.21±0.43) g，而西方蜜蜂(A. mellifera)产浆量达(80.50±7.83) g[24]；在10-HDA含量方面，东方蜜蜂蜂王浆的10-HDA含量为(0.9±0.2)%，而西方蜜蜂蜂王浆的10-HDA含量则为(2.4±0.2)%(表1)；在王浆主蛋白含量方面，东、西方蜜蜂蜂王浆中的MRJPs均占90%，但组成有所差异，其中，东方蜜蜂蜂王浆的MRJPs包括37% MRJP-1、15% MRJP-2、30% MRJP-3、5% MRJP-4和3% MRJP-7，而西方蜜蜂蜂王浆的MRJPs包括6% MRJP-1、20% MRJP-2、40% MRJP-3、12% MRJP-4和12% MRJP-5[24]。
表 1 东方蜜蜂与西方蜜蜂的蜂王浆主要成分比较[32]Table 1. Comparison of the main components of royal jelly between Apis cerana and A. mellifera% 成分
components东方蜜蜂
A. cerana西方蜜蜂
A. mellifera水分 moisture 65.3±2.5 68.3±1.4 蛋白质 protein 16.4±2.5 12.7±0.8 碳水化合物 carbohydrate 9.4±0.6 11.9±0.7 葡萄糖 fructose 4.8±0.5 5.3±0.5 果糖 glucose 3.6±0.4 5.0±0.5 其他 others 1.3±0.7 1.6±0.4 脂肪 lipid 7.4±0.6 6.1±0.4 10-羟基-2-癸烯酸
10-hydroxy-2-decenoic acid0.9±0.2 2.4±0.2 灰分 ash 1.5±0.2 1.0±0.2 2. 王浆主蛋白(MRJPs)参与蜜蜂学习记忆
2.1 MRJPs家族成员在蜜蜂头部的表达
已被鉴定出的9种MRJPs中，虽对每种MRJPs的功能均有一定研究，也发现了各自的一些功能(表2)，然而该基因家族各成员在蜜蜂体内的功能(如它们在蜜蜂体内的基因表达及调控方法和路径等)仍不明确。在9种MRJPs基因中，mrjp-1、mrjp-2、mrjp-3和mrjp-7在蜜蜂蕈形体(也称蘑菇体)中均有表达[13, 42, 57]，其中，mrjp-1基因在蜜蜂咽下腺和蕈形体中均有表达，这也是目前唯一被认为参与了蜜蜂学习与记忆过程的MRJPs基因家族成员[13, 42]。
表 2 蜜蜂体内王浆主蛋白(MRJPs)的表达及其主要功能Table 2. Expression of major royal jelly proteins (MRJPs) within honeybees and its main function王浆主蛋白
MRJPs理化性质
physicochemical property体内表达
expression pattern
within the body预测糖基化位点
predicted
glycosylation sites表达产物糖蛋白含量
在王浆蛋白中的占比/%
proportion of glycoprotein
content in MRJPs已发现在蜜蜂体内的主要功能
identified main functions to honeybee参考文献
references分子质量/ku molecular weight 等电点isoelectric point 氨基酸长度
amino acid length东方蜜蜂
A. cerana西方蜜蜂
A. melliferaMRJP-1 46.86 5.03 413 体内广泛表达
widely expressed in vivo3 37 6 蜜蜂发育与成熟、行为调控、神经系统发育、级型分化、营养等
development and mutation, behavior regulation, nervous system development, caste differentiation, nutrition, and so on[7, 10, 13, 28-29, 33-36] MRJP-2 49.15 6.65 435 蕈形体、咽下腺、脑部
mushroom body,
hypopharyngeal gland, brain2 15 20 卵巢激活、级型决定、社会功能分化、营养等
ovarian activation, caste determination, society function differentiation, nutrition, and so on[8, 10, 13, 29, 35-41] MRJP-3 59.49 6.50 524 体内广泛表达
widely expressed in vivo1 30 40 神经调节、营养等
nervous regulation, nutrition, and so on[10, 29, 33-34, 36, 41-46] MRJP-4 50.67 5.74 444 头部、咽下腺、哺育蜂、蜂王幼虫期
head, hypopharyngeal gland, nurse worker, queen larvae8 5 12 营养等
nutrition, and so on[10, 29, 33, 35-36, 47-49] MRJP-5 68.13 5.95 578 咽下腺、5~26 日龄工蜂
hypopharyngeal gland,
5-26 days old workers4 0 12 促进细胞的生长繁殖、营养等
promote cell growth and reproduction, nutrition, and so on[10, 29-30, 35-37] MRJP-6 47.58 6.01 417 头部、咽下腺、采集蜂
head, hypopharyngeal gland, foragers5 未知
unknown未知
unknown级型分化、营养等
caste differentiation, nutrition, and so on[10, 35, 37, 49-51] MRJP-7 48.66 4.85 426 头部、蕈形体、咽下腺
head, mushroom body, hypopharyngeal gland3 3 0 卵巢激活、营养等
ovarian activation, nutrition, and so on[10, 13, 35-38, 40, 49, 51-52] MRJP-8 45.06 5.81 400 头部、毒囊、胸部、腹部
head, venom, thorax, abdomen6 未知
unknown未知
unknown参与蜂毒引起的过敏反应、营养等
involved in allergic reactions to venom, nutrition, and so on[10, 35, 53-55] MRJP-9 46.27 8.62 403 咽下腺、胸部、腹部、毒囊、触角、受精囊
hypopharyngeal gland, thorax,
abdomen, antenna, spermatheca3 未知
unknown未知
unknown参与蜂毒引起的过敏反应、作为表皮结构成分保护分泌细胞免于蜜蜂毒素引发的损伤、营养等
involved in allergic reactions to venom, acts as a structural component of the epidermis to protect secretory cells from damage caused by toxins, nutrition, and so on[10, 35, 37, 53-56] 2.2 mrjp-1基因对蜜蜂学习记忆的影响
KUCHARSKI 等[42]发现：mrjp-1基因在幼龄工蜂蕈形体中表达，且其表达量随着日龄的增长而上调，推测该基因与幼龄工蜂学习能力随着日龄增加而提高有一定关联。另外，将工蜂脱离蜂群进行隔离饲养后发现：由于处于密闭隔离状态，工蜂缺少必要的感官刺激而表现出学习能力显著降低的现象[58]。HOJO等[13]对正常蜂群饲养蜜蜂和隔离饲养蜜蜂的mrjp-1基因表达量进行比较发现：正常蜂群的mrjp-1基因表达量是隔离饲养蜜蜂的100倍。LI等[59]的研究也证明：蜜蜂嗅觉学习能力下降与mrjp-1基因表达量下降相关。因此，HOJO等[13]得出结论：mrjp-1基因与蜜蜂学习能力相关，降低mrjp-1基因表达量会影响蜜蜂的学习能力。蔚添添等[60]通过RNAi技术将mrjp-1基因沉默表达后，发现蜜蜂学习能力显著降低，这一结果与HOJO 等[13]的结论一致。
如上所述，除mrjp-1基因对蜜蜂学习记忆产生影响之外，其他MRJPs基因是否参与蜜蜂学习记忆的形成(图1)？这一问题有待进一步研究。此外，尚不清楚mrjp-1基因是否影响以及如何影响蜜蜂的长期记忆。
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图 1 蜂王浆对蜜蜂学习记忆的总体影响注：虚线表示尚未得到完全证实的影响。Figure 1. General effect of royal jelly on the learning and memory of honeybeeNote: The dotted lines are effects that have not well been demonstrated.3. 10-HDA对蜜蜂学习记忆的影响
3.1 10-HDA及其生理活性
10-HDA是自然界中唯一存在于蜂王浆中的物质，属不饱和脂肪酸，在蜂王浆中的质量分数为1.4%~2.0%，是蜂王浆中含量最高的脂肪酸成分[61]。1921年，10-HDA首次被发现并提取自工蜂上颚腺，其具有重要的生物学功能，如降血压、抗肿瘤、抗高胆固醇、抗炎等 [61-62]。进一步研究证实10-HDA具有高效的神经调节活性，如10-HDA处理可使大鼠海马神经元显著增加，并促进其神经细胞增殖，提高其增殖率和存活率[63-65]；也可作为新型自噬诱导剂促进帕金森病的神经保护[66-67]。另有研究显示：喂食10-HDA可以促进脊椎动物(如大鼠)大脑神经干细胞中神经元的生成并抑制星形胶质细胞生成[68]，海马区作为大鼠学习记忆的重要大脑功能区，10-HDA能增强其初级海马神经元活性并参与该神经元生长[68-69]。
3.2 10-HDA与蜜蜂学习记忆
目前尚无直接证据表明10-HDA参与了蜜蜂自身学习记忆的形成过程(图1)。NAGARAJA 等[70]以印度蜜蜂(A. cerana indica)和卡尼鄂拉蜂(A. mellifera carnica)雄蜂为研究对象，用不同气味测试其嗅觉学习记忆，发现2种蜜蜂的雄蜂均表现出对10-HDA气味刺激有更好的记忆，其伸吻率显著高于对报警信息素成分乙酸异戊酯的伸吻率。此外，对蜜蜂形态遗传标记的研究结果显示：mrjp3微卫星位点基因与蜜蜂产高含量10-HDA的蜂王浆密切相关[71]。如前所述，蜜蜂大脑蕈形体中也有mrjp-3基因表达[8, 42]，但尚不清楚该基因是否参与蜜蜂学习过程和记忆存储。若10-HDA直接或间接参与了工蜂和蜂王学习记忆的形成过程，那么在一定程度上就能解释蜂王与工蜂认知能力的差异与蜂王浆相关，这一猜测需大量试验验证。
4. 蜂王浆浓度对蜜蜂学习记忆的影响
4.1 对蜜蜂学习行为的影响
SHI等[14]分别用含有0%、10%和20%蜂王浆(royal jelly，RJ)的糖水饲喂出房工蜂，7 d后测定其学习记忆能力，并采用RT-qPCR测定喂食蜂王浆后工蜂2个记忆相关基因(GluRA和Nmdar1)的相对表达量，结果显示：饲喂蜂王浆后工蜂记忆能力显著提高，饲喂10%和20% RJ糖水的工蜂，其Nmdar1基因相对表达量显著高于饲喂0% RJ糖水的工蜂；饲喂20% RJ工蜂的GluRA基因相对表达量显著高于饲喂0% RJ的工蜂，且与对照组无显著差异。此外，用含有0%、10%和40% RJ的糖水饲喂新出房的工蜂和蜂王，5 d后测定其学习和记忆能力，结果显示：饲喂40% RJ的蜂王和工蜂，其学习和记忆能力均显著提高，两者对工蜂气味的辨识能力也显著提高，但对蜂王的辨识能力无明显变化。
4.2 对蜜蜂学习记忆相关基因的影响
谷氨酸是脊椎动物和无脊椎动物大脑中主要的兴奋性神经递质之一，在神经系统发育过程中对细胞分化和突触形成起关键作用[72]。谷氨酸受体基因GluRA (AmGluRA)在工蜂蛹和成年工蜂大脑中均有表达，影响蜜蜂的记忆能力，具体表现为在学习之前(1 h)谷氨酸受体拮抗剂可明显损害工蜂的长期记忆(24 h)，而在学习之后或者记忆检测之前使用拮抗剂则对工蜂记忆无明显影响[73]。同样地，N-甲基-D-天门冬氨酸(N-methyl-D-aspartic acid，NMDA)作为一种神经递质，也存在于影响蕈形体功能行使的蜜蜂大脑神经元中，NMDA受体基因Nmdar1的表达水平对蜜蜂学习记忆的形成过程具有关键作用[74-75]。SHI等[14]对工蜂体内GluRA和Nmdar1基因相对表达量的研究与前人研究结果相符合，证明可以通过蜂王浆影响GluRA和Nmdar1基因的表达水平，进而调控蜜蜂的学习记忆能力。以上研究均显示蜂王浆在一定程度上可以影响蜜蜂的学习和记忆能力，但具有蜂王浆浓度依赖性，其分子机理有待进一步解析。
5. 蜂王浆影响蜜蜂的表观遗传学和学习记忆
5.1 与蜜蜂学习记忆相关的表观遗传学研究
表观遗传学与蜜蜂学习记忆的相关性研究主要是针对DNA甲基化进行探索。蜜蜂体内存在3种甲基化转移酶，分别为Dnmt1、Dnmt2和Dnmt3，与哺乳动物甲基化转移酶非常相似且同源性高[76]，其中Dnmt3与蜜蜂学习记忆的相关性较大[77-79]。据BIERGANS 等[77-78]报道，DNA甲基化转移酶(主要是Dnmt3)参与调控蜜蜂长期记忆相关的嗅觉辨识力，对DNA甲基化转移酶进行抑制后，蜜蜂的学习记忆能力均受到不同程度损害。此外，LOCKETT等[79]和GONG等[80]研究发现：DNA甲基化参与了蜜蜂消退学习的过程，且这一过程表现出表观双向调节现象。
5.2 蜂王浆影响蜜蜂学习记忆的表观遗传学研究
蜂王浆影响蜜蜂DNA甲基化水平，进而调控蜜蜂学习记忆的研究鲜有报道，目前仅发现：经饲喂蜂王浆后，蜂王与工蜂的学习记忆能力均显著提高，但工蜂头部Dnmt3基因的表达与蜜蜂幼虫级型分化过程中蜂王与工蜂幼虫全个体DNA甲基化水平相反[81]；经学习训练后，工蜂Dnmt3基因表达又上调[81]，与LOCKETT等[79]报道的结果相一致。分析其原因可能是：(1) 尽管蜂王和工蜂基因型相同，但级型分化使二者头部DNA甲基化水平本身就有较大差异[82]，DNA甲基化转移酶多重调控功能共同作用，使Dnmt3基因表达呈现不同的变化；(2) 蜂王浆成分复杂，对蜜蜂有多方面的影响，如：其活性成分丁酸苯酯是一种已知的组蛋白去乙酰化酶抑制剂和生长调节剂，该成分可改善小鼠认知缺陷[83]和延长果蝇寿命[84]，在蜜蜂中也具有作为蜂王发育的营养来源、控制大脑基因表达的表观遗传网络调节剂等多重功能[81]，从而影响蜜蜂基因表达，继而对其行为产生影响。因此，认为蜜蜂学习记忆的行为表现可能是蜂王浆食物因素条件下，与表观遗传组成复杂共同网络调控的结果。然而，由于缺乏充足证据，当前仅能从定性角度认为DNA甲基化确实参与了蜜蜂的学习记忆，具体如何参与和调控还需进一步研究。
6. 小结与展望
蜂王浆因可增强人体免疫力和提高记忆力而被人们认识和关注，是不可多得的营养佳品，尽管多种成分已经被鉴定，其功能不断被发现，但因其成分复杂至今未被完全了解。就蜜蜂社会群体而言，蜂王浆作为蜂王和蜜蜂幼虫的食物来源，除了参与调控蜂王与工蜂级型分化外，对蜜蜂个体和群体的影响很少被研究，其在蜜蜂社会中的作用和功能尚未完全解析，就如本研究所述，蜂王浆对蜜蜂认知行为影响的研究也仅处于初步探索阶段。可见，人们对于蜂王浆在蜜蜂社会群体中的作用关注较少，还需要进行更多探索和挖掘。例如：正常蜂群中工蜂的生殖系统无法正常发育，但在无王群中，工蜂卵巢和王浆腺均得到发育并可以成功产卵[85]，那么王浆腺如何参与调控其生殖系统发育并是否影响其认知行为能力？蜂王浆高产蜜蜂的王浆腺更为发达，那么其学习记忆能力是否比普通蜂群中的蜜蜂更好？此外，东方蜜蜂和西方蜜蜂的蜂王浆中有一些成分含量差异较大，这种差异是否会影响蜜蜂的认知能力和生活习性？东方蜜蜂擅长采集零星蜜源，而西方蜜蜂擅长采集大宗蜜源，这些行为是否与二者获得学习记忆与消退记忆的双向调控机制相关？对上述问题的深入探讨和研究，必然会让我们对蜂王浆在蜜蜂社会群体中的作用更加了解，也有助于为东、西方蜜蜂生态适应性差异研究提供更多的理论启示。
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图 1 蜂王浆对蜜蜂学习记忆的总体影响
注：虚线表示尚未得到完全证实的影响。
Figure 1. General effect of royal jelly on the learning and memory of honeybee
Note: The dotted lines are effects that have not well been demonstrated.
表 1 东方蜜蜂与西方蜜蜂的蜂王浆主要成分比较[32]
Table 1 Comparison of the main components of royal jelly between Apis cerana and A. mellifera
% 成分
components东方蜜蜂
A. cerana西方蜜蜂
A. mellifera水分 moisture 65.3±2.5 68.3±1.4 蛋白质 protein 16.4±2.5 12.7±0.8 碳水化合物 carbohydrate 9.4±0.6 11.9±0.7 葡萄糖 fructose 4.8±0.5 5.3±0.5 果糖 glucose 3.6±0.4 5.0±0.5 其他 others 1.3±0.7 1.6±0.4 脂肪 lipid 7.4±0.6 6.1±0.4 10-羟基-2-癸烯酸
10-hydroxy-2-decenoic acid0.9±0.2 2.4±0.2 灰分 ash 1.5±0.2 1.0±0.2 
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表 2 蜜蜂体内王浆主蛋白(MRJPs)的表达及其主要功能
Table 2 Expression of major royal jelly proteins (MRJPs) within honeybees and its main function
王浆主蛋白
MRJPs理化性质
physicochemical property体内表达
expression pattern
within the body预测糖基化位点
predicted
glycosylation sites表达产物糖蛋白含量
在王浆蛋白中的占比/%
proportion of glycoprotein
content in MRJPs已发现在蜜蜂体内的主要功能
identified main functions to honeybee参考文献
references分子质量/ku molecular weight 等电点isoelectric point 氨基酸长度
amino acid length东方蜜蜂
A. cerana西方蜜蜂
A. melliferaMRJP-1 46.86 5.03 413 体内广泛表达
widely expressed in vivo3 37 6 蜜蜂发育与成熟、行为调控、神经系统发育、级型分化、营养等
development and mutation, behavior regulation, nervous system development, caste differentiation, nutrition, and so on[7, 10, 13, 28-29, 33-36] MRJP-2 49.15 6.65 435 蕈形体、咽下腺、脑部
mushroom body,
hypopharyngeal gland, brain2 15 20 卵巢激活、级型决定、社会功能分化、营养等
ovarian activation, caste determination, society function differentiation, nutrition, and so on[8, 10, 13, 29, 35-41] MRJP-3 59.49 6.50 524 体内广泛表达
widely expressed in vivo1 30 40 神经调节、营养等
nervous regulation, nutrition, and so on[10, 29, 33-34, 36, 41-46] MRJP-4 50.67 5.74 444 头部、咽下腺、哺育蜂、蜂王幼虫期
head, hypopharyngeal gland, nurse worker, queen larvae8 5 12 营养等
nutrition, and so on[10, 29, 33, 35-36, 47-49] MRJP-5 68.13 5.95 578 咽下腺、5~26 日龄工蜂
hypopharyngeal gland,
5-26 days old workers4 0 12 促进细胞的生长繁殖、营养等
promote cell growth and reproduction, nutrition, and so on[10, 29-30, 35-37] MRJP-6 47.58 6.01 417 头部、咽下腺、采集蜂
head, hypopharyngeal gland, foragers5 未知
unknown未知
unknown级型分化、营养等
caste differentiation, nutrition, and so on[10, 35, 37, 49-51] MRJP-7 48.66 4.85 426 头部、蕈形体、咽下腺
head, mushroom body, hypopharyngeal gland3 3 0 卵巢激活、营养等
ovarian activation, nutrition, and so on[10, 13, 35-38, 40, 49, 51-52] MRJP-8 45.06 5.81 400 头部、毒囊、胸部、腹部
head, venom, thorax, abdomen6 未知
unknown未知
unknown参与蜂毒引起的过敏反应、营养等
involved in allergic reactions to venom, nutrition, and so on[10, 35, 53-55] MRJP-9 46.27 8.62 403 咽下腺、胸部、腹部、毒囊、触角、受精囊
hypopharyngeal gland, thorax,
abdomen, antenna, spermatheca3 未知
unknown未知
unknown参与蜂毒引起的过敏反应、作为表皮结构成分保护分泌细胞免于蜜蜂毒素引发的损伤、营养等
involved in allergic reactions to venom, acts as a structural component of the epidermis to protect secretory cells from damage caused by toxins, nutrition, and so on[10, 35, 37, 53-56]
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[1] SNODGRASS R E. Anatomy and physiology of the honeybee[M]. Columbus: McGraw-Hill Book Company, inc, 1925.
[2] YANG W C, TIAN Y Y, HAN M F, et al. Longevity extension of worker honey bees (Apis mellifera) by royal jelly: optimal dose and active ingredient[J]. PeerJ, 2017, 5(3): e3118. DOI: 10.7717/peerj.3118.
[3] CRAILSHEIM K. The flow of jelly within a honeybee colony[J]. Journal of Comparative Physiology Biochemical, Systemic and Environmental Physiology, 1992, 162(8): 681. DOI: 10.1007/BF00301617.
[4] 曾志将. 蜜蜂生物学[M]. 北京: 中国农业出版社, 2007. [5] 秦凯鑫, 潘露霞, 王子龙. 蜂王浆主蛋白研究进展[J]. 环境昆虫学报, 2023, 45(4): 892. DOI: 10.3969/j.issn.1674-0858.2023.04.6. [6] EVANS J D, WHEELER D E. Differential gene expression between developing queens and workers in the honey bee, Apis mellifera[J]. Proceedings of the National Academy of Sciences of the USA, 1999, 96(10): 5575. DOI: 10.1073/pnas.96.10.5575.
[7] KAMAKURA M, SUENOBU N, FUKUSHIMA M. Fifty-seven-kDa protein in royal jelly enhances proliferation of primary cultured rat hepatocytes and increases albumin production in the absence of serum[J]. Biochemical and Biophysical Research Communications, 2001, 282(4): 865. DOI: 10.1006/bbrc.2001.4656.
[8] KUCHARSKI R, MALESZKA R. Evaluation of differential gene expression during behavioral development in the honeybee using microarrays and northern blots[J]. Genome Biology, 2002, 3(2): 0007. DOI: 10.1186/gb-2002-3-2-research0007.
[9] KAMAKURA M. Royalactin induces queen differentiation in honeybees[J]. Nature, 2011, 473(7348): 478. DOI: 10.1038/nature10093.
[10] BUTTSTEDT A, MORITZ R F, ERLER S. Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of the yellow gene family[J]. Biological Reviews of the Cambridge Philosophical Society, 2014, 89(2): 255. DOI: 10.1111/brv.12052.
[11] BUTTSTEDT A, IHLING C H, PIETZSCH M, et al. Royalactin is not a royal making of a queen[J]. Nature, 2016, 537(7621): E10. DOI: 10.1038/nature19349.
[12] RAMANATHAN A N K G, NAIR A J, SUGUNAN V S. A review on royal jelly proteins and peptides[J]. Journal of Functional Foods, 2018, 44(3): 255. DOI: 10.1016/j.jff.2018.03.008.
[13] HOJO M, KAGAMI T, SASAKI T, et al. Reduced expression of major royal jelly protein 1 gene in the mushroom bodies of worker honeybees with reduced learning ability[J]. Apidologie, 2010, 41(2): 194. DOI: 10.1051/apido/2009075.
[14] SHI J L, LIAO C H, WANG Z L, et al. Effect of royal jelly on longevity and memory-related traits of Apis mellifera workers[J]. Journal of Asia-Pacific Entomology, 2018, 21(4): 1430. DOI: 10.1016/j.aspen.2018.11.003.
[15] GONG Z W, TAN K, NIEH J C. First demonstration of olfactory learning and long-term memory in honey bee queens[J]. Journal of Experimental Biology, 2018, 221(14): jeb177303. DOI: 10.1242/jeb.177303.
[16] LINDAUER M. Time-compensated sun orientation in bees[J]. Cold Spring Harbor Symposia on Quantitative Biology, 1960, 25: 371. DOI: 10.1101/SQB.1960.025.01.039.
[17] LINDAUER M. Allgemeine sinnesphysiologie orientierung im raum[J]. Forfschr Zoology, 1963, 16: 58.
[18] SRINIVASAN M V, ZHANG S W, ALTWEIN M et al. Honeybee navigation: nature and calibration of the “odometer”[J]. Science, 2000, 287(5454): 851. DOI: 10.1126/science.287.5454.851.
[19] MENZEL R, GIURFA M. Cognitive architecture of a mini-brain: the honeybee[J]. Trends in Cognitive Sciences, 2001, 5(2): 62. DOI: 10.1016/S1364-6613(00)01601-6.
[20] I’ANSON PRICE R, DULEX N, VIAL N, et al. Honeybees forage more successfully without the “dance learning” in challenging environments[J]. Science Advances, 2019, 5(2): 0450. DOI: 10.1126/sciadv.aat0450.
[21] MATSUMOTO Y. Learning and memory in the cricket Gryllus bimaculatus[J]. Physiological Entomology, 2022, 47(3): 147. DOI: 10.3330/hikakuseiriseika.25.11.
[22] OERTEL E. Mating flights of queen bees[J]. Gleanings Bee Culture, 1940, 68: 292.
[23] WINSTON M L. The biology of the honey bee[M]. Cambridge: Harvard University Press, 1987.
[24] FANG Y, FENG M, LI J K. Royal jelly proteome comparison between Apis mellifera ligustica and Apis cerana cerana[J]. Journal of Proteome Research, 2010, 9(5): 2207. DOI: 10.1021/pr900979h.
[25] COLLAZO N, CARPENA M, NUEZ-ESTEVEZ B. Health promoting properties of bee royal jelly: food of the queens[J]. Nutrients, 2021, 13(543): 543. DOI: 10.13140/RG.2.2.32434.73929.
[26] SAFFET E, CAN G Y, ASL Z, et al. Organic acids and their derivatives: minor components of bee pollen, bee bread, royal jelly and bee venom[J]. European food Research and Technology, 2022, 248(12): 3037. DOI: 10.1007/s00217-022-04110-y.
[27] SCHACHER S, CSTELLUCCI V F, KANDEL E R. cAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis[J]. Science, 1988, 240(4859): 1667. DOI: 10.1126/science.2454509.
[28] HANES J, SIMUTH J. Identification and partial characterization of the major royal jelly protein of the honeybee (Apis mellifera L.)[J]. Journal of Apicultural Research, 1992, 31(1): 22. DOI: 10.1080/00218839.1992.11101256.
[29] SCHMITZOVA J, KLAUDINY J, ALBERTT S, et al. A family of major royal jelly proteins of the honeybee Apis mellifera L.[J]. Cellular and Molecular Life Sciences, 1998, 54(9): 1020. DOI: 10.1007/s000180050229.
[30] DRAPEAU M D, ALBERT S, KUCHARSKI R, et al. Evolution of the yellow/major royal jelly protein family and the emergence of social behavior in honey bees[J]. Genome Research, 2006, 16(11): 1385. DOI: 10.1101/gr.5012006.
[31] FUJITA T, KOZUKA-HATA H, AO-KONDO H, et al. Proteomic analysis of the royal jelly and characterization of the functions of its derivation glands in the honeybee[J]. Journal of Proteome Research, 2013, 12(1): 404. DOI: 10.1021/pr300700e.
[32] TAKENAKA T, TAKENAKA Y. Royal jelly from Apis cerana japonica and Apis mellifera[J]. Bioscience, Biotechnology, and Biochemistry, 1996, 60(3): 518. DOI: 10.1271/bbb.60.518.
[33] KLAUDINY J, HANES J, KULIFAJOVA J, et al. Molecular cloning of two cDNAs from the head of the nurse honeybee (Apis mellifera L.) coding for related proteins of royal jelly[J]. Journal of Apicultural Research, 1994, 33(2): 105. DOI: 10.1080/00218839.1994.11100857.
[34] OHASHI K, NATORI S, KUBO T. Change in the mode of gene expression of the hypopharyngeal gland cells with an age-dependent role change of the worker honeybee Apis mellifera L.[J]. Europe Journal of Biochemistry, 1997, 249(3): 797. DOI: 10.1111/j.1432-1033.1997.t01-1-00797.x.
[35] FURUSAWA T, RAKWAL R, NAM H W, et al. Comprehensive royal jelly (RJ) proteomics using one- and two-dimensional proteomics platforms reveals novel RJ proteins and potential phospho/glycoproteins[J]. Journal of Proteome Research, 2008, 7(8): 3194. DOI: 10.1021/pr800061j.
[36] DOBRITZSCH D, AUMER D, FUSZARD M, et al. The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers’ life[J]. Ecological Evolution, 2019, 9(15): 8771. DOI: 10.1002/ece3.5429.
[37] ALBERT S, KLAUDINY J. The MRJP/yellow protein family of Apis mellifera: identification of new members in the EST library[J]. Journal of Insect Physiology, 2004, 50(1): 51. DOI: 10.1016/j.jinsphys.2003.09.008.
[38] THOMPSON G J, KUCHARSKI R, MALESZKA R, et al. Towards a molecular definition of worker sterility: differential gene expression and reproductive plasticity in honey bees[J]. Insect Molecular Biology, 2006, 15(5): 637. DOI: 10.1111/j.1365-2583.2006.00678.x.
[39] NAKAOKA T, TAKEUCHI H, KUBO T. Laying workers in queenless honeybee (Apis mellifera L.) colonies have physiological states similar to that of nurse bees but opposite that of foragers[J]. Journal of Insect Physiology, 2008, 54(5): 806. DOI: 10.1016/j.jinsphys.2008.02.007.
[40] GARCIA L, CARLOS H, GARCIA S, et al. Proteomic analysis of honeybee brain upon ontogenetic and behavioral development[J]. Journal of Proteome Research, 2009, 8(3): 1464. DOI: 10.1021/pr800823r.
[41] PEIXOTO L G, CALÁBRIA L K, GARCIA L, et al. Identification of major royal jelly proteins in the brain of the honeybee Apis mellifera[J]. Journal of Insect Physiology, 2009, 55(8): 671. DOI: 10.1016/j.jinsphys.2009.05.005.
[42] KUCHARSKI R, MALESZKA R, HAYWARD D C, et al. A royal jelly protein is expressed in a subset of Kenyon cells in the mushroom bodies of the honey bee brain[J]. Naturwissenschaften, 1998, 85(7): 343. DOI: 10.1007/s001140050512.
[43] TAKENAKA T. Studies on proteins and carboxylic acid in royal jelly[D]. Machida: Tamagawa University, 1984.
[44] OKA H, EMORI Y, KOBAYASHI N, et al. Suppression of allergic reactions by royal jelly in association with the restoration of macrophage function and the improvement of Th1/Th2 cell responses[J]. International Immunopharmacology, 200l, 1(3): 521. DOI: 10.1016/S1567-5769(00)00007-2.
[45] OKAMOTO I, TANIGUCHI Y, KUNIKATA T, et al. Major royal jelly protein 3 modulates immune responses in vitro and in vivo[J]. Life Science, 2003, 73(6): 2029. DOI: 10.1016/S0024-3205(03)00562-9.
[46] KOHNO K, OKAMOTO I, SANO O, et al. Royal jelly inhibits the production of proinflammatory cytokines by activated macrophages[J]. Bioscience Biotechnology and Biochemistry, 2004, 68(1): 138. DOI: 10.1007/s00726-006-0417-8.
[47] ALBERT S, BHATTACHARYA D, KLAUDINY J, et al. The family of major royal jelly proteins and its evolution[J]. Journal of Molecular Evolution, 1999, 49: 290. DOI: 10.3785/j.issn.1008-9209.2017.06.281.
[48] 刘芳, 苏松坤. 中华蜜蜂王浆蛋白MRJP5的结构分析与功能预测[J]. 蜜蜂杂志, 2011, 31(5): 1. DOI: 10.3969/j.issn.1003-9139.2011.05.001. [49] CHEN X, HU Y, ZHENG H Q, et al. Transcriptome comparison between honey bee queen-and worker-destined larvae[J]. Insects Biochemistry & Molecular Biology, 2012, 42(9): 665. DOI: 10.1016/j.ibmb.2012.05.004.
[50] MALECOVA B, RAMSER J, O’BRIEN J K, et al. Honeybee (Apis mellifera L.) MRJP gene family: computational analysis of putative promoters and genomic structure of mrjp1, the gene coding for the most abundant protein of larval food[J]. Gene, 2003, 303(1): 165. DOI: 10.1016/S0378-1119(02)01174-5.
[51] LIU F, LI W F, LI Z G, et al. High-abundance mRNAs in Apis mellifera: comparison between nurses and foragers[J]. Journal of Insect Physiology, 2011, 57(2): 274. DOI: 10.1016/j.jinsphys.2010.11.015.
[52] ALBERT S, KLAUDINY J. MRJP9, an ancient protein of the honeybee MRJP family with non-nutritional function[J]. Journal of Apicultural Research, 2007, 46(2): 99. DOI: 10.3896/IBRA.1.46.2.06.
[53] PEIREN N, VANROBAEYS F, GRAAF D C, et al. The protein composition of honeybee venom reconsidered by a proteomic approach[J]. Biochemical et Biophysica Acta-Proteins and Proteomics, 2005, 1752(1): 1. DOI: 10.1016/j.bbapap.2005.07.017.
[54] SANTOS K S, SANTOS L D, MENDES M A, et al. Profiling the proteome complement of the secretion from hypopharyngeal gland of Africanized nurse-honeybees (Apis mellifera L.)[J]. Insect Biochemistry and Molecular Biology, 2005, 35(1): 85. DOI: 10.1016/j.ibmb.2004.10.003.
[55] PEIREN N, DE GRAAF D C, VANROBAEYS F, et al. Proteomic analysis of the honey bee worker venom gland focusing on the mechanisms of protection against tissue damage[J]. Toxicon, 2008, 52(1): 72. DOI: 10.1016/j.to-xicon.2008.05.003.
[56] BLANK S, BANTLEON F I, MCINTYRE M, et al. The major royal jelly proteins 8 and 9 (Apim 11) are glycosylated components of Apis mellifera venom with allergenic potential beyond carbohydrate-based reactivity[J]. Clinical and Experimental Allergy, 2012, 42(6): 976. DOI: 10.1111/j.1365-2222.2012.03966.x.
[57] KUCHARSKI R, MALESZKA J, FORET S, et al. Nutritional control of reproductive status in honeybees via DNA methylation[J]. Science, 2008, 319(5871): 1827. DOI: 10.1126/science.1153069.
[58] ICHIKAWA N, SASAKI M. Importance of social stimuli for the development of learning capability in honeybees[J]. Applied Entomological Zoology, 2003, 38(2): 203. DOI: 10.1303/aez.2003.203.
[59] LI Z G, YU T T, CHEN Y P, et al. Brain transcriptome of honeybees (Apis mellifera) exhibiting impaired olfactory learning induced by sub lethal dose of imidacloprid[J]. Pesticide Biochemistry and Physiology, 2019, 156: 36. DOI: 10.1016/j.pestbp.2019.02.001.
[60] 蔚添添, 邱园妹, 候梦赏, 等. RNAi 沉默王浆主蛋白 1 (mrjp1)基因对意大利蜜蜂工蜂学习和记忆的影响[J]. 昆虫学报, 2021, 64(10): 1145. DOI: 10.16380/j.kcxb.2021.10.003. [61] CORNARA L, BIAGI M, XIAO J B, et al. Therapeutic properties of bioactive compounds from different honeybee products[J]. Frontiers in Pharmacology, 2017, 8(412): 1. DOI: 10.3389/fphar.2017.00412.
[62] BURLANDO B, CORNARA L. Honey in dermatology and skin care: a review[J]. Journal of Cosmetic Dermatology, 2013, 12(4): 306. DOI: 10.1111/jocd.12058.
[63] 田静, 钟方旭. 10-HDA对原代培养大鼠海马神经元增殖的研究[J]. 山西大学学报(自然科学版), 2010, 33(2): 282. DOI: 10.13451/j.cnki.shanxi.univ(nat.sci.).2010.02.013. [64] 高荣敬, 钟方旭, 彭友瑞, 等. 10-HDA对体外培养大鼠小脑细胞增殖的影响[J]. 中国食物与营养, 2011, 17(9): 76. DOI: 10.3969/j.issn.1006-9577.2011.09.020. [65] PYRZANOWSKA J, PIECHAL A, BLECHARZ-KLIN K, et al. Long-term administration of greek royal jelly improves spatial memory and influences the concentration of brain neurotransmitters in naturally aged Wistar male rats[J]. Journal of Ethonpharmacology, 2014, 155(1): 343. DOI: 10.1016/j.jep.2014.05.032.
[66] MARTINEZ-CHACON G, PAREDES-BARQUERO M, YAKHINE-DIOP S, et al. Neuroprotective properties of queen bee acid by autophagy induction[J]. Cell Biology and Toxicology, 2021, 39(3): 751. DOI: 10.1007/s10565-021-09625-w.
[67] 缪卓宁, 胡福良. 蜂王浆特有成分10-HDA的研究进展[J]. 蜜蜂杂志, 2020, 40(2): 4. [68] HATTORI N, NOMOTO H, FUKUMITSU H, et al. Royal jelly and its unique fatty acid, 10-hydroxy-trans-2-decenoic acid, promote neurogenesis by neural stem/progenitor cells in vitro[J]. Biomedical Research, 2007, 28(5): 28. DOI: 10.1007/s11033-018-4451-x.
[69] SILVA T G D S E, PAULO M E F D V D, SILVA J R M D, et al. Oral treatment with royal jelly improves memory and presents neuroprotective effects on icv-STZ rat model of sporadic Alzheimer’s disease[J]. Heliyon, 2020, 6(2): e03281. DOI: 10.1016/j.heliyon.2020.e032.
[70] NAGARAJA N, BRUCKNER D. Olfactory learning and memory recall in drones of hive honeybee species[J]. Journal of Entomological Research, 2013, 37(1): 2981.
[71] BRANDORF A Z, IVOILOVA M M. Morpho-genetic markers of honeybees producing royal jelly with a high content of 10-HDA[J]. Agricultural Science Euro-North-East, 2019, 20(3): 283. DOI: 10.30766/2072-9081.2019.20.3.283-289.
[72] DANBOLT N C. Glutamate uptake[J]. Progress in Neurobiology, 2001, 65(1): 1. DOI: 10.1016/S0301-0082(00)00067-8.
[73] KUCHARSKI R, MITRI C, GRAU Y, et al. Characterization of a metabotropic glutamate receptor in the honeybee (Apis mellifera): implications for memory formation[J]. Invertebrate Neuroscience, 2007, 7(2): 99. DOI: 10.1007/s10158-007-0045-3.
[74] ZANNAT M T, LOCATELLI F, RYBAK J, et al. Identification and localisation of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain[J]. Neuroscience Letters, 2006, 398(3): 274. DOI: 10.1016/j.neulet.2006.01.007.
[75] ZACHEPILO T G, II’INYKH Y F, LOPATINA N G, et al. Comparative analysis of the locations of the NR1 and NR2 NMDA receptor subunits in honeybee (Apis mellifera) and fruit fly (Drosophila melanogaster, Canton-S wild-type) cerebral ganglia[J]. Neuroscience Behavior Physiology, 2008, 38(4): 369. DOI: 10.1007/s11055-008-0052-9.
[76] WANG Y, JORDA M, JONES P L, et al. Functional CpG methylation system in a social insect[J]. Science, 2006, 314(5799): 645. DOI: 10.1126/science.1135213.
[77] BIERGANS S D, GALIZIA C G, REINHARD J, et al. Dnmts and Tet target memory associated genes after appetitive olfactory training in honey bees[J]. Scientific Reports, 2015, 5(1): 16223. DOI: 10.1038/srep21656.
[78] BIERGANS S D, JONES J C, TREIBER N, et al. DNA methylation mediates the discriminatory power of associative long-term memory in honeybees[J]. PLoS One, 2012, 7(6): e39349. DOI: 10.1371/journal.pone.0039349.
[79] LOCKETT G A, HELLIWEL P, MALESZKA R. Involvement of DNA methylation in memory processing in the honey bee[J]. Neuroreport, 2010, 21(12): 812. DOI: 10.1097/WNR.0b013e32833ce5be.
[80] GONG Z W, WANG C, TAN K, et al. Inhibiting DNA methylation alters olfactory extinction but not acquisition learning in Apis cerana and Apis mellifera[J]. Journal Insect Physiology, 2016, 90: 43. DOI: 10.1016/j.jinsphys.2016.05.007.
[81] 王文祥. 10-HDA对意蜂幼虫发育影响及中蜂Royalactin mRNA水平和原核表达分析[D]. 南昌: 江西农业大学, 2013. [82] LYKO F, FORET S, KUCHARSKI R, et al. The honey bee epigenomes: differential methylation of brain DNA in queens and workers[J]. PLoS Biology, 2010, 8(11): e1000506. DOI: 10.1371/journal.pbio.1000506.
[83] RICOBARAZA A, CUADRADO-TEJEDOR M, PE’REZ-MEDIAVILLA A, et al. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer’s disease mouse model[J]. Neuropsychopharmacology, 2009, 34(7): 1721. DOI: 10.1038/npp.2008.229.
[84] KANG H L, BENZER S, MIN K T. Life extension in drosophila by feeding a drug[J]. Proceedings of the National Academy of Sciences, 2002, 99(2): 838. DOI: 10.1073/pnas.022631999.
[85] 庄迪, 杨爽, 谭垦. 无王群工蜂卵巢和王浆腺发育的研究[J]. 蜜蜂杂志, 2011, 31(6): 5. DOI: 10.3969/j.issn.1003-9139.2011.06.003.
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