Novel aspects of understanding molecular working mechanisms of salivary glands of worker honeybees (Apis mellifera) investigated by proteomics and phosphoproteomics

Mao, Feng; Yu, Fang; Han, Bin; Zhang, Lan; Lu, Xiaoshan; Li, Jianke

doi:10.1016/j.jprot.2013.05.021

Cited by 22 publications

(21 citation statements)

References 79 publications

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“…The centrality of these five protein families are also consistent with the high representation in the post-embryonic development of other honey bee organs, such as the pupal head (60), brain (61), hemolymph (62), hypopharyngeal gland (63,64), and salivary gland (65).…”

Section: Ligustica) Embryos (Normalized By Gapdh) (A) Is Significantsupporting

confidence: 69%

In-depth Proteomics Characterization of Embryogenesis of the Honey Bee Worker (Apis mellifera ligustica)

Mao

Han

et al. 2014

Molecular & Cellular Proteomics

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Identifying proteome changes of honey bee embryogenesis is of prime importance for unraveling the molecular mechanisms that they underlie. However, many proteomic changes during the embryonic period are not well characterized. We analyzed the proteomic alterations over the complete time course of honey bee worker embryogenesis at 24, 48, and 72 h of age, using mass spectrometry-based proteomics, label-free quantitation, and bioinformatics. Of the 1460 proteins identified the embryo of all three ages, the core proteome (proteins shared by the embryos of all three ages, accounting for 40%) was mainly involved in protein synthesis, metabolic energy, development, and molecular transporter, which indicates their centrality in driving embryogenesis. However, embryos at different developmental stages have their own specific proteome and pathway signatures to coordinate and modulate developmental events. The young embryos (<24 h) stronger expression of proteins related to nutrition storage and nucleic acid metabolism may correlate with the cell proliferation occurring at this stage. The middle aged embryos (24 -48 h) enhanced expression of proteins associated with cell cycle control, transporters, antioxidant activity, and the cytoskeleton suggest their roles to support rudimentary organogenesis. Among these proteins, the biological pathways of aminoacyl-tRNA biosynthesis, ␤-alanine metabolism, and protein export are intensively activated in the embryos of middle age. The old embryos (48 -72 h) elevated expression of proteins implicated in fatty acid metabolism and morphogenesis indicate their functionality for the formation and development of organs and dorsal closure, in which the biological pathways of fatty acid metabolism and RNA transport are highly activated. These findings add novel understanding to the molecular details of honey bee embryogenesis, in which the programmed activation of the proteome matches with the physiological transition observed during embryogenesis. The identified biological pathways and key node proteins allow for further functional analysis and genetic manipulation for both the honey bee embryos and other eusocial insects. Molecular & Cellular Proteomics 13:

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Section: Ligustica) Embryos (Normalized By Gapdh) (A) Is Significantsupporting

confidence: 69%

In-depth Proteomics Characterization of Embryogenesis of the Honey Bee Worker (Apis mellifera ligustica)

Mao

Han

et al. 2014

Molecular & Cellular Proteomics

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“…36 The phosphorylation sites were assigned using Scaffold PTM (version 1.1.3; Proteome Software, Portland, OR, USA) on the basis of the Ascore algorithm. 46 Only a site confidence greater than 95% was considered to be a mapped phosphorylation site in RJ proteins.…”

Section: Database Search and Site Localizationmentioning

confidence: 99%

In-Depth Phosphoproteomic Analysis of Royal Jelly Derived from Western and Eastern Honeybee Species

Han

Yu²,

Mao³

et al. 2014

J. Proteome Res.

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The proteins in royal jelly (RJ) play a pivotal role in the nutrition, immune defense, and cast determination of honeybee larvae and have a wide range of pharmacological and health-promoting functions for humans as well. Although the importance of post-translational modifications (PTMs) in protein function is known, investigation of protein phosphorylation of RJ proteins is still very limited. To this end, two complementary phosphopeptide enrichment materials (Ti(4+)-IMAC and TiO2) and high-sensitivity mass spectrometry were applied to establish a detailed phosphoproteome map and to qualitatively and quantitatively compare the phosphoproteomes of RJ produced by Apis mellifera ligustica (Aml) and Apis cerana cerana (Acc). In total, 16 phosphoproteins carrying 67 phosphorylation sites were identified in RJ derived from western bees, and nine proteins phosphorylated on 71 sites were found in RJ produced by eastern honeybees. Of which, eight phosphorylated proteins were common to both RJ samples, and the same motif ([S-x-E]) was extracted, suggesting that the function of major RJ proteins as nutrients and immune agents is evolutionary preserved in both of these honeybee species. All eight overlapping phosphoproteins showed significantly higher abundance in Acc-RJ than in Aml-RJ, and the phosphorylation of Jelleine-II (an antimicrobial peptide, TPFKLSLHL) at S(6) in Acc-RJ had stronger antimicrobial properties than that at T(1) in Aml-RJ even though the overall antimicrobial activity of Jelleine-II was found to decrease after phosphorylation. The differences in phosphosites, peptide abundance, and antimicrobial activity of the phosphorylated RJ proteins indicate that the two major honeybee species employ distinct phosphorylation strategies that align with their different biological characteristics shaped by evolution. The phosphorylation of RJ proteins are potentially driven by the activity of extracellular serine/threonine protein kinase FAM20C-like protein (FAM20C-like) through the [S-x-E] motif, which is supported by evidence that mRNA and protein expression of FAM20C-like protein kinase are both found in the highest level in the hypopharyngeal gland of nurse bees. Our data represent the first comprehensive RJ phosphorylation atlas, recording patterns of phosphorylated RJ protein abundance and antibacterial activity of some RJ proteins in two major managed honeybee species. These data constitute a firm basis for future research to better understand the biological roles of each RJ protein for honeybee biology and human health care.

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“…3). The proteins with differential expression were clustered into a heat map according to previous studies [36,37] (Fig. 4), which showed that most of the differences were between the MSG-A and the other two regions.…”

Section: Pairwise Comparison Of the Msg-a -M And -P Proteomesmentioning

confidence: 99%

Comparative proteomic analysis of the silkworm middle silk gland reveals the importance of ribosome biogenesis in silk protein production

Che

et al. 2015

Journal of Proteomics

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Novel aspects of understanding molecular working mechanisms of salivary glands of worker honeybees (Apis mellifera) investigated by proteomics and phosphoproteomics

Cited by 22 publications

References 79 publications

In-depth Proteomics Characterization of Embryogenesis of the Honey Bee Worker (Apis mellifera ligustica)

In-depth Proteomics Characterization of Embryogenesis of the Honey Bee Worker (Apis mellifera ligustica)

In-Depth Phosphoproteomic Analysis of Royal Jelly Derived from Western and Eastern Honeybee Species

Comparative proteomic analysis of the silkworm middle silk gland reveals the importance of ribosome biogenesis in silk protein production

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