Mass Spectral Analysis of Neuropeptide Expression and Distribution in the Nervous System of the Lobster <i>Homarus americanus</i>

Chen, Ruibing; Jiang, Xiaoyue; Conaway, Maria C. Prieto; Mohtashemi, Iman; Hui, Limei; Viner, Rosa; Li, Lingjun

doi:10.1021/pr900736t

Cited by 62 publications

(77 citation statements)

References 54 publications

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“…Our group and others have greatly expanded the peptidomes of many model organisms (3, 18 -33). For example, we have discovered more than 200 neuropeptides with several neuropeptide families consisting of as many as 20 -40 members in a simple crustacean model system (5,6,(25)(26)(27)(28)(29)(30)(31)34). However, a majority of these neuropeptides are small peptides with 5-15 amino acid residues long, leaving a gap of identifying larger signaling peptides from organisms without sequenced genome.…”

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confidence: 99%

High-definition De Novo Sequencing of Crustacean Hyperglycemic Hormone (CHH)-family Neuropeptides

Jia

Hui

Cao

et al. 2012

Molecular & Cellular Proteomics

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A complete understanding of the biological functions of large signaling peptides (>4 kDa) requires comprehensive characterization of their amino acid sequences and posttranslational modifications, which presents significant analytical challenges. In the past decade, there has been great success with mass spectrometry-based de novo sequencing of small neuropeptides. However, these approaches are less applicable to larger neuropeptides because of the inefficient fragmentation of peptides larger than 4 kDa and their lower endogenous abundance. The conventional proteomics approach focuses on largescale determination of protein identities via database searching, lacking the ability for in-depth elucidation of individual amino acid residues. Here, we present a multifaceted MS approach for identification and characterization of large crustacean hyperglycemic hormone ( Neuropeptides and hormones comprise a diverse class of signaling molecules involved in numerous essential physiological processes, including analgesia, reward, food intake, learning and memory (1). Disorders of the neurosecretory and neuroendocrine systems influence many pathological processes. For example, obesity results from failure of energy homeostasis in association with endocrine alterations (2, 3). Previous work from our lab used crustaceans as model organisms found that multiple neuropeptides were implicated in control of food intake, including RFamides, tachykinin related peptides, RYamides, and pyrokinins (4 -6).Crustacean hyperglycemic hormone (CHH) 1 family neuropeptides play a central role in energy homeostasis of crustaceans (7-17). Hyperglycemic response of the CHHs was first reported after injection of crude eyestalk extract in crustaceans. Based on their preprohormone organization, the CHH family can be grouped into two sub-families: subfamily-I containing CHH, and subfamily-II containing molt-inhibiting hormone (MIH) and mandibular organ-inhibiting hormone (MOIH). The preprohormones of the subfamily-I have a CHH precursor related peptide (CPRP) that is cleaved off during processing; and preprohormones of the subfamily-II lack the CPRP (9). Uncovering their physiological functions will provide new insights into neuroendocrine regulation of energy homeostasis.Characterization of CHH-family neuropeptides is challenging. They are comprised of more than 70 amino acids and often contain multiple post-translational modifications (PTMs)

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confidence: 99%

High-definition De Novo Sequencing of Crustacean Hyperglycemic Hormone (CHH)-family Neuropeptides

Jia

Hui

Cao

et al. 2012

Molecular & Cellular Proteomics

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“…They can also be detected in many other organs of the American lobster. 48 These three families display similar patterns in Figure 6, and the representative trend of orcokinin at m / z 1502.69 is shown in green trace in Figure 7. Previous reports indicated that FMRFamide and orcokinins appeared in the STNS as early as midembryonic stage (E50).…”

Section: Resultsmentioning

confidence: 63%

“…Notably, the neuropeptides are not evenly distributed in the brain. 47,48 The conversion here is just an approximation to facilitate neurobiologists’ understanding of relationship of total neuropeptide abundance as a function of lobster developmental stage. The calculated results for four selected peptides are illustrated in Figure 7.…”

Section: Resultsmentioning

confidence: 99%

Relative Quantitation of Neuropeptides at Multiple Developmental Stages of the American Lobster Using N,N-Dimethyl Leucine Isobaric Tandem Mass Tags

Jiang

Xiang

Jia

et al. 2018

ACS Chem. Neurosci.

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Neuromodulators and neurotransmitters play important roles in neural network development. The quantitative changes of these signaling molecules often reflect their regulatory roles in physiological processes. Currently, several commercial tags (e.g., iTRAQ and TMT) have been widely used in proteomics. With reduced cost and higher labeling efficiency, we employed a set of custom-developed N,N-dimethyl leucine (DiLeu) 4-plex isobaric tandem mass tags as an attractive alternative for the relative quantitation of neuropeptides in brain tissue of American lobster Homarus americanus at multiple developmental stages. A general workflow for isobaric labeling of neuropeptides followed by LC-MS/MS analysis has been developed, including optimized sample handling procedures. Overall, we were able to quantify 18 trace-amount neuropeptides from 6 different families using a single adult brain as a control. The quantitation results indicated that the expressions of different neuropeptide families had significant changes over distinct developmental stages. Additionally, our data revealed intriguing elevated expression of neuropeptides in the early juvenile development stage. The methodology presented here advanced the workflow of DiLeu as an alternative labeling approach and the application of DiLeu-based quantitative peptidomics, which can be extended to areas beyond neuroscience.

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“…Interestingly, two Atype allatostatins PRNYAFGLamide (m/z 936.51) and PRDYAFGLamide (m/z 937.49) were recently sequenced from the pericardial organs of H. americanus by nanoLC ESI QTOF MS/MS. 37 To test whether they exist in the STG, CE separation was employed to resolve these peaks. Figure 3a is a zoom-in spectrum of the STG extract, showing CabTRP Ia and its isotope envelope.…”

Section: ■ Results and Discussionmentioning

confidence: 99%

Mass Spectral Charting of Neuropeptidomic Expression in the Stomatogastric Ganglion at Multiple Developmental Stages of the Lobster Homarus americanus

Jiang

Chen

Wang

et al. 2012

ACS Chem. Neurosci.

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ABSTRACT:The stomatogastric nervous system (STNS) of the American lobster Homarus americanus serves as a useful model for studies of neuromodulatory substances such as peptides and their roles in the generation of rhythmic behaviors. As a central component of the STNS, the stomatogastric ganglion (STG) is rich in neuropeptides and contains welldefined networks of neurons, serving as an excellent model system to study the effect of neuropeptides on the maturation of neural circuits. Here, we utilize multiple mass spectrometry (MS)-based techniques to study the neuropeptide content and abundance in the STG tissue as related to the developmental stage of the animal. Capillary electrophoresis (CE)-MS was employed to unambiguously identify low abundance neuropeptide complements, which were not fully addressed using previous methods. In total, 35 neuropeptides from 7 different families were detected in the tissue samples. Notably, 10 neuropeptides have been reported for the first time in this study. In addition, we utilized a relative quantitation method to compare neuropeptidomic expression at different developmental stages and observed sequential appearance of several neuropeptides. Multiple isoforms within the same peptide family tend to show similar trends of changes in relative abundance during development. We also determined that the relative abundances of tachykinin peptides increase as the lobster grows, suggesting that the maturation of circuit output may be influenced by the change of neuromodulatory input into the STG. Collectively, this study expands our knowledge about neuropeptides in the crustacean STNS and provides useful information about neuropeptide expression in the maturation process.

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Mass Spectral Analysis of Neuropeptide Expression and Distribution in the Nervous System of the Lobster Homarus americanus

Cited by 62 publications

References 54 publications

High-definition De Novo Sequencing of Crustacean Hyperglycemic Hormone (CHH)-family Neuropeptides

High-definition De Novo Sequencing of Crustacean Hyperglycemic Hormone (CHH)-family Neuropeptides

Relative Quantitation of Neuropeptides at Multiple Developmental Stages of the American Lobster Using N,N-Dimethyl Leucine Isobaric Tandem Mass Tags

Mass Spectral Charting of Neuropeptidomic Expression in the Stomatogastric Ganglion at Multiple Developmental Stages of the Lobster Homarus americanus

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