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Qualitative and Quantitative Proteomics Methods for the Analysis of the Anopheles gambiae Mosquito Proteome

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Short Views on Insect Genomics and Proteomics

Part of the book series: Entomology in Focus ((ENFO,volume 4))

Abstract

Anopheles gambiae is the major African malaria vector. Insecticide and drug resistance highlight the need for novel malaria control strategies. A. gambiae exhibits daily (diel and/or circadian) rhythms in physiology and behavior that include flight, mating, sugar and blood-meal feeding, and oviposition. Olfaction is important for detecting blood-feeding hosts, sugar feeding sources, and oviposition sites. We previously reported on mRNA array-based changes in gene expression under light–dark cycle (diel) and constant dark (circadian) conditions. We were able to characterize 25 known or putative olfactory genes in female heads. We sought to follow up on these reported changes in gene expression and correlate them with expected changes in protein response. Here, we describe our recently developed methods and meta-level results for both qualitative and differential proteomics analyses of A. gambiae mosquitoes collected in a time-of-day-specific framework to assess temporal changes in protein abundance over the 24-h day. The traditional challenges associated with proteomics are amplified in an insect such as the mosquito, which contains a large amount of non-proteinaceous material associated with the cuticle and trachea and a high dynamic background of proteins associated with flight muscles and oxidative metabolism (e.g., myosin, glutathione S-transferases). We thus sought to use targeted, quantitative proteomics to directly measure differences in protein abundance in a time-of-day-dependent manner. We used multiple reaction monitoring (MRM), which has the advantage of being able to probe selected target lists with high sensitivity, wide dynamic range, and good/excellent reproducibility. We first characterized proteins in a qualitative format and subsequently examined subsets of specific proteins of interest in a high-fidelity quantifiable approach. Targeted quantitative multiple/single reaction monitoring (MRM/SRM) proteomics allowed for the measurement of changes in protein abundance in a time-of-day-specific manner over the 24-h diel cycle. Utilizing this accurate technique requires robust and reproducible protein/peptide preparation techniques in order to obtain consistent data. Here, we describe a technique using liquid N2 homogenization-based protein extraction and proteolytic digestion applied to multiple discrete tissues (whole heads, antennae, total head appendages, compound eyes, and bodies), with subsequent liquid chromatography/tandem mass spectrometry (LC/MS/MS)-based analysis of the resulting tryptic peptides. This technique is largely portable and should function well in any arthropod system with little modification. The results of our analyses are the generation of tissue-discrete determination of peptides, targeted quantitative analysis of peptides, and the deposition of datasets in VectorBase.org for use by the vector biology, arthropod, and proteomics research communities.

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Abbreviations

ABC:

Ammonium bicarbonate, Ambic

BEH:

Ethylene-bridged hybrid

CID/CAD:

Collision-induced dissociation/collisionally activated dissociation

CV:

Coefficient of variation

DTT:

Dithiothreitol

EDTA:

Ethylenediaminetetraacetic acid

FASP:

Filter-aided sample prep

FDR:

False discovery rate

IAA:

Iodoacetamide

LC/MS/MS:

Liquid chromatography tandem mass spectrometry

MS-MS/MS:

Mass spectrometry tandem mass spectrometry

MRM/SRM:

Multiple reaction monitoring/selected reaction monitoring

NaDOC:

Sodium deoxycholate

OBP:

Odorant-binding protein

ORF:

Open reading frame

PCR:

Polymerase chain reaction

PMSF:

Phenylmethylsulfonyl fluoride

Q1, Q2, etc.:

First and second quadrupoles

QqQ:

Triple quadrupole

RT:

Retention time

SDS-PAGE:

Sodium dodecyl sulfate-polyacrylamide gel electrophoresis

TCEP:

Tris(2-carboxyethyl)phosphine hydrochloride

TFE:

2,2,2-Trifluoroethanol

THAs:

Total head appendages

TIC:

Total ion current

TOP8,10:

Top 8,10 precursor selection method

UHPLC:

Ultrahigh-performance liquid chromatography

XIC/EIC:

Extracted ion chromatogram

ZT:

Zeitgeber time

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Acknowledgments

This research was supported by grants (to GED) from Eck Institute for Global Health and the Center for Rare and Neglected Diseases, University of Notre Dame (UND), and the Indiana Clinical Translational Sciences Institute, funded in part by a grant (UL1TR001108) from the National Institutes of Health, National Center for Advancing Translational Sciences, Clinical and Translational Sciences Award, and NIGMS (R01-GM087508). We thank B. Boggess and M. Joyce and the UND Mass Spectrometry & Proteomics Facility (MSPF) for their ongoing support and assistance with proteomics research, J. Ghazi for his assistance with sample preparation, and the editors for their careful reading and critique of this chapter.

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Authors and Affiliations

  1. Department of Chemistry and Biochemistry, Nieuwland Science Hall, University of Notre Dame, Notre Dame, IN, USA

    Matthew M. Champion

  2. Department of Biological Sciences, Galvin Life Science Center, Eck Institute for Global Health, University of Notre Dame, Notre Dame, IN, USA

    Aaron D. Sheppard, Samuel S. C. Rund, Stephanie A. Freed, Joseph E. O’Tousa & Giles E. Duffield

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  1. Matthew M. Champion
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Correspondence to Giles E. Duffield .

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Editors and Affiliations

  1. Department of Biochemistry and Molecular Biophysics, Kansas State University, Manhattan, Kansas, USA

    Chandrasekar Raman

  2. Biological Sciences Department Center for Biotech. and Life Sciences, University of Rhode Island, Kingston, Rhode Island, USA

    Marian R. Goldsmith

  3. Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut, USA

    Tolulope A. Agunbiade

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Champion, M.M., Sheppard, A.D., Rund, S.S.C., Freed, S.A., O’Tousa, J.E., Duffield, G.E. (2016). Qualitative and Quantitative Proteomics Methods for the Analysis of the Anopheles gambiae Mosquito Proteome. In: Raman, C., Goldsmith, M., Agunbiade, T. (eds) Short Views on Insect Genomics and Proteomics. Entomology in Focus, vol 4. Springer, Cham. https://doi.org/10.1007/978-3-319-24244-6_2

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