Abstract
Laser-ablation electrospray ionization (LAESI) imaging mass spectrometry (IMS) is an emerging bioanalytical tool for direct imaging and analysis of biological tissues. Performing ionization in an ambient environment, this technique requires little sample preparation and no additional matrix, and can be performed on natural, uneven surfaces. When combined with optical microscopy, the investigation of biological samples by LAESI allows for spatially resolved compositional analysis. We demonstrate here the applicability of LAESI-IMS for the chemical analysis of thin, desiccated biological samples, specifically Neotibicen pruinosus cicada wings. Positive-ion LAESI-IMS accurate ion-map data was acquired from several wing cells and superimposed onto optical images allowing for compositional comparisons across areas of the wing. Various putative chemical identifications were made indicating the presence of hydrocarbons, lipids/esters, amines/amides, and sulfonated/phosphorylated compounds. With the spatial resolution capability, surprising chemical distribution patterns were observed across the cicada wing, which may assist in correlating trends in surface properties with chemical distribution. Observed ions were either (1) equally dispersed across the wing, (2) more concentrated closer to the body of the insect (proximal end), or (3) more concentrated toward the tip of the wing (distal end). These findings demonstrate LAESI-IMS as a tool for the acquisition of spatially resolved chemical information from fragile, dried insect wings. This LAESI-IMS technique has important implications for the study of functional biomaterials, where understanding the correlation between chemical composition, physical structure, and biological function is critical.
References
Bhushan B, Jung YC. Natural and biomimetic artificial surfaces for superhydrophobicity, self-cleaning, low adhesion, and drag reduction. Prog Mater Sci. 2011;56(1):1–108.
Dooley C, Taylor D. Self-healing materials: what can nature teach us? Fatigue Fract Eng Mater Struct. 2017;40(5):655–69.
Gao X, Yan X, Yao X, Xu L, Zhang K, Zhang J, et al. The dry-style antifogging properties of mosquito compound eyes and artificial analogues prepared by soft lithography. Adv Mater. 2007;19(17):2213–7.
Chapman J, Hellio C, Sullivan T, Brown R, Russell S, Kiterringham E, et al. Bioinspired synthetic macroalgae: examples from nature for antifouling applications. Int Biodeter Biodegr. 2014;86:6–13.
Ivanova EP, Hasan J, Webb HK, Truong VK, Watson GS, Watson JA, et al. Natural bactericidal surfaces: mechanical rupture of Pseudomonas aeruginosa cells by cicada wings. Small. 2012;8(16):2489–94.
Hasan J, Webb HK, Truong VK, Pogodin S, Baulin VA, Watson GS, et al. Selective bactericidal activity of nanopatterned superhydrophobic cicada Psaltoda claripennis wing surfaces. Appl Microbiol Biotechnol. 2013;97(20):9257–62.
Oh J, Dana CE, Hong S, Román JK, Jo KD, Hong JW, et al. Exploring the role of habitat on the wettability of cicada wings. ACS Appl Mater Interfaces. 2017;9(32):27173–84.
Ivanova EP, Nguyen SH, Webb HK, Hasan J, Truong Khanh V, Lamb RN, et al. Molecular organization of the nanoscale surface structures of the dragonfly Hemianax papuensis wing epicuticle. PLoS One. 2013;8(7):e67893.
Trusheva B, Trunkova D, Bankova V. Different extraction methods of biologically active components from propolis: a preliminary study. Chem Cent J Springer International Publishing. 2007;1(1):13.
Liu J, Sandahl M, Sjöberg PJR, Turner C. Pressurised hot water extraction in continuous flow mode for thermolabile compounds: extraction of polyphenols in red onions. Anal Bioanal Chem. Springer Berlin Heidelberg. 2014;406(2):441–5.
Papaioannou E, Roukas T, Liakopoulou-Kyriakides M. Effect of biomass pre-treatment and solvent extraction on beta-carotene and lycopene recovery from Blakeslea trispora cells. Prep Biochem Biotechnol. Taylor & Francis Group. 2008;38(3):246–56.
Reis A, Rudnitskaya A, Blackburn GJ, Mohd Fauzi N, Pitt AR, Spickett CM. A comparison of five lipid extraction solvent systems for lipidomic studies of human LDL. J Lipid Res Am Soc Biochem Mol Biol. 2013;54(7):1812–24.
Smelcerovic A, Spiteller M, Zuehlke S. Comparison of methods for the exhaustive extraction of hypericins, flavonoids, and hyperforin from Hypericum perforatum L. J Agric Food Chem. 2006;54(7):2750–3.
Vickerman JC. Molecular imaging and depth profiling by mass spectrometry-SIMS, MALDI or DESI? Analyst. 2011;136(11):2199–217.
Seeley EH, Caprioli RM. 3D imaging by mass spectrometry: a new frontier. Anal Chem. 2012;84(5):2105–10.
Watrous JD, Alexandrov T, Dorrestein PC. The evolving field of imaging mass spectrometry and its impact on future biological research. J Mass Spectrom. 2011;46(2):209–22.
Gode D, Volmer DA. Lipid imaging by mass spectrometry—a review. Analyst. 2013;138(5):1289–315.
Kertesz V, Van Berkel GJ. Improved imaging resolution in desorption electrospray ionization mass spectrometry. Rapid Commun Mass Spectrom. John Wiley & Sons Ltd. 2008;22(17):2639–44.
Pasilis SP, Kertesz V, Van Berkel GJ. Surface scanning analysis of planar arrays of analytes with desorption electrospray ionization-mass spectrometry. Anal Chem. 2007;79(15):5956–62.
Gross JH. Direct analysis in real time—a critical review on DART-MS. Anal Bioanal Chem. Springer Berlin Heidelberg. 2014;406(1):63–80.
Wang H, Sun W, Zhang J, Yang X, Lin T, Ding L. Desorption corona beam ionization source for mass spectrometry. Analyst. 2010;135(4):688–95.
Huang M-Z, Jhang S-S, Shiea J. Electrospray laser desorption ionization (ELDI) mass spectrometry for molecular imaging of small molecules on tissues. Methods Mol Biol. New York, NY: Springer New York. 2015;1203(Chapter 11):107–16.
Hiraoka K, Usmanov DT, Chen LC, Ninomiya S, Mandal MK, Saha S. Probe electrospray ionization (PESI) mass spectrometry with discontinuous atmospheric pressure interface (DAPI). Eur J Mass Spectrom (Chichester). SAGE PublicationsSage UK: London, England. 2015;21(3):327–34.
Pan N, Rao W, Kothapalli NR, Liu R, Burgett AWG, Yang Z. The single-probe: a miniaturized multifunctional device for single cell mass spectrometry analysis. Anal Chem Am Chem Soc. 2014;86(19):9376–80.
Laskin J, Heath BS, Roach PJ, Cazares L, Semmes OJ. Tissue imaging using nanospray desorption electrospray ionization mass spectrometry. Anal Chem. 2012;84(1):141–8.
Van Berkel GJ, Kertesz V, Koeplinger KA, Vavrek M, Kong A-NT. Liquid microjunction surface sampling probe electrospray mass spectrometry for detection of drugs and metabolites in thin tissue sections. J Mass Spectrom. John Wiley & Sons Ltd. 2008;43(4):500–8.
Peng W-P, Yang Y-C, Kang M-W, Tzeng Y-K, Nie Z, Chang H-C, et al. Laser-induced acoustic desorption mass spectrometry of single bioparticles. Angew Chem Int Ed WILEY-VCH Verlag. 2006;45(9):1423–6.
Nemes P, Vertes A. Laser ablation electrospray ionization for atmospheric pressure, in vivo, and imaging mass spectrometry. Anal Chem. 2007;79(21):8098–106.
Nemes P, Vertes A. Ambient mass spectrometry for in vivo local analysis and in situ molecular tissue imaging. Trends Anal Chem TrAC. 2012;34:22–34.
Huang M-Z, Yuan C-H, Cheng S-C, Cho Y-T, Shiea J. Ambient ionization mass spectrometry. Annu Rev Anal Chem. 2010;3(1):43–65.
Wu C, Dill AL, Eberlin LS, Cooks RG, Ifa DR. Mass spectrometry imaging under ambient conditions. Mass Spectrom Rev. 2013;32(3):218–43.
Huang M-Z, Cheng S-C, Jhang S-S, Chou C-C, Cheng C-N, Shiea J, et al. Ambient molecular imaging of dry fungus surface by electrospray laser desorption ionization mass spectrometry. Int J Mass Spectrom. 2012;325–327:172–82.
Chen LC, Yoshimura K, Yu Z, Iwata R, Ito H, Suzuki H, et al. Ambient imaging mass spectrometry by electrospray ionization using solid needle as sampling probe. J Mass Spectrom. 2009;44(10):1469–77.
Shrestha B, Sripadi P, Walsh CM, Razunguzwa TT, Powell MJ, Kehn-Hall K, et al. Rapid, non-targeted discovery of biochemical transformation and biomarker candidates in oncovirus-infected cell lines using LAESI mass spectrometry. Chem Commun. 2012;48(31):3700–2.
Berkenkamp S, Karas M, Hillenkamp F. Ice as a matrix for IR-matrix-assisted laser desorption/ionization: mass spectra from a protein single crystal. Proc Natl Acad Sci U S A. 1996;93(14):7003–7.
Bartels B, Svatoš A. Spatially resolved in vivo plant metabolomics by laser ablation-based mass spectrometry imaging (MSI) techniques: LDI-MSI and LAESI. Front Plant Sci. 2015;6:471.
Cabral EC, Mirabelli MF, Perez CJ, Ifa DR. Blotting assisted by heating and solvent extraction for DESI-MS imaging. J Am Soc Mass Spectrom. 2013;24(6):956–65.
Shrestha B, Nemes P, Nazarian J, Hathout Y, Hoffman EP, Vertes A. Direct analysis of lipids and small metabolites in mouse brain tissue by AP IR-MALDI and reactive LAESI mass spectrometry. Analyst. 2010;135(4):751–8.
Müller WEG, Wang S, Neufurth M, Kokkinopoulou M, Feng Q, Schröder HC, et al. Polyphosphate as a donor of high-energy phosphate for the synthesis of ADP and ATP. J Cell Sci. 2017;130(16):2747–56.
Lockey KH. Lipids of the insect cuticle: origin, composition and function. Comp Biochem Physiol B Biochem Mol Biol. 1988;89(4):595–645.
Kind T, Fiehn O. Seven golden rules for heuristic filtering of molecular formulas obtained by accurate mass spectrometry. BMC Bioinformatics BioMed Central. 2007;8(1):105.
Bae E, Yeo IJ, Jeong B, Shin Y, Shin K-H, Kim S. Study of double bond equivalents and the numbers of carbon and oxygen atom distribution of dissolved organic matter with negative-mode FT-ICR MS. Anal Chem. 2011;83(11):4193–9.
Smith CA, O'Maille G, Want EJ, Qin C, Trauger SA, Brandon TR, et al. METLIN: a metabolite mass spectral database. Ther Drug Monit. 2005;27(6):747–51.
Li H, Smith BK, Márk L, Nemes P, Nazarian J, Vertes A. Ambient molecular imaging by laser ablation electrospray ionization mass spectrometry with ion mobility separation. Int J Mass Spectrom. 2015;377:681–9.
Shrestha B, Vertes A. Situ metabolic profiling of single cells by laser ablation electrospray ionization mass spectrometry. Anal Chem. 2009;81(20):8265–71.
Nemes P, Barton AA, Vertes A. Three-dimensional imaging of metabolites in tissues under ambient conditions by laser ablation electrospray ionization mass spectrometry. Anal Chem. 2009;81(16):6668–75.
Nemes P, Woods AS, Vertes A. Simultaneous imaging of small metabolites and lipids in rat brain tissues at atmospheric pressure by laser ablation electrospray ionization mass spectrometry. Anal Chem. 2010;82(3):982–8.
Miljkovic N, Wang EN. Condensation heat transfer on superhydrophobic surfaces. MRS Bull. 2013;38(05):397–406.
Enright R, Miljkovic N, Al-Obeidi A, Thompson CV, Wang EN. Condensation on superhydrophobic surfaces: the role of local energy barriers and structure length scale. Langmuir. 2012;28(40):14424–32.
Koch K, Ensikat H-J. The hydrophobic coatings of plant surfaces: epicuticular wax crystals and their morphologies, crystallinity and molecular self-assembly. Micron. 2008;39(7):759–72.
Samuels L, Kunst L, Jetter R. Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol. 2008;59(1):683–707.
Buckner JS. Structure and analysis of insect hydrocarbons. Cambridge: Cambridge University Press; 2009.
van Maarseveen C, Jetter R. Composition of the epicuticular and intracuticular wax layers on Kalanchoe daigremontiana (Hamet et Perr. de la Bathie) leaves. Phytochemistry. 2009;70(7):899–906.
Banerjee S, Mazumdar S. Electrospray ionization mass spectrometry: a technique to access the information beyond the molecular weight of the analyte. Int J Anal Chem Hindawi. 2012;2012(8):282574–40.
Kreuz P, Arnold W, Kesel AB. Acoustic microscopic analysis of the biological structure of insect wing membranes with emphasis on their waxy surface. Ann Biomed Eng. 2001;29(12):1054–8.
Knowles JR. Enzyme-catalyzed phosphoryl transfer reactions. Annu Rev Biochem. 1980;49(1):877–919.
Frankiewicz C, Attinger D. Texture and wettability of metallic lotus leaves. Nano. 2016;8(7):3982–90.
Acknowledgements
Scanning electron microscopy was carried out at the Beckman Institute, University of Illinois.
Funding
Funding was provided through the U.S. Army Basic Research Program, supporting the University of Illinois collaborators (N.M. and M.A.) through U.S. Army Construction Engineering Research Laboratory, CESU W9132T-16-2-0011. N.M. gratefully acknowledges funding support from the National Science Foundation under Award No. 1554249 and the International Institute for Carbon Neutral Energy Research (WPI-I2CNER), sponsored by the Japanese Ministry of Education, Culture, Sports, Science and Technology.
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Román, J.K., Walsh, C.M., Oh, J. et al. Spatially resolved chemical analysis of cicada wings using laser-ablation electrospray ionization (LAESI) imaging mass spectrometry (IMS). Anal Bioanal Chem 410, 1911–1921 (2018). https://doi.org/10.1007/s00216-018-0855-7
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DOI: https://doi.org/10.1007/s00216-018-0855-7