In Situ Visual Distribution of Gelsemine, Koumine, and Gelsenicine by MSI in Gelsemiumelegans at Different Growth Stages
Abstract
:1. Introduction
2. Results
2.1. In Situ Visualization of Three Alkaloids in Mature Organs/Tissues
2.2. Visualization of Three Alkaloids in G. elegans Seedlings at Different Stages
2.3. Relative Quantification of Three Alkaloids Based on Image Brightness Intensities
2.4. Method Validation
3. Discussion
4. Materials and Methods
4.1. Chemicals and Reagents
4.2. Plant Growth Conditions
4.3. Frozen Section Preparation for DESI-MSI
4.4. DESI-MSI Instrumentation and Data Acquisition
4.5. Sampling for LC-MS/MS
4.6. Standard Curve Preparation for LC-MS/MS
4.7. LC-MS/MS Instrumentation and Data Acquisition
4.8. Imaging and Data Processing
4.9. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
References
- Struwe, L.; Albert, V.A.; Bremer, B. Cladistics and family level classification of the Gentianales. Cladistics 1994, 10, 175–206. [Google Scholar] [CrossRef]
- Jin, G.L.; Su, Y.P.; Liu, M.; Xu, Y.; Yang, J.; Liao, K.J.; Yu, C.X. Medicinal plants of the genus Gelsemium (Gelsemiaceae, Gentianales)-A review of their phytochemistry, pharmacology, toxicology and traditional use. J. Ethnopharmacol. 2014, 152, 33–52. [Google Scholar] [CrossRef] [PubMed]
- Pascarella, J.B. Mechanisms of prezygotic reproductive isolation between two sympatric species, Gelsemium rankinii and G. sempervirens (Gelsemiaceae), in the southeastern United States. Am. J. Bot. 2007, 94, 468–476. [Google Scholar] [CrossRef] [PubMed]
- Dutt, V.; Thakur, S.; Dhar, V.J.; Sharma, A. The genus Gelsemium: An update. Pharmacogn. Rev. 2010, 4, 185–194. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.C.; Xiao, S.; Yang, K.; Ling, L.; Sun, Z.L.; Liu, Z.-Y. Comprehensive identification and structural characterization of target components from Gelsemium elegans by high-performance liquid chromatography coupled with quadrupole time-of-flight mass spectrometry based on accurate mass databases combined with. J. Mass Spectrom. 2017, 52, 378–396. [Google Scholar] [CrossRef]
- Xu, Y.K.; Liao, S.G.; Na, Z.; Hu, H.B.; Yan, L.; Luo, H.R. Gelsemium alkaloids, immunosuppressive agents from Gelsemium elegans. Fitoterapia 2012, 83, 1120–1124. [Google Scholar] [CrossRef]
- Li, S.; Cheng, X.; Wang, C. A review on traditional uses, phytochemistry, pharmacology, pharmacokinetics and toxicology of the genus Peganum. J. Ethnopharmacol. 2017, 203, 127–162. [Google Scholar] [CrossRef]
- Liu, M.; Huang, H.H.; Yang, J.; Su, Y.P.; Lin, H.W.; Lin, L.Q.; Liao, W.J.; Yu, C.X. The active alkaloids of Gelsemium elegans Benth. are potent anxiolytics. Psychopharmacology 2012, 225, 839–851. [Google Scholar] [CrossRef]
- Ling, Q.; Liu, M.; Wu, M.X.; Xu, Y.; Yang, J.; Huang, H.H.; Yu, C.X. Anti-allodynic and neuroprotective effects of koumine, a Benth alkaloid, in a rat model of diabetic neuropathy. Biol. Pharm. Bull. 2014, 37, 858–864. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.H.; Chen, Y.; Gao, B.; Luo, D.L.; Wen, Y.Y.; Ma, X.L. Apoptotic effect of koumine on human breast cancer cells and the mechanism involved. Cell Biochem. Biophys. 2015, 72, 411–416. [Google Scholar] [CrossRef]
- Zhang, B.F.; Zhang, Q.P.; Hai, L.; Chou, G.X.; Wang, Z.T. Iridoids from leaves of Gelsemium elegans. Phytochemistry 2011, 72, 916–922. [Google Scholar] [CrossRef] [PubMed]
- Su, Y.P.; Jie, S.; Xu, Y.; Mi, Z.; Yu, C.X. Preparative separation of alkaloids from Gelsemium elegans Benth. using pH-zone-refining counter-current chromatography. J. Chromatogr. A 2011, 1218, 3695–3698. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Zhang, J.; Zhang, C.; Sun, X.; Liao, X.; Zheng, W.; Yin, Q.; Yang, J.; Mao, D.; Wang, B.; et al. The qualitative and quantitative analyses of Gelsemium elegans. J. Pharmaceut. Biomed. 2019, 172, 329–338. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Pan, H.; Bai, Y.; Li, H.; Xian, Y.F. Gelsemine, a natural alkaloid extracted from Gelsemium elegans Benth. alleviates neuroinflammation and cognitive impairments in Aβ oligomer-treated mice. Psychopharmacology 2020, 237, 2111–2124. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Zhang, S.Y.; Wang, G.Y.; Li, N.P.; Chen, M.F.; Gu, J.H.; Zhang, D.M.; Wang, L.; Ye, W.C. Five new koumine-type alkaloids from the roots of Gelsemium elegans. Fitoterapia 2017, 118, 112–117. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.E.; Li, Y.D.; Luo, Y.J.; Wang, T.X.; Wang, H.J.; Chen, S.N.; Qu, W.M.; Huang, Z.L. Gelsemine alleviates both neuropathic pain and sleep disturbance in partial sciatic nerve ligation mice. Acta. Pharmacol. Sin. 2015, 36, 1308–1317. [Google Scholar] [CrossRef]
- Meyer, L.; Boujedaini, N.; Patte-Mensah, C.; Mensah-Nyagan, A.G. Pharmacological effect of gelsemine on anxiety-like behavior in rat. Behav. Brain Res. 2013, 253, 90–94. [Google Scholar] [CrossRef]
- Khuong-Huu, F.; Chiaroni, A.; Riche, C. Structure of koumine, an alkaloid from gelsemium elegans benth. Tetrahedron Lett. 1981, 22, 733–734. [Google Scholar] [CrossRef]
- Ying, X.; Qiu, H.Q.; Hao, L.; Liu, M.; Huang, Z.Y.; Yang, J.; Su, Y.P.; Yu, C.X. Effects of koumine, an alkaloid of Gelsemium elegans Benth., on inflammatory and neuropathic pain models and possible mechanism with allopregnanolone. Pharmacol. Biochem. Behav. 2012, 101, 504–514. [Google Scholar]
- Liu, M.; Shen, J.; Liu, H.; Xu, Y.; Su, Y.P.; Yang, J.; Yu, C.X. Gelsenicine from Gelsemium elegans attenuates neuropathic and inflammatory pain in mice. Biol. Pharm. Bull. 2011, 34, 1877–1880. [Google Scholar] [CrossRef] [Green Version]
- Yang, K.; Long, X.M.; Liu, Y.C.; Chen, F.H.; Liu, X.F.; Sun, Z.L.; Liu, Z.Y. Development and in-house validation of a sensitive LC-MS/MS method for simultaneous quantification of gelsemine, koumine and humantenmine in porcine plasma. J. Chromatogr. B 2018, 1076, 54–60. [Google Scholar] [CrossRef] [PubMed]
- Yu, L.; Zeng, R.; Lu, Q.; Wu, S.; Chen, J. Ultrasound/microwave-assisted extraction and comparative analysis of bioactive/toxic indole alkaloids in different medicinal parts of Gelsemium elegans Benth by ultra-high performance liquid chromatography with MS/MS. J. Sep. Sci. 2014, 37, 308–313. [Google Scholar]
- Kogure, N.; Nishiya, C.; Kitajima, M.; Takayama, H. Six new indole alkaloids from Gelsemium sempervirens Ait. f. Tetrahedron Lett. 2005, 46, 5857–5861. [Google Scholar] [CrossRef]
- Lai, C.K.; Chan, Y.W. Confirmation of gelsemium poisoning by targeted analysis of toxic gelsemium alkaloids in urine. J. Anal. Toxicol. 2009, 33, 56–61. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, Y.; Wang, J. HPLC fingerprint of Gelsemium and its source analysis. For. Sci. Technol. 2016, 41, 50–53. [Google Scholar]
- Ponglux, D.; Wongseripipatana, S.; Takayama, H.; Ogata, K.; Aimi, N.; Sakai, S. A new class of indole alkaloid ‘elegansamine’ constructed from a monoterpenoid indole alkaloid and an iridoid. Tetrahedron Lett. 1988, 29, 5395–5396. [Google Scholar] [CrossRef]
- Sun, M.; Hou, X.; Gao, H.; Guo, J.; Kai, X. Two new koumine-type indole alkaloids from Gelsemium elegans Benth. Molecules 2013, 18, 1819–1825. [Google Scholar] [CrossRef]
- Kitajima, M.; Nakamura, T.; Kogure, N.; Ogawa, M.; Mitsuno, Y.; Ono, K.; Yano, S.; Aimi, N.; Takayama, H. Isolation of gelsedine-type indole alkaloids from Gelsemium elegans and evaluation of the cytotoxic activity of gelsemium alkaloids for A431 epidermoid carcinoma cells. J. Nat. Prod. 2006, 69, 715–718. [Google Scholar] [CrossRef]
- Kogure, N.; Someya, A.; Urano, A.; Kitajima, M.; Takayama, H. Total synthesis and full NMR assignment of ourouparine, a yohimbane-type indole alkaloid isolated from Gelsemium sempervirens. J. Nat. Med. 2007, 61, 208–212. [Google Scholar] [CrossRef]
- Babazadeh, S.; Moghaddam, P.A.; Sabatyan, A.; Sharifian, F. Classification of potato tubers based on solanine toxicant using laser-induced light backscattering imaging. Comput. Electron. Agric. 2016, 129, 1–8. [Google Scholar] [CrossRef]
- Ruike, T.; Kanai, Y.; Iwabata, K.; Matsumoto, Y.; Murata, H.; Ishima, M.; Ohta, K.; Oshige, M.; Katsura, S.; Kuramochi, K.; et al. Distribution and metabolism of 14C-Sulfoquinovosylacylpropanediol(14C-SQAP) after a single intravenous administration in tumor-bearing mice. Xenobiotica 2019, 49, 346–362. [Google Scholar] [CrossRef] [PubMed]
- Ahmadian-Fard-Fini, S.; Ghanbari, D.; Amiri, O.; Salavati-Niasari, M. Electro-spinning of cellulose acetate nanofibers/Fe/carbon dot as photoluminescence sensor for mercury (II) and lead (II) ions. Carbohydr. Polym. 2020, 229, 115428. [Google Scholar] [CrossRef] [PubMed]
- Ahmadian-Fard-Fini, S.; Ghanbari, D.; Salavati-Niasari, M. Photoluminescence carbon dot as a sensor for detecting of pseudomonas aeruginosa bacteria: Hydrothermal synthesis of magnetic hollow NiFe2O4-carbon dots nanocomposite material. Compos. Part B Eng. 2019, 161, 564–577. [Google Scholar] [CrossRef]
- Zinatloo-Ajabshir, S.; Mortazavi-Derazkola, S.; Salavati-Niasari, M. Nd2O3-SiO2 nanocomposites: A simple sonochemical preparation, characterization and photocatalytic activity. Ultrason. Sonochem. 2018, 42, 171–182. [Google Scholar] [CrossRef] [PubMed]
- Watrous, J.D.; Dorrestein, P.C. Imaging mass spectrometry in microbiology. Nat. Rev. Microbiol. 2011, 9, 683–694. [Google Scholar] [CrossRef] [Green Version]
- Cornett, D.S.; Reyzer, M.L.; Chaurand, P.; Caprioli, R.M. MALDI imaging mass spectrometry: Molecular snapshots of biochemical systems. Nat. Methods 2007, 4, 828–833. [Google Scholar] [CrossRef]
- Chughtai, K.; Heeren, R. Mass spectrometric imaging for biomedical tissue analysis. Chem. Rev. 2010, 110, 3237–3277. [Google Scholar] [CrossRef] [Green Version]
- Meng, Y.; Cheng, X.; Wang, T.; Hang, W.; Li, X.; Nie, W.; Liu, R.; Lin, Z.; Hang, L.; Yin, Z.; et al. Micro-lensed fiber laser desorption mass spectrometry imaging reveals subcellular distribution of drugs within single cells. Angew. Chem. Int. Ed. Engl. 2020, 59, 17864–17871. [Google Scholar] [CrossRef]
- Takats, Z.; Wiseman, J.M.; Gologan, B.; Cooks, R.G. Mass spectrometry sampling under ambient conditions with desorption electrospray ionization. Science 2004, 306, 471–473. [Google Scholar] [CrossRef] [Green Version]
- Eberlin, L.S.; Ifa, D.R.; Wu, C.; Cooks, R.G. Three-dimensional vizualization of mouse brain by lipid analysis using ambient ionization mass spectrometry. Angew. Chem. 2010, 49, 873–876. [Google Scholar] [CrossRef]
- Kumara, P.M.; Srimany, A.; Ravikanth, G.; Shaanker, R.U.; Pradeep, T. Ambient ionization mass spectrometry imaging of rohitukine, a chromone anti-cancer alkaloid, during seed development in Dysoxylum binectariferum Hook.f (Meliaceae). Phytochemistry 2015, 116, 104–110. [Google Scholar] [CrossRef] [PubMed]
- Yang, K.; Huang, Y.-J.; Xiao, S.; Liu, Y.-C.; Sun, Z.-L.; Liu, Y.-S.; Tang, Q.; Liu, Z.-Y. Identification of gelsemine metabolites in rat liver S9 by high-performance liquid chromatography/quadrupole-time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 2017, 32, 19–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jeong, W.T.; Lim, H.B. A UPLC-ESI-Q-TOF method for rapid and reliable identification and quantification of major indole alkaloids in Catharanthus roseus. J. Chromatogr. B 2018, 1080, 27–36. [Google Scholar] [CrossRef] [PubMed]
- Fu, C.; Yu, P.; Wang, M.; Qiu, F. Phytochemical analysis and geographic assessment of flavonoids, coumarins and sesquiterpenes in Artemisia annua L. based on HPLC-DAD quantification and LC-ESI-QTOF-MS/MS confirmation. Food Chem. 2020, 312, 126070. [Google Scholar] [CrossRef]
- Freitas, J.R.L.E.; Vendramini, P.H.; Melo, J.O.F.; Eberlin, M.N.; Augusti, R. Assessing the spatial distribution of key flavonoids in Mentha × Piperita leaves: An application of desorption electrospray ionization mass spectrometry imaging (DESI-MSI). J. Braz. Chem. Soc. 2019, 30, 1437–1446. [Google Scholar] [CrossRef]
- Liao, Y.; Fu, X.; Zhou, H.; Rao, W.; Zeng, L.; Yang, Z. Visualized analysis of within-tissue spatial distribution of specialized metabolites in tea (Camellia sinensis) using desorption electrospray ionization imaging mass spectrometry. Food Chem. 2019, 292, 204–210. [Google Scholar] [CrossRef]
- Yamamoto, K.; Takahashi, K.; Mizuno, H.; Anegawa, A.; Ishizak, K.; Fukaki, H.; Ohnishi, M.; Yamazaki, M.; Masujima, T.; Mimura, T. Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with imaging MS and single-cell MS. Proc. Natl. Acad. Sci. USA 2016, 113, 3891–3896. [Google Scholar] [CrossRef] [Green Version]
- Dutkiewicz, E.P.; Su, C.-H.; Lee, H.-J.; Hsu, C.-C.; Yang, Y.-L. Visualizing vinca alkaloids in the petal of Catharanthus roseus using functionalized titanium oxide nanowire substrate for surface-assisted laser desorption/ionization imaging mass spectrometry. Plant J. 2021, 105, 1123–1133. [Google Scholar] [CrossRef]
- Huo, Y.; Liu, K.; Lou, X. Strong additive and synergistic effects of polyoxyethylene nonionic surfactant-assisted protein MALDI imaging mass spectrometry. Talanta 2021, 222, 121524. [Google Scholar] [CrossRef]
- Zhan, L.; Huang, X.; Xue, J.; Liu, H.; Xiong, C.; Wang, J.; Nie, Z. MALDI-TOF/TOF tandem mass spectrometry imaging reveals non-uniform distribution of disaccharide isomers in plant tissues. Food Chem. 2021, 338, 127984. [Google Scholar] [CrossRef]
- Kumara, P.M.; Shaanker, R.U.; Pradeep, T. UPLC and ESI-MS analysis of metabolites of Rauvolfia tetraphylla L. and their spatial localization using desorption electrospray ionization (DESI) mass spectrometric imaging. Phytochemistry 2019, 159, 20–29. [Google Scholar] [CrossRef] [PubMed]
- Hemalatha, R.G.; Pradeep, T. Understanding the molecular signatures in leaves and flowers by desorption electrospray ionization mass spectrometry (DESI MS) imaging. J. Agric. Food Chem. 2013, 61, 7477–7487. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.C.; Lin, L.; Cheng, P.; Sun, Z.L.; Wu, Y.; Liu, Z.Y. Fingerprint analysis of Gelsemium elegans by HPLC followed by the targeted identification of chemical constituents using HPLC coupled with quadrupole-time-of-flight mass spectrometry. Fitoterapia 2017, 121, 94–105. [Google Scholar] [CrossRef] [PubMed]
- Zuo, M.T.; Liu, Y.C.; Sun, Z.L.; Li, L.; Tang, Q.; Cheng, P.; Liu, Z.Y. An integrated strategy toward comprehensive characterization and quantification of multiple components from herbal medicine: An application study in Gelsemium elegans. Chin. Herb. Med. 2020, 13, 17–32. [Google Scholar] [CrossRef]
Tissue | Alkaloids | Area Percentages (AP, %) | ||
---|---|---|---|---|
>1400 | 700–1400 | <700 | ||
Root | Gelsemine | 49.0 ± 1.4 | 34.0 ± 2.5 | 17.0 ± 0.4 |
Koumine | 62.4 ± 0.6 | 21.1 ± 1.9 | 16.5 ± 1.2 | |
Gelsenicine | 0.0 | 3.9 ± 1.8 | 96.1 ± 1.8 | |
Stem | Gelsemine | 61.0 ± 2.0 | 23.5 ± 3.1 | 15.5 ± 0.5 |
Koumine | 100 | 0.0 | 0.0 | |
Gelsenicine | 100 | 0.0 | 0.0 | |
Leaf | Gelsemine | 4.9 ± 1.2 | 2.9 ± 3.1 | 92.2 ± 0.8 |
Koumine | 78.9 ± 0.2 | 17.1 ± 2.1 | 10.5 ± 1.9 | |
Gelsenicine | 72.4 ± 2.2 | 16.8 ± 0.1 | 4.30 ± 1.0 |
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Wu, Z.-H.; Su, Y.; Luo, Z.-F.; Sun, Z.-L.; Gong, Z.-H.; Xiao, L.-T. In Situ Visual Distribution of Gelsemine, Koumine, and Gelsenicine by MSI in Gelsemiumelegans at Different Growth Stages. Molecules 2022, 27, 1810. https://doi.org/10.3390/molecules27061810
Wu Z-H, Su Y, Luo Z-F, Sun Z-L, Gong Z-H, Xiao L-T. In Situ Visual Distribution of Gelsemine, Koumine, and Gelsenicine by MSI in Gelsemiumelegans at Different Growth Stages. Molecules. 2022; 27(6):1810. https://doi.org/10.3390/molecules27061810
Chicago/Turabian StyleWu, Zi-Han, Yi Su, Zhou-Fei Luo, Zhi-Liang Sun, Zhi-Hong Gong, and Lang-Tao Xiao. 2022. "In Situ Visual Distribution of Gelsemine, Koumine, and Gelsenicine by MSI in Gelsemiumelegans at Different Growth Stages" Molecules 27, no. 6: 1810. https://doi.org/10.3390/molecules27061810
APA StyleWu, Z.-H., Su, Y., Luo, Z.-F., Sun, Z.-L., Gong, Z.-H., & Xiao, L.-T. (2022). In Situ Visual Distribution of Gelsemine, Koumine, and Gelsenicine by MSI in Gelsemiumelegans at Different Growth Stages. Molecules, 27(6), 1810. https://doi.org/10.3390/molecules27061810