5.9
CiteScore
5.9
Impact Factor
Volume 50 Issue 9
Sep.  2023
Turn off MathJax
Article Contents

Laser capture microdissection for biomedical research: towards high-throughput, multi-omics, and single-cell resolution

doi: 10.1016/j.jgg.2023.07.011 cstr: 32370.14.j.jgg.2023.07.011
Funds:

This work was supported by the National Natural Science Foundation of China (81973701 and 82204772), the Natural Science Foundation of Zhejiang Province (LZ20H290002), the Innovation Team and Talents Cultivation Program of National Administration of Traditional Chinese Medicine (ZYYCXTD-D-202002), the China Postdoctoral Science Foundation (2022M712811), and Westlake Laboratory (Westlake Laboratory of Life Sciences and Biomedicine).

  • Received Date: 2023-04-28
  • Accepted Date: 2023-07-28
  • Rev Recd Date: 2023-07-28
  • Publish Date: 2023-08-05
  • Spatial omics technologies have become powerful methods to provide valuable insights into cells and tissues within a complex context, significantly enhancing our understanding of the intricate and multifaceted biological system. With an increasing focus on spatial heterogeneity, there is a growing need for unbiased, spatially resolved omics technologies. Laser capture microdissection (LCM) is a cutting-edge method for acquiring spatial information that can quickly collect regions of interest (ROIs) from heterogeneous tissues, with resolutions ranging from single cells to cell populations. Thus, LCM has been widely used for studying the cellular and molecular mechanisms of diseases. This review focuses on the differences among four types of commonly used LCM technologies and their applications in omics and disease research. Key attributes of application cases are also highlighted, such as throughput and spatial resolution. In addition, we comprehensively discuss the existing challenges and the great potential of LCM in biomedical research, disease diagnosis, and targeted therapy from the perspective of high-throughput, multi-omics, and single-cell resolution.
  • loading
  • [1]
    Aaltonen, K.E., Ebbesson, A., Wigerup, C., Hedenfalk, I., 2011. Laser capture microdissection (LCM) and whole genome amplification (WGA) of DNA from normal breast tissue - optimization for genome wide array analyses. BMC Res. Notes 4, 69.
    [2]
    Audia, J.E., Campbell, R.M., 2016. Histone modifications and cancer. Cold Spring Harb. Perspect. Biol. 8, a019521.
    [3]
    Augustin, H.G., Koh, G.Y., 2017. Organotypic vasculature: from descriptive heterogeneity to functional pathophysiology. Science 357, eaal2379.
    [4]
    Bandyopadhyay, U., Fenton, W.A., Horwich, A.L., Nagy, M., 2014. Production of RNA for transcriptomic analysis from mouse spinal cord motor neuron cell bodies by laser capture microdissection. J. Vis. Exp., 83, e51168.
    [5]
    Bennett, M.R., Czech, K.A., Arend, L.J., Witte, D.P., Devarajan, P., Potter, S.S., 2007. Laser capture microdissection-microarray analysis of focal segmental glomerulosclerosis glomeruli. Nephron Exp. Nephrol. 107, e30-e40.
    [6]
    Beynon, R.J., 2005. The dynamics of the proteome: strategies for measuring protein turnover on a proteome-wide scale. Brief. Funct. Genom. Proteom. 3, 382-390.
    [7]
    Bian, Z., Gong, Y., Huang, T., Lee, C., Bian, L., Bai, Z., Shi, H., Zeng, Y., Liu, C., He, J., et al., 2020. Deciphering human macrophage development at single-cell resolution. Nature 582, 571-576.
    [8]
    Bichsel, C.A., Goss, J., Alomari, M., Alexandrescu, S., Robb, R., Smith, L.E., Hochman, M., Greene, A.K., Bischoff, J., 2019. Association of somatic GNAQ mutation with capillary malformations in a case of choroidal hemangioma. JAMA Ophthalmol. 137, 91-95.
    [9]
    Boisset, J.C., Vivie, J., Grun, D., Muraro, M.J., Lyubimova, A., van Oudenaarden, A., 2018. Mapping the physical network of cellular interactions. Nat. Methods 15, 547-553.
    [10]
    Boone, D.R., Weisz, H.A., Sell, S.L., Hellmich, H.L., 2018. Laser capture microdissection in traumatic brain injury research: obtaining hippocampal subregions and pools of injured neurons for genomic analyses. Methods Mol. Biol. 1723, 235-245.
    [11]
    Carter, B., Zhao, K., 2021. The epigenetic basis of cellular heterogeneity. Nat. Rev. Genet. 22, 235-250.
    [12]
    Casasent, A.K., Schalck, A., Gao, R., Sei, E., Long, A., Pangburn, W., Casasent, T., Meric-Bernstam, F., Edgerton, M.E., Navin, N.E., 2018. Multiclonal invasion in breast tumors identified by topographic single cell sequencing. Cell 172, 205-217.
    [13]
    Chen, A., Liao, S., Cheng, M., Ma, K., Wu, L., Lai, Y., Qiu, X., Yang, J., Xu, J., Hao, S., et al., 2022. Spatiotemporal transcriptomic atlas of mouse organogenesis using DNA nanoball-patterned arrays. Cell 185, 1777-1792.
    [14]
    Chen, J., Suo, S., Tam, P.P., Han, J.J., Peng, G., Jing, N., 2017. Spatial transcriptomic analysis of cryosectioned tissue samples with Geo-seq. Nat. Protoc. 12, 566-580.
    [15]
    Chen, K.H., Boettiger, A.N., Moffitt, J.R., Wang, S., Zhuang, X., 2015. RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348, aaa6090.
    [16]
    Chen, Z., Zhao, W., Ge, D., Han, Y., Ning, K., Luo, C., Wang, S., Liu, R., Zhang, X., Wang, Q., 2018. LCM-seq reveals the crucial role of LsSOC1 in heat-promoted bolting of lettuce (Lactuca sativa L.). Plant J. 95, 516-528.
    [17]
    Chiu, K.W., Nakano, T., Chen, K.D., Hu, T.H., Lin, C.C., Hsu, L.W., Chen, C.L., Goto, S., 2018. Identification of IL-28B genotype modification in hepatocytes after living donor liver transplantation by laser capture microdissection and pyrosequencing analysis. BioMed. Res. Int. 2018, 1826140.
    [18]
    Dawson, M.A., Kouzarides, T., 2012. Cancer epigenetics: from mechanism to therapy. Cell 150, 12-27.
    [19]
    Dilillo, M., Pellegrini, D., Ait-Belkacem, R., de Graaf, E.L., Caleo, M., Mcdonnell, L.A., 2017. Mass spectrometry imaging, laser capture microdissection, and LC-MS/MS of the same tissue section. J. Proteome Res. 16, 2993-3001.
    [20]
    Drummond, E., Nayak, S., Pires, G., Ueberheide, B., Wisniewski, T., 2018. Isolation of amyloid plaques and neurofibrillary tangles from archived Alzheimer's disease tissue using laser-capture microdissection for downstream proteomics. Methods Mol. Biol. 1723, 319-334.
    [21]
    Eltoum, I.A., Siegal, G.P., Frost, A.R., 2002. Microdissection of histologic sections: past, present, and future. Adv. Anat. Pathol. 9, 316-322.
    [22]
    Emmert-Buck, M.R., Bonner, R.F., Smith, P.D., Chuaqui, R.F., Zhuang, Z., Goldstein, S.R., Weiss, R.A., Liotta, L.A., 1996. Laser capture microdissection. Science 274, 998-1001.
    [23]
    Eraslan, G., Avsec, Z., Gagneur, J., Theis, F.J., 2019. Deep learning: new computational modelling techniques for genomics. Nat. Rev. Genet. 20, 389-403.
    [24]
    Esaki, H., Ewald, D.A., Ungar, B., Rozenblit, M., Zheng, X., Xu, H., Estrada, Y.D., Peng, X., Mitsui, H., Litman, T., et al., 2015. Identification of novel immune and barrier genes in atopic dermatitis by means of laser capture microdissection. J. Allergy Clin. Immunol. 135, 153-163.
    [25]
    Espina, V., Heiby, M., Pierobon, M.,Liotta, L.A., 2007. Laser capture microdissection technology. Expert Rev. Mol. Diagn. 7, 647-657.
    [26]
    Esposito, G., 2007. Complementary techniques: laser capture microdissection - increasing specificity of gene expression profiling of cancer specimens. Adv. Exp. Med. Biol. 593, 54-65.
    [27]
    Figlia, G., Willnow, P., Teleman, A.A., 2020. Metabolites regulate cell signaling and growth via covalent modification of proteins. Dev. Cell 54, 156-170.
    [28]
    Forsthoefel, D.J., Cejda, N.I., Khan, U.W., Newmark, P.A., 2020. Cell-type diversity and regionalized gene expression in the planarian intestine. eLife 9, e52613.
    [29]
    Fridland, S., Choi, J., Nam, M., Schellenberg, S.J., Kim, E., Lee, G., Yoon, N.,Chae, Y.K., 2021. Assessing tumor heterogeneity: integrating tissue and circulating tumor DNA (ctDNA) analysis in the era of immuno-oncology - blood TMB is not the same as tissue TMB. J. Immunother. Cancer 9, e002551.
    [30]
    Gonzaga-Jauregui, C., Lupski, J.R., Gibbs, R.A., 2012. Human genome sequencing in health and disease. Annu. Rev. Med. 63, 35-61.
    [31]
    Gordon, A., Gousset, K., 2021. Utilization of laser capture microdissection coupled to mass spectrometry to uncover the proteome of cellular protrusions. Methods Mol. Biol. 2259, 25-45.
    [32]
    Guillotin, D., Taylor, A.R., Plate, M., Mercer, P.F., Edwards, L.M., Haggart, R., Miele, G., Mcanulty, R.J., Maher, T.M., Hynds, R.E., et al., 2021. Transcriptome analysis of IPF fibroblastic foci identifies key pathways involved in fibrogenesis. Thorax 76, 73-82.
    [33]
    Hamze, M., Desmetz, C., Berthe, M.L., Roger, P., Boulle, N., Brancherau, P., Picard, E., Guzman, C., Tolza, C., Guglielmi, P., 2013. Characterization of resident B cells of vascular walls in human atherosclerotic patients. J. Immunol. 191, 3006-3016.
    [34]
    Haqqani, A.S., Nesic, M., Preston, E., Baumann, E., Kelly, J., Stanimirovic, D., 2005. Characterization of vascular protein expression patterns in cerebral ischemia/reperfusion using laser capture microdissection and ICAT-nanoLC-MS/MS. Faseb J. 19, 1809-1821.
    [35]
    Hardy, T., Zeybel, M., Day, C.P., Dipper, C., Masson, S., Mcpherson, S., Henderson, E., Tiniakos, D., White, S.,French, J., et al., 2017. Plasma DNA methylation: a potential biomarker for stratification of liver fibrosis in non-alcoholic fatty liver disease. Gut 66, 1321-1328.
    [36]
    Hashimoto, H., Vertino, P.M., Cheng, X., 2010. Molecular coupling of DNA methylation and histone methylation. Epigenomics 2, 657-669.
    [37]
    Hasin, Y., Seldin, M., Lusis, A., 2017. Multi-omics approaches to disease. Genome Biol. 18, 83.
    [38]
    Hoffmann, J., Wilhelm, J., Olschewski, A., Kwapiszewska, G., 2016. Microarray analysis in pulmonary hypertension. Eur. Resp. J. 48, 229-241.
    [39]
    Hogg, J.C., Mcdonough, J.E., Gosselink, J.V.,Hayashi, S., 2009. What drives the peripheral lung-remodeling process in chronic obstructive pulmonary disease? Proc. Am. Thorac. Soc. 6, 668-672.
    [40]
    Hong, M., Tao, S., Zhang, L., Diao, L.T., Huang, X., Huang, S., Xie, S.J., Xiao, Z.D., Zhang, H., 2020. RNA sequencing: new technologies and applications in cancer research. J. Hematol. Oncol. 13, 166.
    [41]
    Hsieh, P.P., Olsen, R.J., O'Malley, D.P., Konoplev, S.N., Hussong, J.W., Dunphy, C.H., Perkins, S.L., Cheng, L., Lin, P., Chang, C.C., 2007. The role of Janus Kinase 2 V617F mutation in extramedullary hematopoiesis of the spleen in neoplastic myeloid disorders. Mod. Pathol. 20, 929-935.
    [42]
    Huang, P., Kong, Q., Gao, W., Chu, B., Li, H., Mao, Y., Cai, Z., Xu, R., Tian, R., 2020. Spatial proteome profiling by immunohistochemistry-based laser capture microdissection and data-independent acquisition proteomics. Anal. Chim. Acta 1127, 140-148.
    [43]
    Husted, A.S., Trauelsen, M., Rudenko, O., Hjorth, S.A., Schwartz, T.W., 2017. GPCR-mediated signaling of metabolites. Cell Metab. 25, 777-796.
    [44]
    Iacomino, G., Aufiero, V.R., Marena, P., Venezia, A., Troncone, R., Auricchio, S., Mazzarella, G., 2018. Laser capture microdissection as a tool to study the mucosal immune response in celiac disease. Methods Mol. Biol. 1723, 139-154.
    [45]
    Irahara, N., Nosho, K., Baba, Y., Shima, K., Lindeman, N.I., Hazra, A., Schernhammer, E.S., Hunter, D.J., Fuchs, C.S.,Ogino, S., 2010. Precision of pyrosequencing assay to measure LINE-1 methylation in colon cancer, normal colonic mucosa, and peripheral blood cells. J. Mol. Diagn. 12, 177-183.
    [46]
    Kandathil, A.J., Graw, F., Quinn, J., Hwang, H.S., Torbenson, M., Perelson, A.S., Ray, S.C., Thomas, D.L., Ribeiro, R.M.,Balagopal, A., 2013. Use of laser capture microdissection to map hepatitis C virus-positive hepatocytes in human liver. Gastroenterology 145, 1404-1413.
    [47]
    Ke, R., Mignardi, M., Pacureanu, A., Svedlund, J., Botling, J., Wahlby, C.,Nilsson, M., 2013. In situ sequencing for RNA analysis in preserved tissue and cells. Nat. Methods 10, 857-860.
    [48]
    Khamis, A., Canouil, M., Siddiq, A., Crouch, H., Falchi, M., Bulow, M.V., Ehehalt, F., Marselli, L., Distler, M., Richter, D., et al., 2019. Laser capture microdissection of human pancreatic islets reveals novel eQTLs associated with type 2 diabetes. Mol. Metab. 24, 98-107.
    [49]
    Lappalainen, T., Scott, A.J., Brandt, M., Hall, I.M., 2019. Genomic analysis in the age of human genome sequencing. Cell 177, 70-84.
    [50]
    Lardone, M.C., Reyes, I.N., Ortiz, E., Piottante, A., Palma, C., Ebensperger, M., Castro, A., 2021. Testicular steroid sulfatase overexpression is associated with Leydig cell dysfunction in primary spermatogenic failure. Andrology 9, 657-664.
    [51]
    Leng, L., Ma, J., Zhang, P.P., Xu, S.C., Li, X., Jin, Y., Cai, J., Tang, R., Zhao, L., He, Z.C., et al., 2022. Spatial region-resolved proteome map reveals mechanism of COVID-19-associated heart injury. Cell Rep. 39, 110955.
    [52]
    Liao, J., Lu, X., Shao, X., Zhu, L., Fan, X., 2021. Uncovering an organ's molecular architecture at single-cell resolution by spatially resolved transcriptomics. Trends Biotechnol. 39, 43-58.
    [53]
    Liao, J., Qian, J., Fang, Y., Chen, Z., Zhuang, X., Zhang, N., Shao, X., Hu, Y., Yang, P., Cheng, J., et al., 2022. De novo analysis of bulk RNA-seq data at spatially resolved single-cell resolution. Nat. Commun. 13, 6498.
    [54]
    Lili, L.N., Matyunina, L.V., Walker, L.D., Benigno, B.B., Mcdonald, J.F., 2013. Molecular profiling predicts the existence of two functionally distinct classes of ovarian cancer stroma. BioMed Res. Int. 2013, 846387.
    [55]
    Liu, A., 2010. Laser capture microdissection in the tissue biorepository. J. Biomol. Tech. 21, 120-125.
    [56]
    Liu, J., Shen, C., Aguilera, N., Cukras, C., Hufnagel, R.B., Zein, W.M., Liu, T., Tam, J., 2021. Active cell appearance model induced generative adversarial networks for annotation-efficient cell segmentation and identification on adaptive optics retinal images. IEEE Trans. Med. Imaging 40, 2820-2831.
    [57]
    Lovendorf, M.B., Mitsui, H., Zibert, J.R., Ropke, M.A., Hafner, M., Dyring-Andersen, B., Bonefeld, C.M., Krueger, J.G., Skov, L., 2015. Laser capture microdissection followed by next-generation sequencing identifies disease-related microRNAs in psoriatic skin that reflect systemic microRNA changes in psoriasis. Exp. Dermatol. 24, 187-193.
    [58]
    Lubeck, E., Coskun, A.F., Zhiyentayev, T., Ahmad, M., Cai, L., 2014. Single-cell in situ RNA profiling by sequential hybridization. Nat. Methods 11, 360-361.
    [59]
    Madunic, K., Mayboroda, O.A., Zhang, T., Weber, J., Boons, G.J., Morreau, H., van Vlierberghe, R., van Wezel, T., Lageveen-Kammeijer, G., Wuhrer, M., 2022. Specific (sialyl-)Lewis core 2 O-glycans differentiate colorectal cancer from healthy colon epithelium. Theranostics 12, 4498-4512.
    [60]
    Marcus, R., Maitra, A., Roszik, J., 2017. Recent advances in genomic profiling of adenosquamous carcinoma of the pancreas. J. Pathol. 243, 271-272.
    [61]
    Margolin, D.H., Saunders, E.H., Bronfin, B., de Rosa, N., Axthelm, M.K., Goloubeva, O.G., Eapen, S., Gelman, R.S., Letvin, N.L., 2006. Germinal center function in the spleen during simian HIV infection in rhesus monkeys. J. Immunol. 177, 1108-1119.
    [62]
    Mcdaniel, K., Meng, F., Wu, N., Sato, K., Venter, J., Bernuzzi, F., Invernizzi, P., Zhou, T., Kyritsi, K.,Wan, Y., et al., 2017. Forkhead box A2 regulates biliary heterogeneity and senescence during cholestatic liver injury in micedouble dagger. Hepatology 65, 544-559.
    [63]
    Merienne, N., Meunier, C., Schneider, A., Seguin, J., Nair, S.S., Rocher, A.B., Le Gras, S., Keime, C., Faull, R., Pellerin, L., et al., 2019. Cell-type-specific gene expression profiling in adult mouse brain reveals normal and disease-state signatures. Cell Rep. 26, 2477-2493.
    [64]
    Monajembashi, S., Cremer, C., Cremer, T., Wolfrum, J., Greulich, K.O., 1986. Microdissection of human chromosomes by a laser microbeam. Exp. Cell Res. 167, 262-265.
    [65]
    Moor, A.E., Harnik, Y., Ben-Moshe, S., Massasa, E.E., Rozenberg, M., Eilam, R., Bahar, H.K., Itzkovitz, S., 2018. Spatial reconstruction of single enterocytes uncovers broad zonation along the intestinal villus axis. Cell 175, 1156-1167.
    [66]
    Murphy, S.J., Cheville, J.C., Zarei, S., Johnson, S.H., Sikkink, R.A., Kosari, F., Feldman, A.L., Eckloff, B.W., Karnes, R.J., Vasmatzis, G., 2012. Mate pair sequencing of whole-genome-amplified DNA following laser capture microdissection of prostate cancer. DNA Res. 19, 395-406.
    [67]
    Nichterwitz, S., Chen, G., Aguila, B.J., Yilmaz, M., Storvall, H., Cao, M., Sandberg, R., Deng, Q.,Hedlund, E., 2016. Laser capture microscopy coupled with Smart-seq2 for precise spatial transcriptomic profiling. Nat. Commun. 7, 12139.
    [68]
    Noborn, F., Thomsen, C., Vorontsov, E., Bobbio, E., Sihlbom, C., Nilsson, J., Polte, C.L., Bollano, E., Vukusic, K., Sandstedt, J., et al., 2022. Subtyping of cardiac amyloidosis by mass spectrometry-based proteomics of endomyocardial biopsies. Amyloid. 30, 96-108.
    [69]
    Olivier, M., Asmis, R., Hawkins, G.A., Howard, T.D., Cox, L.A., 2019. The need for multi-omics biomarker signatures in precision medicine. Int. J. Mol. Sci. 20, 4781.
    [70]
    O'Sullivan, S.J., Reyes, B., Vadigepalli, R., Van Bockstaele, E.J., Schwaber, J.S., 2020. Combining laser capture microdissection and microfluidic qPCR to analyze transcriptional profiles of single cells: a systems biology approach to opioid dependence. J. Vis. Exp. 157, 10.3791/60612.
    [71]
    Ouadah, Y., Rojas, E.R., Riordan, D.P., Capostagno, S., Kuo, C.S., Krasnow, M.A., 2019. Rare pulmonary neuroendocrine cells are stem cells regulated by Rb, p53, and notch. Cell 179, 403-416.e23.
    [72]
    Pellegrini, D., Del, G.A., Angella, L., Giordano, N., Dilillo, M., Tonazzini, I., Caleo, M., Cecchini, M., Mcdonnell, L.A., 2019. Quantitative microproteomics based characterization of the central and peripheral nervous system of a mouse model of Krabbe disease. Mol. Cell. Proteom. 18, 1227-1241.
    [73]
    Peng, G., Suo, S., Chen, J., Chen, W., Liu, C., Yu, F., Wang, R., Chen, S., Sun, N., Cui, G., et al., 2016. Spatial transcriptome for the molecular annotation of lineage fates and cell identity in mid-gastrula mouse embryo. Dev. Cell 36, 681-697.
    [74]
    Rawat, M., Nighot, M., Al-Sadi, R., Gupta, Y., Viszwapriya, D., Yochum, G., Koltun, W., Ma, T.Y., 2020. IL1B increases intestinal tight junction permeability by up-regulation of MIR200C-3p, which degrades occludin mRNA. Gastroenterology 159, 1375-1389.
    [75]
    Riva, A., Kuzyk, O., Forsberg, E., Siuzdak, G., Pfann, C., Herbold, C., Daims, H., Loy, A., Warth, B., Berry, D., 2019. A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome. Nat. Commun. 10, 4366.
    [76]
    Rodriques, S.G., Stickels, R.R., Goeva, A., Martin, C.A., Murray, E., Vanderburg, C.R., Welch, J., Chen, L.M., Chen, F., Macosko, E.Z., 2019. Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 363, 1463-1467.
    [77]
    Rosti, V., Villani, L., Riboni, R., Poletto, V., Bonetti, E., Tozzi, L., Bergamaschi, G., Catarsi, P., Dallera, E.,Novara, F., et al., 2013. Spleen endothelial cells from patients with myelofibrosis harbor the JAK2V617F mutation. Blood 121, 360-368.
    [78]
    Saksena, N., Bonam, S.R., Miranda-Saksena, M., 2021. Epigenetic lens to visualize the severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) infection in COVID-19 pandemic. Front. Genet. 12, 581726.
    [79]
    Schaff, D.L., Singh, S., Kim, K.B., Sutcliffe, M.D., Park, K.S., Janes, K.A., 2021. Fragmentation of small-cell lung cancer regulatory states in heterotypic microenvironments. Cancer Res. 81, 1853-1867.
    [80]
    Schlotter, F., Halu, A., Goto, S., Blaser, M.C., Body, S.C., Lee, L.H., Higashi, H., Delaughter, D.M., Hutcheson, J.D.,Vyas, P., et al., 2018. Spatiotemporal multi-omics mapping generates a molecular atlas of the aortic valve and reveals networks driving disease. Circulation 138, 377-393.
    [81]
    Scifo, E., Calza, G., Fuhrmann, M., Soliymani, R., Baumann, M., Lalowski, M., 2017. Recent advances in applying mass spectrometry and systems biology to determine brain dynamics. Expert Rev. Proteom. 14, 545-559.
    [82]
    Sethi, S., Madden, B., Debiec, H., Morelle, J., Charlesworth, M.C., Gross, L., Negron, V., Buob, D., Chaudhry, S., Jadoul, M., et al., 2021. Protocadherin 7-associated membranous nephropathy. J. Am. Soc. Nephrol. 32, 1249-1261.
    [83]
    Sethi, S., Vrana, J.A., Theis, J.D., Leung, N., Sethi, A., Nasr, S.H., Fervenza, F.C., Cornell, L.D., Fidler, M.E.,Dogan, A., 2012. Laser microdissection and mass spectrometry-based proteomics aids the diagnosis and typing of renal amyloidosis. Kidney Int. 82, 226-234.
    [84]
    Shao, X., Liao, J., Li, C., Lu, X., Cheng, J., Fan, X., 2021. CellTalkDB: a manually curated database of ligand-receptor interactions in humans and mice. Brief. Bioinform. 22, bbaa269.
    [85]
    Shen, S., Li, J., Huo, S., Ma, M., Zhu, X., Rasam, S., Duan, X., Qu, M., Titus, M.A., Qu, J., 2021. Parallel, high-quality proteomic and targeted metabolomic quantification using laser capture microdissected tissues. Anal. Chem. 93, 8711-8718.
    [86]
    Shendure, J., Findlay, G.M., Snyder, M.W., 2019. Genomic medicine-progress, pitfalls, and promise. Cell 177, 45-57.
    [87]
    Singh, S., Sutcliffe, M.D., Repich, K., Atkins, K.A., Harvey, J.A., Janes, K.A., 2021. Pan-cancer drivers are recurrent transcriptional regulatory heterogeneities in early-stage luminal breast cancer. Cancer Res. 81, 1840-1852.
    [88]
    Stahl, P.L., Salmen, F., Vickovic, S., Lundmark, A., Navarro, J.F., Magnusson, J., Giacomello, S., Asp, M., Westholm, J.O., Huss, M., et al., 2016. Visualization and analysis of gene expression in tissue sections by spatial transcriptomics. Science 353, 78-82.
    [89]
    Sutherland, C., Wang, Y., Brown, R.V., Foley, J., Mahler, B., Janardhan, K.S., Kovi, R.C.,Jetten, A.M., 2018. Laser capture microdissection of highly pure trabecular meshwork from mouse eyes for gene expression analysis. J. Vis. Exp. 136, 57576.
    [90]
    Tanaka, F., Niwa, J., Ishigaki, S., Katsuno, M., Waza, M., Yamamoto, M., Doyu, M., Sobue, G., 2006. Gene expression profiling toward understanding of ALS pathogenesis. Ann. N.Y. Acad. Sci. 1086, 1-10.
    [91]
    Thennavan, A., Sharma, M., Chandrashekar, C., Hunter, K., Radhakrishnan, R., 2017. Exploring the potential of laser capture microdissection technology in integrated oral biosciences. Oral Dis. 23, 737-748.
    [92]
    Tian, Y., Di Y, Zhang, J., Chen, X., Feng, T., Adu-Nti, F., Shi, M., Fan, J., Zhang, J., Zhang, P., et al., 2019. Angiogenic gene profiles in laser-microdissected microvessels and neurons from ischemic penumbra of rat brain. J. Mol. Neurosci. 67, 643-653.
    [93]
    Timp, W., Timp, G., 2020. Beyond mass spectrometry, the next step in proteomics. Sci. Adv. 6, eaax8978.
    [94]
    Vieujean, S., Hu, S., Bequet, E., Salee, C., Massot, C., Bletard, N., Pierre, N., Quesada, C.F., Baiwir, D., Mazzucchelli, G., et al., 2021. Potential role of epithelial endoplasmic reticulum stress and anterior gradient protein 2 homologue in Crohn's disease fibrosis. J. Crohns Colitis 15, 1737-1750.
    [95]
    Wang, X., Allen, W.E., Wright, M.A., Sylwestrak, E.L., Samusik, N., Vesuna, S., Evans, K., Liu, C., Ramakrishnan, C., Liu, J., et al., 2018. Three-dimensional intact-tissue sequencing of single-cell transcriptional states. Science 361, eaat5691.
    [96]
    Wasserkort, R., Kalmar, A., Valcz, G., Spisak, S., Krispin, M., Toth, K., Tulassay, Z., Sledziewski, A.Z., Molnar, B., 2013. Aberrant septin 9 DNA methylation in colorectal cancer is restricted to a single CpG island. BMC Cancer 13, 398.
    [97]
    Wigger, L., Barovic, M., Brunner, A.D., Marzetta, F., Schoniger, E., Mehl, F., Kipke, N., Friedland, D., Burdet, F., Kessler, C., et al., 2021. Multi-omics profiling of living human pancreatic islet donors reveals heterogeneous beta cell trajectories towards type 2 diabetes. Nat. Metab. 3, 1017-1031.
    [98]
    Xu, C., Houck, J.R., Fan, W., Wang, P., Chen, Y., Upton, M., Futran, N.D., Schwartz, S.M., Zhao, L.P., Chen, C., et al., 2008. Simultaneous isolation of DNA and RNA from the same cell population obtained by laser capture microdissection for genome and transcriptome profiling. J. Mol. Diagn. 10, 129-134.
    [99]
    Yang, J., Wang, Z., Feng, J., Ai, Q., Li, L., He, Y., Li, H., Tang, X., Yu, J., 2015. Application of laser capture microdissection and 16S rRNA gene polymerase chain reaction in the analysis of bacteria colonizing the intestinal tissue of neonates with necrotizing enterocolitis. Pediatr. Infect. Dis. J. 34, e279-e289.
    [100]
    Zhang, L., Lanzoni, G., Battarra, M., Inverardi, L., Zhang, Q., 2017. Proteomic profiling of human islets collected from frozen pancreata using laser capture microdissection. J. Proteom. 150, 149-159.
    [101]
    Zhao, L., Wu, X., Zheng, J., Dong, D., 2021. DNA methylome profiling of circulating tumor cells in lung cancer at single base-pair resolution. Oncogene 40, 1884-1895.
    [102]
    Zhu, Z., Wang, W., Lin, F., Jordan, T., Li, G., Silverman, S., Qiu, S., Joy, A.A., Chen, C., Hockley, D.L., et al., 2021. Genome profiles of pathologist-defined cell clusters by multiregional LCM and G&T-seq in one triple-negative breast cancer patient. Cell Rep. Med. 2, 100404.
    [103]
    Zimmerman, M., Blanc, L., Chen, P.Y., Dartois, V., Prideaux, B., 2018. Spatial quantification of drugs in pulmonary tuberculosis lesions by laser capture microdissection liquid chromatography mass spectrometry (LCM-LC/MS). J. Vis. Exp. 134, 57402.
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (397) PDF downloads (28) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return