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Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent

Xueying Yang,  Shun He,  Xufeng Li,  Zhihou Guo,  Haichang Wang,  Zhuonan Zhang,  Xin Song,  Ke Jia,  Lingjuan He,  Bin Zhou

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文章导航 > Journal of Genetics and Genomics  > 2024 >  51(12): 1474-1484
Xueying Yang, Shun He, Xufeng Li, Zhihou Guo, Haichang Wang, Zhuonan Zhang, Xin Song, Ke Jia, Lingjuan He, Bin Zhou. Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent[J]. 遗传学报, 2024, 51(12): 1474-1484. doi: 10.1016/j.jgg.2024.07.006
引用本文: Xueying Yang, Shun He, Xufeng Li, Zhihou Guo, Haichang Wang, Zhuonan Zhang, Xin Song, Ke Jia, Lingjuan He, Bin Zhou. Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent[J]. 遗传学报, 2024, 51(12): 1474-1484. doi: 10.1016/j.jgg.2024.07.006
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Xueying Yang, Shun He, Xufeng Li, Zhihou Guo, Haichang Wang, Zhuonan Zhang, Xin Song, Ke Jia, Lingjuan He, Bin Zhou. Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent[J]. Journal of Genetics and Genomics, 2024, 51(12): 1474-1484. doi: 10.1016/j.jgg.2024.07.006
Citation: Xueying Yang, Shun He, Xufeng Li, Zhihou Guo, Haichang Wang, Zhuonan Zhang, Xin Song, Ke Jia, Lingjuan He, Bin Zhou. Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent[J]. Journal of Genetics and Genomics, 2024, 51(12): 1474-1484. doi: 10.1016/j.jgg.2024.07.006
shu

Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent

doi: 10.1016/j.jgg.2024.07.006

  • a. School of Life Science, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, Zhejiang 310024, China;

  • b. School of Life Sciences, Westlake University, Hangzhou, Zhejiang 310030, China;

  • c. New Cornerstone Science Laboratory, State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai 200031, China;

  • d. School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China

基金项目: 

This work was supported by the National Key Research & Development Program of China (2021YFA0805100, 2023YFA1800700, 2019YFA0110403, 2019YFA0802000), the National Science Foundation of China (82088101, 32370885, 92368103, 32370897), the Westlake Education Foundation, and the Benyuan Charity Fund, Research Funds of Hangzhou Institute for Advanced Study (2022ZZ01015 and B04006C01600515).

详细信息
    通讯作者:

    Lingjuan He,E-mail:helingjuan@westlake.edu.cn

    Bin Zhou,E-mail:zhoubin@sibs.ac.cn

Synchronized lineage tracing of cell membranes and nuclei by dual recombinases and dual fluorescent

  • a. School of Life Science, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, Zhejiang 310024, China;

  • b. School of Life Sciences, Westlake University, Hangzhou, Zhejiang 310030, China;

  • c. New Cornerstone Science Laboratory, State Key Laboratory of Cell Biology, Shanghai Institute of Biochemistry and Cell Biology, Center for Excellence in Molecular Cell Science, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Shanghai 200031, China;

  • d. School of Life Science and Technology, ShanghaiTech University, Shanghai 201210, China

Funds: 

This work was supported by the National Key Research & Development Program of China (2021YFA0805100, 2023YFA1800700, 2019YFA0110403, 2019YFA0802000), the National Science Foundation of China (82088101, 32370885, 92368103, 32370897), the Westlake Education Foundation, and the Benyuan Charity Fund, Research Funds of Hangzhou Institute for Advanced Study (2022ZZ01015 and B04006C01600515).

    摘要
  • 摘要:

    Genetic lineage tracing has been widely employed to investigate cell lineages and fate. However, conventional reporting systems often label the entire cytoplasm, making it challenging to discern cell boundaries. Additionally, single Cre-loxP recombination systems have limitations in tracing specific cell populations. This study proposes three reporting systems utilizing Cre, Dre, and Dre+Cre mediated recombination. These systems incorporate tdTomato expression on the cell membrane and PhiYFP expression within the nucleus, allowing for clear observation of the nucleus and membrane. The efficacy of these systems is successfully demonstrated by labeling cardiomyocytes and hepatocytes. The potential for dynamic visualization of the cell membrane is showcased using intravital imaging microscopy or three-dimensional imaging. Furthermore, by combining this dual recombinase system with the ProTracer system, hepatocyte proliferation is traced with enhanced precision. This reporting system holds significant importance for advancing the understanding of cell fate studies in development, homeostasis, and diseases.

    Abstract:

    Genetic lineage tracing has been widely employed to investigate cell lineages and fate. However, conventional reporting systems often label the entire cytoplasm, making it challenging to discern cell boundaries. Additionally, single Cre-loxP recombination systems have limitations in tracing specific cell populations. This study proposes three reporting systems utilizing Cre, Dre, and Dre+Cre mediated recombination. These systems incorporate tdTomato expression on the cell membrane and PhiYFP expression within the nucleus, allowing for clear observation of the nucleus and membrane. The efficacy of these systems is successfully demonstrated by labeling cardiomyocytes and hepatocytes. The potential for dynamic visualization of the cell membrane is showcased using intravital imaging microscopy or three-dimensional imaging. Furthermore, by combining this dual recombinase system with the ProTracer system, hepatocyte proliferation is traced with enhanced precision. This reporting system holds significant importance for advancing the understanding of cell fate studies in development, homeostasis, and diseases.

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    • 参考文献(43)
  • Aizarani, N., Saviano, A., Sagar, Mailly, L., Durand, S., Herman, J.S., Pessaux, P., Baumert, T.F., Grun, D., 2019. A human liver cell atlas reveals heterogeneity and epithelial progenitors. Nature 572, 199-204.
    Alexopoulou, A.N., Couchman, J.R., Whiteford, J.R., 2008. The CMV early enhancer/chicken beta actin (CAG) promoter can be used to drive transgene expression during the differentiation of murine embryonic stem cells into vascular progenitors. BMC Cell Biol. 9, 2.
    Anastassiadis, K., Fu, J., Patsch, C., Hu, S., Weidlich, S., Duerschke, K., Buchholz, F., Edenhofer, F., Stewart, A.F., 2009. Dre recombinase, like Cre, is a highly efficient site-specific recombinase in E. coli, mammalian cells and mice. Dis. Model Mech. 2, 508-515.
    Baker, A.H., Peault, B., 2016. A Gli(1)ttering role for perivascular stem cells in blood vessel remodeling. Cell Stem Cell 19, 563-565.
    Basak, O., Krieger, T.G., Muraro, M.J., Wiebrands, K., Stange, D.E., Frias-Aldeguer, J., Rivron, N.C., van de Wetering, M., van Es, J.H., van Oudenaarden, A., et al., 2018. Troy+ brain stem cells cycle through quiescence and regulate their number by sensing niche occupancy. Proc. Natl. Acad. Sci. U. S. A. 115, E610-E619.
    Ben-Zvi, A., Lacoste, B., Kur, E., Andreone, B.J., Mayshar, Y., Yan, H., Gu, C., 2014. Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature 509, 507-511.
    Bralet, M.P., Branchereau, S., Brechot, C., Ferry, N., 1994. Cell lineage study in the liver using retroviral mediated gene transfer. Evidence against the streaming of hepatocytes in normal liver. Am. J. Pathol. 144, 896-905.
    Chan, H.Y., V, S., Xing, X., Kraus, P., Yap, S.P., Ng, P., Lim, S.L., Lufkin, T., 2011. Comparison of IRES and F2A-based locus-specific multicistronic expression in stable mouse lines. PLoS One 6, e28885.
    Chen, F., Jimenez, R.J., Sharma, K., Luu, H.Y., Hsu, B.Y., Ravindranathan, A., Stohr, B.A., Willenbring, H., 2020. Broad distribution of hepatocyte proliferation in liver homeostasis and regeneration. Cell Stem Cell 26, 27-33.
    Davis, J., Maillet, M., Miano, J.M., Molkentin, J.D., 2012. Lost in transgenesis: a user's guide for genetically manipulating the mouse in cardiac research. Circ. Res. 111, 761-777.
    Han, X., Zhang, Z., He, L., Zhu, H., Li, Y., Pu, W., Han, M., Zhao, H., Liu, K., Li, Y., et al., 2021. A suite of new Dre recombinase drivers markedly expands the ability to perform intersectional genetic targeting. Cell Stem Cell 28, 1160-1176.
    He, L., Li, Y., Huang, X., Li, Y., Pu, W., Tian, X., Cai, D., Huang, H., Lui, K.O., Zhou, B., 2018. Genetic lineage tracing of resident stem cells by DeaLT. Nat. Protoc. 13, 2217-2246.
    He, L., Li, Y., Li, Y., Pu, W., Huang, X., Tian, X., Wang, Y., Zhang, H., Liu, Q., Zhang, L., et al., 2017. Enhancing the precision of genetic lineage tracing using dual recombinases. Nat. Med. 23, 1488-1498.
    He, L., Lui, K.O., Zhou, B., 2020. The formation of coronary vessels in cardiac development and disease. Cold Spring Harb. Perspect. Biol. 12, a037168.
    He, L., Pu, W., Liu, X., Zhang, Z., Han, M., Li, Y., Huang, X., Han, X., Li, Y., Liu, K., et al., 2021. Proliferation tracing reveals regional hepatocyte generation in liver homeostasis and repair. Science 371, eabc4346.
    Hermann, M., Stillhard, P., Wildner, H., Seruggia, D., Kapp, V., Sanchez-Iranzo, H., Mercader, N., Montoliu, L., Zeilhofer, H.U., et al., 2014. Binary recombinase systems for high-resolution conditional mutagenesis. Nucleic Acids Res. 42, 3894-3907.
    Kim, J.H., Lee, S.R., Li, L.H., Park, H.J., Park, J.H., Lee, K.Y., Kim, M.K., Shin, B.A., Choi, S.Y., 2011. High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS One 6, e18556.
    Kretzschmar, K., Post, Y., Bannier-Helaouet, M., Mattiotti, A., Drost, J., Basak, O., Li, V.S.W., van den Born, M., Gunst, Q.D., Versteeg, D., et al., 2018. Profiling proliferative cells and their progeny in damaged murine hearts. Proc. Natl. Acad. Sci. U. S. A. 115, E12245-E12254.
    Li, Y., He, L., Huang, X., Bhaloo, S.I., Zhao, H., Zhang, S., Pu, W., Tian, X., Li, Y., Liu, Q., et al., 2018. Genetic lineage tracing of nonmyocyte population by dual recombinases. Circulation 138, 793-805.
    Liu, H., Baliga, R., 2003. Cytochrome P450 2E1 null mice provide novel protection against cisplatin-induced nephrotoxicity and apoptosis. Kidney Int. 63, 1687-1696.
    Liu, K., Meng, X., Liu, Z., Tang, M., Lv, Z., Huang, X., Jin, H., Han, X., Liu, X., Pu, W., et al., 2024. Tracing the origin of alveolar stem cells in lung repair and regeneration. Cell 187, 2428-2445.
    Liu, K., Yu, W., Tang, M., Tang, J., Liu, X., Liu, Q., Li, Y., He, L., Zhang, L., Evans, S.M., et al., 2018. A dual genetic tracing system identifies diverse and dynamic origins of cardiac valve mesenchyme. Development 145, dev167775.
    Liu, Q., Liu, K., Cui, G., Huang, X., Yao, S., Guo, W., Qin, Z., Li, Y., Yang, R., Pu, W., et al., 2019. Lung regeneration by multipotent stem cells residing at the bronchioalveolar-duct junction. Nat. Genet. 51, 728-738.
    Liu, X., Pu, W., He, L., Li, Y., Zhao, H., Li, Y., Liu, K., Huang, X., Weng, W., Wang, Q.D., et al., 2021. Cell proliferation fate mapping reveals regional cardiomyocyte cell-cycle activity in subendocardial muscle of left ventricle. Nat. Commun. 12, 5784.
    Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R., et al., 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140.
    Martin, N.C., McCullough, C.T., Bush, P.G., Sharp, L., Hall, A.C., Harrison, D.J., 2002. Functional analysis of mouse hepatocytes differing in DNA content: volume, receptor expression, and effect of IFNgamma. J. Cell. Physiol. 191, 138-144.
    Miao, Z., Balzer, M.S., Ma, Z., Liu, H., Wu, J., Shrestha, R., Aranyi, T., Kwan, A., Kondo, A., Pontoglio, M., et al., 2021. Single cell regulatory landscape of the mouse kidney highlights cellular differentiation programs and disease targets. Nat. Commun. 12, 2277.
    Ni, Z., Deng, J., Potter, C.M.F., Nowak, W.N., Gu, W., Zhang, Z., Chen, T., Chen, Q., Hu, Y., Zhou, B., et al., 2019. Recipient c-Kit lineage cells repopulate smooth muscle cells of transplant arteriosclerosis in mouse models. Circ. Res. 125, 223-241.
    Pontes-Quero, S., Heredia, L., Casquero-Garcia, V., Fernandez-Chacon, M., Luo, W., Hermoso, A., Bansal, M., Garcia-Gonzalez, I., Sanchez-Munoz, M.S., Perea, J.R., et al., 2017. Dual ifgMosaic: a versatile method for multispectral and combinatorial mosaic gene-function analysis. Cell 170, 800-814.
    Pu, W., Zhang, H., Huang, X., Tian, X., He, L., Wang, Y., Zhang, L., Liu, Q., Li, Y., Li, Y., et al., 2016. Mfsd2a+ hepatocytes repopulate the liver during injury and regeneration. Nat. Commun. 7, 13369.
    Sauer, B., McDermott, J., 2004. DNA recombination with a heterospecific Cre homolog identified from comparison of the pac-c1 regions of P1-related phages. Nucleic Acids Res. 32, 6086-6095.
    Soriano, P., 1999. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
    Tang, J., Wang, H., Huang, X., Li, F., Zhu, H., Li, Y., He, L., Zhang, H., Pu, W., Liu, K., et al., 2020a. Arterial Sca1+ vascular stem cells generate de novo smooth muscle for artery repair and regeneration. Cell Stem Cell 26, 81-96.
    Tang, M., Liu, K., Jin, H., Li, Y., Zhang, S., Liu, X., Han, X., Han, M., Zhang, Z., Zhou, B., 2020b. Simultaneous quantitative assessment of two distinct cell lineages with a nuclear-localized dual genetic reporter. J. Mol. Cell. Cardiol. 146, 60-68.
    Tian, X., Pu, W.T., Zhou, B., 2015. Cellular origin and developmental program of coronary angiogenesis. Circ. Res. 116, 515-530.
    Torre, C., Perret, C., Colnot, S., 2011. Transcription dynamics in a physiological process: β-catenin signaling directs liver metabolic zonation. Int. J. Biochem. Cell Biol. 43, 271-278.
    Wang, L.L., Serrano, C., Zhong, X., Ma, S., Zou, Y., Zhang, C.L., 2021. Revisiting astrocyte to neuron conversion with lineage tracing in vivo. Cell 184, 5465-5481.
    Wang, Y., Huang, X., He, L., Pu, W., Li, Y., Liu, Q., Li, Y., Zhang, L., Yu, W., Zhao, H., et al., 2017. Genetic tracing of hepatocytes in liver homeostasis, injury, and regeneration. J. Biol. Chem. 292, 8594-8604.
    Wang, Z., Shah, S.V., Liu, H., Baliga, R., 2014. Inhibition of cytochrome P450 2E1 and activation of transcription factor Nrf2 are renoprotective in myoglobinuric acute kidney injury. Kidney Int. 86, 338-349.
    Wilkinson, P.D., Delgado, E.R., Alencastro, F., Leek, M.P., Roy, N., Weirich, M.P., Stahl, E.C., Otero, P.A., Chen, M.I., Brown, W.K., et al., 2019. The polyploid state restricts hepatocyte proliferation and liver regeneration in mice. Hepatology 69, 1242-1258.
    Yao, Z., Bai, L., Dou, K., Nie, Y., 2024. Identifying cardiomyocyte ploidy with nuclear area and volume. Circulation 149, 1540-1542.
    Zhang, H., Pu, W., Liu, Q., He, L., Huang, X., Tian, X., Zhang, L., Nie, Y., Hu, S., Lui, K.O., et al., 2016a. Endocardium contributes to cardiac fat. Circ. Res. 118, 254-265.
    Zhang, H., Pu, W., Tian, X., Huang, X., He, L., Liu, Q., Li, Y., Zhang, L., He, L., Liu, K., et al., 2016b. Genetic lineage tracing identifies endocardial origin of liver vasculature. Nat. Genet. 48, 537-543.
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出版历程
  • 收稿日期:  2024-05-03
  • 录用日期:  2024-07-05
  • 修回日期:  2024-07-03
  • 网络出版日期:  2025-06-05
  • 刊出日期:  2024-07-10

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