Nano-structural analysis of engrafted human induced pluripotent stem cell-derived cardiomyocytes in mouse hearts using a genetic-probe APEX2

Biochemical and Biophysical Research Communications

Volumn 505, Issue 4, 2018, Pages 1251-1256

  Hatani, Takeshi ^a,b   Funakoshi, Shunsuke ^b   Deerinck, Thomas J ^c   Bushong, Eric A ^c   Kimura, Takeshi ^a   Takeshima, Hiroshi ^a   Ellisman, Mark H ^c   Hoshijima, Masahiko ^c   Yoshida, Yoshinori ^b  

^a KYOTO UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

APEX2; Cardiac cell transplantation; Electron microscopy; iPSC derived cardiomyocytes; Regeneration therapy

Indexed keywords

ACUTE HEART INFARCTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APEX2; ARTICLE; CARDIAC MUSCLE CELL; CELL DIFFERENTIATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXCITATION CONTRACTION COUPLING; FEASIBILITY STUDY; GENE PROBE; HEART TRANSPLANTATION; HUMAN; HUMAN CELL; IN VIVO STUDY; INDUCED PLURIPOTENT STEM CELL; INDUCED PLURIPOTENT STEM CELL DERIVED CARDIOMYOCYTE; MALE; MICROSCOPY; MOUSE; NANOANALYSIS; NONHUMAN; PRIORITY JOURNAL; SARCOMERE; SCANNING ELECTRON MICROSCOPY; STEM CELL TRANSPLANTATION; TRANSMISSION ELECTRON MICROSCOPY; X RAY MICROSCOPIC TOMOGRAPHY; ANATOMY AND HISTOLOGY; ANIMAL; CARDIAC MUSCLE; CELL LINE; CELL LINEAGE; CYTOLOGY; GENETICS; HEART; HEART INFARCTION; MOLECULAR PROBE; PATHOLOGY; TRANSPLANTATION; ULTRASTRUCTURE;

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; HEART; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MALE; MICE; MOLECULAR PROBES; MYOCARDIAL INFARCTION; MYOCARDIUM; MYOCYTES, CARDIAC;

EID: 85054769240     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2018.10.020     Document Type: Article

References (24)

1. Goldman, S.A., Stem and progenitor cell-based therapy of the central nervous system: hopes, hype, and wishful thinking. Cell stem cell 18 (2016), 174–188.
2. Mandai, M., Watanabe, A., Kurimoto, Y., Hirami, Y., Morinaga, C., Daimon, T., Fujihara, M., Akimaru, H., Sakai, N., Shibata, Y., Terada, M., Nomiya, Y., Tanishima, S., Nakamura, M., Kamao, H., Sugita, S., Onishi, A., Ito, T., Fujita, K., Kawamata, S., Go, M.J., Shinohara, C., Hata, K.I., Sawada, M., Yamamoto, M., Ohta, S., Ohara, Y., Yoshida, K., Kuwahara, J., Kitano, Y., Amano, N., Umekage, M., Kitaoka, F., Tanaka, A., Okada, C., Takasu, N., Ogawa, S., Yamanaka, S., Takahashi, M., Autologous induced stem-cell-derived retinal cells for macular degeneration. N. Engl. J. Med. 376 (2017), 1038–1046.
3. Chong, J.J., Yang, X., Don, C.W., Minami, E., Liu, Y.W., Weyers, J.J., Mahoney, W.M., Van Biber, B., Cook, S.M., Palpant, N.J., Gantz, J.A., Fugate, J.A., Muskheli, V., Gough, G.M., Vogel, K.W., Astley, C.A., Hotchkiss, C.E., Baldessari, A., Pabon, L., Reinecke, H., Gill, E.A., Nelson, V., Kiem, H.P., Laflamme, M.A., Murry, C.E., Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts. Nature 510 (2014), 273–277.
4. Funakoshi, S., Miki, K., Takaki, T., Okubo, C., Hatani, T., Chonabayashi, K., Nishikawa, M., Takei, I., Oishi, A., Narita, M., Hoshijima, M., Kimura, T., Yamanaka, S., Yoshida, Y., Enhanced engraftment, proliferation, and therapeutic potential in heart using optimized human iPSC-derived cardiomyocytes. Sci. Rep., 6, 2016, 19111.
5. Shiba, Y., Gomibuchi, T., Seto, T., Wada, Y., Ichimura, H., Tanaka, Y., Ogasawara, T., Okada, K., Shiba, N., Sakamoto, K., Ido, D., Shiina, T., Ohkura, M., Nakai, J., Uno, N., Kazuki, Y., Oshimura, M., Minami, I., Ikeda, U., Allogeneic transplantation of iPS cell-derived cardiomyocytes regenerates primate hearts. Nature 538 (2016), 388–391.
6. Liu, Y.W., Chen, B., Yang, X., Fugate, J.A., Kalucki, F.A., Futakuchi-Tsuchida, A., Couture, L., Vogel, K.W., Astley, C.A., Baldessari, A., Ogle, J., Don, C.W., Steinberg, Z.L., Seslar, S.P., Tuck, S.A., Tsuchida, H., Naumova, A.V., Dupras, S.K., Lyu, M.S., Lee, J., Hailey, D.W., Reinecke, H., Pabon, L., Fryer, B.H., MacLellan, W.R., Thies, R.S., Murry, C.E., Human embryonic stem cell-derived cardiomyocytes restore function in infarcted hearts of non-human primates. Nat. Biotechnol. 36 (2018), 597–605.
7. Bers, D.M., Cardiac excitation-contraction coupling. Nature 415 (2002), 198–205.
8. Pinali, C., Kitmitto, A., Serial block face scanning electron microscopy for the study of cardiac muscle ultrastructure at nanoscale resolutions. J. Mol. Cell. Cardiol. 76 (2014), 1–11.
9. Das, T., Hoshijima, M., Adding a new dimension to cardiac nano-architecture using electron microscopy: coupling membrane excitation to calcium signaling. J. Mol. Cell. Cardiol. 58 (2013), 5–12.
10. Martell, J.D., Deerinck, T.J., Sancak, Y., Poulos, T.L., Mootha, V.K., Sosinsky, G.E., Ellisman, M.H., Ting, A.Y., Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30 (2012), 1143–1148.
11. Lam, S.S., Martell, J.D., Kamer, K.J., Deerinck, T.J., Ellisman, M.H., Mootha, V.K., Ting, A.Y., Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 12 (2015), 51–54.
12. Sastri, M., Darshi, M., Mackey, M., Ramachandra, R., Ju, S., Phan, S., Adams, S., Stein, K., Douglas, C.R., Kim, J.J., Ellisman, M.H., Taylor, S.S., Perkins, G.A., Sub-mitochondrial localization of the genetic-tagged mitochondrial intermembrane space-bridging components Mic19, Mic60 and Sam50. J. Cell Sci. 130 (2017), 3248–3260.
13. Ohnuki, M., Takahashi, K., Yamanaka, S., Generation and Characterization of Human Induced Pluripotent Stem Cells, Current Protocols in Stem Cell Biology, Chapter 4. 2009 Unit 4A 2.
14. Yang, L., Soonpaa, M.H., Adler, E.D., Roepke, T.K., Kattman, S.J., Kennedy, M., Henckaerts, E., Bonham, K., Abbott, G.W., Linden, R.M., Field, L.J., Keller, G.M., Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population. Nature 453 (2008), 524–528.
15. Miki, K., Endo, K., Takahashi, S., Funakoshi, S., Takei, I., Katayama, S., Toyoda, T., Kotaka, M., Takaki, T., Umeda, M., Okubo, C., Nishikawa, M., Oishi, A., Narita, M., Miyashita, I., Asano, K., Hayashi, K., Osafune, K., Yamanaka, S., Saito, H., Yoshida, Y., Efficient detection and purification of cell populations using synthetic MicroRNA switches. Cell stem cell 16 (2015), 699–711.
16. Hatani, T., Miki, K., Yoshida, Y., Induction of human induced pluripotent stem cells to cardiomyocytes using embryoid bodies. Methods Mol. Biol. 1816 (2018), 79–92.
17. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K., Sasai, Y., Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell stem cell 3 (2008), 519–532.
18. Morizane, A., Doi, D., Takahashi, J., Neural induction with a dopaminergic phenotype from human pluripotent stem cells through a feeder-free floating aggregation culture. Methods Mol. Biol. 1018 (2013), 11–19.
19. Kondo, T., Asai, M., Tsukita, K., Kutoku, Y., Ohsawa, Y., Sunada, Y., Imamura, K., Egawa, N., Yahata, N., Okita, K., Takahashi, K., Asaka, I., Aoi, T., Watanabe, A., Watanabe, K., Kadoya, C., Nakano, R., Watanabe, D., Maruyama, K., Hori, O., Hibino, S., Choshi, T., Nakahata, T., Hioki, H., Kaneko, T., Naitoh, M., Yoshikawa, K., Yamawaki, S., Suzuki, S., Hata, R., Ueno, S., Seki, T., Kobayashi, K., Toda, T., Murakami, K., Irie, K., Klein, W.L., Mori, H., Asada, T., Takahashi, R., Iwata, N., Yamanaka, S., Inoue, H., Modeling Alzheimer's disease with iPSCs reveals stress phenotypes associated with intracellular Abeta and differential drug responsiveness. Cell stem cell 12 (2013), 487–496.
20. Nishizawa, M., Chonabayashi, K., Nomura, M., Tanaka, A., Nakamura, M., Inagaki, A., Nishikawa, M., Takei, I., Oishi, A., Tanabe, K., Ohnuki, M., Yokota, H., Koyanagi-Aoi, M., Okita, K., Watanabe, A., Takaori-Kondo, A., Yamanaka, S., Yoshida, Y., Epigenetic variation between human induced pluripotent stem cell lines is an indicator of differentiation capacity. Cell stem cell 19 (2016), 341–354.
21. Hayashi, T., Martone, M.E., Yu, Z., Thor, A., Doi, M., Holst, M.J., Ellisman, M.H., Hoshijima, M., Three-dimensional electron microscopy reveals new details of membrane systems for Ca2+ signaling in the heart. J. Cell Sci. 122 (2009), 1005–1013.
22. Wong, J., Baddeley, D., Bushong, E.A., Yu, Z., Ellisman, M.H., Hoshijima, M., Soeller, C., Nanoscale distribution of ryanodine receptors and caveolin-3 in mouse ventricular myocytes: dilation of t-tubules near junctions. Biophys. J. 104 (2013), L22–L24.
23. van Berlo, J.H., Molkentin, J.D., An emerging consensus on cardiac regeneration. Nat. Med. 20 (2014), 1386–1393.
24. Barcena, M., Koster, A.J., Electron tomography in life science. Semin. Cell Dev. Biol. 20 (2009), 920–930.