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Recording of cellular physiological histories along optically readable self-assembling protein chains

View ORCID ProfileChangyang Linghu, Bobae An, Monika Shpokayte, Orhan T. Celiker, Nava Shmoel, Chi Zhang, Won Min Park, Steve Ramirez, View ORCID ProfileEdward S. Boyden
doi: https://doi.org/10.1101/2021.10.13.464006
Changyang Linghu
1Brain and Cognitive Sciences, MIT, Cambridge, MA 02139
2Biological Engineering, MIT, Cambridge, MA 02139
3Media Arts and Sciences, MIT, Cambridge, MA 02139
4McGovern Institute, MIT, Cambridge, MA 02139
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  • ORCID record for Changyang Linghu
Bobae An
1Brain and Cognitive Sciences, MIT, Cambridge, MA 02139
2Biological Engineering, MIT, Cambridge, MA 02139
3Media Arts and Sciences, MIT, Cambridge, MA 02139
4McGovern Institute, MIT, Cambridge, MA 02139
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Monika Shpokayte
5Graduate Program for Neuroscience, Boston University, Boston, MA, 02215
6Psychological and Brain Sciences, Boston University, Boston, MA, 02215
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Orhan T. Celiker
1Brain and Cognitive Sciences, MIT, Cambridge, MA 02139
2Biological Engineering, MIT, Cambridge, MA 02139
3Media Arts and Sciences, MIT, Cambridge, MA 02139
4McGovern Institute, MIT, Cambridge, MA 02139
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Nava Shmoel
1Brain and Cognitive Sciences, MIT, Cambridge, MA 02139
2Biological Engineering, MIT, Cambridge, MA 02139
3Media Arts and Sciences, MIT, Cambridge, MA 02139
4McGovern Institute, MIT, Cambridge, MA 02139
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Chi Zhang
1Brain and Cognitive Sciences, MIT, Cambridge, MA 02139
2Biological Engineering, MIT, Cambridge, MA 02139
3Media Arts and Sciences, MIT, Cambridge, MA 02139
4McGovern Institute, MIT, Cambridge, MA 02139
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Won Min Park
7Chemical Engineering, Kansas State University, Manhattan, KS, 66506
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Steve Ramirez
6Psychological and Brain Sciences, Boston University, Boston, MA, 02215
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Edward S. Boyden
1Brain and Cognitive Sciences, MIT, Cambridge, MA 02139
2Biological Engineering, MIT, Cambridge, MA 02139
3Media Arts and Sciences, MIT, Cambridge, MA 02139
4McGovern Institute, MIT, Cambridge, MA 02139
8Howard Hughes Medical Institute, MIT, Cambridge, MA 02139
9K Lisa Yang Center for Bionics, MIT, Cambridge, MA 02139
10Center for Neurobiological Engineering, MIT, Cambridge, MA 02139
11Koch Institute, MIT, Cambridge, MA 02139
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  • ORCID record for Edward S. Boyden
  • For correspondence: edboyden@mit.edu
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Abstract

Observing cellular physiological histories is key to understanding normal and disease-related processes, but longitudinal imaging is laborious and equipment-intensive. A tantalizing possibility is that cells could record such histories in the form of digital biological information within themselves, for later high-throughput readout. Here we show that this concept can be realized through information storage in the form of growing protein chains made out of multiple self-assembling subunits bearing different labels, each corresponding to a different cellular state or function, so that the physiological history of the cell can be visually read out along the chain of proteins. Conveniently, such protein chains are fully genetically encoded, and easily readable with simple, conventional optical microscopy techniques, compatible with visualization of cellular shape and molecular content. We use such expression recording islands (XRIs) to record gene expression timecourse downstream of pharmacological and physiological stimuli, in cultured neurons and in living mouse brain.

Competing Interest Statement

C.L. and E.S.B. declare they applied for a US patent based on the work presented in this paper.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 13, 2021.
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Recording of cellular physiological histories along optically readable self-assembling protein chains
Changyang Linghu, Bobae An, Monika Shpokayte, Orhan T. Celiker, Nava Shmoel, Chi Zhang, Won Min Park, Steve Ramirez, Edward S. Boyden
bioRxiv 2021.10.13.464006; doi: https://doi.org/10.1101/2021.10.13.464006
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Recording of cellular physiological histories along optically readable self-assembling protein chains
Changyang Linghu, Bobae An, Monika Shpokayte, Orhan T. Celiker, Nava Shmoel, Chi Zhang, Won Min Park, Steve Ramirez, Edward S. Boyden
bioRxiv 2021.10.13.464006; doi: https://doi.org/10.1101/2021.10.13.464006

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