Integrated intracellular organization and its variations in human iPS cells

Viana, Matheus P.; Chen, Jianxu; Knijnenburg, Theo A.; Vasan, Ritvik; Yan, Calysta; Arakaki, Joy E.; Bailey, Matte; Berry, Ben; Borensztejn, Antoine; Brown, Eva M.; Carlson, Sara; Cass, Julie A.; Chaudhuri, Basudev; Metzler, Kimberly R. Cordes; Coston, Mackenzie E.; Crabtree, Zach J.; Davidson, Steve; DeLizo, Colette M.; Dhaka, Shailja; Dinh, Stephanie Q.; Do, Thao P.; Domingus, Justin; Donovan-Maiye, Rory M.; Ferrante, Alexandra J.; Foster, Tyler J.; Frick, Christopher L.; Fujioka, Griffin; Fuqua, Margaret A.; Gehring, Jamie L.; Gerbin, Kaytlyn A.; Grancharova, Tanya; Gregor, Benjamin W.; Harrylock, Lisa J.; Haupt, Amanda; Hendershott, Melissa C.; Hookway, Caroline; Horwitz, Alan R.; Hughes, H. Christopher; Isaac, Eric J.; Johnson, Gregory R.; Kim, Brian; Leonard, Andrew N.; Leung, Winnie W.; Lucas, Jordan J.; Ludmann, Susan A.; Lyons, Blair M.; Malik, Haseeb; McGregor, Ryan; Medrash, Gabe E.; Meharry, Sean L.; Mitcham, Kevin; Mueller, Irina A.; Murphy-Stevens, Timothy L.; Nath, Aditya; Nelson, Angelique M.; Oluoch, Sandra A.; Paleologu, Luana; Popiel, T. Alexander; Riel-Mehan, Megan M.; Roberts, Brock; Schaefbauer, Lisa M.; Schwarzl, Magdalena; Sherman, Jamie; Slaton, Sylvain; Sluzewski, M. Filip; Smith, Jacqueline E.; Sul, Youngmee; Swain-Bowden, Madison J.; Tang, W. Joyce; Thirstrup, Derek J.; Toloudis, Daniel M.; Tucker, Andrew P.; Valencia, Veronica; Wiegraebe, Winfried; Wijeratna, Thushara; Yang, Ruian; Zaunbrecher, Rebecca J.; Labitigan, Ramon Lorenzo D.; Sanborn, Adrian L.; Johnson, Graham T.; Gunawardane, Ruwanthi N.; Gaudreault, Nathalie; Theriot, Julie A.; Rafelski, Susanne M.

Integrated intracellular organization and its variations in human iPS cells

Matheus P. Viana, Jianxu Chen, Theo A. Knijnenburg, Ritvik Vasan, Calysta Yan, Joy E. Arakaki, Matte Bailey, Ben Berry, Antoine Borensztejn, Eva M. Brown, Sara Carlson, Julie A. Cass, Basudev Chaudhuri, Kimberly R. Cordes Metzler, Mackenzie E. Coston, Zach J. Crabtree, Steve Davidson, Colette M. DeLizo, Shailja Dhaka, Stephanie Q. Dinh, Thao P. Do, Justin Domingus, Rory M. Donovan-Maiye, Alexandra J. Ferrante, Tyler J. Foster, Christopher L. Frick, Griffin Fujioka, Margaret A. Fuqua, Jamie L. Gehring, Kaytlyn A. Gerbin, Tanya Grancharova, Benjamin W. Gregor, Lisa J. Harrylock, Amanda Haupt, Melissa C. Hendershott, Caroline Hookway, Alan R. Horwitz, H. Christopher Hughes, Eric J. Isaac, Gregory R. Johnson, Brian Kim, Andrew N. Leonard, Winnie W. Leung, Jordan J. Lucas, Susan A. Ludmann, Blair M. Lyons, Haseeb Malik, Ryan McGregor, Gabe E. Medrash, Sean L. Meharry, Kevin Mitcham, Irina A. Mueller, Timothy L. Murphy-Stevens, Aditya Nath, Angelique M. Nelson, Sandra A. Oluoch, Luana Paleologu, T. Alexander Popiel, Megan M. Riel-Mehan, Brock Roberts, Lisa M. Schaefbauer, Magdalena Schwarzl, Jamie Sherman, Sylvain Slaton, M. Filip Sluzewski, Jacqueline E. Smith, Youngmee Sul, Madison J. Swain-Bowden, W. Joyce Tang, Derek J. Thirstrup, Daniel M. Toloudis, Andrew P. Tucker, Veronica Valencia, Winfried Wiegraebe, Thushara Wijeratna, Ruian Yang, Rebecca J. Zaunbrecher, Ramon Lorenzo D. Labitigan, Adrian L. Sanborn, Graham T. Johnson, Ruwanthi N. Gunawardane, Nathalie Gaudreault, Julie A. Theriot and Susanne M. Rafelski ()
Additional contact information
Matheus P. Viana: Allen Institute for Cell Science
Jianxu Chen: Allen Institute for Cell Science
Theo A. Knijnenburg: Allen Institute for Cell Science
Ritvik Vasan: Allen Institute for Cell Science
Calysta Yan: Allen Institute for Cell Science
Joy E. Arakaki: Allen Institute for Cell Science
Matte Bailey: Allen Institute for Cell Science
Ben Berry: Allen Institute for Cell Science
Antoine Borensztejn: Allen Institute for Cell Science
Eva M. Brown: Allen Institute for Cell Science
Sara Carlson: Allen Institute for Cell Science
Julie A. Cass: Allen Institute for Cell Science
Basudev Chaudhuri: Allen Institute for Cell Science
Kimberly R. Cordes Metzler: Allen Institute for Cell Science
Mackenzie E. Coston: Allen Institute for Cell Science
Zach J. Crabtree: Allen Institute for Cell Science
Steve Davidson: Allen Institute for Cell Science
Colette M. DeLizo: Allen Institute for Cell Science
Shailja Dhaka: Allen Institute for Cell Science
Stephanie Q. Dinh: Allen Institute for Cell Science
Thao P. Do: Allen Institute for Cell Science
Justin Domingus: Allen Institute for Cell Science
Rory M. Donovan-Maiye: Allen Institute for Cell Science
Alexandra J. Ferrante: Allen Institute for Cell Science
Tyler J. Foster: Allen Institute for Cell Science
Christopher L. Frick: Allen Institute for Cell Science
Griffin Fujioka: Allen Institute for Cell Science
Margaret A. Fuqua: Allen Institute for Cell Science
Jamie L. Gehring: Allen Institute for Cell Science
Kaytlyn A. Gerbin: Allen Institute for Cell Science
Tanya Grancharova: Allen Institute for Cell Science
Benjamin W. Gregor: Allen Institute for Cell Science
Lisa J. Harrylock: Allen Institute for Cell Science
Amanda Haupt: Allen Institute for Cell Science
Melissa C. Hendershott: Allen Institute for Cell Science
Caroline Hookway: Allen Institute for Cell Science
Alan R. Horwitz: Allen Institute for Cell Science
H. Christopher Hughes: Allen Institute for Cell Science
Eric J. Isaac: Allen Institute for Cell Science
Gregory R. Johnson: Allen Institute for Cell Science
Brian Kim: Allen Institute for Cell Science
Andrew N. Leonard: Allen Institute for Cell Science
Winnie W. Leung: Allen Institute for Cell Science
Jordan J. Lucas: Allen Institute for Cell Science
Susan A. Ludmann: Allen Institute for Cell Science
Blair M. Lyons: Allen Institute for Cell Science
Haseeb Malik: Allen Institute for Cell Science
Ryan McGregor: Allen Institute for Cell Science
Gabe E. Medrash: Allen Institute for Cell Science
Sean L. Meharry: Allen Institute for Cell Science
Kevin Mitcham: Allen Institute for Cell Science
Irina A. Mueller: Allen Institute for Cell Science
Timothy L. Murphy-Stevens: Allen Institute for Cell Science
Aditya Nath: Allen Institute for Cell Science
Angelique M. Nelson: Allen Institute for Cell Science
Sandra A. Oluoch: Allen Institute for Cell Science
Luana Paleologu: Allen Institute for Cell Science
T. Alexander Popiel: Allen Institute for Cell Science
Megan M. Riel-Mehan: Allen Institute for Cell Science
Brock Roberts: Allen Institute for Cell Science
Lisa M. Schaefbauer: Allen Institute for Cell Science
Magdalena Schwarzl: Allen Institute for Cell Science
Jamie Sherman: Allen Institute for Cell Science
Sylvain Slaton: Allen Institute for Cell Science
M. Filip Sluzewski: Allen Institute for Cell Science
Jacqueline E. Smith: Allen Institute for Cell Science
Youngmee Sul: Allen Institute for Cell Science
Madison J. Swain-Bowden: Allen Institute for Cell Science
W. Joyce Tang: Allen Institute for Cell Science
Derek J. Thirstrup: Allen Institute for Cell Science
Daniel M. Toloudis: Allen Institute for Cell Science
Andrew P. Tucker: Allen Institute for Cell Science
Veronica Valencia: Allen Institute for Cell Science
Winfried Wiegraebe: Allen Institute for Cell Science
Thushara Wijeratna: Allen Institute for Cell Science
Ruian Yang: Allen Institute for Cell Science
Rebecca J. Zaunbrecher: Allen Institute for Cell Science
Ramon Lorenzo D. Labitigan: University of Washington
Adrian L. Sanborn: Stanford University
Graham T. Johnson: Allen Institute for Cell Science
Ruwanthi N. Gunawardane: Allen Institute for Cell Science
Nathalie Gaudreault: Allen Institute for Cell Science
Julie A. Theriot: University of Washington
Susanne M. Rafelski: Allen Institute for Cell Science

Nature, 2023, vol. 613, issue 7943, 345-354

Abstract: Abstract Understanding how a subset of expressed genes dictates cellular phenotype is a considerable challenge owing to the large numbers of molecules involved, their combinatorics and the plethora of cellular behaviours that they determine1,2. Here we reduced this complexity by focusing on cellular organization—a key readout and driver of cell behaviour3,4—at the level of major cellular structures that represent distinct organelles and functional machines, and generated the WTC-11 hiPSC Single-Cell Image Dataset v1, which contains more than 200,000 live cells in 3D, spanning 25 key cellular structures. The scale and quality of this dataset permitted the creation of a generalizable analysis framework to convert raw image data of cells and their structures into dimensionally reduced, quantitative measurements that can be interpreted by humans, and to facilitate data exploration. This framework embraces the vast cell-to-cell variability that is observed within a normal population, facilitates the integration of cell-by-cell structural data and allows quantitative analyses of distinct, separable aspects of organization within and across different cell populations. We found that the integrated intracellular organization of interphase cells was robust to the wide range of variation in cell shape in the population; that the average locations of some structures became polarized in cells at the edges of colonies while maintaining the ‘wiring’ of their interactions with other structures; and that, by contrast, changes in the location of structures during early mitotic reorganization were accompanied by changes in their wiring.

Date: 2023
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DOI: 10.1038/s41586-022-05563-7

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