Abstract

From coffee beans flowing in a chute to cells remodelling in a living tissue, a wide variety of close-packed collective systems—both inert and living—have the potential to jam. The collective can sometimes flow like a fluid or jam and rigidify like a solid. The unjammed-to-jammed transition remains poorly understood, however, and structural properties characterizing these phases remain unknown. Using primary human bronchial epithelial cells, we show that the jamming transition in asthma is linked to cell shape, thus establishing in that system a structural criterion for cell jamming. Surprisingly, the collapse of critical scaling predicts a counter-intuitive relationship between jamming, cell shape and cell–cell adhesive stresses that is borne out by direct experimental observations. Cell shape thus provides a rigorous structural signature for classification and investigation of bronchial epithelial layer jamming in asthma, and potentially in any process in disease or development in which epithelial dynamics play a prominent role.

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Acknowledgements

Authors thank the staff of the UNC CF Center, Tissue Procurement and Cell Culture Core at the University of North Carolina, Chapel Hill. This research was supported by the Francis Family Foundation, the Alfred P. Sloan Foundation, the American Heart Association (13SDG14320004), the National Research Foundation of Korea (NRF-2013S1A2A2035518), the National Science Foundation (BMMB-1334611, DMR-1352184) and the National Institutes of Health (K25HL091124, P30DK065988, P30ES000002, HL007118, R01HL102373, R01HL107561, P01HL120839).

Author information

Author notes

    • Jin-Ah Park
    •  & Jae Hun Kim

    These authors contributed equally to this work.

Affiliations

  1. Harvard T.H. Chan School of Public Health, Boston, Massachusetts 02115, USA

    • Jin-Ah Park
    • , Jae Hun Kim
    • , Jennifer A. Mitchel
    • , Nader Taheri Qazvini
    • , Chan Young Park
    • , Maureen McGill
    • , Sae-Hoon Kim
    • , Bomi Gweon
    • , Jacob Notbohm
    • , Robert Steward Jr
    • , Stephanie Burger
    • , Dhananjay T. Tambe
    • , Corey Hardin
    • , Stephanie A. Shore
    • , James P. Butler
    • , Jeffrey M. Drazen
    •  & Jeffrey J. Fredberg
  2. Syracuse University, Syracuse, New York 13244, USA

    • Dapeng Bi
    •  & M. Lisa Manning
  3. School of Chemistry, College of Science, University of Tehran, Tehran 14179, Iran

    • Nader Taheri Qazvini
  4. Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA

    • Kelan Tantisira
    • , Elliot Israel
    • , Elizabeth P. Henske
    • , Scott T. Weiss
    •  & James P. Butler
  5. The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27514, USA

    • Scott H. Randell
  6. Children’s Hospital, Boston, Massachusetts 02215, USA

    • Alvin T. Kho
  7. Department of Mechanical Engineering, University of South Alabama, Mobile, Alabama 36688, USA

    • Dhananjay T. Tambe
  8. Harvard University, Cambridge, Massachusetts 02138, USA

    • David A. Weitz
  9. Mayo Clinic College of Medicine, Rochester, Minnesota 55905, USA

    • Daniel J. Tschumperlin

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Contributions

J.-A.P. designed experiments, carried out time-lapse imaging of HBECs in ALI culture and interpreted data. J.H.K. designed measurements of physical forces within HBECs and analysed data. J.H.K. and M.M. carried out force-measurement experiments. J.H.K., N.T.Q., C.Y.P. and C.H. analysed the dynamics of cellular motions. D.B. and J.A.M. analysed cell-shape parameters. D.B. modelled cell-shape parameters and cell motility. J.A.M. and S.-H.K. carried out time-lapse imaging of HBECs in ALI culture. D.T.T., B.G., J.N., R.S. and S.B. contributed to preparation of physical-force measurements. S.H.R. contributed to the design of experiments and provided primary HBECs. D.A.W., D.J.T., S.T.W., M.L.M., J.P.B., J.M.D. and J.J.F. guided data interpretation and analysis of cellular migration and the jamming transition. S.H.R., A.T.K., S.A.S., E.I., S.T.W., E.P.H., K.T. and J.M.D. guided data interpretation on the biological relevance of cellular migration. J.-A.P., J.H.K., D.B., M.L.M. and J.J.F., wrote the manuscript. J.-A.P. and J.J.F. oversaw the project.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jin-Ah Park.

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https://doi.org/10.1038/nmat4357

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