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Epithelial plasticity and innate immune activation promote lung tissue remodeling following respiratory viral infection

Author

Listed:
  • Andrew K. Beppu

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Juanjuan Zhao

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Changfu Yao

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Gianni Carraro

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Edo Israely

    (Cedars-Sinai Medical Center)

  • Anna Lucia Coelho

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Katherine Drake

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Cory M. Hogaboam

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • William C. Parks

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

  • Jay K. Kolls

    (School of Medicine)

  • Barry R. Stripp

    (Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center
    Cedars-Sinai Medical Center)

Abstract

Epithelial plasticity has been suggested in lungs of mice following genetic depletion of stem cells but is of unknown physiological relevance. Viral infection and chronic lung disease share similar pathological features of stem cell loss in alveoli, basal cell (BC) hyperplasia in small airways, and innate immune activation, that contribute to epithelial remodeling and loss of lung function. We show that a subset of distal airway secretory cells, intralobar serous (IS) cells, are activated to assume BC fates following influenza virus infection. Injury-induced hyperplastic BC (hBC) differ from pre-existing BC by high expression of IL-22Ra1 and undergo IL-22-dependent expansion for colonization of injured alveoli. Resolution of virus-elicited inflammation results in BC to IS re-differentiation in repopulated alveoli, and increased local expression of protective antimicrobial factors, but fails to restore normal alveolar epithelium responsible for gas exchange.

Suggested Citation

  • Andrew K. Beppu & Juanjuan Zhao & Changfu Yao & Gianni Carraro & Edo Israely & Anna Lucia Coelho & Katherine Drake & Cory M. Hogaboam & William C. Parks & Jay K. Kolls & Barry R. Stripp, 2023. "Epithelial plasticity and innate immune activation promote lung tissue remodeling following respiratory viral infection," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41387-3
    DOI: 10.1038/s41467-023-41387-3
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    References listed on IDEAS

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    1. Wei Zuo & Ting Zhang & Daniel Zheng'An Wu & Shou Ping Guan & Audrey-Ann Liew & Yusuke Yamamoto & Xia Wang & Siew Joo Lim & Matthew Vincent & Mark Lessard & Christopher P. Crum & Wa Xian & Frank McKeon, 2015. "p63+Krt5+ distal airway stem cells are essential for lung regeneration," Nature, Nature, vol. 517(7536), pages 616-620, January.
    2. Gioele La Manno & Ruslan Soldatov & Amit Zeisel & Emelie Braun & Hannah Hochgerner & Viktor Petukhov & Katja Lidschreiber & Maria E. Kastriti & Peter Lönnerberg & Alessandro Furlan & Jean Fan & Lars E, 2018. "RNA velocity of single cells," Nature, Nature, vol. 560(7719), pages 494-498, August.
    3. Purushothama Rao Tata & Hongmei Mou & Ana Pardo-Saganta & Rui Zhao & Mythili Prabhu & Brandon M. Law & Vladimir Vinarsky & Josalyn L. Cho & Sylvie Breton & Amar Sahay & Benjamin D. Medoff & Jayaraj Ra, 2013. "Dedifferentiation of committed epithelial cells into stem cells in vivo," Nature, Nature, vol. 503(7475), pages 218-223, November.
    4. Alexandra Van Keymeulen & Ana Sofia Rocha & Marielle Ousset & Benjamin Beck & Gaëlle Bouvencourt & Jason Rock & Neha Sharma & Sophie Dekoninck & Cédric Blanpain, 2011. "Distinct stem cells contribute to mammary gland development and maintenance," Nature, Nature, vol. 479(7372), pages 189-193, November.
    5. Caroline A. Lindemans & Marco Calafiore & Anna M. Mertelsmann & Margaret H. O’Connor & Jarrod A. Dudakov & Robert R. Jenq & Enrico Velardi & Lauren F. Young & Odette M. Smith & Gillian Lawrence & Juli, 2015. "Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration," Nature, Nature, vol. 528(7583), pages 560-564, December.
    6. Andrew E. Vaughan & Alexis N. Brumwell & Ying Xi & Jeffrey E. Gotts & Doug G. Brownfield & Barbara Treutlein & Kevin Tan & Victor Tan & Feng Chun Liu & Mark R. Looney & Michael A. Matthay & Jason R. R, 2015. "Lineage-negative progenitors mobilize to regenerate lung epithelium after major injury," Nature, Nature, vol. 517(7536), pages 621-625, January.
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