Characterization of intercellular communication and mitochondrial donation by mesenchymal stromal cells derived from the human lung

Stem Cell Res Ther. 2016 Jul 12;7(1):91. doi: 10.1186/s13287-016-0354-8.

Abstract

Background: Bone marrow-derived mesenchymal stromal cells (BM-MSCs) are capable of repairing wounded lung epithelial cells by donating cytoplasmic material and mitochondria. Recently, we characterized two populations of human lung-derived mesenchymal stromal cells isolated from digested parenchymal lung tissue (LT-MSCs) from healthy individuals or from lung transplant recipients' bronchoalveolar lavage fluid (BAL-MSCs). The aim of this study was to determine whether LT-MSCs and BAL-MSCs are also capable of donating cytoplasmic content and mitochondria to lung epithelial cells.

Methods: Cytoplasmic and mitochondrial transfer was assessed by co-culturing BEAS2B epithelial cells with Calcein AM or Mitotracker Green FM-labelled MSCs. Transfer was then measured by flow cytometry and validated by fluorescent microscopy. Molecular inhibitors were used to determine the contribution of microtubules/tunnelling nanotubes (TNTs, cytochalasin D), gap junctions (carbenoxolone), connexin-43 (gap26) and microvesicles (dynasore).

Results: F-actin microtubules/TNTs extending from BM-MSCs, LT-MSCs and BAL-MSCs to bronchial epithelial cells formed within 45 minutes of co-culturing cells. Each MSC population transferred a similar volume of cytoplasmic content to epithelial cells. Inhibiting microtubule/TNTs, gap junction formation and microvesicle endocytosis abrogated the transfer of cytoplasmic material from BM-MSCs, LT-MSCs and BAL-MSCs to epithelial cells. In contrast, blocking connexin-43 gap junction formation had no effect on cytoplasmic transfer. All MSC populations donated mitochondria to bronchial epithelial cells with similar efficiency. Mitochondrial transfer was reduced in all co-cultures after microtubule/TNT or endocytosis inhibition. Gap junction formation inhibition reduced mitochondrial transfer in BM-MSC and BAL-MSC co-cultures but had no effect on transfer in LT-MSC co-cultures. Connexin-43 inhibition did not impact mitochondrial transfer. Finally, bronchial epithelial cells were incapable of donating cytoplasmic content or mitochondria to any MSC population.

Conclusion: Similar to their bone marrow counterparts, LT-MSCs and BAL-MSCs can donate cytoplasmic content and mitochondria to bronchial epithelial cells via multiple mechanisms. Given that BM-MSCs utilize these mechanisms to mediate the repair of damaged bronchial epithelial cells, both LT-MSCs and BAL-MSCs will probably function similarly.

Keywords: Bronchoalveolar lavage; Intercellular communication; Mesenchymal stem cells; Mesenchymal stromal cells; Mitochondrial donation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Biological Transport
  • Bone Marrow Cells / metabolism*
  • Bone Marrow Cells / ultrastructure
  • Bronchoalveolar Lavage Fluid / cytology
  • Cell Communication
  • Cell Line
  • Coculture Techniques
  • Connexin 43 / genetics
  • Connexin 43 / metabolism
  • Epithelial Cells / metabolism*
  • Epithelial Cells / ultrastructure
  • Female
  • Gap Junctions / metabolism
  • Gap Junctions / ultrastructure
  • Gene Expression
  • Humans
  • Lung / metabolism*
  • Lung / ultrastructure
  • Male
  • Mesenchymal Stem Cells / metabolism*
  • Mesenchymal Stem Cells / ultrastructure
  • Microscopy, Fluorescence
  • Microtubules / metabolism
  • Microtubules / ultrastructure
  • Middle Aged
  • Mitochondria / metabolism*
  • Mitochondria / ultrastructure
  • Primary Cell Culture

Substances

  • Connexin 43
  • GJA1 protein, human