Human adipose tissue mesenchymal stromal cells and their extracellular vesicles act differentially on lung mechanics and inflammation in experimental allergic asthma

Stem Cell Research and Therapy

Volumn 8, Issue 1, 2017, Pages

  De Castro, Ligia Lins ^a   Xisto, Debora Gonçalves ^a   Kitoko, Jamil Zola ^a   Cruz, Fernanda Ferreira ^a   Olsen, Priscilla Christina ^a   Redondo, Patricia Albuquerque Garcia ^a   Ferreira, Tatiana Paula Teixeira ^b   Weiss, Daniel Jay ^c   Martins, Marco Aurélio ^b   Morales, Marcelo Marcos ^a   Rocco, Patricia Rieken MacEdo ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Asthma; Extracellular vesicles; Inflammation; Mesenchymal stromal cells; Remodeling

Indexed keywords

CD4 ANTIGEN; EOTAXIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 4; INTERLEUKIN 5; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADULT; AIRWAY RESISTANCE; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHOALVEOLAR LAVAGE FLUID; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL FUNCTION; COLLAGEN FIBER; CONTROLLED STUDY; EOSINOPHIL; EOSINOPHIL COUNT; EXOSOME; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG COMPLIANCE; LUNG MECHANICS; LUNG PARENCHYMA; LUNG PRESSURE; LYMPHOCYTE COUNT; MESENCHYMAL STROMA CELL; MIDDLE AGED; MOUSE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN CONTENT; REGULATORY T LYMPHOCYTE; THYMUS; TIDAL VOLUME; YOUNG ADULT; ADIPOSE TISSUE; ANIMAL; ASTHMA; BREATHING MECHANICS; IMMUNOLOGY; LUNG; PATHOLOGY; PATHOPHYSIOLOGY; TRANSPLANTATION; XENOGRAFT;

ADIPOSE TISSUE; ANIMALS; ASTHMA; EXTRACELLULAR VESICLES; FEMALE; HETEROGRAFTS; HUMANS; LUNG; MESENCHYMAL STROMAL CELLS; MICE; RESPIRATORY MECHANICS;

EID: 85021287232     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-017-0600-8     Document Type: Article

References (46)

1. Global Initiative for Asthma. Global Strategy for Asthma Management and Prevention. 2016. Available from ginasthma.org/wp-content/uploads/2016/04/GINA-2016-main-report-tracked.pdf. Accessed 13 June 2017.
2. Barnes PJ. New therapies for asthma: is there any progress? Trends Pharmacol Sci. 2010;31(7):335-43.
3. Papierniak ES, Lowenthal DT, Harman E. Novel therapies in asthma: leukotriene antagonists, biologic agents, and beyond. Am J Ther. 2013;20(1):79-103.
4. Singh D, Petavy F, Macdonald AJ, Lazaar AL, O'Connor BJ. The inhaled phosphodiesterase 4 inhibitor GSK256066 reduces allergen challenge responses in asthma. Respir Res. 2010;11:26.
5. Yazid S, Sinniah A, Solito E, Calder V, Flower RJ. Anti-allergic cromones inhibit histamine and eicosanoid release from activated human and murine mast cells by releasing Annexin A1. PLoS One. 2013;8(3):e58963.
6. Cho KS, Park MK, Kang SA, Park HY, Hong SL, Park HK, Yu HS, Roh HJ. Adipose-derived stem cells ameliorate allergic airway inflammation by inducing regulatory T cells in a mouse model of asthma. Mediat Inflamm. 2014;2014:436476.
7. Park HK, Cho KS, Park HY, Shin DH, Kim YK, Jung JS, Park SK, Roh HJ. Adipose-derived stromal cells inhibit allergic airway inflammation in mice. Stem Cells Dev. 2010;19(11):1811-8.
8. Marinas-Pardo L, Mirones I, Amor-Carro O, Fraga-Iriso R, Lema-Costa B, Cubillo I, Rodriguez Milla MA, Garcia-Castro J, Ramos-Barbon D. Mesenchymal stem cells regulate airway contractile tissue remodeling in murine experimental asthma. Allergy. 2014;69(6):730-40.
9. Cho KS, Lee JH, Park MK, Park HK, Yu HS, Roh HJ. Prostaglandin E2 and transforming growth factor-beta play a critical role in suppression of allergic airway inflammation by adipose-derived stem cells. PLoS One. 2015;10(7):e0131813.
10. Martinez-Gonzalez I, Cruz MJ, Moreno R, Morell F, Munoz X, Aran JM. Human mesenchymal stem cells resolve airway inflammation, hyperreactivity, and histopathology in a mouse model of occupational asthma. Stem Cells Dev. 2014;23(19):2352-63.
11. Cruz FF, Borg ZD, Goodwin M, Sokocevic D, Wagner DE, Coffey A, Antunes M, Robinson KL, Mitsialis SA, Kourembanas S, et al. Systemic administration of human bone marrow-derived mesenchymal stromal cell extracellular vesicles ameliorates aspergillus hyphal extract-induced allergic airway inflammation in immunocompetent mice. Stem Cells Transl Med. 2015;4(11):1302-16.
12. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy. 2013;15(6):641-8.
13. Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, et al. Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol. 2009;20(5):1053-67.
14. Silva PL, Passaro CP, Cagido VR, Bozza M, Dolhnikoff M, Negri EM, Morales MM, Capelozzi VL, Zin WA, Rocco PR. Impact of lung remodelling on respiratory mechanics in a model of severe allergic inflammation. Respir Physiol Neurobiol. 2008;160(3):239-48.
15. Abreu SC, Antunes MA, de Castro JC, de Oliveira MV, Bandeira E, Ornellas DS, Diaz BL, Morales MM, Xisto DG, Rocco PR. Bone marrow-derived mononuclear cells vs. mesenchymal stromal cells in experimental allergic asthma. Respir Physiol Neurobiol. 2013;187(2):190-8.
16. Xisto DG, Farias LL, Ferreira HC, Picanco MR, Amitrano D, Lapa ESJR, Negri EM, Mauad T, Carnielli D, Silva LF, et al. Lung parenchyma remodeling in a murine model of chronic allergic inflammation. Am J Respir Crit Care Med. 2005;171(8):829-37.
17. Burburan SM, Xisto DG, Ferreira HC, Riva Ddos R, Carvalho GM, Zin WA, Rocco PR. Lung mechanics and histology during sevoflurane anesthesia in a model of chronic allergic asthma. Anesth Analg. 2007;104(3):631-7.
18. Bates JH, Ludwig MS, Sly PD, Brown K, Martin JG, Fredberg JJ. Interrupter resistance elucidated by alveolar pressure measurement in open-chest normal dogs. J Appl Physiol (1985). 1988;65(1):408-14.
19. Saldiva PH, Zin WA, Santos RL, Eidelman DH, Milic-Emili J. Alveolar pressure measurement in open-chest rats. J Appl Physiol (1985). 1992;72(1):302-6.
20. Ferreira TP, Mariano LL, Ghilosso-Bortolini R, de Arantes AC, Fernandes AJ, Berni M, Cecchinato V, Uguccioni M, Maj R, Barberis A, et al. Potential of PEGylated Toll-like receptor 7 ligands for controlling inflammation and functional changes in mouse models of asthma and silicosis. Front Immunol. 2016;7:95.
21. Lowe AP, Broadley KJ, Nials AT, Ford WR, Kidd EJ. Adjustment of sensitisation and challenge protocols restores functional and inflammatory responses to ovalbumin in guinea-pigs. J Pharmacol Toxicol Methods. 2015;72:85-93.
22. Meyerholz DK, Griffin MA, Castilow EM, Varga SM. Comparison of histochemical methods for murine eosinophil detection in an RSV vaccine-enhanced inflammation model. Toxicol Pathol. 2009;37(2):249-55.
23. Abreu SC, Antunes MA, Mendonca L, Branco VC, de Melo EB, Olsen PC, Diaz BL, Weiss DJ, Paredes BD, Xisto DG, et al. Effects of bone marrow mononuclear cells from healthy or ovalbumin-induced lung inflammation donors on recipient allergic asthma mice. Stem Cell Res Ther. 2014;5(5):108.
24. Abreu SC, Antunes MA, Xisto DG, Cruz FF, Branco VC, Bandeira E, Zola Kitoko J, de Araujo AF, Dellatorre-Texeira L, Olsen PC, et al. Bone marrow, adipose, and lung tissue-derived murine mesenchymal stromal cells release different mediators and differentially affect airway and lung parenchyma in experimental asthma. Stem Cells Transl Med. 2017;6(6):1557-67.
25. da Silva AL, Magalhaes RF, Branco VC, Silva JD, Cruz FF, Marques PS, Ferreira TP, Morales MM, Martins MA, Olsen PC, et al. The tyrosine kinase inhibitor dasatinib reduces lung inflammation and remodelling in experimental allergic asthma. Br J Pharmacol. 2016;173(7):1236-47.
26. Antunes MA, Abreu SC, Silva AL, Parra-Cuentas ER, Ab'Saber AM, Capelozzi VL, Ferreira TP, Martins MA, Silva PM, Rocco PR. Sex-specific lung remodeling and inflammation changes in experimental allergic asthma. J Appl Physiol (1985). 2010;109(3):855-63.
27. Zhu Y, Liu T, Song K, Fan X, Ma X, Cui Z. Adipose-derived stem cell: a better stem cell than BMSC. Cell Biochem Funct. 2008;26(6):664-75.
28. Lee JK, Park SR, Jung BK, Jeon YK, Lee YS, Kim MK, Kim YG, Jang JY, Kim CW. Exosomes derived from mesenchymal stem cells suppress angiogenesis by down-regulating VEGF expression in breast cancer cells. PLoS One. 2013;8(12):e84256.
29. Monsel A, Zhu YG, Gennai S, Hao Q, Hu S, Rouby JJ, Rosenzwajg M, Matthay MA, Lee JW. Therapeutic effects of human mesenchymal stem cell-derived microvesicles in severe pneumonia in mice. Am J Respir Crit Care Med. 2015;192(3):324-36.
30. Zhu YG, Feng XM, Abbott J, Fang XH, Hao Q, Monsel A, Qu JM, Matthay MA, Lee JW. Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells. 2014;32(1):116-25.
31. Hamid Q, Tulic M. Immunobiology of asthma. Annu Rev Physiol. 2009;71:489-507.
32. Borowski A, Kuepper M, Horn U, Knupfer U, Zissel G, Hohne K, Luttmann W, Krause S, Virchow Jr JC, Friedrich K. Interleukin-13 acts as an apoptotic effector on lung epithelial cells and induces pro-fibrotic gene expression in lung fibroblasts. Clin Exp Allergy. 2008;38(4):619-28.
33. Bellini A, Marini MA, Bianchetti L, Barczyk M, Schmidt M, Mattoli S. Interleukin (IL)-4, IL-13, and IL-17A differentially affect the profibrotic and proinflammatory functions of fibrocytes from asthmatic patients. Mucosal Immunol. 2012;5(2):140-9.
34. Rankin SM, Conroy DM, Williams TJ. Eotaxin and eosinophil recruitment: implications for human disease. Mol Med Today. 2000;6(1):20-7.
35. Kovacs EJ. Fibrogenic cytokines: the role of immune mediators in the development of scar tissue. Immunol Today. 1991;12(1):17-23.
36. Halwani R, Al-Muhsen S, Al-Jahdali H, Hamid Q. Role of transforming growth factor-beta in airway remodeling in asthma. Am J Respir Cell Mol Biol. 2011;44(2):127-33.
37. Makinde T, Murphy RF, Agrawal DK. The regulatory role of TGF-beta in airway remodeling in asthma. Immunol Cell Biol. 2007;85(5):348-56.
38. Raundhal M, Morse C, Khare A, Oriss TB, Milosevic J, Trudeau J, Huff R, Pilewski J, Holguin F, Kolls J, et al. High IFN-gamma and low SLPI mark severe asthma in mice and humans. J Clin Invest. 2015;125(8):3037-50.
39. Moore KW, O'Garra A, de Waal MR, Vieira P, Mosmann TR. Interleukin-10. Annu Rev Immunol. 1993;11:165-90.
40. da Silva AL, Martini SV, Abreu SC, Samary Cdos S, Diaz BL, Fernezlian S, de Sa VK, Capelozzi VL, Boylan NJ, Goya RG, et al. DNA nanoparticle-mediated thymulin gene therapy prevents airway remodeling in experimental allergic asthma. J Control Release. 2014;180:125-33.
41. Matsumoto K, Inoue H, Tsuda M, Honda Y, Kibe A, Machida K, Yoshiura Y, Nakanishi Y. Different roles of interleukin-10 in onset and resolution of asthmatic responses in allergen-challenged mice. Respirology. 2005;10(1):18-26.
42. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002;99(10):3838-43.
43. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, Dazzi F. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood. 2003;101(9):3722-9.
44. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005;105(4):1815-22.
45. Luz-Crawford P, Kurte M, Bravo-Alegria J, Contreras R, Nova-Lamperti E, Tejedor G, Noel D, Jorgensen C, Figueroa F, Djouad F, et al. Mesenchymal stem cells generate a CD4 + CD25 + Foxp3+ regulatory T cell population during the differentiation process of Th1 and Th17 cells. Stem Cell Res Ther. 2013;4(3):65.
46. Lathrop MJ, Brooks EM, Bonenfant NR, Sokocevic D, Borg ZD, Goodwin M, Loi R, Cruz F, Dunaway CW, Steele C, et al. Mesenchymal stromal cells mediate Aspergillus hyphal extract-induced allergic airway inflammation by inhibition of the Th17 signaling pathway. Stem Cells Transl Med. 2014;3(2):194-205.