Strategies to improve the therapeutic effects of mesenchymal stromal cells in respiratory diseases

Stem Cell Research and Therapy

Volumn 9, Issue 1, 2018, Pages

  Silva, Luisa H A ^a   Antunes, Mariana A ^a,b   Dos Santos, Claudia C ^c   Weiss, Daniel J ^d   Cruz, Fernanda F ^a,b   Rocco, Patricia R M ^a,b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b National Institute of Science and Technology for Gene Therapy   (Brazil)

^c ST MICHAEL'S HOSPITAL   (Canada)

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

Author keywords

Genetic manipulation; Hypoxia; Mesenchymal stromal cells; Serum deprivation

Indexed keywords

HEAT SHOCK PROTEIN;

BIOLOGICAL ACTIVITY; CELL FUNCTION; CELL HYPOXIA; CELL MEMBRANE POTENTIAL; CELL PROTECTION; CELL SURVIVAL; CELL THERAPY; CLINICAL EVALUATION; DEPLETION; DISEASE MODEL; GENE EXPRESSION; GENETIC MANIPULATION; HEAT SHOCK; HUMAN; INFLAMMATION; ISCHEMIC PRECONDITIONING; MESENCHYMAL STROMA CELL; NONHUMAN; OXIDATIVE STRESS; PRECLINICAL STUDY; PRIORITY JOURNAL; RESPIRATORY TRACT DISEASE; REVIEW; SERUM DEPLETION; STEM CELL TRANSPLANTATION; SURVIVAL RATE; THERAPY EFFECT; TREATMENT OUTCOME; ANIMAL; CLINICAL TRIAL (TOPIC); MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; METABOLISM; PATHOLOGY;

ANIMALS; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; RESPIRATORY TRACT DISEASES;

EID: 85042621979     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/s13287-018-0802-8     Document Type: Review

References (52)

1. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006;8:315-7.
2. Ryan A, Murphy M, Barry F. Mesenchymal stem/stromal cell therapy. In: Atkinson K, editor. The Biology and therapeutic application of mesenchymal cells. Hoboken: Wiley; 2017. p. 426-40.
3. Abreu SC, Weiss DJ, Rocco PRM. Extracellular vesicles derived from mesenchymal stromal cells: a therapeutic option in respiratory diseases? Stem Cell Res Ther. 2016;7:53.
4. Spees JL, Lee RH, Gregory CA. Mechanisms of mesenchymal stem/stromal cell function. Stem Cell Res Ther. 2016;7:125.
5. Sinclair KA, Yerkovich ST, Hopkins PM-A, Chambers DC. Characterization of intercellular communication and mitochondrial donation by mesenchymal stromal cells derived from the human lung. Stem Cell Res Ther. 2016;7:91.
6. Maron-Gutierrez T, Silva JD, Asensi KD, Bakker-Abreu I, Shan Y, Diaz BL, Goldenberg RCS, Mei SHJ, Stewart DJ, Morales MM, Rocco PRM, Dos Santos CC. Effects of mesenchymal stem cell therapy on the time course of pulmonary remodeling depend on the etiology of lung injury in mice. Crit Care Med. 2013;41:e319-33.
7. Cruz FF, Borg ZD, Goodwin M, Sokocevic D, Wagner DE, Coffey A, Antunes M, Robinson KL, Mitsialis SA, Kourembanas S, Thane K, Hoffman AM, McKenna DH, Rocco PRM, Weiss DJ. 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;4:1302-16.
8. Abreu SC, Antunes MA, Xisto DG, Cruz FF, Branco VC, Bandeira E, Kitoko J, de Araújo AF, Dellatorre-Texeira L, Olsen PC, Weiss DJ, Diaz BL, Morales MM, Rocco PR. 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;6:1557-67.
9. Antunes MA, Abreu SC, Cruz FF, Teixeira AC, Lopes-Pacheco M, Bandeira E, Olsen PC, Diaz BL, Takyia CM, Freitas IP, Rocha NN, Capelozzi VL, Xisto DG, Weiss DJ, Morales MM, Rocco PR. Effects of different mesenchymal stromal cell sources and delivery routes in experimental emphysema. Respir Res. 2014;15:118.
10. Lassance RM, Prota LFM, Maron-Gutierrez T, Garcia CSNB, Abreu SC, Pássaro CP, Xisto DG, Castiglione RC, Carreira H, Ornellas DS, Santana MCE, Souza SAL, Gutfilen B, Fonseca LMB, Rocco PRM, Morales MM. Intratracheal instillation of bone marrow-derived cell in an experimental model of silicosis. Respir Physiol Neurobiol. 2009;169:227-33.
11. Weiss DJ, Casaburi R, Flannery R, LeRoux-Williams M, Tashkin DP. A placebo-controlled, randomized trial of mesenchymal stem cells in COPD. Chest. 2013;143:1590-8.
12. Morales MM, Souza SAL, Loivos LP, Lima MA, Szklo A, Vairo L, Brunswick THK, Gutfilen B, Lopes-Pacheco M, Araújo AJ, Cardoso AP, Goldenberg RC, Rocco PRM, Fonseca LMB. Lapa e Silva JR. Pilot safety study of intrabronchial instillation of bone marrow-derived mononuclear cells in patients with silicosis. BMC Pulm Med. 2015;15:66.
13. Stolk J, Broekman W, Mauad T, Zwaginga JJ, Roelofs H, Fibbe WE, Oostendorp J, Bajema I, Versteegh MIM, Taube C, Hiemstra PS. A phase I study for intravenous autologous mesenchymal stromal cell administration to patients with severe emphysema. QJM. 2016;109:331-6.
14. Zheng G, Huang L, Tong H, Shu Q, Hu Y, Ge M, Deng K, Zhang L, Zou B, Cheng B, Xu J. Treatment of acute respiratory distress syndrome with allogeneic adipose-derived mesenchymal stem cells: a randomized, placebo-controlled pilot study. Respir Res. 2014;15:39.
15. Wilson JG, Liu KD, Zhuo H, Caballero L, McMillan M, Fang X, Cosgrove K, Vojnik R, Calfee CS, Lee J-W, Rogers AJ, Levitt J, Wiener-Kronish J, Bajwa EK, Leavitt A, McKenna D, Thompson BT, Matthay MA. Mesenchymal stem (stromal) cells for treatment of ARDS: a phase 1 clinical trial. Lancet Respir Med. 2015;3:24-32.
16. McIntyre LA, Moher D, Fergusson DA, Sullivan KJ, Mei SHJ, Lalu M, Marshall J, Mcleod M, Griffin G, Grimshaw J, Turgeon A, Avey MT, Rudnicki MA, Jazi M, Fishman J, Stewart DJ. Canadian Critical Care Translational Biology Group. Efficacy of mesenchymal stromal cell therapy for acute lung injury in preclinical animal models: a systematic review. PLoS One. 2016;11:e0147170.
17. Mei SHJ, Dos Santos CC, Stewart DJ. Advances in stem cell and cell-based gene therapy approaches for experimental acute lung injury: a review of preclinical studies. Hum Gene Ther. 2016;27:802-12.
18. Eggenhofer E, Benseler V, Kroemer A, Popp FC, Geissler EK, Schlitt HJ, Baan CC, Dahlke MH, Hoogduijn MJ. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol. 2012;3:297.
19. Wang H, Cao F, De A, Cao Y, Contag C, Gambhir SS, Wu JC, Chen X. Trafficking mesenchymal stem cell engraftment and differentiation in tumor-bearing mice by bioluminescence imaging. Stem Cells. 2009;27:1548-58.
20. Yang J-X, Zhang N, Wang H-W, Gao P, Yang Q-P, Wen Q-P. CXCR4 Receptor overexpression in mesenchymal stem cells facilitates treatment of acute lung injury in rats. J Biol Chem. 2015;290:1994-2006.
21. Silva LHA, da Silva JR, Ferreira GA, Silva RC, Lima ECD, Azevedo RB, Oliveira DM. Labeling mesenchymal cells with DMSA-coated gold and iron oxide nanoparticles: assessment of biocompatibility and potential applications. J Nanobiotechnology. 2016;14:59.
22. Sart S, Ma T, Li Y. Preconditioning stem cells for in vivo delivery. Biores Open Access. 2014;3:137-49.
23. Lee KA, Shim W, Paik MJ, Lee SC, Shin JY, Ahn YH, Park K, Kim JH, Choi S, Lee G. Analysis of changes in the viability and gene expression profiles of human mesenchymal stromal cells over time. Cytotherapy. 2009;11:688-97.
24. François M, Copland IB, Yuan S, Romieu-Mourez R, Waller EK, Galipeau J. Cryopreserved mesenchymal stromal cells display impaired immunosuppressive properties as a result of heat-shock response and impaired interferon-γ licensing. Cytotherapy. 2012;14:147-52.
25. Cruz FF, Borg ZD, Goodwin M, Sokocevic D, Wagner D, McKenna DH, Rocco PRM, Weiss DJ. Freshly thawed and continuously cultured human bone marrow-derived mesenchymal stromal cells comparably ameliorate allergic airways inflammation in immunocompetent mice. Stem Cells Transl Med. 2015;4:615-24.
26. Pei M. Environmental preconditioning rejuvenates adult stem cells' proliferation and chondrogenic potential. Biomaterials. 2017;117:10-23.
27. Wang H, Yang Y-F, Zhao L, Xiao F-J, Zhang Q-W, Wen M-L, Wu C-T, Peng R-Y, Wang L-S. Hepatocyte growth factor gene-modified mesenchymal stem cells reduce radiation-induced lung injury. Hum Gene Ther. 2013;24:343-53.
28. Chen S, Chen X, Wu X, Wei S, Han W, Lin J, Kang M, Chen L. Hepatocyte growth factor-modified mesenchymal stem cells improve ischemia/reperfusion-induced acute lung injury in rats. Gene Ther. 2016;24:3.
29. Amiri F, Jahanian-Najafabadi A, Roudkenar MH. In vitro augmentation of mesenchymal stem cells viability in stressful microenvironments. Cell Stress Chaperones. 2015;20:237-51.
30. Boregowda SV, Krishnappa V, Chambers JW, Lograsso PV, Lai W-T, Ortiz LA, Phinney DG. Atmospheric oxygen inhibits growth and differentiation of marrow-derived mouse mesenchymal stem cells via a p53-dependent mechanism: implications for long-term culture expansion. Stem Cells. 2012;30:975-87.
31. Fehrer C, Brunauer R, Laschober G, Unterluggauer H, Reitinger S, Kloss F, Gülly C, Gaßner R, Lepperdinger G. Reduced oxygen tension attenuates differentiation capacity of human mesenchymal stem cells and prolongs their lifespan. Aging Cell. 2007;6:745-57.
32. Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang J-A, Wei L. Transplantation of hypoxia-preconditioned mesenchymal stem cells improves infarcted heart function via enhanced survival of implanted cells and angiogenesis. J Thorac Cardiovasc Surg. 2008;135:799-808.
33. Han Y-S, Lee JH, Yoon YM, Yun CW, Noh H, Lee SH. Hypoxia-induced expression of cellular prion protein improves the therapeutic potential of mesenchymal stem cells. Cell Death Dis. 2016;7:e2395.
34. Lan Y-W, Choo K-B, Chen C-M, Hung T-H, Chen Y-B, Hsieh C-H, Kuo H-P, Chong K-Y. Hypoxia-preconditioned mesenchymal stem cells attenuate bleomycin-induced pulmonary fibrosis. Stem Cell Res Ther. 2015;6:97.
35. Li S, Deng Y, Feng J, Ye W. Oxidative preconditioning promotes bone marrow mesenchymal stem cells migration and prevents apoptosis. Cell Biol Int. 2009;33:411-8.
36. Moloney TC, Hoban DB, Barry FP, Howard L, Dowd E. Kinetics of thermally induced heat shock protein 27 and 70 expression by bone marrow-derived mesenchymal stem cells. Protein Sci. 2012;21:904-9.
37. Gao F, Hu X, Xie X, Xu Q, Wang Y, Liu X. Heat shock protein 90 protects rat mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis via the PI3K/Akt and ERK1/2 pathways. J Zhejiang. 2010;11:608-17.
38. Moya A, Larochette N, Paquet J, Deschepper M, Bensidhoum M, Izzo V, Kroemer G, Petite H, Logeart-Avramoglou D. Quiescence preconditioned human multipotent stromal cells adopt a metabolic profile favorable for enhanced survival under ischemia. Stem Cells. 2017;35:181-96.
39. Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;168:960-76.
40. Galleu A, Riffo-Vasquez Y, Trento C, Lomas C, Dolcetti L, Cheung TS, von Bonin M, Barbieri L, Halai K, Ward S, Weng L, Chakraverty R, Lombardi G, Watt FM, Orchard K, Marks DI, Apperley J, Bornhauser M, Walczak H, Bennett C, Dazzi F. Apoptosis in mesenchymal stromal cells induces in vivo recipient-mediated immunomodulation. Sci Transl Med. 2017;9:eaam7828.
41. Chang C-L, Leu S, Sung H-C, Zhen Y-Y, Cho C-L, Chen A, Tsai T-H, Chung S-Y, Chai H-T, Sun C-K, Yen C-H, Yip H-K. Impact of apoptotic adipose-derived mesenchymal stem cells on attenuating organ damage and reducing mortality in rat sepsis syndrome induced by cecal puncture and ligation. J Transl Med. 2012;10:244.
42. Bustos ML, Huleihel L, Meyer EM, Donnenberg AD, Donnenberg VS, Sciurba JD, Mroz L, McVerry BJ, Ellis BM, Kaminski N, Rojas M. Activation of human mesenchymal stem cells impacts their therapeutic abilities in lung injury by increasing interleukin (IL)-10 and IL-1RN levels. Stem Cells Transl Med. 2013;2:884-95.
43. Hong Y, Kim Y-S, Hong S-H, Oh Y-M. Therapeutic effects of adipose-derived stem cells pretreated with pioglitazone in an emphysema mouse model. Exp Mol Med. 2016;48:e266.
44. Wang Q, Shen C, Zhu H, Zhou W, Guo X. N-acetylcysteine-pretreated human embryonic mesenchymal stem cell administration protects against bleomycin-induced lung injury. Am J Med Sci. 2013;346:113-22.
45. Yang Z, Concannon J, Ng KS, Seyb K, Mortensen LJ, Ranganath S, Gu F, Levy O, Tong Z, Martyn K, Zhao W, Lin CP, Ma G, Karp JM. Tetrandrine identified in a small molecule screen to activate mesenchymal stem cells for enhanced immunomodulation. Sci Rep. 2016;6:30263.
46. Zhao Y-F, Xiong W, Wu X-L. Mesenchymal stem cell-based developmental endothelial locus-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice. Mol Med Rep. 2014;9:1583-9.
47. Martínez-González I, Roca O, Masclans JR, Moreno R, Salcedo MT, Baekelandt V, Cruz MJ, Rello J, Aran JM. Human mesenchymal stem cells overexpressing the IL-33 antagonist soluble IL-1 receptor-like-1 attenuate endotoxin-induced acute lung injury. Am J Respir Cell Mol Biol. 2013;49:552-62.
48. He H, Liu L, Chen Q, Liu A, Cai S, Yang Y, Lu X, Qiu H. Mesenchymal stem cells overexpressing angiotensin-converting enzyme 2 rescue lipopolysaccharide-induced lung injury. Cell Transplant. 2015;24:1699-715.
49. Chen H, Xiang H, Wu B, Zhang X, Li M, Liu J, Li J, Ren Z, Du B, He K, Zeng Q, Yang C. Manganese superoxide dismutase gene modified mesenchymal stem cells attenuates acute radiation-induced lung injury. Hum Gene Ther. 2017;28:523-32.
50. Liang OD, Mitsialis SA, Chang MS, Vergadi E, Lee C, Aslam M, Fernandez-Gonzalez A, Liu X, Baveja R, Kourembanas S. Mesenchymal stromal cells expressing heme oxygenase-1 reverse pulmonary hypertension. Stem Cells. 2011;29:99-107.
51. Chen Y-B, Lan Y-W, Chen L-G, Huang T-T, Choo K-B, Cheng WTK, Lee H-S, Chong K-Y. Mesenchymal stem cell-based HSP70 promoter-driven VEGFA induction by resveratrol alleviates elastase-induced emphysema in a mouse model. Cell Stress Chaperones. 2015;20:979-89.
52. Granton J, Langleben D, Kutryk MB, Camack N, Galipeau J, Courtman DW, Stewart DJ. Endothelial NO-synthase gene-enhanced progenitor cell therapy for pulmonary arterial hypertension: the PHACeT Trial. Circ Res. 2015;117:645-54.