Boosting therapeutic efficacy of mesenchymal stem cells in pulmonary fibrosis: The role of genetic modification and preconditioning strategies

Document Type : Review Article

Authors

1 Physiology Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences, Kerman, Iran

2 Department of Laboratory Hematology and Blood Banking, Faculty of Allied Medicine, Kerman University of Medical Sciences, Kerman, Iran

3 Department of Physiology and Pharmacology, Afzalipour Medical Faculty, Kerman University of Medical Sciences, Kerman, Iran

4 Applied Cellular and Molecular Research Center, Kerman University of Medical Sciences, Kerman, Iran

5 Herbal and Traditional Medicines Research Center, Kerman University of Medical Sciences, Kerman, Iran

6 Abnormal Uterine Bleeding Research Center, Semnan University of Medical Sciences, Semnan, Iran

7 School of Pharmacy, Semnan University of Medical Sciences, Semnan, Iran

8 Pharmaceutical Sciences and Cosmetic Products Research Center, Kerman University of Medical Sciences, Kerman, Iran

9 Department of Toxicology and Pharmacology, Faculty of Pharmacy, Kerman University of Medical Sciences, Kerman, Iran

Abstract

Pulmonary fibrosis (PF) is the end stage of severe lung diseases, in which the lung parenchyma is replaced by fibrous scar tissue. The result is a remarkable reduction in pulmonary compliance, which may lead to respiratory failure and even death. Idiopathic pulmonary fibrosis (IPF) is the most prevalent form of PF, with no reasonable etiology. However, some factors are believed to be behind the etiology of PF, including prolonged administration of several medications (e.g., bleomycin and amiodarone), environmental contaminant exposure (e.g., gases, asbestos, and silica), and certain systemic diseases (e.g., systemic lupus erythematosus). Despite significant developments in the diagnostic approach to PF in the last few years, efforts to find more effective treatments remain challenging. With their immunomodulatory, anti-inflammatory, and anti-fibrotic properties, stem cells may provide a promising approach for treating a broad spectrum of fibrotic conditions. However, they may lose their biological functions after long-term in vitro culture or exposure to harsh in vivo situations. To overcome these limitations, numerous modification techniques, such as genetic modification, preconditioning, and optimization of cultivation methods for stem cell therapy, have been adopted. Herein, we summarize the previous investigations that have been designed to assess the effects of stem cell preconditioning or genetic modification on the regenerative capacity of stem cells in PF.

Keywords

Main Subjects

References

1. Wuyts WA, Agostini C, Antoniou KM, Bouros D, Chambers R, et al. The pathogenesis of pulmonary fibrosis: a moving target. Eur Respir J 2013; 41:1207-1218.
2. Xu J, Li L, Xiong J, Zheng Y, Ye Q, Li Y. Cyclophosphamide combined with bone marrow mesenchymal stromal cells protects against bleomycin-induced lung fibrosis in mice. Ann  Clin Lab Sci 2015; 45:292-300.
3. Rafii R, Juarez MM, Albertson TE, Chan AL. A review of current and novel therapies for idiopathic pulmonary fibrosis. J Thorac Dis 2013; 5:48-74.
4. Ruigrok MJ, Frijlink HW, Melgert BN, Olinga P, Hinrichs WL. Gene therapy strategies for idiopathic pulmonary fibrosis: recent advances, current challenges, and future directions. Mol Ther Methods Clin Dev 2021; 20:483-496.
5. Poursalehi HR, Fekri MS, Far FS, Mandegari A, Izadi A, Mahmoodi R, et al. Early and late preventive effect of Nigella sativa on the bleomycin-induced pulmonary fibrosis in rats: an experimental study. Avicenna J Phytomed 2018; 8:263-275.
6. Javad-Mousavi SA, Hemmati AA, Mehrzadi S, Hosseinzadeh A, Houshmand G, Nooshabadi MRR, et al. Protective effect of berberis vulgaris fruit extract against paraquat-induced pulmonary fibrosis in rats. Biomed Pharmacother 2016; 81:329-336.
7. Mehrabani M, Goudarzi M, Mehrzadi S, Siahpoosh A, Mohammadi M, Khalili H, et al. Crocin: a protective natural antioxidant against pulmonary fibrosis induced by bleomycin. Pharmacol Rep 2020; 72:992-1001.
8. Samareh Fekri M, Mandegary A, Sharififar F, Poursalehi HR, Nematollahi MH, Izadi A, et al. Protective effect of standardized extract of Myrtus communis L. (myrtle) on experimentally bleomycin-induced pulmonary fibrosis: biochemical and histopathological study. Drug Chem Toxicol 2018; 41:408-414.
9. Samareh-Fekri M, Poursalehi H-R, Mandegary A, Sharififar F, Mahmoudi R, Izadi A, et al. The effect of methanol extract of fennel on bleomycin-induced pulmonary fibrosis in rats. J Kerman Univ Medical Sci 2015; 22:470-483.
10. Mehrzadi S, Hosseini P, Mehrabani M, Siahpoosh A, Goudarzi M, Khalili H, et al. Attenuation of bleomycin-induced pulmonary fibrosis in Wistar rats by combination treatment of two natural phenolic compounds: quercetin and gallic acid. Nutr Cancer 2021; 73:2039-2049.
11. McNulty K, Janes SM. Stem cells and pulmonary fibrosis: cause or cure? Proc Am Thorac Soc 2012; 9:164-171.
12. Ortiz LA, DuTreil M, Fattman C, Pandey AC, Torres G, Go K, et al. Interleukin 1 receptor antagonist mediates the antiinflammatory and antifibrotic effect of mesenchymal stem cells during lung injury. Proc Natl Acad Sci U S A 2007; 104:11002-11007.
13. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci 2003; 100:8407-8411.
14. Kumamoto M, Nishiwaki T, Matsuo N, Kimura H, Matsushima K. Minimally cultured bone marrow mesenchymal stem cells ameliorate fibrotic lung injury. Eur Respir J 2009; 34:740-748.
15. Epperly MW, Guo H, Gretton JE, Greenberger JS. Bone marrow origin of myofibroblasts in irradiation pulmonary fibrosis. Am J Respir Cell Mol Biol 2003; 29:213-224.
16. Zakrzewski W, Dobrzyński M, Szymonowicz M, Rybak Z. Stem cells: past, present, and future. Stem Cell Res Ther 2019; 10:1-22.
17. Wu R, Hu X, Wang Ja. Concise review: optimized strategies for stem cell‐based therapy in myocardial repair: clinical translatability and potential limitation. Stem Cells 2018; 36:482-500.
18. Mirzamohammadi S, Mehrabani M, Tekiyehmaroof N, Sharifi A. Protective effect of 17β-estradiol on serum deprivation-induced apoptosis and oxidative stress in bone marrow-derived mesenchymal stem cells. Hum Exp Toxicol 2016; 35:312-322.
19. Bahrampour Juybari K, Kamarul T, Najafi M, Jafari D, Sharifi AM. Restoring the IL-1β/NF-κB-induced impaired chondrogenesis by diallyl disulfide in human adipose-derived mesenchymal stem cells via attenuation of reactive oxygen species and elevation of antioxidant enzymes. Cell Tissue Res 2018; 373:407-419.
20. Safari S, Eidi A, Mehrabani M, Fatemi MJ, Sharifi AM. Conditioned medium of adipose-derived mesenchymal stem cells as a promising candidate to protect high glucose-induced injury in cultured C28I2 chondrocytes. Adv Pharm Bull 2022; 12:632-640.
21. Putri WE, Endaryanto A, Rantam FA, Prakoeswa CRS. Mesenchymal stem cells-conditioned medium (secretome) in skin aging: a systematic review. Int J Pharm Res 2019; 13:613-635.
22. Mirzamohammadi S, Aali E, Najafi R, Kamarul T, Mehrabani M, Aminzadeh A, et al. Effect of 17β-estradiol on mediators involved in mesenchymal stromal cell trafficking in cell therapy of diabetes. Cytotherapy 2015; 17:46-57.
23. Herberts CA, Kwa MS, Hermsen HP. Risk factors in the development of stem cell therapy. J Transl Med 2011; 9:1-14.
24. Juybari KB, Pourhanifeh MH, Hosseinzadeh A, Hemati K, Mehrzadi S. Melatonin potentials against viral infections including COVID-19: current evidence and new findings. Virus Res 2020; 287:198108-198121.
25. Najar M, Bouhtit F, Melki R, Afif H, Hamal A, Fahmi H, et al. Mesenchymal stromal cell-based therapy: new perspectives and challenges. J Clin Med 2019; 8:626-634.
26. Aminzadeh A, Maroof NT, Mehrabani M, Juybari KB, Sharifi AM. Investigating the alterations of oxidative stress status, antioxidant defense mechanisms, MAP kinase and mitochondrial apoptotic pathway in adipose-derived mesenchymal stem cells from STZ diabetic rats. Cell J 2020; 22:38-48.
27. Wang Y, Zhang Z, Chi Y, Zhang Q, Xu F, Yang Z, et al. Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation. Cell Death Dis 2013; 4:950-961.
28. Robey TE, Saiget MK, Reinecke H, Murry CE. Systems approaches to preventing transplanted cell death in cardiac repair. J Mol Cell Cardiol 2008; 45:567-581.
29. Hu C, Li L. Preconditioning influences mesenchymal stem cell properties in vitro and in vivo. J Cell Mol Med 2018; 22:1428-1442.
30. Shafiq M, Jung Y, Kim SH. Insight on stem cell preconditioning and instructive biomaterials to enhance cell adhesion, retention, and engraftment for tissue repair. Biomaterials 2016; 90:85-115.
31. Moeinabadi-Bidgoli K, Babajani A, Yazdanpanah G, Farhadihosseinabadi B, Jamshidi E, Bahrami S, et al. Translational insights into stem cell preconditioning: from molecular mechanisms to preclinical applications. Biomed Pharmacother 2021; 142:112026-112044.
32. Averyanov A, Koroleva I, Konoplyannikov M, Revkova V, Lesnyak V, Kalsin V, et al. First-in-human high-cumulative-dose stem cell therapy in idiopathic pulmonary fibrosis with rapid lung function decline. Stem Cells Transl Med 2020; 9:6-16.
33. Campo A, González-Ruiz JM, Andreu E, Alcaide AB, Ocón MM, De-Torres J, et al. Endobronchial autologous bone marrow–mesenchymal stromal cells in idiopathic pulmonary fibrosis: a phase I trial. ERJ Open Res 2021; 7:1-12.
34. Glassberg MK, Minkiewicz J, Toonkel RL, Simonet ES, Rubio GA, DiFede D, et al. Allogeneic human mesenchymal stem cells in patients with idiopathic pulmonary fibrosis via intravenous delivery (AETHER): a phase I safety clinical trial. Chest 2017; 151:971-981.
35. Tzouvelekis A, Paspaliaris V, Koliakos G, Ntolios P, Bouros E, Oikonomou A, et al. A prospective, non-randomized, no placebo-controlled, phase Ib clinical trial to study the safety of the adipose derived stromal cells-stromal vascular fraction in idiopathic pulmonary fibrosis. J Transl Med 2013; 11:1-13.
36. Liu W, Wang H, Yu W, Bi X, Chen J, Chen L, et al. Teatment of silicosis with hepatocyte growth factor-modified autologous bone marrow stromal cells: a non-randomized study with follow-up. Genet Mol Res 2015; 14:10672-10681.
37. Wu J, Zhou X, Tan Y, Wang L, Li T, Li Z, et al. Phase 1 trial for treatment of COVID‐19 patients with pulmonary fibrosis using hESC‐IMRCs. Cell Prolif 2020; 53:12944-12947.
38. Chambers DC, Enever D, Ilic N, Sparks L, Whitelaw K, Ayres J, et al. A phase 1b study of placenta‐derived mesenchymal stromal cells in patients with idiopathic pulmonary fibrosis. Respirology 2014; 19:1013-1018.
39. Kim SH, Moon H-H, Kim HA, Hwang K-C, Lee M, Choi D. Hypoxia-inducible vascular endothelial growth factor-engineered mesenchymal stem cells prevent myocardial ischemic injury. Mol Ther 2011; 19:741-750.
40. Cheng Z, Ou L, Zhou X, Li F, Jia X, Zhang Y, et al. Targeted migration of mesenchymal stem cells modified with CXCR4 gene to infarcted myocardium improves cardiac performance. Mol Ther 2008; 16:571-579.
41. Borden BA, Yockman J, Kim SW. Thermoresponsive hydrogel as a delivery scaffold for transfected rat mesenchymal stem cells. Mol pharm 2010; 7:963-968.
42. Yang S, Liu P, Jiang Y, Wang Z, Dai H, Wang C. Therapeutic applications of mesenchymal stem cells in idiopathic pulmonary fibrosis. Front Cell Dev Biol 2021; 9:477-490.
43. Marofi F, Vahedi G, Biglari A, Esmaeilzadeh A, Athari SS. Mesenchymal stromal/stem cells: a new era in the cell-based targeted gene therapy of cancer. Front Immunol 2017; 8:1770-1786.
44. Shahror RA, Wu C-C, Chiang Y-H, Chen K-Y. Genetically modified mesenchymal stem cells: the next generation of stem cell-based therapy for TBI. Int J Mol Sci 2020; 21:4051-4068.
45. Schäfer R, Spohn G, Baer PC. Mesenchymal stem/stromal cells in regenerative medicine: can preconditioning strategies improve therapeutic efficacy. Transfus Med Hemother 2016; 43:256-267.
46. Li X, An G, Wang Y, Liang D, Zhu Z, Lian X, et al. Anti-fibrotic effects of bone morphogenetic protein-7-modified bone marrow mesenchymal stem cells on silica-induced pulmonary fibrosis. Exp Mol Pathol 2017; 102:70-77.
47. Manson SR, Song JB, Hruska KA, Austin PF. HDAC dependent transcriptional repression of Bmp-7 potentiates TGF-β mediated renal fibrosis in obstructive uropathy. J Urol 2014; 191:242-252.
48. Wang L-P, Dong J-Z, Xiong L-J, Shi K-Q, Zou Z-L, Zhang S-N, et al. BMP-7 attenuates liver fibrosis via regulation of epidermal growth factor receptor. Int J Clin Exp Pathol 2014; 7:3537-3547.
49. Urbina P, Singla DK. BMP-7 attenuates adverse cardiac remodeling mediated through M2 macrophages in prediabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 2014; 307:762-772.
50. Grimminger F, Günther A, Vancheri C. The role of tyrosine kinases in the pathogenesis of idiopathic pulmonary fibrosis. Eur Respir J 2015; 45:1426-1433.
51. Ono M, Ohkouchi S, Kanehira M, Tode N, Kobayashi M, Ebina M, et al. Mesenchymal stem cells correct inappropriate epithelial–mesenchyme relation in pulmonary fibrosis using stanniocalcin-1. Mol Ther 2015; 23:549-560.
52. Marshall RP, Gohlke P, Chambers RC, Howell DC, Bottoms SE, Unger T, et al. Angiotensin II and the fibroproliferative response to acute lung injury. Am J Physiol Lung Cell Mol Physiol 2004 ;286:156-164.
53. Imai Y, Kuba K, Rao S, Huan Y, Guo F, Guan B, et al. Angiotensin-converting enzyme 2 protects from severe acute lung failure. Nature 2005; 436:112-116.
54. Min F, Gao F, Li Q, Liu Z. Therapeutic effect of human umbilical cord mesenchymal stem cells modified by angiotensin-converting enzyme 2 gene on bleomycin-induced lung fibrosis injury. Mol Med Rep 2015; 11:2387-2396.
55. Liu D, Kong F, Yuan Y, Seth P, Xu W, Wang H, et al.  Decorin-modified umbilical cord mesenchymal stem cells (MSCs) attenuate radiation-induced lung injuries via regulating inflammation, fibrotic factors, and immune responses. Int J Radiat Oncol Biol Phys 2018; 101:945-956.
56. Rojas M, Xu J, Woods CR, Mora AL, Spears W, Roman J, et al. Bone marrow–derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005; 33:145-152.
57. Ishizawa K, Kubo H, Yamada M, Kobayashi S, Numasaki M, Ueda S, et al. Bone marrow‐derived cells contribute to lung regeneration after elastase‐induced pulmonary emphysema. FEBS Lett 2004; 556:249-252.
58. Gazdhar A, Susuri N, Hostettler K, Gugger M, Knudsen L, Roth M, et al. HGF expressing stem cells in usual interstitial pneumonia originate from the bone marrow and are antifibrotic. PLoS One 2013; 8:65453-65466.
59. Cahill EF, Kennelly H, Carty F, Mahon BP, English K. Hepatocyte growth factor is required for mesenchymal stromal cell protection against bleomycin‐induced pulmonary fibrosis. Stem Cells Transl Med 2016; 5:1307-1318.
60. Li X, Wang Y, An G, Liang D, Zhu Z, Lian X, et al. Bone marrow mesenchymal stem cells attenuate silica-induced pulmonary fibrosis via paracrine mechanisms. Toxicol Lett 2017; 270:96-107.
61. Lan Y-W, Theng S-M, Huang T-T, Choo K-B, Chen C-M, Kuo H-P, et al. Oncostatin M-preconditioned mesenchymal stem cells alleviate bleomycin-induced pulmonary fibrosis through paracrine effects of the hepatocyte growth factor. Stem Cells Transl Med 2017; 6:1006-1017.
62. Morikawa O, Walker TA, Nielsen LD, Pan T, Cook JL, Mason RJ. Effect of adenovector-mediated gene transfer of keratinocyte growth factor on the proliferation of alveolar type II cells in vitro and in vivo. Am J Respir Cell Mol Biol 2000; 23:626-635.
63. Xie T, Liang J, Geng Y, Liu N, Kurkciyan A, Kulur V, et al. MicroRNA-29c prevents pulmonary fibrosis by regulating epithelial cell renewal and apoptosis. Am J Respir Cell Mol Biol 2017; 57:721-732.
64. Aguilar S, Scotton CJ, McNulty K, Nye E, Stamp G, Laurent G, et al. Bone marrow stem cells expressing keratinocyte growth factor via an inducible lentivirus protects against bleomycin-induced pulmonary fibrosis. PloS One 2009; 4:8013-8026.
65. Han J, Liu Y, Liu H, Li Y. Genetically modified mesenchymal stem cell therapy for acute respiratory distress syndrome. Stem Cell Res Ther 2019; 10:1-9.
66. Kwon O-S, Kim K-T, Lee E, Kim M, Choi S-H, Li H, et al. Induction of MiR-21 by stereotactic body radiotherapy contributes to the pulmonary fibrotic response. PLoS One 2016; 11:1-16.
67. Roderburg C, Luedde T. Circulating microRNAs as markers of liver inflammation, fibrosis and cancer. J Hepatol 2014; 61:1434-1437.
68. Chen K, Boettiger A, Moffitt J, Wang S, Zhuang X. RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 2015; 348:1-36.
69. Li Q, Zhang D, Wang Y, Sun P, Hou X, Larner J, et al. MiR-21/Smad 7 signaling determines TGF-β1-induced CAF formation. Sci Rep 2013; 3:1-9.
70. Li P, Li J, Chen T, Wang H, Chu H, Chang J, et al. Expression analysis of serum microRNAs in idiopathic pulmonary fibrosis. Int J Mol Med 2014; 33:1554-1562.
71. Xie T, Liang J, Guo R, Liu N, Noble PW, Jiang D. Comprehensive microRNA analysis in bleomycin-induced pulmonary fibrosis identifies multiple sites of molecular regulation. Physiol Genomics 2011; 43:479-487.
72. Maltby S, Plank M, Tay HL, Collison A, Foster PS. Targeting microRNA function in respiratory diseases: mini-review. Front Physiol 2016; 7:21-31.
73. Liu G, Friggeri A, Yang Y, Milosevic J, Ding Q, Thannickal VJ, et al. MiR-21 mediates fibrogenic activation of pulmonary fibroblasts and lung fibrosis. J Exp Med 2010; 207:1589-1597.
74. Wang C, Gu S, Cao H, Li Z, Xiang Z, Hu K, et al. MiR-877-3p targets Smad7 and is associated with myofibroblast differentiation and bleomycin-induced lung fibrosis. Sci Rep 2016; 6:1-11.
75. Pottier N, Maurin T, Chevalier B, Puisségur M-P, Lebrigand K, Robbe-Sermesant K, et al. Identification of keratinocyte growth factor as a target of microRNA-155 in lung fibroblasts: implication in epithelial-mesenchymal interactions. PloS One 2009; 4:6718-6734.
76. Yang S, Banerjee S, de Freitas A, Sanders YY, Ding Q, Matalon S, et al. Participation of miR-200 in pulmonary fibrosis. Am J Pathol 2012; 180:484-493.
77. Liang H, Xu C, Pan Z, Zhang Y, Xu Z, Chen Y, et al.  The antifibrotic effects and mechanisms of microRNA-26a action in idiopathic pulmonary fibrosis. Mol Ther 2014; 22:1122-1133.
78. Ji X, Wu B, Fan J, Han R, Luo C, Wang T, et al. The anti-fibrotic effects and mechanisms of microRNA-486-5p in pulmonary fibrosis. Sci Rep 2015; 5:1-12.
79. Huleihel L, Sellares J, Cardenes N, Álvarez D, Faner R, Sakamoto K, et al. Modified mesenchymal stem cells using miRNA transduction alter lung injury in a bleomycin model. Am J Physiol Lung Cell Mol Physiol 2017; 313:92-103.
80. Chen X, Shi C, Wang C, Liu W, Chu Y, Xiang Z, et al. The role of miR-497-5p in myofibroblast differentiation of LR-MSCs and pulmonary fibrogenesis. Sci Rep 2017; 7:1-13.
81. Shi L, Han Q, Hong Y, Li W, Gong G, Cui J, et al. Inhibition of miR-199a-5p rejuvenates aged mesenchymal stem cells derived from patients with idiopathic pulmonary fibrosis and improves their therapeutic efficacy in experimental pulmonary fibrosis. Stem Cell Res Ther 2021; 12:1-17.
82. Laganà A, Veneziano D, Russo F, Pulvirenti A, Giugno R, Croce CM, et al. Computational design of artificial RNA molecules for gene regulation. Methods Mol Biol 2015; 1269:393-412.
83. Monga I, Qureshi A, Thakur N, Gupta AK, Kumar M. ASPsiRNA: a resource of ASP-siRNAs having therapeutic potential for human genetic disorders and algorithm for prediction of their inhibitory efficacy. G3 (Bethesda) 2017; 7:2931-2943.
84. Fernandes F, Kotharkar P, Chakravorty A, Kowshik M, Talukdar I. Nanocarrier mediated siRNA delivery targeting stem cell differentiation. Curr Stem Cell Res Ther 2020; 15:155-172.
85. Hou J, Ji Q, Ji J, Ju S, Xu C, Yong X, et al. Co-delivery of siPTPN13 and siNOX4 via (myo) fibroblast-targeting polymeric micelles for idiopathic pulmonary fibrosis therapy. Theranostics 2021; 11:3244-3261.
86. Williford J-M, Wu J, Ren Y, Archang MM, Leong KW, Mao H-Q. Recent advances in nanoparticle-mediated siRNA delivery. Ann Rev Biomed Eng 2014; 16:347-370.
87. Tsai L-R, Chen M-H, Chien C-T, Chen M-K, Lin F-S, Lin KM-C, et al. A single-monomer derived linear-like PEI-co-PEG for siRNA delivery and silencing. Biomaterials 2011; 32:3647-3653.
88. Feng L, Yang X, Shi X, Tan X, Peng R, Wang J, et al. Polyethylene glycol and polyethylenimine dual‐functionalized nano‐graphene oxide for photothermally enhanced gene delivery. Small 2013; 9:1989-1997.
89. Ji Q, Hou J, Yong X, Gong G, Muddassir M, Tang T, et al. Targeted dual small interfering ribonucleic acid delivery via non‐viral polymeric vectors for pulmonary fibrosis therapy. Adv Mater 2021; 33:1-12.
90. Chen X, Shi C, Cao H, Chen L, Hou J, Xiang Z, et al. The hedgehog and Wnt/β-catenin system machinery mediate myofibroblast differentiation of LR-MSCs in pulmonary fibrogenesis. Cell Death Dis 2018; 9:639-654.
91. Shi C, Chen X, Yin W, Sun Z, Hou J, Han X. Wnt8b regulates myofibroblast differentiation of lung-resident mesenchymal stem cells via the activation of Wnt/β-catenin signaling in pulmonary fibrogenesis. Differentiation 2022; 125:35-44.
92. Wu G, Chang F, Fang H, Zheng X, Zhuang M, Liu X, et al. Non-muscle myosin II knockdown improves survival and therapeutic effects of implanted bone marrow-derived mesenchymal stem cells in lipopolysaccharide-induced acute lung injury. Ann Transl Med 2021; 9:262-273.
93. Saparov A, Ogay V, Nurgozhin T, Jumabay M, Chen WC. Preconditioning of human mesenchymal stem cells to enhance their regulation of the immune response. Stem Cells Int 2016; 2016:1-10.
94. Mehrabani M, Najafi M, Kamarul T, Mansouri K, Iranpour M, Nematollahi M, et al. Deferoxamine preconditioning to restore impaired HIF‐1α‐mediated angiogenic mechanisms in adipose‐derived stem cells from STZ‐induced type 1 diabetic rats. Cell Prolif 2015; 48:532-549.
95. Haider HK, Ashraf M. Preconditioning and stem cell survival. J Cardiovasc Transl Res 2010; 3:89-102.
96. Francis K, Wei L. Human embryonic stem cell neural differentiation and enhanced cell survival promoted by hypoxic preconditioning. Cell Death Dis 2010; 1:22-22.
97. Takeda K, Ning F, Domenico J, Okamoto M, Ashino S, Kim SH, et al. Activation of p70S6 kinase-1 in mesenchymal stem cells is essential to lung tissue repair. Stem Cells Transl Med 2018; 7:551-558.
98. Wang H, Yang YF, Zhao L, Xiao FJ, Zhang QW, Wen ML, et al. Hepatocyte growth factor gene-modified mesenchymal stem cells reduce radiation-induced lung injury. Hum Gene Ther 2013; 24:343-353.
99. Petrella F, Coccè V, Masia C, Milani M, Salè EO, Alessandri G, et al. Paclitaxel-releasing mesenchymal stromal cells inhibit in vitro proliferation of human mesothelioma cells. Biomed Pharmacother. 2017; 87:755-758.
100. Horie S, Gaynard S, Murphy M, Barry F, Scully M, O’Toole D, et al. Cytokine pre-activation of cryopreserved xenogeneic-free human mesenchymal stromal cells enhances resolution and repair following ventilator-induced lung injury potentially via a KGF-dependent mechanism. Intensive Care Med Exp 2020; 8:8-23.
101. Li D, Liu Q, Qi L, Dai X, Liu H, Wang Y. Low levels of TGF-β1 enhance human umbilical cord-derived mesenchymal stem cell fibronectin production and extend survival time in a rat model of lipopolysaccharide-induced acute lung injury. Mol Med Rep 2016; 14:1681-1692.
102. Antebi B, Rodriguez LA, Walker KP, Asher AM, Kamucheka RM, Alvarado L, et al. Short-term physiological hypoxia potentiates the therapeutic function of mesenchymal stem cells. Stem Cell Res Ther 2018; 9:1-15.
103. Zhang W, Liu L, Huo Y, Yang Y, Wang Y. Hypoxia-pretreated human MSCs attenuate acute kidney injury through enhanced angiogenic and antioxidative capacities. Biomed Res Int 2014; 2014:1-10.
104. Hu X, Yu SP, Fraser JL, Lu Z, Ogle ME, Wang JA, et al. 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.
105. Theus MH, Wei L, Cui L, Francis K, Hu X, Keogh C, et al. In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol 2008; 210:656-670.
106. Jaussaud J, Biais M, Calderon J, Chevaleyre J, Duchez P, Ivanovic Z, et al. Hypoxia-preconditioned mesenchymal stromal cells improve cardiac function in a swine model of chronic myocardial ischaemia. Eur J Cardiothorac Surg 2013; 43:1050-1057.
107. Chang CP, Chio CC, Cheong CU, Chao CM, Cheng BC, Lin MT. Hypoxic preconditioning enhances the therapeutic potential of the secretome from cultured human mesenchymal stem cells in experimental traumatic brain injury. Clin Sci (Lond) 2013; 124:165-176.
108. Mottaghi S, Larijani B, Sharifi AM. Apelin 13: a novel approach to enhance efficacy of hypoxic preconditioned mesenchymal stem cells for cell therapy of diabetes. Med Hypotheses 2012; 79:717-718.
109. Yu J, Yin S, Zhang W, Gao F, Liu Y, Chen Z, et al. Hypoxia preconditioned bone marrow mesenchymal stem cells promote liver regeneration in a rat massive hepatectomy model. Stem Cell Res Ther 2013; 4:83-92.
110. Tsai C-C, Yew T-L, Yang D-C, Huang W-H, Hung S-C. Benefits of hypoxic culture on bone marrow multipotent stromal cells. Am J Blood Res 2012; 2:148-159.
111. Liu L, Gao J, Yuan Y, Chang Q, Liao Y, Lu F. Hypoxia preconditioned human adipose derived mesenchymal stem cells enhance angiogenic potential via secretion of increased VEGF and bFGF. Cell Biol Int 2013; 37:551-560.
112. McLaren AT, Marsden PA, Mazer CD, Baker AJ, Stewart DJ, Tsui AK, et al. Increased expression of HIF-1α, nNOS, and VEGF in the cerebral cortex of anemic rats. Am J Physiol Regul Integr Comp Physiol 2007; 292:403-414.
113. Mehrabani M, Nematollahi MH, Tarzi ME, Juybari KB, Abolhassani M, Sharifi AM, et al. Protective effect of hydralazine on a cellular model of Parkinson’s disease: a possible role of hypoxia-inducible factor (HIF)-1α. Biochem Cell Biol 2020; 98:405-414.
114. McGettrick AF, O’Neill LA. The role of HIF in immunity and inflammation. Cell Metab 2020; 32:524-536.
115. Fábián Z. The effects of hypoxia on the immune-modulatory properties of bone marrow-derived mesenchymal stromal cells. Stem Cells Int 2019; 2019:1-13.
116. Liu YY, Chiang CH, Hung SC, Chian CF, Tsai CL, Chen WC, et al.  Hypoxia-preconditioned mesenchymal stem cells ameliorate ischemia/reperfusion-induced lung injury. PLoS One 2017; 12:1-20.
117. Lan YW, Choo KB, Chen CM, Hung TH, Chen YB, Hsieh CH, et al. Hypoxia-preconditioned mesenchymal stem cells attenuate bleomycin-induced pulmonary fibrosis. Stem Cell Res Ther 2015; 6:97-114.
118. Kitajima Y, Ide T, Ohtsuka T, Miyazaki K. Induction of hepatocyte growth factor activator gene expression under hypoxia activates the hepatocyte growth factor/c‐Met system via hypoxia inducible factor‐1 in pancreatic cancer. Cancer Sci 2008; 99:1341-1347.
119. Lan YW, Theng SM, Huang TT, Choo KB, Chen CM, Kuo HP, et al. Oncostatin M‐preconditioned mesenchymal stem cells alleviate bleomycin‐induced pulmonary fibrosis through paracrine effects of the hepatocyte growth factor. Stem Cells Transl Med 2017; 6:1006-1017.
120. Zhao F, Liu W, Yue S, Yang L, Hua Q, Zhou Y, et al. Pretreatment with G-CSF could enhance the antifibrotic effect of BM-MSCs on pulmonary fibrosis. Stem Cells Int 2019; 2019:1-13.
121. Zhao FY, Cheng TY, Yang L, Huang YH, Li C, Han JZ, et al. G-CSF inhibits pulmonary fibrosis by promoting BMSC homing to the lungs via SDF-1/CXCR4 chemotaxis. Sci Rep 2020; 10:10515-10526.
122. Rozier P, Maumus M, Maria ATJ, Toupet K, Jorgensen C, Guilpain P, et al. Lung fibrosis is improved by extracellular vesicles from IFNγ-primed mesenchymal stromal cells in murine systemic sclerosis. Cells 2021; 10:2727-2743.
123. Ryan J, Barry F, Murphy J, Mahon BP. Interferon-γ does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 2007; 149:353-363.
124. Sheng H, Wang Y, Jin Y, Zhang Q, Zhang Y, Wang L, et al. A critical role of IFNγ in priming MSC-mediated suppression of T cell proliferation through up-regulation of B7-H1. Cell Res 2008; 18:846-857.
125. Yao L, Liu Cj, Luo Q, Gong M, Chen J, Wang LJ, et al. Protection against hyperoxia‐induced lung fibrosis by KGF‐induced MSC s mobilization in neonatal rats. Pediatr Transplant 2013; 17:676-682.
126. Wang Q, Shen C, Zhu H, Zhou W-G, Guo X-C, Wu M-J, et al. N-acetylcysteine-pretreated human embryonic mesenchymal stem cell administration protects against bleomycin-induced lung injury. Am J Med Sci 2013; 346:113-122.
127. Mahmoudi T, Abdolmohammadi K, Bashiri H, Mohammadi M, Rezaie MJ, Fathi F, et al. Hydrogen peroxide preconditioning promotes protective effects of umbilical cord vein mesenchymal stem cells in experimental pulmonary fibrosis. Adv Pharm Bull 2020; 10:72-80.
128. Dave A, Kar S, Banerjee ER. Effect of CoCl2 or H2O2 pre-conditioned mesenchymal stem cells in a mouse model of pulmonary fibrosis. Biomed Res Ther 2018; 5:2208-2222.
129. Peng X, Li X, Li C, Yue S, Huang Y, Huang P, et al. NMDA receptor activation inhibits the protective effect of BMMSCs on bleomycininduced lung epithelial cell damage by inhibiting ERK signaling and the paracrine factor HGF. Int J Mol Med 2019; 44:227-239.
130. Li X, Li C, Tang Y, Huang Y, Cheng Q, Huang X, et al. NMDA receptor activation inhibits the antifibrotic effect of BM-MSCs on bleomycin-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2018; 315:404-421.
Iranian Journal of Basic Medical Sciences
Volume 26, Issue 9
September 2023
Pages 1001-1015

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