Role of aryl hydrocarbon receptor in mesenchymal stromal cell activation: A minireview

World Journal of Stem Cells

Volumn 9, Issue 9, 2017, Pages 152-158

  de Almeida, Danilo Candido ^a   Evangelista, Laura Sibele Martins ^a   Cămara, Niels Olsen Saraiva ^b  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Aryl hydrocarbon receptor; Cell activation and immunosuppression; Mesenchymal stromal cells

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR;

CELL ACTIVATION; CELL PROTECTION; CYTOKINE PRODUCTION; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; MESENCHYMAL STROMA CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SHORT SURVEY;

EID: 85041730611     PISSN: None     EISSN: 19480210     Source Type: Journal    
DOI: 10.4252/wjsc.v9.i9.152     Document Type: Short Survey

References (55)

1. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968; 6: 230-247 [PMID: 5654088]
2. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991; 9: 641-650 [PMID: 1870029 DOI: 10.1002/jor.1100090504]
3. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8: 315-317 [PMID: 16923606 DOI: 10.1080/1465 3240600855905]
4. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006; 119: 2204-2213 [PMID: 16684817 DOI: 10.1242/jcs.02932]
5. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Péault B. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 2008; 3: 301-313 [PMID: 18786417 DOI: 10.1016/j.stem.2008.07.003]
6. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-147 [PMID: 10102814]
7. Covas DT, Siufi JL, Silva AR, Orellana MD. Isolation and culture of umbilical vein mesenchymal stem cells. Braz J Med Biol Res 2003; 36: 1179-1183 [PMID: 12937783]
8. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001; 7: 211-228 [PMID: 11304456 DOI: 10.1089/107632701300062859]
9. de Almeida DC, Donizetti-Oliveira C, Barbosa-Costa P, Origassa CS, Câmara NO. In search of mechanisms associated with mesenchymal stem cell-based therapies for acute kidney injury. Clin Biochem Rev 2013; 34: 131-144 [PMID: 24353358]
10. Camussi G, Deregibus MC, Tetta C. Paracrine/endocrine mechanism of stem cells on kidney repair: role of microvesicle-mediated transfer of genetic information. Curr Opin Nephrol Hypertens 2010; 19: 7-12 [PMID: 19823086 DOI: 10.1097/MNH.0b013e328332fb6f]
11. de Almeida DC, Bassi ÊJ, Azevedo H, Anderson L, Origassa CS, Cenedeze MA, de Andrade-Oliveira V, Felizardo RJ, da Silva RC, Hiyane MI, Semedo P, Dos Reis MA, Moreira-Filho CA, Verjovski-Almeida S, Pacheco-Silva Á, Câmara NO. A Regulatory miRNA-mRNA Network Is Associated with Tissue Repair Induced by Mesenchymal Stromal Cells in Acute Kidney Injury. Front Immunol 2017; 7: 645 [PMID: 28096802 DOI: 10.3389/fimmu.2016.00645]
12. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, Mancardi G, Uccelli A. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005; 106: 1755-1761 [PMID: 15905186 DOI: 10.1182/blood-2005-04-1496]
13. Ortiz LA, Gambelli F, McBride C, Gaupp D, Baddoo M, Kaminski N, Phinney DG. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 2003; 100: 8407-8411 [PMID: 12815096 DOI: 10.1073/pnas.1432929100]
14. Semedo P, Correa-Costa M, Antonio Cenedeze M, Maria Avancini Costa Malheiros D, Antonia dos Reis M, Shimizu MH, Seguro AC, Pacheco-Silva A, Saraiva Camara NO. Mesenchymal stem cells attenuate renal fibrosis through immune modulation and remodeling properties in a rat remnant kidney model. Stem Cells 2009; 27: 3063-3073 [PMID: 19750536 DOI: 10.1002/stem.214]
15. Martire A, Bedada FB, Uchida S, Pöling J, Krüger M, Warnecke H, Richter M, Kubin T, Herold S, Braun T. Mesenchymal stem cells attenuate inflammatory processes in the heart and lung via inhibition of TNF signaling. Basic Res Cardiol 2016; 111: 54 [PMID: 27435289 DOI: 10.1007/s00395-016-0573-2]
16. Ciccocioppo R, Bernardo ME, Sgarella A, Maccario R, Avanzini MA, Ubezio C, Minelli A, Alvisi C, Vanoli A, Calliada F, Dionigi P, Perotti C, Locatelli F, Corazza GR. Autologous bone marrow-derived mesenchymal stromal cells in the treatment of fistulising Crohn's disease. Gut 2011; 60: 788-798 [PMID: 21257987 DOI: 10.1136/gut.2010.214841]
17. Tang Y, Chen Y, Wang X, Song G, Li Y, Shi L. Combinatorial Intervention with Mesenchymal Stem Cells and Granulocyte Colony-Stimulating Factor in a Rat Model of Ulcerative Colitis. Dig Dis Sci 2015; 60: 1948-1957 [PMID: 25894931 DOI: 10.1007/s10620-015-3655-3]
18. Muroi K, Miyamura K, Ohashi K, Murata M, Eto T, Kobayashi N, Taniguchi S, Imamura M, Ando K, Kato S, Mori T, Teshima T, Mori M, Ozawa K. Unrelated allogeneic bone marrow-derived mesenchymal stem cells for steroid-refractory acute graft-versus-host disease: a phase I/II study. Int J Hematol 2013; 98: 206-213 [PMID: 23860964 DOI: 10.1007/s12185-013-1399-4]
19. Cortinovis M, Casiraghi F, Remuzzi G, Perico N. Mesenchymal stromal cells to control donor-specific memory T cells in solid organ transplantation. Curr Opin Organ Transplant 2015; 20: 79-85 [PMID: 25563995 DOI: 10.1097/MOT.0000000000000145]
20. Keating A. Mesenchymal stromal cells: new directions. Cell Stem Cell 2012; 10: 709-716 [PMID: 22704511 DOI: 10.1016/j.stem.2012.05.015]
21. Lee MW, Ryu S, Kim DS, Sung KW, Koo HH, Yoo KH. Strategies to improve the immunosuppressive properties of human mesenchymal stem cells. Stem Cell Res Ther 2015; 6: 179 [PMID: 26445096 DOI: 10.1186/s13287-015-0178-y]
22. Wagner W. Senescence is heterogeneous in mesenchymal stromal cells: kaleidoscopes for cellular aging. Cell Cycle 2010; 9: 2923-2924 [PMID: 20699668 DOI: 10.4161/cc.9.15.12741]
23. Nemeth K, Mayer B, Mezey E. Modulation of bone marrow stromal cell functions in infectious diseases by toll-like receptor ligands. J Mol Med (Berl) 2010; 88: 5-10 [PMID: 19756450 DOI: 10.1007/s00109-009-0523-7]
24. Prockop DJ, Oh JY. Mesenchymal stem/stromal cells (MSCs): role as guardians of inflammation. Mol Ther 2012; 20: 14-20 [PMID: 22008910 DOI: 10.1038/mt.2011.211]
25. Polchert D, Sobinsky J, Douglas G, Kidd M, Moadsiri A, Reina E, Genrich K, Mehrotra S, Setty S, Smith B, Bartholomew A. IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol 2008; 38: 1745-1755 [PMID: 18493986 DOI: 10.1002/eji.200738129]
26. Quintana FJ, Sherr DH. Aryl hydrocarbon receptor control of adaptive immunity. Pharmacol Rev 2013; 65: 1148-1161 [PMID: 23908379 DOI: 10.1124/pr.113.007823]
27. Fardel O. Cytokines as molecular targets for aryl hydrocarbon receptor ligands: implications for toxicity and xenobiotic detoxification. Expert Opin Drug Metab Toxicol 2013; 9: 141-152 [PMID: 23230817 DOI: 10.1517/17425255.2013.738194]
28. Vogel CF, Khan EM, Leung PS, Gershwin ME, Chang WL, Wu D, Haarmann-Stemmann T, Hoffmann A, Denison MS. Cross-talk between aryl hydrocarbon receptor and the inflammatory response: a role for nuclear factor-κB. J Biol Chem 2014; 289: 1866-1875 [PMID: 24302727 DOI: 10.1074/jbc.M113.505578]
29. Denison MS, Nagy SR. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu Rev Pharmacol Toxicol 2003; 43: 309-334 [PMID: 12540743 DOI: 10.1146/annurev.pharmtox.43.100901.135828]
30. Stockinger B, Di Meglio P, Gialitakis M, Duarte JH. The aryl hydrocarbon receptor: multitasking in the immune system. Annu Rev Immunol 2014; 32: 403-432 [PMID: 24655296 DOI: 10.1146/annurev-immunol-032713-120245]
31. Allan LL, Mann KK, Matulka RA, Ryu HY, Schlezinger JJ, Sherr DH. Bone marrow stromal-B cell interactions in polycyclic aromatic hydrocarbon-induced pro/pre-B cell apoptosis. Toxicol Sci 2003; 76: 357-365 [PMID: 14514961 DOI: 10.1093/toxsci/kfg239]
32. Li XM, Peng J, Gu W, Guo XJ. TCDD-Induced Activation of Aryl Hydrocarbon Receptor Inhibits Th17 Polarization and Regulates Non-Eosinophilic Airway Inflammation in Asthma. PLoS One 2016; 11: e0150551 [PMID: 26938767 DOI: 10.1371/journal.pone.0150551]
33. Platzer B, Richter S, Kneidinger D, Waltenberger D, Woisetschläger M, Strobl H. Aryl hydrocarbon receptor activation inhibits in vitro differentiation of human monocytes and Langerhans dendritic cells. J Immunol 2009; 183: 66-74 [PMID: 19535631 DOI: 10.4049/jimmunol.0802997]
34. Vogel CF, Wu D, Goth SR, Baek J, Lollies A, Domhardt R, Grindel A, Pessah IN. Aryl hydrocarbon receptor signaling regulates NF-κB RelB activation during dendritic-cell differentiation. Immunol Cell Biol 2013; 91: 568-575 [PMID: 23999131 DOI: 10.1038/icb.2013.43]
35. Komura K, Hayashi S, Makino I, Poellinger L, Tanaka H. Aryl hydrocarbon receptor/dioxin receptor in human monocytes and macrophages. Mol Cell Biochem 2001; 226: 107-118 [PMID: 11768231]
36. Kimura A, Abe H, Tsuruta S, Chiba S, Fujii-Kuriyama Y, Sekiya T, Morita R, Yoshimura A. Aryl hydrocarbon receptor protects against bacterial infection by promoting macrophage survival and reactive oxygen species production. Int Immunol 2014; 26: 209-220 [PMID: 24343818 DOI: 10.1093/intimm/dxt067]
37. Memari B, Bouttier M, Dimitrov V, Ouellette M, Behr MA, Fritz JH, White JH. Engagement of the Aryl Hydrocarbon Receptor in Mycobacterium tuberculosis-Infected Macrophages Has Pleiotropic Effects on Innate Immune Signaling. J Immunol 2015; 195: 4479-4491 [PMID: 26416282 DOI: 10.4049/jimmunol.1501141]
38. Casado FL, Singh KP, Gasiewicz TA. Aryl hydrocarbon receptor activation in hematopoietic stem/progenitor cells alters cell function and pathway-specific gene modulation reflecting changes in cellular trafficking and migration. Mol Pharmacol 2011; 80: 673-682 [PMID: 21791576 DOI: 10.1124/mol.111.071381]
39. Unnisa Z, Singh KP, Henry EC, Donegan CL, Bennett JA, Gasiewicz TA. Aryl Hydrocarbon Receptor Deficiency in an Exon 3 Deletion Mouse Model Promotes Hematopoietic Stem Cell Proliferation and Impacts Endosteal Niche Cells. Stem Cells Int 2016; 2016: 4536187 [PMID: 27366154 DOI: 10.1155/2016/4536187]
40. Nguyen NT, Hanieh H, Nakahama T, Kishimoto T. The roles of aryl hydrocarbon receptor in immune responses. Int Immunol 2013; 25: 335-343 [PMID: 23580432 DOI: 10.1093/intimm/dxt011]
41. Yamaguchi K, Matulka RA, Shneider AM, Toselli P, Trombino AF, Yang S, Hafer LJ, Mann KK, Tao XJ, Tilly JL, Near RI, Sherr DH. Induction of PreB cell apoptosis by 7,12-dimethylbenz[a]anthracene in long-term primary murine bone marrow cultures. Toxicol Appl Pharmacol 1997; 147: 190-203 [PMID: 9439715 DOI: 10.1006/taap.1997.8263]
42. Near RI, Matulka RA, Mann KK, Gogate SU, Trombino AF, Sherr DH. Regulation of preB cell apoptosis by aryl hydrocarbon receptor/transcription factor-expressing stromal/adherent cells. Proc Soc Exp Biol Med1999; 221: 242-252 [PMID: 10404042]
43. Yamaguchi K, Near RI, Matulka RA, Shneider A, Toselli P, Trombino AF, Sherr DH. Activation of the aryl hydrocarbon receptor/transcription factor and bone marrow stromal cell-dependent preB cell apoptosis. J Immunol 1997; 158: 2165-2173 [PMID: 9036962]
44. Jensen BA, Leeman RJ, Schlezinger JJ, Sherr DH. Aryl hydrocarbon receptor (AhR) agonists suppress interleukin-6 expression by bone marrow stromal cells: an immunotoxicology study. Environ Health 2003; 2: 16 [PMID: 14678569 DOI: 10.1186/1476-069X-2-16]
45. McMurray RW, Hoffman RW, Nelson W, Walker SE. Cytokine mRNA expression in the B/W mouse model of systemic lupus erythematosus--analyses of strain, gender, and age effects. Clin Immunol Immunopathol 1997; 84: 260-268 [PMID: 9281384]
46. Nakahara H, Song J, Sugimoto M, Hagihara K, Kishimoto T, Yoshizaki K, Nishimoto N. Anti-interleukin-6 receptor antibody therapy reduces vascular endothelial growth factor production in rheumatoid arthritis. Arthritis Rheum 2003; 48: 1521-1529 [PMID: 12794819 DOI: 10.1002/art.11143]
47. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Müller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003; 374: 1-20 [PMID: 12773095 DOI: 10.1042/BJ20030407]
48. Xu T, Zhou Y, Qiu L, Do DC, Zhao Y, Cui Z, Wang H, Liu X, Saradna A, Cao X, Wan M, Gao P. Aryl Hydrocarbon Receptor Protects Lungs from Cockroach Allergen-Induced Inflammation by Modulating Mesenchymal Stem Cells. J Immunol 2015; 195: 5539-5550 [PMID: 26561548 DOI: 10.4049/jimmunol.1501198]
49. Podechard N, Fardel O, Corolleur M, Bernard M, Lecureur V. Inhibition of human mesenchymal stem cell-derived adipogenesis by the environmental contaminant benzo(a)pyrene. Toxicol In Vitro 2009; 23: 1139-1144 [PMID: 19486938 DOI: 10.1016/j.tiv.2009.05.011]
50. Rathore K, Cekanova M. Effects of environmental carcinogen benzo(a)pyrene on canine adipose-derived mesenchymal stem cells. Res Vet Sci 2015; 103: 34-43 [PMID: 26679793 DOI: 10.1016/j.rvsc.2015.09.012]
51. Tong Y, Niu M, Du Y, Mei W, Cao W, Dou Y, Yu H, Du X, Yuan H, Zhao W. Aryl hydrocarbon receptor suppresses the osteogenesis of mesenchymal stem cells in collagen-induced arthritic mice through the inhibition of β-catenin. Exp Cell Res 2017; 350: 349-357 [PMID: 28007558 DOI: 10.1016/j.yexcr.2016.12.009]
52. Zhou Y, Jiang R, An L, Wang H, Cheng S, Qiong S, Weng Y. Benzo[a]pyrene impedes self-renewal and differentiation of mesenchymal stem cells and influences fracture healing. Sci Total Environ 2017; 587-588: 305-315 [PMID: 28249752 DOI: 10.1016/j.scitotenv.2017.02.152]
53. Hinden L, Shainer R, Almogi-Hazan O, Or R. Ex Vivo Induced Regulatory Human/Murine Mesenchymal Stem Cells as Immune Modulators. Stem Cells 2015; 33: 2256-2267 [PMID: 25850816 DOI: 10.1002/stem.2026]
54. Ankrum J, Karp JM. Mesenchymal stem cell therapy: Two steps forward, one step back. Trends Mol Med 2010; 16: 203-209 [PMID: 20335067 DOI: 10.1016/j.molmed.2010.02.005]
55. Galipeau J. The mesenchymal stromal cells dilemma--does a negative phase III trial of random donor mesenchymal stromal cells in steroid-resistant graft-versus-host disease represent a death knell or a bump in the road? Cytotherapy 2013; 15: 2-8 [PMID: 23260081 DOI: 10.1016/j.jcyt.2012.10.002]