Concise review: Mesenchymal stromal cell-based approaches for the treatment of acute respiratory distress and sepsis syndromes

Stem Cells Translational Medicine

Volumn 6, Issue 4, 2017, Pages 1141-1151

  Johnson, Christian L ^a   Soeder, Yorick ^a   Dahlke, Marc H ^a  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

Author keywords

Acute respiratory distress syndrome; Cell therapy; Immunomodulation; Mesenchymal stromal cells; Sepsis syndrome

Indexed keywords

GAMMA INTERFERON; HIGH MOBILITY GROUP B1 PROTEIN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; KERATINOCYTE GROWTH FACTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; PROSTAGLANDIN E2; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR;

ACUTE LUNG INJURY; ADULT RESPIRATORY DISTRESS SYNDROME; BACTERIAL CLEARANCE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CECAL LIGATION AND PUNCTURE-INDUCED SEPSIS; CELL THERAPY; CYTOKINE RELEASE; HUMAN; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; INFLAMMATORY INFILTRATE; MACROPHAGE MIGRATION; MESENCHYMAL STROMA CELL; MORTALITY RATE; MULTICENTER STUDY (TOPIC); NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SEPSIS; TREATMENT OUTCOME; VENTILATOR INDUCED LUNG INJURY; ANIMAL; BIOLOGICAL THERAPY; IMMUNOLOGY; MESENCHYMAL STEM CELL; PHYSIOLOGY; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ANIMALS; CELL- AND TISSUE-BASED THERAPY; HUMANS; MESENCHYMAL STEM CELLS; RESPIRATORY DISTRESS SYNDROME, ADULT; SEPSIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

EID: 85017542180     PISSN: 21576564     EISSN: 21576580     Source Type: Journal    
DOI: 10.1002/sctm.16-0415     Document Type: Review

References (89)

1. Adhikari NK, Fowler RA, Bhagwanjee S et al. Critical care and the global burden of critical illness in adults. Lancet 2010;376: 1339–1346.
2. Fleischmann C, Scherag A, Adhikari NK et al. Assessment of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. Am J Respir Crit Care Med 2016;193:259–272.
3. Pittet D, Rangel-Frausto S, Li N et al. Systemic inflammatory response syndrome, sepsis, severe sepsis and septic shock: Incidence, morbidities and outcomes in surgical ICU patients. Intensive Care Med 1995;21:302– 309.
4. Engel C, Brunkhorst FM, Bone HG et al. Epidemiology of sepsis in Germany: Results from a national prospective multicenter study. Intensive Care Med 2007;33:606–618.
5. Salvo I, de Cian W, Musicco M et al. The Italian SEPSIS study: Preliminary results on the incidence and evolution of SIRS, sepsis, severe sepsis and septic shock. Intensive Care Med 1995;21(suppl 2):S244–S249.
6. Tupchong K, Koyfman A, Foran M. Sepsis, severe sepsis, and septic shock: A review of the literature. Afr J Emerg Med 2015;5:127– 135.
7. Deutschman CS, Tracey KJ. Sepsis: Current dogma and new perspectives. Immunity 2014;40:463–475.
8. Angus DC, Linde-Zwirble WT, Lidicker J et al. Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care. Crit Care Med 2001;29:1303–1310.
9. Singer M, Deutschman CS, Seymour CW et al. The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA 2016;315:801–810.
10. Lyle NH, Pena OM, Boyd JH et al. Barriers to the effective treatment of sepsis: Antimicrobial agents, sepsis definitions, and host-directed therapies. Ann N Y Acad Sci 2014; 1323:101–114.
11. Levy MM, Fink MP, Marshall JC et al. 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Crit Care Med 2003;31:1250–1256.
12. Simpson SQ. New sepsis criteria: A change we should not make. Chest 2016;149: 1117–1118.
13. Deutschman CS. Imprecise medicine: The limitations of sepsis-3. Crit Care Med 2016;44:857–858.
14. Martinon F, Burns K, Tschopp J. The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 2002;10: 417–426.
15. Huang W, Tang Y, Li L. HMGB1, a potent proinflammatory cytokine in sepsis. Cytokine 2010;51:119–126.
16. Boomer JS, To K, Chang KC et al. Immunosuppression in patients who die of sepsis and multiple organ failure. JAMA 2011;306: 2594–2605.
17. Monneret G, Venet F, Pachot A et al. Monitoring immune dysfunctions in the septic patient: A new skin for the old ceremony. Mol Med 2008;14:64–78.
18. Andersson U, Tracey KJ. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 2011;29: 139–162.
19. Lagu T, Rothberg MB, Shieh MS et al. Hospitalizations, costs, and outcomes of severe sepsis in the United States 2003 to 2007. Crit Care Med 2012;40:754–761.
20. Dellinger RP, Levy MM, Rhodes A et al. Surviving sepsis campaign: International guidelines for management of severe sepsis and septic shock: 2012. Crit Care Med 2013; 41:580–637.
21. Angus DC, Barnato AE, Bell D et al. A systematic review and meta-analysis of early goal-directed therapy for septic shock: The ARISE, ProCESS and ProMISe Investigators. Intensive Care Med 2015;41:1549–1560.
22. Opal SM, Fisher CJ Jr., Dhainaut JF et al. Confirmatory interleukin-1 receptor antagonist trial in severe sepsis: A phase III, randomized, double-blind, placebo-controlled, multicenter trial. The Interleukin-1 Receptor Antagonist Sepsis Investigator Group. Crit Care Med 1997;25:1115–1124.
23. Abraham E, Laterre PF, Garbino J et al. Lenercept (p55 tumor necrosis factor receptor fusion protein) in severe sepsis and early septic shock: A randomized, double-blind, placebo-controlled, multicenter phase III trial with 1,342 patients. Crit Care Med 2001;29: 503–510.
24. Bernard GR, Vincent JL, Laterre PF et al. Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 2001;344:699–709.
25. Werdan K, Pilz G, Bujdoso O et al. Score-based immunoglobulin G therapy of patients with sepsis: The SBITS study. Crit Care Med 2007;35:2693–2701.
26. Rice TW, Wheeler AP, Bernard GR et al. A randomized, double-blind, placebo-controlled trial of TAK-242 for the treatment of severe sepsis. Crit Care Med 2010;38:1685– 1694.
27. Guntupalli K, Dean N, Morris PE et al. A phase 2 randomized, double-blind, placebo-controlled study of the safety and efficacy of talactoferrin in patients with severe sepsis. Crit Care Med 2013;41:706–716.
28. Opal SM, Dellinger RP, Vincent JL et al. The next generation of sepsis clinical trial designs: What is next after the demise of recombinant human activated protein C?*. Crit Care Med 2014;42:1714–1721.
29. van der Poll T. Preclinical sepsis models. Surg Infect (Larchmt) 2012;13:287–292.
30. Vincent JL, Sakr Y, Sprung CL et al. Sepsis in European intensive care units: Results of the SOAP study. Crit Care Med 2006;34:344– 353.
31. Fink MP. Animal models of sepsis. Virulence 2014;5:143–153.
32. Wang P, Chaudry IH. A single hit model of polymicrobial sepsis: Cecal ligation and puncture. Sepsis 1998;2:227–233.
33. Chamberlain G, Fox J, Ashton B et al. Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007;25:2739–2749.
34. Le Blanc K, Tammik L, Sundberg B et al. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histo-compatibility complex. Scand J Immunol 2003; 57:11–20.
35. Ren G, Zhang L, Zhao X et al. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008;2:141– 150.
36. English K, Ryan JM, Tobin L et al. Cell contact, prostaglandin E(2) and transforming growth factor beta 1 play non-redundant roles in human mesenchymal stem cell induction of CD41CD25(High) forkhead box P31 regulatory T cells. Clin Exp Immunol 2009;156:149– 160.
37. Prevosto C, Zancolli M, Canevali P et al. Generation of CD41 or CD81 regulatory T cells upon mesenchymal stem cell-lymphocyte interaction. Haematologica 2007;92:881–888.
38. Obermajer N, Popp FC, Soeder Y et al. Conversion of Th17 into IL-17A(neg) regulatory T cells: A novel mechanism in prolonged allograft survival promoted by mesenchymal stem cell-supported minimized immunosuppressive therapy. J Immunol 2014;193:4988– 4999.
39. Polak JM, Bishop AE. Stem cells and tissue engineering: Past, present, and future. Ann N Y Acad Sci 2006;1068:352–366.
40. Barry FP, Murphy JM, English K et al. Immunogenicity of adult mesenchymal stem cells: Lessons from the fetal allograft. Stem Cells Dev 2005;14:252–265.
41. Casiraghi F, Remuzzi G, Abbate M et al. Multipotent mesenchymal stromal cell therapy and risk of malignancies. Stem Cell Rev 2013;9:65–79.
42. Eggenhofer E, Benseler V, Kroemer A et al. Mesenchymal stem cells are short-lived and do not migrate beyond the lungs after intravenous infusion. Front Immunol 2012;3: 297.
43. Devaney J, Horie S, Masterson C et al. Human mesenchymal stromal cells decrease the severity of acute lung injury induced by E. coli in the rat. Thorax 2015;70:625–635.
44. Marquez-Curtis LA, Janowska-Wieczorek A, McGann LE et al. Mesenchymal stromal cells derived from various tissues: Biological, clinical and cryopreservation aspects. Cryobiology 2015;71:181–197.
45. Pollock K, Sumstad D, Kadidlo D et al. Clinical mesenchymal stromal cell products undergo functional changes in response to freezing. Cytotherapy 2015;17:38–45.
46. Sepulveda JC, Tome M, Fernandez ME et al. Cell senescence abrogates the therapeutic potential of human mesenchymal stem cells in the lethal endotoxemia model. Stem Cells 2014;32:1865–1877.
47. ED 2015;4:899–904.
48. Panes J, Garcia-Olmo D, Van Assche G et al. Expanded allogeneic adipose-derived mesenchymal stem cells (Cx601) for complex perianal fistulas in Crohn’s disease: A phase 3 randomised, double-blind controlled trial. Lancet 2016;388:1281–1290.
49. Gupta N, Su X, Popov B et al. Intrapul-monary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol 2007;179:1855– 1863.
50. Gonzalez-Rey E, Anderson P, Gonzalez MA et al. Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 2009;58:929– 939.
51. Nemeth K, Leelahavanichkul A, Yuen PS et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 2009;15:42–49.
52. Bi LK, Tang B, Zhu B et al. Systemic delivery of IL-10 by Bone marrow derived stromal cells has therapeutic benefits in sepsis therapy. Prog Biochem Biophys 2010;37:678– 685.
53. Lee SH, Jang AS, Kim YE et al. Modulation of cytokine and nitric oxide by mesenchymal stem cell transfer in lung injury/fibrosis. Respir Res 2010;11:16.
54. Mei SH, Haitsma JJ, Dos Santos CC et al. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 2010;182:1047–1057.
55. Kim ES, Chang YS, Choi SJ et al. Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells attenuates Escherichia coli-induced acute lung injury in mice. Respir Res 2011;12:108.
56. Liang ZX, Sun JP, Wang P et al. Bone marrow-derived mesenchymal stem cells protect rats from endotoxin-induced acute lung injury. Chin Med J (Engl) 2011;124:2715–2722.
57. Sun J, Han ZB, Liao W et al. Intrapulmo-nary delivery of human umbilical cord mesenchymal stem cells attenuates acute lung injury by expanding CD41CD251 Forkhead Boxp3 (FOXP3)1 regulatory T cells and balancing anti- and pro-inflammatory factors. Cell Physiol Biochem 2011;27:587–596.
58. Chang CL, Leu S, Sung HC et al. 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.
59. Gupta N, Krasnodembskaya A, Kapetanaki M et al. Mesenchymal stem cells enhance survival and bacterial clearance in murine Escherichia coli pneumonia. Thorax 2012;67:533–539.
60. Krasnodembskaya A, Samarani G, Song Y et al. Human mesenchymal stem cells reduce mortality and bacteremia in gram-negative sepsis in mice in part by enhancing the phagocytic activity of blood monocytes. Am J Physiol Lung Cell Mol Physiol 2012;302:L1003–L1013.
61. Li J, Li D, Liu X et al. Human umbilical cord mesenchymal stem cells reduce systemic inflammation and attenuate LPS-induced acute lung injury in rats. J Inflamm (Lond) 2012;9:33.
62. Curley GF, Ansari B, Hayes M et al. Effects of intratracheal mesenchymal stromal cell therapy during recovery and resolution after ventilator-induced lung injury. Anesthesiology 2013;118:924–932.
63. Yang H, Wen Y, Hou-you Y et al. Combined treatment with bone marrow mesenchymal stem cells and methylprednisolone in paraquat-induced acute lung injury. BMC Emerg Med 2013;13(suppl 1):S5.
64. Zhao Y, Yang C, Wang H et al. Therapeutic effects of bone marrow-derived mesenchymal stem cells on pulmonary impact injury complicated with endotoxemia in rats. Int Immunopharmacol 2013;15:246–253.
65. Chen HH, Lin KC, Wallace CG et al. Additional benefit of combined therapy with mela-tonin and apoptotic adipose-derived mesenchymal stem cell against sepsis-induced kidney injury. J Pineal Res 2014;57:16–32.
66. Chao YH, Wu HP, Wu KH et al. An increase in CD31CD41CD251 regulatory T cells after administration of umbilical cord-derived mesenchymal stem cells during sepsis. PLoS One 2014;9:e110338.
67. Pedrazza L, Lunardelli A, Luft C et al. Mesenchymal stem cells decrease splenocytes apoptosis in a sepsis experimental model. Inflamm Res 2014;63:719–728.
68. Alcayaga-Miranda F, Cuenca J, Martin A et al. Combination therapy of menstrual derived mesenchymal stem cells and antibiotics ameliorates survival in sepsis. Stem Cell Res Ther 2015;6:199.
69. Guldner A, Maron-Gutierrez T, Abreu SC et al. Expanded endothelial progenitor cells mitigate lung injury in septic mice. Stem Cell Res Ther 2015;6:230.
70. Wang Y, Tan L, Jin J et al. Non-cultured dermal-derived mesenchymal cells attenuate sepsis induced by cecal ligation and puncture in mice. Sci Rep 2015;5:16973.
71. Hayes M, Curley GF, Masterson C et al. Mesenchymal stromal cells are more effective than the MSC secretome in diminishing injury and enhancing recovery following ventilator-induced lung injury. Intensive Care Med Exp 2015;3:29.
72. Monsel A, Zhu YG, Gennai S et al. Therapeutic effects of human mesenchymal stem cell-derived microvesicles in severe pneumonia in mice. Am J Respir Crit Care Med 2015; 192:324–336.
73. ED 2016;5:1048–1057.
74. Sung PH, Chiang HJ, Chen CH et al. Combined therapy with adipose-derived mesenchymal stem cells and ciprofloxacin against acute urogenital organ damage in rat sepsis syndrome induced by intrapelvic injection of cecal bacteria. STEM CELLS TRANSL MED 2016;5: 782–792.
75. Hall SR, Tsoyi K, Ith B et al. Mesenchymal stromal cells improve survival during sepsis in the absence of heme oxygenase-1: The importance of neutrophils. STEM CELLS 2013;31: 397–407.
76. Krasnodembskaya A, Song Y, Fang X et al. Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem Cells 2010;28:2229–2238.
77. Lee JW, Krasnodembskaya A, McKenna DH et al. Therapeutic effects of human mesenchymal stem cells in ex vivo human lungs injured with live bacteria. Am J Respir Crit Care Med 2013;187:751–760.
78. Monsel A, Zhu YG, Gudapati V et al. Mesenchymal stem cell derived secretome and extracellular vesicles for acute lung injury and other inflammatory lung diseases. Expert Opin Biol Ther 2016;16:859–871.
79. Zheng G, Huang L, Tong H et al. Treatment of acute respiratory distress syndrome with allogeneic adipose-derived mesenchymal stem cells: A randomized, placebo-controlled pilot study. Respir Res 2014;15:39.
80. Galstian GM, Parovichnikova EN, Makarova PM et al. The results of the Russian clinical trial of mesenchymal stromal cells (MSCs) in severe neutropenic patients (pts) with septic shock (SS) (RUMCESS trial). Blood 2015;126:2220.
81. Wilson JG, Liu KD, Zhuo H et al. Mesenchymal stem (stromal) cells for treatment of ARDS: A phase 1 clinical trial. Lancet Respir Med 2015;3:24–32.
82. ED 2015;4:1199–1213.
83. Ranieri VM, Thompson BT, Barie PS et al. Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med 2012;366: 2055–2064.
84. Riedemann NC, Guo RF, Ward PA. The enigma of sepsis. J Clin Invest 2003;112:460– 467.
85. Moodley Y, Sturm M, Shaw K et al. Human mesenchymal stem cells attenuate early damage in a ventilated pig model of acute lung injury. Stem Cell Res 2016;17:25– 31.
86. Asmussen S, Ito H, Traber DL et al. Human mesenchymal stem cells reduce the severity of acute lung injury in a sheep model of bacterial pneumonia. Thorax 2014;69:819– 825.
87. Streitz M, Miloud T, Kapinsky M et al. Standardization of whole blood immune phenotype monitoring for clinical trials: Panels and methods from the ONE study. Transplant Res 2013;2:17.
88. Geissler EK. The ONE Study compares cell therapy products in organ transplantation: Introduction to a review series on suppressive monocyte-derived cells. Transplant Res 2012; 1:11.
89. American College of Chest Physicians/ Society of Critical Care Medicine Consensus Conference: Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Crit Care Med 1992;20: 864–874.