Human CD34+ progenitor cells freshly isolated from umbilical cord blood attenuate inflammatory lung injury following LPS challenge

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Huang, Xiaojia ^a,b   Sun, Kai ^a   Zhao, Yidan D ^a   Vogel, Stephen M ^a   Song, Yuanling ^c   Mahmud, Nadim ^a   Zhao, You Yang ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b JIANGSU UNIVERSITY   (China)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CD34 ANTIGEN; LIPOPOLYSACCHARIDE; MYELOPEROXIDASE;

ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CD34 SELECTION; CD34+ PROGENITOR CELL; CELL ISOLATION; CELL PROLIFERATION; COHORT ANALYSIS; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VIVO STUDY; LUNG BLOOD VESSEL; LUNG ENDOTHELIUM; MALE; MEDIATOR RELEASE; MOUSE; MOUSE MODEL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PROTEIN EXPRESSION; STEM CELL; STEM CELL TRANSPLANTATION; SURVIVAL RATE; UMBILICAL CORD BLOOD; ANIMAL; CELL SEPARATION; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; FETUS BLOOD; INFLAMMATION; LUNG; LUNG INJURY; METABOLISM; PATHOLOGY; SURVIVAL; VASCULARIZATION;

ANIMALS; ANTIGENS, CD34; CELL PROLIFERATION; CELL SEPARATION; ENDOTHELIAL CELLS; FETAL BLOOD; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; LUNG; LUNG INJURY; MICE; STEM CELL TRANSPLANTATION; STEM CELLS; SURVIVAL ANALYSIS;

EID: 84895899488     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088814     Document Type: Article

References (52)

1. Matthay MA, Ware LB, Zimmerman GA (2012) The acute respiratory distress syndrome. J Clin Invest 122: 2731-2740.
2. Rubenfeld GD, Caldwell E, Peabody E, Weaver J, Martin DP, et al. (2005) Incidence and outcomes of acute lung injury. N Engl J Med 353: 1685-1693. (Pubitemid 41464707)
3. Ware LB, Matthay MA (2000) The acute respiratory distress syndrome. N Engl J Med 342: 1334-1349. (Pubitemid 30408719)
4. Matthay MA, Zimmerman GA (2005) Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogenesis and rational management. Am J Respir Cell Mol Biol 33: 319-327. (Pubitemid 41416281)
5. Gupta N, Su X, Popov B, Lee JW, Serikov V, et al. (2007) Intrapulmonary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol 179: 1855- 1863.
6. Danchuk S, Ylostalo JH, Hossain F, Sorge R, Ramsey A, et al. (2011) Human multipotent stromal cells attenuate lipopolysaccharide-induced acute lung injury in mice via secretion of tumor necrosis factor-alpha-induced protein 6. Stem Cell Res Ther 2: 27.
7. Islam MN, Das SR, Emin MT, Wei M, Sun L, et al. (2012) Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury. Nat Med 18: 759-765.
8. Gonzalez-Rey E, Anderson P, Gonzalez MA, Rico L, Buscher D, et al. (2009) Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 58: 929-939.
9. Krasnodembskaya A, Samarani G, Song Y, Zhuo H, Su X, et al. (2012) 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 302: L1003-1013.
10. Krasnodembskaya A, Song Y, Fang X, Gupta N, Serikov V, et al. (2010) Antibacterial effect of human mesenchymal stem cells is mediated in part from secretion of the antimicrobial peptide LL-37. Stem Cells 28: 2229-2238.
11. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, et al. (2009) Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15: 42-49.
12. Lee JW, Fang X, Gupta N, Serikov V, Matthay MA (2009) Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Natl Acad Sci U S A 106: 16357-16362.
13. Lee JW, Krasnodembskaya A, McKenna DH, Song Y, Abbott J, et al. (2013) Therapeutic effects of human mesenchymal stem cells in ex vivo human lungs injured with live bacteria. Am J Respir Crit Care Med 187: 751-760.
14. Gotts JE, Matthay MA (2011) Mesenchymal stem cells and acute lung injury. Crit Care Clin 27: 719-733.
15. Weiss DJ, Kolls JK, Ortiz LA, Panoskaltsis-Mortari A, Prockop DJ (2008) Stem cells and cell therapies in lung biology and lung diseases. Proc Am Thorac Soc 5: 637-667. (Pubitemid 352031537)
16. Simmons DL, Satterthwaite AB, Tenen DG, Seed B (1992) Molecular cloning of a cDNA encoding CD34, a sialomucin of human hematopoietic stem cells. J Immunol 148: 267-271.
17. Civin CI, Strauss LC, Brovall C, Fackler MJ, Schwartz JF, et al. (1984) Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody raised against KG-1a cells. J Immunol 133: 157-165. (Pubitemid 14076703)
18. Andrews RG, Singer JW, Bernstein ID (1986) Monoclonal antibody 12-8 recognizes a 115-kd molecule present on both unipotent and multipotent hematopoietic colony-forming cells and their precursors. Blood 67: 842-845. (Pubitemid 16130285)
19. Soligo D, Delia D, Oriani A, Cattoretti G, Orazi A, et al. (1991) Identification of CD34+ cells in normal and pathological bone marrow biopsies by QBEND10 monoclonal antibody. Leukemia 5: 1026-1030.
20. Ito A, Nomura S, Hirota S, Suda J, Suda T, et al. (1995) Enhanced expression of CD34 messenger RNA by developing endothelial cells of mice. Lab Invest 72: 532-538.
21. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, et al. (1997) Isolation of putative progenitor endothelial cells for angiogenesis. Science 275: 964-967. (Pubitemid 27087709)
22. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, et al. (2001) Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 7: 430-436. (Pubitemid 32298545)
23. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS, et al. (2003) Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neovascularization of myocardial ischemia. Circulation 107: 461-468. (Pubitemid 36158050)
24. Schatteman GC, Hanlon HD, Jiao C, Dodds SG, Christy BA (2000) Bloodderived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 106: 571-578. (Pubitemid 30666390)
25. Murohara T, Ikeda H, Duan J, Shintani S, Sasaki K, et al. (2000) Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 105: 1527-1536. (Pubitemid 30390303)
26. Taguchi A, Soma T, Tanaka H, Kanda T, Nishimura H, et al. (2004) Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J Clin Invest 114: 330-338. (Pubitemid 39071605)
27. Shyu WC, Lin SZ, Chiang MF, Su CY, Li H (2006) Intracerebral peripheral blood stem cell (CD34+) implantation induces neuroplasticity by enhancing beta1 integrin-mediated angiogenesis in chronic stroke rats. J Neurosci 26: 3444-3453.
28. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, et al. (2002) Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation 106: 3009-3017. (Pubitemid 35440281)
29. Losordo DW, Kibbe MR, Mendelsohn F, Marston W, Driver VR, et al. (2012) A randomized, controlled pilot study of autologous CD34+ cell therapy for critical limb ischemia. Circ Cardiovasc Interv 5: 821-830.
30. Araki H, Yoshinaga K, Boccuni P, Zhao Y, Hoffman R, et al. (2007) Chromatin-modifying agents permit human hematopoietic stem cells to undergo multiple cell divisions while retaining their repopulating potential. Blood 109: 3570-3578. (Pubitemid 46572552)
31. Zhao YY, Gao XP, Zhao YD, Mirza MK, Frey RS, et al. (2006) Endothelial cell-restricted disruption of FoxM1 impairs endothelial repair following LPS-induced vascular injury. J Clin Invest 116: 2333-2343. (Pubitemid 44330132)
32. Mirza MK, Yuan J, Gao XP, Garrean S, Brovkovych V, et al. (2010) Caveolin-1 deficiency dampens Toll-like receptor 4 signaling through eNOS activation. Am J Pathol 176: 2344-2351.
33. Huang X, Zhao YY (2012) Transgenic expression of FoxM1 promotes endothelial repair following lung injury induced by polymicrobial sepsis in mice. PLoS One 7: e50094.
34. Subramaniam M, Saffaripour S, Watson SR, Mayadas TN, Hynes RO, et al. (1995) Reduced recruitment of inflammatory cells in a contact hypersensitivity response in P-selectin-deficient mice. J Exp Med 181: 2277-2282.
35. De Paepe ME, Mao Q, Ghanta S, Hovanesian V, Padbury JF (2011) Alveolar epithelial cell therapy with human cord blood-derived hematopoietic progenitor cells. Am J Pathol 178: 1329-1339.
36. Chang YS, Choi SJ, Ahn SY, Sung DK, Sung SI, et al. (2013) Timing of umbilical cord blood derived mesenchymal stem cells transplantation determines therapeutic efficacy in the neonatal hyperoxic lung injury. PLoS One 8: e52419.
37. Pierro M, Ionescu L, Montemurro T, Vadivel A, Weissmann G, et al. (2013) Short-term, long-term and paracrine effect of human umbilical cord-derived stem cells in lung injury prevention and repair in experimental bronchopulmonary dysplasia. Thorax 68: 475-484.
38. Moodley Y, Atienza D, Manuelpillai U, Samuel CS, Tchongue J, et al. (2009) Human umbilical cord mesenchymal stem cells reduce fibrosis of bleomycin-induced lung injury. Am J Pathol 175: 303-313.
39. Kim ES, Chang YS, Choi SJ, Kim JK, Yoo HS, et al. (2011) Intratracheal transplantation of human umbilical cord blood-derived mesenchymal stem cells attenuates Escherichia coli-induced acute lung injury in mice. Respir Res 12: 108.
40. Mao Q, Chu S, Ghanta S, Padbury JF, De Paepe ME (2013) Ex vivo expanded human cord blood-derived hematopoietic progenitor cells induce lung growth and alveolarization in injured newborn lungs. Respir Res 14: 37.
41. Zhao YD, Ohkawara H, Rehman J, Wary KK, Vogel SM, et al. (2009) Bone marrow progenitor cells induce endothelial adherens junction integrity by sphingosine-1-phosphate-mediated Rac1 and Cdc42 signaling. Circ Res 105: 696-704, 698 p following 704.
42. Zhao YD, Ohkawara H, Vogel SM, Malik AB, Zhao YY (2010) Bone marrow-derived progenitor cells prevent thrombin-induced increase in lung vascular permeability. Am J Physiol Lung Cell Mol Physiol 298: L36-44.
43. Gao X, Xu N, Sekosan M, Mehta D, Ma SY, et al. (2001) Differential role of CD18 integrins in mediating lung neutrophil sequestration and increased microvascular permeability induced by Escherichia coli in mice. J Immunol 167: 2895-2901. (Pubitemid 32768924)
44. Wiener-Kronish JP, Albertine KH, Matthay MA (1991) Differential responses of the endothelial and epithelial barriers of the lung in sheep to Escherichia coli endotoxin. J Clin Invest 88: 864-875.
45. O'Reilly MA. (2001) DNA damage and cell cycle checkpoints in hyperoxic lung injury: braking to facilitate repair. Am J Physiol Lung Cell Mol Physiol 281:L291-305.
46. Ionescu L, Byrne RN, van Haaften T, Vadivel A, Alphonse RS, et al. (2012) Stem cell conditioned medium improves acute lung injury in mice: in vivo evidence for stem cell paracrine action. Am J Physiol Lung Cell Mol Physiol 303: L967-977.
47. Dreher L, Elvers-Hornung S, Brinkmann I, Huck V, Henschler R, et al. (2013) Cultivation in human serum reduces adipose tissue-derived mesenchymal stromal cell adhesion to laminin and endothelium and reduces capillary entrapment. Stem Cells Dev 22: 791-803.
48. Geissler S, Textor M, Kuhnisch J, Konnig D, Klein O, et al. (2012) Functional comparison of chronological and in vitro aging: differential role of the cytoskeleton and mitochondria in mesenchymal stromal cells. PLoS One 7: e52700.
49. Izadpanah R, Kaushal D, Kriedt C, Tsien F, Patel B, et al. (2008) Long-term in vitro expansion alters the biology of adult mesenchymal stem cells. Cancer Res 68: 4229-4238.
50. Tarte K, Gaillard J, Lataillade JJ, Fouillard L, Becker M, et al. (2010) Clinical-grade production of human mesenchymal stromal cells: occurrence of aneuploidy without transformation. Blood 115: 1549-1553.
51. Rubio D, Garcia S, Paz MF, De la Cueva T, Lopez-Fernandez LA, et al. (2008) Molecular characterization of spontaneous mesenchymal stem cell transformation. PLoS One 3: e1398.
52. Sullivan MJ (2008) Banking on cord blood stem cells. Nat Rev Cancer 8: 555-563.