Secreted factors from bone marrow stromal cells upregulate IL-10 and reverse acute kidney injury

Stem Cells International

Volumn , Issue , 2012, Pages

  Milwid, Jack M ^a,b   Ichimura, Takaharu ^c   Li, Matthew ^a   Jiao, Yunxin ^a   Lee, Jungwoo ^a   Yarmush, Joshua S ^a   Parekkadan, Biju ^a   Tilles, Arno W ^d   Bonventre, Joseph V ^b,c   Yarmush, Martin L ^a,e  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d Sentien Biotechnologies Inc   (United States)

^e RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CISPLATIN; CREATININE; CYCLINE; INTERLEUKIN 10; INTERLEUKIN 10 ANTIBODY; KIDNEY INJURY MOLECULE 1;

ACUTE KIDNEY FAILURE; ACUTE KIDNEY TUBULE NECROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW STROMAL CELL; CONDITIONED MEDIUM; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CULTURE MEDIUM; DISEASE SEVERITY; GLOMERULUS FILTRATION RATE; HISTOPATHOLOGY; INTRAVENOUS ADMINISTRATION; KIDNEY INJURY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENAL PROTECTION; STROMA CELL; SURVIVAL; UPREGULATION; UREA NITROGEN BLOOD LEVEL;

ANIMALIA; RATTUS;

EID: 84872124923     PISSN: None     EISSN: 16879678     Source Type: Journal    
DOI: 10.1155/2012/392050     Document Type: Article

References (52)

1. Schrier R. W., Wang W., Acute renal failure and sepsis. The New England Journal of Medicine 2004 351 2 159 169 2-s2.0-3042810297
2. Chertow G. M., Burdick E., Honour M., Bonventre J. V., Bates D. W., Acute kidney injury, mortality, length of stay, and costs in hospitalized patients. Journal of the American Society of Nephrology 2005 16 11 3365 3370 2-s2.0-33644874086 10.1681/ASN.2004090740 (Pubitemid 46179340)
3. Bonventre J. V., Jörres A., Ronco C., Kellum J. A., Mechanisms of acute kidney injury and repair. Management of Acute Kidney Problems 2010 Berlin, Germany Springer 13 20
4. Bonventre J. V., Dialysis in acute kidney injury-more is not better. New England Journal of Medicine 2008 359 1 82 84 2-s2.0-46449092994 10.1056/NEJMe0803765 (Pubitemid 351931101)
5. Brivet F. G., Kleinknecht D. J., Loirat P., Landais P. J. M., Acute renal failure in intensive care units-causes, outcome, and prognostic factors of hospital mortality: a prospective, multicenter study. Critical Care Medicine 1996 24 2 192 198 2-s2.0-0030022536 10.1097/00003246-199602000-00003 (Pubitemid 26065324)
6. Palevsky P. M., Zhang J. H., O'Connor T. Z., Chertow G. M., Crowley S. T., Choudhury D., Finkel K., Kellum J. A., Paganini E., Schein R. M. H., Smith M. W., Swanson K. M., Thompson B. T., Vijayan A., Watnick S., Star R. A., Peduzzi P., Intensity of renal support in critically ill patients with acute kidney injury. New England Journal of Medicine 2008 359 1 7 20 2-s2.0-65849527219 10.1056/NEJMoa0802639 (Pubitemid 351931092)
7. Kyung Jo S., Rosner M. H., Okusa M. D., Pharmacologic treatment of acute kidney injury: why drugs haven't worked and what is on the horizon. Clinical Journal of the American Society of Nephrology 2007 2 2 356 365 2-s2.0-34548438633 10.2215/CJN.03280906
8. Tögel F. E., Westenfelder C., Mesenchymal stem cells: a new therapeutic tool for AKI. Nature Reviews Nephrology 2010 6 3 179 183 2-s2.0-77649091092 10.1038/nrneph.2009.229
9. Aggarwal S., Pittenger M. F., Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005 105 4 1815 1822 2-s2.0-13544249606 10.1182/blood-2004-04-1559 (Pubitemid 40223708)
10. Uccelli A., Moretta L., Pistoia V., Mesenchymal stem cells in health and disease. Nature Reviews Immunology 2008 8 9 726 736 2-s2.0-50249158511 10.1038/nri2395
11. Chamberlain G., Fox J., Ashton B., Middleton J., Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells 2007 25 11 2739 2749 2-s2.0-36248932643 10.1634/stemcells.2007-0197 (Pubitemid 350127858)
12. Pittenger M., Sleuthing the source of regeneration by MSCs. Cell Stem Cell 2009 5 1 8 10 2-s2.0-67649217247 10.1016/j.stem.2009.06.013
13. Németh K., Leelahavanichkul A., Yuen P. S. T., Mayer B., Parmelee A., Doi K., Robey P. G., Leelahavanichkul K., Koller B. H., Brown J. M., Hu X., Jelinek I., Star R. A., Mezey É.., Bone marrow stromal cells attenuate sepsis via prostaglandin E 2-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nature Medicine 2009 15 1 42 49 2-s2.0-58149326737 10.1038/nm.1905
14. van Poll D., Parekkadan B., Borel Rinkes I. H. M., Mesenchymal stem cell therapy for protection and repair of injured vital organs. Cellular and Molecular Bioengineering 2008 1 1 42 50
15. Yagi H., Parekkadan B., Suganuma K., Soto-Gutierrez A., Tompkins R. G., Tilles A. W., Yarmush M. L., Long-term superior performance of a stem cell/hepatocyte device for the treatment of acute liver failure. Tissue Engineering A 2009 15 11 3377 3388 2-s2.0-72649101116 10.1089/ten.tea.2008.0681
16. Tögel F., Hu Z., Weiss K., Isaac J., Lange C., Westenfelder C., Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms. American Journal of Physiology 2005 289 1 F31 F42 2-s2.0-20844440562 10.1152/ajprenal.00007.2005 (Pubitemid 40863570)
17. Tögel F., Weiss K., Yang Y., Hu Z., Zhang P., Westenfelder C., Vasculotropic, paracrine actions of infused mesenchymal stem cells are important to the recovery from acute kidney injury. American Journal of Physiology 2007 292 5 F1626 F1635 2-s2.0-34247854809 10.1152/ajprenal.00339.2006 (Pubitemid 46701891)
18. Bruno S., Grange C., Deregibus M. C., Calogero R. A., Saviozzi S., Collino F., Morando L., Busca A., Falda M., Bussolati B., Tetta C., Camussi G., Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. Journal of the American Society of Nephrology 2009 20 5 1053 1067 2-s2.0-65649089130 10.1681/ASN.2008070798
19. Duffield J. S., Park K. M., Hsiao L.-L., Kelley V. R., Scadden D. T., Ichimura T., Bonventre J. V., Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. Journal of Clinical Investigation 2005 115 7 1743 1755 10.1172/JCI22593 (Pubitemid 40979713)
20. Lee R. H., Pulin A. A., Seo M. J., Kota D. J., Ylostalo J., Larson B. L., Semprun-Prieto L., Delafontaine P., Prockop D. J., Intravenous hMSCs improve myocardial infarction in mice because cells embolized in lung are activated to secrete the anti-inflammatory protein TSG-6. Cell Stem Cell 2009 5 1 54 63 2-s2.0-67649171661 10.1016/j.stem.2009.05.003
21. Zangi L., Margalit R., Reich-Zeliger S., Bachar-Lustig E., Beilhack A., Negrin R., Reisner Y., Direct imaging of immune rejection and memory induction by allogeneic mesenchymal stromal cells. Stem Cells 2009 27 11 2865 2874 2-s2.0-72849151523 10.1002/stem.217
22. Parekkadan B., Van Poll D., Suganuma K., Carter E. A., Berthiaume F., Tilles A. W., Yarmush M. L., Mesenchymal stem cell-derived molecules reverse fulminant hepatic failure. PLoS ONE 2007 2 9, article e941 2-s2.0-41549162430 10.1371/journal.pone.0000941 (Pubitemid 351460809)
23. Jiao Y., Milwid J. M., Yarmush M. L., Cuturi M., Anegon I., A mesenchymal stem cell potency assay. Suppression and Regulation of Immune Responses 2010 Totowa, NJ, USA Humana Press and Springer
24. Van Poll D., Parekkadan B., Cho C. H., Berthiaume F., Nahmias Y., Tilles A. W., Yarmush M. L., Mesenchymal stem cell-derived molecules directly modulate hepatocellular death and regeneration in vitro and in vivo. Hepatology 2008 47 5 1634 1643 2-s2.0-43949143205 10.1002/hep.22236 (Pubitemid 351702746)
25. Tao Y., Kim J., Schrier R. W., Edelstein C. L., Rapamycin markedly slows disease progression in a rat model of polycystic kidney disease. Journal of the American Society of Nephrology 2005 16 1 46 51 2-s2.0-18744380752 10.1681/ASN.2004080660 (Pubitemid 43073155)
26. Ichimura T., Asseldonk E. J. P. V., Humphreys B. D., Gunaratnam L., Duffield J. S., Bonventre J. V., Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. Journal of Clinical Investigation 2008 118 5 1657 1668 2-s2.0-43049125804 10.1172/JCI34487 (Pubitemid 351632370)
27. Ichimura T., Bonventre J. V., Bailly V., Wei H., Hession C. A., Cate R. L., Sanicola M., Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury. Journal of Biological Chemistry 1998 273 7 4135 4142 2-s2.0-0032512724 10.1074/jbc.273.7.4135 (Pubitemid 28103282)
28. McNeil C., New standard of care for cervical cancer sets stage for next questions. Journal of the National Cancer Institute 1999 91 6 500 501 2-s2.0-0033577092
29. Neijt J. P., Engelholm S. A., Tuxen M. K., Sorensen P. G., Hansen M., Sessa C., De Swart C. A. M., Hirsch F. R., Lund B., Van Houwelingen H. C., Exploratory phase III study of paclitaxel and cisplatin versus paclitaxel and carboplatin in advanced ovarian cancer. Journal of Clinical Oncology 2000 18 17 3084 3092 2-s2.0-0033850178
30. Wittes R. E., Brescia F., Young C. W., Combination chemotherapy with cis diamminedichloroplatinum (II) and bleomycin in tumors of the head and neck. Oncology 1975 32 5-6 202 207 2-s2.0-0016586869
31. Borch R. F., Pleasants M. E., Inhibition of cis-platinum nephrotoxicity by diethyldithiocarbamate rescue in a rat model. Proceedings of the National Academy of Sciences of the United States of America 1979 76 12 6611 6614 2-s2.0-0000950934 (Pubitemid 10163448)
32. Kelly K. J., Meehan S. M., Colvin R. B., Williams W. W., Bonventre J. V., Protection from toxicant-mediated renal injury in the rat with anti-CD54 antibody. Kidney International 1999 56 3 922 931 2-s2.0-0032844716 10.1046/j.1523-1755.1999.00629.x (Pubitemid 29411719)
33. Fillastre J. P., Raguenez-Viotte G., Cisplatin nephrotoxicity. Toxicology Letters 1989 46 1-3 163 175 2-s2.0-0024544753 (Pubitemid 19084010)
34. Vogetseder A., Karadeniz A., Kaissling B., Hir M. L., Tubular cell proliferation in the healthy rat kidney. Histochemistry and Cell Biology 2005 124 2 97 104 2-s2.0-26444483895 10.1007/s00418-005-0023-y (Pubitemid 41429764)
35. Maggini J., Mirkin G., Bognanni I., Holmberg J., Piazzón I. M., Nepomnaschy I., Costa H., Cañones C., Raiden S., Vermeulen M., Geffner J. R., Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS ONE 2010 5 2 2-s2.0-77949537626 10.1371/journal.pone.0009252 e9252
36. De Waal Malefyt R., Abrams J., Bennett B., Figdor C. G., De Vries J. E., Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. Journal of Experimental Medicine 1991 174 5 1209 1220 2-s2.0-0026094306
37. Ichimura T., Hung C. C., Yang S. A., Stevens J. L., Bonventre J. V., Kidney injury molecule-1: a tissue and urinary biomarker for nephrotoxicant-induced renal injury. American Journal of Physiology 2004 286 3 F552 F563 2-s2.0-1242343823 (Pubitemid 38233650)
38. Bonventre J. V., Kidney injury molecule-1 (KIM-1): a urinary biomarker and much more. Nephrology Dialysis Transplantation 2009 24 11 3265 3268 2-s2.0-73649123753 10.1093/ndt/gfp010
39. Morigi M., Introna M., Imberti B., Corna D., Abbate M., Rota C., Rottoli D., Benigni A., Perico N., Zoja C., Rambaldi A., Remuzzi A., Remuzzia G., Human bone marrow mesenchymal stem cells accelerate recovery of acute renal injury and prolong survival in mice. Stem Cells 2008 26 8 2075 2082 2-s2.0-55049087497 10.1634/stemcells.2007-0795
40. Eliopoulos N., Zhao J., Bouchentouf M., Forner K., Birman E., Yuan S., Boivin M. N., Martineau D., Human marrow-derived mesenchymal stromal cells decrease cisplatin renotoxicity in vitro and in vivo and enhance survival of mice post-intraperitoneal injection. American Journal of Physiology 2010 299 6 F1288 F1298 2-s2.0-78649947922 10.1152/ajprenal.00671.2009
41. Parekkadan B., Milwid J. M., Mesenchymal stem cells as therapeutics. Annual Review of Biomedical Engineering 2010 12 87 117 2-s2.0-77955617561 10.1146/annurev-bioeng-070909-105309
42. Bi B., Schmitt R., Israilova M., Nishio H., Cantley L. G., Stromal cells protect against acute tubular injury via an endocrine effect. Journal of the American Society of Nephrology 2007 18 9 2486 2496 2-s2.0-34548489620 10.1681/ASN.2007020140 (Pubitemid 47378865)
43. Nasef A., Chapel A., Mazurier C., Bouchet S., Lopez M., Mathieu N., Sensebé L., Zhang Y., Gorin N. C., Thierry D., Fouillard L., Identification of IL-10 and TGF- β transcripts involved in the inhibition of T-lymphocyte proliferation during cell contact with human mesenchymal stem cells. Gene Expression 2007 13 4-5 217 226 2-s2.0-34347371299 (Pubitemid 47024153)
44. Maeda H., Kuwahara H., Ichimura Y., Ohtsuki M., Kurakata S., Shiraishi A., TGF- β enhances macrophage ability to produce IL-10 in normal and tumor- bearing mice. Journal of Immunology 1995 155 10 4926 4932 2-s2.0-0028972556 (Pubitemid 3010832)
45. McGeachy M. J., Bak-Jensen K. S., Chen Y., Tato C. M., Blumenschein W., McClanahan T., Cua D. J., TGF- β and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain TH-17 cell-mediated pathology. Nature Immunology 2007 8 12 1390 1397 2-s2.0-36248965294 10.1038/ni1539 (Pubitemid 350138974)
46. Haynesworth S. E., Baber M. A., Caplan A. I., Cytokine expression by human marrow-derived mesenchymal progenitor cells in vitro: effects of dexamethasone and IL-1 Journal of Cellular Physiology 1996 166 3 585 592 2-s2.0-27644450590 10.1002/(SICI)1097-4652(199603)166:3<585::AID-JCP13>3. 0.CO;2-6 (Pubitemid 26095485)
47. Nicola M. D., Carlo-Stella C., Magni M., Milanesi M., Longoni P. D., Matteucci P., Grisanti S., Gianni A. M., Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002 99 10 3838 3843 2-s2.0-0037093058 10.1182/blood.V99.10.3838 (Pubitemid 34534559)
48. Deng J., Kohda Y., Chiao H., Wang Y., Hu X., Hewitt S. M., Miyaji T., McLeroy P., Nibhanupudy B., Li S., Star R. A., Interleukin-10 inhibits ischemic and cisplatin-induced acute renal injury. Kidney International 2001 60 6 2118 2128 2-s2.0-0035176820 10.1046/j.1523-1755.2001.00043.x (Pubitemid 33070455)
49. Li M., Tilles A. W., Milwid J. M., Hammad M., Lee J., Yarmush M. L., Parekkadan B., Phenotypic and functional characterization of human bone marrow stromal cells in hollow-fibre bioreactors. Journal of Tissue Engineering and Regenerative Medicine 2012 6 5 369 377 2-s2.0-79959619366 10.1002/term.439
50. Spaggiari G. M., Capobianco A., Abdelrazik H., Becchetti F., Mingari M. C., Moretta L., Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood 2008 111 3 1327 1333 2-s2.0-38949183675 10.1182/blood-2007-02-074997 (Pubitemid 351213419)
51. Kunter U., Rong S., Boor P., Eitner F., Müller-Newen G., Djuric Z., Van Roeyen C. R., Konieczny A., Ostendorf T., Villa L., Milovanceva-Popovska M., Kerjaschki D., Floege J., Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. Journal of the American Society of Nephrology 2007 18 6 1754 1764 2-s2.0-34249883938 10.1681/ASN.2007010044 (Pubitemid 46870312)
52. Aguilar S., Nye E., Chan J., Loebinger M., Spencer-Dene B., Fisk N., Stamp G., Bonnet D., Janes S. M., Murine but not human mesenchymal stem cells generate osteosarcoma-like lesions in the lung. Stem Cells 2007 25 6 1586 1594 2-s2.0-34547115678 10.1634/stemcells.2006-0762 (Pubitemid 47106029)