Hematopoietic and mesenchymal stem cell transplantation for severe and refractory systemic lupus erythematosus

Clinical Immunology

Volumn 148, Issue 2, 2013, Pages 186-197

  Sui, Weiguo ^a   Hou, Xianliang ^a,b   Che, Wenti ^a   Chen, Jiejing ^a   Ou, Minglin ^a   Xue, Wen ^a   Dai, Yong ^a  

^a Central Laboratory of Guilin 181st Hospital   (China)

^b GUANGXI NORMAL UNIVERSITY   (China)

Author keywords

Autoimmune disease; Stem cell transplantation; Systemic lupus erythematosus

Indexed keywords

5' NUCLEOTIDASE; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; COMPLEMENT COMPONENT C3; CYCLIN DEPENDENT KINASE 4; CYCLIN DEPENDENT KINASE 6; CYCLOPHOSPHAMIDE; CYTOCHROME C; ENDOGLIN; F ACTIN; GRANULOCYTE COLONY STIMULATING FACTOR; HERMES ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 7; MESSENGER RNA; PREDNISONE; PROTEIN P16; PROTEIN P21; REACTIVE OXYGEN METABOLITE; SMAD PROTEIN; THY 1 ANTIGEN; TRANSCRIPTION FACTOR FKHRL1; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VINCULIN;

AUTOLOGOUS STEM CELL TRANSPLANTATION; AUTOPHAGOSOME; AUTOTRANSPLANTATION; CELL ACTIVATION; CELL DIFFERENTIATION; CELL EXPANSION; CELL FUNCTION; CELL PROLIFERATION; CYTOKINE RELEASE; DENDRITIC CELL; DISEASE ACTIVITY; DISEASE FREE SURVIVAL; DRUG EFFICACY; DRUG SAFETY; FOLLOW UP; HEART INFARCTION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOMODULATION; IN VITRO STUDY; IN VIVO STUDY; KARYOTYPE; KIDNEY FUNCTION; MAINTENANCE THERAPY; MESENCHYMAL STEM CELL TRANSPLANTATION; NATURAL KILLER CELL; NONHUMAN; OSTEOPOROSIS; OVERALL SURVIVAL; PERIPHERAL BLOOD STEM CELL; PHENOTYPE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SICKLE CELL ANEMIA; STEM CELL MOBILIZATION; SYSTEMIC LUPUS ERYTHEMATOSUS; TH1 CELL; TH2 CELL; THALASSEMIA;

AUTOIMMUNE DISEASE; STEM CELL TRANSPLANTATION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MESENCHYMAL STEM CELL TRANSPLANTATION;

EID: 84879336866     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2013.05.014     Document Type: Review

References (112)

1. Sui W., Hou X., Che W., Yang M., Dai Y. The applied basic research of systemic lupus erythematosus based on the biological omics. Genes Immun. 2013, 14:133-146.
2. Arbuckle M.R., McClain M.T., Rubertone M.V., Scofield R.H., Dennis G.J., James J.A., Harley J.B. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 2003, 10:1526-1533.
3. Tokano Y., Morimoto S., Amano H., Kawanishi T., Yano T., Tomyo M., Sugawara M., Kobayashi S., Tsuda H., Takasaki Y., Hashimoto H. The relationship between initial clinical manifestation and long-term prognosis of patients with systemic lupus erythematosus. Mod. Rheumatol. 2005, 15:275-282.
4. Cervera R., Khamashta M.A., Font J., Sebastiani G.D., Gil A., Lavilla P., Aydintug A.O., Jedryka-Góral A., de Ramón E., Fernández-Nebro A., Galeazzi M., Haga H.J., Mathieu A., Houssiau F., Ruiz-Irastorza G., Ingelmo M., Hughes G.R. Morbidity and mortality in systemic lupus erythematosus during a 5-year period. A multi-center prospective study of 1000 patients. European working party on systemic lupus erythematosus. Med. (Baltimore) 1999, 78:167-175.
5. Lo M.S., Tsokos G.C. Treatment of systemic lupus erythematosus: new advances in targeted therapy. Ann. N. Y. Acad. Sci. 2012, 1247:138-152.
6. Navarro-Zarza J.E., Alvarez-Hernández E., Casasola-Vargas J.C. Prevalence of community-acquired and nosocomial infections in hospitalized patients with systemic lupus erythematosus. Lupus 2010, 19:43-48.
7. Ruiz-Irastorza G., Olivares N., Ruiz-Arruza I., Martinez-Berriotxoa A., Egurbide M.V., Aguirre C. Predictors of major infections in systemic lupus erythematosus. Arthritis Res. Ther. 2009, 11:R109.
8. Bernatsky S., Boivin J.F., Joseph L., Manzi S., Ginzler E., Gladman D.D., Urowitz M., Fortin P.R., Petri M., Barr S., Gordon C., Bae S.C., Isenberg D., Zoma A., Aranow C., Dooley M.A., Nived O., Sturfelt G., Steinsson K., Alarcón G., Senécal J.L., Zummer M., Hanly J., Ensworth S., Pope J., Edworthy S., Rahman A., Sibley J., El-Gabalawy H., McCarthy T., St Pierre Y., Clarke A., Ramsey-Goldman R. Mortality in systemic lupus erythematosus. Arthritis Rheum. 2006, 54:2550-2557.
9. Tsokos G.C. Systemic lupus erythematosus. N. Engl. J. Med. 2011, 365:2110-2121.
10. Lichtman E.I., Helfgott S.M., Kriegel M.A. Emerging therapies for systemic lupus erythematosus - focus on targeting interferon-alpha. Clin. Immunol. 2012, 143:210-221.
11. Crispín J.C., Tsokos G.C. Novel molecular targets in the treatment of systemic lupus erythematosus. Autoimmun. Rev. 2008, 7:256-261.
12. Paz Z., Tsokos G.C. New therapeutics in systemic lupus erythematosus. Curr. Opin. Rheumatol. 2013, 25:297-303.
13. Ramos-Casals M., Diaz-Lagares C., Khamashta M.A. Rituximab and lupus: good in real life, bad in controlled trials. Comment on the article by Lu et al. Arthritis Rheum. 2009, 61:1281-1282.
14. Ramos-Casals M., Soto M.J., Cuadrado M.J., Khamashta M.A. Rituximab in systemic lupus erythematosus: a systematic review of off-label use in 188 cases. Lupus 2009, 18:767-776.
15. Furtado J., Isenberg D.A. B cell elimination in systemic lupus erythematosus. Clin. Immunol. 2013, 146:90-103.
16. Lampeter E.F., McCann S.R., Kolb H. Transfer of diabetes type 1 by bone-marrow transplantation. Lancet 1998, 351:568-569.
17. Kishimoto Y., Yamamoto Y., Ito T., Matsumoto N., Ichiyoshi H., Katsurada T., Date M., Ohga S., Kitajima H., Ikehara S., Fukuhara S. Transfer of autoimmune thyroiditis and resolution of palmoplantar pustular psoriasis following allogeneic bone marrow transplantation. Bone Marrow Transplant. 1997, 19:1041-1043.
18. Burt R.K., Slavin S., Burns W.H., Marmont A.M. Induction of tolerance in autoimmune diseases by hematopoietic stem cell transplantation: getting closer to a cure. Blood 2002, 99:768-784.
19. El-Badri N.S., Hakki A., Ferrari A., Shamekh R., Good R.A. Autoimmune disease: is it a disorder of the microenvironment?. Immunol. Res. 2008, 41:79-86.
20. Sun L., Zhang H., Feng X., Hou Y., Lu L., Fan L. Abnormality of bone marrow-derived stem cells in patients with systemic lupus erythematosus. Lupus 2007, 16:121-128.
21. Gu Z., Zhao S., Zhang H., Xu T., Jin O., Zhou K., Liu H., Zhang T., Sun L. Characterization of the ultrastructure and cytoskeleton of bone marrow-derived mesenchymal stem cells in patients with systemic lupus erythematosus. Chin. J. Rheumatol. 2008, 12:497-500.
22. Tang Y., Xie H., Chen J., Geng L., Chen H., Li X., Hou Y., Lu L., Shi S., Zeng X., Sun L. Activated NF-KB in bone marrow mesenchymal stem cells from SLE patients inhibits osteogenic differentiation through down-regulating Smad signaling. Stem Cells Dev. 2013, 22:668-678.
23. Tang Y., Ma X., Zhang H., Gu Z., Hou Y., Gilkeson G., Lu L., Zeng X., Sun L. Gene expression profile reveals abnormalities of multiple signaling pathways in mesenchymal stem cell derived from patients with systemic lupus erythematosus. Clin. Dev. Immunol. Aug. 27 2012, (Epub, Epub ahead of print). 10.1155/2012/826182.
24. Gu Z., Cao X., Jiang J., Li L., Da Z., Liu H., Cheng C. Upregulation of p16INK4A promotes cellular senescence of bone marrow-derived mesenchymal stem cells from systemic lupus erythematosus patients. Cell. Signal. 2012, 24:2307-2314.
25. Nie Y., Lau C., Lie A., Chan G., Mok M. Defective phenotype of mesenchymal stem cells in patients with systemic lupus erythematosus. Lupus 2010, 19:850-859.
26. Papadaki H.A., Boumpas D.T., Gibson F.M., Jayne D.R., Axford J.S., Gordon-Smith E.C., Marsh J.C., Eliopoulos G.D. Increased apoptosis of bone marrow CD34(+) cells and impaired function of bone marrow stromal cells in patients with systemic lupus erythematosus. Br. J. Haematol. 2001, 115:167-174.
27. Westerweel P.E., Luijten R.K., Hoefer I.E., Koomans H.A., Derksen R.H., Verhaar M.C. Haematopoietic and endothelial progenitor cells are deficient in quiescent systemic lupus erythematosus. Ann. Rheum. Dis. 2007, 66:865-870.
28. Hill J.M., Zalos G., Halcox J.P., Schenke W.H., Waclawiw M.A., Quyyumi A.A., et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N. Engl. J. Med. 2003, 348:593-600.
29. Li X., Liu L., Meng D., Wang D., Zhang J., Shi D., Liu H., Xu H., Lu L., Sun L. Enhanced apoptosis and senescence of bone marrow-derived mesenchymal stem cells in patients with systemic lupus erythematosus. Stem Cells Dev. 2012, 21:2387-2394.
30. Heo J.Y., Jing K., Song K.S., Seo K.S., Park J.H., Kim J.S., Jung Y.J., Hur G.M., Jo D.Y., Kweon G.R., Yoon W.H., Lim K., Hwang B.D., Jeon B.H., Park J.I. Downregulation of APE1/Ref-1 is involved in the senescence of mesenchymal stem cells. Stem Cells 2009, 27:1455-1462.
31. Ebert R., Ulmer M., Zeck S., Meissner-Weigl J., Schneider D., Stopper H., Schupp N., Kassem M., Jakob F. Selenium supplementation restores the antioxidative capacity and prevents cell damage in bone marrow stromal cells in vitro. Stem Cells 2006, 24:1226-1235.
32. Pyrovolaki K., Mavroudi I., Sidiropoulos P., Eliopoulos A.G., Boumpas D.T., Papadaki H.A. Increased expression of CD40 on bone marrow CD34+ hematopoietic progenitor cells in patients with systemic lupus erythematosus. Arthritis Rheum. 2009, 60:543-552.
33. Niu H., Fang G., Tang Y., Xie L., Yang H., Morel L., Diamond B., Zou Y.R. The function of hematopoietic stem cells is altered by both genetic and inflammatory factors in lupus mice. Blood 2013, 121:1986-1994.
34. Apostolidis S.A., Lieberman L.A., Kis-Toth K., Crispín J.C., Tsokos G.C. The dysregulation of cytokine networks in systemic lupus erythematosus. J. Interferon Cytokine Res. 2011, 31:769-779.
35. Suen J.L., Li H.T., Jong Y.J., Chiang B.L., Yen J.H. Altered homeostasis of CD4(+) FoxP3(+) regulatory T-cell subpopulations in systemic lupus erythematosus. Immunology 2009, 127:196-205.
36. Maeda K., Malykhin A., Teague-Weber B.N., Sun X.H., Farris A.D., Coggeshall K.M. Interleukin-6 aborts lymphopoiesis and elevates production of myeloid cells in systemic lupus erythematosus-prone B6.Sle1.Yaa animals. Blood 2009, 113:4534-4540.
37. Essers M.A., Offner S., Blanco-Bose W.E., Waibler Z., Kalinke U., Duchosal M.A., Trumpp A. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 2009, 458:904-908.
38. Kang Y.J., Yang S.J., Park G., Cho B., Min C.K., Kim T.Y., Lee J.S., Oh I.H. A novel function of interleukin-10 promoting self-renewal of hematopoietic stem cells. Stem Cells 2007, 25:1814-1822.
39. Pronk C.J., Veiby O.P., Bryder D., Jacobsen S.E. Tumor necrosis factor restricts hematopoietic stem cell activity in mice: involvement of two distinct receptors. J. Exp. Med. 2011, 208:1563-1570.
40. Drappa J., Brot N., Elkon K.B. The Fas protein is expressed at high levels on CD4+CD8+ thymocytes and activated mature lymphocytes in normal mice but not in the lupus-prone strain, Mrl lpr/lpr. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:10340-10344.
41. Zhou K., Zhang H., Jin O., Feng X., Yao G., Hou Y., Sun L. Transplantation of human bone marrow mesenchymal stem cell ameliorates the autoimmune pathogenesis in MRL/lpr Mice. Cell. Mol. Immunol. 2008, 5:417-424.
42. Sun L., Akiyama K., Zhang H., Yamaza T., Hou Y., Zhao S., Xu T., Le A., Shi S. Mesenchymal stem cell transplantation reverses multiorgan dysfunction in systemic lupus erythematosus mice and humans. Stem Cells 2009, 27:1421-1432.
43. Gu Z., Akiyama K., Ma X., Zhang H., Feng X., Yao G., Hou Y., Lu L., Gilkeson G.S., Silver R.M., Zeng X., Shi S., Sun L. Transplantation of umbilical cord mesenchymal stem cells alleviates lupus nephritis in MRL/lpr mice. Lupus 2010, 19:1502-1514.
44. Choi E.W., Shin I.S., Park S.Y., Park J.H., Kim J.S., Yoon E.J., Kang S.K., Ra J.C., Hong S.H. Reversal of serological, immunological and histological dysfunction in systemic lupus erythematosus mice by long term serial adipose tissuederived mesenchymal stem cell transplantation. Arthritis Rheum. 2012, 64:243-253.
45. Youd M., Blickarz C., Woodworth L., Touzjian T., Edling A., Tedstone J., Ruzek M., Tubo R., Kaplan J., Lodie T. Allogeneic mesenchymal stem cells do not protect NZB×NZW F1 mice from developing lupus disease. Clin. Exp. Immunol. 2010, 161:176-186.
46. Gu F., Molano I., Ruiz P., Sun L., Gilkeson G.S. Differential effect of allogeneic versus syngeneic mesenchymal stem cell transplantation in MRL/lpr and (NZB/NZW)F1 mice. Clin. Immunol. 2012, 145:142-152.
47. Marmont A.M., Van Bekkum D.W. Stem cells transplantation for severe autoimmune diseases: new proposal but still unanswered questions. Bone Marrow Transplant. 1995, 16:497-498.
48. Carrion F., Nova E., Ruiz C., Diaz F., Inostroza C., Rojo D., Monckeberg G., Figueroa F.E. Autologous mesenchymal stem cell treatment increased T regulatory cells with no effect on disease activity in two systemic lupus erythematosus patients. Lupus 2010, 19:317-322.
49. Bocelli-Tyndall C., Bracci L., Spagnoli G., Braccini A., Bouchenaki M., Ceredig R., Pistoia V., Martin I., Tyndall A. Bone marrow mesenchymal stromal cells (BM-MSCs) from healthy donors and auto-immune disease patients reduce the proliferation of autologous- and allogeneic-stimulated lymphocytes in vitro. Rheumatology (Oxford) 2007, 46:403-408.
50. Tyndall A., Gratwohl A. Blood and marrow stem cell transplants in autoimmune disease. A consensus report written on behalf of the European League against Rheumatism (EULAR) and the European Group for Blood and Marrow Transplantation (EBMT). Br. J. Rheumatol. 1997, 36:390-392.
51. Jayne D., Tyndall A. Autologous stem cell transplantation for systemic lupus erythematosus. Lupus 2004, 13:359-365.
52. Burt R.K., Traynor A., Statkute L., Barr W.G., Rosa R., Schroeder J., Verda L., Krosnjar N., Quigley K., Yaung K., Villa Bs M., Takahashi M., Jovanovic B., Oyama Y. Nonmyeloablative hematopoietic stem cell transplantation for systemic lupus erythematosus. JAMA 2006, 295:527-535.
53. Farge D., Labopin M., Tyndall A., Fassas A., Mancardi G.L., Van Laar J., Ouyang J., Kozak T., Moore J., Kötter I., Chesnel V., Marmont A., Gratwohl A., Saccardi R. Autologous hematopoietic stem cell transplantation for autoimmune diseases: an observational study on 12years' experience from the European Group for Blood and Marrow Transplantation Working Party on Autoimmune Diseases. Haematologica 2010, 95:284-292.
54. Alexander T., Thiel A., Rosen O., Massenkeil G., Sattler A., Kohler S., Mei H., Radtke H., Gromnica-Ihle E., Burmester G.R., Arnold R., Radbruch A., Hiepe F. Depletion of autoreactive immunologic memory followed by autologous hematopoietic stem cell transplantation in patients with refractory SLE induces long-term remission through de novo generation of a juvenile and tolerant immune system. Blood 2009, 113:214-223.
55. Illei G.G., Cervera R., Burt R.K., Doria A., Hiepe F., Jayne D., Pavletic S., Martin T., Marmont A., Saccardi R., Voskuyl A.E., Farge D. Current state and future directions of autologous hematopoietic stem cell transplantation in systemic lupus erythematosus. Ann. Rheum. Dis. 2011, 70:2071-2074.
56. Snowden J.A., Saccardi R., Allez M., Ardizzone S., Arnold R., Cervera R., Denton C., Hawkey C., Labopin M., Mancardi G., Martin R., Moore J.J., Passweg J., Peters C., Rabusin M., Rovira M., van Laar J.M., Farge D. Haematopoietic SCT in severe autoimmune diseases: updated guidelines of the European Group for Blood and Marrow Transplantation. Bone Marrow Transplant. 2012, 46:77-90.
57. Alchi B., Jayne D., Labopin M., Kotova O., Sergeevicheva V., Alexander T., Gualandi F., Gruhn B., Ouyang J., Rzepecki P., Held G., Sampol A., Voswinkel J., Ljungman P., Fassas A., Badoglio M., Saccardi R. Autologous haematopoietic stem cell transplantation for systemic lupus erythematosus: data from the European Group for Blood and Marrow Transplantation registry. Lupus 2013, 22:245-253.
58. Wang D., Zhang H., Liang J., Li X., Feng X., Wang H., Hua B., Liu B., Lu L., Gilkeson G.S., Silver R.M., Chen W., Shi S., Sun L. Allogeneic mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus: 4years experience. Cell Transplant. Oct. 31 2012, http://dx.doi.org/10.3727/096368912X658719 (Elctronic publication ahead of print).
59. Carrion F.A., Figueroa F.E. Mesenchymal stem cells for the treatment of systemic lupus erythematosus: is the cure for connective tissue diseases within connective tissue?. Stem Cell Res. Ther. 2011, 2:23.
60. Kunter U., Rong S., Djuric Z., Boor P., Müller-Newen G., Yu D., Floege J. Transplanted mesenchymal stem cells accelerate glomerular healing in experimental glomerulonephritis. J. Am. Soc. Nephrol. 2006, 17:2202-2212.
61. Richaud-Patin Y., Alcocer-Varela J., Llorente L. High levels of TH2 cytokine gene expression in systemic lupus erythematosus. Rev. Investig. Clin. 1995, 47:267-272.
62. Horwitz D.A., Gray J.D., Behrendsen S.C., Kubin M., Rengaraju M., Ohtsuka K., Trinchieri G. Decreased production of interleukin-12 and other Th1-type cytokines in patients with recent-onset systemic lupus erythematosus. Arthritis Rheum. 1998, 41:838-844.
63. Gröndal G., Gunnarsson I., Rönnelid J., Rogberg S., Klareskog L., Lundberg I. Cytokine production, serum levels and disease activity in systemic lupus erythematosus. Clin. Exp. Rheumatol. 2000, 18:565-570.
64. Sun L., Wang D., Liang J., Zhang H., Feng X., Wang H., Hua B., Liu B., Ye S., Hu X., Xu W., Zeng X., Hou Y., Gilkeson G.S., Silver R.M., Lu L., Shi S. Umbilical cord mesenchymal stem cell transplantation in severe and refractory systemic lupus erythematosus. Arthritis Rheum. 2010, 62:2467-2475.
65. Chang J.W., Hung S.P., Wu H.H., Wu W.M., Yang A.H., Tsai H.L., Yang L.Y., Lee O.K. Therapeutic effects of umbilical cord blood-derived mesenchymal stem cell transplantation in experimental lupus nephritis. Cell Transplant. 2011, 20:245-257.
66. Collins E., Gilkeson G. Hematopoetic and mesenchymal stem cell transplantation in the treatment of refractory systemic lupus erythematosus - where are we now?. Clin. Immunol. 2013, 10.1016/j.clim.2013.01.009.
67. Jiang X.X., Zhang Y., Liu B., Zhang S.X., Wu Y., Yu X.D., Mao N. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005, 105:4120-4126.
68. 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, 111:1327-1333.
69. Asari S., Itakura S., Ferreri K., Liu C.P., Kuroda Y., Kandeel F., Mullen Y. Mesenchymal stem cells suppress B-cell terminal differentiation. Exp. Hematol. 2009, 37:604-615.
70. Bacchetta R., Passerini L., Gambineri E., Dai M., Allan S.E., Perroni L., Dagna-Bricarelli F., Sartirana C., Matthes-Martin S., Lawitschka A., Azzari C., Ziegler S.F., Levings M.K., Roncarolo M.G. Defective regulatory and effector T cell functions in patients with FOXP3 mutations. J. Clin. Invest. 2006, 116:1713-1722.
71. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 2004, 22:531-562.
72. Hahn B.H., Anderson M., Le E., Cava A.L. Anti-DNA Ig peptides promote Treg cell activity in systemic lupus erythematosus patients. Arthritis Rheum. 2008, 58:2488-2497.
73. reg balance in patients with systemic lupus erythematosus. Clin. Immunol. 2011, 141:197-204.
74. Nalbandian A., Crispín J.C., Tsokos G.C. Interleukin-17 and systemic lupus erythematosus: current concepts. Clin. Exp. Immunol. 2009, 157:209-215.
75. Yamaza T., Kentaro A., Chen C., Liu Y., Shi Y., Gronthos S., Wang S., Shi S. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res. Ther. 2010, 1:5.
76. El-Magadmi M., Bodill H., Ahmad Y., Durrington P.N., Mackness M., Walker M., Bernstein R.M., Bruce I.N. Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation 2004, 110:399-404.
77. Johnson S.R., Harvey P.J., Floras J.S., Iwanochko M., Ibanez D., Gladman D.D., Urowitz M. Impaired brachial artery endothelium dependent flow mediated dilation in systemic lupus erythematosus: preliminary observations. Lupus 2004, 13:590-593.
78. Rajagopalan S., Somers E.C., Brook R.D., Kehrer C., Pfenninger D., Lewis E., Chakrabarti A., Richardson B.C., Shelden E., McCune W.J., Kaplan M.J. Endothelial cell apoptosis in systemic lupus erythematosus: a common pathway for abnormal vascular function and thrombosis propensity. Blood 2004, 103:3677-3683.
79. Kinsey G.R., Li L., Okusa M.D. Inflammation in acute kidney injury. Nephron Exp. Nephrol. 2008, 109:e102-e107.
80. Morioka T. Role of glomerular endothelial cells in glomerular disease. Nippon Jinzo Gakkai Shi 2008, 50:547-553.
81. Oswald J., Boxberger S., Jørgensen B., Feldmann S., Ehninger G., Bornhäuser M., Werner C. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 2004, 22:377-384.
82. Li K., Han Q., Yan X., Liao L., Zhao R.C. Not a process of simple vicariousness, the differentiation of human adipose-derived mesenchymal stem cells to renal tubular epithelial cells plays an important role in acute kidney injury repairing. Stem Cells Dev. 2010, 19:1267-1275.
83. Stock P., Brückner S., Ebensing S., Hempel M., Dollinger M.M., Christ B. The generation of hepatocytes from mesenchymal stem cells and engraftment into murine liver. Nat. Protoc. 2010, 5:617-627.
84. Ren G., Zhang L., Zhao X., Xu G., Zhang Y., Roberts A.I., Zhao R.C., Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008, 2:141-150.
85. Ren G., Su J., Zhang L., Zhao X., Ling W., L'huillie A., Zhang J., Lu Y., Roberts A.I., Ji W., Zhang H., Rabson A.B., Shi Y. Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 2009, 27:1954-1962.
86. Chen L., Tredget E.E., Wu P.Y., Wu Y. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS One 2008, 3:e1886.
87. Gnecchi M., He H., Liang O.D., Melo L.G., Morello F., Mu H., Noiseux N., Zhang L., Pratt R.E., Ingwall J.S., Dzau V.J. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat. Med. 2005, 11:367-368.
88. Timmers L., Lim S.K., Hoefer I.E., Arslan F., Lai R.C., van Oorschot A.A., Goumans M.J., Strijder C., Sze S.K., Choo A., Piek J.J., Doevendans P.A., Pasterkamp G., de Kleijn D.P. Human mesenchymal stem cell-conditioned medium improves cardiac function following myocardial infarction. Stem Cell Res. 2011, 6:206-214.
89. Tögel F.E., Westenfelder C. Mesenchymal stem cells: a new therapeutic tool for AKI. Nat. Rev. Nephrol. 2010, 6:179-183.
90. Robak E., Woźniacka A., Sysa-Jedrzejowska A., Stepień H., Robak T. Serum levels of angiogenic cytokines in systemic lupus erythematosus and their correlation with disease activity. Eur. Cytokine Netw. 2001, 12:445-452.
91. Navarro C., Candia-Zúñiga L., Silveira L.H., Ruiz V., Gaxiola M., Avila M.C., Amigo M.C. Vascular endothelial growth factor plasma levels in patients with systemic lupus erythematosus and primary antiphospholipid syndrome. Lupus 2002, 11:21-24.
92. Shi Y., Su J., Roberts A.I., Shou P., Rabson A.B., Ren G. How mesenchymal stem cells interact with tissue immune responses. Trends Immunol. 2012, 33:136-143.
93. Chen K., Wang D., Du W.T., Han Z.B., Ren H., Chi Y., Yang S.G., Zhu D.L., Bayard F., Han Z.C. Human umbilical cord mesenchymal stem cells hUC-MSCs exert immunosuppressive activities through a PGE2-dependent mechanism. Clin. Immunol. 2010, 135:448-458.
94. Petri M., Jones R.J., Brodsky R.A. High-dose cyclophosphamide without stem cell transplantation in systemic lupus erythematosus. Arthritis Rheum. 2003, 48:166-173.
95. DeZern A.E., Petri M., Drachman D.B., Kerr D., Hammond E.R., Kowalski J., Tsai H.L., Loeb D.M., Anhalt G., Wigley F., Jones R.J., Brodsky R.A. High dose cyclophosphamide without stem cell rescue in 207 patients with aplastic anemia and other autoimmune diseases. Med. (Baltimore) 2011, 90:89-98.
96. Burt R.K., Marmont A., Oyama Y., Slavin S., Arnold R., Hiepe F., Fassas A., Snowden J., Schuening F., Myint H., Patel D.D., Collier D., Heslop H., Krance R., Statkute L., Verda L., Traynor A., Kozak T., Hintzen R.Q., Rose J.W., Voltarelli J., Loh Y., Territo M., Cohen B.A., Craig R.M., Varga J., Barr W.G. Randomized controlled trials of autologous hematopoietic stem cell transplantation for autoimmune diseases: the evolution from myeloablative to lymphoablative transplant regimens. Arthritis Rheum. 2006, 54:3750-3760.
97. Tyndall A., Saccardi R. Haematopoietic stem cell transplantation in the treatment of severe autoimmune disease: results from phase I/II studies, prospective randomized trials and future directions. Clin. Exp. Immunol. 2005, 141:1-9.
98. Traynor A.E., Barr W.G., Rosa R.M., Rodriguez J., Oyama Y., Baker S., Brush M., Burt R.K. Hematopoietic stem cell transplantation for severe and refractory lupus. Analysis after five years and fifteen patients. Arthritis Rheum. 2002, 46:2917-2923.
99. Kamrava M.R., Anderson E.M., Kalunian K., Bashey A., Holman P., Medina B., Ball E.D., Carrier E. T-cell depletion improves outcome after autologous stem cell transplant in patients with systemic lupus erythematosus. Bone Marrow Transplant. 2005, 35:205-206.
100. Kohno K., Nagafuji K., Tsukamoto H., Horiuchi T., Takase K., Aoki K., Henzan H., Kamezaki K., Takenaka K., Miyamoto T., Teshima T., Harada M., Akashi K. Infectious complications in patients receiving autologous CD34-selected hematopoietic stem cell transplantation for severe autoimmune diseases. Transpl. Infect. Dis. 2009, 11:318-323.
101. Wada H., Terasako K., Kamiya Y., Sato M., Kimura S.I., Okuda S., Kako S., Yamazaki R., Oshima K., Nishida J., Moriguchi M., Terai C., Kanda Y. Immune recovery after autologous PBSC transplantation without in vitro graft manipulation for refractory systemic lupus erythematosus. Bone Marrow Transplant. 2011, 46:1450-1454.
102. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by de fined factors. Cell 2006, 126:663-676.
103. Takahashi K., Tanabe K., Ohnuki M., Narita M., Ichisaka T., Tomoda K., Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
104. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., Slukvin I.I., Thomson J.A. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
105. Park I.H., Zhao R., West J.A., Yabuuchi A., Huo H., Ince T.A., Lerou P.H., Lensch M.W., Daley G.Q. Reprogramming of human somatic cells to pluripotency with defined factors. Nature 2008, 451:141-146.
106. Maherali N., Hochedlinger K. Induced pluripotency of mouse and human somatic cells. Cold Spring Harb Symp. Quant. Biol. 2008, 73:157-162.
107. Yamanaka S. A fresh look at iPS cells. Cell 2009, 137:13-17.
108. Chen Y., Luo R., Xu Y., Cai X., Li W., Tan K., Huang J., Dai Y. Generation of systemic lupus erythematosus-specific induced pluripotent stem cells from urine. Rheumatol. Int. Feb. 22 2013, (Epub, ahead of print). 10.1007/s00296-013-2704-5.
109. Varas F., Stadtfeld M., de Andres-Aguayo L., Maherali N., di Tullio A., Pantano L., Notredame C., Hochedlinger K., Graf T. Fibroblast derived induced pluripotent stem cells show no common retroviral vector insertions. Stem Cells 2008, 27:300-306.
110. Ye L., Chang J.C., Lin C., Qi Z., Yu J., Kan Y.W. Generation of induced pluripotent stem cells using site-specific integration with phage integrase. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:19467-19472.
111. Hanna J., Wernig M., Markoulaki S., Sun C.W., Meissner A., Cassady J.P., Beard C., Brambrink T., Wu L.C., Townes T.M., Jaenisch R. Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 2007, 318:1920-1923.
112. Balow J.E. Clinical presentation and monitoring of lupus nephritis. Lupus 2005, 14:25-30.