Bone marrow-derived immature myeloid cells are a main source of circulating suPAR contributing to proteinuric kidney disease

Nature Medicine

Volumn 23, Issue 1, 2017, Pages 100-106

  Hahm, Eunsil ^a   Wei, Changli ^a   Fernandez, Isabel ^a   Li, Jing ^a   Tardi, Nicholas J ^a   Tracy, Melissa ^a   Wadhwani, Shikha ^a   Cao, Yanxia ^a   Peev, Vasil ^a   Zloza, Andrew ^a,b   Lusciks, Jevgenijs ^a   Hayek, Salim S ^c   O'Connor, Christopher ^d   Bitzer, Markus ^d   Gupta, Vineet ^a   Sever, Sanja ^e   Sykes, David B ^f   Scadden, David T ^f   Reiser, Jochen ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

^f Harvard University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UROKINASE RECEPTOR; PLAUR PROTEIN, MOUSE;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL EXPANSION; CELL LINEAGE; CELL POPULATION; CELL STIMULATION; CELL TRANSFER; CHIMERA; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; GLOMERULAR DYSFUNCTION; HEMATOPOIETIC CELL; HUMAN; HUMAN CELL; IRRADIATION; KIDNEY FUNCTION; MALE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PODOCYTE; PRIORITY JOURNAL; PROTEINURIA; XENOGRAFT; ANIMAL; CHRONIC KIDNEY FAILURE; DISEASE MODEL; FOCAL GLOMERULOSCLEROSIS; GLOMERULUS; KNOCKOUT MOUSE; METABOLISM; SCID MOUSE; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; BONE MARROW CELLS; DISEASE MODELS, ANIMAL; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; KIDNEY GLOMERULUS; MICE; MICE, KNOCKOUT; MICE, SCID; MICE, TRANSGENIC; MYELOID CELLS; PROTEINURIA; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; RENAL INSUFFICIENCY, CHRONIC;

EID: 85004045051     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4242     Document Type: Article

References (40)

1. Fogo, A.B. Mechanisms of progression of chronic kidney disease. Pediatr. Nephrol. 22, 2011-2022 (2007).
2. Hayek, S.S. et al. Soluble urokinase receptor and chronic kidney disease. N. Engl. J. Med. 373, 1916-1925 (2015).
3. Wei, C. et al. Modification of kidney barrier function by the urokinase receptor. Nat. Med. 14, 55-63 (2008).
4. Wei, C. et al. Circulating urokinase receptor as a cause of focal segmental glomerulosclerosis. Nat. Med. 17, 952-960 (2011).
5. Cravedi, P., Kopp, J.B. & Remuzzi, G. Recent progress in the pathophysiology and treatment of FSGS recurrence. Am. J. Transplant. 13, 266-274 (2013).
6. Winn, M.P. et al. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308, 1801-1804 (2005).
7. D'Agati, V.D., Kaskel, F.J. & Falk, R.J. Focal segmental glomerulosclerosis. N. Engl. J. Med. 365, 2398-2411 (2011).
8. Kitiyakara, C., Eggers, P. & Kopp, J.B. Twenty-one-year trend in ESRD due to focal segmental glomerulosclerosis in the United States. Am. J. Kidney Dis. 44, 815-825 (2004).
9. Fogo, A.B. Causes and pathogenesis of focal segmental glomerulosclerosis. Nat. Rev. Nephrol. 11, 76-87 (2015).
10. Gallon, L., Leventhal, J., Skaro, A., Kanwar, Y. & Alvarado, A. Resolution of recurrent focal segmental glomerulosclerosis after retransplantation. N. Engl. J. Med. 366, 1648-1649 (2012).
11. McCarthy, E.T., Sharma, M. & Savin, V.J. Circulating permeability factors in idiopathic nephrotic syndrome and focal segmental glomerulosclerosis. Clin. J. Am. Soc. Nephrol. 5, 2115-2121 (2010).
12. Savin, V.J. et al. Circulating factor associated with increased glomerular permeability to albumin in recurrent focal segmental glomerulosclerosis. N. Engl. J. Med. 334, 878-883 (1996).
13. Thunø, M., Macho, B. & Eugen-Olsen, J. suPAR: the molecular crystal ball. Dis. Markers 27, 157-172 (2009).
14. Blasi, F. & Carmeliet, P. uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 3, 932-943 (2002).
15. Smith, H.W. & Marshall, C.J. Regulation of cell signalling by uPAR. Nat. Rev. Mol. Cell Biol. 11, 23-36 (2010).
16. Faul, C. et al. The actin cytoskeleton of kidney podocytes is a direct target of the antiproteinuric effect of cyclosporine A. Nat. Med. 14, 931-938 (2008).
17. Reiser, J. et al. Induction of B7-1 in podocytes is associated with nephrotic syndrome. J. Clin. Invest. 113, 1390-1397 (2004).
18. Bertelli, R. et al. LPS nephropathy in mice is ameliorated by IL-2 independently of regulatory T cells activity. PLoS One 9, e111285 (2014).
19. Shultz, L.D. et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J. Immunol. 174, 6477-6489 (2005).
20. Basu, S., Hodgson, G., Katz, M. & Dunn, A.R. Evaluation of role of G-CSF in the production, survival, and release of neutrophils from bone marrow into circulation. Blood 100, 854-861 (2002).
21. Liu, F., Wu, H.Y., Wesselschmidt, R., Kornaga, T. & Link, D.C. Impaired production and increased apoptosis of neutrophils in granulocyte colony-stimulating factor receptor-deficient mice. Immunity 5, 491-501 (1996).
22. Kopp, J.B. et al. Transgenic mice with increased plasma levels of TGF-beta 1 develop progressive renal disease. Lab. Invest. 74, 991-1003 (1996).
23. Schiffer, M. et al. Apoptosis in podocytes induced by TGF-beta and Smad7. J. Clin. Invest. 108, 807-816 (2001).
24. Kistler, A.D. et al. Transient receptor potential channel 6 (TRPC6) protects podocytes during complement-mediated glomerular disease. J. Biol. Chem. 288, 36598-36609 (2013).
25. Hudkins, K.L. et al. BTBR Ob/Ob mutant mice model progressive diabetic nephropathy. J. Am. Soc. Nephrol. 21, 1533-1542 (2010).
26. Yu, H. et al. Rac1 activation in podocytes induces rapid foot process effacement and proteinuria. Mol. Cell. Biol. 33, 4755-4764 (2013).
27. Papeta, N. et al. Prkdc participates in mitochondrial genome maintenance and prevents Adriamycin-induced nephropathy in mice. J. Clin. Invest. 120, 4055-4064 (2010).
28. Alfano, M. et al. Full-length soluble urokinase plasminogen activator receptor down-modulates nephrin expression in podocytes. Sci. Rep. 5, 13647 (2015).
29. Cathelin, D. et al. Administration of recombinant soluble urokinase receptor per se is not sufficient to induce podocyte alterations and proteinuria in mice. J. Am. Soc. Nephrol. 25, 1662-1668 (2014).
30. Spinale, J.M. et al. A reassessment of soluble urokinase-type plasminogen activator receptor in glomerular disease. Kidney Int. 87, 564-574 (2015).
31. Delville, M. et al. A circulating antibody panel for pretransplant prediction of FSGS recurrence after kidney transplantation. Sci. Transl. Med. 6, 256ra136 (2014).
32. Huang, J. et al. Urinary soluble urokinase receptor levels are elevated and pathogenic in patients with primary focal segmental glomerulosclerosis. BMC Med. 12, 81 (2014).
33. Holmes, C. & Stanford, W.L. Concise review: stem cell antigen-1: expression, function, and enigma. Stem Cells 25, 1339-1347 (2007).
34. Shi, X. et al. Toll-like receptor 4/stem cell antigen 1 signaling promotes hematopoietic precursor cell commitment to granulocyte development during the granulopoietic response to Escherichia coli bacteremia. Infect. Immun. 81, 2197-2205 (2013).
35. Shultz, L.D., Brehm, M.A., Garcia-Martinez, J.V. & Greiner, D.L. Humanized mice for immune system investigation: progress, promise and challenges. Nat. Rev. Immunol. 12, 786-798 (2012).
36. Brehm, M.A., Shultz, L.D. & Greiner, D.L. Humanized mouse models to study human diseases. Curr. Opin. Endocrinol. Diabetes Obes. 17, 120-125 (2010).
37. Ito, R., Takahashi, T., Katano, I. & Ito, M. Current advances in humanized mouse models. Cell. Mol. Immunol. 9, 208-214 (2012).
38. Sellier-Leclerc, A.L. et al. A humanized mouse model of idiopathic nephrotic syndrome suggests a pathogenic role for immature cells. J. Am. Soc. Nephrol. 18, 2732-2739 (2007).
39. Niu, H. et al. The function of hematopoietic stem cells is altered by both genetic and inflammatory factors in lupus mice. Blood 121, 1986-1994 (2013).
40. Zhao, J.L. et al. Conversion of danger signals into cytokine signals by hematopoietic stem and progenitor cells for regulation of stress-induced hematopoiesis. Cell Stem Cell 14, 445-459 (2014).