Human vascular progenitor cells derived from renal arteries are endothelial-like and assist in the repair of injured renal capillary networks

Kidney International

Volumn 91, Issue 1, 2017, Pages 129-143

  Pang, Paul ^a   Abbott, Molly ^a   Chang, Steven L ^a   Abdi, Malyun ^a   Chauhan, Nikita ^a   Mistri, Murti ^a   Ghofrani, Joshua ^a   Fucci, Quynh Anh ^a   Walker, Colleen ^a   Leonardi, Corey ^a   Grady, Samuel ^a   Halim, Arvin ^a   Hoffman, Ryan ^c   Lu, Tzongshi ^a   Cao, Huixia ^a   Tullius, Stefan G ^a   Malek, Sayeed ^a   Kumar, Sanjaya ^a   Steele, Graeme ^a   Kibel, Adam ^a   Freedman, Benjamin S ^b   Waikar, Sushrut S ^a   Siedlecki, Andrew M ^a   more..

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c Touro University College of Pharmacy and School of Osteopathic Medicine   (United States)

Author keywords

acute kidney injury; endothelium; hyperfiltration; ischemia reperfusion; stem cell

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX2; CD34 ANTIGEN; CREATININE; CXCR4 PROTEIN, HUMAN; ENDOGLIN; HYDROGEN PEROXIDE; IMMUNOGLOBULIN RECEPTOR; KDR PROTEIN, HUMAN; MICRORNA; MIRN218 MICRORNA, HUMAN; NERVE PROTEIN; ROUNDABOUT RECEPTOR; VASCULOTROPIN RECEPTOR 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY SPECIFICITY; ARTICLE; CAPILLARY DENSITY; CELL POPULATION; CELL TRANSFORMATION; CONTROLLED STUDY; EXOSOME; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY ARTERY; KIDNEY ISCHEMIA; KIDNEY PERFUSION; MICROVASCULATURE; MOUSE; NEPHRECTOMY; NEPHRON; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RENAL ARTERY DERIVED VASCULAR PROGENITOR CELL; SHORT TANDEM REPEAT; STEM CELL; ACUTE KIDNEY INJURY; ANIMAL; AUTOTRANSPLANTATION; BLOOD; CAPILLARY; CELL MOTION; CHEMICALLY INDUCED; COCULTURE; CYTOLOGY; DISEASE MODEL; ENDOTHELIUM; FEASIBILITY STUDY; KIDNEY; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROCEDURES; STEM CELL TRANSPLANTATION; VASCULARIZATION; WOUND HEALING;

ACUTE KIDNEY INJURY; ANIMALS; ANTIGENS, CD34; CAPILLARIES; CELL MOVEMENT; COCULTURE TECHNIQUES; CREATININE; DISEASE MODELS, ANIMAL; ENDOGLIN; ENDOTHELIUM; EXOSOMES; FEASIBILITY STUDIES; HUMANS; HYDROGEN PEROXIDE; KIDNEY; MICE; MICRORNAS; NERVE TISSUE PROTEINS; RECEPTORS, CXCR4; RECEPTORS, IMMUNOLOGIC; RENAL ARTERY; STEM CELL TRANSPLANTATION; STEM CELLS; TRANSPLANTATION, AUTOLOGOUS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; WOUND HEALING;

EID: 84999673397     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1016/j.kint.2016.07.037     Document Type: Article

References (45)

1. 1 Crisan, M., Yap, S., Casteilla, L., et al. A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3 (2008), 301–313.
2. 2 Campagnolo, P., Cesselli, D., Al Haj Zen, A., et al. Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 121 (2010), 1735–1745.
3. 3 Asahara, T., Murohara, T., Sullivan, A., et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 275 (1997), 964–967.
4. 4 Invernici, G., Emanueli, C., Madeddu, P., et al. Human fetal aorta contains vascular progenitor cells capable of inducing vasculogenesis, angiogenesis, and myogenesis in vitro and in a murine model of peripheral ischemia. Am J Pathol 170 (2007), 1879–1892.
5. 5 Wood, H.B., May, G., Healy, L., Enver, T., Morriss-Kay, G.M., CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood 90 (1997), 2300–2311.
6. 6 Kawamoto, A., Katayama, M., Handa, N., et al. Intramuscular transplantation of G-CSF-mobilized CD34(+) cells in patients with critical limb ischemia: a phase I/IIa, multicenter, single-blinded, dose-escalation clinical trial. Stem Cells 27 (2009), 2857–2864.
7. 7 Bonventre, J.V., Yang, L., Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest 121 (2011), 4210–4221.
8. 8 Kramann, R., Tanaka, M., Humphreys, B.D., Fluorescence microangiography for quantitative assessment of peritubular capillary changes after AKI in mice. J Am Soc Nephrol 25 (2014), 1924–1931.
9. 9 Siedlecki, A., Irish, W., Brennan, D.C., Delayed graft function in the kidney transplant. Am J Transplant 11 (2011), 2279–2296.
10. 10 Hostetter, T.H., Olson, J.L., Rennke, H.G., Venkatachalam, M.A., Brenner, B.M., Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. J Am Soc Nephrol 12 (2001), 1315–1325.
11. 11 Dekkers, I.A., Blijdorp, K., Cransberg, K., et al. Long-term nephrotoxicity in adult survivors of childhood cancer. Clin J Am Soc Nephrol 8 (2013), 922–929.
12. 12 Muzaale, A.D., Massie, A.B., Wang, M.C., et al. Risk of end-stage renal disease following live kidney donation. JAMA 311 (2014), 579–586.
13. 13 Huang, W.C., Levey, A.S., Serio, A.M., et al. Chronic kidney disease after nephrectomy in patients with renal cortical tumours: a retrospective cohort study. Lancet Oncol 7 (2006), 735–740.
14. 14 Li, C., Issa, R., Kumar, P., et al. CD105 prevents apoptosis in hypoxic endothelial cells. J Cell Sci 116 (2003), 2677–2685.
15. 15 Anderberg, C., Cunha, S.I., Zhai, Z., et al. Deficiency for endoglin in tumor vasculature weakens the endothelial barrier to metastatic dissemination. J Exper Med 210 (2013), 563–579.
16. 16 Dominici, M., Le Blanc, K., Mueller, I., et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8 (2006), 315–317.
17. 17 Nagaya, N., Kangawa, K., Kanda, M., et al. Hybrid cell-gene therapy for pulmonary hypertension based on phagocytosing action of endothelial progenitor cells. Circulation 108 (2003), 889–895.
18. 18 Fabriek, B.O., van Bruggen, R., Deng, D.M., et al. The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood 113 (2009), 887–892.
19. 19 Duffield, J.S., Park, K.M., Hsiao, L.L., et al. Restoration of tubular epithelial cells during repair of the postischemic kidney occurs independently of bone marrow-derived stem cells. J Clin Invest 115 (2005), 1743–1755.
20. 20 Li, B., Cohen, A., Hudson, T.E., Motlagh, D., Amrani, D.L., Duffield, J.S., Mobilized human hematopoietic stem/progenitor cells promote kidney repair after ischemia/reperfusion injury. Circulation 121 (2010), 2211–2220.
21. 21 Abdellatif, M., Differential expression of microRNAs in different disease states. Circ Res 110 (2012), 638–650.
22. 22 Creemers, E.E., Tijsen, A.J., Pinto, Y.M., Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease?. Circ Res 110 (2012), 483–495.
23. 23 O'Toole, T.E., Abplanalp, W., Li, X., et al. Acrolein decreases endothelial cell migration and insulin sensitivity through induction of let-7a. Toxicol Sci 140 (2014), 271–282.
24. 24 Wang, H.W., Huang, T.S., Lo, H.H., et al. Deficiency of the microRNA-31-microRNA-720 pathway in the plasma and endothelial progenitor cells from patients with coronary artery disease. Arterioscler Thromb Vasc Biol 34 (2014), 857–869.
25. 25 Reagan, M.R., Mishima, Y., Glavey, S.V., et al. Investigating osteogenic differentiation in multiple myeloma using a novel 3D bone marrow niche model. Blood 124 (2014), 3250–3259.
26. 26 Middleton, J., Americh, L., Gayon, R., et al. A comparative study of endothelial cell markers expressed in chronically inflamed human tissues: MECA-79, Duffy antigen receptor for chemokines, von Willebrand factor, CD31, CD34, CD105 and CD146. J Pathol 206 (2005), 260–268.
27. 27 Werner, N., Kosiol, S., Schiegl, T., et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 353 (2005), 999–1007.
28. 28 Walter, D.H., Haendeler, J., Reinhold, J., et al. Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease. Circ Res 97 (2005), 1142–1151.
29. 29 Zernecke, A., Bidzhekov, K., Ozuyaman, B., et al. CD73/ecto-5'-nucleotidase protects against vascular inflammation and neointima formation. Circulation 113 (2006), 2120–2127.
30. 30 Bellingan, G., Maksimow, M., Howell, D.C., et al. The effect of intravenous interferon-beta-1a (FP-1201) on lung CD73 expression and on acute respiratory distress syndrome mortality: an open-label study. Lancet Respir Med 2 (2014), 98–107.
31. 31 Xing, L., Cui, R., Peng, L., et al. Mesenchymal stem cells, not conditioned medium, contribute to kidney repair after ischemia-reperfusion injury. Stem Cell Res Ther, 5, 2014, 101.
32. 32 Chen, Y., Qian, H., Zhu, W., et al. Hepatocyte growth factor modification promotes the amelioration effects of human umbilical cord mesenchymal stem cells on rat acute kidney injury. Stem Cells Dev 20 (2011), 103–113.
33. 33 Anjos-Afonso, F., Bonnet, D., Nonhematopoietic/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment. Blood 109 (2007), 1298–1306.
34. 34 Burks, S.R., Nguyen, B.A., Tebebi, P.A., et al. Pulsed focused ultrasound pretreatment improves mesenchymal stromal cell efficacy in preventing and rescuing established acute kidney injury in mice. Stem Cells 33 (2015), 1241–1253.
35. 35 Hostetter, T.H., Olson, J.L., Rennke, H.G., Venkatachalam, M.A., Brenner, B.M., Hyperfiltration in remnant nephrons: a potentially adverse response to renal ablation. Am J Physiol 241 (1981), F85–F93.
36. 36 Lafayette, R.A., Mayer, G., Park, S.K., Meyer, T.W., Angiotensin II receptor blockade limits glomerular injury in rats with reduced renal mass. J Clin Invest 90 (1992), 766–771.
37. 37 Small, E.M., Sutherland, L.B., Rajagopalan, K.N., Wang, S., Olson, E.N., MicroRNA-218 regulates vascular patterning by modulation of Slit-Robo signaling. Circ Res 107 (2010), 1336–1344.
38. 38 Mathew, L.K., Skuli, N., Mucaj, V., et al. miR-218 opposes a critical RTK-HIF pathway in mesenchymal glioblastoma. Proc Natl Acad Sci U S A 111 (2014), 291–296.
39. 39 Alajez, N.M., Lenarduzzi, M., Ito, E., et al. MiR-218 suppresses nasopharyngeal cancer progression through downregulation of survivin and the SLIT2-ROBO1 pathway. Cancer Res 71 (2011), 2381–2391.
40. 40 Siedlecki, A.M., Jin, X., Thomas, W., Hruska, K.A., Muslin, A.J., RGS4, a GTPase activator, improves renal function in ischemia-reperfusion injury. Kidney Int 80 (2011), 263–271.
41. 41 Pang, P., Jin, X., Proctor, B.M., et al. RGS4 inhibits angiotensin II signaling and macrophage localization during renal reperfusion injury independent of vasospasm. Kidney Int 87 (2015), 771–783.
42. 42 Kramann, R., Schneider, R.K., DiRocco, D.P., et al. Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 16 (2015), 51–66.
43. 43 Siedlecki, A.M., Jin, X., Muslin, A.J., Uremic cardiac hypertrophy is reversed by rapamycin but not by lowering of blood pressure. Kidney Int 75 (2009), 800–808.
44. 44 Siedlecki, A., Anderson, J.R., Jin, X., et al. RGS4 controls renal blood flow and inhibits cyclosporine-mediated nephrotoxicity. Am J Transplant 10 (2010), 231–241.
45. 45 Roccaro, A.M., Sacco, A., Maiso, P., et al. BM mesenchymal stromal cell-derived exosomes facilitate multiple myeloma progression. J Clin Invest 123 (2013), 1542–1555.