Renal progenitors: an evolutionary conserved strategy for kidney regeneration (original) (raw)

• Remuzzi, G., Benigni, A. & Remuzzi, A. Mechanisms of progression and regression of renal lesions of chronic nephropathies and diabetes. J. Clin. Invest. 116, 288–296 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Remuzzi, A. et al. ACE inhibition reduces glomerulosclerosis and regenerates glomerular tissue in a model of progressive renal disease. Kidney Int. 69, 1124–1130 (2006).
  Article CAS PubMed Google Scholar
• Ma, L. J. et al. Regression of glomerulosclerosis with high-dose angiotensin inhibition is linked to decreased plasminogen activator inhibitor-1. J. Am. Soc. Nephrol. 16, 966–976 (2005).
  Article CAS PubMed Google Scholar
• Reimschuessel, R. A fish model of renal regeneration and development. ILAR J. 42, 285–291 (2001).
  Article CAS PubMed Google Scholar
• Tanaka, E. & Reddien, P. W. The cellular basis for animal regeneration. Dev. Cell. 21, 172–185 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Brockes, J. P. & Kumar, A. Comparative aspects of animal regeneration. Annu. Rev. Cell. Dev. Biol. 24, 525–549 (2008).
  Article CAS PubMed Google Scholar
• Reimschuessel, R., Bennett, R. O., May, E. A. & Lipsky, M. M. Development of newly formed nephrons in the goldfish kidney following hexachlorobutadiene-induced nephrotoxicity. Toxicol. Pathol. 18, 32–38 (1990).
  Article CAS PubMed Google Scholar
• Elger, M. et al. Nephrogenesis is induced by partial nephrectomy in the Elasmobranch Leucoraja erinacea. J. Am. Soc. Nephrol. 14, 1506–1518 (2003).
  Article PubMed Google Scholar
• Davidson, A. J. Uncharted waters: nephrogenesis and renal regeneration in fish and mammals. Pediatr. Nephrol. 26, 1435–1443 (2011).
  Article PubMed Google Scholar
• Romagnani, P. From Proteus to Prometheus: learning from fish to modulate regeneration. J. Am. Soc Nephrol. 21, 726–728 (2010).
  Article CAS PubMed Google Scholar
• Blanpain, C., Horsley, V. & Fuchs, E. Epithelial stem cells: turning over new leaves. Cell 128, 445–458 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Shahragim, T. Stem cell: what's in a name? Nature Reports Stem Cells http://dx.doi.org/10.1038/stemcells.2009.90.
• Shenghui, H., Nakada, D. & Morrison, S. J. Mechanisms of stem cell self-renewal. Annu. Rev. Cell. Dev. Biol. 25, 377–406 (2009).
  Article CAS Google Scholar
• Weissman, I. L., Anderson, D. J. & Gage, F. Stem and progenitor cells: origin, phenotype, lineage commitment and transdifferentiation. Annu. Rev. Cell. Dev. Biol. 17, 387–403 (2001).
  Article CAS PubMed Google Scholar
• Romagnani, P. Toward the identification of a “renopoietic system”? Stem Cells 27, 2247–2253 (2009).
  Article PubMed PubMed Central Google Scholar
• Dantzler, W. H. & Braun, J. Vertebrate renal system in Handbook of Physiology (ed. Dantzler, W. H.) Section 13: Comparative Physiology (Oxford University Press, New York, 1997).
  Google Scholar
• Barraclough, G. (ed.) The Times Atlas of World History (Times Books, London, 1978).
  Google Scholar
• Gascoigne, B. History of Evolution. HistoryWorld [online], (2001).
  Google Scholar
• Dow, J. A. & Romero, M. F. Drosophila provides rapid modeling of renal development, function, and disease. Am. J. Physiol. Renal Physiol. 299, 1237–1244 (2010).
  Article CAS Google Scholar
• Dressler, G. R. The cellular basis of kidney development. Annu. Rev. Cell. Dev. Biol. 22, 509–529 (2006).
  Article CAS PubMed Google Scholar
• Schedl, A. Renal abnormalities and their developmental origin. Nat. Rev. Genet. 8, 791–802 (2007).
  Article CAS PubMed Google Scholar
• Liu, W. et al. “Avian-type” renal medullary tubule organization causes immaturity of urine-concentrating ability in neonates. Kidney Int. 60, 680–693 (2001).
  Article CAS PubMed Google Scholar
• Cha, J. H. et al. Cell proliferation in the loop of Henle in the developing rat kidney. J. Am. Soc. Nephrol. 12, 1410–1421 (2001).
  CAS PubMed Google Scholar
• Diep, C. Q. et al. Identification of adult nephron progenitors capable of kidney regeneration in zebrafish. Nature 470, 95–100 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, W., Boucher, R. C., Bollig, F., Englert, C. & Hildebrandt, F. Characterization of mesonephric development and regeneration using transgenic zebrafish. Am. J. Physiol. Renal Physiol. 299, F1040–F1047 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, W. & Hildebrandt, F. Inducible podocyte injury and proteinuria in transgenic zebrafish. J. Am. Soc. Nephrol. 23, 1039–1047 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zeng, X. & Hou, S. X. Kidney stem cells found in adult zebrafish. Cell Stem Cell 8, 247–249 (2011).
  Article CAS PubMed Google Scholar
• Singh, S. R., Liu, W. & Hou, S. X. The adult Drosophila malpighian tubules are maintained by multipotent stem cells. Cell Stem Cell 1, 191–203 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Singh, S. R. & Hou, S. X. Lessons learned about adult kidney stem cells from the malpighian tubules of Drosophila. J. Am. Soc. Nephrol. 19, 660–666 (2008).
  Article PubMed Google Scholar
• Tulina, N. & Matunis, E. Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546–2549 (2001).
  Article CAS PubMed Google Scholar
• Kiger, A. A., Jones, D. L., Schulz, C., Rogers, M. B. & Fuller, M. T. Stem cell self-renewal specified by JAK-STAT activation in response to a support cell cue. Science 294, 2542–2545 (2001).
  Article CAS PubMed Google Scholar
• Gray, P. The development of the amphibian kidney. I. The development of the mesonephros of rana temporaria. Q. J. Micr. Sci. 73, 507–545 (1930).
  Google Scholar
• Fox, H. in Biology of the Reptilian (Gans, C. & Parsons, T. S.) 1–157 (Academic Press, London, 1977).
  Google Scholar
• Beuchat, C. A. & Braun, E. J. Allometry of the kidney: implications for the ontogeny of osmoregulation. Am. J. Physiol. 255, 760–767 (1988).
  Article Google Scholar
• Solomon, S. E. The morphology of the kidney of the green turtle. J. Anat. 140, 355–369 (1985).
  PubMed PubMed Central Google Scholar
• Wideman, R. F. Jr. Maturation of glomerular size distribution profiles in domestic fowl (Gallus gallus). J. Morphol. 201, 205–213 (1989).
  Article PubMed Google Scholar
• Nishimura, H. et al. Aquaporin-2 water channel in developing quail kidney: possible role in programming adult fluid homeostasis. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, 2147–2158 (2007).
  Article CAS Google Scholar
• Bakir, L. & De Rouffignac, C. Urinary concentrating ability: insights from comparative anatomy. Am. J. Physiol. 249, 643–666 (1985).
  Google Scholar
• Kobayashi, A. et al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell 3, 169–181 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Barker, N. et al. Lgr5+ve stem/progenitor cells contribute to nephron formation during kidney development. Cell Reports 2, 540–552 (2012).
  Article CAS PubMed Google Scholar
• Oliver, J. A., Maarouf, O., Cheema, F. H., Martens, T. P. & Al-Awqati, Q. The renal papilla is a niche for adult kidney stem cells. J. Clin. Invest. 114, 795–804 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Dekel, B. et al. Isolation and characterization of nontubular sca-1+lin-multipotent stem/progenitor cells from adult mouse kidney. J. Am. Soc. Nephrol. 17, 3300–3314 (2006).
  Article PubMed Google Scholar
• Bussolati, B. et al. Isolation of renal progenitor cells from adult human kidney. Am. J. Pathol. 166, 545–555 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Humphreys, B. D. et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell 2, 284–291 (2008).
  Article CAS PubMed Google Scholar
• Kitamura, S. et al. Establishment and characterization of renal progenitor like cells from S3 segment of nephron in rat adult kidney. FASEB J. 19, 1789–1797 (2005).
  Article CAS PubMed Google Scholar
• Gupta, S. et al. Isolation and characterization of kidney-derived stem cells. J. Am. Soc. Nephrol. 17, 3028–3040 (2006).
  Article CAS PubMed Google Scholar
• Maeshima, A., Sakurai, H. & Nigam, S. K. Adult kidney tubular cell population showing phenotypic plasticity, tubulogenic capacity, and integration capability into developing kidney. J. Am. Soc. Nephrol. 17, 188–198 (2006).
  Article CAS PubMed Google Scholar
• Challen, G. A., Bertoncello, I., Deane, J. A., Ricardo, S. D. & Little, M. H. Kidney side population reveals multilineage potential and renal functional capacity but also cellular heterogeneity. J. Am. Soc. Nephrol. 17, 1896–1912 (2006).
  Article CAS PubMed Google Scholar
• Langworthy, M., Zhou, B., de Caestecker, M., Moeckel, G. & Baldwin, H. S. NFATc1 identifies a population of proximal tubule cell progenitors. J. Am. Soc. Nephrol. 20, 311–321 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Humphreys, B. D. et al. Repair of injured proximal tubule does not involve specialized progenitors. Proc. Natl Acad. Sci. USA 108, 9226–9231 (2011).
  Article PubMed PubMed Central Google Scholar
• Wen, X., Murugan, R., Peng, Z. & Kellum, J. A. Pathophysiology of acute kidney injury: a new perspective. Contrib. Nephrol. 165, 39–45 (2010).
  Article PubMed Google Scholar
• Smeets, B. et al. Proximal tubular cells contain a phenotypically distinct, scattered cell population involved in tubular regeneration. J. Pathol. http://dx.doi.org/10.1002/path.4125.
• Appel, D. et al. Recruitment of podocytes from glomerular parietal epithelial cells. J. Am. Soc. Nephrol. 20, 333–343 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Grouls, S. et al. Lineage specification of parietal epithelial cells requires β-catenin/Wnt signaling. J. Am. Soc. Nephrol. 23, 63–72 (2012).
  Article CAS PubMed Google Scholar
• Benigni, A. et al. Inhibiting ACE promotes renal repair by limiting progenitor cells proliferation and restoring the glomerular architecture. Am. J. Pathol. 179, 628–638 (2011).
  Article PubMed PubMed Central Google Scholar
• Peti-Peterdi, J. & Sipos, A. A high-powered view of the filtration barrier. J. Am. Soc. Nephrol. 21, 1835–1841 (2010).
  Article PubMed Google Scholar
• Coskun, V. et al. CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain. Proc. Natl Acad. Sci. USA 105, 1026–1031 (2008).
  Article PubMed PubMed Central Google Scholar
• Ivanova, L., Hiatt, M. J., Yoder, M. C., Tarantal, A. F. & Matsell, D. G. Ontogeny of CD24 in human kidney. Kidney Int. 77, 1123–1131 (2010).
  Article CAS PubMed Google Scholar
• Sagrinati, C. et al. Isolation and characterization of multipotent progenitor cells from the Bowman's capsule of adult human kidneys. J. Am. Soc. Nephrol. 17, 2443–2456 (2006).
  Article CAS PubMed Google Scholar
• Mazzinghi, B. et al. Essential but differential role for CXCR4 and CXCR7 in the therapeutic homing of human renal progenitor cells. J. Exp. Med. 205, 479–490 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ronconi, E. et al. Regeneration of glomerular podocytes by human renal progenitors. J. Am. Soc. Nephrol. 20, 322–332 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Lazzeri, E. et al. Regenerative potential of embryonic renal multipotent progenitors in acute renal failure. J. Am. Soc. Nephrol. 18, 3128–3138 (2007).
  Article CAS PubMed Google Scholar
• Angelotti, M. L. et al. Characterization of renal progenitors committed toward the tubular lineage and their regenerative potential in renal tubular injury. Stem Cells 30, 1714–1725 (2012).
  Article CAS PubMed Google Scholar
• Sallustio, F. et al. TLR2 plays a role in the activation of human resident renal stem/progenitor cells. FASEB J. 24, 514–525 (2010).
  Article CAS PubMed Google Scholar
• Lindgren, D. et al. Isolation and characterization of progenitor-like cells from human renal proximal tubules. Am. J. Pathol. 178, 828–837 (2011).
  Article PubMed PubMed Central Google Scholar
• Ward, H. H. et al. Adult human CD133/1(+) kidney cells isolated from papilla integrate into developing kidney tubules. Biochim. Biophys. Acta 1812, 1344–1157 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Bussolati, B. et al. Hypoxia modulates the undifferentiated phenotype of human renal inner medullary CD133+ progenitors through Oct4/miR-145 balance. Am. J. Physiol. Renal. Physiol. 302, F116–F128 (2012).
  Article CAS PubMed Google Scholar
• Loverre, A. et al. Increase of proliferating renal progenitor cells in acute tubular necrosis underlying delayed graft function. Transplantation 85, 1112–1119 (2008).
  Article PubMed Google Scholar
• Ye, Y. et al. Proliferative capacity of stem/progenitor-like cells in the kidney may associate with the outcome of patients with acute tubular necrosis. Hum. Pathol. 42, 1132–1141 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Sallustio, F. et al. Human renal stem/progenitor cells repair tubular epithelial cell injury through TLR2-driven inhibin-A and microvesicle-shuttled decorin. Kidney Int. (in press).
• Axelson, H. & Johansson, M. E. Renal stem cells and their implications for kidney cancer. Semin. Cancer Biol. http://dx.doi.org/10.1016/j.semcancer.2012.06.005.
• Borg, B., Antonopoulou, E., Andersson, E., Carlberg, T. & Mayer, I. Effectiveness of several androgens in stimulating kidney hypertrophy, a secondary sexual character, in castrated male three-spined sticklebacks, Gasterosteus aculeatus. Can. J. Zool. 71, 2327–2329 (1993).
  Article CAS Google Scholar
• Rushbrook, B. J. & Barber, I. Nesting, courtship and kidney hypertrophy in _Schistocephalus_-infected male three-spined stickleback from an upland lake. J. Fish Biol. 69, 870–882 (2006).
  Article Google Scholar
• Bely, A. E. & Nyberg, K. J. Evolution of animal regeneration: re-emergence of a field. Trends Ecol. Evol. 25, 161–170 (2010).
  Article PubMed Google Scholar
• Shepherd, G. M. The human sense of smell: are we better than what we think? PLoS Biol. 2, 572–575 (2004).
  Article CAS Google Scholar
• Bely, A. E. Evolutionary loss of animal regeneration: pattern and process. Integr. Comp. Biol. 50, 515–527 (2010).
  Article PubMed Google Scholar
• Quigley, R. Developmental changes in renal function. Curr. Opin. Pediatr. 24, 184–190 (2012).
  Article PubMed Google Scholar
• Dantzler, W. H. & Braun, E. J. Comparative nephron function in reptiles, birds, and mammals. Am. J. Physiol. 239, R197–R213 (1980).
  Article CAS PubMed Google Scholar
• Goss, R. J. Principles of Regeneration. (Academic Press, New York, 1969).
  Google Scholar
• Reichman, J. Evolution of regeneration capabilities. Am. Nat. 123, 752–763 (1984).
  Article Google Scholar
• Guffey, C. Costs associated with leg autotomy in the harvestmen Leiobunum nigripes and Leiobunum vittatum (Arachnida: Opiliones). Can. J. Zool. 77, 824–830 (1999).
  Article Google Scholar
• Brueseke, M. A. et al. Leg autotomy in the wolf spider Pardosa milvina: a common phenomenon with few apparent costs. Am. Midl. Nat. 146, 153–160 (2001).
  Article Google Scholar
• Brautigam, S. E. & Persons, M. H. The effect of limb loss on the courtship and mating behavior of the wolf spider Pardosa milvina (Araneae: Lycosidae). Insect Behav. 16, 571–587 (2003).
  Article Google Scholar
• Luyckx, V. A. & Brenner, B. M. The clinical importance of nephron mass. J. Am. Soc. Nephrol. 21, 898–910 (2010).
  Article PubMed Google Scholar
• Tan, J. C. et al. Glomerular function, structure, and number in renal allografts from older deceased donors. J. Am. Soc. Nephrol. 20, 181–188 (2009).
  Article PubMed PubMed Central Google Scholar