Tracking the stochastic fate of cells of the renin lineage after podocyte depletion using multicolor reporters and intravital imaging

PLoS ONE

Volumn 12, Issue 3, 2017, Pages

  Kaverina, Natalya V ^a   Kadoya, Hiroyuki ^b,c   Eng, Diana G ^a   Rusiniak, Michael E ^d   Sequeira Lopez, Maria Luisa S ^e   Gomez, R Ariel ^e   Pippin, Jeffrey W ^a   Gross, Kenneth W ^d   Peti Peterdi, Janos ^b   Shankland, Stuart J ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c KAWASAKI MEDICAL SCHOOL   (Japan)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLAUDIN 1; CYAN FLUORESCENT PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1C; GREEN FLUORESCENT PROTEIN; NEPHRIN; PODOCIN; RED FLUORESCENT PROTEIN; RENIN; TRANSCRIPTION FACTOR PAX8; WT1 PROTEIN; YELLOW FLUORESCENT PROTEIN; CDKN1C PROTEIN, MOUSE; CLDN1 PROTEIN, MOUSE; MEMBRANE PROTEIN; PAX8 PROTEIN, MOUSE; REPRESSOR PROTEIN; SIGNAL PEPTIDE; WT1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOWMAN CAPSULE; CELL DAMAGE; CELL DENSITY; CELL FATE; CELL LINEAGE; CELL MIGRATION; CLONAL VARIATION; CONTROLLED STUDY; DEPLETION; EPITHELIUM CELL; FOCAL GLOMERULOSCLEROSIS; INTRAVITAL MICROSCOPY; JUXTAGLOMERULAR CELL; KIDNEY PROXIMAL TUBULE; MESANGIUM CELL; MOUSE; MULTIPHOTON MICROSCOPY; NONHUMAN; PLASMA RENIN ACTIVITY; PODOCYTE; PROGENITOR CELL LINE; ADULT STEM CELL; ANIMAL; CELL MOTION; CYTOLOGY; DISEASE MODEL; FEMALE; GLOMERULUS; MARKOV CHAIN; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ADULT STEM CELLS; ANIMALS; CELL LINEAGE; CELL MOVEMENT; CLAUDIN-1; CYCLIN-DEPENDENT KINASE INHIBITOR P57; DISEASE MODELS, ANIMAL; EPITHELIAL CELLS; FEMALE; GLOMERULOSCLEROSIS, FOCAL SEGMENTAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRAVITAL MICROSCOPY; KIDNEY GLOMERULUS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; PAX8 TRANSCRIPTION FACTOR; PODOCYTES; RENIN; REPRESSOR PROTEINS; STOCHASTIC PROCESSES;

EID: 85016083782     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0173891     Document Type: Article

References (36)

1. Asanuma K, Yanagida-Asanuma E, Takagi M, Kodama F, Tomino Y. The role of podocytes in proteinuria. Nephrology. 2007; 12 Suppl 3:S15-20. https://doi.org/10.1111/j.1440-1797.2007.00876.x PMID: 17995522
2. Peired A, Lazzeri E, Lasagni L, Romagnani P. Glomerular regeneration: when can the kidney regenerate from injury and what turns failure into success? Nephron Experimental nephrology. 2014; 126 (2):70. https://doi.org/10.1159/000360669 PMID: 24854644
3. Wu DT, Bitzer M, Ju W, Mundel P, Bottinger EP. TGF-beta concentration specifies differential signaling profiles of growth arrest/differentiation and apoptosis in podocytes. Journal of the American Society of Nephrology JASN. 2005; 16(11):3211-21. https://doi.org/10.1681/ASN.2004121055 PMID: 16207831
4. D'Agati VD. Pathobiology of focal segmental glomerulosclerosis: new developments. Current opinion in nephrology and hypertension. 2012; 21(3):243-50. https://doi.org/10.1097/MNH.0b013e32835200df PMID: 22357339
5. Wharram BL, Goyal M, Wiggins JE, Sanden SK, Hussain S, Filipiak WE, et al. Podocyte depletion causes glomerulosclerosis: diphtheria toxin-induced podocyte depletion in rats expressing human diphtheria toxin receptor transgene. Journal of the American Society of Nephrology JASN. 2005; 16 (10):2941-52. https://doi.org/10.1681/ASN.2005010055 PMID: 16107576
6. Matsusaka T, Xin J, Niwa S, Kobayashi K, Akatsuka A, Hashizume H, et al. Genetic engineering of glomerular sclerosis in the mouse via control of onset and severity of podocyte-specific injury. Journal of the American Society of Nephrology JASN. 2005; 16(4):1013-23. https://doi.org/10.1681/ASN. 2004080720 PMID: 15758046
7. Grahammer F, Wanner N, Huber TB. Podocyte regeneration: who can become a podocyte? The American journal of pathology. 2013; 183(2):333-5. https://doi.org/10.1016/j.ajpath.2013.04.009 PMID: 23727347
8. Shankland SJ, Pippin JW, Duffield JS. Progenitor cells and podocyte regeneration. Seminars in nephrology. 2014; 34(4):418-28. PubMed Central PMCID: PMC4163204. https://doi.org/10.1016/j. semnephrol.2014.06.008 PMID: 25217270
9. Moeller MJ, Smeets B. Role of parietal epithelial cells in kidney injury: the case of rapidly progressing glomerulonephritis and focal and segmental glomerulosclerosis. Nephron Experimental nephrology. 2014; 126(2):97. https://doi.org/10.1159/000360677 PMID: 24854649
10. Castellanos-Rivera RM, Pentz ES, Lin E, Gross KW, Medrano S, Yu J, et al. Recombination signal binding protein for Ig-kappaJ region regulates juxtaglomerular cell phenotype by activating the myo-endocrine program and suppressing ectopic gene expression. Journal of the American Society of Nephrology JASN. 2015; 26(1):67-80. PubMed Central PMCID: PMC4279731. https://doi.org/10.1681/ ASN.2013101045 PMID: 24904090
11. Sequeira Lopez ML, Pentz ES, Nomasa T, Smithies O, Gomez RA. Renin cells are precursors for multiple cell types that switch to the renin phenotype when homeostasis is threatened. Developmental cell. 2004; 6(5):719-28. PMID: 15130496
12. Pichaiwong W, Hudkins KL, Wietecha T, Nguyen TQ, Tachaudomdach C, Li W, et al. Reversibility of structural and functional damage in a model of advanced diabetic nephropathy. Journal of the American Society of Nephrology JASN. 2013; 24(7):1088-102. PubMed Central PMCID: PMC3699819. https:// doi.org/10.1681/ASN.2012050445 PMID: 23641056
13. Pippin JW, Kaverina NV, Eng DG, Krofft RD, Glenn ST, Duffield JS, et al. Cells of renin lineage are adult pluri-potent progenitors in experimental glomerular disease. American journal of physiology Renal physiology. 2015:ajprenal 00438 2014.
14. Castellanos Rivera RM, Monteagudo MC, Pentz ES, Glenn ST, Gross KW, Carretero O, et al. Transcriptional regulator RBP-J regulates the number and plasticity of renin cells. Physiological genomics. 2011; 43(17):1021-8. PubMed Central PMCID: PMC3180736. https://doi.org/10.1152/ physiolgenomics.00061.2011 PMID: 21750232
15. Lichtnekert J, Kaverina NV, Eng DG, Gross KW, Kutz JN, Pippin JW, et al. Renin-Angiotensin-Aldosterone System Inhibition Increases Podocyte Derivation from Cells of Renin Lineage. Journal of the American Society of Nephrology JASN. 2016.
16. Thoma C. Glomerular disease: To the rescue-migrating renin lineage cells heal the injured glomerular mesangium. Nature reviews Nephrology. 2014; 10(8):424.
17. Starke C, Betz H, Hickmann L, Lachmann P, Neubauer B, Kopp JB, et al. Renin lineage cells repopulate the glomerular mesangium after injury. J Am Soc Nephrol. 2015; 26(1):48-54. PubMed Central PMCID: PMCPMC4279744. https://doi.org/10.1681/ASN.2014030265 PMID: 24904091
18. Lin EE, Sequeira-Lopez ML, Gomez RA. RBP-J in FOXD1+ renal stromal progenitors is crucial for the proper development and assembly of the kidney vasculature and glomerular mesangial cells. American journal of physiology Renal physiology. 2014; 306(2):F249-58. PubMed Central PMCID: PMC3920017. https://doi.org/10.1152/ajprenal.00313.2013 PMID: 24226518
19. Stefanska A, Peault B, Mullins JJ. Renal pericytes: multifunctional cells of the kidneys. Pflugers Archiv European journal of physiology. 2013; 465(6):767-73. https://doi.org/10.1007/s00424-013-1263-7 PMID: 23588377
20. Berg AC, Chernavvsky-Sequeira C, Lindsey J, Gomez RA, Sequeira-Lopez ML. Pericytes synthesize renin. World journal of nephrology. 2013; 2(1):11-6. PubMed Central PMCID: PMC3782206. https:// doi.org/10.5527/wjn.v2.i1.11 PMID: 24175260
21. Nezu M, Souma T, Yamamoto M. [Renal erythropoietin-producing cells and kidney disease]. Nihon rinsho Japanese journal of clinical medicine. 2014; 72(9):1691-700. PMID: 25518424
22. Gharib SA, Pippin JW, Ohse T, Pickering SG, Krofft RD, Shankland SJ. Transcriptional landscape of glomerular parietal epithelial cells. PloS one. 2014; 9(8):e105289. PubMed Central PMCID: PMC4134297. https://doi.org/10.1371/journal.pone.0105289 PMID: 25127402
23. Di Girolamo N, Bobba S, Raviraj V, Delic NC, Slapetova I, Nicovich PR, et al. Tracing the fate of limbal epithelial progenitor cells in the murine cornea. Stem cells. 2015; 33(1):157-69. https://doi.org/10.1002/ stem.1769 PMID: 24966117
24. Snippert HJ, van der Flier LG, Sato T, van Es JH, van den Born M, Kroon-Veenboer C, et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell. 2010; 143(1):134-44. https://doi.org/10.1016/j.cell.2010.09.016 PMID: 20887898
25. Ritsma L, Steller EJ, Ellenbroek SI, Kranenburg O, Borel Rinkes IH, van Rheenen J. Surgical implantation of an abdominal imaging window for intravital microscopy. Nature protocols. 2013; 8(3):583-94. https://doi.org/10.1038/nprot.2013.026 PMID: 23429719
26. Hackl MJ, Burford JL, Villanueva K, Lam L, Susztak K, Schermer B, et al. Tracking the fate of glomerular epithelial cells in vivo using serial multiphoton imaging in new mouse models with fluorescent lineage tags. Nature medicine. 2013; 19(12):1661-6. PubMed Central PMCID: PMC3884556. https://doi.org/ 10.1038/nm.3405 PMID: 24270544
27. Zhang J, Pippin JW, Vaughan MR, Krofft RD, Taniguchi Y, Romagnani P, et al. Retinoids augment the expression of podocyte proteins by glomerular parietal epithelial cells in experimental glomerular disease. Nephron Experimental nephrology. 2012; 121(1-2):e23-37. PubMed Central PMCID: PMC3574166. https://doi.org/10.1159/000342808 PMID: 23107969
28. Zhang J, Pippin JW, Krofft RD, Naito S, Liu ZH, Shankland SJ. Podocyte repopulation by renal progenitor cells following glucocorticoids treatment in experimental FSGS. American journal of physiology Renal physiology. 2013; 304(11):F1375-89. PubMed Central PMCID: PMC3680690. https://doi.org/10. 1152/ajprenal.00020.2013 PMID: 23486009
29. Kang JJ, Toma I, Sipos A, McCulloch F, Peti-Peterdi J. Quantitative imaging of basic functions in renal (patho)physiology. American journal of physiology Renal physiology. 2006; 291(2):F495-502. https:// doi.org/10.1152/ajprenal.00521.2005 PMID: 16609147
30. Venkatareddy M, Wang S, Yang Y, Patel S, Wickman L, Nishizono R, et al. Estimating podocyte number and density using a single histologic section. Journal of the American Society of Nephrology JASN. 2014; 25(5):1118-29. PubMed Central PMCID: PMC4005315. https://doi.org/10.1681/ASN. 2013080859 PMID: 24357669
31. Kaverina NV, Eng DG, Schneider RR, Pippin JW, Shankland SJ. Partial podocyte replenishment in experimental FSGS derives from nonpodocyte sources. Am J Physiol Renal Physiol. 2016; 310(11): F1397-413. PubMed Central PMCID: PMCPMC4935768. https://doi.org/10.1152/ajprenal.00369.2015 PMID: 27076646
32. Eng DG, Sunseri MW, Kaverina NV, Roeder SS, Pippin JW, Shankland SJ. Glomerular parietal epithelial cells contribute to adult podocyte regeneration in experimental focal segmental glomerulosclerosis. Kidney Int. 2015; 88(5):999-1012. PubMed Central PMCID: PMCPMC4654724. https://doi.org/10. 1038/ki.2015.152 PMID: 25993321
33. Zhang J, Yanez D, Floege A, Lichtnekert J, Krofft RD, Liu ZH, et al. ACE-inhibition increases podocyte number in experimental glomerular disease independent of proliferation. J Renin Angiotensin Aldosterone Syst. 2015; 16(2):234-48. PubMed Central PMCID: PMCPMC4412792. https://doi.org/10.1177/ 1470320314543910 PMID: 25143333
34. Susztak K, Raff AC, Schiffer M, Bottinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes. 2006; 55 (1):225-33. PMID: 16380497
35. Ohse T, Chang AM, Pippin JW, Jarad G, Hudkins KL, Alpers CE, et al. A new function for parietal epithelial cells: a second glomerular barrier. American journal of physiology Renal physiology. 2009; 297 (6):F1566-74. PubMed Central PMCID: PMC2801333. https://doi.org/10.1152/ajprenal.00214.2009 PMID: 19794110
36. Pippin JW, Sparks MA, Glenn ST, Buitrago S, Coffman TM, Duffield JS, et al. Cells of renin lineage are progenitors of podocytes and parietal epithelial cells in experimental glomerular disease. Am J Pathol. 2013; 183(2):542-57. PubMed Central PMCID: PMCPMC3730767. https://doi.org/10.1016/j.ajpath. 2013.04.024 PMID: 23769837