Identification of a foetal epigenetic compartment in adult human kidney

References

• Schofield R. The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells. 1978;4(1–2):7–25.
   Google Scholar
• Crane GM, Jeffery E, Morrison SJ. Adult haematopoietic stem cell niches. Nat Rev Immunol. 2017;17(9):573–590.
   Google Scholar
• Tan DW, Barker N. Intestinal stem cells and their defining niche. Curr Top Dev Biol. 2014;107:77–107.
   Google Scholar
• Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7(2):150–161.
   Google Scholar
• Witzgall R, Brown D, Schwarz C, et al. Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J Clin Invest. 1994;93(5):2175–2188.
   Google Scholar
• Bonventre JV. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J Am Soc Nephrol. 2003;14(Suppl 1):S55–61.
   Google Scholar
• Humphreys BD, Czerniak S, DiRocco DP, et al. Repair of injured proximal tubule does not involve specialized progenitors. Proc Natl Acad Sci U S A. 2011;108(22):9226–9231.
   Google Scholar
• Angelotti ML, Ronconi E, Ballerini L, et al. Characterization of renal progenitors committed toward tubular lineage and their regenerative potential in renal tubular injury. Stem Cells. 2012;30:1714–1725.
   Google Scholar
• Villanueva S, Cespedes C, Vio CP. Ischemic acute renal failure induces the expression of a wide range of nephrogenic proteins. Am J Physiol Regul Integr Comp Physiol. 2006;290(4):R861–870.
   Google Scholar
• Oliver JA, Maarouf O, Cheema FH, et al. The renal papilla is a niche for adult kidney stem cells. J Clin Invest. 2004;114(6):795–804
   Google Scholar
• Vogetseder A, Karadeniz A, Kaissling B, et al. Tubular cell proliferation in the healthy rat kidney. Histochem Cell Biol. 2005;124(2):97–104.
   Google Scholar
• Oliver JA. Adult renal stem cells and renal repair. Curr Opin Nephrol Hypertens. 2004;13(1):17–22.
   Google Scholar
• Oliver JA, Maarouf O, Cheema FH, et al. The renal papilla is a niche for adult kidney stem cells. J Clin Invest. 2004;114(6):795–804.
   Google Scholar
• Oliver JA, Sampogna RV, Jalal S, et al. A subpopulation of label-retaining cells of the kidney papilla regenerates injured kidney medullary tubules. Stem Cell Reports. 2016;6(5):757–771.
   Google Scholar
• Kramann R, Kusaba T, Humphreys BD. Who regenerates the kidney tubule? Nephrol Dial Transplant. 2015;30(6):903–910.
   Google Scholar
• Little MH, Kairath P. Does renal repair recapitulate kidney development? J Am Soc Nephrol. 2017;28(1):34–46.
   Google Scholar
• Yatabe Y, Tavare S, Shibata D. Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci U S A. 2001;98(19):10839–10844.
   Google Scholar
• Roost MS, Slieker RC, Bialecka M, et al. DNA methylation and transcriptional trajectories during human development and reprogramming of isogenic pluripotent stem cells. Nat Commun. 2017;8(1):908.
   Google Scholar
• Hiler D, Chen X, Hazen J, et al. Quantification of retinogenesis in 3D cultures reveals epigenetic memory and higher efficiency in iPSCs derived from rod photoreceptors. Cell Stem Cell. 2015;17(1):101–115.
   Google Scholar
• Hu Q, Friedrich AM, Johnson LV, et al. Memory in induced pluripotent stem cells: reprogrammed human retinal-pigmented epithelial cells show tendency for spontaneous redifferentiation. Stem Cells. 2010;28(11):1981–1991.
   Google Scholar
• Hargus G, Ehrlich M, Arauzo-Bravo MJ, et al. Origin-dependent neural cell identities in differentiated human iPSCs in vitro and after transplantation into the mouse brain. Cell Rep. 2014;8(6):1697–1703.
   Google Scholar
• Bar-Nur O, Russ HA, Efrat S, et al. Epigenetic memory and preferential lineage-specific differentiation in induced pluripotent stem cells derived from human pancreatic islet beta cells. Cell Stem Cell. 2011;9(1):17–23.
   Google Scholar
• Quattrocelli M, Swinnen M, Giacomazzi G, et al. Mesodermal iPSC-derived progenitor cells functionally regenerate cardiac and skeletal muscle. J Clin Invest. 2015;125(12):4463–4482.
   Google Scholar
• Kim K, Zhao R, Doi A, et al. Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat Biotechnol. 2011;29(12):1117–1119.
   Google Scholar
• Vitaloni M, Pulecio J, Bilic J, et al. MicroRNAs contribute to induced pluripotent stem cell somatic donor memory. J Biol Chem. 2014;289(4):2084–2098.
   Google Scholar
• Polo JM, Liu S, Figueroa ME, et al. Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol. 2010;28(8):848–855.
   Google Scholar
• Ohi Y, Qin H, Hong C, et al. Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat Cell Biol. 2011;13(5):541–549.
   Google Scholar
• Salas LA, Wiencke JK, Koestler DC, et al. Tracing human stem cell lineage during development using DNA methylation. Genome Res. 2018;28(9):1285–1295.
   Google Scholar
• Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;132(4):631–644.
   Google Scholar
• Copley MR, Eaves CJ. Developmental changes in hematopoietic stem cell properties. Exp Mol Med. 2013;45(11):e55.
   Google Scholar
• Manesia JK, Franch M, Tabas-Madrid D, et al. Distinct molecular signature of murine fetal liver and adult hematopoietic stem cells identify novel regulators of hematopoietic stem cell function. Stem Cells Dev. 2017;26(8):573–584.
   Google Scholar
• Zhang Z, Wiencke JK, Koestler DC, et al. Absence of an embryonic stem cell DNA methylation signature in human cancer. BMC Cancer. 2019;19(1):711.
   Google Scholar
• McMahon AP. Development of the mammalian kidney. Curr Top Dev Biol. 2016;117:31–64.
   Google Scholar
• Lee JW, Chou CL, Knepper MA. Deep sequencing in microdissected renal tubules identifies nephron segment-specific transcriptomes. J Am Soc Nephrol. 2015;26(11):2669–2677.
   Google Scholar
• Higgins JP, Wang L, Kambham N, et al. Gene expression in the normal adult human kidney assessed by complementary DNA microarray. Mol Biol Cell. 2004;15(2):649–656.
   Google Scholar
• Papadopoulos T, Krochmal M, Cisek K, et al. Omics databases on kidney disease: where they can be found and how to benefit from them. Clin Kidney J. 2016;9(3):343–352.
   Google Scholar
• Brezis M, Rosen S. Hypoxia of the renal medulla–its implications for disease. N Engl J Med. 1995;332(10):647–655.
   Google Scholar
• Russell PS, Hong J, Windsor JA, et al. Renal lymphatics: anatomy, physiology, and clinical implications. Front Physiol. 2019;10:251.
   Google Scholar
• Neuhofer W, Beck FX. Survival in hostile environments: strategies of renal medullary cells. Physiology (Bethesda). 2006;21:171–180.
   Google Scholar
• Chen Y, Fry BC, Layton AT. Modeling glucose metabolism and lactate production in the kidney. Math Biosci. 2017;289:116–129.
   Google Scholar
• Jauniaux E, Gulbis B, Burton GJ. Physiological implications of the materno-fetal oxygen gradient in human early pregnancy. Reprod Biomed Online. 2003;7(2):250–253.
   Google Scholar
• Dunwoodie SL. The role of hypoxia in development of the mammalian embryo. Dev Cell. 2009;17(6):755–773.
   Google Scholar
• Patel SR, Ranghini E, Dressler GR. Mechanisms of gene activation and repression by pax proteins in the developing kidney. Pediatr Nephrol. 2014;29(4):589–595.
   Google Scholar
• Kobayashi A, Valerius MT, Mugford JW, et al. Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development. Cell Stem Cell. 2008;3(2):169–181.
   Google Scholar
• Humphreys BD, Valerius MT, Kobayashi A, et al. Intrinsic epithelial cells repair the kidney after injury. Cell Stem Cell. 2008;2(3):284–291.
   Google Scholar
• Sharma R, Sanchez-Ferras O, Bouchard M. Pax genes in renal development, disease and regeneration. Semin Cell Dev Biol. 2015;44:97–106.
   Google Scholar
• Alarcon P, Rodriguez-Seguel E, Fernandez-Gonzalez A, et al. A dual requirement for Iroquois genes during xenopus kidney development. Dev. 2008;135(19):3197–3207.
   Google Scholar
• Massa F, Garbay S, Bouvier R, et al. Hepatocyte nuclear factor 1beta controls nephron tubular development. Dev. 2013;140(4):886–896.
   Google Scholar
• Heliot C, Desgrange A, Buisson I, et al. HNF1B controls proximal-intermediate nephron segment identity in vertebrates by regulating notch signalling components and Irx1/2. Dev. 2013;140(4):873–885.
   Google Scholar
• Patterson LT, Potter SS. Atlas of Hox gene expression in the developing kidney. Dev Dyn. 2004;229(4):771–779.
   Google Scholar
• Pickering CM, Grady C, Medvar B, et al. Proteomic profiling of nuclear fractions from native renal inner medullary collecting duct cells. Physiol Genomics. 2016;48(2):154–166.
   Google Scholar
• Walker KA, Sims-Lucas S, Bates CM. Fibroblast growth factor receptor signaling in kidney and lower urinary tract development. Pediatr Nephrol. 2016;31(6):885–895.
   Google Scholar
• Villanueva S, Cespedes C, Gonzalez AA, et al. Inhibition of bFGF-receptor type 2 increases kidney damage and suppresses nephrogenic protein expression after ischemic acute renal failure. Am J Physiol Regul Integr Comp Physiol. 2008;294:R819–828.
   Google Scholar
• Villanueva S, Cespedes C, Gonzalez A, et al. bFGF induces an earlier expression of nephrogenic proteins after ischemic acute renal failure. Am J Physiol Regul Integr Comp Physiol. 2006;291:R1677–1687.
   Google Scholar
• Villanueva S, Glavic A, Ruiz P, et al. Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction. Dev Biol. 2002;241(2):289–301.
   Google Scholar
• Lindgren D, Eriksson P, Krawczyk K, et al. Cell-type-specific gene programs of the normal human nephron define kidney cancer subtypes. Cell Rep. 2017;20(6):1476–1489.
   Google Scholar
• Lindgren D, Sjolund J, Axelson H. tracing renal cell carcinomas back to the nephron. Trends Cancer. 2018;4:472–484.
   Google Scholar
• Park J, Shrestha R, Qiu C, et al. Single-cell transcriptomics of the mouse kidney reveals potential cellular targets of kidney disease. Sci. 2018;360(6390):758–763.
   Google Scholar
• Saroufim A, Messai Y, Hasmim M, et al. Tumoral CD105 is a novel independent prognostic marker for prognosis in clear-cell renal cell carcinoma. Br J Cancer. 2014;110(7):1778–1784.
   Google Scholar
• Mikami S, Mizuno R, Kosaka T, et al. Expression of TNF-alpha and CD44 is implicated in poor prognosis, cancer cell invasion, metastasis and resistance to the sunitinib treatment in clear cell renal cell carcinomas. Int J Cancer. 2015;136(7):1504–1514.
   Google Scholar
• Li X, Ma X, Chen L, et al. Prognostic value of CD44 expression in renal cell carcinoma: a systematic review and meta-analysis. Sci Rep. 2015;5(1):13157.
   Google Scholar
• Peired AJ, Sisti A, Romagnani P. Mesenchymal stem cell-based therapy for kidney disease: a review of clinical evidence. Stem Cells Int. 2016;2016:4798639.
   Google Scholar
• Farkas SA, Milutin-Gasperov N, Grce M, et al. Genome-wide DNA methylation assay reveals novel candidate biomarker genes in cervical cancer. Epigenet. 2013;8(11):1213–1225.
   Google Scholar
• Smith RG, Hannon E, De Jager PL, et al. Elevated DNA methylation across a 48-kb region spanning the HOXA gene cluster is associated with Alzheimer’s disease neuropathology. Alzheimers Dement. 2018;14(12):1580–1588.
   Google Scholar
• Legendre CR, Demeure MJ, Whitsett TG, et al. Pathway implications of aberrant global methylation in adrenocortical cancer. PLoS One. 2016;11(3):e0150629.
   Google Scholar
• Huang KK, Ramnarayanan K, Zhu F, et al. Genomic and epigenomic profiling of high-risk intestinal metaplasia reveals molecular determinants of progression to gastric cancer. Cancer Cell. 2018;33(1):137–150 e135.
   Google Scholar
• Price EM, Penaherrera MS, Portales-Casamar E, et al. Profiling placental and fetal DNA methylation in human neural tube defects. Epigenet Chromatin. 2016;9(1):6.
   Google Scholar
• Charlton J, Williams RD, Weeks M, et al. Methylome analysis identifies a wilms tumor epigenetic biomarker detectable in blood. Genome Biol. 2014;15(8):434.
   Google Scholar
• Ko YA, Mohtat D, Suzuki M, et al. Cytosine methylation changes in enhancer regions of core pro-fibrotic genes characterize kidney fibrosis development. Genome Biol. 2013;14(10):R108.
   Google Scholar
• Acevedo N, Reinius LE, Vitezic M, et al. Age-associated DNA methylation changes in immune genes, histone modifiers and chromatin remodeling factors within 5 years after birth in human blood leukocytes. Clin Epigenetics. 2015;7(1):34.
   Google Scholar
• Urdinguio RG, Torro MI, Bayon GF, et al. Longitudinal study of DNA methylation during the first 5 years of life. J Transl Med. 2016;14:160.
   Google Scholar
• Alisch RS, arwick BG, Chopra P, et al. Age-associated DNA methylation in pediatric populations. Genome Res. 2012;22(4):623–632.
   Google Scholar
• Hannum G, Guinney J, Zhao L, et al. Genome-wide methylation profiles reveal quantitative views of human aging rates. Mol Cell. 2013;49(2):359–367.
   Google Scholar
• Reinius LE, Acevedo N, Joerink M, et al. Differential DNA methylation in purified human blood cells: implications for cell lineage and studies on disease susceptibility. PLoS One. 2012;7(7):e41361.
   Google Scholar
• Tserel L, Kolde R, Limbach M, et al. Age-related profiling of DNA methylation in CD8+ T cells reveals changes in immune response and transcriptional regulator genes. Sci Rep. 2015;5(1):13107.
   Google Scholar
• Heyn H, Li N, Ferreira HJ, et al. Distinct DNA methylomes of newborns and centenarians. Proc Natl Acad Sci U S A. 2012;109(26):10522–10527.
   Google Scholar
• Bakulski KM, Feinberg JI, Andrews SV, et al. DNA methylation of cord blood cell types: Applications for mixed cell birth studies. Epigenetics. 2016;11(5):354–362
   Google Scholar
• Gervin K, Page CM, Aass HC, et al. Cell type specific DNA methylation in cord blood: A 450K-reference data set and cell count-based validation of estimated cell type composition. Epigenetics. 2016;11(9):690–698.
   Google Scholar
• Hart T, Komori HK, LaMere S, et al. Finding the active genes in deep RNA-seq gene expression studies. BMC Genomics. 2013;14(1):778.
   Google Scholar
• Laurens Van Der Maaten GH. visualizing data using t-SNE. J Mach Learn Res. 2008;9:2579-2605.
   Google Scholar
• Krijthe JH Rtsne: t-distributed stochastic neighbor embedding using a barnes-hut implementation. (2015).
   Google Scholar
• Anders S, Pyl PT, Huber W. HTSeq–a Python framework to work with high-throughput sequencing data. Bioinf. 2015;31:166–169.
   Google Scholar
• Bakulski KM, Feinberg JI, Andrews SV, et al. DNA methylation of cord blood cell types: applications for mixed cell birth studies. Epigenet. 2016;11(5):354–362.
   Google Scholar
• Houseman EA, Accomando WP, Koestler DC, et al. DNA methylation arrays as surrogate measures of cell mixture distribution. BMC Bioinf. 2012;13:86.
   Google Scholar
• Zhou Y, Zhou B, Pache L, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10(1):1523.
   Google Scholar
• Flechner SM, Kurian SM, Head SR, et al. Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes. Am J Transplant. 2004;4(9):1475–1489.
   Google Scholar
• Rodwell GE, Sonu R, Zahn JM, et al. A transcriptional profile of aging in the human kidney. PLoS Biol. 2004;2(12):e427.
   Google Scholar
• Molinaro AM, Lostritto K, Van Der Laan M. partDSA: deletion/substitution/addition algorithm for partitioning the covariate space in prediction. Bioinf. 2010;26(10):1357–1363.
   Google Scholar
• Lostritto K, Strawderman RL, Molinaro AM. A partitioning deletion/substitution/addition algorithm for creating survival risk groups. Biom. 2012;68(4):1146–1156.
   Google Scholar
• Stewart BJ, Ferdinand JR, Young MD, et al. Spatiotemporal immune zonation of the human kidney. Sci. 2019;365(6460):1461–1466.
   Google Scholar
• Wegener AM, Letourneur F, Hoeveler A, et al. The T cell receptor/CD3 complex is composed of at least two autonomous transduction modules. Cell. 1992;68(1):83–95.
   Google Scholar
• Hamilton KL, Devor DC. Basolateral membrane K+ channels in renal epithelial cells. Am J Physiol Renal Physiol. 2012;302(9):F1069–1081.
   Google Scholar
• Pulkkinen K, Murugan S, Vainio S. Wnt signaling in kidney development and disease. Organogenesis. 2008;4(2):55–59.
   Google Scholar
• Chen F. Genetic and developmental basis for urinary tract obstruction. Pediatr Nephrol. 2009;24(9):1621–1632.
   Google Scholar
• Vogels R, Charite J, De Graaff W, et al. Proximal cis-acting elements cooperate to set Hoxb-7 (Hox-2.3) expression boundaries in transgenic mice. Dev. 1993;118:71–82.
   Google Scholar
• Narlis M, Grote D, Gaitan Y, et al. Pax2 and Pax8 regulate branching morphogenesis and nephron differentiation in the developing kidney. J Am Soc Nephrol. 2007;18(4):1121–1129.
   Google Scholar
• Hamilton KL, Devor DC. Basolateral membrane K+ channels in renal epithelial cells. Am J Physiol Renal Physiol. 2012;302(9):F1069–F1081.
   Google Scholar
• Lindstrom NO, Tran T, Guo J, et al. Conserved and divergent molecular and anatomic features of human and mouse nephron patterning. J Am Soc Nephrol. 2018;29(3):825–840.
   Google Scholar
• Cheval L, Pierrat F, Rajerison R, et al. Of mice and men: divergence of gene expression patterns in kidney. PLoS One. 2012;7(10):e46876.
   Google Scholar
• Kusaba T, Lalli M, Kramann R, et al. Differentiated kidney epithelial cells repair injured proximal tubule. Proc Natl Acad Sci U S A. 2014;111(4):1527–1532.
   Google Scholar
• Huling J, Yoo JJ. Comparing adult renal stem cell identification, characterization and applications. J Biomed Sci. 2017;24(1):32.
   Google Scholar
• Rangarajan S, Sunil B, Fan C, et al. Distinct populations of label-retaining cells in the adult kidney are defined temporally and exhibit divergent regional distributions. Am J Physiol Renal Physiol. 2014;307(11):F1274–1282.
   Google Scholar
• Nombela-Arrieta C, Pivarnik G, Winkel B, et al. Quantitative imaging of haematopoietic stem and progenitor cell localization and hypoxic status in the bone marrow microenvironment. Nat Cell Biol. 2013;15(5):533–543.
   Google Scholar
• Ito K, Suda T. Metabolic requirements for the maintenance of self-renewing stem cells. Nat Rev Mol Cell Biol. 2014;15(4):243–256.
   Google Scholar
• Suda T, Takubo K, Semenza GL. Metabolic regulation of hematopoietic stem cells in the hypoxic niche. Cell Stem Cell. 2011;9(4):298–310.
   Google Scholar
• Morikawa T, Takubo K. Hypoxia regulates the hematopoietic stem cell niche. Pflugers Arch. 2016;468(1):13–22.
   Google Scholar
• Redondo PA, Pavlou M, Loizidou M, et al. Elements of the niche for adult stem cell expansion. J Tissue Eng. 2017;8:2041731417725464.
   Google Scholar