The Yin and Yang of Kidney Development and Wilms' Tumors

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2015 Mar 5

PMID 25737276

Citations 78

Authors

Peter Hohenstein

Kathy Pritchard-Jones

Jocelyn Charlton

Affiliations

Soon will be listed here.

Abstract

Wilms' tumor, or nephroblastoma, is the most common pediatric renal cancer. The tumors morphologically resemble embryonic kidneys with a disrupted architecture and are associated with undifferentiated metanephric precursors. Here, we discuss genetic and epigenetic findings in Wilms' tumor in the context of renal development. Many of the genes implicated in Wilms' tumorigenesis are involved in the control of nephron progenitors or the microRNA (miRNA) processing pathway. Whereas the first group of genes has been extensively studied in normal development, the second finding suggests important roles for miRNAs in general-and specific miRNAs in particular-in normal kidney development that still await further analysis. The recent identification of Wilms' tumor cancer stem cells could provide a framework to integrate these pathways and translate them into new or improved therapeutic interventions.

Citing Articles

Inter-Ethnic Variations in the Clinical, Pathological, and Molecular Characteristics of Wilms Tumor.

Lim K, Loh A Cancers (Basel). 2024; 16(17).

PMID: 39272909 PMC: 11393868. DOI: 10.3390/cancers16173051.

Single-cell multiomics reveals ENL mutation perturbs kidney developmental trajectory by rewiring gene regulatory landscape.

Song L, Li Q, Xia L, Sahay A, Qiu Q, Li Y Nat Commun. 2024; 15(1):5937.

PMID: 39009564 PMC: 11250843. DOI: 10.1038/s41467-024-50171-w.

LMO family gene polymorphisms and Wilms tumor susceptibility in Chinese children: a five-center case-control study.

Fu W, Deng L, Yan X, Hua R, Zhang J, Zhou H BMC Cancer. 2024; 24(1):772.

PMID: 38937681 PMC: 11209997. DOI: 10.1186/s12885-024-12557-3.

Characterization of Alternative Splicing in High-Risk Wilms' Tumors.

Trink Y, Urbach A, Dekel B, Hohenstein P, Goldberger J, Kalisky T Int J Mol Sci. 2024; 25(8).

PMID: 38674106 PMC: 11050615. DOI: 10.3390/ijms25084520.

The Burgeoning Significance of Liquid-Liquid Phase Separation in the Pathogenesis and Therapeutics of Cancers.

Xu W, Qu Q, Zhuang H, Teng X, Wei Y, Luo J Int J Biol Sci. 2024; 20(5):1652-1668.

PMID: 38481812 PMC: 10929184. DOI: 10.7150/ijbs.92988.

References

Sun F, Dean W, Kelsey G, Allen N, Reik W . Transactivation of Igf2 in a mouse model of Beckwith-Wiedemann syndrome. Nature. 1998; 389(6653):809-15. DOI: 10.1038/39797. View

Prosser H, Koike-Yusa H, Cooper J, Law F, Bradley A . A resource of vectors and ES cells for targeted deletion of microRNAs in mice. Nat Biotechnol. 2011; 29(9):840-5. PMC: 3242032. DOI: 10.1038/nbt.1929. View

Dekel B, Metsuyanim S, Schmidt-Ott K, Fridman E, Jacob-Hirsch J, Simon A . Multiple imprinted and stemness genes provide a link between normal and tumor progenitor cells of the developing human kidney. Cancer Res. 2006; 66(12):6040-9. DOI: 10.1158/0008-5472.CAN-05-4528. View

Ding L, Paszkowski-Rogacz M, Nitzsche A, Slabicki M, Heninger A, de Vries I . A genome-scale RNAi screen for Oct4 modulators defines a role of the Paf1 complex for embryonic stem cell identity. Cell Stem Cell. 2009; 4(5):403-15. DOI: 10.1016/j.stem.2009.03.009. View

Das A, Tanigawa S, Karner C, Xin M, Lum L, Chen C . Stromal-epithelial crosstalk regulates kidney progenitor cell differentiation. Nat Cell Biol. 2013; 15(9):1035-44. PMC: 3891676. DOI: 10.1038/ncb2828. View

Ehrlich D, Bruder E, Thome M, Gutt C, von Knebel Doeberitz M, Niggli F . Nuclear accumulation of beta-catenin protein indicates activation of wnt signaling in chemically induced rat nephroblastomas. Pediatr Dev Pathol. 2009; 13(1):1-8. PMC: 2990985. DOI: 10.2350/08-03-0443.1. View

Koufos A, Grundy P, Morgan K, Aleck K, Hadro T, Lampkin B . Familial Wiedemann-Beckwith syndrome and a second Wilms tumor locus both map to 11p15.5. Am J Hum Genet. 1989; 44(5):711-9. PMC: 1715635. View

Berger A, Knudson A, Pandolfi P . A continuum model for tumour suppression. Nature. 2011; 476(7359):163-9. PMC: 3206311. DOI: 10.1038/nature10275. View

Hubertus J, Lacher M, Rottenkolber M, Muller-Hocker J, Berger M, Stehr M . Altered expression of imprinted genes in Wilms tumors. Oncol Rep. 2010; 25(3):817-23. DOI: 10.3892/or.2010.1113. View

10.

Ehrlich M, Hopkins N, Jiang G, Dome J, Yu M, Woods C . Satellite DNA hypomethylation in karyotyped Wilms tumors. Cancer Genet Cytogenet. 2003; 141(2):97-105. DOI: 10.1016/s0165-4608(02)00668-4. View

11.

Schneid H, Vazquez M, Seurin D, Le Bouc Y . Loss of heterozygosity in non-tumoral tissue in two children with Beckwith-Wiedemann syndrome. Growth Regul. 1991; 1(4):168-70. View

12.

Hubertus J, Zitzmann F, Trippel F, Muller-Hocker J, Stehr M, von Schweinitz D . Selective methylation of CpGs at regulatory binding sites controls NNAT expression in Wilms tumors. PLoS One. 2013; 8(6):e67605. PMC: 3692448. DOI: 10.1371/journal.pone.0067605. View

13.

Koller K, Das S, Leuschner I, Korbelius M, Hoefler G, Guertl B . Identification of the transcription factor HOXB4 as a novel target of miR-23a. Genes Chromosomes Cancer. 2013; 52(8):709-15. DOI: 10.1002/gcc.22066. View

14.

Wagner K, Cooper W, Grundy R, Caldwell G, Jones C, Wadey R . Frequent RASSF1A tumour suppressor gene promoter methylation in Wilms' tumour and colorectal cancer. Oncogene. 2002; 21(47):7277-82. DOI: 10.1038/sj.onc.1205922. View

15.

Holm T, Jackson-Grusby L, Brambrink T, Yamada Y, Rideout 3rd W, Jaenisch R . Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell. 2005; 8(4):275-85. DOI: 10.1016/j.ccr.2005.09.007. View

16.

Stark K, Vainio S, Vassileva G, McMahon A . Epithelial transformation of metanephric mesenchyme in the developing kidney regulated by Wnt-4. Nature. 1994; 372(6507):679-83. DOI: 10.1038/372679a0. View

17.

Huff V . Wilms' tumours: about tumour suppressor genes, an oncogene and a chameleon gene. Nat Rev Cancer. 2011; 11(2):111-21. PMC: 4332715. DOI: 10.1038/nrc3002. View

18.

Harari-Steinberg O, Metsuyanim S, Omer D, Gnatek Y, Gershon R, Pri-Chen S . Identification of human nephron progenitors capable of generation of kidney structures and functional repair of chronic renal disease. EMBO Mol Med. 2013; 5(10):1556-68. PMC: 3799579. DOI: 10.1002/emmm.201201584. View

19.

Major M, Camp N, Berndt J, Yi X, Goldenberg S, Hubbert C . Wilms tumor suppressor WTX negatively regulates WNT/beta-catenin signaling. Science. 2007; 316(5827):1043-6. DOI: 10.1126/science/1141515. View

20.

Ripoche M, Kress C, Poirier F, Dandolo L . Deletion of the H19 transcription unit reveals the existence of a putative imprinting control element. Genes Dev. 1997; 11(12):1596-604. DOI: 10.1101/gad.11.12.1596. View