HNF1B mutations associate with hypomagnesemia and renal magnesium wasting.

Mutations in hepatocyte nuclear factor 1B (HNF1B), which is a transcription factor expressed in tissues including renal epithelia, associate with abnormal renal development. While studying renal phenotypes of children with HNF1B mutations, we identified a teenager who presented with tetany and hypomagnesemia. We retrospectively reviewed radiographic and laboratory data for all patients from a single center who had been screened for an HNF1B mutation. We found heterozygous mutations in 21 (23%) of 91 cases of renal malformation. All mutation carriers had abnormal fetal renal ultrasonography. Plasma magnesium levels were available for 66 patients with chronic kidney disease (stages 1 to 3). Striking, 44% (eight of 18) of mutation carriers had hypomagnesemia (<1.58 mg/dl) compared with 2% (one of 48) of those without mutations (P < 0.0001). The median plasma magnesium was significantly lower among mutation carriers than those without mutations (1.68 versus 2.02 mg/dl; P < 0.0001). Because hypermagnesuria and hypocalciuria accompanied the hypomagnesemia, we analyzed genes associated with hypermagnesuria and detected highly conserved HNF1 recognition sites in FXYD2, a gene that can cause autosomal dominant hypomagnesemia and hypocalciuria when mutated. Using a luciferase reporter assay, we demonstrated HNF1B-mediated transactivation of FXYD2. These results extend the phenotype of HNF1B mutations to include hypomagnesemia. HNF1B regulates transcription of FXYD2, which participates in the tubular handling of Mg(2+), thus describing a role for HNF1B not only in nephrogenesis but also in the maintenance of tubular function.

[1]  S. Ellard,et al.  Whole gene deletion of the hepatocyte nuclear factor-1beta gene in a patient with the prune-belly syndrome. , 2008, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[2]  A. Hattersley,et al.  Clinical implications of a molecular genetic classification of monogenic β-cell diabetes , 2008, Nature Clinical Practice Endocrinology &Metabolism.

[3]  R. Reilly,et al.  Hereditary etiologies of hypomagnesemia , 2008, Nature Clinical Practice Nephrology.

[4]  J. Hou,et al.  Claudin-16 and claudin-19 interact and form a cation-selective tight junction complex. , 2008, The Journal of clinical investigation.

[5]  A. Hattersley,et al.  Hepatocyte nuclear factor-1beta gene deletions--a common cause of renal disease. , 2007, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[6]  R. F. Luco,et al.  Distinct Roles of HNF1 Β , HNF1 α , and HNF4 α in Regulating Pancreas Development, Β -Cell Function and Growth , 2007 .

[7]  Sabine Tejpar,et al.  Impaired basolateral sorting of pro-EGF causes isolated recessive renal hypomagnesemia. , 2007, The Journal of clinical investigation.

[8]  Kjell Tullus,et al.  Progression of chronic renal failure in children with dysplastic kidneys , 2007, Pediatric Nephrology.

[9]  J. Schanstra,et al.  Anomalies of the TCF2 gene are the main cause of fetal bilateral hyperechogenic kidneys. , 2007, Journal of the American Society of Nephrology : JASN.

[10]  M. Hubank,et al.  Microarray interrogation of human metanephric mesenchymal cells highlights potentially important molecules in vivo. , 2007, Physiological genomics.

[11]  A. Woolf,et al.  Unilateral renal agenesis and the congenital solitary functioning kidney: developmental, genetic and clinical perspectives , 2007, BJU international.

[12]  S. Ellard,et al.  Hepatocyte nuclear factor‐1 beta mutations cause neonatal diabetes and intrauterine growth retardation: support for a critical role of HNF‐1β in human pancreatic development , 2006, Diabetic medicine : a journal of the British Diabetic Association.

[13]  R. Salomon,et al.  Prevalence of mutations in renal developmental genes in children with renal hypodysplasia: results of the ESCAPE study. , 2006, Journal of the American Society of Nephrology : JASN.

[14]  Mihaela Zavolan,et al.  Effects of Dicer and Argonaute down-regulation on mRNA levels in human HEK293 cells , 2006, Nucleic acids research.

[15]  R. Kleta,et al.  Bartter Syndromes and Other Salt-Losing Tubulopathies , 2006, Nephron Physiology.

[16]  H. Kusuhara,et al.  Regulation of the Expression of Human Organic Anion Transporter 3 by Hepatocyte Nuclear Factor 1α/β and DNA Methylation , 2006, Molecular Pharmacology.

[17]  C. Baumann,et al.  Severe pancreas hypoplasia and multicystic renal dysplasia in two human fetuses carrying novel HNF1beta/MODY5 mutations. , 2006, Human molecular genetics.

[18]  K. Geering FXYD proteins: new regulators of Na-K-ATPase. , 2006, American journal of physiology. Renal physiology.

[19]  G. Ryffel,et al.  Identification of target genes of the transcription factor HNF1β and HNF1α in a human embryonic kidney cell line , 2005 .

[20]  V. Vallon,et al.  Enhanced passive Ca2+ reabsorption and reduced Mg2+ channel abundance explains thiazide-induced hypocalciuria and hypomagnesemia. , 2005, The Journal of clinical investigation.

[21]  A. Hattersley,et al.  Mutations in hepatocyte nuclear factor-1β and their related phenotypes , 2005, Journal of Medical Genetics.

[22]  Cristel G. Thomas,et al.  Germline hepatocyte nuclear factor 1α and 1β mutations in renal cell carcinomas , 2005 .

[23]  Andreas Reimann,et al.  A transcriptional network in polycystic kidney disease , 2004, The EMBO journal.

[24]  T. Gudermann,et al.  Insights into the molecular nature of magnesium homeostasis. , 2004, American journal of physiology. Renal physiology.

[25]  P. Igarashi,et al.  Mutation of hepatocyte nuclear factor-1beta inhibits Pkhd1 gene expression and produces renal cysts in mice. , 2004, The Journal of clinical investigation.

[26]  F. Verrey,et al.  Isoform specificity of human Na+,K+‐ATPase localization and aldosterone regulation in mouse kidney cells , 2004, The Journal of physiology.

[27]  A. Hattersley,et al.  Atypical familial juvenile hyperuricemic nephropathy associated with a hepatocyte nuclear factor-1beta gene mutation. , 2003, Kidney international.

[28]  A. Edefonti,et al.  The biochemical diagnosis of Gitelman disease and the definition of "hypocalciuria" , 2003, Pediatric Nephrology.

[29]  A. Hattersley,et al.  Severe hyperglycemia after renal transplantation in a pediatric patient with a mutation of the hepatocyte nuclear factor-1beta gene. , 2002, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[30]  P. Igarashi,et al.  Regulation of kidney-specific Ksp-cadherin gene promoter by hepatocyte nuclear factor-1beta. , 2002, American journal of physiology. Renal physiology.

[31]  K. Sweadner,et al.  Distribution and oligomeric association of splice forms of Na(+)-K(+)-ATPase regulatory gamma-subunit in rat kidney. , 2002, American journal of physiology. Renal physiology.

[32]  A. Hattersley,et al.  Hepatocyte Nuclear Factor-1β: A New Kindred with Renal Cysts and Diabetes and Gene Expression in Normal Human Development , 2001 .

[33]  K. Sweadner,et al.  Genomic Organization of the Human FXYD2 Gene Encoding the γ Subunit of the Na,K-ATPase , 2000 .

[34]  H. Bokhoven,et al.  Dominant isolated renal magnesium loss is caused by misrouting of the Na+,K+-ATPase γ-subunit , 2000, Nature Genetics.

[35]  T. Frayling,et al.  Abnormal nephron development associated with a frameshift mutation in the transcription factor hepatocyte nuclear factor-1β1: 1See Editorial by Woolf, p. 1202 , 2000 .

[36]  M. Yaniv,et al.  Expression of the vHNF1/HNF1β homeoprotein gene during mouse organogenesis , 1999, Mechanisms of Development.

[37]  L. Bostad,et al.  A novel syndrome of diabetes mellitus, renal dysfunction and genital malformation associated with a partial deletion of the pseudo-POU domain of hepatocyte nuclear factor-1beta. , 1999, Human molecular genetics.

[38]  J. Takeda,et al.  Frameshift Mutation, A263fsinsGG, in the Hepatocyte Nuclear Factor-1β Gene Associated With Diabetes and Renal Dysfunction , 1998, Diabetes.

[39]  M. Elisaf,et al.  Fractional excretion of magnesium in normal subjects and in patients with hypomagnesemia. , 1997, Magnesium research.

[40]  M. Yaniv,et al.  HNF1, a homeoprotein member of the hepatic transcription regulatory network , 1992, BioEssays : news and reviews in molecular, cellular and developmental biology.

[41]  P. A. Friedman,et al.  Mechanism of calcium transport stimulated by chlorothiazide in mouse distal convoluted tubule cells. , 1992, The Journal of clinical investigation.

[42]  B. Levy-Wilson,et al.  Hepatocyte nuclear factor 1 and C/EBP are essential for the activity of the human apolipoprotein B gene second-intron enhancer , 1992, Molecular and cellular biology.

[43]  G. Crabtree,et al.  HNF-1, a member of a novel class of dimerizing homeodomain proteins. , 1991, The Journal of biological chemistry.

[44]  G. Crabtree,et al.  A variant nuclear protein in dedifferentiated hepatoma cells binds to the same functional sequences in the beta fibrinogen gene promoter as HNF‐1. , 1988, The EMBO journal.

[45]  D. Babcock,et al.  Sonographic measurements and appearance of normal kidneys in children. , 1985, AJR. American journal of roentgenology.

[46]  S. Massry,et al.  The physicochemical state and renal handling of divalent ions in chronic renal failure. , 1969, Archives of internal medicine.

[47]  P. Igarashi,et al.  HNF-1beta regulates transcription of the PKD modifier gene Kif12. , 2009, Journal of the American Society of Nephrology : JASN.

[48]  R. F. Luco,et al.  Distinct roles of HNF1beta, HNF1alpha, and HNF4alpha in regulating pancreas development, beta-cell function and growth. , 2007, Endocrine development.

[49]  S. V. D. van de Graaf,et al.  Physiology of epithelial Ca2+ and Mg2+ transport. , 2007, Reviews of physiology, biochemistry and pharmacology.

[50]  Jean-François Nicolas,et al.  Defective planar cell polarity in polycystic kidney disease , 2006, Nature Genetics.

[51]  H. Kusuhara,et al.  Regulation of the expression of human organic anion transporter 3 by hepatocyte nuclear factor 1alpha/beta and DNA methylation. , 2006, Molecular pharmacology.

[52]  C. Bellanné-Chantelot,et al.  Renal phenotypes related to hepatocyte nuclear factor-1beta (TCF2) mutations in a pediatric cohort. , 2006, Journal of the American Society of Nephrology : JASN.

[53]  G. Ryffel,et al.  Identification of target genes of the transcription factor HNF1beta and HNF1alpha in a human embryonic kidney cell line. , 2005, Biochimica et biophysica acta.

[54]  Cristel G. Thomas,et al.  Germline hepatocyte nuclear factor 1alpha and 1beta mutations in renal cell carcinomas. , 2005, Human molecular genetics.

[55]  G. Ryffel,et al.  Pattern of genes influenced by conditional expression of the transcription factors HNF6, HNF4alpha and HNF1beta in a pancreatic beta-cell line. , 2004, Nucleic acids research.

[56]  G. Ryffel,et al.  Pattern of genes influenced by conditional expression of the transcription factors HNF6, HNF4α and HNF1β in a pancreatic β-cell line , 2004 .

[57]  A. Hattersley,et al.  Mutations in the hepatocyte nuclear factor-1beta gene are associated with familial hypoplastic glomerulocystic kidney disease. , 2001, American journal of human genetics.

[58]  D. Cole,et al.  Magnesium transport in the renal distal convoluted tubule. , 2001, Physiological reviews.

[59]  T. Frayling,et al.  Abnormal nephron development associated with a frameshift mutation in the transcription factor hepatocyte nuclear factor-1 beta. , 2000, Kidney international.

[60]  K. Sweadner,et al.  Genomic organization of the human FXYD2 gene encoding the gamma subunit of the Na,K-ATPase. , 2000, Biochemical and biophysical research communications.

[61]  H. van Bokhoven,et al.  Dominant isolated renal magnesium loss is caused by misrouting of the Na(+),K(+)-ATPase gamma-subunit. , 2000, Nature genetics.

[62]  G. Bell,et al.  Mutation in hepatocyte nuclear factor-1 beta gene (TCF2) associated with MODY. , 1997, Nature genetics.