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Article ; Online: A roadmap for the genetic analysis of renal aging.

Noordmans, Gerda A / Hillebrands, Jan-Luuk / van Goor, Harry / Korstanje, Ron

2015 Volume 14, Issue 5, Page(s) 725–733

Abstract: Several studies show evidence for the genetic basis of renal disease, which renders some individuals more prone than others to accelerated renal aging. Studying the genetics of renal aging can help us to identify genes involved in this process and to ... ...

Abstract	Several studies show evidence for the genetic basis of renal disease, which renders some individuals more prone than others to accelerated renal aging. Studying the genetics of renal aging can help us to identify genes involved in this process and to unravel the underlying pathways. First, this opinion article will give an overview of the phenotypes that can be observed in age-related kidney disease. Accurate phenotyping is essential in performing genetic analysis. For kidney aging, this could include both functional and structural changes. Subsequently, this article reviews the studies that report on candidate genes associated with renal aging in humans and mice. Several loci or candidate genes have been found associated with kidney disease, but identification of the specific genetic variants involved has proven to be difficult. CUBN, UMOD, and SHROOM3 were identified by human GWAS as being associated with albuminuria, kidney function, and chronic kidney disease (CKD). These are promising examples of genes that could be involved in renal aging, and were further mechanistically evaluated in animal models. Eventually, we will provide approaches for performing genetic analysis. We should leverage the power of mouse models, as testing in humans is limited. Mouse and other animal models can be used to explain the underlying biological mechanisms of genes and loci identified by human GWAS. Furthermore, mouse models can be used to identify genetic variants associated with age-associated histological changes, of which Far2, Wisp2, and Esrrg are examples. A new outbred mouse population with high genetic diversity will facilitate the identification of genes associated with renal aging by enabling high-resolution genetic mapping while also allowing the control of environmental factors, and by enabling access to renal tissues at specific time points for histology, proteomics, and gene expression.
MeSH term(s)	Aging/genetics ; Animals ; Gene Expression ; Humans ; Kidney/metabolism ; Phenotype
Language	English
Publishing date	2015-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2113083-8
ISSN	1474-9726 ; 1474-9718
ISSN (online)	1474-9726
ISSN	1474-9718
DOI	10.1111/acel.12378
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Article ; Online: Genetic analysis of intracapillary glomerular lipoprotein deposits in aging mice.

Noordmans, Gerda A / Huang, Yuan / Savage, Holly / van Dijk, Marcory C R F / Schaart, Gert / van den Bergh Weerman, Marius A / Heeringa, Peter / Hillebrands, Jan-Luuk / Korstanje, Ron / van Goor, Harry

PloS one

2014 Volume 9, Issue 10, Page(s) e111308

Abstract: Background: Renal aging is characterized by functional and structural changes like decreased glomerular filtration rate, and glomerular, tubular and interstitial damage. To gain insight in pathways involved in renal aging, we studied aged mouse strains ... ...

Abstract	Background: Renal aging is characterized by functional and structural changes like decreased glomerular filtration rate, and glomerular, tubular and interstitial damage. To gain insight in pathways involved in renal aging, we studied aged mouse strains and used genetic analysis to identify genes associated with aging phenotypes. Methods: Upon morphological screening in kidneys from 20-month-old mice from 26 inbred strains we noted intracapillary PAS-positive deposits. The severity of these deposits was quantified by scoring of a total of 50 glomeruli per section (grade 0-4). Electron microscopy and immunohistochemical staining for apoE, apoB, apoA-IV and perilipin-2 was performed to further characterize the lesions. To identify loci associated with these PAS-positive intracapillary glomerular deposits, we performed haplotype association mapping. Results: Six out of 26 mouse strains showed glomerular PAS-positive deposits. The severity of these deposits varied: NOD(0.97), NZW(0.41), NON(0.30), B10(0.21), C3 H(0.9) and C57BR(0.7). The intracapillary deposits were strongly positive for apoE and weakly positive for apoB and apoA-IV. Haplotype association mapping showed a strong association with a 30-Kb haplotype block on Chr 1 within the Esrrg gene. We investigated 1 Mb on each site of this region, which includes the genes Spata17, Gpatch2, Esrrg, Ush2a and Kctd3. Conclusions: By analyzing 26 aged mouse strains we found that some strains developed an intracapillary PAS and apoE-positive lesion and identified a small haplotype block on Chr 1 within the Esrrg gene to be associated with these lipoprotein deposits. The region spanning this haplotype block contains the genes Spata17, Gpatch2, Esrrg, Ush2a and Kctd3, which are all highly expressed in the kidney. Esrrg might be involved in the evolvement of these glomerular deposits by influencing lipid metabolism and possibly immune reponses.
MeSH term(s)	Aging/genetics ; Aging/metabolism ; Animals ; Apolipoproteins/genetics ; Apolipoproteins/metabolism ; Carrier Proteins/genetics ; Carrier Proteins/metabolism ; Genetic Linkage ; Genetic Loci ; Haplotypes ; Kidney Glomerulus/growth & development ; Kidney Glomerulus/metabolism ; Kidney Glomerulus/ultrastructure ; Male ; Mice ; Mice, Inbred Strains ; Perilipin-1 ; Phosphoproteins/genetics ; Phosphoproteins/metabolism
Chemical Substances	Apolipoproteins ; Carrier Proteins ; Perilipin-1 ; Phosphoproteins
Language	English
Publishing date	2014-10-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0111308
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Article ; Online: Identification of novel genes associated with renal tertiary lymphoid organ formation in aging mice.

Huang, Yuan / Caputo, Christina R / Noordmans, Gerda A / Yazdani, Saleh / Monteiro, Luiz Henrique / van den Born, Jaap / van Goor, Harry / Heeringa, Peter / Korstanje, Ron / Hillebrands, Jan-Luuk

PloS one

2014 Volume 9, Issue 3, Page(s) e91850

Abstract: A hallmark of aging-related organ deterioration is a dysregulated immune response characterized by pathologic leukocyte infiltration of affected tissues. Mechanisms and genes involved are as yet unknown. To identify genes associated with aging-related ... ...

Abstract	A hallmark of aging-related organ deterioration is a dysregulated immune response characterized by pathologic leukocyte infiltration of affected tissues. Mechanisms and genes involved are as yet unknown. To identify genes associated with aging-related renal infiltration, we analyzed kidneys from aged mice (≥20 strains) for infiltrating leukocytes followed by Haplotype Association Mapping (HAM) analysis. Immunohistochemistry revealed CD45+ cell clusters (predominantly T and B cells) in perivascular areas coinciding with PNAd+ high endothelial venules and podoplanin+ lymph vessels indicative of tertiary lymphoid organs. Cumulative cluster size increased with age (analyzed at 6, 12 and 20 months). Based on the presence or absence of clusters in male and female mice at 20 months, HAM analysis revealed significant associations with loci on Chr1, Chr2, Chr8 and Chr14 in male mice, and with loci on Chr4, Chr7, Chr13 and Chr14 in female mice. Wisp2 (Chr2) showed the strongest association (P = 5.00×10(-137)) in male mice; Ctnnbip1 (P = 6.42×10(-267)) and Tnfrsf8 (P = 5.42×10(-245)) (both on Chr4) showed the strongest association in female mice. Both Wisp2 and Ctnnbip1 are part of the Wnt-signaling pathway and the encoded proteins were expressed within the tertiary lymphoid organs. In conclusion, this study revealed differential lymphocytic infiltration and tertiary lymphoid organ formation in aged mouse kidneys across different inbred mouse strains. HAM analysis identified candidate genes involved in the Wnt-signaling pathway that may be causally linked to tertiary lymphoid organ formation.
MeSH term(s)	Adaptor Proteins, Signal Transducing ; Aging/genetics ; Aging/immunology ; Aging/pathology ; Animals ; Female ; Genetic Association Studies ; Immunohistochemistry ; Intracellular Signaling Peptides and Proteins/genetics ; Intracellular Signaling Peptides and Proteins/metabolism ; Ki-1 Antigen/genetics ; Ki-1 Antigen/metabolism ; Kidney/immunology ; Kidney/metabolism ; Kidney/pathology ; Liver/immunology ; Liver/metabolism ; Liver/pathology ; Lymphatic Vessels/pathology ; Lymphoid Tissue/immunology ; Lymphoid Tissue/metabolism ; Lymphoid Tissue/pathology ; Male ; Mice ; Phenotype ; Polymorphism, Single Nucleotide ; Sex Factors
Chemical Substances	Adaptor Proteins, Signal Transducing ; CTNNBIP1 protein, human ; Intracellular Signaling Peptides and Proteins ; Ki-1 Antigen ; WISP-2 protein, mouse
Language	English
Publishing date	2014-03-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0091850
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Genetic analysis of mesangial matrix expansion in aging mice and identification of Far2 as a candidate gene.

Noordmans, Gerda A / Caputo, Christina R / Huang, Yuan / Sheehan, Susan M / Bulthuis, Marian / Heeringa, Peter / Hillebrands, Jan-Luuk / van Goor, Harry / Korstanje, Ron

Journal of the American Society of Nephrology : JASN

2013 Volume 24, Issue 12, Page(s) 1995–2001

Abstract: Aging of the kidney is associated with renal damage, in particular mesangial matrix expansion (MME). Identifying the genes involved in this process will help to unravel the mechanisms of aging and aid in the design of novel therapeutic modalities aimed ... ...

Abstract	Aging of the kidney is associated with renal damage, in particular mesangial matrix expansion (MME). Identifying the genes involved in this process will help to unravel the mechanisms of aging and aid in the design of novel therapeutic modalities aimed at prevention and regression. In this study, structural changes in glomeruli of 24 inbred mouse strains were characterized in male mice at 6, 12, and 20 months of age. Haplotype association mapping was used to determine genetic loci associated with the presence of MME at 20 months. This analysis identified a significant association with a 200-kb haplotype block on chromosome 6 containing Far2. Sequencing revealed that mouse strains with MME contain a 9-bp sequence in the 5' untranslated region of Far2 that is absent in most of the strains without MME. Real-time PCR showed a two-fold increase in the expression of Far2 in the kidneys of strains with the insert, and subsequent experiments performed in vitro with luciferase reporter vectors showed that this sequence difference causes differential expression of Far2. Overexpression of Far2 in a mouse mesangial cell line induced upregulation of platelet activating factor and the fibrotic marker TGF-β. This upregulation of MME-promoting factors may result, in part, from the FAR2-catalyzed reduction of fatty acyl-coenzyme A to fatty alcohols, which are possible precursors of platelet activating factor. Overall, these data suggest the identification of a novel pathway involved in renal aging that may yield therapeutic targets for reducing MME.
MeSH term(s)	Aging/pathology ; Aging/physiology ; Aldehyde Oxidoreductases/genetics ; Animals ; Chromosome Mapping ; Haplotypes ; Kidney Glomerulus/pathology ; Kidney Glomerulus/physiology ; Male ; Mesangial Cells/pathology ; Mesangial Cells/physiology ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Inbred DBA ; Mice, Inbred MRL lpr ; Mice, Inbred NOD ; Species Specificity
Chemical Substances	Aldehyde Oxidoreductases (EC 1.2.-) ; FAR2 protein, mouse (EC 1.2.1.84)
Language	English
Publishing date	2013-09-05
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1085942-1
ISSN	1533-3450 ; 1046-6673
ISSN (online)	1533-3450
ISSN	1046-6673
DOI	10.1681/ASN.2012080838
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Identification of novel genes associated with renal tertiary lymphoid organ formation in aging mice.

Yuan Huang / Christina R Caputo / Gerda A Noordmans / Saleh Yazdani / Luiz Henrique Monteiro / Jaap van den Born / Harry van Goor / Peter Heeringa / Ron Korstanje / Jan-Luuk Hillebrands

PLoS ONE, Vol 9, Iss 3, p e

2014 Volume 91850

Abstract	A hallmark of aging-related organ deterioration is a dysregulated immune response characterized by pathologic leukocyte infiltration of affected tissues. Mechanisms and genes involved are as yet unknown. To identify genes associated with aging-related renal infiltration, we analyzed kidneys from aged mice (≥20 strains) for infiltrating leukocytes followed by Haplotype Association Mapping (HAM) analysis. Immunohistochemistry revealed CD45+ cell clusters (predominantly T and B cells) in perivascular areas coinciding with PNAd+ high endothelial venules and podoplanin+ lymph vessels indicative of tertiary lymphoid organs. Cumulative cluster size increased with age (analyzed at 6, 12 and 20 months). Based on the presence or absence of clusters in male and female mice at 20 months, HAM analysis revealed significant associations with loci on Chr1, Chr2, Chr8 and Chr14 in male mice, and with loci on Chr4, Chr7, Chr13 and Chr14 in female mice. Wisp2 (Chr2) showed the strongest association (P = 5.00×10(-137)) in male mice; Ctnnbip1 (P = 6.42×10(-267)) and Tnfrsf8 (P = 5.42×10(-245)) (both on Chr4) showed the strongest association in female mice. Both Wisp2 and Ctnnbip1 are part of the Wnt-signaling pathway and the encoded proteins were expressed within the tertiary lymphoid organs. In conclusion, this study revealed differential lymphocytic infiltration and tertiary lymphoid organ formation in aged mouse kidneys across different inbred mouse strains. HAM analysis identified candidate genes involved in the Wnt-signaling pathway that may be causally linked to tertiary lymphoid organ formation.
Keywords	Medicine ; R ; Science ; Q
Subject code	570
Language	English
Publishing date	2014-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Genetic analysis of intracapillary glomerular lipoprotein deposits in aging mice.

Gerda A Noordmans / Yuan Huang / Holly Savage / Marcory C R F van Dijk / Gert Schaart / Marius A van den Bergh Weerman / Peter Heeringa / Jan-Luuk Hillebrands / Ron Korstanje / Harry van Goor

PLoS ONE, Vol 9, Iss 10, p e

2014 Volume 111308

Abstract: Renal aging is characterized by functional and structural changes like decreased glomerular filtration rate, and glomerular, tubular and interstitial damage. To gain insight in pathways involved in renal aging, we studied aged mouse strains and used ... ...

Abstract	Renal aging is characterized by functional and structural changes like decreased glomerular filtration rate, and glomerular, tubular and interstitial damage. To gain insight in pathways involved in renal aging, we studied aged mouse strains and used genetic analysis to identify genes associated with aging phenotypes.Upon morphological screening in kidneys from 20-month-old mice from 26 inbred strains we noted intracapillary PAS-positive deposits. The severity of these deposits was quantified by scoring of a total of 50 glomeruli per section (grade 0-4). Electron microscopy and immunohistochemical staining for apoE, apoB, apoA-IV and perilipin-2 was performed to further characterize the lesions. To identify loci associated with these PAS-positive intracapillary glomerular deposits, we performed haplotype association mapping.Six out of 26 mouse strains showed glomerular PAS-positive deposits. The severity of these deposits varied: NOD(0.97), NZW(0.41), NON(0.30), B10(0.21), C3 H(0.9) and C57BR(0.7). The intracapillary deposits were strongly positive for apoE and weakly positive for apoB and apoA-IV. Haplotype association mapping showed a strong association with a 30-Kb haplotype block on Chr 1 within the Esrrg gene. We investigated 1 Mb on each site of this region, which includes the genes Spata17, Gpatch2, Esrrg, Ush2a and Kctd3.By analyzing 26 aged mouse strains we found that some strains developed an intracapillary PAS and apoE-positive lesion and identified a small haplotype block on Chr 1 within the Esrrg gene to be associated with these lipoprotein deposits. The region spanning this haplotype block contains the genes Spata17, Gpatch2, Esrrg, Ush2a and Kctd3, which are all highly expressed in the kidney. Esrrg might be involved in the evolvement of these glomerular deposits by influencing lipid metabolism and possibly immune reponses.
Keywords	Medicine ; R ; Science ; Q
Subject code	616
Language	English
Publishing date	2014-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Absence of MyD88 signaling induces donor-specific kidney allograft tolerance.

Wu, Huiling / Noordmans, Gerda A / O'Brien, Maya R / Ma, Jin / Zhao, Cathy Y / Zhang, Geoff Y / Kwan, Tony K T / Alexander, Stephen I / Chadban, Steven J

Journal of the American Society of Nephrology : JASN

2012 Volume 23, Issue 10, Page(s) 1701–1716

Abstract: Toll-like receptors (TLRs) play a fundamental role in innate immunity and provide a link between innate and adaptive responses to an allograft; however, whether the development of acute and chronic allograft rejection requires TLR signaling is unknown. ... ...

Abstract	Toll-like receptors (TLRs) play a fundamental role in innate immunity and provide a link between innate and adaptive responses to an allograft; however, whether the development of acute and chronic allograft rejection requires TLR signaling is unknown. Here, we studied TLR signaling in a fully MHC-mismatched, life-sustaining murine model of kidney allograft rejection. Mice deficient in the TLR adaptor protein MyD88 developed donor antigen-specific tolerance, which protected them from both acute and chronic allograft rejection and increased their survival after transplantation compared with wild-type controls. Administration of an anti-CD25 antibody to MyD88-deficient recipients depleted CD4(+)CD25(+)FoxP3(+) cells and broke tolerance. In addition, defective development of Th17 immune responses to alloantigen both in vitro and in vivo occurred, resulting in an increased ratio of Tregs to Th17 effectors. Thus, MyD88 deficiency was associated with an altered balance of Tregs over Th17 cells, promoting tolerance instead of rejection. This study provides evidence that targeting innate immunity may be a clinically relevant strategy to facilitate transplantation tolerance.
MeSH term(s)	Animals ; Cytokines/genetics ; Cytokines/metabolism ; Graft Rejection/immunology ; Graft Rejection/prevention & control ; Graft Survival/immunology ; Humans ; Immune Tolerance ; Immunity, Innate ; Interleukin-2 Receptor alpha Subunit/antagonists & inhibitors ; Isoantigens ; Kidney Transplantation/immunology ; Lymphocyte Culture Test, Mixed ; Lymphocyte Depletion ; Male ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Mice, Knockout ; Myeloid Differentiation Factor 88/deficiency ; Myeloid Differentiation Factor 88/genetics ; Myeloid Differentiation Factor 88/immunology ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Signal Transduction/immunology ; T-Lymphocytes, Regulatory/immunology ; Th17 Cells/immunology ; Tissue Donors ; Transplantation, Homologous
Chemical Substances	Cytokines ; Interleukin-2 Receptor alpha Subunit ; Isoantigens ; Myd88 protein, mouse ; Myeloid Differentiation Factor 88 ; RNA, Messenger
Language	English
Publishing date	2012-08-09
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1085942-1
ISSN	1533-3450 ; 1046-6673
ISSN (online)	1533-3450
ISSN	1046-6673
DOI	10.1681/ASN.2012010052
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Identification of novel genes associated with renal tertiary lymphoid organ formation in aging mice

Huang, Yuan / Caputo, Christina R. / Noordmans, Gerda A. / Yazdani, Saleh / Monteiro, Luiz Henrique / van den Born, Jaap / van Goor, Harry / Heeringa, Peter / Korstanje, Ron / Hillebrands, Jan-Luuk

Huang , Y , Caputo , C R , Noordmans , G A , Yazdani , S , Monteiro , L H , van den Born , J , van Goor , H , Heeringa , P , Korstanje , R & Hillebrands , J-L 2014 , ' Identification of novel genes associated with renal tertiary lymphoid organ formation in aging mice ' , PLoS ONE , vol. 9 , no. 3 , e91850 . https://doi.org/10.1371/journal.pone.0091850 ; ISSN:1932-6203

2014

Abstract	A hallmark of aging-related organ deterioration is a dysregulated immune response characterized by pathologic leukocyte infiltration of affected tissues. Mechanisms and genes involved are as yet unknown. To identify genes associated with aging-related renal infiltration, we analyzed kidneys from aged mice (≥20 strains) for infiltrating leukocytes followed by Haplotype Association Mapping (HAM) analysis. Immunohistochemistry revealed CD45+ cell clusters (predominantly T and B cells) in perivascular areas coinciding with PNAd+ high endothelial venules and podoplanin+ lymph vessels indicative of tertiary lymphoid organs. Cumulative cluster size increased with age (analyzed at 6, 12 and 20 months). Based on the presence or absence of clusters in male and female mice at 20 months, HAM analysis revealed significant associations with loci on Chr1, Chr2, Chr8 and Chr14 in male mice, and with loci on Chr4, Chr7, Chr13 and Chr14 in female mice. Wisp2 (Chr2) showed the strongest association (P = 5.00×10(-137)) in male mice; Ctnnbip1 (P = 6.42×10(-267)) and Tnfrsf8 (P = 5.42×10(-245)) (both on Chr4) showed the strongest association in female mice. Both Wisp2 and Ctnnbip1 are part of the Wnt-signaling pathway and the encoded proteins were expressed within the tertiary lymphoid organs. In conclusion, this study revealed differential lymphocytic infiltration and tertiary lymphoid organ formation in aged mouse kidneys across different inbred mouse strains. HAM analysis identified candidate genes involved in the Wnt-signaling pathway that may be causally linked to tertiary lymphoid organ formation.
Keywords	ENDOTHELIAL-CELLS ; CHRONIC REJECTION ; IMMUNE-RESPONSE ; HUMAN KIDNEY ; NEOGENESIS ; DISEASE ; EXPRESSION ; CD30 ; FAMILY ; TISSUE
Subject code	570
Language	English
Publishing date	2014-03-17
Publishing country	nl
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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