Distinct Functional Requirements for Podocalyxin in Immature and Mature Podocytes Reveal Mechanisms of Human Kidney Disease.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
10 06 2020
Historique:
received: 01 01 2020
accepted: 21 04 2020
entrez: 12 6 2020
pubmed: 12 6 2020
medline: 24 11 2020
Statut: epublish

Résumé

Dominant and recessive mutations in podocalyxin (PODXL) are associated with human kidney disease. Interestingly, some PODXL mutations manifest as anuria while others are associated with proteinuric kidney disease. PODXL heterozygosity is associated with adult-onset kidney disease and podocalyxin shedding into the urine is a common biomarker of a variety nephrotic syndromes. It is unknown, however, how various lesions in PODXL contribute to these disparate disease pathologies. Here we generated two mouse stains: one that deletes Podxl in developmentally mature podocytes (Podxl

Identifiants

pubmed: 32523052
doi: 10.1038/s41598-020-64907-3
pii: 10.1038/s41598-020-64907-3
pmc: PMC7286918
doi:

Substances chimiques

Sialoglycoproteins 0
podocalyxin 0
Puromycin Aminonucleoside 58-60-6

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

9419

Subventions

Organisme : CIHR
ID : MOP125992
Pays : Canada

Références

Debruin, E. J. et al. Podocalyxin regulates murine lung vascular permeability by altering endothelial cell adhesion. PloS one. 9(10), e108881 (2014).
doi: 10.1371/journal.pone.0108881
Nielsen, J. S. & McNagny, K. M. Novel functions of the CD34 family. J Cell Sci. 121(Pt 22), 3683–92 (2008).
doi: 10.1242/jcs.037507
Nielsen, J. S. & McNagny, K. M. The role of podocalyxin in health and disease. J Am Soc Nephrol. 20(8), 1669–76 (2009).
doi: 10.1681/ASN.2008070782
Dekan, G., Gabel, C. & Farquhar, M. G. Sulfate contributes to the negative charge of podocalyxin, the major sialoglycoprotein of the glomerular filtration slits. Proc Natl Acad Sci USA 88(12), 5398–402 (1991).
doi: 10.1073/pnas.88.12.5398
Kerjaschki, D., Sharkey, D. J. & Farquhar, M. G. Identification and characterization of podocalyxin–the major sialoprotein of the renal glomerular epithelial cell. J Cell Biol. 98(4), 1591–6 (1984).
doi: 10.1083/jcb.98.4.1591
Kerjaschki, D., Vernillo, A. T. & Farquhar, M. G. Reduced sialylation of podocalyxin–the major sialoprotein of the rat kidney glomerulus–in aminonucleoside nephrosis. Am J Pathol. 118(3), 343–9 (1985).
pubmed: 3976840 pmcid: 1887944
Kershaw, D. B. et al. Molecular cloning and characterization of human podocalyxin-like protein. Orthologous relationship to rabbit PCLP1 and rat podocalyxin. J Biol Chem. 272(25), 15708–14 (1997).
doi: 10.1074/jbc.272.25.15708
Kershaw, D. B. et al. Molecular cloning, expression, and characterization of podocalyxin-like protein 1 from rabbit as a transmembrane protein of glomerular podocytes and vascular endothelium. J Biol Chem. 270(49), 29439–46 (1995).
doi: 10.1074/jbc.270.49.29439
Doyonnas, R. et al. Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J Exp Med. 194(1), 13–27 (2001).
doi: 10.1084/jem.194.1.13
Freedman, B. S. & Steinman, T. I. iPS cell technology: Future impact on renal care. Nephrol News Issues. 29(9):18, 20-1, (2015).
Kim, Y. K. et al. Gene-edited Human Kidney Organoids Reveal Mechanisms of Disease in Podocyte Development. Stem Cells. 2017.
Freedman, B. S. et al. Modelling kidney disease with CRISPR-mutant kidney organoids derived from human pluripotent epiblast spheroids. Nat Commun. 6, 8715 (2015).
doi: 10.1038/ncomms9715
Kang, H. G. et al. Loss of podocalyxin causes a novel syndromic type of congenital nephrotic syndrome. Exp Mol Med. 49(12), e414 (2017).
doi: 10.1038/emm.2017.227
Barisoni, L., Schnaper, H. W. & Kopp, J. B. A proposed taxonomy for the podocytopathies: a reassessment of the primary nephrotic diseases. Clin J Am Soc Nephrol. 2(3), 529–42 (2007).
doi: 10.2215/CJN.04121206
Rosenberg, A. Z. & Kopp, J. B. Focal Segmental Glomerulosclerosis. Clin J Am Soc Nephrol. 12(3), 502–17. (2017).
doi: 10.2215/CJN.05960616
Pollak, M. R. Inherited podocytopathies: FSGS and nephrotic syndrome from a genetic viewpoint. J Am Soc Nephrol. 13(12), 3016–23 (2002).
doi: 10.1097/01.ASN.0000039569.34360.5E
Pollak, M. R. Familial FSGS. Adv Chronic Kidney Dis. 21(5), 422–5 (2014).
doi: 10.1053/j.ackd.2014.06.001
Barua, M. et al. Exome sequencing and in vitro studies identified podocalyxin as a candidate gene for focal and segmental glomerulosclerosis. Kidney Int. 85(1), 124–33 (2014).
doi: 10.1038/ki.2013.354
Lin, F. J. et al. First identification of PODXL nonsense mutations in autosomal dominant focal segmental glomerulosclerosis. Clin Sci (Lond). 2018.
Refaeli, I., Hughes, M. R. & McNagny, K. M. The first identified heterozygous nonsense mutations in podocalyxin offer new perspectives on the biology of podocytopathies. Clin Sci (Lond). 133(3), 443–7 (2019).
doi: 10.1042/CS20181067
Moeller, M. J., Sanden, S. K., Soofi, A., Wiggins, R. C. & Holzman, L. B. Podocyte-specific expression of cre recombinase in transgenic mice. Genesis. 35(1), 39–42 (2003).
doi: 10.1002/gene.10164
Bonventre JV. Kidney injury molecule-1: a translational journey. Trans Am Clin Climatol Assoc;125(293-9; discussion 9. 2014.
Hiromura, K. et al. Podocyte expression of the CDK-inhibitor p57 during development and disease. Kidney Int. 60(6), 2235–46 (2001).
doi: 10.1046/j.1523-1755.2001.00057.x
D’Agati, V. D., Fogo, A. B., Bruijn, J. A. & Jennette, J. C. Pathologic classification of focal segmental glomerulosclerosis: a working proposal. Am J Kidney Dis. 43(2), 368–82 (2004).
doi: 10.1053/j.ajkd.2003.10.024
Nielsen, J. S. et al. The CD34-related molecule podocalyxin is a potent inducer of microvillus formation. PLoS One. 2(2), e237 (2007).
doi: 10.1371/journal.pone.0000237
Bryant, D. M. et al. A molecular switch for the orientation of epithelial cell polarization. Dev Cell. 31(2), 171–87 (2014).
doi: 10.1016/j.devcel.2014.08.027
Little, M. H. Amsterdam; Boston: Academic Press; 2015:1 online resource (xvii, 595 p.).
Rumballe, B. A. et al. Nephron formation adopts a novel spatial topology at cessation of nephrogenesis. Dev Biol. 360(1), 110–22 (2011).
doi: 10.1016/j.ydbio.2011.09.011
Pippin, J. W. et al. Inducible rodent models of acquired podocyte diseases. Am J Physiol Renal Physiol. 296(2), F213–29 (2009).
doi: 10.1152/ajprenal.90421.2008
Kasembeli, A. N. et al. APOL1 Risk Variants Are Strongly Associated with HIV-Associated Nephropathy in Black South Africans. J Am Soc Nephrol. 26(11), 2882–90 (2015).
doi: 10.1681/ASN.2014050469
Ikuma, D. et al. The correlation of urinary podocytes and podocalyxin with histological features of lupus nephritis. Lupus. 27(3), 484–93. (2018).
doi: 10.1177/0961203317734918
Ye, H. et al. Urinary podocalyxin positive-element occurs in the early stage of diabetic nephropathy and is correlated with a clinical diagnosis of diabetic nephropathy. J Diabetes Complications. 28(1), 96–100 (2014).
doi: 10.1016/j.jdiacomp.2013.08.006
Shoji, M., Kobayashi, K., Takemoto, M., Sato, Y. & Yokote, K. Urinary podocalyxin levels were associated with urinary albumin levels among patients with diabetes. Biomarkers. 21(2), 164–7 (2016).
doi: 10.3109/1354750X.2015.1118551
Suwanpen, C. et al. Urinary podocalyxin, the novel biomarker for detecting early renal change in obesity. J Nephrol. 29(1), 37–44 (2016).
doi: 10.1007/s40620-015-0199-8
Kwon, S. H. et al. Elevated urinary podocyte-derived extracellular microvesicles in renovascular hypertensive patients. Nephrol Dial Transplant. (2016).

Auteurs

Ido Refaeli (I)

The Biomedical Research Centre, University of British Columbia, Vancouver, BC, Canada.
Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada.

Michael R Hughes (MR)

The Biomedical Research Centre, University of British Columbia, Vancouver, BC, Canada. mhughes@brc.ubc.ca.
Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada. mhughes@brc.ubc.ca.

Alvin Ka-Wai Wong (AK)

The Biomedical Research Centre, University of British Columbia, Vancouver, BC, Canada.

Mei Lin Z Bissonnette (MLZ)

Department of Pathology and Laboratory Medicine, University of British Columbia, Vancouver, BC, Canada.

Calvin D Roskelley (CD)

Life Sciences Institute, Department of Cellular and Physiological Sciences, University of British Columbia, Vancouver, BC, Canada.

A Wayne Vogl (A)

Life Sciences Institute, Department of Cellular and Physiological Sciences, University of British Columbia, Vancouver, BC, Canada.

Sean J Barbour (SJ)

Division of Nephrology, Department of Medicine, University of British Columbia, Vancouver, BC, Canada.

Benjamin S Freedman (BS)

Division of Nephrology, Department of Medicine, University of Washington School of Medicine, Seattle, WA, USA.
Kidney Research Institute, University of Washington School of Medicine, Seattle, WA, USA.
Institute for Stem Cell and Regenerative Medicine, University of Washington School of Medicine, Seattle, WA, USA.

Kelly M McNagny (KM)

The Biomedical Research Centre, University of British Columbia, Vancouver, BC, Canada. kelly@brc.ubc.ca.
Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada. kelly@brc.ubc.ca.
School of Biomedical Engineering, University of British Columbia, Vancouver, BC, Canada. kelly@brc.ubc.ca.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH