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Clinical and genetic heterogeneity in familial steroid-sensitive nephrotic syndrome

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Abstract

Background

Familial steroid-sensitive nephrotic syndrome (SSNS) is a rare condition. The disease pathophysiology remains elusive. However, bi-allelic mutations in the EMP2 gene were identified, and specific variations in HLA-DQA1 were linked to a high risk of developing the disease.

Methods

Clinical data were analyzed in 59 SSNS families. EMP2 gene was sequenced in families with a potential autosomal recessive (AR) inheritance. Exome sequencing was performed in a subset of 13 families with potential AR inheritance. Two variations in HLA-DQA1 were genotyped in the whole cohort.

Results

Transmission was compatible with an AR (n = 33) or autosomal dominant (AD, n = 26) inheritance, assuming that familial SSNS is a monogenic trait. Clinical features did not differ between AR and AD groups. All patients, including primary (n = 7) and secondary steroid resistant nephrotic syndrone (SRNS), (n = 13) were sensitive to additional immunosuppressive therapy. Both HLA-DQA1 variations were found to be highly linked to the disease (OR = 4.34 and OR = 4.89; p < 0.001). Exome sequencing did not reveal any pathogenic mutation, neither did EMP2 sequencing.

Conclusions

Taken together, these results highlight the clinical and genetic heterogeneity in familial SSNS. Clinical findings sustain an immune origin in all patients, whatever the initial steroid-sensitivity. The absence of a variant shared by two families and the HLA-DQA1 variation enrichments suggest a complex mode of inheritance.

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Abbreviations

AR:

Autosomal recessive

AD:

Autosomal dominant

EMP2:

Epithelial member protein 2

FR:

Frequent relapsers

FSGS:

Focal and segmental glomerulosclerosis

OR:

Odds ratio

SRNS:

Steroid-resistant nephrotic syndrome

SSNS:

Steroid-sensitive nephrotic syndrome

WES:

Whole exome sequencing

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Acknowledgements

We thank all patients with familial SSNS and their families for their participation in this study. We thank Dr Kalmàn Tory for helpful discussions.

Web resources

The URLs for data presented herein are as follows:

dBSNP: https://www.ncbi.nlm.nih.gov/SNP/

1000genomes project: http://www.internationalgenome.org

PolyPhen: http://genetics.bwh.harvard.edu

SIFT http://sift.jcvi.org

Mutation Taster http://www.mutationtaster.org

ExaC: http://exac.broadinstitute.org

ProteinAtlas: http://www.proteinatlas.org

GeneMatcher: https://genematcher.org

Funding

Financial support for this work was provided by grants from the European Union’s Seventh Framework Programme (FP7/2007–2013/n°305608-EURenOmics), the “Investments for the Future” program (ANR-10-IAHU-01), and the “Fondation-maladies rares” (FONDATION_HTS-RD – I201309001) to C. Antignac, and The «Fondation pour la Recherche Médicale» (FRM n° DEA20130727711) to G. Dorval.

Author information

Authors and Affiliations

  1. INSERM UMR1163, Laboratory of Hereditary Kidney Diseases, Imagine Institute, 24 Boulevard du Montparnasse, 75015, Paris, France

    Guillaume Dorval, Olivier Gribouval, Vanesa Martinez-Barquero, Eduardo Machuca, Marie-Josèphe Tête, Rémi Salomon, Corinne Antignac & Olivia Boyer

  2. Paris Descartes-Sorbonne Paris Cité University, Imagine Institute, Paris, France

    Guillaume Dorval, Olivier Gribouval, Vanesa Martinez-Barquero, Marie-Josèphe Tête, Rémi Salomon, Corinne Antignac & Olivia Boyer

  3. Department of Pediatric Nephrology, Assistance Publique-Hôpitaux de Paris, Robert Debré Hospital, Paris, France

    Véronique Baudouin & Georges Deschênes

  4. Department of Nephrology, University Hospital of Tours, Tours, France

    Stéphane Benoit, Sylvie Cloarec & Hubert Nivet

  5. Department of Pediatrics, Sfax University, Sfax, Tunisia

    Imen Chabchoub & Mongia Hachicha

  6. Department of Pediatrics, University Hospital of Angers, Angers, France

    Gérard Champion

  7. Department of Nephrology and Organ Transplantation, University Hospital Rangueil, Toulouse, France

    Dominique Chauveau, Dominique Durand, Nassim Kamar & David Ribes

  8. Department of Pediatrics, Division of Pediatric Nephrology, Lausanne University Hospital, Lausanne, Switzerland

    Hassib Chehade

  9. Department of Pediatrics, Monastir University, Monastir, Tunisia

    Chokri Chouchane

  10. Department of Pediatric Nephrology, Claude-Bernard Lyon 1 University, Bron, France

    Pierre Cochat

  11. Department of Human Genetics, Institute of Pathology and Genetics, Gosselies, Belgium

    Karin Dahan

  12. Nephrology and Immunology Department, University Hospital of Nantes, Nantes, France

    Jacques Dantal & Maryvonne Hourmant

  13. Department of Nephrology, University Hospital of Bordeaux, Bordeaux, France

    Yahsou Delmas

  14. Department of Pediatrics, Saint-Quentin Hospital, Saint-Quentin, France

    Phillippe Dolhem

  15. Kocaeli Academy for Solidarity, Kocaeli, Turkey

    Zelal Ekinci

  16. Department of Nephrology, Assistance Publique-Hôpitaux de Paris, Necker-Enfants Malades Hospital, Paris, France

    Khalil El Karoui, Jean-Pierre Grunfeld & Aurélie Hummel

  17. Nephrology Dialysis Transplantation Children’s Unit, University Hospital Hautepierre, Strasbourg, France

    Michel Fischbach

  18. Department of Pediatrics, University Hospital of Limoges, Limoges, France

    Vincent Guigonis

  19. Department of Pediatric Nephrology, Assistance Publique-Hôpitaux de Paris, Armand Trousseau Hospital, Paris, France

    Julien Hogan & Tim Ulinski

  20. Department of Nephrology, University Hospital Hautepierre, Strasbourg, France

    Thierry Krummel

  21. Department of Genetics, University Hospital of Bordeaux, Bordeaux, France

    Didier Lacombe

  22. Department of Pediatrics, University Hospital of Bordeaux, Bordeaux, France

    Brigitte Llanas

  23. Department of Nephrology and Dialysis, Assistance Publique-Hôpitaux de Paris, Tenon Hospital, Paris, France

    Laurent Mesnard, Pierre Ronco & Eric Rondeau

  24. Sorbonne University, UPMC University Paris 06, Paris, France

    Laurent Mesnard & Pierre Ronco

  25. INSERM, UMR_S 1155, 75020, Paris, France

    Laurent Mesnard & Pierre Ronco

  26. College of Medicine, Sultan Qaboos University, Muscat, Oman

    Nabil Mohsin

  27. Department of Pediatric Nephrology, Centre de référence du syndrome néphrotique idiopathique de l’enfant et l’adulte, Assistance Publique-Hôpitaux de Paris, Necker-Enfants Malades Hospital, Paris, France

    Patrick Niaudet, Rémi Salomon & Olivia Boyer

  28. Centre de Référence Syndrome Néphrotique Idiopathique de l’enfant et de l’adulte, Paris, France

    Patrick Niaudet, Rémi Salomon, Corinne Antignac & Olivia Boyer

  29. Department of Pediatrics, Division of Pediatric Nephrology, Geneva University Hospital, Geneva, Switzerland

    Paloma Parvex

  30. Departement of Pediatrics, Nephrology Unit, University Hospital of Reims, Reims, France

    Christine Pietrement

  31. Faculty of Medicine, Laboratory of Biochemistry and Molecular Biology, UMR, CNRS/URCA n°7369, University of Champagne-Ardenne, Reims, France

    Christine Pietrement

  32. Department of Pediatrics, Assistance Publique-Hôpitaux de Paris, Jean Verdier Hospital, Bondy, France

    Loic de Pontual

  33. Department of Nephrology and Transplantation, University Hospital of Lyon, Lyon, France

    Claire Pouteil Noble

  34. Department of Nephrology and Kidney Transplantation, The Conception Hospital, Marseille, France

    Marion Sallee

  35. Department of Multidisciplinary Pediatrics Timone, Assistance Publique Hôpitaux de Marseille, Aix-Marseille University, Marseille, France

    Michel Tsimaratos

  36. Department of Genetics, Assistance Publique-Hôpitaux de Paris, Necker-Enfants malades Hospital, Paris, France

    Corinne Antignac

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  1. Guillaume Dorval
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  2. Olivier Gribouval
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  4. Eduardo Machuca
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  5. Marie-Josèphe Tête
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  9. Gérard Champion
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  10. Dominique Chauveau
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  27. Julien Hogan
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  28. Maryvonne Hourmant
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  29. Aurélie Hummel
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  34. Laurent Mesnard
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  40. Loic de Pontual
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  48. Rémi Salomon
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Corresponding author

Correspondence to Guillaume Dorval.

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Written informed consent was obtained from participants or their parents, and the study was approved by the Comité de Protection des Personnes “Ile-De-France II.”

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The authors have no conflicts of interest relevant to this article to disclose.

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Dorval, G., Gribouval, O., Martinez-Barquero, V. et al. Clinical and genetic heterogeneity in familial steroid-sensitive nephrotic syndrome. Pediatr Nephrol 33, 473–483 (2018). https://doi.org/10.1007/s00467-017-3819-9

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  • DOI: https://doi.org/10.1007/s00467-017-3819-9

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