Common risk variants in NPHS1 and TNFSF15 are associated with childhood steroid-sensitive nephrotic syndrome

doi:10.1016/j.kint.2020.05.029

. 2020 Nov;98(5):1308-1322.

doi: 10.1016/j.kint.2020.05.029. Epub 2020 Jun 14.

Common risk variants in NPHS1 and TNFSF15 are associated with childhood steroid-sensitive nephrotic syndrome

Xiaoyuan Jia¹, Tomohiko Yamamura², Rasheed Gbadegesin³, Michelle T McNulty⁴, Kyuyong Song⁵, China Nagano², Yuki Hitomi¹, Dongwon Lee⁶, Yoshihiro Aiba⁷, Seik-Soon Khor¹, Kazuko Ueno¹, Yosuke Kawai¹, Masao Nagasaki⁸, Eisei Noiri⁹, Tomoko Horinouchi², Hiroshi Kaito¹⁰, Riku Hamada¹¹, Takayuki Okamoto¹², Koichi Kamei¹³, Yoshitsugu Kaku¹⁴, Rika Fujimaru¹⁵, Ryojiro Tanaka¹⁶, Yuko Shima¹⁷; Research Consortium on Genetics of Childhood Idiopathic Nephrotic Syndrome in Japan; Jiwon Baek⁵, Hee Gyung Kang¹⁸, Il-Soo Ha¹⁸, Kyoung Hee Han¹⁹, Eun Mi Yang²⁰; Korean Consortium of Hereditary Renal Diseases in Children; Asiri Abeyagunawardena³, Brandon Lane³, Megan Chryst-Stangl³, Christopher Esezobor²¹, Adaobi Solarin²²; Midwest Pediatric Nephrology Consortium (Genetics of Nephrotic Syndrome Study Group); Claire Dossier²³, Georges Deschênes²⁴; NEPHROVIR; Marina Vivarelli²⁵, Hanna Debiec²⁶, Kenji Ishikura¹³, Masafumi Matsuo²⁷, Kandai Nozu², Pierre Ronco²⁶, Hae Il Cheong¹⁸, Matthew G Sampson⁶, Katsushi Tokunaga²⁸, Kazumoto Iijima²⁹

Collaborators, Affiliations

Collaborators

Yoshinori Araki, Yoshinobu Nagaoka, Takayuki Okamoto, Yasuyuki Sato, Asako Hayashi, Toshiyuki Takahashi, Hayato Aoyagi, Michihiko Ueno, Masanori Nakanishi, Nariaki Toita, Kimiaki Uetake, Norio Kobayashi, Shoji Fujita, Kazushi Tsuruga, Naonori Kumagai, Hiroki Kudo, Eriko Tanaka, Tae Omori, Mari Okada, Yoshiho Hatai, Tomohiro Udagawa, Yaeko Motoyoshi, Kenji Ishikura, Koichi Kamei, Masao Ogura, Mai Sato, Yuji Kano, Motoshi Hattori, Kenichiro Miura, Yutaka Harita, Shoichiro Kanda, Emi Sawanobori, Anna Kobayashi, Manabu Kojika, Yoko Ohwada, Kunimasa Yan, Hiroshi Hataya, Riku Hamada, Chikako Terano, Ryoko Harada, Yuko Hamasaki, Junya Hashimoto, Shuichi Ito, Hiroyuki Machida, Aya Inaba, Takeshi Matsuyama, Miwa Goto, Masaki Shimizu, Kazuhide Ohta, Yohei Ikezumi, Takeshi Yamada, Toshiaki Suzuki, Soichi Tamamura, Yukiko Mori, Yoshihiko Hidaka, Daisuke Matsuoka, Tatsuya Kinoshita, Shunsuke Noda, Masashi Kitahara, Naoya Fujita, Satoshi Hibino, Kazumoto Iijima, Kandai Nozu, Hiroshi Kaito, Shogo Minamikawa, Tomohiko Yamamura, China Nagano, Tomoko Horinouchi, Keita Nakanishi, Junya Fujimura, Nana Sakakibara, Yuya Aoto, Shinya Ishiko, Ryojiro Tanaka, Kyoko Kanda, Yosuke Inaguma, Yuya Hashimura, Shingo Ishimori, Naohiro Kamiyoshi, Takayuki Shibano, Yasuhiro Takeshima, Rika Fujimaru, Hiroaki Ueda, Akira Ashida, Hideki Matsumura, Takuo Kubota, Taichi Kitaoka, Yusuke Okuda, Toshihiro Sawai, Tomoyuki Sakai, Yuko Shima, Taketsugu Hama, Mikiya Fujieda, Masayuki Ishihara, Shigeru Itoh, Takuma Iwaki, Maki Shimizu, Koji Nagatani, Shoji Kagami, Maki Urushihara, Yoshitsugu Kaku, Manao Nishimura, Miwa Yoshino, Ken Hatae, Maiko Hinokiyama, Rie Kuroki, Yasufumi Ohtsuka, Masafumi Oka, Shinji Nishimura, Tadashi Sato, Seiji Tanaka, Ayuko Zaitsu, Hitoshi Nakazato, Hiroshi Tamura, Koichi Nakanishi, Min Hyun Cho, Tae-Sun Ha, Hae Il Cheong, Hee Gyung Kang, Il-Soo Ha, Ji Hyun Kim, Peong Gang Park, Myung Hyun Cho, Kyoung Hee Han, Eun Mi Yang, Alejandro Quiroga, Asha Moudgil, Blanche Chavers, Charles Kwon, Corinna Bowers, Deb Gipson, Deepa Chand, Donald Jack Weaver, Elizabeth Abraham, Halima Janjua, Jen-Jar Lin, Larry Greenbaum, Mahmoud Kallash, Michelle Rheault, Nilka De Jeus Gonzalez, Patrick Brophy, Rasheed Gbadegesin, Shashi Nagaraj, Susan Massengill, Tarak Srivastava, Tray Hunley, Yi Cai, Abiodun Omoloja, Cynthia Silva, Adebowale Adeyemo, Shenal Thalgahagoda, Jameela A Kari, Sherif El Desoky, Mohammed Abdelhadi, Rachida Akil, Sonia Azib, Romain Basmaci, Gregoire Benoist, Philippe Bensaid, Philippe Blanc, Olivia Boyer, Julie Bucher, Anne Chace, Arnaud Chalvon, Marion Cheminee, Sandrine Chendjou, Patrick Daoud, Georges Deschênes, Claire Dossier, Ossam Elias, Chantal Gagliadone, Vincent Gajdos, Aurélien Galerne, Evelyne Jacqz Aigrain, Lydie Joly Sanchez, Mohamed Khaled, Fatima Khelfaoui, Yacine Laoudi, Anis Larakeb, Tarek Limani, Fouad Mahdi, Alexis Mandelcwaijg, Stephanie Muller, Kacem Nacer, Sylvie Nathanson, Béatrice Pellegrino, Isabelle Pharaon, Véronica Roudault, Sébastien Rouget, Marc Saf, Tabassom Simon, Cedric Tahiri, Tim Ulinski, Férielle Zenkhri

Affiliations

¹ Department of Human Genetics, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
² Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan.
³ Department of Pediatrics, Division of Nephrology, Duke University Medical Center, Durham, North Carolina, USA.
⁴ Department of Medicine-Nephrology, Boston Children's Hospital, Boston, Massachussetts, USA; Medical and Population Genetics, Broad Institute, Cambridge, Massachussetts, USA.
⁵ Department of Biochemistry and Molecular Biology, University of Ulsan College of Medicine, Seoul, Korea.
⁶ Department of Medicine-Nephrology, Boston Children's Hospital, Boston, Massachussetts, USA; Medical and Population Genetics, Broad Institute, Cambridge, Massachussetts, USA; Harvard Medical School, Boston, Massachussetts, USA.
⁷ Clinical Research Center, National Hospital Organization Nagasaki Medical Center, Omura, Japan.
⁸ Department of Integrative Genomics, Tohoku Medical Megabank Organization, Tohoku University, Sendai, Japan.
⁹ Department of Hemodialysis and Apheresis, The University of Tokyo Hospital, Tokyo, Japan.
¹⁰ Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan; Department of Nephrology, Hyogo Prefectural Kobe Children's Hospital, Kobe, Japan.
¹¹ Department of Nephrology, Tokyo Metropolitan Children's Medical Center, Tokyo, Japan.
¹² Department of Pediatrics, Hokkaido University Hospital, Sapporo, Japan.
¹³ Division of Nephrology and Rheumatology, National Center for Child Health and Development, Tokyo, Japan.
¹⁴ Department of Nephrology, Fukuoka Children's Hospital, Fukuoka, Japan.
¹⁵ Department of Pediatrics, Osaka City General Hospital, Osaka, Japan.
¹⁶ Department of Nephrology, Hyogo Prefectural Kobe Children's Hospital, Kobe, Japan.
¹⁷ Department of Pediatrics, Wakayama Medical University, Wakayama, Japan.
¹⁸ Department of Pediatrics, Seoul National University Children's Hospital, Seoul, Korea.
¹⁹ Department of Pediatrics, Jeju National University School of Medicine, Jeju, Korea.
²⁰ Department of Pediatrics, Chonnam National University Children's Hospital, Gwangju, Korea.
²¹ Department of Paediatrics, College of Medicine, University of Lagos, Lagos, Nigeria.
²² Department of Pediatrics, Lagos State University Teaching Hospital, Ikeja, Nigeria.
²³ Department of Paediatric Nephrology, Public Assistance Hospital of Paris, Robert-Debré Hospital, Paris, France.
²⁴ Center of Research on Inflammation, Institut National de la Santé et de la Recherche Médicale UMR 1149, University Sorbonne-Paris, Paris, France.
²⁵ Division of Nephrology and Dialysis, Bambino Gesù Children's Hospital and Research Institute, Rome, Italy.
²⁶ Sorbonne University, INSERM UMR_S1155, and Nephrology Day Hospital, Department of Nephrology, Hôpital Tenon, Paris France.
²⁷ Research Center for Locomotion Biology, Kobe Gakuin University, Kobe, Japan; KNC Department of Nucleic Acid Drug Discovery, Faculty of Rehabilitation, Kobe Gakuin University, Kobe, Japan.
²⁸ Department of Human Genetics, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan. Electronic address: katokunaga@ri.ncgm.go.jp.
²⁹ Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan. Electronic address: iijima@med.kobe-u.ac.jp.

PMID: 32554042
PMCID: PMC8101291
DOI: 10.1016/j.kint.2020.05.029

Common risk variants in NPHS1 and TNFSF15 are associated with childhood steroid-sensitive nephrotic syndrome

Xiaoyuan Jia et al. Kidney Int. 2020 Nov.

. 2020 Nov;98(5):1308-1322.

doi: 10.1016/j.kint.2020.05.029. Epub 2020 Jun 14.

Authors

Collaborators

Yoshinori Araki, Yoshinobu Nagaoka, Takayuki Okamoto, Yasuyuki Sato, Asako Hayashi, Toshiyuki Takahashi, Hayato Aoyagi, Michihiko Ueno, Masanori Nakanishi, Nariaki Toita, Kimiaki Uetake, Norio Kobayashi, Shoji Fujita, Kazushi Tsuruga, Naonori Kumagai, Hiroki Kudo, Eriko Tanaka, Tae Omori, Mari Okada, Yoshiho Hatai, Tomohiro Udagawa, Yaeko Motoyoshi, Kenji Ishikura, Koichi Kamei, Masao Ogura, Mai Sato, Yuji Kano, Motoshi Hattori, Kenichiro Miura, Yutaka Harita, Shoichiro Kanda, Emi Sawanobori, Anna Kobayashi, Manabu Kojika, Yoko Ohwada, Kunimasa Yan, Hiroshi Hataya, Riku Hamada, Chikako Terano, Ryoko Harada, Yuko Hamasaki, Junya Hashimoto, Shuichi Ito, Hiroyuki Machida, Aya Inaba, Takeshi Matsuyama, Miwa Goto, Masaki Shimizu, Kazuhide Ohta, Yohei Ikezumi, Takeshi Yamada, Toshiaki Suzuki, Soichi Tamamura, Yukiko Mori, Yoshihiko Hidaka, Daisuke Matsuoka, Tatsuya Kinoshita, Shunsuke Noda, Masashi Kitahara, Naoya Fujita, Satoshi Hibino, Kazumoto Iijima, Kandai Nozu, Hiroshi Kaito, Shogo Minamikawa, Tomohiko Yamamura, China Nagano, Tomoko Horinouchi, Keita Nakanishi, Junya Fujimura, Nana Sakakibara, Yuya Aoto, Shinya Ishiko, Ryojiro Tanaka, Kyoko Kanda, Yosuke Inaguma, Yuya Hashimura, Shingo Ishimori, Naohiro Kamiyoshi, Takayuki Shibano, Yasuhiro Takeshima, Rika Fujimaru, Hiroaki Ueda, Akira Ashida, Hideki Matsumura, Takuo Kubota, Taichi Kitaoka, Yusuke Okuda, Toshihiro Sawai, Tomoyuki Sakai, Yuko Shima, Taketsugu Hama, Mikiya Fujieda, Masayuki Ishihara, Shigeru Itoh, Takuma Iwaki, Maki Shimizu, Koji Nagatani, Shoji Kagami, Maki Urushihara, Yoshitsugu Kaku, Manao Nishimura, Miwa Yoshino, Ken Hatae, Maiko Hinokiyama, Rie Kuroki, Yasufumi Ohtsuka, Masafumi Oka, Shinji Nishimura, Tadashi Sato, Seiji Tanaka, Ayuko Zaitsu, Hitoshi Nakazato, Hiroshi Tamura, Koichi Nakanishi, Min Hyun Cho, Tae-Sun Ha, Hae Il Cheong, Hee Gyung Kang, Il-Soo Ha, Ji Hyun Kim, Peong Gang Park, Myung Hyun Cho, Kyoung Hee Han, Eun Mi Yang, Alejandro Quiroga, Asha Moudgil, Blanche Chavers, Charles Kwon, Corinna Bowers, Deb Gipson, Deepa Chand, Donald Jack Weaver, Elizabeth Abraham, Halima Janjua, Jen-Jar Lin, Larry Greenbaum, Mahmoud Kallash, Michelle Rheault, Nilka De Jeus Gonzalez, Patrick Brophy, Rasheed Gbadegesin, Shashi Nagaraj, Susan Massengill, Tarak Srivastava, Tray Hunley, Yi Cai, Abiodun Omoloja, Cynthia Silva, Adebowale Adeyemo, Shenal Thalgahagoda, Jameela A Kari, Sherif El Desoky, Mohammed Abdelhadi, Rachida Akil, Sonia Azib, Romain Basmaci, Gregoire Benoist, Philippe Bensaid, Philippe Blanc, Olivia Boyer, Julie Bucher, Anne Chace, Arnaud Chalvon, Marion Cheminee, Sandrine Chendjou, Patrick Daoud, Georges Deschênes, Claire Dossier, Ossam Elias, Chantal Gagliadone, Vincent Gajdos, Aurélien Galerne, Evelyne Jacqz Aigrain, Lydie Joly Sanchez, Mohamed Khaled, Fatima Khelfaoui, Yacine Laoudi, Anis Larakeb, Tarek Limani, Fouad Mahdi, Alexis Mandelcwaijg, Stephanie Muller, Kacem Nacer, Sylvie Nathanson, Béatrice Pellegrino, Isabelle Pharaon, Véronica Roudault, Sébastien Rouget, Marc Saf, Tabassom Simon, Cedric Tahiri, Tim Ulinski, Férielle Zenkhri

Affiliations

¹ Department of Human Genetics, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
² Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan.
³ Department of Pediatrics, Division of Nephrology, Duke University Medical Center, Durham, North Carolina, USA.
⁴ Department of Medicine-Nephrology, Boston Children's Hospital, Boston, Massachussetts, USA; Medical and Population Genetics, Broad Institute, Cambridge, Massachussetts, USA.
⁵ Department of Biochemistry and Molecular Biology, University of Ulsan College of Medicine, Seoul, Korea.
⁶ Department of Medicine-Nephrology, Boston Children's Hospital, Boston, Massachussetts, USA; Medical and Population Genetics, Broad Institute, Cambridge, Massachussetts, USA; Harvard Medical School, Boston, Massachussetts, USA.
⁷ Clinical Research Center, National Hospital Organization Nagasaki Medical Center, Omura, Japan.
⁸ Department of Integrative Genomics, Tohoku Medical Megabank Organization, Tohoku University, Sendai, Japan.
⁹ Department of Hemodialysis and Apheresis, The University of Tokyo Hospital, Tokyo, Japan.
¹⁰ Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan; Department of Nephrology, Hyogo Prefectural Kobe Children's Hospital, Kobe, Japan.
¹¹ Department of Nephrology, Tokyo Metropolitan Children's Medical Center, Tokyo, Japan.
¹² Department of Pediatrics, Hokkaido University Hospital, Sapporo, Japan.
¹³ Division of Nephrology and Rheumatology, National Center for Child Health and Development, Tokyo, Japan.
¹⁴ Department of Nephrology, Fukuoka Children's Hospital, Fukuoka, Japan.
¹⁵ Department of Pediatrics, Osaka City General Hospital, Osaka, Japan.
¹⁶ Department of Nephrology, Hyogo Prefectural Kobe Children's Hospital, Kobe, Japan.
¹⁷ Department of Pediatrics, Wakayama Medical University, Wakayama, Japan.
¹⁸ Department of Pediatrics, Seoul National University Children's Hospital, Seoul, Korea.
¹⁹ Department of Pediatrics, Jeju National University School of Medicine, Jeju, Korea.
²⁰ Department of Pediatrics, Chonnam National University Children's Hospital, Gwangju, Korea.
²¹ Department of Paediatrics, College of Medicine, University of Lagos, Lagos, Nigeria.
²² Department of Pediatrics, Lagos State University Teaching Hospital, Ikeja, Nigeria.
²³ Department of Paediatric Nephrology, Public Assistance Hospital of Paris, Robert-Debré Hospital, Paris, France.
²⁴ Center of Research on Inflammation, Institut National de la Santé et de la Recherche Médicale UMR 1149, University Sorbonne-Paris, Paris, France.
²⁵ Division of Nephrology and Dialysis, Bambino Gesù Children's Hospital and Research Institute, Rome, Italy.
²⁶ Sorbonne University, INSERM UMR_S1155, and Nephrology Day Hospital, Department of Nephrology, Hôpital Tenon, Paris France.
²⁷ Research Center for Locomotion Biology, Kobe Gakuin University, Kobe, Japan; KNC Department of Nucleic Acid Drug Discovery, Faculty of Rehabilitation, Kobe Gakuin University, Kobe, Japan.
²⁸ Department of Human Genetics, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan. Electronic address: katokunaga@ri.ncgm.go.jp.
²⁹ Department of Pediatrics, Kobe University Graduate School of Medicine, Kobe, Japan. Electronic address: iijima@med.kobe-u.ac.jp.

PMID: 32554042
PMCID: PMC8101291
DOI: 10.1016/j.kint.2020.05.029

Abstract

To understand the genetics of steroid-sensitive nephrotic syndrome (SSNS), we conducted a genome-wide association study in 987 childhood SSNS patients and 3,206 healthy controls with Japanese ancestry. Beyond known associations in the HLA-DR/DQ region, common variants in NPHS1-KIRREL2 (rs56117924, P=4.94E-20, odds ratio (OR) =1.90) and TNFSF15 (rs6478109, P=2.54E-8, OR=0.72) regions achieved genome-wide significance and were replicated in Korean, South Asian and African populations. Trans-ethnic meta-analyses including Japanese, Korean, South Asian, African, European, Hispanic and Maghrebian populations confirmed the significant associations of variants in NPHS1-KIRREL2 (P_meta=6.71E-28, OR=1.88) and TNFSF15 (P_meta=5.40E-11, OR=1.33) loci. Analysis of the NPHS1 risk alleles with glomerular NPHS1 mRNA expression from the same person revealed allele specific expression with significantly lower expression of the transcript derived from the risk haplotype (Wilcox test p=9.3E-4). Because rare pathogenic variants in NPHS1 cause congenital nephrotic syndrome of the Finnish type (CNSF), the present study provides further evidence that variation along the allele frequency spectrum in the same gene can cause or contribute to both a rare monogenic disease (CNSF) and a more complex, polygenic disease (SSNS).

Keywords: glomerulus; nephrotic syndrome; pediatric nephrology; podocyte.

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Figures

**Figure 1.. Flowchart.**
Main outline of the discovery genome-wide association study (GWAS), replication of candidate SNPs outside *HLA* with multiple populations and trans-ethnic meta-analysis. GINS-J: The Research Consortium on Genetics of Childhood Nephrotic Syndrome in Japan, KCHRD: Korean Consortium of Hereditary Renal Diseases in Children, MWPNC: Midwest Pediatric Nephrology Consortium, NPHROVIR: Children Cohort Nephrosis and Virus, ItSpa: Italian and Spanish cohort.

**Figure 2.. Manhattan plot in the discovery GWAS.**
In the discovery stage, 987 patients with childhood SSNS and 3,206 healthy adult controls with 6,834,340 autosomal SNVs and INDELs after whole-genome imputation were included. P-values were calculated using logistic regression and adjusting for sex and PC1-4.

**Figure 3.. Regional plots of loci with genome-wide significance (P<5E-08) or marginal genome-wide significance in the discovery stage.**
**(A)** Classical *HLA* region on chromosome 6 exhibited the most significant association (P-value=2.80E-33). **(B)** Candidate locus with genome-wide significance on chromosome 19 (P-value=4.94E-20). **(C)** Candidate locus with genome-wide significance on chromosome 9 (P-value=2.54E-08). **(D)** Candidate locus with marginal genome-wide significance on chromosome 18 (P=7.68E-08).

**Figure 4.. Glomerular *NPHS1* mRNA expression in NEPTUNE cohort**
**(A)** *NPHS1* fragments per kilobase million (FPKM) expression comparing samples withand without *NPHS1* risk haplotype. Samples with the *NPHS1* risk haplotype do not show significantly different expression levels (Wilcox test p=0.39). **(B)** Allele-specific expression (ASE) comparing samples with and without *NPHS1* risk haplotype. ASE = |0.5 − (haplotype A / total reads)|. In patients with the risk alleles, haplotype A harbors all five *NPHS1* risk variants, in patients without the risk haplotype, haplotype A is randomly selected from one of their two haplotypes. Sample with less than two heterozygous SNPs or in the bottom 10% of total counts are indicated in gray. Samples with the *NPHS1* risk haplotype show significant allele specific expression with lower expression of the risk haplotype (Wilcox test p=9.3E-4).

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References

1. Noone DG, Iijima K, Parekh R. Idiopathic nephrotic syndrome in children. Lancet. 2018;39:61–74. doi: 10.1016/S0140-6736(18)30536-1. - DOI - PubMed
1. Chanchlani R, Parekh RS. Ethnic Differences in Childhood Nephrotic Syndrome. Front Pediatr. 2016;4:39. doi: 10.3389/fped.2016.00039. - DOI - PMC - PubMed
1. Kikunaga K, Ishikura K, Terano C, et al. High incidence of idiopathic nephrotic syndrome in East Asian children: a nationwide survey in Japan (JP-SHINE study). Clin Exp Nephrol. 2017;21:651–657. doi: 10.1007/s10157-016-1319-z. - DOI - PubMed
1. White RH The familial nephrotic syndrome. I. A European survey. Clin Nephrol. 1973;1:215–219. - PubMed
1. Lane BM, Cason R, Esezobor CI, et al. Genetics of Childhood Steroid Sensitive Nephrotic Syndrome: An Update. Front Pediatr 2019;7:8. doi: 10.3389/fped.2019.00008. - DOI - PMC - PubMed

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[1] Noone DG, Iijima K, Parekh R. Idiopathic nephrotic syndrome in children. Lancet. 2018;39:61–74. doi: 10.1016/S0140-6736(18)30536-1. - DOI - PubMed

[2] Noone DG, Iijima K, Parekh R. Idiopathic nephrotic syndrome in children. Lancet. 2018;39:61–74. doi: 10.1016/S0140-6736(18)30536-1. - DOI - PubMed

[3] Chanchlani R, Parekh RS. Ethnic Differences in Childhood Nephrotic Syndrome. Front Pediatr. 2016;4:39. doi: 10.3389/fped.2016.00039. - DOI - PMC - PubMed

[4] Chanchlani R, Parekh RS. Ethnic Differences in Childhood Nephrotic Syndrome. Front Pediatr. 2016;4:39. doi: 10.3389/fped.2016.00039. - DOI - PMC - PubMed

[5] Kikunaga K, Ishikura K, Terano C, et al. High incidence of idiopathic nephrotic syndrome in East Asian children: a nationwide survey in Japan (JP-SHINE study). Clin Exp Nephrol. 2017;21:651–657. doi: 10.1007/s10157-016-1319-z. - DOI - PubMed

[6] Kikunaga K, Ishikura K, Terano C, et al. High incidence of idiopathic nephrotic syndrome in East Asian children: a nationwide survey in Japan (JP-SHINE study). Clin Exp Nephrol. 2017;21:651–657. doi: 10.1007/s10157-016-1319-z. - DOI - PubMed

[7] White RH The familial nephrotic syndrome. I. A European survey. Clin Nephrol. 1973;1:215–219. - PubMed

[8] White RH The familial nephrotic syndrome. I. A European survey. Clin Nephrol. 1973;1:215–219. - PubMed

[9] Lane BM, Cason R, Esezobor CI, et al. Genetics of Childhood Steroid Sensitive Nephrotic Syndrome: An Update. Front Pediatr 2019;7:8. doi: 10.3389/fped.2019.00008. - DOI - PMC - PubMed

[10] Lane BM, Cason R, Esezobor CI, et al. Genetics of Childhood Steroid Sensitive Nephrotic Syndrome: An Update. Front Pediatr 2019;7:8. doi: 10.3389/fped.2019.00008. - DOI - PMC - PubMed

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Common risk variants in NPHS1 and TNFSF15 are associated with childhood steroid-sensitive nephrotic syndrome

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Common risk variants in NPHS1 and TNFSF15 are associated with childhood steroid-sensitive nephrotic syndrome

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