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01-11-2018 | Glycogen Storage Disease

Polycystic kidney features of the renal pathology in glycogen storage disease type I: possible evolution to renal neoplasia

Authors: Monika Gjorgjieva, Laure Monteillet, Julien Calderaro, Gilles Mithieux, Fabienne Rajas

Published in: Journal of Inherited Metabolic Disease | Issue 6/2018

Abstract

Glycogen storage disease type I (GSDI) is a rare genetic pathology characterized by glucose-6 phosphatase (G6Pase) deficiency, translating in hypoglycemia during short fasts. Besides metabolic perturbations, GSDI patients develop long-term complications, especially chronic kidney disease (CKD). In GSDI patients, CKD is characterized by an accumulation of glycogen and lipids in kidneys, leading to a gradual decline in renal function. At a molecular level, the activation of the renin-angiotensin system is responsible for the development of renal fibrosis, eventually leading to renal failure. The same CKD phenotype was observed in a mouse model with a kidney-specific G6Pase deficiency (K.G6pc−/− mice). Furthermore, GSDI patients and mice develop frequently renal cysts at late stages of the nephropathy, classifying GSDI as a potential polycystic kidney disease (PKD). PKDs are genetic disorders characterized by multiple renal cyst formation, frequently caused by the loss of expression of polycystic kidney genes, such as PKD1/2 and PKHD1. Interestingly, these genes are deregulated in K.G6pc−/− kidneys, suggesting their possible role in GSDI cystogenesis. Finally, renal cysts are known to predispose to renal malignancy development. In addition, HNF1B loss is a malignancy prediction factor. Interestingly, Hnf1b expression was decreased in K.G6pc−/− kidneys. While a single case of renal cancer has been reported in a GSDI patient, a clear cell renal carcinoma was recently observed in one K.G6pc−/− mouse (out of 36 studied mice) at a later stage of the disease. This finding highlights the need to further analyze renal cyst development in GSDI patients in order to evaluate the possible associated risk of carcinogenesis, even if the risk might be limited.

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Baker L, Dahlem S, Goldfarb S, Kern EFO, Stanley CA, Egler J, Olshan JS, Heyman S (1989) Hyperfiltration and renal disease in glycogen storage disease, type I. Kidney Int 35:1345–1350CrossRefPubMed

Bienaimé F, Canaud G, El Karoui K, Gallazzini M, Terzi F (2016) Molecular pathways of chronic kidney disease progression. Nephrol Ther 12(Suppl 1):S35–S38CrossRefPubMed

Bingham C, Bulman MP, Ellard S, Allen LI, Lipkin GW, Hoff WG, Woolf AS, Rizzoni G, Novelli G, Nicholls AJ et al (2001) Mutations in the hepatocyte nuclear factor-1beta gene are associated with familial hypoplastic glomerulocystic kidney disease. Am J Hum Genet 68:219–224CrossRefPubMed

Bonsib SM (2009) Renal cystic diseases and renal neoplasms: a mini-review. Clin J Am Soc Nephrol 4:1998–2007CrossRefPubMed

Bosniak MA (1986) The current radiological approach to renal cysts. Radiology 158:1–10CrossRefPubMed

Bruni N, Rajas F, Montano S, Chevalier-Porst F, Maire I, Mithieux G (1999) Enzymatic characterization of four new mutations in the glucose-6 phosphatase (G6PC) gene which cause glycogen storage disease type 1a. Ann Hum Genet 63:141–146CrossRefPubMed

Buchner A, Castro M, Hennig A, Popp T, Assmann G, Stief CG, Zimmermann W (2010) Downregulation of HNF-1B in renal cell carcinoma is associated with tumor progression and poor prognosis. Urology 76:507CrossRefPubMed

Calderaro J, Labrune P, Morcrette G, Rebouissou S, Franco D, Prévot S, Quaglia A, Bedossa P, Libbrecht L, Terracciano L et al (2013) Molecular characterization of hepatocellular adenomas developed in patients with glycogen storage disease type I. J Hepatol 58:350–357CrossRefPubMed

Chen YT (1991) Type I glycogen storage disease: kidney involvement, pathogenesis and its treatment. Pediatr Nephrol 5:71–76CrossRefPubMed

Chevalier-Porst F, Bozon D, Bonardot AM, Bruni N, Mithieux G, Mathieu M, Maire I (1996) Mutation analysis in 24 French patients with glycogen storage disease type 1a. J Med Genet 33:358–360CrossRefPubMedPubMedCentral

Clar J, Gri B, Calderaro J, Birling M-C, Hérault Y, Smit GPA, Mithieux G, Rajas F (2014) Targeted deletion of kidney glucose-6 phosphatase leads to nephropathy. Kidney Int 86:747–756CrossRefPubMedPubMedCentral

Clissold RL, Hamilton AJ, Hattersley AT, Ellard S, Bingham C (2015) HNF1B-associated renal and extra-renal disease—an expanding clinical spectrum. Nat Rev Nephrol 11:102CrossRefPubMed

Dambska M, Labrador EB, Kuo CL, Weinstein DA (2017) Prevention of complications in glycogen storage disease type Ia with optimization of metabolic control. Pediatr Diabetes 18:327–331CrossRefPubMed

Devarajan P (2010) Review: neutrophil gelatinase-associated lipocalin: a troponin-like biomarker for human acute kidney injury. Nephrology 15:419–428CrossRefPubMed

Donadieu J, Barkaoui M, Bézard F, Bertrand Y, Pondarré C, Guibaud P (2000) Renal carcinoma in a patient with glycogen storage disease Ib receiving long-term granulocyte colony-stimulating factor therapy. J Pediatr Hematol Oncol 22:188–189CrossRefPubMed

Eccles MR, Stayner CA (2014) Polycystic kidney disease—where gene dosage counts. F1000Prime Rep 6:24CrossRefPubMedPubMedCentral

Edghill EL, Bingham C, Ellard S, Hattersley AT (2006) Mutations in hepatocyte nuclear factor-1beta and their related phenotypes. J Med Genet 43:84–90CrossRefPubMed

Eknoyan G (2009) A clinical view of simple and complex renal cysts. J Am Soc Nephrol 20:1874–1876CrossRefPubMed

Faguer S, Decramer S, Chassaing N, Bellanné-Chantelot C, Calvas P, Beaufils S, Bessenay L, Lengelé J-P, Dahan K, Ronco P et al (2011) Diagnosis, management, and prognosis of HNF1B nephropathy in adulthood. Kidney Int 80:768–776CrossRefPubMed

Fedeles SV, Gallagher A-R, Somlo S (2014) Polycystin-1: a master regulator of intersecting cystic pathways. Trends Mol Med 20:251–260CrossRefPubMedPubMedCentral

Fischer E, Legue E, Doyen A, Nato F, Nicolas J-F, Torres V, Yaniv M, Pontoglio M (2006) Defective planar cell polarity in polycystic kidney disease. Nat Genet 38:21CrossRefPubMed

Follit JA, Li L, Vucica Y, Pazour GJ (2010) The cytoplasmic tail of fibrocystin contains a ciliary targeting sequence. J Cell Biol 188:21–28CrossRefPubMedPubMedCentral

Franco LM, Krishnamurthy V, Bali D, Weinstein DA, Arn P, Clary B, Boney A, Sullivan J, Frush DP, Chen Y-T et al (2005) Hepatocellular carcinoma in glycogen storage disease type Ia: a case series. J Inherit Metab Dis 28:153–162CrossRefPubMed

Froissart R, Piraud M, Boudjemline AM, Vianey-Saban C, Petit F, Hubert-Buron A, Eberschweiler PT, Gajdos V, Labrune P (2011) Glucose-6-phosphatase deficiency. Orphanet J Rare Dis 6:27CrossRefPubMedPubMedCentral

Garcia-Gonzalez MA, Menezes LF, Piontek KB, Kaimori J, Huso DL, Watnick T, Onuchic LF, Guay-Woodford LM, Germino GG (2007) Genetic interaction studies link autosomal dominant and recessive polycystic kidney disease in a common pathway. Hum Mol Genet 16:1940–1950CrossRefPubMedPubMedCentral

Gjorgjieva M, Raffin M, Duchampt A, Perry A, Stefanutti A, Brevet M, Tortereau A, Dubourg L, Hubert-Buron A, Mabille M et al (2016) Progressive development of renal cysts in glycogen storage disease type I. Hum Mol Genet 25:3784–3797CrossRefPubMed

Graumann O, Osther SS, Osther PJS (2011) Characterization of complex renal cysts: a critical evaluation of the Bosniak classification. Scand J Urol Nephrol 45:84–90CrossRefPubMed

Gresh L, Fischer E, Reimann A, Tanguy M, Garbay S, Shao X, Hiesberger T, Fiette L, Igarashi P, Yaniv M et al (2004) A transcriptional network in polycystic kidney disease. EMBO J 23:1657–1668CrossRefPubMedPubMedCentral

Harris PC (2002) Molecular basis of polycystic kidney disease: PKD1, PKD2 and PKHD1. Curr Opin Nephrol Hypertens 11:309–314CrossRefPubMed

Harris PC, Torres VE (2009) Polycystic kidney disease. Annu Rev Med 60:321–337CrossRefPubMedPubMedCentral

Hiesberger T, Shao X, Gourley E, Reimann A, Pontoglio M, Igarashi P (2005) Role of the hepatocyte nuclear factor-1beta (HNF-1beta) C-terminal domain in Pkhd1 (ARPKD) gene transcription and renal cystogenesis. J Biol Chem 280:10578–10586CrossRefPubMed

Horikawa Y, Iwasaki N, Hara M, Furuta H, Hinokio Y, Cockburn BN, Lindner T, Yamagata K, Ogata M, Tomonaga O et al (1997) Mutation in hepatocyte nuclear factor-1 beta gene (TCF2) associated with MODY. Nat Genet 17:384–385CrossRefPubMed

Hosseini M, Antic T, Paner GP, Chang A (2014) Pathologic spectrum of cysts in end-stage kidneys: possible precursors to renal neoplasia. Hum Pathol 45:1406–1413CrossRefPubMed

Igarashi P, Shao X, McNally BT, Hiesberger T (2005) Roles of HNF-1beta in kidney development and congenital cystic diseases. Kidney Int 68:1944–1947CrossRef

Iwasaki N, Ogata M, Tomonaga O, Kuroki H, Kasahara T, Yano N, Iwamoto Y (1998) Liver and kidney function in Japanese patients with maturity-onset diabetes of the young. Diabetes Care 21:2144–2148CrossRefPubMed

Jiang S-T, Chiou Y-Y, Wang E, Lin H-K, Lin Y-T, Chi Y-C, Wang C-KL, Tang M-J, Li H (2006) Defining a link with autosomal-dominant polycystic kidney disease in mice with congenitally low expression of Pkd1. Am J Pathol 168:205–220CrossRefPubMedPubMedCentral

Jilg CA, Drendel V, Bacher J, Pisarski P, Neeff H, Drognitz O, Schwardt M, Gläsker S, Malinoc A, Erlic Z et al (2013) Autosomal dominant polycystic kidney disease: prevalence of renal neoplasias in surgical kidney specimens. Nephron Clin Pract 123:13–21CrossRefPubMed

Karoui KE, Viau A, Dellis O, Bagattin A, Nguyen C, Baron W, Burtin M, Broueilh M, Heidet L, Mollet G et al (2016) Endoplasmic reticulum stress drives proteinuria-induced kidney lesions via Lipocalin 2. Nat Commun 7:10330CrossRefPubMedPubMedCentral

Kim S, Nie H, Nesin V, Tran U, Outeda P, Bai C-X, Keeling J, Maskey D, Watnick T, Wessely O et al (2016) The polycystin complex mediates WNT/Ca2+ signaling. Nat Cell Biol 18:752–764CrossRefPubMedPubMedCentral

Kishnani PS, Austin SL, Abdenur JE, Arn P, Bali DS, Boney A, Chung WK, Dagli AI, Dale D, Koeberl D et al (2014) Diagnosis and management of glycogen storage disease type I: a practice guideline of the American College of Medical Genetics and Genomics. Genet Med e1:16

Kornfeld J-W, Baitzel C, Könner AC, Nicholls HT, Vogt MC, Herrmanns K, Scheja L, Haumaitre C, Wolf AM, Knippschild U et al (2013) Obesity-induced overexpression of miR-802 impairs glucose metabolism through silencing of Hnf1b. Nature 494:111–115CrossRefPubMed

Labrune P (2002) Glycogen storage disease type I: indications for liver and/or kidney transplantation. Eur J Pediatr 161:S53–S55CrossRefPubMed

Lan HY (2011) Diverse roles of TGF-β/Smads in renal fibrosis and inflammation. Int J Biol Sci 7:1056–1067CrossRefPubMedPubMedCentral

Lantinga-van Leeuwen IS, Dauwerse JG, Baelde HJ, Leonhard WN, van de Wal A, Ward CJ, Verbeek S, Deruiter MC, Breuning MH, de Heer E et al (2004) Lowering of Pkd1 expression is sufficient to cause polycystic kidney disease. Hum Mol Genet 13:3069–3077CrossRefPubMed

Le Corre S, Viau A, Burtin M, El-Karoui K, Cnops Y, Terryn S, Debaix H, Bérissi S, Gubler M-C, Devuyst O et al (2015) Cystic gene dosage influences kidney lesions after nephron reduction. Nephron 129:42–51CrossRefPubMed

Lee SH, Somlo S (2014) Cyst growth, polycystins, and primary cilia in autosomal dominant polycystic kidney disease. Kidney Res Clin Pract 33:73–78CrossRefPubMedPubMedCentral

Leonhard WN, Happe H, Peters DJM (2016) Variable cyst development in autosomal dominant polycystic kidney disease: the biologic context. J Am Soc Nephrol 27:3530–3538CrossRefPubMedPubMedCentral

Liu Z, Zhu Y, Wang Y, Fu Q, Fu H, Wang Z, Zhang J, Li G, Xu J, Dai B (2017) Prognostic value of granulocyte colony-stimulating factor in patients with non-metastatic clear cell renal cell carcinoma. Oncotarget 8:69961PubMedPubMedCentral

Loftus H, Ong ACM (2013) Cystic kidney diseases: many ways to form a cyst. Pediatr Nephrol 28:33–49CrossRefPubMed

Lu W, Shen X, Pavlova A, Lakkis M, Ward CJ, Pritchard L, Harris PC, Genest DR, Perez-Atayde AR, Zhou J (2001) Comparison of Pkd1-targeted mutants reveals that loss of polycystin-1 causes cystogenesis and bone defects. Hum Mol Genet 10:2385–2396CrossRefPubMed

Madariaga L, Morinière V, Jeanpierre C, Bouvier R, Loget P, Martinovic J, Dechelotte P, Leporrier N, Thauvin-Robinet C, Jensen UB et al (2013) Severe prenatal renal anomalies associated with mutations in HNF1B or PAX2 genes. Clin J Am Soc Nephrol 8:1179–1187CrossRefPubMedPubMedCentral

Martens DHJ, Rake JP, Navis G, Fidler V, van Dael CML, Smit GPA (2009) Renal function in glycogen storage disease type I, natural course, and renopreservative effects of ACE inhibition. Clin J Am Soc Nephrol 4:1741–1746CrossRefPubMedPubMedCentral

Massa F, Garbay S, Bouvier R, Sugitani Y, Noda T, Gubler M-C, Heidet L, Pontoglio M, Fischer E (2013) Hepatocyte nuclear factor 1β controls nephron tubular development. Development 140:886–896CrossRefPubMed

Meng X-M, Tang PM-K, Li J, Lan HY (2015) TGF-β/Smad signaling in renal fibrosis. Front Physiol 6:82CrossRefPubMedPubMedCentral

Muglia VF, Prando A (2015) Renal cell carcinoma: histological classification and correlation with imaging findings. Radiol Bras 48:166–174CrossRefPubMedPubMedCentral

Mundy HR, Lee PJ (2002) Glycogenosis type I and diabetes mellitus: a common mechanism for renal dysfunction? Med Hypotheses 59:110–114CrossRefPubMed

Okechuku GO, Shoemaker LR, Dambska M, Brown LM, Mathew J, Weinstein DA (2017) Tight metabolic control plus ACE inhibitor therapy improves GSD I nephropathy. J Inherit Metab Dis 40:703–708CrossRefPubMed

Ong ACM, Harris PC (2005) Molecular pathogenesis of ADPKD: the polycystin complex gets complex. Kidney Int 67:1234–1247CrossRefPubMed

Pei Y (2001) A “two-hit” model of cystogenesis in autosomal dominant polycystic kidney disease? Trends Mol Med 7:151–156CrossRefPubMed

Pritchard L, Sloane-Stanley JA, Sharpe JA, Aspinwall R, Lu W, Buckle V, Strmecki L, Walker D, Ward CJ, Alpers CE et al (2000) A human PKD1 transgene generates functional polycystin-1 in mice and is associated with a cystic phenotype. Hum Mol Genet 9:2617–2627CrossRefPubMed

Rajas F, Labrune P, Mithieux G (2013) Glycogen storage disease type 1 and diabetes: learning by comparing and contrasting the two disorders. Diabetes Metab 39:377–387CrossRefPubMed

Rake JP, Visser G, Labrune P, Leonard JV, Ullrich K, Smit GPA (2002) Glycogen storage disease type I: diagnosis, management, clinical course and outcome. Results of the European Study on Glycogen Storage Disease Type I (ESGSD I). Eur J Pediatr 161(Suppl 1):S20–S34CrossRefPubMed

Rebouissou S, Vasiliu V, Thomas C, Bellanné-Chantelot C, Bui H, Chrétien Y, Timsit J, Rosty C, Laurent-Puig P, Chauveau D et al (2005) Germline hepatocyte nuclear factor 1alpha and 1beta mutations in renal cell carcinomas. Hum Mol Genet 14:603–614CrossRefPubMed

Reitsma-Bierens WCC, Smit GPA, Troelstra JA (1992) Renal function and kidney size in glycogen storage disease type I. Pediatr Nephrol 6:236–238CrossRefPubMed

Rogers KA, Moreno SE, Smith LA, Husson H, Bukanov NO, Ledbetter SR, Budman Y, Lu Y, Wang B, Ibraghimov-Beskrovnaya O et al (2016) Differences in the timing and magnitude of Pkd1 gene deletion determine the severity of polycystic kidney disease in an orthologous mouse model of ADPKD. Physiol Rep 4

Seeger-Nukpezah T, Geynisman DM, Nikonova AS, Benzing T, Golemis EA (2015) The hallmarks of cancer: relevance to the pathogenesis of polycystic kidney disease. Nat Rev Nephrol 11:515–534CrossRefPubMedPubMedCentral

Soty M, Gautier-Stein A, Rajas F, Mithieux G (2017) Gut-brain glucose signaling in energy homeostasis. Cell Metab 25:1231–1242CrossRefPubMed

Thivierge C, Kurbegovic A, Couillard M, Guillaume R, Coté O, Trudel M (2006) Overexpression of PKD1 causes polycystic kidney disease. Mol Cell Biol 26:1538–1548CrossRefPubMedPubMedCentral

Thomas R, Sanna-Cherchi S, Warady BA, Furth SL, Kaskel FJ, Gharavi AG (2011) HNF1B and PAX2 mutations are a common cause of renal hypodysplasia in the CKiD cohort. Pediatr Nephrol 26:897–903CrossRefPubMedPubMedCentral

Verhave JC, Bech AP, Wetzels JFM, Nijenhuis T (2016) Hepatocyte nuclear factor 1β–associated kidney disease: more than renal cysts and diabetes. J Am Soc Nephrol 27:345–353CrossRef

Viau A, Karoui KE, Laouari D, Burtin M, Nguyen C, Mori K, Pillebout E, Berger T, Mak TW, Knebelmann B et al (2010) Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 120:4065–4076CrossRefPubMedPubMedCentral

Walters W, Braasch WF (1934) Surgical aspect of polycystic kidney. Surg Gynec Obstet 58:647–650

Warren KS, McFarlane J (2005) The Bosniak classification of renal cystic masses. BJU Int 95:939–942CrossRefPubMed

Wu G, D’Agati V, Cai Y, Markowitz G, Park JH, Reynolds DM, Maeda Y, Le TC, Hou H, Kucherlapati R et al (1998) Somatic inactivation of Pkd2 results in polycystic kidney disease. Cell 93:177–188CrossRefPubMed

Wu Y, Dai X-Q, Li Q, Chen CX, Mai W, Hussain Z, Long W, Montalbetti N, Li G, Glynne R et al (2006) Kinesin-2 mediates physical and functional interactions between polycystin-2 and fibrocystin. Hum Mol Genet 15:3280–3292CrossRefPubMed

Wu X, He Y, Jing Y, Li K, Zhang J (2010) Albumin overload induces apoptosis in renal tubular epithelial cells through a CHOP-dependent pathway. OMICS 14:61–73CrossRefPubMed

Yiu WH, Pan C-J, Ruef RA, Peng W-T, Starost MF, Mansfield BC, Chou JY (2008a) The angiotensin system mediates renal fibrosis in glycogen storage disease type Ia nephropathy. Kidney Int 73:716–723CrossRefPubMed

Yiu WH, Pan C-J, Ruef RA, Peng W-T, Starost MF, Mansfield BC, Chou JY (2008b) Angiotensin mediates renal fibrosis in the nephropathy of glycogen storage disease type Ia. Kidney Int 73:716–723CrossRefPubMed

Yu T-M, Chuang Y-W, Yu M-C, Chen C-H, Yang C-K, Huang S-T, Lin C-L, Shu K-H, Kao C-H (2016) Risk of cancer in patients with polycystic kidney disease: a propensity-score matched analysis of a nationwide, population-based cohort study. Lancet Oncol 17:1419–1425CrossRefPubMed

Title: Polycystic kidney features of the renal pathology in glycogen storage disease type I: possible evolution to renal neoplasia
Authors: Monika Gjorgjieva
Laure Monteillet
Julien Calderaro
Gilles Mithieux
Fabienne Rajas
Publication date: 01-11-2018
Publisher: Springer Netherlands
Published in: Journal of Inherited Metabolic Disease / Issue 6/2018
Print ISSN: 0141-8955
Electronic ISSN: 1573-2665
DOI: https://doi.org/10.1007/s10545-018-0207-y

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