Home LiteratureArticle Details
PMID: 23623387 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Yunis-Varón syndrome is caused by mutations in FIG4, encoding a phosphoinositide phosphatase.

American journal of human genetics ·Vol. 92 ·No. 5 ·2013-05-02 ·Pages 781-91

Campeau PM, Lenk GM, Lu JT, Bae Y, Burrage L, Turnpenny P, Román Corona-Rivera J, Morandi L, Mora M, Reutter H, Vulto-van Silfhout AT, Faivre L, Haan E, Gibbs RA, Meisler MH, Lee BH

Abstract

Yunis-Varón syndrome (YVS) is an autosomal-recessive disorder with cleidocranial dysplasia, digital anomalies, and severe neurological involvement. Enlarged vacuoles are found in neurons, muscle, and cartilage. By whole-exome sequencing, we identified frameshift and missense mutations of FIG4 in affected individuals from three unrelated families. FIG4 encodes a phosphoinositide phosphatase required for regulation of PI(3,5)P(2) levels, and thus endosomal trafficking and autophagy. In a functional assay, both missense substitutions failed to correct the vacuolar phenotype of Fig4-null mouse fibroblasts. Homozygous Fig4-null mice exhibit features of YVS, including neurodegeneration and enlarged vacuoles in neurons. We demonstrate that Fig4-null mice also have small skeletons with reduced trabecular bone volume and cortical thickness and that cultured osteoblasts accumulate large vacuoles. Our findings demonstrate that homozygosity or compound heterozygosity for null mutations of FIG4 is responsible for YVS, the most severe known human phenotype caused by defective phosphoinositide metabolism. In contrast, in Charcot-Marie-Tooth disease type 4J (also caused by FIG4 mutations), one of the FIG4 alleles is hypomorphic and disease is limited to the peripheral nervous system. This genotype-phenotype correlation demonstrates that absence of FIG4 activity leads to central nervous system dysfunction and extensive skeletal anomalies. Our results describe a role for PI(3,5)P(2) signaling in skeletal development and maintenance.

MeSH Terms
Animals Base Sequence Bone Development/genetics Cleidocranial Dysplasia/genetics,pathology Ectodermal Dysplasia/genetics,pathology Exome/genetics Fibroblasts Flavoproteins/genetics Frameshift Mutation/genetics Genetic Predisposition to Disease/genetics Genotype Humans Limb Deformities, Congenital/genetics,pathology Mice Micrognathism/genetics,pathology Molecular Sequence Data Mutation, Missense/genetics Phosphatidylinositol Phosphates/metabolism Phosphoric Monoester Hydrolases Sequence Analysis, DNA
Chemicals
Flavoproteins Phosphatidylinositol Phosphates phosphatidylinositol 3,5-diphosphate FIG4 protein, human Phosphoric Monoester Hydrolases
Authors & Affiliations
16 authors, click to expand affiliations / ORCID
Campeau Philippe M
Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.
Lenk Guy M
Lu James T
Bae Yangjin
Burrage Lindsay
Turnpenny Peter
Román Corona-Rivera Jorge
Morandi Lucia
Mora Marina
Reutter Heiko
Vulto-van Silfhout Anneke T
Faivre Laurence
Haan Eric
Gibbs Richard A
Meisler Miriam H
Lee Brendan H
Supplementary Concepts
Yunis Varon syndrome (Disease)
References (48)
48 references, click to expand
  1. Further delineation of the Yunis-Varon syndrome.
    J Med Genet. 1989 Jan;26(1):55-8 PMID: 2918527
  2. Mutations in KAT6B, encoding a histone acetyltransferase, cause Genitopatellar syndrome.
    Am J Hum Genet. 2012 Feb 10;90(2):282-9 PMID: 22265014
  3. New ocular findings in two sisters with Yunis-Varón syndrome and literature review.
    Eur J Med Genet. 2011 Jan-Feb;54(1):76-81 PMID: 20932945
  4. Primary pulmonary hypertension, congenital heart defect, central nervous system malformations, hypo- and aplastic toes: another case of Yunis-Varón syndrome or report of a new entity.
    Eur J Med Genet. 2012 Jan;55(1):27-31 PMID: 22044576
  5. Extensive molecular genetic analysis of the 3p14.3 region in patients with Zimmermann-Laband syndrome.
    Am J Med Genet A. 2007 Nov 15;143A(22):2668-74 PMID: 17937436
  6. Osteosclerosis owing to Notch gain of function is solely Rbpj-dependent.
    J Bone Miner Res. 2010 Oct;25(10):2175-83 PMID: 20499347
  7. Exome sequencing identifies INPPL1 mutations as a cause of opsismodysplasia.
    Am J Hum Genet. 2013 Jan 10;92(1):144-9 PMID: 23273569
  8. Generalized lysosomal storage in Yunis Varón syndrome.
    Neuromuscul Disord. 1995 Sep;5(5):423-8 PMID: 7496176
  9. Yunis-Varon syndrome: further delineation of the phenotype.
    Am J Med Genet A. 2008 Feb 15;146A(4):532-7 PMID: 18203163
  10. Cleidocranial dysostosis, severe micrognathism, bilateral absence of thumbs and first metatarsal bone, and distal aphalangia: a new genetic syndrome.
    Am J Dis Child. 1980 Jul;134(7):649-53 PMID: 7395825
  11. Neuronal expression of Fig4 is both necessary and sufficient to prevent spongiform neurodegeneration.
    Hum Mol Genet. 2012 Aug 15;21(16):3525-34 PMID: 22581779
  12. Endosomal phosphoinositides and human diseases.
    Traffic. 2008 Aug;9(8):1240-9 PMID: 18429927
  13. Yunis Varon syndrome.
    Indian J Pediatr. 2006 Apr;73(4):353-5 PMID: 16816498
  14. Human WIPI-1 puncta-formation: a novel assay to assess mammalian autophagy.
    FEBS Lett. 2007 Jul 24;581(18):3396-404 PMID: 17618624
  15. Yeast vacuole inheritance and dynamics.
    Annu Rev Genet. 2003;37:435-60 PMID: 14616069
  16. Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology.
    Trends Mol Med. 2012 Jun;18(6):317-27 PMID: 22578719
  17. Congenital CNS hypomyelination in the Fig4 null mouse is rescued by neuronal expression of the PI(3,5)P(2) phosphatase Fig4.
    J Neurosci. 2011 Nov 30;31(48):17736-51 PMID: 22131434
  18. Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system.
    Nucleic Acids Res. 2013 Jan;41(Database issue):D996-D1008 PMID: 23193282
  19. A case of Yunis-Varon syndrome complicated with complete cleft lip and palate.
    Am J Med Genet A. 2004 Feb 15;125A(1):92-3 PMID: 14755473
  20. Yunis-Varon syndrome with severe osteodysplasty.
    J Med Genet. 1990 Feb;27(2):114-21 PMID: 2319578
  21. Yunis-Varon syndrome: the first case of German origin.
    Clin Dysmorphol. 1996 Jul;5(3):217-22 PMID: 8818450
  22. Crystal structure of the yeast Sac1: implications for its phosphoinositide phosphatase function.
    EMBO J. 2010 May 5;29(9):1489-98 PMID: 20389282
  23. VAC14 nucleates a protein complex essential for the acute interconversion of PI3P and PI(3,5)P(2) in yeast and mouse.
    EMBO J. 2008 Dec 17;27(24):3221-34 PMID: 19037259
  24. Dynamic control of neuroexocytosis by phosphoinositides in health and disease.
    Prog Lipid Res. 2011 Jan;50(1):52-61 PMID: 20705095
  25. Atrophy of the left lobe of the liver and anomalous hepatic vessel in a patient with Yunis-Varon syndrome.
    J Clin Gastroenterol. 1999 Sep;29(2):210-1 PMID: 10478891
  26. Missense mutations abolishing DNA binding of the osteoblast-specific transcription factor OSF2/CBFA1 in cleidocranial dysplasia.
    Nat Genet. 1997 Jul;16(3):307-10 PMID: 9207800
  27. Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J.
    Nature. 2007 Jul 5;448(7149):68-72 PMID: 17572665
  28. Pathogenic mechanism of the FIG4 mutation responsible for Charcot-Marie-Tooth disease CMT4J.
    PLoS Genet. 2011 Jun;7(6):e1002104 PMID: 21655088
  29. Yunis-Varon syndrome: evidence for a lysosomal storage disease.
    Am J Med Genet. 2000 Nov 13;95(2):157-60 PMID: 11078567
  30. [Yunis-Varon syndrome: a case report].
    Gac Med Mex. 2012 Jan-Feb;148(1):81-2 PMID: 22367312
  31. Hypodontia, impacted permanent teeth, spinal defects, and cardiomegaly in a previously diagnosed case of the Yunis-Varon syndrome.
    Oral Surg Oral Med Oral Pathol. 1992 Apr;73(4):456-60 PMID: 1533447
  32. Whole-exome sequencing identifies mutations in the nucleoside transporter gene SLC29A3 in dysosteosclerosis, a form of osteopetrosis.
    Hum Mol Genet. 2012 Nov 15;21(22):4904-9 PMID: 22875837
  33. Whole-genome analysis reveals that mutations in inositol polyphosphate phosphatase-like 1 cause opsismodysplasia.
    Am J Hum Genet. 2013 Jan 10;92(1):137-43 PMID: 23273567
  34. Cleidocranial dysplasia with neonatal death due to central nervous system injury in utero: case report and literature review.
    Pediatr Dev Pathol. 1998 Jul-Aug;1(4):314-8 PMID: 10463294
  35. Distinctive genetic and clinical features of CMT4J: a severe neuropathy caused by mutations in the PI(3,5)P₂ phosphatase FIG4.
    Brain. 2011 Jul;134(Pt 7):1959-71 PMID: 21705420
  36. Yunis-Varon syndrome.
    Indian Pediatr. 2005 Apr;42(4):373-5 PMID: 15876600
  37. Aplasia of the thumbs and great toes as the outstanding feature of Yunis and Varon syndrome. A new entity. A new observation.
    Ann Genet. 1988;31(4):241-3 PMID: 3265308
  38. ArPIKfyve regulates Sac3 protein abundance and turnover: disruption of the mechanism by Sac3I41T mutation causing Charcot-Marie-Tooth 4J disorder.
    J Biol Chem. 2010 Aug 27;285(35):26760-26764 PMID: 20630877
  39. FUS, TARDBP, and SOD1 mutations in a Taiwanese cohort with familial ALS.
    Neurobiol Aging. 2011 Mar;32(3):553.e13-21 PMID: 20472325
  40. PtdIns(3,5)P2 and autophagy in mouse models of neurodegeneration.
    Autophagy. 2010 Jan;6(1):170-1 PMID: 20009544
  41. Mouse clavicular development: analysis of wild-type and cleidocranial dysplasia mutant mice.
    Dev Dyn. 1997 Sep;210(1):33-40 PMID: 9286593
  42. Brief clinical report: the syndrome of Yunis and Varón--report of a further case.
    Am J Med Genet. 1983 Mar;14(3):539-44 PMID: 6859104
  43. Assembly of a Fab1 phosphoinositide kinase signaling complex requires the Fig4 phosphoinositide phosphatase.
    Mol Biol Cell. 2008 Oct;19(10):4273-86 PMID: 18653468
  44. Congenital heart malformation in Yunis-Varón syndrome.
    J Med Genet. 1993 Sep;30(9):788-92 PMID: 8411078
  45. Deleterious variants of FIG4, a phosphoinositide phosphatase, in patients with ALS.
    Am J Hum Genet. 2009 Jan;84(1):85-8 PMID: 19118816
  46. Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2.
    Hum Mol Genet. 2009 Dec 15;18(24):4868-78 PMID: 19793721
  47. [Yunis-Varon syndrome].
    Ryoikibetsu Shokogun Shirizu. 2001;(34 Pt 2):839-40 PMID: 11529050
  48. The FIG4 gene does not play a major role in causing ALS in Italian patients.
    Amyotroph Lateral Scler Frontotemporal Degener. 2013 Apr;14(3):228-9 PMID: 23336365
Article Info
Journal
American journal of human genetics
Abbr.
Am J Hum Genet
ISSN
1537-6605
Published
2013-05-02
Epub
2013-00-25
Pages
781-91
Language
English
Region
United States
NLM ID
0370475
PMCID
PMC3644641
Subset
IM
Grants
NCATS NIH HHS · UL1 TR000433 · United States
NICHD NIH HHS · P01 HD022657 · United States
NHGRI NIH HHS · U54 HG003273 · United States
NIMH NIH HHS · F30 MH098571-01 · United States
NIGMS NIH HHS · R01 GM024872 · United States
NIGMS NIH HHS · R01 GM24872 · United States
NICHD NIH HHS · P01 HD070394 · United States
NHGRI NIH HHS · U54 HG003273-09 · United States
NICHD NIH HHS · P01 HD22657 · United States
NIMH NIH HHS · F30 MH098571 · United States
Telethon · GTB07001 · Italy
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com