Small 6q16.1 Deletions Encompassing POU3F2 Cause Susceptibility to Obesity and Variable Developmental Delay with Intellectual Disability.

Genetic studies of intellectual disability and identification of monogenic causes of obesity in humans have made immense contribution toward the understanding of the brain and control of body mass. The leptin > melanocortin > SIM1 pathway is dysregulated in multiple monogenic human obesity syndromes but its downstream targets are still unknown. In ten individuals from six families, with overlapping 6q16.1 deletions, we describe a disorder of variable developmental delay, intellectual disability, and susceptibility to obesity and hyperphagia. The 6q16.1 deletions segregated with the phenotype in multiplex families and were shown to be de novo in four families, and there was dramatic phenotypic overlap among affected individuals who were independently ascertained without bias from clinical features. Analysis of the deletions revealed a ∼350 kb critical region on chromosome 6q16.1 that encompasses a gene for proneuronal transcription factor POU3F2, which is important for hypothalamic development and function. Using morpholino and mutant zebrafish models, we show that POU3F2 lies downstream of SIM1 and controls oxytocin expression in the hypothalamic neuroendocrine preoptic area. We show that this finding is consistent with the expression patterns of POU3F2 and related genes in the human brain. Our work helps to further delineate the neuro-endocrine control of energy balance/body mass and demonstrates that this molecular pathway is conserved across multiple species.

[1]  Gregory M. Cooper,et al.  A Copy Number Variation Morbidity Map of Developmental Delay , 2011, Nature Genetics.

[2]  J. Michaud,et al.  ARNT2 acts as the dimerization partner of SIM1 for the development of the hypothalamus , 2000, Mechanisms of Development.

[3]  E. Glasgow,et al.  The zebrafish bHLH PAS transcriptional regulator, single‐minded 1 (sim1), is required for isotocin cell development , 2006, Developmental dynamics : an official publication of the American Association of Anatomists.

[4]  E. Glasgow,et al.  Ontogeny of vasotocin‐expressing cells in zebrafish: Selective requirement for the transcriptional regulators orthopedia and single‐minded 1 in the preoptic area , 2008, Developmental dynamics : an official publication of the American Association of Anatomists.

[5]  H. Yao,et al.  Oxytocin mediates early experience–dependent cross-modal plasticity in the sensory cortices , 2014, Nature Neuroscience.

[6]  Stylianos E. Antonarakis,et al.  Mendelian disorders deserve more attention , 2006, Nature Reviews Genetics.

[7]  Pawel Stankiewicz,et al.  Genomic Disorders: Molecular Mechanisms for Rearrangements and Conveyed Phenotypes , 2005, PLoS genetics.

[8]  Pasko Rakic,et al.  POU-III transcription factors (Brn1, Brn2, and Oct6) influence neurogenesis, molecular identity, and migratory destination of upper-layer cells of the cerebral cortex. , 2013, Cerebral cortex.

[9]  L. Nguyen,et al.  Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. , 2006, Developmental cell.

[10]  Beverley Balkau,et al.  Loss-of-function mutations in SIM1 contribute to obesity and Prader-Willi-like features. , 2013, The Journal of clinical investigation.

[11]  J. Michaud,et al.  Impact of Sim1 gene dosage on the development of the paraventricular and supraoptic nuclei of the hypothalamus , 2009, The European journal of neuroscience.

[12]  I. Farooqi,et al.  Genetic approaches to understanding human obesity. , 2011, The Journal of clinical investigation.

[13]  A. Monaco,et al.  A forkhead-domain gene is mutated in a severe speech and language disorder , 2001, Nature.

[14]  S. Minoshima,et al.  Role of TBX1 in human del22q11.2 syndrome , 2003, The Lancet.

[15]  E. Glasgow,et al.  Zebrafish orthopedia (otp) is required for isotocin cell development , 2007, Development Genes and Evolution.

[16]  Nancy Hopkins,et al.  Insertional mutagenesis in zebrafish rapidly identifies genes essential for early vertebrate development , 2002, Nature Genetics.

[17]  H. Burbano,et al.  A recent evolutionary change affects a regulatory element in the human FOXP2 gene. , 2013, Molecular biology and evolution.

[18]  Janice M. Fullerton,et al.  Genome-wide association study reveals two new risk loci for bipolar disorder , 2014, Nature Communications.

[19]  C. Kimmel,et al.  Stages of embryonic development of the zebrafish , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[20]  C. S. Carter,et al.  Oxytocin pathways and the evolution of human behavior. , 2014, Annual review of psychology.

[21]  Kali T. Witherspoon,et al.  Refining analyses of copy number variation identifies specific genes associated with developmental delay , 2014, Nature Genetics.

[22]  M. Rosenfeld,et al.  Transcriptional Regulation of Cortical Neuron Migration by POU Domain Factors , 2002, Science.

[23]  M. Nalls,et al.  Human Obesity Associated with an Intronic SNP in the Brain-Derived Neurotrophic Factor Locus. , 2015, Cell reports.

[24]  A. Zinn,et al.  Profound obesity associated with a balanced translocation that disrupts the SIM1 gene. , 2000, Human molecular genetics.

[25]  A. Zinn,et al.  Oxytocin deficiency mediates hyperphagic obesity of Sim1 haploinsufficient mice. , 2008, Molecular endocrinology.

[26]  Marni J. Falk,et al.  Mutations in FBXL4, encoding a mitochondrial protein, cause early-onset mitochondrial encephalomyopathy. , 2013, American journal of human genetics.

[27]  Mehul Dattani,et al.  Rare variants in single-minded 1 (SIM1) are associated with severe obesity. , 2013, The Journal of clinical investigation.

[28]  Lydia Ng,et al.  The Allen Brain Atlas , 2014 .

[29]  Nga Thi Thuy Nguyen,et al.  Genomicus update 2015: KaryoView and MatrixView provide a genome-wide perspective to multispecies comparative genomics , 2014, Nucleic Acids Res..

[30]  Tomas W. Fitzgerald,et al.  Large-scale discovery of novel genetic causes of developmental disorders , 2014, Nature.

[31]  J. Kleinman,et al.  Spatiotemporal transcriptome of the human brain , 2011, Nature.

[32]  H. Leonard,et al.  The epidemiology of mental retardation: challenges and opportunities in the new millennium. , 2002, Mental retardation and developmental disabilities research reviews.

[33]  Tetsuo Noda,et al.  Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. , 2002, Genes & development.

[34]  P. Sawchenko,et al.  Development and survival of the endocrine hypothalamus and posterior pituitary gland requires the neuronal POU domain factor Brn-2. , 1995, Genes & development.

[35]  G. Uhl,et al.  Brain-derived neurotrophic factor and obesity in the WAGR syndrome. , 2008, The New England journal of medicine.

[36]  J. Michaud,et al.  Development of neuroendocrine lineages requires the bHLH-PAS transcription factor SIM1. , 1998, Genes & development.

[37]  N. Carter,et al.  Deciphering Developmental Disorders , 2012 .

[38]  Insuk Lee,et al.  Characterising and Predicting Haploinsufficiency in the Human Genome , 2010, PLoS genetics.

[39]  J. Rosenfeld,et al.  Genotype–phenotype correlation in interstitial 6q deletions: a report of 12 new cases , 2012, neurogenetics.

[40]  D. Ledbetter,et al.  Deletions of chromosome 15 as a cause of the Prader-Willi syndrome. , 1981, The New England journal of medicine.

[41]  E. Glasgow,et al.  Expression of isotocin-neurophysin mRNA in developing zebrafish. , 2003, Gene expression patterns : GEP.

[42]  Jane Worthington,et al.  Leri's pleonosteosis, a congenital rheumatic disease, results from microduplication at 8q22.1 encompassing GDF6 and SDC2 and provides insight into systemic sclerosis pathogenesis. , 2015, Annals of the rheumatic diseases.

[43]  K. Jishage,et al.  The POU domain transcription factor Brn-2 is required for the determination of specific neuronal lineages in the hypothalamus of the mouse. , 1995, Genes & development.

[44]  J. Friedman,et al.  Obesity in the new millennium , 2000, Nature.