A role for TENM1 mutations in congenital general anosmia

Clinical Genetics

Volumn 90, Issue 3, 2016, Pages 211-219

  Alkelai, A ^a   Olender, T ^a   Haffner Krausz, R ^a   Tsoory, M M ^a   Boyko, V ^a   Tatarskyy, P ^a   Gross Isseroff, R ^a   Milgrom, R ^a   Shushan, S ^a,b   Blau, I ^c   Cohn, E ^a   Beeri, R ^d   Levy Lahad, E ^c   Pras, E ^e,f   Lancet, D ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b WOLFSON MEDICAL CENTER   (Israel)

^c MEIR MEDICAL CENTER   (Israel)

^d SHAARE ZEDEK MEDICAL CENTER   (Israel)

^e GERTNER INSTITUTE FOR EPIDEMIOLOGY AND HEALTH POLICY RESEARCH   (Israel)

^f TEL AVIV UNIVERSITY   (Israel)

Author keywords

CGA; congenital general anosmia; CRISPR Cas9 system; ODZ1; olfaction; Teneurin; TENM1

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOSMIA; ANXIETY; ARTICLE; CONGENITAL GENERAL ANOSMIA; CONTROLLED STUDY; CRISPR CAS SYSTEM; FEMALE; GENE; GENE EXPRESSION; HUMAN; LOCOMOTION; MALE; MISSENSE MUTATION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SMELLING; TENM1 GENE; WHOLE EXOME SEQUENCING; X CHROMOSOMAL INHERITANCE;

EID: 84983432443     PISSN: 00099163     EISSN: 13990004     Source Type: Journal    
DOI: 10.1111/cge.12782     Document Type: Article

References (60)

1. Landis BN, Konnerth CG, Hummel T. A study on the frequency of olfactory dysfunction. Laryngoscope 2004: 114: 1764–1769.
2. Karstensen HG, Tommerup N. Isolated and syndromic forms of congenital anosmia. Clin Genet 2012: 81: 210–215.
3. Temmel AF, Quint C, Schickinger-Fischer B et al. Characteristics of olfactory disorders in relation to major causes of olfactory loss. Arch Otolaryngol Head Neck Surg 2002: 128: 635–641.
4. Ciofalo A, Filiaci F, Romeo R et al. Epidemiological aspects of olfactory dysfunction. Rhinology 2006: 44: 78–82.
5. Croy I, Negoias S, Novakova L et al. Learning about the functions of the olfactory system from people without a sense of smell. PLoS One 2012: 7: e33365.
6. Legouis R, Cohen-Salmon M, Del Castillo I et al. Isolation and characterization of the gene responsible for the X chromosome-linked Kallmann syndrome. Biomed Pharmacother 1994: 48: 241–246.
7. Goldberg YP, MacFarlane J, MacDonald ML et al. Loss-of-function mutations in the Nav1.7 gene underlie congenital indifference to pain in multiple human populations. Clin Genet 2007: 71: 311–319.
8. Nilsen KB, Nicholas AK, Woods CG et al. Two novel SCN9A mutations causing insensitivity to pain. Pain 2009: 143: 155–158.
9. Jongmans MC, van Ravenswaaij-Arts CM, Pitteloud N et al. CHD7 mutations in patients initially diagnosed with Kallmann syndrome – the clinical overlap with CHARGE syndrome. Clin Genet 2009: 75: 65–71.
10. Vuorela PE, Penttinen MT, Hietala MH et al. A familial CHARGE syndrome with a CHD7 nonsense mutation and new clinical features. Clin Dysmorphol 2008: 17: 249–253.
11. Qu Q, Liu J, Ni D et al. Diagnosis and clinical characteristics of congenital anosmia: case series report. J Otolaryngol Head Neck Surg 2010: 39: 723–731.
12. Karstensen HG, Mang Y, Fark T et al. The first mutation in CNGA2 in two brothers with anosmia. Clin Genet 2015: 88: 293–296.
13. Feldmesser E, Bercovich D, Avidan N et al. Mutations in olfactory signal transduction genes are not a major cause of human congenital general anosmia. Chem Senses 2007: 32: 21–30.
14. Singh N, Grewal MS, Austin JH. Familial anosmia. Arch Neurol 1970: 22: 40–44.
15. Hardelin JP, Dode C. The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2, et al. Sex Dev 2008: 2: 181–193.
16. Dode C, Hardelin JP. Clinical genetics of Kallmann syndrome. Ann Endocrinol (Paris) 2010: 71: 149–157.
17. Franco B, Guioli S, Pragliola A et al. A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 1991: 353: 529–536.
18. Dode C, Levilliers J, Dupont JM et al. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 2003: 33: 463–465.
19. Falardeau J, Chung WC, Beenken A et al. Decreased FGF8 signaling causes deficiency of gonadotropin-releasing hormone in humans and mice. J Clin Invest 2008: 118: 2822–2831.
20. Miraoui H, Dwyer AA, Sykiotis GP et al. Mutations in FGF17, IL17RD, DUSP6, SPRY4, and FLRT3 are identified in individuals with congenital hypogonadotropic hypogonadism. Am J Hum Genet 2013: 92: 725–743.
21. Dode C, Teixeira L, Levilliers J et al. Kallmann syndrome: mutations in the genes encoding prokineticin-2 and prokineticin receptor-2. PLoS Genet 2006: 2: e175.
22. Kim HG, Kurth I, Lan F et al. Mutations in CHD7, encoding a chromatin-remodeling protein, cause idiopathic hypogonadotropic hypogonadism and Kallmann syndrome. Am J Hum Genet 2008: 83: 511–519.
23. Moya-Plana A, Villanueva C, Laccourreye O et al. PROKR2 and PROK2 mutations cause isolated congenital anosmia without gonadotropic deficiency. Eur J Endocrinol 2013: 168: 31–37.
24. Doty RL, Shaman P, Dann M. Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function. Physiol Behav 1984: 32: 489–502.
25. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009: 25: 1754–1760.
26. Li H, Handsaker B, Wysoker A et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009: 25: 2078–2079.
27. McKenna A, Hanna M, Banks E et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010: 20: 1297–1303.
28. Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 2010: 38: e164.
29. Stelzer G, Plaschkes I, Oz-Levi D et al. VarElect: the phenotype-based variation prioritizer of the GeneCards Suite. BMC Genomics 2016 in press.
30. Purcell S, Neale B, Todd-Brown K et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 2007: 81: 559–575.
31. Manichaikul A, Mychaleckyj JC, Rich SS et al. Robust relationship inference in genome-wide association studies. Bioinformatics 2010: 26: 2867–2873.
32. Wang H, Yang H, Shivalila CS et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 2013: 153: 910–918.
33. Dierssen M, Fotaki V, Martinez de Lagran M et al. Neurobehavioral development of two mouse lines commonly used in transgenic studies. Pharmacol Biochem Behav 2002: 73: 19–25.
34. Magen I, Ostritsky R, Richter F et al. Intranasal NAP (davunetide) decreases tau hyperphosphorylation and moderately improves behavioral deficits in mice overexpressing alpha-synuclein. Pharmacol Res Perspect 2014: 2: e00065.
35. Witt RM, Galligan MM, Despinoy JR et al. Olfactory behavioral testing in the adult mouse. J Vis Exp 2009: 23: 949.
36. Neufeld-Cohen A, Tsoory MM, Evans AK et al. A triple urocortin knockout mouse model reveals an essential role for urocortins in stress recovery. Proc Natl Acad Sci U S A 2010: 107: 19020–19025.
37. Cooper A, Grigoryan G, Guy-David L et al. Trisomy of the G protein-coupled K+ channel gene, Kcnj6, affects reward mechanisms, cognitive functions, and synaptic plasticity in mice. Proc Natl Acad Sci U S A 2012: 109: 2642–2647.
38. Matsumoto S, Yamazaki C, Masumoto KH et al. Abnormal development of the olfactory bulb and reproductive system in mice lacking prokineticin receptor PKR2. Proc Natl Acad Sci U S A 2006: 103: 4140–4145.
39. Bergman JE, Bosman EA, van Ravenswaaij-Arts CM et al. Study of smell and reproductive organs in a mouse model for CHARGE syndrome. Eur J Hum Genet 2010: 18: 171–177.
40. Liu X, Jian X, Boerwinkle E. dbNSFP v2.0: a database of human non-synonymous SNVs and their functional predictions and annotations. Hum Mutat 2013: 34: E2393–E2402.
41. Minet AD, Rubin BP, Tucker RP et al. Teneurin-1, a vertebrate homologue of the Drosophila pair-rule gene ten-m, is a neuronal protein with a novel type of heparin-binding domain. J Cell Sci 1999: 112 (Pt 12): 2019–2032.
42. Rubin BP, Tucker RP, Martin D et al. Teneurins: a novel family of neuronal cell surface proteins in vertebrates, homologous to the Drosophila pair-rule gene product Ten-m. Dev Biol 1999: 216: 195–209.
43. Hong W, Mosca TJ, Luo L. Teneurins instruct synaptic partner matching in an olfactory map. Nature 2012: 484: 201–207.
44. Mosca TJ, Hong W, Dani VS et al. Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature 2012: 484: 237–241.
45. Carithers LJ, Moore HM. The Genotype-Tissue Expression (GTEx) Project. Biopreserv Biobank 2015: 13: 307–308.
46. Dobyns WB, Filauro A, Tomson BN et al. Inheritance of most X-linked traits is not dominant or recessive, just X-linked. Am J Med Genet A 2004: 129A: 136–143.
47. Baumgartner S, Martin D, Hagios C et al. Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene. EMBO J 1994: 13: 3728–3740.
48. Levine A, Bashan-Ahrend A, Budai-Hadrian O et al. Odd Oz: a novel Drosophila pair rule gene. Cell 1994: 77: 587–598.
49. Zheng L, Michelson Y, Freger V et al. Drosophila Ten-m and filamin affect motor neuron growth cone guidance. PLoS One 2011: 6: e22956.
50. Mosca TJ, Luo L. Synaptic organization of the Drosophila antennal lobe and its regulation by the Teneurins. Elife 2014: 3: e03726.
51. Drabikowski K, Trzebiatowska A, Chiquet-Ehrismann R. ten-1, an essential gene for germ cell development, epidermal morphogenesis, gonad migration, and neuronal pathfinding in Caenorhabditis elegans. Dev Biol 2005: 282: 27–38.
52. Kenzelmann D, Chiquet-Ehrismann R, Leachman NT et al. Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo. BMC Dev Biol 2008: 8: 30.
53. Zhou XH, Brandau O, Feng K et al. The murine Ten-m/Odz genes show distinct but overlapping expression patterns during development and in adult brain. Gene Expr Patterns 2003: 3: 397–405.
54. Pankevich DE, Baum MJ, Cherry JA. Olfactory sex discrimination persists, whereas the preference for urinary odorants from estrous females disappears in male mice after vomeronasal organ removal. J Neurosci 2004: 24: 9451–9457.
55. Bakker ST, de Winter JP, te Riele H. Learning from a paradox: recent insights into Fanconi anaemia through studying mouse models. Dis Model Mech 2013: 6: 40–47.
56. Muller U. Ten years of gene targeting: targeted mouse mutants, from vector design to phenotype analysis. Mech Dev 1999: 82: 3–21.
57. Phaneuf D, Wakamatsu N, Huang JQ et al. Dramatically different phenotypes in mouse models of human Tay-Sachs and Sandhoff diseases. Hum Mol Genet 1996: 5: 1–14.
58. Montagutelli X. Effect of the genetic background on the phenotype of mouse mutations. J Am Soc Nephrol 2000: 11 (Suppl. 16): S101–S105.
59. Barbaric I, Miller G, Dear TN. Appearances can be deceiving: phenotypes of knockout mice. Brief Funct Genomic Proteomic 2007: 6: 91–103.
60. Aldahmesh MA, Mohammed JY, Al-Hazzaa S et al. Homozygous null mutation in ODZ3 causes microphthalmia in humans. Genet Med 2012: 14: 900–904.