CoChat
Sign Up
Cited by 6Axon Guidance and Neuronal SignalingDevelopmental Biology and Gene RegulationNeuroscience and Neuropharmacology Research

Nomenclature and Comparative Morphology of the Teneurin/TCAP/ADGRL Protein Families

Open access
Sita, Luciane V., Diniz, Giovanne B., Horta-Junior, José A. C., Casatti, Claudio A., Bittencourt, Jackson C.·2019·Frontiers in Neuroscience
DOI 10.3389/fnins.2019.00425PMC PMC6510184
Open this paper in CoChat — free accountOpen PDF

Abstract

The teneurins are a family of glycosylated type II transmembrane proteins synthesized in several tissue from both vertebrate and invertebrate species. These proteins interact with the latrophilins, a group of adhesion G protein-coupled receptors. Both teneurins and latrophilins may have been acquired by choanoflagellates through horizontal gene transfer from a toxin-target system present in prokaryotes. Teneurins are highly conserved in eukaryotes, with four paralogs (TEN1, TEN2, TEN3, and TEN4) in most vertebrates playing a role in the normal neural development, axonal guiding, synapse formation and synaptic maintenance. In this review, we summarize the main findings concerning the distribution and morphology of the teneurins and latrophilins, both during development and in adult animals. We also briefly discuss the current knowledge in the distribution of the teneurin C-terminal associated protein (TCAP), a peptidergic sequence at the terminal portion of teneurins that may be independently processed and secreted. Through the analysis of anatomical data, we draw parallels to the evolution of those proteins and the increasing complexity of this system, which mirrors the increase in metazoan sensory complexity. This review underscores the need for further studies investigating the distribution of teneurins and latrophilins and the use of different animal models.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.3389/fnins.2019.00425

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Both ADGRL and NRXN pathways are involved in synaptic function and psychiatric disorders.

    “Both pathways are involved in synaptic function and psychiatric disorders45–47.”

    From PLCG2 downregulation impairs synaptic function and increases Alzheimer’s disease hallmarks in neuronal cultures (2026) · cites this paper as [45]

    The Introduction and Nomenclature section says that latrophilins (ADGRLs) and neurexins interact in a complex involved in synapse formation and maintenance. The paper does not establish that both pathways are involved in psychiatric disorders; its References list an ADHD-related latrophilin study, but provide no corresponding claim about neurexins. (LLM, conf=0.83)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 86 · Cited by 6

Research works printed but not linked: 82

  1. Anderson G. R. Maxeiner S. Sando R. Tsetsenis T. Malenka R. C. Südhof T. C. (2017). Postsynaptic adhesion GPCR latrophilin-2 mediates target recognition in entorhinal-hippocampal synapse assembly. J. Cell Biol. 216 3831– 3846. 10.1083/jcb.201703042 28972101 PMC5674891 · DOI
  2. Antinucci P. Nikolaou N. Meyer M. P. Hindges R. (2013). Teneurin-3 specifies morphological and functional connectivity of retinal ganglion cells in the vertebrate visual system. Cell Rep. 5 582– 592. 10.1016/j.celrep.2013.09.045 24183672 PMC3898612 · DOI
  3. Arcos-Burgos M. Jain M. Acosta M. Shively S. Stanescu H. Wallis D. (2010). A common variant of the latrophilin 3 gene, LPHN3, confers susceptibility to ADHD and predicts effectiveness of stimulant medication. Mol. Psychiatry 15: 1053. 10.1038/mp.2010.6 20157310 · DOI
  4. Baumgartner S. Chiquet-Ehrismann R. (1993). Tena, a Drosophila gene related to tenascin, shows selective transcript localization. Mech. Dev. 40 165– 176. 7684246
  5. Baumgartner S. Martin D. Hagios C. Chiquet-Ehrismann R. (1994). Tenm, a Drosophila gene related to tenascin, is a new pair-rule gene. EMBO J. 13 3728– 3740. 8070401 PMC395283
  6. Ben-Zur T. Feige E. Motro B. Wides R. (2000). The mammalian Odz gene family: homologs of a Drosophila pair-rule gene with expression implying distinct yet overlapping developmental roles. Dev. Biol. 217 107– 120. 10625539
  7. Ben-Zur T. Wides R. (1999). Mapping Homologs of Drosophila odd Oz (odz): Doc4/Odz4to mouse chromosome 7, Odz1to mouse chromosome 11; and ODZ3 to human chromosome Xq25. Genomics 1 102– 103. 10331952
  8. Berns D. S. DeNardo L. A. Pederick D. T. Luo L. (2018). Teneurin-3 controls topographic circuit assembly in the hippocampus. Nature 554: 328. 10.1038/nature25463 29414938 PMC7282895 · DOI
  9. Boucard A. A. Maxeiner S. Südhof T. C. (2014). Latrophilins function as heterophilic cell-adhesion molecules by binding to teneurins REGULATION BY ALTERNATIVE SPLICING. J. Biol. Chem. 289 387– 402. 10.1074/jbc.M113.504779 24273166 PMC3879561 · DOI
  10. Carr O. P. Glendining K. A. Leamey C. A. Marotte L. R. (2013). Overexpression of Ten-m3 in the retina alters ipsilateral retinocollicular projections in the wallaby (Macropus eugenii). Int. J. Dev. Neurosci. 31 496– 504. 10.1016/j.ijdevneu.2013.05.011 23747822 · DOI
  11. Carr O. P. Glendining K. A. Leamey C. A. Marotte L. R. (2014). Retinal overexpression of Ten-m3 alters ipsilateral retinogeniculate projections in the wallaby (Macropus eugenii). Neurosci. Lett. 566 167– 171. 10.1016/j.neulet.2014.02.048 24602979 · DOI
  12. Chand D. Casatti C. A. de Lannoy L. Song L. Kollara A. Barsyte-Lovejoy D. (2013). C-terminal processing of the teneurin proteins: independent actions of a teneurin C-terminal associated peptide in hippocampal cells. Mol. Cell. Neurosci. 52 38– 50. 10.1016/j.mcn.2012.09.006 23026563 · DOI
  13. Chand D. Colacci M. Dixon K. Kollara A. Brown T. J. Lovejoy D. A. (2014). C-terminal region of teneurin-1 co-localizes with the dystroglycan complex in adult mouse testes and regulates testicular size and testosterone production. Histochem. Cell Biol. 141 191– 211. 10.1007/s00418-013-1154-1 24154551 · DOI
  14. Chen Y. Xu M. De Almeida R. Lovejoy D. A. (2013). Teneurin C-terminal associated peptides (TCAP): modulators of corticotropin-releasing factor (CRF) physiology and behavior. Front. Neurosci. 7: 166. 10.3389/fnins.2013.00166 24062636 PMC3775549 · DOI
  15. Colacci M. De Almeida R. Chand D. Lovejoy S. R. Sephton D. Vercaemer B. (2015). Characterization of the teneurin C-terminal associated peptide (TCAP) in the vase tunicate, Ciona intestinalis: a novel peptide system associated with energy metabolism and reproduction. Gen. Comp. Endocrinol. 216 161– 170. 10.1016/j.ygcen.2015.01.021 25687741 · DOI
  16. D’Aquila A. L. Hsieh A. H.-R. Hsieh A. H.-M. Almeida R. Lovejoy S. R. Lovejoy D. A. (2017). Expression and actions of corticotropin-releasing factor/diuretic hormone-like peptide (CDLP) and teneurin C-terminal associated peptide (TCAP) in the vase tunicate, Ciona intestinalis: antagonism of the feeding response. Gen. Comp. Endocrinol. 246 105– 115. 10.1016/j.ygcen.2016.06.015 27292788 · DOI
  17. Davletov B. A. Shamotienko O. G. Lelianova V. G. Grishin E. V. Ushkaryov Y. A. (1996). Isolation and biochemical characterization of a Ca2+-independent α-latrotoxin-binding protein. J. Biol. Chem. 271 23239– 23245. 8798521
  18. Dehal P. Boore J. L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3: e314. 10.1371/journal.pbio.0030314 16128622 PMC1197285 · DOI · Paper page
  19. Dharmaratne N. Glendining K. A. Young T. R. Tran H. Sawatari A. Leamey C. A. (2012). Ten-m3 is required for the development of topography in the ipsilateral retinocollicular pathway. PLoS One 7: e43083. 10.1371/journal.pone.0043083 23028443 PMC3446960 · DOI
  20. Doyle S. E. Scholz M. J. Greer K. A. Hubbard A. D. Darnell D. K. Antin P. B. (2006). Latrophilin-2 is a novel component of the epithelial-mesenchymal transition within the atrioventricular canal of the embryonic chicken heart. Dev. Dyn. 235 3213– 3221. 17016846
  21. Drabikowski K. Trzebiatowska A. Chiquet-Ehrismann R. (2005). ten-1, an essential gene for germ cell development, epidermal morphogenesis, gonad migration, and neuronal pathfinding in Caenorhabditis elegans. Dev. Biol. 282 27– 38. 15936327
  22. Fascetti N. Baumgartner S. (2002). Expression of Drosophila Ten-a, a dimeric receptor during embryonic development. Mech. Dev. 114 197– 200. 12175511
  23. Graumann R. Di Capua G. A. Oyarzún J. E. Vásquez M. A. Liao C. Brañes J. A. (2017). Expression of teneurins is associated with tumor differentiation and patient survival in ovarian cancer. PLoS One 12: e0177244. 10.1371/journal.pone.0177244 28472127 PMC5417686 · DOI
  24. Hamann J. Aust G. Araç D. Engel F. B. Formstone C. Fredriksson R. (2015). International union of basic and clinical pharmacology. XCIV. adhesion G protein–coupled receptors. Pharmacol. Rev. 67 338– 367. 10.1124/pr.114.009647 25713288 PMC4394687 · DOI
  25. Hong W. Mosca T. J. Luo L. (2012). Teneurins instruct synaptic partner matching in an olfactory map. Nature 484: 201. 10.1038/nature10926 22425994 PMC3345284 · DOI
  26. Husić M. Barsyte-Lovejoy D. Lovejoy D. A. (2019). Teneurin C-terminal associated peptide (TCAP)-1 and latrophilin interaction in HEK293 cells: evidence for modulation of intercellular adhesion. Front. Endocrinol. 10: 22. 10.3389/fendo.2019.00022 30774623 PMC6367273 · DOI
  27. Ichtchenko K. Bittner M. A. Krasnoperov V. Little A. R. Chepurny O. Holz R. W. (1999). A novel ubiquitously expressed α-latrotoxin receptor is a member of the CIRL family of G-protein-coupled receptors. J. Biol. Chem. 274 5491– 5498. 10026162
  28. Ichtchenko K. Khvotchev M. Kiyatkin N. Simpson L. Sugita S. Sudhof T. C. (1998). alpha-latrotoxin action probed with recombinant toxin: receptors recruit alpha-latrotoxin but do not transduce an exocytotic signal. EMBO J. 17 6188– 6199. 10.1093/emboj/17.21.6188 9799228 PMC1170945 · DOI
  29. Jackson V. A. del Toro D. Carrasquero M. Roversi P. Harlos K. Klein R. (2015). Structural basis of latrophilin-FLRT interaction. Structure 23 774– 781. 10.1016/j.str.2015.01.013 25728924 PMC4396693 · DOI
  30. Kenzelmann D. Chiquet-Ehrismann R. Leachman N. T. Tucker R. P. (2008). Teneurin-1 is expressed in interconnected regions of the developing brain and is processed in vivo. BMC Dev. Biol. 8: 30. 10.1186/1471-213X-8-30 18366734 PMC2289808 · DOI
  31. Krasnoperov V. G. Beavis R. Chepurny O. G. Little A. R. Plotnikov A. N. Petrenko A. G. (1996). The calcium-independent receptor of α-latrotoxin is not a neurexin. Biochem. Biophys. Res. Commun. 227 868– 875. 8886023
  32. Krasnoperov V. G. Bittner M. A. Beavis R. Kuang Y. Salnikow K. V. Chepurny O. G. (1997). α-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18 925– 937. 9208860
  33. Langenhan T. Prömel S. Mestek L. Esmaeili B. Waller-Evans H. Hennig C. (2009). Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo. Dev. Cell 17 494– 504. 10.1016/j.devcel.2009.08.008 19853563 PMC2819344 · DOI
  34. Leamey C. A. Glendining K. A. Kreiman G. Kang N.-D. Wang K. H. Fassler R. (2007a). Differential gene expression between sensory neocortical areas: potential roles for Ten_m3 and Bcl6 in patterning visual and somatosensory pathways. Cereb. Cortex 18 53– 66. 17478416
  35. Leamey C. A. Merlin S. Lattouf P. Sawatari A. Zhou X. Demel N. (2007b). Ten_m3 regulates eye-specific patterning in the mammalian visual pathway and is required for binocular vision. PLoS Biol. 5: e241. 17803360 PMC1964777
  36. Lelianova V. G. Davletov B. A. Sterling A. Rahman M. A. Grishin E. V. Totty N. F. (1997). α-Latrotoxin receptor, latrophilin, is a novel member of the secretin family of G protein-coupled receptors. J. Biol. Chem. 272 21504– 21508. 9261169
  37. Levine A. Bashan-Ahrend A. Budai-Hadrian O. Gartenberg D. Menasherow S. Wides R. (1994). Odd Oz: a novel Drosophila pair rule gene. Cell 77 587– 598. 7514504
  38. Levine A. Weiss C. Wides R. (1997). Expression of the pair-rule gene odd Oz (odz) in imaginal tissues. Dev. Dyn. 209 1– 14. 9142491
  39. Li H. Bishop K. M. O’leary D. D. (2006). Potential target genes of EMX2 include Odz/Ten-M and other gene families with implications for cortical patterning. Mol. Cell. Neurosci. 33 136– 149. 16919471
  40. Li J. Shalev-Benami M. Sando R. Jiang X. Kibrom A. Wang J. (2018). Structural basis for teneurin function in circuit-wiring: a toxin motif at the synapse. Cell 173 735. e15– 748.e15. 10.1016/j.cell.2018.03.036 29677516 PMC5912346 · DOI
  41. Lossie A. C. Nakamura H. Thomas S. E. Justice M. J. (2005). Mutation of l7Rn3 shows that Odz4 is required for mouse gastrulation. Genetics 169 285– 299. 15489520 PMC1448887
  42. Lovejoy D. A. Al Chawaf A. Cadinouche M. A. (2006). Teneurin C-terminal associated peptides: an enigmatic family of neuropeptides with structural similarity to the corticotropin-releasing factor and calcitonin families of peptides. Gen. Comp. Endocrinol. 148 299– 305. 16524574
  43. Lu Y. C. Nazarko O. V. Sando R. III Salzman G. S. Li N.-S. Südhof T. C. (2015). Structural basis of latrophilin-FLRT-UNC5 interaction in cell adhesion. Structure 23 1678– 1691. 10.1016/j.str.2015.06.024 26235030 PMC4851429 · DOI
  44. Matsushita H. Lelianova V. G. Ushkaryov Y. A. (1999). The latrophilin family: multiply spliced G protein-coupled receptors with differential tissue distribution. FEBS Lett. 443 348– 352. 10025961
  45. Mee C. J. Tomlinson S. R. Perestenko P. V. Pomerai D. Duce I. R. Usherwood P. N. R. (2004). Latrophilin is required for toxicity of black widow spider venom in Caenorhabditis elegans. Biochem. J. 378 185– 191. 14594448 PMC1223931
  46. Meyer A. Van de Peer Y. (2005). From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27 937– 945. 10.1002/bies.20293 16108068 · DOI
  47. Mieda M. Kikuchi Y. Hirate Y. Aoki M. Okamoto H. (1999). Compartmentalized expression of zebrafish ten-m3 and ten-m4, homologues of the Drosophila tenm/odd Oz gene, in the central nervous system. Mech. Dev. 87 223– 227. 10495292
  48. Minet A. D. Chiquet-Ehrismann R. (2000). Phylogenetic analysis of teneurin genes and comparison to the rearrangement hot spot elements of E. coli. Gene 257 87– 97. 11054571
  49. Minet A. D. Rubin B. P. Tucker R. P. Baumgartner S. Chiquet-Ehrismann R. (1999). 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. 112(Pt 12), 2019– 2032. 10341219
  50. Mörck C. Vivekanand V. Jafari G. Pilon M. (2010). C. elegans ten-1 is synthetic lethal with mutations in cytoskeleton regulators, and enhances many axon guidance defective mutants. BMC Dev. Biol. 10: 55. 10.1186/1471-213X-10-55 20497576 PMC2887410 · DOI
  51. Ohno S. (2013). Evolution By Gene Duplication. Berlin: Springer Science & Business Media.
  52. Oohashi T. Zhou X.-H. Feng K. Richter B. Mörgelin M. Perez M. T. (1999). Mouse ten-m/Odz is a new family of dimeric type II transmembrane proteins expressed in many tissues. J. Cell Biol. 145 563– 577. 10225957 PMC2185078
  53. Otaki J. M. Firestein S. (1999). Neurestin: putative transmembrane molecule implicated in neuronal development. Dev. Biol. 212 165– 181. 10419693
  54. Qian X. Barsyte-Lovejoy D. Wang L. Chewpoy B. Gautam N. Al Chawaf A. (2004). Cloning and characterization of teneurin C-terminus associated peptide (TCAP)-3 from the hypothalamus of an adult rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 137 205– 216. 15158132
  55. Rubin B. P. Tucker R. P. Brown-Luedi M. Martin D. Chiquet-Ehrismann R. (2002). Teneurin 2 is expressed by the neurons of the thalamofugal visual system in situ and promotes homophilic cell-cell adhesion in vitro. Development 129 4697– 4705. 12361962
  56. Rubin B. P. Tucker R. P. Martin D. Chiquet-Ehrismann R. (1999). Teneurins: a novel family of neuronal cell surface proteins in vertebrates, homologous to the Drosophila pair-rule gene product Ten-m. Dev. Biol. 216 195– 209. 10.1006/dbio.1999.9503 10588872 · DOI
  57. Sacerdot C. Louis A. Bon C. Berthelot C. Crollius H. R. (2018). Chromosome evolution at the origin of the ancestral vertebrate genome. Genome Biol. 19: 166. 10.1186/s13059-018-1559-1 30333059 PMC6193309 · DOI · Paper page
  58. Scholz N. Gehring J. Guan C. Ljaschenko D. Fischer R. Lakshmanan V. (2015). The adhesion GPCR latrophilin/CIRL shapes mechanosensation. Cell Rep. 11 866– 874. 10.1016/j.celrep.2015.04.008 25937282 · DOI
  59. Silva J.-P. Lelianova V. G. Ermolyuk Y. S. Vysokov N. Hitchen P. G. Berninghausen O. (2011). Latrophilin 1 and its endogenous ligand Lasso/teneurin-2 form a high-affinity transsynaptic receptor pair with signaling capabilities. Proc. Natl. Acad. Sci. U.S.A. 108 12113– 12118. 10.1073/pnas.1019434108 21724987 PMC3141932 · DOI
  60. Sugita S. Ichtchenko K. Khvotchev M. Südhof T. C. (1998). α-Latrotoxin receptor CIRL/latrophilin 1 (CL1) defines an unusual family of ubiquitous G-protein-linked receptors G-PROTEIN COUPLING NOT REQUIRED FOR TRIGGERING EXOCYTOSIS. J. Biol. Chem. 273 32715– 32724. 9830014
  61. Tews D. Fromme T. Keuper M. Hofmann S. Debatin K.-M. Klingenspor M. (2017). Teneurin-2 (TENM2) deficiency induces UCP1 expression in differentiating human fat cells. Mol. Cell. Endocrinol. 443 106– 113. 10.1016/j.mce.2017.01.015 28088466 · DOI
  62. Tews D. Schwar V. Scheithauer M. Weber T. Fromme T. Klingenspor M. (2014). Comparative gene array analysis of progenitor cells from human paired deep neck and subcutaneous adipose tissue. Mol. Cell. Endocrinol. 395 41– 50. 10.1016/j.mce.2014.07.011 25102227 · DOI
  63. Torres-da-Silva K. Tessarin G. Dias C. Guiati I. Ervolino E. Gonçalves A. (2017). Teneurin-2 presence in rat and human odontoblasts. PLoS One 12: e0184794. 10.1371/journal.pone.0184794 28926618 PMC5604987 · DOI
  64. Tran H. Sawatari A. Leamey C. A. (2015). The glycoprotein Ten-m3 mediates topography and patterning of thalamostriatal projections from the parafascicular nucleus in mice. Eur. J. Neurosci. 41 55– 68. 10.1111/ejn.12767 25406022 · DOI
  65. Trzebiatowska A. Topf U. Sauder U. Drabikowski K. Chiquet-Ehrismann R. (2008). Caenorhabditis elegans teneurin, ten-1, is required for gonadal and pharyngeal basement membrane integrity and acts redundantly with integrin ina-1 and dystroglycan dgn-1. Mol. Biol. Cell 19 3898– 3908. 10.1091/mbc.E08-01-0028 18632986 PMC2526705 · DOI
  66. Tucker R. P. (2013). Horizontal gene transfer in choanoflagellates. J. Exp. Zool. Part B 320 1– 9. 10.1002/jez.b.22480 22997182 · DOI
  67. Tucker R. P. Beckmann J. Leachman N. T. Schöler J. Chiquet-Ehrismann R. (2012). Phylogenetic analysis of the teneurins: conserved features and premetazoan ancestry. Mol. Biol. Evol. 29 1019– 1029. 10.1093/molbev/msr271 22045996 PMC3278476 · DOI
  68. Tucker R. P. Chiquet-Ehrismann R. (2006). Teneurins: a conserved family of transmembrane proteins involved in intercellular signaling during development. Dev. Biol. 290 237– 245. 16406038
  69. Tucker R. P. Chiquet-Ehrismann R. Chevron M. P. Martin D. Hall R. J. Rubin B. P. (2001). Teneurin-2 is expressed in tissues that regulate limb and somite pattern formation and is induced in vitro and in situ by FGF8. Dev. Dyn. 220 27– 39. 11146505
  70. Tucker R. P. Kenzelmann D. Trzebiatowska A. Chiquet-Ehrismann R. (2007). Teneurins: transmembrane proteins with fundamental roles in development. Int. J. Biochem. Cell Biol. 39 292– 297. 17095284
  71. Tucker R. P. Martin D. Kos R. Chiquet-Ehrismann R. (2000). The expression of teneurin-4 in the avian embryo. Mech. Dev. 98 187– 191. 11044628
  72. Wang L. Rotzinger S. Al Chawaf A. Elias C. F. Baršytë-Lovejoy D. Qian X. (2005). Teneurin proteins possess a carboxy terminal sequence with neuromodulatory activity. Mol. Brain Res. 133 253– 265. 10.1016/j.molbrainres.2004.10.019 15710242 · DOI
  73. Wang X. Z. Kuroda M. Sok J. Batchvarova N. Kimmel R. Chung P. (1998). Identification of novel stress-induced genes downstream of chop. EMBO J. 17 3619– 3630. 9649432 PMC1170698
  74. Willson J. Amliwala K. Davis A. Cook A. Cuttle M. F. Kriek N. (2004). Latrotoxin receptor signaling engages the UNC-13-dependent vesicle-priming pathway in C. elegans. Curr. Biol. 14 1374– 1379. 15296755
  75. Wilson R. Ainscough R. Anderson K. Baynes C. Berks M. Bonfield J. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368 32– 38. 10.1038/368032a0 7906398 · DOI
  76. Woelfle R. D’Aquila A. L. Pavloviæ T. Husiæ M. Lovejoy D. A. (2015). Ancient interaction between the teneurin C-terminal associated peptides (TCAP) and latrophilin ligand-receptor coupling: a role in behavior. Front. Neurosci. 9: 146. 10.3389/fnins.2015.00146 25964737 PMC4408839 · DOI
  77. Young T. R. Bourke M. Zhou X. Oohashi T. Sawatari A. Fässler R. (2013). Ten-m2 is required for the generation of binocular visual circuits. J. Neurosci. 33 12490– 12509. 10.1523/JNEUROSCI.4708-12.2013 23884953 PMC6618674 · DOI
  78. Young T. R. Leamey C. A. (2009). Teneurins: important regulators of neural circuitry. Int. J. Biochem. Cell Biol. 41 990– 993. 10.1016/j.biocel.2008.06.014 18723111 · DOI
  79. Zhang D. de Souza R. F. Anantharaman V. Iyer L. M. Aravind L. (2012). Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol. Dir. 7: 18. 10.1186/1745-6150-7-18 22731697 PMC3482391 · DOI
  80. Zheng L. Michelson Y. Freger V. Avraham Z. Venken K. J. Bellen H. J. (2011). Drosophila ten-m and filamin affect motor neuron growth cone guidance. PLoS One 6: e22956. 10.1371/journal.pone.0022956 21857973 PMC3152545 · DOI
  81. Zhou X.-H. Brandau O. Feng K. Oohashi T. Ninomiya Y. Rauch U. (2003). The murine Ten-m/Odz genes show distinct but overlapping expression patterns during development and in adult brain. Gene Exp. Patterns 3 397– 405. 12915301
  82. Zuko A. Oguro-Ando A. Post H. Taggenbrock R. L. Van Dijk R. E. Altelaar A. (2016). Association of cell adhesion molecules contactin-6 and latrophilin-1 regulates neuronal apoptosis. Front. Mol. Neurosci. 9: 143 10.3389/fnmol.2016.00143 PMC5156884 28018171 · DOI

Authors
Sita, L. V., Diniz, G. B., Horta-Junior, J. A. C., Casatti, C. A., & Bittencourt, J. C.
Affiliations
Universidade de São Paulo (BR)
Corresponding author
Bittencourt, Jackson C.
ORCID
Venue
Frontiers in Neuroscience
Publisher
Frontiers Media SA
Published
2019-05-03
Volume
13
Pages
425-425
ISSN
1662-453X (ISSN-L)
DOI
10.3389/fnins.2019.00425
PMC
PMC6510184
OpenAlex
W2943477013
Cited by
6
References
86
Citations by year
2026: 3 · 2024: 2 · 2023: 1
FWCI
0.00
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • UNESP Institutional Repository (São Paulo State University) (submittedVersion, other-oa)
Funders
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (2016/02224-1, 2016/02748-0)
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
teneurins, latrophilin, adhesion G protein-coupled receptors, type II membrane protein, horizontal gene transfer, choanoflagellates, paralogs, neural development, axon guidance, synaptogenesis, synapse maintenance, TCAP, sensory evolution, protein distribution

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review