Oriented Cell Division in the . Embryo Is Coordinated by G-Protein Signaling Dependent on the Adhesion GPCR LAT-1

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During embryogenesis an entire organism develops from a single cell. This process is vital for the formation of life, thus cell division occurs with a very distinct orientation and pattern that is tightly controlled by several signaling pathways. The mechanisms underlying these pathways are complex and not yet fully understood. In the roundworm Caenorhabditis elegans, a common genetic model, the patterns and orientations in which cells divide in the embryo have been well characterized offering an ideal model to study the molecular mechanisms involved. Here, we show that the signal mediated by the adhesion G protein-coupled receptor LAT-1 is based on cAMP. This second messenger is essential for the orientation of distinct cell division planes in the early embryo. Studies based on a lat-1 knockout mutant reveal that LAT-1 signaling affects the levels of the second messenger cAMP in the cells via a specific G protein. Thereby the receptor is activated by an intrinsic sequence. This pathway is the first one clearly shown to involve a G protein-coupled receptor-dependent G-protein signal in orientation of embryonic cell division, offering a novel level of regulation of this process among other described pathways.

Vyšlo v časopise: Oriented Cell Division in the . Embryo Is Coordinated by G-Protein Signaling Dependent on the Adhesion GPCR LAT-1. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005624
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005624

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Zdroje

1. Gillies TE, Cabernard C (2011) Cell division orientation in animals. Curr Biol 21: R599–609. doi: 10.1016/j.cub.2011.06.055 21820628

2. Lu MS, Johnston CA (2013) Molecular pathways regulating mitotic spindle orientation in animal cells. Development 140: 1843–1856. doi: 10.1242/dev.087627 23571210

3. Segalen M, Bellaiche Y (2009) Cell division orientation and planar cell polarity pathways. Semin Cell Dev Biol 20: 972–977. doi: 10.1016/j.semcdb.2009.03.018 19447051

4. Gonczy P, Rose LS (2005) Asymmetric cell division and axis formation in the embryo. WormBook. 2007/12/01 ed. pp. 1–20.

5. Kemphues K (2000) PARsing embryonic polarity. Cell 101: 345–348. 10830161

6. Pellettieri J, Seydoux G (2002) Anterior-posterior polarity in C. elegans and Drosophila—PARallels and differences. Science 298: 1946–1950. 12471246

7. Tsou MF, Ku W, Hayashi A, Rose LS (2003) PAR-dependent and geometry-dependent mechanisms of spindle positioning. J Cell Biol 160: 845–855. 12642612

8. Sulston JE, Schierenberg E, White JG, Thomson JN (1983) The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100: 64–119. 6684600

9. Rocheleau CE, Downs WD, Lin R, Wittmann C, Bei Y, et al. (1997) Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 90: 707–716. 9288750

10. Thorpe CJ, Schlesinger A, Carter JC, Bowerman B (1997) Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm. Cell 90: 695–705. 9288749

11. Walston T, Tuskey C, Edgar L, Hawkins N, Ellis G, et al. (2004) Multiple Wnt signaling pathways converge to orient the mitotic spindle in early C. elegans embryos. Dev Cell 7: 831–841. 15572126

12. Hutter H, Schnabel R (1994) glp-1 and inductions establishing embryonic axes in C. elegans. Development 120: 2051–2064. 7925009

13. Priess JR (2005) Notch signaling in the C. elegans embryo. WormBook. 2007/12/01 ed. pp. 1–16.

14. Langenhan T, Prömel S, Mestek L, Esmaeili B, Waller-Evans H, et al. (2009) Latrophilin signaling links anterior-posterior tissue polarity and oriented cell divisions in the C. elegans embryo. Dev Cell 17: 494–504. doi: 10.1016/j.devcel.2009.08.008 19853563

15. Krasnoperov VG, Bittner MA, Beavis R, Kuang Y, Salnikow KV, et al. (1997) alpha-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18: 925–937. 9208860

16. Sudhof TC (2001) alpha-Latrotoxin and its receptors: neurexins and CIRL/latrophilins. Annu Rev Neurosci 24: 933–962. 11520923

17. Willson J, Amliwala K, Davis A, Cook A, Cuttle MF, et al. (2004) Latrotoxin receptor signaling engages the UNC-13-dependent vesicle-priming pathway in C. elegans. Curr Biol 14: 1374–1379. 15296755

18. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, et al. (2003) Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr Biol 13: 1129–1133. 12842012

19. Strutt H, Strutt D (2008) Differential stability of flamingo protein complexes underlies the establishment of planar polarity. Curr Biol 18: 1555–1564. doi: 10.1016/j.cub.2008.08.063 18804371

20. Monk KR, Oshima K, Jors S, Heller S, Talbot WS (2011) Gpr126 is essential for peripheral nerve development and myelination in mammals. Development 138: 2673–2680. doi: 10.1242/dev.062224 21613327

21. Shima Y, Kengaku M, Hirano T, Takeichi M, Uemura T (2004) Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev Cell 7: 205–216. 15296717

22. Piao X, Hill RS, Bodell A, Chang BS, Basel-Vanagaite L, et al. (2004) G protein-coupled receptor-dependent development of human frontal cortex. Science 303: 2033–2036. 15044805

23. Langenhan T, Aust G, Hamann J (2013) Sticky signaling—adhesion class G protein-coupled receptors take the stage. Sci Signal 6: re3. doi: 10.1126/scisignal.2003825 23695165

24. Liebscher I, Schöneberg T, Prömel S (2013) Progress in demystification of adhesion G protein-coupled receptors. Biol Chem 394: 937–950. doi: 10.1515/hsz-2013-0109 23518449

25. Prömel S, Frickenhaus M, Hughes S, Mestek L, Staunton D, et al. (2012) The GPS motif is a molecular switch for bimodal activities of adhesion class G protein-coupled receptors. Cell Rep 2: 321–331. doi: 10.1016/j.celrep.2012.06.015 22938866

26. Prömel S, Langenhan T, Arac D (2013) Matching structure with function: the GAIN domain of adhesion-GPCR and PKD1-like proteins. Trends Pharmacol Sci 34: 470–478. doi: 10.1016/j.tips.2013.06.002 23850273

27. Arac D, Boucard AA, Bolliger MF, Nguyen J, Soltis SM, et al. (2012) A novel evolutionarily conserved domain of cell-adhesion GPCRs mediates autoproteolysis. Embo J 31: 1364–1378. doi: 10.1038/emboj.2012.26 22333914

28. de Mendoza A, Sebe-Pedros A, Ruiz-Trillo I (2014) The evolution of the GPCR signaling system in eukaryotes: modularity, conservation, and the transition to metazoan multicellularity. Genome Biol Evol 6: 606–619. doi: 10.1093/gbe/evu038 24567306

29. Lefkowitz RJ, Cotecchia S, Samama P, Costa T (1993) Constitutive activity of receptors coupled to guanine nucleotide regulatory proteins. Trends Pharmacol Sci 14: 303–307. 8249148

30. Eggerickx D, Denef JF, Labbe O, Hayashi Y, Refetoff S, et al. (1995) Molecular cloning of an orphan G-protein-coupled receptor that constitutively activates adenylate cyclase. Biochem J 309 (Pt 3): 837–843.

31. Bohnekamp J, Schöneberg T (2011) Cell adhesion receptor GPR133 couples to Gs protein. J Biol Chem 286: 41912–41916. doi: 10.1074/jbc.C111.265934 22025619

32. Conklin BR, Farfel Z, Lustig KD, Julius D, Bourne HR (1993) Substitution of three amino acids switches receptor specificity of Gq alpha to that of Gi alpha. Nature 363: 274–276. 8387644

33. Park JH, Ohshima S, Tani T, Ohshima Y (1997) Structure and expression of the gsa-1 gene encoding a G protein alpha(s) subunit in C. elegans. Gene 194: 183–190. 9272860

34. Korswagen HC, Park JH, Ohshima Y, Plasterk RH (1997) An activating mutation in a Caenorhabditis elegans Gs protein induces neural degeneration. Genes Dev 11: 1493–1503. 9203577

35. Liebscher I, Schon J, Petersen SC, Fischer L, Auerbach N, et al. (2014) A Tethered Agonist within the Ectodomain Activates the Adhesion G Protein-Coupled Receptors GPR126 and GPR133. Cell Rep 9: 2018–2026. doi: 10.1016/j.celrep.2014.11.036 25533341

36. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191. doi: 10.1093/bioinformatics/btp033 19151095

37. Herman MA, Wu M (2004) Noncanonical Wnt signaling pathways in C. elegans converge on POP-1/TCF and control cell polarity. Front Biosci 9: 1530–1539. 14977564

38. Ruvkun G, Hobert O (1998) The taxonomy of developmental control in Caenorhabditis elegans. Science 282: 2033–2041. 9851920

39. Sawa H, Lobel L, Horvitz HR (1996) The Caenorhabditis elegans gene lin-17, which is required for certain asymmetric cell divisions, encodes a putative seven-transmembrane protein similar to the Drosophila frizzled protein. Genes Dev 10: 2189–2197. 8804313

40. Bergmann DC, Lee M, Robertson B, Tsou MF, Rose LS, et al. (2003) Embryonic handedness choice in C. elegans involves the Galpha protein GPA-16. Development 130: 5731–5740. 14534142

41. Gotta M, Ahringer J (2001) Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat Cell Biol 3: 297–300. 11231580

42. Tsou MF, Hayashi A, Rose LS (2003) LET-99 opposes Galpha/GPR signaling to generate asymmetry for spindle positioning in response to PAR and MES-1/SRC-1 signaling. Development 130: 5717–5730. 14534135

43. Afshar K, Willard FS, Colombo K, Johnston CA, McCudden CR, et al. (2004) RIC-8 is required for GPR-1/2-dependent Galpha function during asymmetric division of C. elegans embryos. Cell 119: 219–230. 15479639

44. Fievet BT, Rodriguez J, Naganathan S, Lee C, Zeiser E, et al. (2013) Systematic genetic interaction screens uncover cell polarity regulators and functional redundancy. Nat Cell Biol 15: 103–112. doi: 10.1038/ncb2639 23242217

45. Cabello J, Neukomm LJ, Gunesdogan U, Burkart K, Charette SJ, et al. (2010) The Wnt pathway controls cell death engulfment, spindle orientation, and migration through CED-10/Rac. PLoS Biol 8: e1000297. doi: 10.1371/journal.pbio.1000297 20126385

46. Lelianova VG, Davletov BA, Sterling A, Rahman MA, Grishin EV, et al. (1997) Alpha-latrotoxin receptor, latrophilin, is a novel member of the secretin family of G protein-coupled receptors. J Biol Chem 272: 21504–21508. 9261169

47. Zallen JA (2007) Planar polarity and tissue morphogenesis. Cell 129: 1051–1063. 17574020

48. Barnes AP, Solecki D, Polleux F (2008) New insights into the molecular mechanisms specifying neuronal polarity in vivo. Curr Opin Neurobiol 18: 44–52. doi: 10.1016/j.conb.2008.05.003 18514505

49. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM (2007) LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 129: 565–577. 17482549

50. Brenner S (1974) The genetics of Caenorhabditis elegans. Genetics 77: 71–94. 4366476

51. Schöneberg T, Schulz A, Biebermann H, Gruters A, Grimm T, et al. (1998) V2 vasopressin receptor dysfunction in nephrogenic diabetes insipidus caused by different molecular mechanisms. Hum Mutat 12: 196–205. 9711877

52. Timmons L, Fire A (1998) Specific interference by ingested dsRNA. Nature 395: 854. 9804418

53. Kamath RS, Martinez-Campos M, Zipperlen P, Fraser AG, Ahringer J (2001) Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol 2: RESEARCH0002.

54. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685. 5432063

55. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675. 22930834

56. Bischoff M, Schnabel R (2006) A posterior centre establishes and maintains polarity of the Caenorhabditis elegans embryo by a Wnt-dependent relay mechanism. PLoS Biol 4: e396. 17121454