The Actomyosin Machinery Is Required for Retinal Lumen Formation


Biological tubes are integral units of tissues and organs such as lung, kidney, and the cardiovascular system. The fundamental design of tubes involves a central lumen wrapped by a sheet of cells. To function properly, the tubes require a precise genetic control over their creation, the diametric growth and maintenance of the lumen during development. In the fruit fly, Drosophila melanogaster, the photoreceptor cells of the eye form a tubular structure. The formation of the retinal lumen is critical for separating and positioning the light sensing organelles of each photoreceptor cell to achieve visual sensitivity. In an effort to investigate the mechanisms of Drosophila retinal lumen formation, we identified a contractile machinery that was present at the apical portion of photoreceptor cells. Our data is consistent with the idea that a contractile force contributes to the initial separation of the juxtaposed apical membranes and subsequent enlargement of the luminal space. Our work suggests that building a biological tube requires not only an extrinsic pushing force provided by the growing central lumen, but also a cell intrinsic pulling force powered by contraction of cells lining the lumen. Our findings expand and demonstrate the coordination of several molecular mechanisms to generate a tube.


Vyšlo v časopise: The Actomyosin Machinery Is Required for Retinal Lumen Formation. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004608
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004608

Souhrn

Biological tubes are integral units of tissues and organs such as lung, kidney, and the cardiovascular system. The fundamental design of tubes involves a central lumen wrapped by a sheet of cells. To function properly, the tubes require a precise genetic control over their creation, the diametric growth and maintenance of the lumen during development. In the fruit fly, Drosophila melanogaster, the photoreceptor cells of the eye form a tubular structure. The formation of the retinal lumen is critical for separating and positioning the light sensing organelles of each photoreceptor cell to achieve visual sensitivity. In an effort to investigate the mechanisms of Drosophila retinal lumen formation, we identified a contractile machinery that was present at the apical portion of photoreceptor cells. Our data is consistent with the idea that a contractile force contributes to the initial separation of the juxtaposed apical membranes and subsequent enlargement of the luminal space. Our work suggests that building a biological tube requires not only an extrinsic pushing force provided by the growing central lumen, but also a cell intrinsic pulling force powered by contraction of cells lining the lumen. Our findings expand and demonstrate the coordination of several molecular mechanisms to generate a tube.


Zdroje

1. AndrewDJ, EwaldAJ (2010) Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration. Dev Biol 341: 34–55.

2. DattaA, BryantDM, MostovKE (2011) Molecular regulation of lumen morphogenesis. Curr Biol 21: R126–136.

3. LubarskyB, KrasnowMA (2003) Tube morphogenesis: Making and shaping biological tubes. Cell 112: 19–28.

4. BeitelGJ, KrasnowMA (2000) Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127: 3271–3282.

5. ForsterD, ArmbrusterK, LuschnigS (2010) Sec24-Dependent Secretion Drives Cell-Autonomous Expansion of Tracheal Tubes in Drosophila. Curr Biol 20: 62–68.

6. GriederNC, CaussinusE, ParkerDS, CadiganK, AffolterM, et al. (2008) gamma COP Is Required for Apical Protein Secretion and Epithelial Morphogenesis in Drosophila melanogaster. Plos One 3: e3241.

7. TsarouhasV, SentiKA, JayaramSA, TiklovaK, HemphalaJ, et al. (2007) Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev Cell 13: 214–225.

8. LoweryLA, SiveH (2005) Initial formation of zebrafish brain ventricles occurs independently of circulation and requires the nagie oko and snakehead/atp1a1a.1 gene products. Development 132: 2057–2067.

9. BagnatM, CheungID, MostovKE, StainierDYR (2007) Genetic control of single lumen formation in the zebrafish gut. Nat Cell Biol 9: 954–U119.

10. OlverRE, StrangLB (1974) Ion Fluxes across Pulmonary Epithelium and Secretion of Lung Liquid in Fetal Lamb. Journal of Physiology-London 241: 327–357.

11. MyatMM, AndrewDJ (2002) Epithelial tube morphology is determined by the polarized growth and delivery of apical membrane. Cell 111: 879–891.

12. OmoriY, MalickiJ (2006) oko meduzy and related crumbs genes are determinants of apical cell features in the vertebrate embryo. Curr Biol 16: 945–957.

13. CaganRL, ReadyDF (1989) The emergence of order in the Drosophila pupal retina. Dev Biol 136: 346–362.

14. KirschfeldK (1967) [The projection of the optical environment on the screen of the rhabdomere in the compound eye of the Musca]. Exp Brain Res 3: 248–270.

15. Land MF, Nilsson DE (2002) Animal Eyes: Oxford University Press.

16. HusainN, PellikkaM, HongH, KlimentovaT, ChoeKM, et al. (2006) The agrin/perlecan-related protein eyes shut is essential for epithelial lumen formation in the Drosophila retina. Dev Cell 11: 483–493.

17. ZelhofAC, HardyRW, BeckerA, ZukerCS (2006) Transforming the architecture of compound eyes. Nature 443: 696–699.

18. NieJ, MahatoS, MustillW, TippingC, BhattacharyaSS, et al. (2012) Cross species analysis of Prominin reveals a conserved cellular role in invertebrate and vertebrate photoreceptor cells. Dev Biol 371: 312–320.

19. ReinkeR, KrantzDE, YenD, ZipurskySL (1988) Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human. Cell 52: 291–301.

20. Van VactorDJr, KrantzDE, ReinkeR, ZipurskySL (1988) Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell 52: 281–290.

21. GurudevN, YuanM, KnustE (2014) chaoptin, prominin, eyes shut and crumbs form a genetic network controlling the apical compartment of Drosophila photoreceptor cells. Biol Open 3: 332–341.

22. KrantzDE, ZipurskySL (1990) Drosophila chaoptin, a member of the leucine-rich repeat family, is a photoreceptor cell-specific adhesion molecule. EMBO J 9: 1969–1977.

23. FrancescN, KirschfeK (1971) Phenomena of Pseudopupil in Compound Eye of Drosophila. Kybernetik 9: 159–182.

24. FyrbergEA, BondBJ, HersheyND, MixterKS, DavidsonN (1981) The actin genes of Drosophila: protein coding regions are highly conserved but intron positions are not. Cell 24: 107–116.

25. FyrbergEA, MahaffeyJW, BondBJ, DavidsonN (1983) Transcripts of the six Drosophila actin genes accumulate in a stage- and tissue-specific manner. Cell 33: 115–123.

26. WagnerCR, MahowaldAP, MillerKG (2002) One of the two cytoplasmic actin isoforms in Drosophila is essential. Proceedings of the National Academy of Sciences of the United States of America 99: 8037–8042.

27. ArikawaK, HicksJL, WilliamsDS (1990) Identification of actin filaments in the rhabdomeral microvilli of Drosophila photoreceptors. J Cell Biol 110: 1993–1998.

28. KaragiosisSA, ReadyDF (2004) Moesin contributes an essential structural role in Drosophila photoreceptor morphogenesis. Development 131: 725–732.

29. LiBX, SatohAK, ReadyDF (2007) Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J Cell Biol 177: 659–669.

30. LongleyRLJr, ReadyDF (1995) Integrins and the development of three-dimensional structure in the Drosophila compound eye. Dev Biol 171: 415–433.

31. TuxworthRI, TitusMA (2000) Unconventional myosins: anchors in the membrane traffic relay. Traffic 1: 11–18.

32. ValeRD (2003) The molecular motor toolbox for intracellular transport. Cell 112: 467–480.

33. YangZ, ChenY, LilloC, ChienJ, YuZ, et al. (2008) Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice. J Clin Invest 118: 2908–2916.

34. IzaddoostS, NamSC, BhatMA, BellenHJ, ChoiKW (2002) Drosophila Crumbs is a positional cue in photoreceptor adherens junctions and rhabdomeres. Nature 416: 178–183.

35. PellikkaM, TanentzapfG, PintoM, SmithC, McGladeCJ, et al. (2002) Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416: 143–149.

36. ChartierFJ, HardyEJ, LapriseP (2012) Crumbs limits oxidase-dependent signaling to maintain epithelial integrity and prevent photoreceptor cell death. J Cell Biol 198: 991–998.

37. JohnsonK, GraweF, GrzeschikN, KnustE (2002) Drosophila crumbs is required to inhibit light-induced photoreceptor degeneration. Curr Biol 12: 1675–1680.

38. MartinAC (2010) Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev Biol 341: 114–125.

39. SawyerJM, HarrellJR, ShemerG, Sullivan-BrownJ, Roh-JohnsonM, et al. (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341: 5–19.

40. Vicente-ManzanaresM, MaX, AdelsteinRS, HorwitzAR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10: 778–790.

41. CorrigallD, WaltherRF, RodriguezL, FichelsonP, PichaudF (2007) Hedgehog signaling is a principal inducer of Myosin-II-driven cell ingression in Drosophila epithelia. Dev Cell 13: 730–742.

42. EscuderoLM, BischoffM, FreemanM (2007) Myosin II regulates complex cellular arrangement and epithelial architecture in Drosophila. Dev Cell 13: 717–729.

43. LeeA, TreismanJE (2004) Excessive Myosin activity in mbs mutants causes photoreceptor movement out of the Drosophila eye disc epithelium. Mol Biol Cell 15: 3285–3295.

44. KornED, HammerJA3rd (1988) Myosins of nonmuscle cells. Annual review of biophysics and biophysical chemistry 17: 23–45.

45. EdwardsKA, ChangXJ, KiehartDP (1995) Essential light chain of Drosophila nonmuscle myosin II. J Muscle Res Cell Motil 16: 491–498.

46. KaressRE, ChangXJ, EdwardsKA, KulkarniS, AguileraI, et al. (1991) The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65: 1177–1189.

47. KiehartDP, LutzMS, ChanD, KetchumAS, LaymonRA, et al. (1989) Identification of the gene for fly non-muscle myosin heavy chain: Drosophila myosin heavy chains are encoded by a gene family. EMBO J 8: 913–922.

48. FrankeJD, MontagueRA, KiehartDP (2005) Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr Biol 15: 2208–2221.

49. FrankeJD, MontagueRA, KiehartDP (2010) Nonmuscle myosin II is required for cell proliferation, cell sheet adhesion and wing hair morphology during wing morphogenesis. Dev Biol 345: 117–132.

50. WinterCG, WangB, BallewA, RoyouA, KaressR, et al. (2001) Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105: 81–91.

51. AmanoM, ItoM, KimuraK, FukataY, ChiharaK, et al. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J Biol Chem 271: 20246–20249.

52. MatsuiT, AmanoM, YamamotoT, ChiharaK, NakafukuM, et al. (1996) Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. EMBO J 15: 2208–2216.

53. IpYT, ParkRE, KosmanD, YazdanbakhshK, LevineM (1992) dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev 6: 1518–1530.

54. KimuraK, ItoM, AmanoM, ChiharaK, FukataY, et al. (1996) Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273: 245–248.

55. RoyouA, FieldC, SissonJC, SullivanW, KaressR (2004) Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Molecular Biology of the Cell 15: 838–850.

56. BaumannO (2004) Spatial pattern of nonmuscle myosin-II distribution during the development of the Drosophila compound eye and implications for retinal morphogenesis. Dev Biol 269: 519–533.

57. Martin-BelmonteF, YuW, Rodriguez-FraticelliAE, EwaldAJ, WerbZ, et al. (2008) Cell-polarity dynamics controls the mechanism of lumen formation in epithelial morphogenesis. Curr Biol 18: 507–513.

58. StrilicB, KuceraT, EglingerJ, HughesMR, McNagnyKM, et al. (2009) The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell 17: 505–515.

59. ChaitinMH, CoelhoN (1992) Immunogold localization of myosin in the photoreceptor cilium. Invest Ophthalmol Vis Sci 33: 3103–3108.

60. MawMA, CorbeilD, KochJ, HellwigA, Wilson-WheelerJC, et al. (2000) A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration. Hum Mol Genet 9: 27–34.

61. WilliamsDS, HallettMA, ArikawaK (1992) Association of myosin with the connecting cilium of rod photoreceptors. J Cell Sci 103(Pt 1): 183–190.

62. SteinbergRH, FisherSK, AndersonDH (1980) Disc morphogenesis in vertebrate photoreceptors. J Comp Neurol 190: 501–508.

63. WilliamsDS (1991) Actin filaments and photoreceptor membrane turnover. Bioessays 13: 171–178.

64. RichardM, GraweF, KnustE (2006) DPATJ plays a role in retinal morphogenesis and protects against light-dependent degeneration of photoreceptor cells in the Drosophila eye. Dev Dyn 235: 895–907.

65. KiehartDP, FeghaliR (1986) Cytoplasmic myosin from Drosophila melanogaster. J Cell Biol 103: 1517–1525.

66. FrankeJD, BouryAL, GeraldNJ, KiehartDP (2006) Native nonmuscle myosin II stability and light chain binding in Drosophila melanogaster. Cell Motil Cytoskeleton 63: 604–622.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa