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The Intersection of the Extrinsic Hedgehog and WNT/Wingless Signals with the Intrinsic Hox Code Underpins Branching Pattern and Tube Shape Diversity in the Airways


Tubes are common structural elements of many internal organs,

facilitating fluid flow and material exchange. To meet the local needs of diverse tissues, the branching patterns and tube shapes vary regionally. Diametric tapering and specialized branch targeting to the brain represent two common examples of variations with organismal benefits in the Drosophila airways and our vascular system. Several extrinsic signals instruct tube diversifications but the impact of intrinsic factors remains underexplored. Here, we show that the local, tube-intrinsic Hox code instructs the pattern and shape of the dorsal trunk (DT), the main Drosophila airway. In the cephalic part (DT1), where Bithorax Complex (BX-C) Hox genes are not expressed, the extrinsic Hedgehog signal is epistatic to WNT/Wingless signals. Hedgehog instructs anterior DT1 cells to take a long and narrow tube fate targeting the brain. In more posterior metameres, BX-C genes make the extrinsic WNT/Wingless signals epistatic over Hedgehog. There, WNT/Wingless instruct all DT cells to take the thick and short tube fate. Moreover, BX-C genes modulate the outputs of WNT/wingless signaling, making the DT tubes thicker in more posterior metameres. We provide a model for how intrinsic factors modify extrinsic signaling to control regional tube morphologies in a network.


Vyšlo v časopise: The Intersection of the Extrinsic Hedgehog and WNT/Wingless Signals with the Intrinsic Hox Code Underpins Branching Pattern and Tube Shape Diversity in the Airways. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004929
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004929

Souhrn

Tubes are common structural elements of many internal organs,

facilitating fluid flow and material exchange. To meet the local needs of diverse tissues, the branching patterns and tube shapes vary regionally. Diametric tapering and specialized branch targeting to the brain represent two common examples of variations with organismal benefits in the Drosophila airways and our vascular system. Several extrinsic signals instruct tube diversifications but the impact of intrinsic factors remains underexplored. Here, we show that the local, tube-intrinsic Hox code instructs the pattern and shape of the dorsal trunk (DT), the main Drosophila airway. In the cephalic part (DT1), where Bithorax Complex (BX-C) Hox genes are not expressed, the extrinsic Hedgehog signal is epistatic to WNT/Wingless signals. Hedgehog instructs anterior DT1 cells to take a long and narrow tube fate targeting the brain. In more posterior metameres, BX-C genes make the extrinsic WNT/Wingless signals epistatic over Hedgehog. There, WNT/Wingless instruct all DT cells to take the thick and short tube fate. Moreover, BX-C genes modulate the outputs of WNT/wingless signaling, making the DT tubes thicker in more posterior metameres. We provide a model for how intrinsic factors modify extrinsic signaling to control regional tube morphologies in a network.


Zdroje

1. Lubarsky B, Krasnow MA (2003) Tube morphogenesis: making and shaping biological tubes. Cell 112: 19–28. 12526790

2. Andrew DJ, Ewald AJ (2010) Morphogenesis of epithelial tubes: Insights into tube formation, elongation, and elaboration. Dev Biol 341: 34–55. doi: 10.1016/j.ydbio.2009.09.024 19778532

3. Ochoa-Espinosa A, Affolter M (2012) Branching morphogenesis: from cells to organs and back. Cold Spring Harb Perspect Biol 4.

4. Kusumbe AP, Ramasamy SK, Adams RH (2014) Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature 507: 323–328. doi: 10.1038/nature13145 24646994

5. Eilken HM, Adams RH (2010) Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol 22: 617–625. doi: 10.1016/j.ceb.2010.08.010 20817428

6. Ghabrial A, Luschnig S, Metzstein MM, Krasnow MA (2003) Branching morphogenesis of the Drosophila tracheal system. Annu Rev Cell Dev Biol 19: 623–647. 14570584

7. Cantile M, Schiavo G, Terracciano L, Cillo C (2008) Homeobox genes in normal and abnormal vasculogenesis. Nutr Metab Cardiovasc Dis 18: 651–658. doi: 10.1016/j.numecd.2008.08.001 19013779

8. Kachgal S, Mace KA, Boudreau NJ (2012) The dual roles of homeobox genes in vascularization and wound healing. Cell Adh Migr 6: 457–470. doi: 10.4161/cam.22164 23076135

9. Pruett ND, Hajdu Z, Zhang J, Visconti RP, Kern MJ, et al. (2012) Changing topographic Hox expression in blood vessels results in regionally distinct vessel wall remodeling. Biol Open 1: 430–435. doi: 10.1242/bio.2012039 23213434

10. Pruett ND, Visconti RP, Jacobs DF, Scholz D, McQuinn T, et al. (2008) Evidence for Hox-specified positional identities in adult vasculature. BMC Dev Biol 8: 93. doi: 10.1186/1471-213X-8-93 18826643

11. Schottenfeld J, Song Y, Ghabrial AS (2010) Tube continued: morphogenesis of the Drosophila tracheal system. Curr Opin Cell Biol 22: 633–639. doi: 10.1016/j.ceb.2010.07.016 20739171

12. Affolter M, Caussinus E (2008) Tracheal branching morphogenesis in Drosophila: new insights into cell behaviour and organ architecture. Development 135: 2055–2064. doi: 10.1242/dev.014498 18480161

13. Manning G, Krasnow MA (1993) The Development of Drosophila melanogaster. Plainview, N.Y.: Cold Spring Harbor Laboratory Press.

14. Samakovlis C, Hacohen N, Manning G, Sutherland DC, Guillemin K, et al. (1996) Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122: 1395–1407. 8625828

15. Hartenstein V, Jan YN (1992) Studying Drosophila Embryogenesis with P-Lacz Enhancer Trap Lines. Rouxs Archives of Developmental Biology 201: 194–220.

16. Tanaka-Matakatsu M, Uemura T, Oda H, Takeichi M, Hayashi S (1996) Cadherin-mediated cell adhesion and cell motility in Drosophila trachea regulated by the transcription factor Escargot. Development 122: 3697–3705. 9012491

17. Samakovlis C, Manning G, Steneberg P, Hacohen N, Cantera R, et al. (1996) Genetic control of epithelial tube fusion during Drosophila tracheal development. Development 122: 3531–3536. 8951068

18. Jiang L, Crews ST (2003) The Drosophila dysfusion basic helix-loop-helix (bHLH)-PAS gene controls tracheal fusion and levels of the trachealess bHLH-PAS protein. Mol Cell Biol 23: 5625–5637. doi: 10.1128/MCB.23.16.5625-5637.2003 12897136

19. Uv A, Cantera R, Samakovlis C (2003) Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol 13: 301–309. 12791296

20. Sutherland D, Samakovlis C, Krasnow MA (1996) branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 87: 1091–1101. 8978613

21. Klambt C, Glazer L, Shilo BZ (1992) breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 6: 1668–1678. 1325393

22. Reichman-Fried M, Dickson B, Hafen E, Shilo BZ (1994) Elucidation of the role of breathless, a Drosophila FGF receptor homolog, in tracheal cell migration. Genes Dev 8: 428–439. 8125257

23. Lee T, Hacohen N, Krasnow M, Montell DJ (1996) Regulated Breathless receptor tyrosine kinase activity required to pattern cell migration and branching in the Drosophila tracheal system. Genes Dev 10: 2912–2921. 8918892

24. Vincent S, Ruberte E, Grieder NC, Chen CK, Haerry T, et al. (1997) DPP controls tracheal cell migration along the dorsoventral body axis of the Drosophila embryo. Development 124: 2741–2750. 9226445

25. Chen CK, Kuhnlein RP, Eulenberg KG, Vincent S, Affolter M, et al. (1998) The transcription factors KNIRPS and KNIRPS RELATED control cell migration and branch morphogenesis during Drosophila tracheal development. Development 125: 4959–4968. 9811580

26. Ribeiro C, Ebner A, Affolter M (2002) In vivo imaging reveals different cellular functions for FGF and Dpp signaling in tracheal branching morphogenesis. Dev Cell 2: 677–683. 12015974

27. Chihara T, Hayashi S (2000) Control of tracheal tubulogenesis by Wingless signaling. Development 127: 4433–4442. 11003842

28. Llimargas M (2000) Wingless and its signalling pathway have common and separable functions during tracheal development. Development 127: 4407–4417. 11003840

29. Llimargas M, Lawrence PA (2001) Seven Wnt homologues in Drosophila: a case study of the developing tracheae. Proc Natl Acad Sci U S A 98: 14487–14492. doi: 10.1073/pnas.251304398 11717401

30. Kuhnlein RP, Schuh R (1996) Dual function of the region-specific homeotic gene spalt during Drosophila tracheal system development. Development 122: 2215–2223. 8681802

31. Ribeiro C, Neumann M, Affolter M (2004) Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr Biol 14: 2197–2207. 15620646

32. Shaye DD, Casanova J, Llimargas M (2008) Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat Cell Biol 10: 964–970. doi: 10.1038/ncb1756 18641639

33. Buti E, Mesquita D, Araujo SJ (2014) Hedgehog is a positive regulator of FGF signalling during embryonic tracheal cell migration. PLoS One 9: e92682. doi: 10.1371/journal.pone.0092682 24651658

34. Glazer L, Shilo BZ (2001) Hedgehog signaling patterns the tracheal branches. Development 128: 1599–1606. 11290298

35. Kato K, Chihara T, Hayashi S (2004) Hedgehog and Decapentaplegic instruct polarized growth of cell extensions in the Drosophila trachea. Development 131: 5253–5261. 15456724

36. Llimargas M, Casanova J (1997) ventral veinless, a POU domain transcription factor, regulates different transduction pathways required for tracheal branching in Drosophila. Development 124: 3273–3281. 9310322

37. Biehs B, Kechris K, Liu S, Kornberg TB (2010) Hedgehog targets in the Drosophila embryo and the mechanisms that generate tissue-specific outputs of Hedgehog signaling. Development 137: 3887–3898. doi: 10.1242/dev.055871 20978080

38. Beitel GJ, Krasnow MA (2000) Genetic control of epithelial tube size in the Drosophila tracheal system. Development 127: 3271–3282. 10887083

39. Lewis EB (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565–570. 103000

40. Carroll SB (1995) Homeotic genes and the evolution of arthropods and chordates. Nature 376: 479–485. 7637779

41. Mann RS, Morata G (2000) The developmental and molecular biology of genes that subdivide the body of Drosophila. Annu Rev Cell Dev Biol 16: 243–271. 11031237

42. Shubin N, Tabin C, Carroll S (2009) Deep homology and the origins of evolutionary novelty. Nature 457: 818–823. doi: 10.1038/nature07891 19212399

43. Mann RS, Carroll SB (2002) Molecular mechanisms of selector gene function and evolution. Curr Opin Genet Dev 12: 592–600. 12200165

44. Pearson JC, Lemons D, McGinnis W (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Genet 6: 893–904. 16341070

45. Mallo M, Wellik DM, Deschamps J (2010) Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344: 7–15. doi: 10.1016/j.ydbio.2010.04.024 20435029

46. Castelli-Gair J, Greig S, Micklem G, Akam M (1994) Dissecting the temporal requirements for homeotic gene function. Development 120: 1983–1995. 7925003

47. Averof M, Akam M (1995) Hox genes and the diversification of insect and crustacean body plans. Nature 376: 420–423. 7630416

48. Averof M, Patel NH (1997) Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388: 682–686. 9262403

49. Merabet S, Hombria JC, Hu N, Pradel J, Graba Y (2005) Hox-controlled reorganisation of intrasegmental patterning cues underlies Drosophila posterior spiracle organogenesis. Development 132: 3093–3102. 15930099

50. Sanchez-Higueras C, Sotillos S, Castelli-Gair Hombria J (2014) Common origin of insect trachea and endocrine organs from a segmentally repeated precursor. Curr Biol 24: 76–81. doi: 10.1016/j.cub.2013.11.010 24332544

51. Kaufman TC, Lewis R, Wakimoto B (1980) Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B. Genetics 94: 115–133. 17248988

52. Sanchez-Herrero E, Vernos I, Marco R, Morata G (1985) Genetic organization of Drosophila bithorax complex. Nature 313: 108–113. 3917555

53. Maeda RK, Karch F (2006) The ABC of the BX-C: the bithorax complex explained. Development 133: 1413–1422. 16556913

54. Chiang C, Young KE, Beachy PA (1995) Control of Drosophila tracheal branching by the novel homeodomain gene unplugged, a regulatory target for genes of the bithorax complex. Development 121: 3901–3912. 8582298

55. Hu N, Castelli-Gair J (1999) Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Dev Biol 214: 197–210. 10491268

56. Nusslein-Volhard C, Wieschaus E (1980) Mutations affecting segment number and polarity in Drosophila. Nature 287: 795–801. 6776413

57. Chung S, Chavez C, Andrew DJ (2011) Trachealess (Trh) regulates all tracheal genes during Drosophila embryogenesis. Dev Biol 360: 160–172. doi: 10.1016/j.ydbio.2011.09.014 21963537

58. Shiga Y, TanakaMatakatsu M, Hayashi S (1996) A nuclear GFP beta-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Development Growth & Differentiation 38: 99–106.

59. Hamada F, Tomoyasu Y, Takatsu Y, Nakamura M, Nagai S, et al. (1999) Negative regulation of Wingless signaling by D-axin, a Drosophila homolog of axin. Science 283: 1739–1742. 10073940

60. Willert K, Logan CY, Arora A, Fish M, Nusse R (1999) A Drosophila Axin homolog, Daxin, inhibits Wnt signaling. Development 126: 4165–4173. 10457025

61. Cliffe A, Hamada F, Bienz M (2003) A role of Dishevelled in relocating Axin to the plasma membrane during wingless signaling. Curr Biol 13: 960–966. 12781135

62. Caviglia S, Luschnig S (2013) The ETS domain transcriptional repressor Anterior open inhibits MAP kinase and Wingless signaling to couple tracheal cell fate with branch identity. Development 140: 1240–1249. doi: 10.1242/dev.087874 23444354

63. Price JV, Clifford RJ, Schupbach T (1989) The maternal ventralizing locus torpedo is allelic to faint little ball, an embryonic lethal, and encodes the Drosophila EGF receptor homolog. Cell 56: 1085–1092. 2493993

64. Wappner P, Gabay L, Shilo BZ (1997) Interactions between the EGF receptor and DPP pathways establish distinct cell fates in the tracheal placodes. Development 124: 4707–4716. 9409686

65. Rutledge BJ, Zhang K, Bier E, Jan YN, Perrimon N (1992) The Drosophila spitz gene encodes a putative EGF-like growth factor involved in dorsal-ventral axis formation and neurogenesis. Genes Dev 6: 1503–1517. 1644292

66. Bier E, Jan LY, Jan YN (1990) rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev 4: 190–203. 2110920

67. Urban S, Lee JR, Freeman M (2001) Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107: 173–182. 11672525

68. Affolter M, Nellen D, Nussbaumer U, Basler K (1994) Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGF beta homologs during Drosophila embryogenesis. Development 120: 3105–3117. 7720555

69. Nellen D, Affolter M, Basler K (1994) Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78: 225–237. 8044837

70. Wieschaus E, Nussleinvolhard C, Jurgens G (1984) Mutations Affecting the Pattern of the Larval Cuticle in Drosophila-Melanogaster .3. Zygotic Loci on the X-Chromosome and 4th Chromosome. Wilhelm Rouxs Archives of Developmental Biology 193: 296–307.

71. Noordermeer J, Klingensmith J, Perrimon N, Nusse R (1994) dishevelled and armadillo act in the wingless signalling pathway in Drosophila. Nature 367: 80–83. 7906389

72. Siegfried E, Wilder EL, Perrimon N (1994) Components of wingless signalling in Drosophila. Nature 367: 76–80. 8107779

73. Jiang J, Hui CC (2008) Hedgehog signaling in development and cancer. Dev Cell 15: 801–812. doi: 10.1016/j.devcel.2008.11.010 19081070

74. Chen Y, Jiang J (2013) Decoding the phosphorylation code in Hedgehog signal transduction. Cell Res 23: 186–200. doi: 10.1038/cr.2013.10 23337587

75. Hidalgo A, Ingham P (1990) Cell patterning in the Drosophila segment: spatial regulation of the segment polarity gene patched. Development 110: 291–301. 2081466

76. Ingham PW (1993) Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. Nature 366: 560–562. 8255293

77. DiNardo S, Heemskerk J, Dougan S, O’Farrell PH (1994) The making of a maggot: patterning the Drosophila embryonic epidermis. Curr Opin Genet Dev 4: 529–534. 7950320

78. Aza-Blanc P, Ramirez-Weber FA, Laget MP, Schwartz C, Kornberg TB (1997) Proteolysis that is inhibited by hedgehog targets Cubitus interruptus protein to the nucleus and converts it to a repressor. Cell 89: 1043–1053. 9215627

79. Methot N, Basler K (1999) Hedgehog controls limb development by regulating the activities of distinct transcriptional activator and repressor forms of Cubitus interruptus. Cell 96: 819–831. 10102270

80. Methot N, Basler K (2001) An absolute requirement for Cubitus interruptus in Hedgehog signaling. Development 128: 733–742. 11171398

81. Parker DS, White MA, Ramos AI, Cohen BA, Barolo S (2011) The cis-regulatory logic of Hedgehog gradient responses: key roles for gli binding affinity, competition, and cooperativity. Sci Signal 4: ra38. doi: 10.1126/scisignal.2002077 21653228

82. Hepker J, Wang QT, Motzny CK, Holmgren R, Orenic TV (1997) Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development 124: 549–558. 9053330

83. Karim MR, Moore AW (2011) Convergent local identity and topographic projection of sensory neurons. J Neurosci 31: 17017–17027. doi: 10.1523/JNEUROSCI.2815-11.2011 22114271

84. Dai P, Akimaru H, Ishii S (2003) A hedgehog-responsive region in the Drosophila wing disc is defined by debra-mediated ubiquitination and lysosomal degradation of Ci. Dev Cell 4: 917–928. 12791275

85. Martizez Arias A, Baker NE, Ingham PW (1988) Role of segment polarity genes in the definition and maintenance of cell states in the Drosophila embryo. Development 103: 157–170. 3197626

86. Wilk R, Weizman I, Shilo BZ (1996) trachealess encodes a bHLH-PAS protein that is an inducer of tracheal cell fates in Drosophila. Genes Dev 10: 93–102. 8557198

87. Chen Y, Gallaher N, Goodman RH, Smolik SM (1998) Protein kinase A directly regulates the activity and proteolysis of cubitus interruptus. Proc Natl Acad Sci U S A 95: 2349–2354. 9482888

88. Merabet S, Litim-Mecheri I, Karlsson D, Dixit R, Saadaoui M, et al. (2011) Insights into Hox protein function from a large scale combinatorial analysis of protein domains. PLoS Genet 7: e1002302. doi: 10.1371/journal.pgen.1002302 22046139

89. Syed ZA, Bouge AL, Byri S, Chavoshi TM, Tang E, et al. (2012) A luminal glycoprotein drives dose-dependent diameter expansion of the Drosophila melanogaster hindgut tube. PLoS Genet 8: e1002850. doi: 10.1371/journal.pgen.1002850 22876194

90. Camprodon FJ, Castelligair JE (1994) Ultrabithorax Protein Expression in Breakpoint Mutants—Localization of Single, Cooperative and Redundant Cis Regulatory Elements. Rouxs Archives of Developmental Biology 203: 411–421.

91. Struhl G, White RA (1985) Regulation of the Ultrabithorax gene of Drosophila by other bithorax complex genes. Cell 43: 507–519. 3935322

92. Tsarouhas V, Senti KA, Jayaram SA, Tiklova K, Hemphala J, et al. (2007) Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev Cell 13: 214–225. 17681133

93. Forster D, Luschnig S (2012) Src42A-dependent polarized cell shape changes mediate epithelial tube elongation in Drosophila. Nat Cell Biol 14: 526–534. doi: 10.1038/ncb2456 22446736

94. Forster D, Armbruster K, Luschnig S (2010) Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila. Curr Biol 20: 62–68. doi: 10.1016/j.cub.2009.11.062 20045324

95. Tiklova K, Tsarouhas V, Samakovlis C (2013) Control of airway tube diameter and integrity by secreted chitin-binding proteins in Drosophila. PLoS One 8: e67415. doi: 10.1371/journal.pone.0067415 23826295

96. Fraichard S, Bouge AL, Chauvel I, Bouhin H (2006) Tenectin, a novel extracellular matrix protein expressed during Drosophila melanogaster embryonic development. Gene Expr Patterns 6: 772–776. 16510317

97. Choo SW, White R, Russell S (2011) Genome-wide analysis of the binding of the Hox protein Ultrabithorax and the Hox cofactor Homothorax in Drosophila. PLoS One 6: e14778. doi: 10.1371/journal.pone.0014778 21483667

98. Herriges JC, Yi L, Hines EA, Harvey JF, Xu G, et al. (2012) Genome-scale study of transcription factor expression in the branching mouse lung. Dev Dyn 241: 1432–1453. doi: 10.1002/dvdy.23823 22711520

99. Lindsley DL, Zimm GG, Lindsley DL (1992) The genome of Drosophila melanogaster. San Diego: Academic Press. viii, 1133 p., 1138 leaves of plates p.

100. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401–415. 8223268

101. Le T, Liang Z, Patel H, Yu MH, Sivasubramaniam G, et al. (2006) A new family of Drosophila balancer chromosomes with a w—dfd-GMR yellow fluorescent protein marker. Genetics 174: 2255–2257. doi: 10.1534/genetics.106.063461 17057238

102. Starz-Gaiano M, Cho NK, Forbes A, Lehmann R (2001) Spatially restricted activity of a Drosophila lipid phosphatase guides migrating germ cells. Development 128: 983–991. 11222152

103. St Pierre SE, Ponting L, Stefancsik R, McQuilton P, FlyBase C (2014) FlyBase 102--advanced approaches to interrogating FlyBase. Nucleic Acids Res 42: D780–788. doi: 10.1093/nar/gkt1092 24234449

104. Li-Kroeger D, Witt LM, Grimes HL, Cook TA, Gebelein B (2008) Hox and senseless antagonism functions as a molecular switch to regulate EGF secretion in the Drosophila PNS. Dev Cell 15: 298–308. doi: 10.1016/j.devcel.2008.06.001 18694568

105. Lohmann I, McGinnis N, Bodmer M, McGinnis W (2002) The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper. Cell 110: 457–466. 12202035

106. Ohshiro T, Saigo K (1997) Transcriptional regulation of breathless FGF receptor gene by binding of TRACHEALESS/dARNT heterodimers to three central midline elements in Drosophila developing trachea. Development 124: 3975–3986. 9374395

107. Barrio R, de Celis JF, Bolshakov S, Kafatos FC (1999) Identification of regulatory regions driving the expression of the Drosophila spalt complex at different developmental stages. Dev Biol 215: 33–47. 10525348

108. Hosono C, Takaira K, Matsuda R, Saigo K (2003) Functional subdivision of trunk visceral mesoderm parasegments in Drosophila is required for gut and trachea development. Development 130: 439–449. 12490551

109. Bradley PL, Andrew DJ (2001) ribbon encodes a novel BTB/POZ protein required for directed cell migration in Drosophila melanogaster. Development 128: 3001–3015. 11532922

110. Inbal A, Volk T, Salzberg A (2004) Recruitment of ectodermal attachment cells via an EGFR-dependent mechanism during the organogenesis of Drosophila proprioceptors. Dev Cell 7: 241–250. 15296720

111. Skeath JB (1998) The Drosophila EGF receptor controls the formation and specification of neuroblasts along the dorsal-ventral axis of the Drosophila embryo. Development 125: 3301–3312. 9693134

112. Kumar JP, Tio M, Hsiung F, Akopyan S, Gabay L, et al. (1998) Dissecting the roles of the Drosophila EGF receptor in eye development and MAP kinase activation. Development 125: 3875–3885. 9729495

113. Hopmann R, Duncan D, Duncan I (1995) Transvection in the iab-5,6,7 region of the bithorax complex of Drosophila: homology independent interactions in trans. Genetics 139: 815–833. 7713434

114. Perrimon N, Noll E, McCall K, Brand A (1991) Generating lineage-specific markers to study Drosophila development. Dev Genet 12: 238–252. 1651183

115. Estacio-Gomez A, Moris-Sanz M, Schafer AK, Perea D, Herrero P, et al. (2013) Bithorax-complex genes sculpt the pattern of leucokinergic neurons in the Drosophila central nervous system. Development 140: 2139–2148. doi: 10.1242/dev.090423 23633511

116. Urbach R, Technau GM (2003) Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130: 3621–3637. 12835380

117. Lee JJ, von Kessler DP, Parks S, Beachy PA (1992) Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71: 33–50. 1394430

118. Patel NH (1994) Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol 44: 445–487. 7707967

119. Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Berlin; New York: Springer. xvii, 405 p. p.

120. White RA, Wilcox M (1984) Protein products of the bithorax complex in Drosophila. Cell 39: 163–171. 6091908

121. Kosman D, Small S, Reinitz J (1998) Rapid preparation of a panel of polyclonal antibodies to Drosophila segmentation proteins. Dev Genes Evol 208: 290–294. 9683745

122. Xie B, Charlton-Perkins M, McDonald E, Gebelein B, Cook T (2007) Senseless functions as a molecular switch for color photoreceptor differentiation in Drosophila. Development 134: 4243–4253. 17978002

123. Henderson KD, Isaac DD, Andrew DJ (1999) Cell fate specification in the Drosophila salivary gland: the integration of homeotic gene function with the DPP signaling cascade. Dev Biol 205: 10–21. 9882494

124. Celniker SE, Keelan DJ, Lewis EB (1989) The molecular genetics of the bithorax complex of Drosophila: characterization of the products of the Abdominal-B domain. Genes Dev 3: 1424–1436. 2575066

125. Blochlinger K, Bodmer R, Jan LY, Jan YN (1990) Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev 4: 1322–1331. 1977661

126. Yip ML, Lamka ML, Lipshitz HD (1997) Control of germ-band retraction in Drosophila by the zinc-finger protein HINDSIGHT. Development 124: 2129–2141. 9187140

127. Sampedro J, Guerrero I (1991) Unrestricted expression of the Drosophila gene patched allows a normal segment polarity. Nature 353: 187–190. 1653907

128. Jeon M, Zinn K (2009) Receptor tyrosine phosphatases control tracheal tube geometries through negative regulation of Egfr signaling. Development 136: 3121–3129. doi: 10.1242/dev.033597 19675131

129. Goto S, Hayashi S (1997) Specification of the embryonic limb primordium by graded activity of Decapentaplegic. Development 124: 125–132. 9006073

130. Merabet S, Ebner A, Affolter M (2005) The Drosophila Extradenticle and Homothorax selector proteins control branchless/FGF expression in mesodermal bridge-cells. EMBO Rep 6: 762–768. doi: 10.1038/sj.embor.7400462 16007069

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Získaná hemofilie - Povědomí o nemoci a její diagnostika
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Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

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