全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2013 

Notch and PKC Are Involved in Formation of the Lateral Region of the Dorso-Ventral Axis in Drosophila Embryos

DOI: 10.1371/journal.pone.0067789

Full-Text   Cite this paper   Add to My Lib

Abstract:

The Notch gene encodes an evolutionarily conserved cell surface receptor that generates regulatory signals based on interactions between neighboring cells. In Drosophila embryos it is normally expressed at a low level due to strong negative regulation. When this negative regulation is abrogated neurogenesis in the ventral region is suppressed, the development of lateral epidermis is severely disrupted, and the dorsal aminoserosa is expanded. Of these phenotypes only the anti-neurogenic phenotype could be linked to excess canonical Notch signaling. The other phenotypes were linked to high levels of Notch protein expression at the surface of cells in the lateral regions indicating that a non-canonical Notch signaling activity normally functions in these regions. Results of our studies reported here provide evidence. They show that Notch activities are inextricably linked to that of Pkc98E, the homolog of mammalian PKCδ. Notch and Pkc98E up-regulate the levels of the phosphorylated form of IκBCactus, a negative regulator of Toll signaling, and Mothers against dpp (MAD), an effector of Dpp signaling. Our data suggest that in the lateral regions of the Drosophila embryos Notch activity, in conjunction with Pkc98E activity, is used to form the slopes of the opposing gradients of Toll and Dpp signaling that specify cell fates along the dorso-ventral axis.

References

[1]  Poulson DF (1937) Chromosomal deficiencies and embryonic development of Drosophila melanogadter. Proc Natl Acad Sci USA 23: 133–38.
[2]  LeComte M, Wesley UV, Mok LP, Shepherd A, Wesley C (2006). Evidence for the involvement of dominant-negative Notch molecules in the normal course of Drosophila development. Dev Dyn 235, 411–426.
[3]  Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284, 770–776.
[4]  Tien A-C, Rajaon A, Bellen HJ (2009) A Notch updated. J Cell Bio. 184: 621–629.
[5]  Shepherd AK, Singh R, Wesley CS (2009) Notch mRNA expression in Drosophila embryos is negatively regulated at the level of mRNA 3′ processing. PLoS One 4: e8063.
[6]  Shepherd A, Wesley U, Wesley C (2010) Notch and Delta mRNAs in early-stage and mid-stage drosophila embryos exhibit complementary patterns of protein-producing potentials. Dev Dyn. 239: 1220–1233.
[7]  Cabrera CV (1990). Lateral inhibition and cell fate during neurogenesis in Drosophila: the interactions between scute, Notch and Delta. Development 110, 733–742.
[8]  Wesley CS, Saez L (2000) Analysis of notch lacking the carboxyl terminus identified in Drosophila embryos. J Cell Biol 149, 683–696.
[9]  Lieber T, Kidd S, Alcamo E, Corbin V, Young MW (1993) Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev 7, 1949–1965.
[10]  Struhl G, Fitzgerald K, Greenwald I (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74, 331–345.
[11]  Brennan K, Tateson R, Lewis K, Arias AM (1997) A functional analysis of Notch mutations in Drosophila. Genetics 147: 177–188.
[12]  Wesley CS, Mok LP (2003) Regulation of Notch signaling by a novel mechanism involving suppressor of hairless stability and carboxyl terminus-truncated notch. Mol Cell Biol 23: 5581–5593.
[13]  Fortini ME, Rebay I, Caron LA, Artavanis-Tsakonas S (1993) An activated Notch receptor blocks cell-fate commitment in the developing Drosophila eye. Nature 365: 555–557.
[14]  Struhl G, Adachi A (1998) Nuclear access and action of notch in vivo. Cell 93: 649–660.
[15]  Heitzler P, Simpson P (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64: 1083–1092.
[16]  Bardot B, Mok LP, Thayer T, Ahimou F, Wesley C (2005) The Notch amino terminus regulates protein levels and Delta-induced clustering of Drosophila Notch receptors. Exp Cell Res 304: 202–223.
[17]  Fryer CJ, Lamar E, Turbachova I, Kintner C, Jones KA (2002) Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev 16: 1397–1411.
[18]  Fryer CJ, White JB, Jones KA (2004) Mastermind recruits CycC:CDK8 to phosphorylate the Notch ICD and coordinate activation with turnover. Mol Cell 16: 509–520.
[19]  Ahimou F, Mok LP, Bardot B, Wesley C (2004) The adhesion force of Notch with Delta and the rate of Notch signaling. J Cell Biol 167: 1217–1229.
[20]  Wilkin MB, Baron M (2005) Endocytic regulation of Notch activation and down-regulation (review). Mol Membr Biol 22: 279–289.
[21]  Lyman D, Young MW (1993) Further evidence for function of the Drosophila Notch protein as a transmembrane receptor. Proc Natl Acad Sci U S A 90: 10395–10399.
[22]  Le Borgne R, Bardin A, Schweisguth F (2005) The roles of receptor and ligand endocytosis in regulating Notch signaling. Development 132: 1751–1762.
[23]  Fehon RG, Kooh PJ, Rebay I, Regan CL, Xu T, et al. (1990) Molecular interaction between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61: 523–534.
[24]  Parks AL, Kleug KM, Stout JR, Muskavitch MA (2000) Ligand endocytosis drives receptor dissociation and activation in the Notch pathway. Development 127: 1373–1385.
[25]  Mishra-Gorur K, Rand MD, Perez-Villamil B, Artavanis-Tsakonas S (2002) Down-regulation of Delta by proteolytic processing. J Cell Biol 159: 313–324.
[26]  Mok L-P, Qin T, Bardot B, LeComte M, Homayouni A, et al. (2005) Delta activity independent of its activity as a ligand of Notch. BMC Dev Biol 5: 6.
[27]  Kidd S, Lieber T, Young MW (1998) Ligand-induced cleavage and regulation of nuclear entry of Notch in Drosophila melanogaster embryos. Genes Dev 12: 3728–40.
[28]  Baker R, Schubiger G (1996) Autonomous and nonautonomous Notch functions for embryonic muscle and epidermis development in Drosophila. Development 122: 617–626.
[29]  Major R, Irvine KD (2005) Influence of Notch on dorsoventral compartmentalization and actin organization in the Drosophila wing. Development 132: 3823–3833.
[30]  Langdon T, Hayward P, Brennan K, Wirtz-Peitz F, Sanders P, et al. (2006) Notch receptor encodes two structurally separable functions in Drosophila: A genetic analysis. Dev Dyn 235: 998–1013.
[31]  Hayward P, Brennan K, Sanders P, Balayo T, DasGupta R, et al. (2005) Notch modulates Wnt signaling by associating with Armadillo/beta-catenin and regulating its transcriptional activity. Development 132: 1819–30.
[32]  de Celis JF, Garcia Bellido A (1994) Roles of the Notch gene in Drosophila wing morhogenesis. Mech Dev 46: 109–122.
[33]  Heitzler P (2010) Biodiversity and noncanonical Notch signaling. Curr Top Dev Biol 92: 457–81.
[34]  Wesley CS (1999) Notch and Wingless regulate cuticle patterning genes. Mol Cell Biol 19: 5743–5758.
[35]  Wesley CS, Guo H, Chaudhry KA, Thali MJ, Yin JC, et al. (2011) Loss of PTB or negative regulation of Notch mRNA reveals distinct zones of Notch and Actin protein accumulation in Drosophila embryo. PLoS One 6: e21876.
[36]  Roth S (2003) The origin of dorso-ventral polarity in Drosophila. Phil Trans R Soc Lond B 358: 1317–1329.
[37]  Moussian B, Roth S (2005) Dorsoventral axis formation in the Drosophila embryo-shaping and transducing a morphogen gradient. Curr Biol 15: R887–R899.
[38]  O’Connor MB, Umulis D, Othmer HG, Blair SS (2006) Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133: 183–193.
[39]  Lall S, Patel NH (2001) Conservation and divergence in molecular mechanisms of axis formation. Ann Rev Genet 35: 407–437.
[40]  Umulis D, O’Connor MB, Blair SS (2009) The extracellular regulation of bone morphogenetic protein signaling. Development 136: 3715–3728.
[41]  Reach M, Galindo RL, Towb P, Allen JL, Karin M, et al. (1996) A gradient of Cactus protein degradation establishes dorso-ventral polarity in the Drosophila embryo. Dev Biol 180: 353–364.
[42]  Geisler R, Bergmann A, Hiromi Y, Nüsslein-Volhard C (1992) cactus, a gene involved in dorsoventral pattern formation of Drosophila, is related to the I kappa B gene family of vertebrates. Cell 71: 613–621.
[43]  Kidd S (1992) Characterization of the Drosophila cactus locus and analysis of interactions between cactus and dorsal proteins. Cell 71: 623–635.
[44]  Govind S, Brennan L, Steward R (1993) Homeostatic balance between dorsal and cactus proteins in the Drosophila embryos. Development 117: 135–148.
[45]  Roth S, Hiromi Y, Godt D, Nusslein-Volhard C (1991) cactus, a maternal gene required for proper formation of the dorsoventral morphogen gradient in Drosophila embryos. Development 112: 371–388.
[46]  Whalen AM, Steward R (1993) Dissociation of the Dorsal-Cactus complex and phosphorylation of the Dorsal protein correlate with the nuclear localization of Dorsal. J Cell Biol 123: 523–534.
[47]  Anderson KV, Jurgens G, Nusslein-Volhard C (1985) Establishment of Dorsal-ventral polarity in the Drosophila embryo: genetic studies on the role of the Toll gene product. Cell 42: 779–789.
[48]  Belvin MP, Jin Y, Anderson KV (1995) Cactus protein degradation mediates Drosophila dorsal-ventral signaling. Genes Dev 9: 783–793.
[49]  Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer, 2nd Edition, p405.
[50]  Morel V, Schweisguth F (2000) Repression by Suppressor of Hairless and activation by Notch are required to define a single row of single-minded expressing cells in the Drosophila embryo. Genes Dev 14: 377–388.
[51]  Bardin AJ, Schweisguth F (2006) Bearded family members inhibit neuralized-mediated endocytosis and signaling activity of Delta in Drosophila. Dev. Cell 10: 245–255.
[52]  Cowden J, Levine M (2002) The snail repressor positions Notch signaling in the Drosophila embryo. Development 129: 1785–1793.
[53]  Dansereau DA, Lunke MD, Finkielsztein A, Russell MA, Brook WJ (2002) Hephaestus encodes a polypyrimidine tract binding protein that regulates Notch signalling during wing development in Drosophila melanogaster. Development 129: 5553–66.
[54]  Wesley CS, Saez L (2000) Notch responds differently to Delta and Wingless in cultured Drosophila cells. J Biol Chem 275: 9099–9101.
[55]  Payre F, Vincent A, Carreno S (1999) ovo/svb integrates Wingless and Der pathwasy to control epidermis differentiation. Nature 400: 271–275.
[56]  Delon I, Chanut-Delalande H, Payre F (2003) The Ovo/Shavenbaby transcription factor specifies actin remodeling during epidermal differentiation in Drosophila. Mech Dev 120: 747–758.
[57]  Chanut-Delalande H, Fernandes I, Roch F, Payre F, Plaza S (2006) Shavenbaby couples patterning to epidermal cell shape control. PloS Biology e290.
[58]  Schaeffer E, Smith D, Mardon G, Quinn W, Zuker C (1989) Isolation and characterization of two new Drosophila protein kinase C genes, including one specifically expressed in photoreceptor cells. Cell 57: 403–412.
[59]  Rosenthal A, Rhee L, Yadegari R, Paro R, Ullrich A, et al. (1987) Structure and nucleotide sequence of a Drosophila melanogaster protein kinase C gene. EMBO J 6: 433–441.
[60]  Shieh BH, Parker L, Popescu D (2002) Protein kinase C (PKC) isoforms in Drosophila. J Biochem 132: 523–527.
[61]  Loegering DJ, Lennartz MR (2011) Protein Kinase C and Toll-like Receptor signaling. Enzyme Research 2011 2011: 537821.
[62]  Bynagari-Settipalli YS, Chari R, Kilpatrick L, Kunapuli SP (2010) Protein kinase C- possible therapeutic target to treat cardiovascular diseases. Cardiovasc Hematol Disord Drug Targets 10: 292–308.
[63]  de Barry J, Liegeois CM, Janoshazi A (2010) Protein kinase C as a peripheral biomarker for Alzheimer’s disease. Exp Gerontol 45: 64–69.
[64]  Lee MR, Duan W, Tan SL (2008) Protein kinase C isozymers as potential therapeutic targets in immune disorders. Expert Opin Ther Targets 12: 535–552.
[65]  Koivunen J, Aaltonen A, Peltonen J (2006) Protein kinase C (PKC) family in cancer progression. Cancer Lett 235: 1–10.
[66]  Alkon DL, Sun M-K, Nelson TJ (2006) PKC signaling deficits: a mechanistic hypothesis for the origins of Alzheimer’s disease. Trends Pharmocol Sci 28: 51–60.
[67]  Kankel MW, Hurlbut GD, Upadhyay G, Jajnik V, Yedvobnick B, et al. (2007) Investigating the genetic circuitry of Mastermind in Drosophila, a Notch signal effector. Genetics 177: 2493–2505.
[68]  Cruz C, Glavic A, Casado M, de Celis J (2009) A gain-of-function screen identifying genes required fro growth and pattern formation of the Srosophila melanogaster wing. Genetics 183: 1005–1026.
[69]  Norga KK, Gurganus MC, Dilda CL, Yamamoto A, Lyman RF, et al. (2003) Quantitative analysis of bristle number in Drosophhila melanogaster mutants identifies genes involved in neural development. Curr Biol 13: 1388–1396.
[70]  Fernandez NQ, Grosshans J, Goltz JS, Stein D (2001) Separable and redundant regulatory determinants in Cactus mediate its dorsal group dependent degradation. Development 128: 2963–2974.
[71]  Ye Y, Lukinova N, Fortini ME (1999) Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature 328: 525–529.
[72]  Struhl G, Greenwald I (1999) Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature 398: 522–525.
[73]  Lieber T, Kidd S, Young MW (2002) kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev 16: 209–221.
[74]  Gho M, Lecourtois M, Geroud G, Posakony JW, Schweisguth F (1996) Subcellular localization of Suppressor of Hairless in Drosophila sense organ cells during Notch signalong. Development 122: 1673–1682.
[75]  Struhl G, Adachi A (2000) Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol Cell 6: 625–636.
[76]  Blokzijl A, Dahlqvist C, Reissmann E, Falk A, Moliner A, et al. (2003) Cross-talk between the Notch and TGF-b signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J Cell Biol 163: 723–728.
[77]  Samon JB, Champekar A, Minter LM, Telfer JC, Miele L et al. (2008. Notch1 and TGFβ1 cooperatively regulate Foxp3 expression and the maintenance pf peripheral regulatory T cells. Blood 112: 1813–1821.
[78]  Takizawa T, Ochlai W, Nakashima K, Taga T (2003) Enhanced gene activation by Notch and BMP signaling cross-talk. Nucl Acids Res 31: 5723–5731.
[79]  Besse F, de Quinto SL, Marchand V, Trucco A, Ephrussi A (2009) Drosophila PTB promotes formation of high-order RNP particles and represses oskar translation. Genes Dev 23: 195–207.
[80]  Lopez-Schier H, St. Johnston D (2001) Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev 15: 1393–405.
[81]  Torres IL, Lopez-Schier H, St. Johnston D (2003) A Notch/Delta-dependent relay mechanism establishes anterior-posterior polarity in Drosophila. Dev Cell 5: 547–558.
[82]  Roth S (2001) Drosophila oogenesis: Coordinating germ line and soma. Curr Bio 11: R779–781.
[83]  Song X, Call GB, Kirilly D, Xie T (2007) Notch signaling controls germline stem cell niche formation in the Drosophila ovary. Development 134: 1071–1080.
[84]  Ben-Yaacov S., Le Borgne R, Abramson I, Schweisguth F, Schejter ED (2001) Wasp, the Drosophila Wiskott-Aldrich syndrome gene homologue, is required for cell fate decisions mediated by Notch signaling. J Cell Biol 152, 1–13.
[85]  Selkoe D, Kopan R (2003) Notch and Presenilin: regulated intramembrane proteolysis links development and degeneration. Annu Rev Neurosci 26, 565–597.
[86]  Joutel A, Corpecho C, Ducros A, Vahedi K, Chabriat H, et al. (1996) Notch3 mutations in CADASIL, a hereditary adult-onset condition causing stroke and dementia. Nature 383: 707–710.
[87]  Pear WS, Aster JC (2004) T cell acute lymphoblastic leukemia/lymphoma: a human cancer commonly associated with aberrant NOTCH1 signaling. Curr Opin Hematol 11, 426–433.
[88]  Fischer DF, van Dijk R, Sluijs JA, Nair SM, Racchi M, et al. (2005) Activation of the Notch pathway in Down syndrome: cross-talk of Notch and APP. FASEB J 19: 1451–1458.
[89]  Beverly LJ, Felsher DW, Capobianco AJ (2005) Suppression of p53 by Notch in lymphomagenesis: implications for initiation and regression. Cancer Res 65: 7159–7168.
[90]  Ishikura N, Clever JL, Bouzamondo-Bernstein E, Samayoa E, Prusiner SB, et al. (2005) Notch-1 activation and dendritic atrophy in prion disease. Proc Natl Acad Sci U S A 102: 886–891.
[91]  Garg V, Muth AN, Ransom JF, Schluterman MK, Barnes, etal. (2005) Mutations in NOTCH1 cause aortic valve disease. Nature 437, 270–274.
[92]  Costa RM, Honjo T, Silva AJ (2003) Learning and memory deficits in Notch mutant mice. Curr Biol 13: 1348–1354.
[93]  Hertzog P (2008) A Notch in the Toll Belt. Immunity 29: 663–665.
[94]  Muir A, Greenspan DS (2011) Metalloproteinases in Drosophila to humans that are central players in developmental processes. J Biol Chem 286: 41905–41911.
[95]  Munger JS, Sheppard D (2011) Cross talk among TGF-β signaling pathways, integrins, and the extracellular matrix. Cold Sping Harb Perspect Biol 3: 1–17.
[96]  Moresco EM, LaVine D, Beutler B (2011) Toll-like receptors. Curr Biol 21: R488–R493.
[97]  Abdelsadik A, Trad A (2011) Toll-like receptors on the fork roads between innate and adaptive immunity. Hum Immunol 72: 1188–1193.
[98]  Dasu MR, Ramirez S, Isseroff RR (2012) Toll-like receptor and diabetes: a therapeutic perspective. Clin Sci 122: 203–214.
[99]  Okun E, Griffioen KJ, Mattson MP (2011) Toll-like receptor signaling in neuroal plasticity and disease. Trends Neurosci 34: 269–281.
[100]  Hanke ML, Kielian T (2011) Toll-like receptors in health and disease in the brain: mechanisms and therapeutic potential. Clin Sci 121: 367–387.
[101]  Bayat V, Jaiswal M, Bellen HJ (2011) The BMP signaling pathway at the Drosophila neuromuscular junction and its links to neurodegenerative diseases. Curr Opin Neurobiol 21: 182–188.
[102]  Suhir H, Etzioni A (2010) The role of Toll-like receptor signaling in human immunedeficiencies. Clin Rev Allergy Immunol 38: 11–19.
[103]  Tekeuchi O, Akira S (2010) Pattern recognition and inflammation. Cell 140: 805–820.
[104]  Vallejo JG (2011) Role of toll-like receptors in cardiovascular diseases. Clin Sci 121: 1–10.
[105]  Wang J, Greene SB, Martin JF (2011) BMP signaling in congenital heart disease: new developments and future directions. Birth Defects Res A Clin Mol Teratol 91: 441–448.
[106]  Ashburner M, Golic KG, Hawley RS (2004) Drosophila. A Laboratory Handbook. 2nd Edition. Cold Spring Harbor Laboratory Press, New York, USA, p.1409.
[107]  Sullivan W, Ashburner M, Hawley RS (2000) Drosophila Protocols. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, p.697.
[108]  Sambrook J, Russell D (2001) Molecular Cloning: A Laboratory Manual. 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
[109]  Harlow E, Lane D (1999). Using Antibodies: A laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.
[110]  Spector DL, Goldman RD, Leinwand LA (1998) Cells: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, USA.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133