The proteoglycan Trol controls the architecture of the extracellular matrix and balances proliferation and differentiation of blood progenitors in the Drosophila lymph gland

Developmental Biology

Volumn 384, Issue 2, 2013, Pages 301-312

  Grigorian, Melina ^a   Liu, Ting ^a   Banerjee, Utpal ^a   Hartenstein, Volker ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Drosophila; Extracellular matrix; Hedgehog; Hematopoiesis; Lymph gland; Perlecan

Indexed keywords

PERLECAN; SONIC HEDGEHOG PROTEIN;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BLOOD CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EXTRACELLULAR MATRIX; GENE LOSS; GENE OVEREXPRESSION; HEMATOPOIESIS; LYMPH NODE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; ERINACEIDAE; VERTEBRATA;

EID: 84887606692     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.03.007     Document Type: Article

References (71)

1. Arikawa-Hirasawa E., Watanabe H., Takami H., Hassell J.R., Yamada Y. Perlecan is essential for cartilage and cephalic development. Nat. Genet. 1999, 23:354-358.
2. Asha H., Nagy I., Kovacs G., Stetson D., Ando I., Dearolf C.R. Analysis of Ras-induced overproliferation in Drosophila hemocytes. Genetics 2003, 163:203-215.
3. Ashburner M. Drosophila. A Laboratory Manual 1989, Cold Spring Harbor Laboratory Press, New York.
4. Bellaiche Y., The I., Perrimon N. Tout-velu is a Drosophila homologue of the putative tumour suppressor EXT-1 and is needed for Hh diffusion. Nature 1998, 394:85-88.
5. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 1999, 68:729-777.
6. Bruckner K., Kockel L., Duchek P., Luque C.M., Rorth P., Perrimon N. The PDGF/VEGF receptor controls blood cell survival in Drosophila. Dev. Cell. 2004, 7:73-84.
7. Caldwell M.C., Datta S. Expression of cyclin E or DP/E2F rescues the G1 arrest of trol mutant neuroblasts in the Drosophila larval central nervous system. Mech. Dev. 1998, 79:121-130.
8. Callejo A., Torroja C., Quijada L., Guerrero I. Hedgehog lipid modifications are required for Hedgehog stabilization in the extracellular matrix. Development 2006, 133:471-483.
9. Costell M., Gustafsson E., Aszodi A., Morgelin M., Bloch W., Hunziker E., Addicks K., Timpl R., Fassler R. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell Biol. 1999, 147:1109-1122.
10. Crozatier M., Meister M. Drosophila haematopoiesis. Cell Microbiol. 2007, 9:1117-1126.
11. Datta S. Control of proliferation activation in quiescent neuroblasts of the Drosophila central nervous system. Development 1995, 121:1173-1182.
12. Datta S., Kankel D.R. l(1)trol and l(1)devl, loci affecting the development of the adult central nervous system in Drosophila melanogaster. Genetics 1992, 130:523-537.
13. Dragojlovick-Munther, M., Martinez-Agosto, J., Extracellular matrix-modulated FGF signaling in Drosophila blood progenitors regulates their differentiation via a ras/ETS/FOG pathway and TORC1 function. Dev. Biol. , this issue. http://dx.doi.org/10.1016/j.ydbio.2013.04.004.
14. Durbeej M. Laminins. Cell Tissue Res. 2010, 339:259-268.
15. Emerald B.S., Cohen S.M. Spatial and temporal regulation of the homeotic selector gene Antennapedia is required for the establishment of leg identity in Drosophila. Dev. Biol. 2004, 267:462-472.
16. Esko J.D., Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 2002, 71:435-471.
17. Fessler L.I., Campbell A.G., Duncan K.G., Fessler J.H. Drosophila laminin: characterization and localization. J. Cell Biol. 1987, 105:2383-2391.
18. Friedrich M.V., Gohring W., Morgelin M., Brancaccio A., David G., Timpl R. Structural basis of glycosaminoglycan modification and of heterotypic interactions of perlecan domain V. J. Mol. Biol. 1999, 294:259-270.
19. Friedrich M.V., Schneider M., Timpl R., Baumgartner S. Perlecan domain V of Drosophila melanogaster. Sequence, recombinant analysis and tissue expression. Eur. J. Biochem. 2000, 267:3149-3159.
20. Fuki I.V., Iozzo R.V., Williams K.J. Perlecan heparan sulfate proteoglycan: a novel receptor that mediates a distinct pathway for ligand catabolism. J. Biol. Chem. 2000, 275:25742-25750.
21. Gallet A., Ruel L., Staccini-Lavenant L., Therond P.P. Cholesterol modification is necessary for controlled planar long-range activity of Hedgehog in Drosophila epithelia. Development 2006, 133:407-418.
22. Ghiglione C., Devergne O., Georgenthum E., Carballes F., Medioni C., Cerezo D., Noselli S. The Drosophila cytokine receptor Domeless controls border cell migration and epithelial polarization during oogenesis. Development 2002, 129:5437-5447.
23. Grigorian M., Mandal L., Hartenstein V. Hematopoiesis at the onset of metamorphosis: terminal differentiation and dissociation of the Drosophila lymph gland. Dev. Genes. Evol. 2011, 221:121-131.
24. Grigorian M., Hartenstein V. Hematopoiesis and hematopoietic organs in arthropods. Dev. Genes Evol. 2013, 223:103-115.
25. Han C., Belenkaya T.Y., Wang B., Lin X. Drosophila glypicans control the cell-to-cell movement of Hedgehog by a dynamin-independent process. Development 2004, 131:601-611.
26. Hassell J., Yamada Y., Arikawa-Hirasawa E. Role of perlecan in skeletal development and diseases. Glycoconjugate J. 2002, 19:263-267.
27. Henry M.D., Satz J.S., Brakebusch C., Costell M., Gustafsson E., Fassler R., Campbell K.P. Distinct roles for dystroglycan, beta1 integrin and perlecan in cell surface laminin organization. J. Cell Sci. 2001, 114:1137-1144.
28. Hoffmann J., Zachary D., Hoffmann D., Brehelin M. Postembryonic development and differentiation: hematopoietic tissues and their functions in some insects. Insect Hemocytes 1979, 29-82. Cambridge University Press, London. A. Gupta (Ed.).
29. Ingham P.W. Localized hedgehog activity controls spatial limits of wingless transcription in the Drosophila embryo. Nature 1993, 366:560-562.
30. Iozzo R.V. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell Biol. 2005, 6:646-656.
31. Jung S.H., Evans C.J., Uemura C., Banerjee U. The Drosophila lymph gland as a developmental model of hematopoiesis. Development 2005, 132:2521-2533.
32. Kelso R.J., Buszczak M., Quinones A.T., Castiblanco C., Mazzalupo S., Cooley L. Flytrap, a database documenting a GFP protein-trap insertion screen in Drosophila melanogaster. Nucleic Acids Res. 2004, 32:D418-D420.
33. Klein G., Conzelmann S., Beck S., Timpl R., Muller C.A. Perlecan in human bone marrow: a growth-factor-presenting, but anti-adhesive, extracellular matrix component for hematopoietic cells. Matrix Biol. 1995, 14:457-465.
34. Knibiehler B., Mirre C., Cecchini J., Le Parco Y. Haemocytes accumulate collagen transcripts during Drosophila melanogaster metamorphosis. Roux's Arch. Dev. Biol. 1987, 196:243-247.
35. Korpos E., Wu C., Song J., Hallmann R., Sorokin L. Role of the extracellular matrix in lymphocyte migration. Cell Tissue Res. 2010, 339:47-57.
36. Kurucz E., Markus R., Zsamboki J., Folkl-Medzihradszky K., Darula Z., Vilmos P., Udvardy A., Krausz I., Lukacsovich T., Gateff E., Zettervall C.J., Hultmark D., Ando I. Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 2007, 17:649-654.
37. Kusche-Gullberg M., Garrison K., MacKrell A.J., Fessler L.I., Fessler J.H. Laminin A chain: expression during Drosophila development and genomic sequence. EMBO J. 1992, 11:4519-4527.
38. Kvist A.J., Johnson A.E., Morgelin M., Gustafsson E., Bengtsson E., Lindblom K., Aszodi A., Fassler R., Sasaki T., Timpl R., Aspberg A. Chondroitin sulfate perlecan enhances collagen fibril formation. Implications for perlecan chondrodysplasias. J. Biol. Chem. 2006, 281:33127-33139.
39. Lanot R., Zachary D., Holder F., Meister M. Postembryonic hematopoiesis in Drosophila. Dev. Biol. 2001, 230:243-257.
40. Laurila P., Leivo I. Basement membrane and interstitial matrix components form separate matrices in heterokaryons of PYS-2 cells and fibroblasts. J. Cell Sci. 1993, 104(Pt 1):59-68.
41. Lin X. Functions of heparan sulfate proteoglycans in cell signaling during development. Development 2004, 131:6009-6021.
42. Lin X., Perrimon N. Developmental roles of heparan sulfate proteoglycans in Drosophila. Glycoconjugate J. 2002, 19:363-368.
43. Lindner J.R., Hillman P.R., Barrett A.L., Jackson M.C., Perry T.L., Park Y., Datta S. The Drosophila Perlecan gene trol regulates multiple signaling pathways in different developmental contexts. BMC. Dev. Biol. 2007, 7:121.
44. Lunstrum G.P., Bachinger H.P., Fessler L.I., Duncan K.G., Nelson R.E., Fessler J.H. Drosophila basement membrane procollagen IV. I. Protein characterization and distribution. J. Biol. Chem. 1988, 263:18318-18327.
45. Makhijani K., Alexander B., Tanaka T., Rulifson E., Bruckner K. The peripheral nervous system supports blood cell homing and survival in the Drosophila larva. Development 2011, 138:5379-5391.
46. Mandal L., Martinez-Agosto J.A., Evans C.J., Hartenstein V., Banerjee U. A Hedgehog- and Antennapedia-dependent niche maintains Drosophila haematopoietic precursors. Nature 2007, 446:320-324.
47. Martinez-Agosto J.A., Mikkola H.K., Hartenstein V., Banerjee U. The hematopoietic stem cell and its niche: a comparative view. Genes Dev. 2007, 21:3044-3060.
48. Medioni C., Noselli S. Dynamics of the basement membrane in invasive epithelial clusters in Drosophila. Development 2005, 132:3069-3077.
49. Melrose J., Hayes A.J., Whitelock J.M., Little C.B. Perlecan, the jack of all trades proteoglycan of cartilaginous weight-bearing connective tissues. Bioessays 2008, 30:457-469.
50. Mondal B.C., Mukherjee T., Mandal L., Evans C.J., Sinenko S.A., Martinez-Agosto J.A., Banerjee U. Interaction between differentiating cell- and niche-derived signals in hematopoietic progenitor maintenance. Cell 2011, 147:1589-1600.
51. Muller H.M., Dimopoulos G., Blass C., Kafatos F.C. A hemocyte-like cell line established from the malaria vector Anopheles gambiae expresses six prophenoloxidase genes. J. Biol. Chem. 1999, 274:11727-11735.
52. Murdoch A.D., Dodge G.R., Cohen I., Tuan R.S., Iozzo R.V. Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Biol. Chem. 1992, 267:8544-8557.
53. Murray M.A., Fessler L.I., Palka J. Changing distributions of extracellular matrix components during early wing morphogenesis in Drosophila. Dev. Biol. 1995, 168:150-165.
54. Nardi J.B., Pilas B., Ujhelyi E., Garsha K., Kanost M.R. Hematopoietic organs of Manduca sexta and hemocyte lineages. Dev. Genes Evol. 2003, 213:477-491.
55. Nelson R.E., Fessler L.I., Takagi Y., Blumberg B., Keene D.R., Olson P.F., Parker C.G., Fessler J.H. Peroxidasin: a novel enzyme-matrix protein of Drosophila development. EMBO J. 1994, 13:3438-3447.
56. Nybakken K., Perrimon N. Heparan sulfate proteoglycan modulation of developmental signaling in Drosophila. Biochim. Biophys. Acta 2002, 1573:280-291.
57. Park Y., Fujioka M., Kobayashi M., Jaynes J.B., Datta S. even skipped is required to produce a trans-acting signal for larval neuroblast proliferation that can be mimicked by ecdysone. Development 2001, 128:1899-1909.
58. Park Y., Rangel C., Reynolds M.M., Caldwell M.C., Johns M., Nayak M., Welsh C.J., McDermott S., Datta S. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev. Biol. 2003, 253:247-257.
59. Pastor-Pareja J.C., Xu T. Shaping cells and organs in drosophila by opposing roles of fat body-secreted collagen iv and perlecan. Dev. Cell 2011, 21:245-256.
60. Rogalski T.M., Mullen G.P., Bush J.A., Gilchrist E.J., Moerman D.G. UNC-52/perlecan isoform diversity and function in Caenorhabditis elegans. Biochem. Soc. Trans. 2001, 29:171-176.
61. Sabeh F., Ota I., Holmbeck K., Birkedal-Hansen H., Soloway P., Balbin M., Lopez-Otin C., Shapiro S., Inada M., Krane S., Allen E., Chung D., Weiss S.J. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J. Cell Biol. 2004, 167:769-781.
62. Sasse P., Malan D., Fleischmann M., Roell W., Gustafsson E., Bostani T., Fan Y., Kolbe T., Breitbach M., Addicks K., Welz A., Brem G., Hescheler J., Aszodi A., Costell M., Bloch W., Fleischmann B.K. Perlecan is critical for heart stability. Cardiovasc. Res. 2008, 80:435-444.
63. Segev A., Nili N., Strauss B.H. The role of perlecan in arterial injury and angiogenesis. Cardiovasc. Res. 2004, 63:603-610.
64. Sinenko S.A., Mandal L., Martinez-Agosto J.A., Banerjee U. Dual role of wingless signaling in stem-like hematopoietic precursor maintenance in Drosophila. Dev. Cell. 2009, 16:756-763.
65. Subramanian A., Wayburn B., Bunch T., Volk T. Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development 2007, 134:1269-1278.
66. Urbano J.M., Torgler C.N., Molnar C., Tepass U., Lopez-Varea A., Brown N.H., de Celis J.F., Martin-Bermudo M.D. Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis. Development 2009, 136:4165-4176.
67. Ward E.J., Skeath J.B. Characterization of a novel subset of cardiac cells and their progenitors in the Drosophila embryo. Development 2000, 127:4959-4969.
68. Whitelock J.M., Melrose J., Iozzo R.V. Diverse cell signaling events modulated by perlecan. Biochemistry 2008, 47:11174-11183.
69. Yan D., Lin X. Shaping morphogen gradients by proteoglycans. Cold Spring Harb. Perspect. Biol. 2009, 1:a002493.
70. Yurchenco P.D., Amenta P.S., Patton B.L. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 2004, 22:521-538.
71. Zoeller J.J., McQuillan A., Whitelock J., Ho S.Y., Iozzo R.V. A central function for perlecan in skeletal muscle and cardiovascular development. J. Cell Biol. 2008, 181:381-394.