Two different sources of Perlecan cooperate for its function in the basement membrane of the Drosophila wing imaginal disc.
HS chains
Perlecan-GFP
basement membrane biogenesis
isoforms
morphogenesis
organ shape
Journal
Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927
Informations de publication
Date de publication:
04 2021
04 2021
Historique:
revised:
16
11
2020
received:
26
05
2020
accepted:
16
11
2020
pubmed:
4
12
2020
medline:
3
3
2022
entrez:
3
12
2020
Statut:
ppublish
Résumé
The basement membrane (BM) provides mechanical shaping of tissues during morphogenesis. The Drosophila BM proteoglycan Perlecan is vital for this process in the wing imaginal disc. This function is thought to be fostered by the heparan sulfate chains attached to the domain I of vertebrate Perlecan. However, this domain is not present in Drosophila, and the source of Perlecan for the wing imaginal disc BM remains unclear. Here, we tackle these two issues. In silico analysis shows that Drosophila Perlecan holds a domain I. Moreover, by combining in situ hybridization of Perlecan mRNA and protein staining, together with tissue-specific Perlecan depletion, we find that there is an autonomous and a non-autonomous source for Perlecan deposition in the wing imaginal disc BM. We further show that both sources cooperate for correct distribution of Perlecan in the wing imaginal disc and morphogenesis of this tissue. These results show that Perlecan is fully conserved in Drosophila, providing a valuable in vivo model system to study its role in BM function. The existence of two different sources for Perlecan incorporation in the wing imaginal disc BM raises the possibility that inter-organ communication mediated at the level of the BM is involved in organogenesis.
Sections du résumé
BACKGROUND
The basement membrane (BM) provides mechanical shaping of tissues during morphogenesis. The Drosophila BM proteoglycan Perlecan is vital for this process in the wing imaginal disc. This function is thought to be fostered by the heparan sulfate chains attached to the domain I of vertebrate Perlecan. However, this domain is not present in Drosophila, and the source of Perlecan for the wing imaginal disc BM remains unclear. Here, we tackle these two issues.
RESULTS
In silico analysis shows that Drosophila Perlecan holds a domain I. Moreover, by combining in situ hybridization of Perlecan mRNA and protein staining, together with tissue-specific Perlecan depletion, we find that there is an autonomous and a non-autonomous source for Perlecan deposition in the wing imaginal disc BM. We further show that both sources cooperate for correct distribution of Perlecan in the wing imaginal disc and morphogenesis of this tissue.
CONCLUSIONS
These results show that Perlecan is fully conserved in Drosophila, providing a valuable in vivo model system to study its role in BM function. The existence of two different sources for Perlecan incorporation in the wing imaginal disc BM raises the possibility that inter-organ communication mediated at the level of the BM is involved in organogenesis.
Substances chimiques
Heparan Sulfate Proteoglycans
0
perlecan
143972-95-6
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
542-561Subventions
Organisme : NIH HHS
ID : P40 OD018537
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM084947
Pays : United States
Informations de copyright
© 2020 American Association of Anatomists.
Références
Sekiguchi R, Yamada KM. Basement membranes in development and disease. Curr Top Dev Biol. 2018;130:143-191. https://doi.org/10.1016/bs.ctdb.2018.02.005.
Ramos-Lewis W, Page-McCaw A. Basement membrane mechanics shape development: lessons from the fly. Matrix Biol. 2019;75-76:72-81. https://doi.org/10.1016/j.matbio.2018.04.004.
Skeath JB, Wilson BA, Romero SE, Snee MJ, Zhu Y, Lacin H. The extracellular metalloprotease AdamTS-A anchors neural lineages in place within and preserves the architecture of the central nervous system. Development. 2017;144(17):3102-3113. https://doi.org/10.1242/dev.145854.
Srivastava A, Pastor-Pareja JC, Igaki T, Pagliarini R, Xu T. Basement membrane remodeling is essential for drosophila disc eversion and tumor invasion. Proc Natl Acad Sci U S A. 2007;104(8):2721-2726. https://doi.org/10.1073/pnas.0611666104.
Sui L, Alt S, Weigert M, et al. Differential lateral and basal tension drive folding of drosophila wing discs through two distinct mechanisms. Nat Commun. 2018;9(1):4620. https://doi.org/10.1038/s41467-018-06497-3.
Isabella AJ, Horne-Badovinac S. Rab10-mediated secretion synergizes with tissue movement to build a polarized basement membrane architecture for organ morphogenesis. Dev Cell. 2016;38(1):47-60. https://doi.org/10.1016/j.devcel.2016.06.009.
Chlasta J, Milani P, Runel G, et al. Variations in basement membrane mechanics are linked to epithelial morphogenesis. Development. 2017;144(23):4350-4362. https://doi.org/10.1242/dev.152652.
Crest J, Diz-Muñoz A, Chen DY, Fletcher DA, Bilder D. Organ sculpting by patterned extracellular matrix stiffness. elife. 2017;6:e24958. https://doi.org/10.7554/eLife.24958.
Isabella AJ, Horne-Badovinac S. Dynamic regulation of basement membrane protein levels promotes egg chamber elongation in drosophila. Dev Biol. 2015;406(2):212-221. https://doi.org/10.1016/j.ydbio.2015.08.018.
Pastor-Pareja JC, Xu T. Shaping cells and organs in drosophila by opposing roles of fat body-secreted collagen IV and perlecan. Dev Cell. 2011;21(2):245-256. https://doi.org/10.1016/j.devcel.2011.06.026.
Pollard JW. Trophic macrophages in development and disease. Nat Rev Immunol. 2009;9(4):259-270. https://doi.org/10.1038/nri2528.
Sangaletti S, Di Carlo E, Gariboldi S, et al. Macrophage-derived SPARC bridges tumor cell-extracellular matrix interactions toward metastasis. Cancer Res. 2008;68(21):9050-9059. https://doi.org/10.1158/0008-5472.can-08-1327.
Schnoor M, Cullen P, Lorkowski J, et al. Production of type VI collagen by human macrophages: a new dimension in macrophage functional heterogeneity. J Immunol. 2008;180(8):5707-5719. https://doi.org/10.4049/jimmunol.180.8.5707.
Chang MY, Chan CK, Braun KR, et al. Monocyte-to-macrophage differentiation: synthesis and secretion of a complex extracellular matrix. J Biol Chem. 2012;287(17):14122-14135. https://doi.org/10.1074/jbc.M111.324988.
Zigmond E, Samia-Grinberg S, Pasmanik-Chor M, et al. Infiltrating monocyte-derived macrophages and resident kupffer cells display different ontogeny and functions in acute liver injury. J Immunol. 2014;193(1):344-353. https://doi.org/10.4049/jimmunol.1400574.
Afik R, Zigmond E, Vugman M, et al. Tumor macrophages are pivotal constructors of tumor collagenous matrix. J Exp Med. 2016;213(11):2315-2331. https://doi.org/10.1084/jem.20151193.
Matsubayashi Y, Louani A, Dragu A, et al. A moving source of matrix components is essential for De novo basement membrane formation. Curr Biol. 2017;27(22):3526-3534.e4. https://doi.org/10.1016/j.cub.2017.10.001.
Wolfstetter G, Dahlitz I, Pfeifer K, et al. Characterization of Drosophila Nidogen/entactin reveals roles in basement membrane stability, barrier function and nervous system patterning. Development. 2019;146(2). https://doi.org/10.1242/dev.168948.
Dai J, Estrada B, Jacobs S, et al. Dissection of Nidogen function in drosophila reveals tissue-specific mechanisms of basement membrane assembly. PLoS Genet. 2018;14(9):e1007483. https://doi.org/10.1371/journal.pgen.1007483.
Zang Y, Wan M, Liu M, et al. Plasma membrane overgrowth causes fibrotic collagen accumulation and immune activation in drosophila adipocytes. Elife. 2015;4:e07187. https://doi.org/10.7554/eLife.07187.
Gubbiotti MA, Neill T, Iozzo RV. A current view of perlecan in physiology and pathology: a mosaic of functions. Matrix Biol. 2017;57-58:285-298. https://doi.org/10.1016/j.matbio.2016.09.003.
Dolan M, Horchar T, Rigatti B, Hassell JR. Identification of sites in domain I of perlecan that regulate heparan sulfate synthesis. J Biol Chem. 1997;272(7):4316-4322.
Costell M, Gustafsson E, Aszódi A, et al. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol. 1999;147(5):1109-1122.
Arikawa-Hirasawa E, Watanabe H, Takami H, Hassell JR, Yamada Y. Perlecan is essential for cartilage and cephalic development. Nat Genet. 1999;23(3):354-358. https://doi.org/10.1038/15537.
Zoeller JJ, McQuillan A, Whitelock J, Ho SY, Iozzo RV. A central function for perlecan in skeletal muscle and cardiovascular development. J Cell Biol. 2008;181(2):381-394. https://doi.org/10.1083/jcb.200708022.
Olsen BR. Life without perlecan has its problems. J Cell Biol. 1999;147(5):909-912. https://doi.org/10.1083/jcb.147.5.909.
Rossi M, Morita H, Sormunen R, et al. Heparan sulfate chains of perlecan are indispensable in the lens capsule but not in the kidney. EMBO J. 2003;22(2):236-245. https://doi.org/10.1093/emboj/cdg019.
Meyer F, Moussian B. Drosophila multiplexin (Dmp) modulates motor axon pathfinding accuracy. Develop Growth Differ. 2009;51(5):483-498. https://doi.org/10.1111/j.1440-169X.2009.01111.x.
Momota R, Naito I, Ninomiya Y, Ohtsuka A. Drosophila type XV/XVIII collagen, Mp, is involved in wingless distribution. Matrix Biol. 2011;30(4):258-266. https://doi.org/10.1016/j.matbio.2011.03.008.
Harpaz N, Ordan E, Ocorr K, Bodmer R, Volk T. Multiplexin promotes heart but not aorta morphogenesis by polarized enhancement of slit/robo activity at the heart lumen. PLoS Genet. 2013;9(6):e1003597. https://doi.org/10.1371/journal.pgen.1003597.
Lerner DW, McCoy D, Isabella AJ, et al. A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell. 2013;24(2):159-168. https://doi.org/10.1016/j.devcel.2012.12.005.
Schneider M, Khalil AA, Poulton J, et al. Perlecan and Dystroglycan act at the basal side of the drosophila follicular epithelium to maintain epithelial organization. Development. 2006;133(19):3805-3815. https://doi.org/10.1242/dev.02549.
Voigt A, Pflanz R, Schäfer U, Jäckle H. Perlecan participates in proliferation activation of quiescent drosophila neuroblasts. Dev Dyn. 2002;224(4):403-412. https://doi.org/10.1002/dvdy.10120.
Farach-Carson MC, Warren CR, Harrington DA, Carson DD. Border patrol: insights into the unique role of perlecan/heparan sulfate proteoglycan 2 at cell and tissue borders. Matrix Biol. 2014;34:64-79. https://doi.org/10.1016/j.matbio.2013.08.004.
Morita H, Yoshimura A, Inui K, et al. Heparan sulfate of perlecan is involved in glomerular filtration. J Am Soc Nephrol. 2005;16(6):1703-1710. https://doi.org/10.1681/ASN.2004050387.
Friedrich MV, Schneider M, Timpl R, Baumgartner S. Perlecan domain V of Drosophila melanogaster. Sequence, recombinant analysis and tissue expression. Eur J Biochem. 2000;267(11):3149-3159.
Park Y, Rangel C, Reynolds MM, et al. Drosophila perlecan modulates FGF and hedgehog signals to activate neural stem cell division. Dev Biol. 2003;253(2):247-257.
Herranz H, Weng R, Cohen SM. Crosstalk between epithelial and mesenchymal tissues in tumorigenesis and imaginal disc development. Curr Biol. 2014;24(13):1476-1484. https://doi.org/10.1016/j.cub.2014.05.043.
Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Léopold P. A nutrient sensor mechanism controls drosophila growth. Cell. 2003;114(6):739-749. https://doi.org/10.1016/s0092-8674(03)00713-x.
Besse F, Mertel S, Kittel RJ, et al. The Ig cell adhesion molecule Basigin controls compartmentalization and vesicle release at Drosophila melanogaster synapses. J Cell Biol. 2007;177(5):843-855. https://doi.org/10.1083/jcb.200701111.
Pédelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS. Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol. 2006;24(1):79-88. https://doi.org/10.1038/nbt1172.
Esko JD, Zhang L. Influence of core protein sequence on glycosaminoglycan assembly. Curr Opin Struct Biol. 1996;6(5):663-670.
Merz DC, Alves G, Kawano T, Zheng H, Culotti JG. UNC-52/perlecan affects gonadal leader cell migrations in C. elegans hermaphrodites through alterations in growth factor signaling. Dev Biol. 2003;256(1):173-186.
Celestrin K, Díaz-Balzac CA, Tang LTH, Ackley BD, Bülow HE. Four specific immunoglobulin domains in UNC-52/Perlecan function with NID-1/Nidogen during dendrite morphogenesis in Caenorhabditis elegans. Development. 2018;145(10). https://doi.org/10.1242/dev.158881.
Mullen GP, Rogalski TM, Bush JA, Gorji PR, Moerman DG. Complex patterns of alternative splicing mediate the spatial and temporal distribution of perlecan/UNC-52 in Caenorhabditis elegans. Mol Biol Cell. 1999;10(10):3205-3221. https://doi.org/10.1091/mbc.10.10.3205.
Warren CR, Kassir E, Spurlin J, Martinez J, Putnam NH, Farach-Carson MC. Evolution of the perlecan/HSPG2 gene and its activation in regenerating Nematostella vectensis. PLoS One. 2015;10(4):e0124578. https://doi.org/10.1371/journal.pone.0124578.
Kusche-Gullberg M, Garrison K, MacKrell AJ, Fessler LI, Fessler JH. Laminin a chain: expression during drosophila development and genomic sequence. EMBO J. 1992;11(12):4519-4527.
Yurchenco PD, Patton BL. Developmental and pathogenic mechanisms of basement membrane assembly. Curr Pharm Des. 2009;15(12):1277-1294.
Momota R, Narasaki M, Komiyama T, Naito I, Ninomiya Y, Ohtsuka A. Drosophila type XV/XVIII collagen mutants manifest integrin mediated mitochondrial dysfunction, which is improved by cyclosporin a and losartan. Int J Biochem Cell Biol. 2013;45(5):1003-1011. https://doi.org/10.1016/j.biocel.2013.02.001.
Van De Bor V, Zimniak G, Papone L, et al. Companion blood cells control ovarian stem cell niche microenvironment and homeostasis. Cell Rep. 2015;13(3):546-560. https://doi.org/10.1016/j.celrep.2015.09.008.
Xu T, Rubin GM. Analysis of genetic mosaics in developing and adult drosophila tissues. Development. 1993;117(4):1223-1237.
Brankatschk M, Eaton S. Lipoprotein particles cross the blood-brain barrier in drosophila. J Neurosci. 2010;30(31):10441-10447. https://doi.org/10.1523/JNEUROSCI.5943-09.2010.
Asha H, Nagy I, Kovacs G, Stetson D, Ando I, Dearolf CR. Analysis of Ras-induced overproliferation in drosophila hemocytes. Genetics. 2003;163(1):203-215.
Lehner CF, O'Farrell PH. The roles of drosophila cyclins A and B in mitotic control. Cell. 1990;61(3):535-547.