A Novel Tissue in an Established Model System: the Drosophila Pupal Midgut

Overview

Journal Dev Genes Evol

Specialty Biology

Date 2011 May 11

PMID 21556856

Citations 27

Authors

Shigeo Takashima

Amelia Younossi-Hartenstein

Paola A Ortiz

Volker Hartenstein

Affiliations

Soon will be listed here.

Abstract

The Drosophila larval and adult midguts are derived from two populations of endodermal progenitors that separate from each other in the early embryo. As larval midgut cells differentiate into an epithelial layer, adult midgut progenitors (AMPs) remain as small clusters of proliferating, undifferentiated cells attached to the basal surface of the larval gut epithelium. During the first few hours of metamorphosis, AMPs merge into a continuous epithelial tube that overgrows the larval layer and differentiates into the adult midgut; at the same time, the larval midgut degenerates. As shown in this paper, there is a second, transient pupal midgut that develops from the AMPs at the beginning of metamorphosis and that intercalates between the adult and larval midgut epithelia. Cells of the transient pupal midgut form a multilayered tube that exhibits signs of differentiation, in the form of septate junctions and rudimentary apical microvilli. Some cells of the pupal midgut develop as endocrine cells. The pupal midgut remains closely attached to the degenerating larval midgut cells. Along with these cells, pupal midgut cells are sequestered into the lumen where they form the compact "yellow body." The formation of a pupal midgut has been reported from several other species and may represent a general feature of intestinal metamorphosis in insects.

Citing Articles

Microbiome composition and turnover in the face of complex lifecycles and bottlenecks: insights through the study of dung beetles.

Jones J, Newton I, Moczek A Appl Environ Microbiol. 2024; 91(1):e0127824.

PMID: 39704535 PMC: 11784073. DOI: 10.1128/aem.01278-24.

The emergence of circadian timekeeping in the intestine.

Parasram K, Zuccato A, Shin M, Willms R, Deveale B, Foley E Nat Commun. 2024; 15(1):1788.

PMID: 38413599 PMC: 10899604. DOI: 10.1038/s41467-024-45942-4.

Understanding Developmental Cell Death Using as a Model System.

Umargamwala R, Manning J, Dorstyn L, Denton D, Kumar S Cells. 2024; 13(4.

PMID: 38391960 PMC: 10886741. DOI: 10.3390/cells13040347.

Characterization of genetic and molecular tools for studying the endogenous expression of Lactate dehydrogenase in Drosophila melanogaster.

Rai M, Carter S, Shefali S, Chawla G, Tennessen J PLoS One. 2024; 19(1):e0287865.

PMID: 38170735 PMC: 10763966. DOI: 10.1371/journal.pone.0287865.

Gut barrier defects, intestinal immune hyperactivation and enhanced lipid catabolism drive lethality in NGLY1-deficient Drosophila.

Pandey A, Galeone A, Han S, Story B, Consonni G, Mueller W Nat Commun. 2023; 14(1):5667.

PMID: 37704604 PMC: 10499810. DOI: 10.1038/s41467-023-40910-w.

References

Jirikowski G, Kreissl S, Richter S, Wolff C . Muscle development in the marbled crayfish--insights from an emerging model organism (Crustacea, Malacostraca, Decapoda). Dev Genes Evol. 2010; 220(3-4):89-105. DOI: 10.1007/s00427-010-0331-7. View

Denton D, Shravage B, Simin R, Baehrecke E, Kumar S . Larval midgut destruction in Drosophila: not dependent on caspases but suppressed by the loss of autophagy. Autophagy. 2009; 6(1):163-5. PMC: 2819273. DOI: 10.4161/auto.6.1.10601. View

Krajniak K, Greenberg M . The localization of FMRFamide in the nervous and somatic tissues of Nereis virens and its effects upon the isolated esophagus. Comp Biochem Physiol C Comp Pharmacol Toxicol. 1992; 101(1):93-100. DOI: 10.1016/0742-8413(92)90205-l. View

Andries J . Junctional structures in the metamorphosing midgut of Aeshna cyanea (Insecta, Odonata). Cell Tissue Res. 1979; 202(1):9-15. DOI: 10.1007/BF00239216. View

Mathur D, Bost A, Driver I, Ohlstein B . A transient niche regulates the specification of Drosophila intestinal stem cells. Science. 2010; 327(5962):210-3. PMC: 2857772. DOI: 10.1126/science.1181958. View

Denton D, Shravage B, Simin R, Mills K, Berry D, Baehrecke E . Autophagy, not apoptosis, is essential for midgut cell death in Drosophila. Curr Biol. 2009; 19(20):1741-6. PMC: 2783269. DOI: 10.1016/j.cub.2009.08.042. View

Satake H, Kawada T . Overview of the primary structure, tissue-distribution, and functions of tachykinins and their receptors. Curr Drug Targets. 2006; 7(8):963-74. DOI: 10.2174/138945006778019273. View

Affolter M, Walldorf U, Kloter U, Schier A, Gehring W . Regional repression of a Drosophila POU box gene in the endoderm involves inductive interactions between germ layers. Development. 1993; 117(4):1199-210. DOI: 10.1242/dev.117.4.1199. View

Yeo S, Lloyd A, Kozak K, Dinh A, Dick T, Yang X . On the functional overlap between two Drosophila POU homeo domain genes and the cell fate specification of a CNS neural precursor. Genes Dev. 1995; 9(10):1223-36. DOI: 10.1101/gad.9.10.1223. View

10.

Ohlstein B, Spradling A . The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature. 2005; 439(7075):470-4. DOI: 10.1038/nature04333. View

11.

Jiang H, Edgar B . EGFR signaling regulates the proliferation of Drosophila adult midgut progenitors. Development. 2009; 136(3):483-93. PMC: 2687592. DOI: 10.1242/dev.026955. View

12.

Uwo M, Ui-Tei K, Park P, Takeda M . Replacement of midgut epithelium in the greater wax moth, Galleria mellonela, during larval-pupal moult. Cell Tissue Res. 2002; 308(2):319-31. DOI: 10.1007/s00441-002-0515-1. View

13.

Hartenstein V, Jan Y . Studying Drosophila embryogenesis with P-lacZ enhancer trap lines. Rouxs Arch Dev Biol. 2017; 201(4):194-220. DOI: 10.1007/BF00188752. View

14.

Takashima S, Adams K, Ortiz P, Ying C, Moridzadeh R, Younossi-Hartenstein A . Development of the Drosophila entero-endocrine lineage and its specification by the Notch signaling pathway. Dev Biol. 2011; 353(2):161-72. PMC: 3873147. DOI: 10.1016/j.ydbio.2011.01.039. View

15.

Bach E, Ekas L, Ayala-Camargo A, Flaherty M, Lee H, Perrimon N . GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr Patterns. 2006; 7(3):323-31. DOI: 10.1016/j.modgep.2006.08.003. View

16.

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(3):121-31. PMC: 4278756. DOI: 10.1007/s00427-011-0364-6. View

17.

Woods D, Bryant P . Apical junctions and cell signalling in epithelia. J Cell Sci Suppl. 1993; 17:171-81. DOI: 10.1242/jcs.1993.supplement_17.25. View

18.

Tepass U, Haag T, Omatyar L, Torok T, Hartenstein V . shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 1996; 10(6):672-85. DOI: 10.1101/gad.10.6.672. View

19.

Noirot-Timothee C, Noirot C . Septate and scalariform junctions in arthropods. Int Rev Cytol. 2010; 63:97-140. DOI: 10.1016/s0074-7696(08)61758-1. View

20.

Baldwin K, Hakim R . Change of form of septate and gap junctions during development of the insect midgut. Tissue Cell. 1987; 19(4):549-58. DOI: 10.1016/0040-8166(87)90047-4. View