The Origin of Islet-like Cells in Drosophila Identifies Parallels to the Vertebrate Endocrine Axis

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2007 Dec 7

PMID 18056636

Citations 46

Authors

Shu Wang

Natalia Tulina

Daniel L Carlin

Eric J Rulifson

Affiliations

Soon will be listed here.

Abstract

Single-cell resolution lineage information is a critical key to understanding how the states of gene regulatory networks respond to cell interactions and thereby establish distinct cell fates. Here, we identify a single pair of neural stem cells (neuroblasts) as progenitors of the brain insulin-producing neurosecretory cells of Drosophila, which are homologous to islet beta cells. Likewise, we identify a second pair of neuroblasts as progenitors of the neurosecretory Corpora cardiaca cells, which are homologous to the glucagon-secreting islet alpha cells. We find that both progenitors originate as neighboring cells from anterior neuroectoderm, which expresses genes orthologous to those expressed in the vertebrate adenohypophyseal placode, the source of endocrine anterior pituitary and neurosecretory hypothalamic cells [Whitlock KE (2005) Trends Endocrinol Metab 16:145-151]. This ontogenic-molecular concordance suggests that a rudimentary brain endocrine axis was present in the common ancestor of humans and flies, where it orchestrated the islet-like endocrine functions of insulin and glucagon biology.

Citing Articles

Genome-wide analysis identifies Homothorax and Extradenticle as regulators of insulin in Drosophila Insulin-Producing cells.

Winant M, Buhler K, Clements J, De Groef S, Hens K, Vulsteke V PLoS Genet. 2022; 18(9):e1010380.

PMID: 36095003 PMC: 9499297. DOI: 10.1371/journal.pgen.1010380.

Nutrient Sensing via Gut in .

Chopra G, Kaushik S, Kain P Int J Mol Sci. 2022; 23(5).

PMID: 35269834 PMC: 8910450. DOI: 10.3390/ijms23052694.

The gut hormone Allatostatin C/Somatostatin regulates food intake and metabolic homeostasis under nutrient stress.

Kubrak O, Koyama T, Ahrentlov N, Jensen L, Malita A, Naseem M Nat Commun. 2022; 13(1):692.

PMID: 35121731 PMC: 8816919. DOI: 10.1038/s41467-022-28268-x.

New resources for the Drosophila 4th chromosome: FRT101F enabled mitotic clones and Bloom syndrome helicase enabled meiotic recombination.

Goldsmith S, Shimell M, Tauscher P, Daly S, Shimmi O, OConnor M G3 (Bethesda). 2022; 12(4).

PMID: 35084488 PMC: 8982423. DOI: 10.1093/g3journal/jkac019.

The Glucagon-Like Adipokinetic Hormone in - Biosynthesis and Secretion.

Hughson B Front Physiol. 2022; 12:710652.

PMID: 35002748 PMC: 8733639. DOI: 10.3389/fphys.2021.710652.

References

Sander M, German M . The beta cell transcription factors and development of the pancreas. J Mol Med (Berl). 1997; 75(5):327-40. DOI: 10.1007/s001090050118. View

Whitlock K . Origin and development of GnRH neurons. Trends Endocrinol Metab. 2005; 16(4):145-51. DOI: 10.1016/j.tem.2005.03.005. View

Urbach R, Schnabel R, Technau G . The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development. 2003; 130(16):3589-606. DOI: 10.1242/dev.00528. View

Ochoa-Espinosa A, Yucel G, Kaplan L, Pare A, Pura N, Oberstein A . The role of binding site cluster strength in Bicoid-dependent patterning in Drosophila. Proc Natl Acad Sci U S A. 2005; 102(14):4960-5. PMC: 555997. DOI: 10.1073/pnas.0500373102. View

Skeath J, Thor S . Genetic control of Drosophila nerve cord development. Curr Opin Neurobiol. 2003; 13(1):8-15. DOI: 10.1016/s0959-4388(03)00007-2. View

Tatar M, Bartke A, Antebi A . The endocrine regulation of aging by insulin-like signals. Science. 2003; 299(5611):1346-51. DOI: 10.1126/science.1081447. View

Li X, Oghi K, Zhang J, Krones A, Bush K, Glass C . Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis. Nature. 2003; 426(6964):247-54. DOI: 10.1038/nature02083. View

Copenhaver P, Taghert P . Origins of the insect enteric nervous system: differentiation of the enteric ganglia from a neurogenic epithelium. Development. 1991; 113(4):1115-32. DOI: 10.1242/dev.113.4.1115. View

Rulifson E, Kim S, Nusse R . Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science. 2002; 296(5570):1118-20. DOI: 10.1126/science.1070058. View

10.

de Velasco B, Shen J, Go S, Hartenstein V . Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Dev Biol. 2004; 274(2):280-94. DOI: 10.1016/j.ydbio.2004.07.015. View

11.

Martinez C, Rodriguez A, Jimenez F . Distribution and function of the lethal of scute gene product during early neurogenesis in Drosophila. Development. 1991; 113(2):445-54. DOI: 10.1242/dev.113.2.445. View

12.

Casso D, Kornberg T . GFP-tagged balancer chromosomes for Drosophila melanogaster. Mech Dev. 2000; 91(1-2):451-4. DOI: 10.1016/s0925-4773(00)00248-3. View

13.

de Velasco B, Mandal L, Mkrtchyan M, Hartenstein V . Subdivision and developmental fate of the head mesoderm in Drosophila melanogaster. Dev Genes Evol. 2005; 216(1):39-51. DOI: 10.1007/s00427-005-0029-4. View

14.

Urbach R, Technau G . Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development. 2003; 130(16):3621-37. DOI: 10.1242/dev.00533. View

15.

Seo H, Curtiss J, Mlodzik M, Fjose A . Six class homeobox genes in drosophila belong to three distinct families and are involved in head development. Mech Dev. 1999; 83(1-2):127-39. DOI: 10.1016/s0925-4773(99)00045-3. View

16.

Weigmann K, Cohen S . Lineage-tracing cells born in different domains along the PD axis of the developing Drosophila leg. Development. 1999; 126(17):3823-30. DOI: 10.1242/dev.126.17.3823. View

17.

Seo H, Drivenes , Ellingsen S, Fjose A . Expression of two zebrafish homologues of the murine Six3 gene demarcates the initial eye primordia. Mech Dev. 1998; 73(1):45-57. DOI: 10.1016/s0925-4773(98)00028-8. View

18.

Rulifson E, Wu C, Nusse R . Pathway specificity by the bifunctional receptor frizzled is determined by affinity for wingless. Mol Cell. 2000; 6(1):117-26. View

19.

Falkmer S . Phylogeny and ontogeny of the neuroendocrine cells of the gastrointestinal tract. Endocrinol Metab Clin North Am. 1993; 22(4):731-52. View

20.

Schlosser G, Ahrens K . Molecular anatomy of placode development in Xenopus laevis. Dev Biol. 2004; 271(2):439-66. DOI: 10.1016/j.ydbio.2004.04.013. View