Cells into tubes: Molecular and physical principles underlying lumen formation in tubular organs

Camelo, Carolina; Luschnig, Stefan

doi:10.1016/bs.ctdb.2020.09.002

Cited by 12 publications

(7 citation statements)

References 124 publications

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“…Regarding the former, chinmo was selectively depleted in the salivary glands (SGs) using the forkhead ( fkh ) driver ( fkhGal4 ), which is active in this tissue from embryogenesis onwards. The SG is a secretory organ that develops from embryonic epithelial placodes (Abrams et al, 2003; Bradley et al, 2001; Camelo and Luschnig, 2021) and increases dramatically in size by cell endoreplication during the larval period (Edgar et al, 2014; Zielke et al, 2013). This tissue is responsible for producing glycosylated mucin for the lubrication of food during the larval period (Costantino et al, 2008; Farkaš et al, 2014; Riddiford, 1993; Syed et al, 2008) and for synthesising glue proteins for the attachment of the pupa to a solid surface at the onset of metamorphosis (Andres et al, 1993; Costantino et al, 2008; Kaieda et al, 2017).…”

Section: Resultsmentioning

confidence: 99%

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Chafino

Giannios

Casanova

et al. 2022

Preprint

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During development, the growing organism transits through a series of temporally regulated morphological stages to generate the adult form. In humans, for example, development progresses from childhood through to puberty and then to adulthood, when sexual maturity is attained. Similarly, in holometabolous insects, immature juveniles transit to the adult form through an intermediate pupal stage when larval tissues are eliminated and the imaginal progenitor cells form the adult structures. The identity of the larval, pupal and adult stages depends on the sequential expression of the transcription factors chinmo, Br-C and E93. However, how these transcription factors determine temporal identity in developing tissues is poorly understood. Here we report on the role of the larval specifier chinmo in larval and adult progenitor cells during fly development. Interestingly, chinmo promotes growth in larval and imaginal tissues in a Br-C-independent and -dependent manner, respectively. In addition, we found that the absence of chinmo during metamorphosis is critical for proper adult differentiation. Importantly, we also provide evidence that, in contrast to the well-known role of chinmo as a pro-oncogene, Br-C and E93 act as tumour suppressors. Finally, we reveal that the function of chinmo as a juvenile specifier is conserved in hemimetabolous insects as its homolog has a similar role in Blatella germanica. Taken together, our results suggest that the sequential expression of the transcription factors Chinmo, Br-C and E93 during larva, pupa an adult respectively, coordinate the formation of the different organs that constitute the adut organism.

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Section: Resultsmentioning

confidence: 99%

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Chafino

Giannios

Casanova

et al. 2022

Preprint

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“…Cyst formation, interstitial fibrosis, and inflammation are the characteristic pathological changes in NPHP. Cyst formation is a process influenced by many factors, such as cytoskeletal dynamics, intracellular and extracellular mechanical forces, and polarized membrane transport [ 43 , 44 , 45 ]. Crosstalk between different cytoskeletons is necessary to ensure a constant subcellular lumen diameter and to prevent cyst formation [ 45 ].…”

Section: Discussionmentioning

confidence: 99%

“…Cyst formation is a process influenced by many factors, such as cytoskeletal dynamics, intracellular and extracellular mechanical forces, and polarized membrane transport [ 43 , 44 , 45 ]. Crosstalk between different cytoskeletons is necessary to ensure a constant subcellular lumen diameter and to prevent cyst formation [ 45 ]. Cytoskeletal disturbances are common features of cyst formation.…”

Section: Discussionmentioning

confidence: 99%

Reducing GEF-H1 Expression Inhibits Renal Cyst Formation, Inflammation, and Fibrosis via RhoA Signaling in Nephronophthisis

Lai

Chen

et al. 2023

IJMS

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Nephronophthisis (NPHP) is the most prevalent monogenic disease leading to end-stage renal failure in childhood. RhoA activation is involved in NPHP pathogenesis. This study explored the role of the RhoA activator guanine nucleotide exchange factor (GEF)-H1 in NPHP pathogenesis. We analyzed the expression and distribution of GEF-H1 in NPHP1 knockout (NPHP1KO) mice using Western blotting and immunofluorescence, followed by GEF-H1 knockdown. Immunofluorescence and renal histology were used to examine the cysts, inflammation, and fibrosis. A RhoA GTPase activation assay and Western blotting were used to detect the expression of downstream GTP-RhoA and p-MLC2, respectively. In NPHP1 knockdown (NPHP1KD) human kidney proximal tubular cells (HK2 cells), we detected the expressions of E-cadherin and α-smooth muscle actin (α-SMA). In vivo, increased expression and redistribution of GEF-H1, and higher levels of GTP-RhoA and p-MLC2 in renal tissue of NPHP1KO mice were observed, together with renal cysts, fibrosis, and inflammation. These changes were alleviated by GEF-H1 knockdown. In vitro, the expression of GEF-H1 and activation of RhoA were also increased, with increased expression of α-SMA and decreased E-cadherin. GEF-H1 knockdown reversed these changes in NPHP1KD HK2 cells. Thus, the GEF-H1/RhoA/MLC2 axis is activated in NPHP1 defects and may play a pivotal role in NPHP pathogenesis.

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“…These cells form a three dimensional (3D) rosette of polarized cells that initiate single lumen formation at their center. The opening of a microlumen is facilitated in part by secretion of negatively-charged Podocalyxin, creating ionic repulsion forces, as well as by actomyosin-generated contractile forces (Camelo and Luschnig, 2021; Dekan et al, 1991; Schottenfeld-Roames et al, 2014; Strilic et al, 2009). Once a pancreatic microlumen has been formed through these mechanisms, it then fuses with other microlumens and with the foregut lumen (Villasenor et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Rab11 is essential to pancreas morphogenesis, lumen formation and endocrine mass

Barlow

Htike

Fassetta

et al. 2022

Preprint

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The molecular links between tissue-level morphogenesis and the differentiation of cell lineages in the pancreas remain elusive despite a decade of studies. We previously showed that in pancreas both these processes depend on proper lumenogenesis. The Rab GTPase Rab11 has been shown to be essential to epithelial lumen formation in vitro, however few studies have addressed its functions in vivo and none have tested its requirement in pancreas. Here, we show that Rab11 is critical to proper pancreas development. Co-deletion of the Rab11 isoforms Rab11A and Rab11B in the developing pancreatic epithelium (Rab11pancDKO) results in ~50% neonatal lethality, and surviving adult Rab11pancDKO mice exhibit defective endocrine function. Loss of Rab11 in the embryonic pancreas results in morphogenetic defects of the epithelium linked to defective lumen formation and interconnection. In contrast to wildtype cells, Rab11pancDKO cells attempt to form multiple lumens, resulting in a failure to coordinate a single apical membrane initiation site (AMIS) between groups of cells. We show that these defects are due to failures in vesicle trafficking, as apical components remain trapped within Rab11pancDKO cells. Together, these observations suggest Rab11 directly regulates epithelial lumen formation and morphogenesis. Our report links intracellular trafficking to organ morphogenesis in vivo, and presents a novel framework for decoding pancreatic development.

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Cells into tubes: Molecular and physical principles underlying lumen formation in tubular organs

Cited by 12 publications

References 124 publications

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Antagonistic role of the BTB-zinc finger transcription factors Chinmo and Broad-Complex in the juvenile/pupal transition and in growth control

Reducing GEF-H1 Expression Inhibits Renal Cyst Formation, Inflammation, and Fibrosis via RhoA Signaling in Nephronophthisis

Rab11 is essential to pancreas morphogenesis, lumen formation and endocrine mass

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