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Article ; Online: Steroid hormone signaling synchronizes cell migration machinery, adhesion and polarity to direct collective movement.

Bhattacharya, Mallika / Starz-Gaiano, Michelle

2024 Volume 137, Issue 5

Abstract: Migratory cells - either individually or in cohesive groups - are critical for spatiotemporally regulated processes such as embryonic development and wound healing. Their dysregulation is the underlying cause of formidable health problems such as ... ...

Abstract	Migratory cells - either individually or in cohesive groups - are critical for spatiotemporally regulated processes such as embryonic development and wound healing. Their dysregulation is the underlying cause of formidable health problems such as congenital abnormalities and metastatic cancers. Border cell behavior during Drosophila oogenesis provides an effective model to study temporally regulated, collective cell migration in vivo. Developmental timing in flies is primarily controlled by the steroid hormone ecdysone, which acts through a well-conserved, nuclear hormone receptor complex. Ecdysone signaling determines the timing of border cell migration, but the molecular mechanisms governing this remain obscure. We found that border cell clusters expressing a dominant-negative form of ecdysone receptor extended ineffective protrusions. Additionally, these clusters had aberrant spatial distributions of E-cadherin (E-cad), apical domain markers and activated myosin that did not overlap. Remediating their expression or activity individually in clusters mutant for ecdysone signaling did not restore proper migration. We propose that ecdysone signaling synchronizes the functional distribution of E-cadherin, atypical protein kinase C (aPKC), Discs large (Dlg1) and activated myosin post-transcriptionally to coordinate adhesion, polarity and contractility and temporally control collective cell migration.
MeSH term(s)	Animals ; Drosophila Proteins/metabolism ; Ecdysone/metabolism ; Drosophila/metabolism ; Cadherins/genetics ; Cadherins/metabolism ; Cell Movement/physiology ; Myosins/metabolism ; Drosophila melanogaster/metabolism ; Cell Polarity/physiology ; Cell Adhesion
Chemical Substances	Drosophila Proteins ; Ecdysone (3604-87-3) ; Cadherins ; Myosins (EC 3.6.4.1)
Language	English
Publishing date	2024-03-08
Publishing country	England
Document type	Journal Article
ZDB-ID	2993-2
ISSN	1477-9137 ; 0021-9533
ISSN (online)	1477-9137
ISSN	0021-9533
DOI	10.1242/jcs.261164
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Article ; Online: Mechanisms and modeling of cell migration.

Starz-Gaiano, Michelle

Seminars in cell & developmental biology

2020 Volume 100, Page(s) 130–132

MeSH term(s)	Cell Movement ; Humans ; Models, Biological
Language	English
Publishing date	2020-01-06
Publishing country	England
Document type	Editorial ; Introductory Journal Article ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2019.12.013
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Article ; Online: Mind bomb 2 promotes cell migration and epithelial structure by regulating adhesion complexes and the actin cytoskeleton.

Trivedi, Sunny / Bhattacharya, Mallika / Starz-Gaiano, Michelle

Developmental biology

2022 Volume 491, Page(s) 94–104

Abstract: Cell migration is essential in animal development and co-opted during metastasis and inflammatory diseases. Some cells migrate collectively, which requires them to balance epithelial characteristics such as stable cell-cell adhesions with features of ... ...

Abstract	Cell migration is essential in animal development and co-opted during metastasis and inflammatory diseases. Some cells migrate collectively, which requires them to balance epithelial characteristics such as stable cell-cell adhesions with features of motility like rapid turnover of adhesions and dynamic cytoskeletal structures. How this is regulated is not entirely clear but important to understand. While investigating Drosophila oogenesis, we found that the putative E3 ubiquitin ligase, Mind bomb 2 (Mib2), is required to promote epithelial stability and the collective cell migration of border cells. Through biochemical analysis, we identified components of Mib2 complexes, which include E-cadherin and α- and β-catenins, as well as actin regulators. We also found that three Mib2 interacting proteins, RhoGAP19D, Supervillin, and Myosin heavy chain-like, affect border cell migration. mib2 mutant main body follicle cells have drastically reduced E-cadherin-based adhesion complexes and diminished actin filaments. We conclude that Mib2 acts to stabilize E-cadherin-based adhesion complexes and promote a robust actin cytoskeletal network, which is important for maintenance of epithelial integrity. The interaction with cadherin adhesion complexes and other cytoskeletal regulators contribute to its role in collective cell migration. Since Mib2 is well conserved, it may have similar functional significance in other organisms.
MeSH term(s)	Actin Cytoskeleton/metabolism ; Actins/metabolism ; Animals ; Cadherins/metabolism ; Cell Adhesion ; Cell Movement/physiology ; Drosophila/metabolism ; Myosin Heavy Chains ; Ubiquitin-Protein Ligases/genetics ; Ubiquitin-Protein Ligases/metabolism
Chemical Substances	Actins ; Cadherins ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; Myosin Heavy Chains (EC 3.6.4.1)
Language	English
Publishing date	2022-09-05
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	1114-9
ISSN	1095-564X ; 0012-1606
ISSN (online)	1095-564X
ISSN	0012-1606
DOI	10.1016/j.ydbio.2022.08.009
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Article ; Online: Drosophila Jak/STAT Signaling: Regulation and Relevance in Human Cancer and Metastasis.

Trivedi, Sunny / Starz-Gaiano, Michelle

International journal of molecular sciences

2018 Volume 19, Issue 12

Abstract: Over the past three-decades, Janus kinase (Jak) and signal transducer and activator of transcription (STAT) signaling has emerged as a paradigm to understand the involvement of signal transduction in development and disease pathology. At the molecular ... ...

Abstract	Over the past three-decades, Janus kinase (Jak) and signal transducer and activator of transcription (STAT) signaling has emerged as a paradigm to understand the involvement of signal transduction in development and disease pathology. At the molecular level, cytokines and interleukins steer Jak/STAT signaling to transcriptional regulation of target genes, which are involved in cell differentiation, migration, and proliferation. Jak/STAT signaling is involved in various types of blood cell disorders and cancers in humans, and its activation is associated with carcinomas that are more invasive or likely to become metastatic. Despite immense information regarding Jak/STAT regulation, the signaling network has numerous missing links, which is slowing the progress towards developing drug therapies. In mammals, many components act in this cascade, with substantial cross-talk with other signaling pathways. In
MeSH term(s)	Animals ; Blood Cells/metabolism ; Cell Movement ; Drosophila/metabolism ; Drosophila Proteins/metabolism ; Gene Expression Regulation, Developmental ; Humans ; Janus Kinases/metabolism ; Neoplasms/metabolism ; STAT Transcription Factors/metabolism ; Signal Transduction ; Stem Cells/metabolism
Chemical Substances	Drosophila Proteins ; STAT Transcription Factors ; Janus Kinases (EC 2.7.10.2)
Language	English
Publishing date	2018-12-14
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms19124056
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Article ; Online: Cytokine exocytosis and JAK/STAT activation in the

Saadin, Afsoon / Starz-Gaiano, Michelle

Journal of cell science

2018 Volume 131, Issue 23

Abstract: How vesicle trafficking components actively contribute to regulation of paracrine signaling is unclear. We genetically uncovered a requirement for α-soluble NSF attachment protein (α-Snap) in the activation of the Janus kinase/signal transducer and ... ...

Abstract	How vesicle trafficking components actively contribute to regulation of paracrine signaling is unclear. We genetically uncovered a requirement for α-soluble NSF attachment protein (α-Snap) in the activation of the Janus kinase/signal transducer and activator of transcription (JAK/STAT) pathway during
MeSH term(s)	Animals ; Cytokines/metabolism ; Drosophila ; Exocytosis/physiology ; Female ; Janus Kinases/metabolism ; Ovary/metabolism ; Signal Transduction ; Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins/metabolism
Chemical Substances	Cytokines ; Soluble N-Ethylmaleimide-Sensitive Factor Attachment Proteins ; Janus Kinases (EC 2.7.10.2)
Language	English
Publishing date	2018-11-30
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2993-2
ISSN	1477-9137 ; 0021-9533
ISSN (online)	1477-9137
ISSN	0021-9533
DOI	10.1242/jcs.217638
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Article ; Online: Assessing the Age-Specific Phagocytic Ability of Adult Drosophila melanogaster Hemocytes using an In Vivo Phagocytosis Assay.

Campbell, Shonda M / Starz-Gaiano, Michelle / Leips, Jeff

Journal of visualized experiments : JoVE

2020 , Issue 160

Abstract: Phagocytosis is an essential function of the innate immune response. This process is carried out by phagocytic hemocytes whose primary function is to recognize a wide range of particles and destroy microbial pathogens. As organisms age, this process ... ...

Abstract	Phagocytosis is an essential function of the innate immune response. This process is carried out by phagocytic hemocytes whose primary function is to recognize a wide range of particles and destroy microbial pathogens. As organisms age, this process begins to decline, yet little is known about the underlying mechanisms or the genetic basis of immunosenescence. Here, an injection based in vivo phagocytosis assay is used to assess age related changes in different aspects of phagocytosis, such as binding, engulfment, and degradation of internalized particles, by quantifying phagocytic events in hemocytes in adult Drosophila. Drosophila melanogaster has become an ideal model to investigate age related changes in innate immune function for many reasons. For one, many genetic components and functions of the innate immune response, including phagocytosis, are evolutionarily conserved between Drosophila and mammals. Because of that, results obtained from using this protocol are likely to be widely relevant to understanding the age related changes in immune function in a variety of organisms. Additionally, we note that this method provides quantitative estimates of hemocyte phagocytic ability, which could be useful for a variety of research topics, and need not be limited to studies of aging.
MeSH term(s)	Aging/physiology ; Animals ; Biological Assay/methods ; Dissection ; Drosophila melanogaster/cytology ; Female ; Fluorescent Dyes/metabolism ; Hemocytes/cytology ; Hemocytes/metabolism ; Hydrogen-Ion Concentration ; Image Processing, Computer-Assisted ; Injections ; Phagocytes/cytology ; Phagocytes/metabolism ; Phagocytosis ; Staining and Labeling ; Tissue Fixation
Chemical Substances	Fluorescent Dyes
Language	English
Publishing date	2020-06-11
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Video-Audio Media
ZDB-ID	2259946-0
ISSN	1940-087X ; 1940-087X
ISSN (online)	1940-087X
ISSN	1940-087X
DOI	10.3791/60983
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Article: Development and Analysis of a Quantitative Mathematical Model of Bistability in the Cross Repression System Between APT and SLBO Within the JAK/STAT Signaling Pathway.

Berez, Alyssa / Peercy, Bradford E / Starz-Gaiano, Michelle

Frontiers in physiology

2020 Volume 11, Page(s) 803

Abstract: Cell migration is a key component in development, homeostasis, immune function, and pathology. It is important to understand the molecular activity that allows some cells to migrate. ...

Abstract	Cell migration is a key component in development, homeostasis, immune function, and pathology. It is important to understand the molecular activity that allows some cells to migrate.
Language	English
Publishing date	2020-07-28
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2020.00803
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Article ; Online: Clustered cell migration: Modeling the model system of Drosophila border cells.

Peercy, Bradford E / Starz-Gaiano, Michelle

Seminars in cell & developmental biology

2019 Volume 100, Page(s) 167–176

Abstract: In diverse developmental contexts, certain cells must migrate to fulfill their roles. Many questions remain unanswered about the genetic and physical properties that govern cell migration. While the simplest case of a single cell moving alone has been ... ...

Abstract	In diverse developmental contexts, certain cells must migrate to fulfill their roles. Many questions remain unanswered about the genetic and physical properties that govern cell migration. While the simplest case of a single cell moving alone has been well-studied, additional complexities arise in considering how cohorts of cells move together. Significant differences exist between models of collectively migrating cells. We explore the experimental model of migratory border cell clusters in Drosophila melanogaster egg chambers, which are amenable to direct observation and precise genetic manipulations. This system involves two special characteristics that are worthy of attention: border cell clusters contain a limited number of both migratory and non-migratory cells that require coordination, and they navigate through a heterogeneous three-dimensional microenvironment. First, we review how clusters of motile border cells are specified and guided in their migration by chemical signals and the physical impact of adjacent tissue interactions. In the second part, we examine questions around the 3D structure of the motile cluster and surrounding microenvironment in understanding the limits to cluster size and speed of movement through the egg chamber. Mathematical models have identified sufficient gene regulatory networks for specification, the key forces that capture emergent behaviors observed in vivo, the minimal regulatory topologies for signaling, and the distribution of key signaling cues that direct cell behaviors. This interdisciplinary approach to studying border cells is likely to reveal governing principles that apply to different types of cell migration events.
MeSH term(s)	Animals ; Cell Movement ; Drosophila melanogaster/cytology ; Female ; Models, Biological ; Ovary/cytology ; Ovary/metabolism
Language	English
Publishing date	2019-12-11
Publishing country	England
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	1312473-0
ISSN	1096-3634 ; 1084-9521
ISSN (online)	1096-3634
ISSN	1084-9521
DOI	10.1016/j.semcdb.2019.11.010
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Article ; Online: Identification of Novel Regulators of the JAK/STAT Signaling Pathway that Control Border Cell Migration in the Drosophila Ovary.

Saadin, Afsoon / Starz-Gaiano, Michelle

G3 (Bethesda, Md.)

2016 Volume 6, Issue 7, Page(s) 1991–2002

Abstract: The Janus Kinase/Signal Transducer and Activator of Transcription (JAK/STAT) signaling pathway is an essential regulator of cell migration both in mammals and fruit flies. Cell migration is required for normal embryonic development and immune response ... ...

Abstract	The Janus Kinase/Signal Transducer and Activator of Transcription (JAK/STAT) signaling pathway is an essential regulator of cell migration both in mammals and fruit flies. Cell migration is required for normal embryonic development and immune response but can also lead to detrimental outcomes, such as tumor metastasis. A cluster of cells termed "border cells" in the Drosophila ovary provides an excellent example of a collective cell migration, in which two different cell types coordinate their movements. Border cells arise within the follicular epithelium and are required to invade the neighboring cells and migrate to the oocyte to contribute to a fertilizable egg. Multiple components of the STAT signaling pathway are required during border cell specification and migration; however, the functions and identities of other potential regulators of the pathway during these processes are not yet known. To find new components of the pathway that govern cell invasiveness, we knocked down 48 predicted STAT modulators using RNAi expression in follicle cells, and assayed defective cell movement. We have shown that seven of these regulators are involved in either border cell specification or migration. Examination of the epistatic relationship between candidate genes and Stat92E reveals that the products of two genes, Protein tyrosine phosphatase 61F (Ptp61F) and brahma (brm), interact with Stat92E during both border cell specification and migration.
MeSH term(s)	Animals ; Cell Cycle Proteins/genetics ; Cell Cycle Proteins/metabolism ; Cell Movement ; Drosophila Proteins/genetics ; Drosophila Proteins/metabolism ; Drosophila melanogaster/genetics ; Drosophila melanogaster/growth & development ; Drosophila melanogaster/metabolism ; Epistasis, Genetic ; Female ; Gene Expression Regulation, Developmental ; Gene Knockdown Techniques ; Oogenesis/genetics ; Ovarian Follicle/cytology ; Ovarian Follicle/growth & development ; Ovarian Follicle/metabolism ; Protein Tyrosine Phosphatases, Non-Receptor/genetics ; Protein Tyrosine Phosphatases, Non-Receptor/metabolism ; RNA Interference ; STAT Transcription Factors/genetics ; STAT Transcription Factors/metabolism ; Signal Transduction ; Trans-Activators/genetics ; Trans-Activators/metabolism
Chemical Substances	Cell Cycle Proteins ; Drosophila Proteins ; STAT Transcription Factors ; Stat92E protein, Drosophila ; Trans-Activators ; brm protein, Drosophila ; Protein Tyrosine Phosphatases, Non-Receptor (EC 3.1.3.48) ; Ptp61F protein, Drosophila (EC 3.1.3.48)
Language	English
Publishing date	2016-07-07
Publishing country	United States
Document type	Journal Article
ZDB-ID	2629978-1
ISSN	2160-1836 ; 2160-1836
ISSN (online)	2160-1836
ISSN	2160-1836
DOI	10.1534/g3.116.028100
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Article: Circuitous Genetic Regulation Governs a Straightforward Cell Migration.

Saadin, Afsoon / Starz-Gaiano, Michelle

Trends in genetics : TIG

2016 Volume 32, Issue 10, Page(s) 660–673

Abstract: Drosophila border cells undergo a straightforward and stereotypical collective migration during egg development. However, a complex genetic program underlies this process. A variety of approaches, including biochemical, genetic, and imaging strategies ... ...

Abstract	Drosophila border cells undergo a straightforward and stereotypical collective migration during egg development. However, a complex genetic program underlies this process. A variety of approaches, including biochemical, genetic, and imaging strategies have identified many regulatory components, revealing layers of control. This complexity suggests that the active processes of evaluating the environment, remodeling the cytoskeleton, and coordinating movements among cells, demand rapid systems for modulating cell behaviors. Multiple signaling inputs, nodes of integration, and feedback loops act as molecular rheostats to fine-tune gene expression levels and physical responses. Since key genetic regulators of border cell migration have been shown to be required in other types of cell migration, this model system continues to provide an important avenue for genetic discovery.
Language	English
Publishing date	2016-10
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	619240-3
ISSN	1362-4555 ; 0168-9525 ; 0168-9479
ISSN (online)	1362-4555
ISSN	0168-9525 ; 0168-9479
DOI	10.1016/j.tig.2016.08.001
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