Expression and Functional Analysis of cofilin1-like in Craniofacial Development in Zebrafish
2
조회
0
다운로드
0
인용
0
참고문헌
키워드
초록
Pharyngeal pouches, a series of outgrowths of the pharyngeal endoderm, are a key epithelial structure governing facial skeleton development in vertebrates. Pouch formation is achieved through collective cell migration and rearrangement of pouch-forming cells controlled by actin cytoskeleton dynamics. While essential transcription factors and signaling molecules have been identified in pouch formation, regulators of actin cytoskeleton dynamics have not been reported yet in any vertebrates. Cofilin1-like (Cfl1l) is a fish-specific member of the Actin-depolymerizing factor (ADF)/Cofilin family, a critical regulator of actin cytoskeleton dynamics in eukaryotic cells. Here, we report the expression and function of cfl1l in pouch development in zebrafish. We first showed that fish cfl1l might be an ortholog of vertebrate adf, based on phylogenetic analysis of vertebrate adf and cfl genes. During pouch formation, cfl1l was expressed sequentially in the developing pouches but not in the posterior cell mass in which future pouch-forming cells are present. However, pouches, as well as facial cartilages whose development is dependent upon pouch formation, were unaffected by lossof- function mutations in cfl1l. Although it could not be completely ruled out a possibility of a genetic redundancy of Cfl1l with other Cfls, our results suggest that the cfl1l expression in the developing pouches might be dispensable for regulating actin cytoskeleton dynamics in pouch-forming cells.
Abstract
Pharyngeal pouches, a series of outgrowths of the pharyngeal endoderm, are a key epithelial structure governing facial skeleton development in vertebrates. Pouch formation is achieved through collective cell migration and rearrangement of pouch-forming cells controlled by actin cytoskeleton dynamics. While essential transcription factors and signaling molecules have been identified in pouch formation, regulators of actin cytoskeleton dynamics have not been reported yet in any vertebrates. Cofilin1-like (Cfl1l) is a fish-specific member of the Actin-depolymerizing factor (ADF)/Cofilin family, a critical regulator of actin cytoskeleton dynamics in eukaryotic cells. Here, we report the expression and function of cfl1l in pouch development in zebrafish. We first showed that fish cfl1l might be an ortholog of vertebrate adf, based on phylogenetic analysis of vertebrate adf and cfl genes. During pouch formation, cfl1l was expressed sequentially in the developing pouches but not in the posterior cell mass in which future pouch-forming cells are present. However, pouches, as well as facial cartilages whose development is dependent upon pouch formation, were unaffected by lossof- function mutations in cfl1l. Although it could not be completely ruled out a possibility of a genetic redundancy of Cfl1l with other Cfls, our results suggest that the cfl1l expression in the developing pouches might be dispensable for regulating actin cytoskeleton dynamics in pouch-forming cells.
참고문헌 (57)
- Abe H, "Xenopus laevis actin-depolymerizing factor", cofilin : A phosphorylation-regulated protein essential for development, 1996, pp.132, 871~885
- Agnew BJ, "Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site", J Biol Chem, 270, pp.17582~17587 (1995)
- Agrawal PB, "Normal myofibrillar development followed by progressive sarcomeric disruption with actin accumulations in a mouse Cfl2knockout demonstrates requirement of cofilin-2 for muscle maintenance", Hum Mol Genet, 21, pp.2341~2356 (2012)
- Ashworth S, "Cofilin-1 inactivation leads to proteinuria : Studies in zebrafish, mice and humans", PLOS ONE, 5, pp.e12626~ (2010)
- Park JK, "Cofilin-1 inactivation leads to proteinuria : Studies in zebrafish, mice and humans", PLOS ONE, 5, pp.e12626~ (2010)
- Baker M, "Gene editing at CRISPR speed", Nat Biotechnol, 32, pp.309~312 (2014)
- Choe CP, "Wnt-dependent epithelial transitions drive pharyngeal pouch formation", Dev Cell, 24, pp.296~309 (2013)
- Choe CP, "Tbx1 controls the morphogenesis of pharyngeal pouch epithelia through mesodermal Wnt11r and Fgf8a", Development, 141, pp.3583~3593 (2014)
- Choe CP, "Eph-Pak2a signaling regulates branching of the pharyngeal endoderm by inhibiting late-stage epithelial dynamics", Development, 142, pp.1089~1094 (2015)
- Crump JG, "An essential role for Fgfs in endodermal pouch formation influences later craniofacial skeletal patterning", Development, 131, pp.5703~5716 (2004)
- Dickmeis T, "A crucial component of the endoderm formation pathway, CASANOVA, is encoded by a novel sox-related gene", Genes Dev, 15, pp.1487~1492 (2001)
- Driscoll DA, "A genetic etiology for DiGeorge syndrome : Consistent deletions and microdeletions of 22q11", Am J Hum Genet, 50, pp.924~933 (1992)
- Edlund RK, "Foxi transcription factors promote pharyngeal arch development by regulating formation of FGF signaling centers", Dev Biol, 390, pp.1~13 (2014)
- Fukuda R, "Mechanical forces regulate cardiomyocyte myofilament maturation via the VCL-SSH1-CFL axis", Dev Cell, 51, pp.62~77 (2019)[DOI]
- Graham A, "Deconstructing the pharyngeal metamere", J Exp Zool B Mol Dev Evol, 310, pp.336~344 (2008)
- Grevellec A, "The pharyngeal pouches and clefts : Development, evolution, structure and derivatives", Semin Cell Dev Biol, 21, pp.325~332 (2010)
- Gurniak CB, "The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration", Dev Biol, 278, pp.231~241 (2005)
- Herzog W, "Fgf3signaling from the ventral diencephalon is required for early specification and subsequent survival of the zebrafish adenohypophysis", Development, 131, pp.3681~3692 (2004)
- Hwang WY, "Efficient genome editing in zebrafish using a CRISPR-Cas system", Nat Biotechnol, 31, pp.227~229 (2013)
- Ikeda S, "Aberrant actin cytoskeleton leads to accelerated proliferation of corneal epithelial cells in mice deficient for destrin(actin depolymerizing factor)", Hum Mol Genet, 12, pp.1029~1036 (2003)
- 전해원, "A Role for buttonhead in the Early Head and Trunk Development in the Beetle Tribolium castaneum", 발생과 생식, 23(1), pp.63~72 (2019), 한국발생생물학회
- Jin S, "Foxi1 promotes late-stage pharyngeal pouch morphogenesis through ectodermal Wnt4a activation", Dev Biol, 441, pp.12~18 (2018)
- Kikuchi Y, "Casanova encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish", Genes Dev, 15, pp.1493~1505 (2001)
- Kremneva E, "Cofilin-2 controls actin filament length in muscle sarcomeres", Dev Cell, 31, pp.215~226 (2014)
- Kuure S, "Actin depolymerizing factors cofilin1 and destrin are required for ureteric bud branching morphogenesis", PLOS Genet, 6, pp.e1001176~ (2010)
- Lappalainen P, "Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis", EMBO J, 16, pp.5520~5530 (1997)
- Lappalainen P, "The ADF homology(ADF-H)domain : A highly exploited actin-binding module", Mol Biol Cell, 9, pp.1951~1959 (1998)
- Li L, "BMP signaling is required for nkx2. 3-positive pharyngeal pouch progenitor specification in zebrafish", PLOS Genet, 15, pp.e1007996~ (2019)
- Lin CW, "Loss of cofilin 1 disturbs actin dynamics, adhesion between enveloping and deep cell layers and cell movements during gastrulation in zebrafish", PLOS ONE, 5, pp.e15331~ (2010)
- Lindsay EA, "Tbx1 haploinsufficiency in the DiGeorge syndrome region causes aortic arch defects in mice", Nature, 410, pp.97~101 (2001)
- Liu YH, "Zebrafish Pax1a and Pax1b are required for pharyngeal pouch morphogenesis and ceratobranchial cartilage development", Mech Dev, 161, pp.103598~ (2020)
- Lovely CB, "Bmp signaling mediates endoderm pouch morphogenesis by regulating Fgf signaling in zebrafish", Development, 143, pp.2000~2011 (2016)
- Miller CT, "Sucker encodes a zebrafish Endothelin-1 required for ventral pharyngeal arch development", Development, 127, pp.3815~3828 (2000)
- Moriyama K, "Phosphorylation of Ser-3 of cofilin regulates its essential function on actin", Genes Cells, 1, pp.73~86 (1996)
- Munsie LN, "Cofilin nuclear-cytoplasmic shuttling affects cofilin actin rod formation during stress", J Cell Sci, 125, pp.3977~3988 (2012)
- Nissen RM, "Zebrafish foxi one modulates cellular responses to Fgf signaling required for the integrity of ear and jaw patterning", Development, 130, pp.2543~2554 (2003)
- Obinata T, "Low molecular-weight G-actin binding proteins involved in the regulation of actin assembly during myofibrillogenesis", Cell Struct Funct, 22, pp.181~189 (1997)
- Ohashi K, "Roles of cofilin in development and its mechanisms of regulation", Dev Growth Differ, 57, pp.275~290 (2015)
- Okada K, "Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka", Development, 143, pp.1800~1810 (2016)
- Olson HM, "Lamellipodia-like protrusions and focal adhesions contribute to collective cell migration in zebrafish", Dev Biol, 469, pp.125~134 (2021)
- Ono S, "Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics", Int Rev Cytol, 258, pp.1~82 (2007)
- Peters H, "Pax9-deficient mice lack pharyngeal pouch derivatives and teeth and exhibit craniofacial and limb abnormalities", Genes Dev, 12, pp.2735~2747 (1998)
- Piotrowski T, "The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans", Development, 130, pp.5043~5052 (2003)
- Piotrowski T, "The endoderm plays an important role in patterning the segmented pharyngeal region in zebrafish(Danio rerio)", Dev Biol, 225, pp.339~356 (2000)
- Quinlan R, "The role of actin cables in directing the morphogenesis of the pharyngeal pouches", Development, 131, pp.593~599 (2004)
- Rohatgi R, "The interaction between N-WASP and the Arp2", 3 complex links Cdc42-dependent signals to actin assembly, 1999, pp.97, 221~231
- Shishkin S, "Cofilin-1 and other ADF", cofilin superfamily members in human malignant cells, 2016, pp.18, 10~
- Sievers F, "Multiple Sequence Alignment. Methods in Molecular Biology, vol. 2231", pp.3~16 (2021), Humana
- Solomon KS, "Zebrafish foxi1 mediates otic placode formation and jaw development", Development, 130, pp.929~940 (2003)
- Stamatakis A, "RAxML-VI-HPC : Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models", Bioinformatics, 22, pp.2688~2690 (2006)
- Tallafuß A, "Tracing of her5 progeny in zebrafish transgenics reveals the dynamics of midbrain-hindbrain neurogenesis and maintenance", Development, 130, pp.4307~4323 (2003)
- Tran HT, "ARVCF depletion cooperates with Tbx1deficiency in the development of 22q11. 2DS-like phenotypes in Xenopus", Dev Dyn, 240, pp.2680~2687 (2011)
- Wagner DE, "Single-cell mapping of gene expression landscapes and lineage in the zebrafish embryo", Science, 360, pp.981~987 (2018)
- Wakayama Y, "Cdc42 mediates Bmpinduced sprouting angiogenesis through Fmnl3-driven assembly of endothelial filopodia in zebrafish", Dev Cell, 32, pp.109~122 (2015)
- Yonezawa N, "An actin-interacting heptapeptide in the cofilin sequence", Eur J Biochem, 183, pp.235~238 (1989)
- Zuniga E, "Gremlin 2 regulates distinct roles of BMP and Endothelin 1 signaling in dorsoventral patterning of the facial skeleton", Development, 138, pp.5147~5156 (2011)
- Zuniga E, "Jagged-Notch signaling ensures dorsal skeletal identity in the vertebrate face", Development, 137, pp.1843~1852 (2010)