Arginylation-Dependent Neural Crest Cell Migration Is Essential for Mouse Development
Coordinated cell migration during development is crucial for morphogenesis and largely relies on cells of the neural crest lineage that migrate over long distances to give rise to organs and tissues throughout the body. Recent studies of protein arginylation implicated this poorly understood posttranslational modification in the functioning of actin cytoskeleton and in cell migration in culture. Knockout of arginyltransferase (Ate1) in mice leads to embryonic lethality and severe heart defects that are reminiscent of cell migration–dependent phenotypes seen in other mouse models. To test the hypothesis that arginylation regulates cell migration during morphogenesis, we produced Wnt1-Cre Ate1 conditional knockout mice (Wnt1-Ate1), with Ate1 deletion in the neural crest cells driven by Wnt1 promoter. Wnt1-Ate1 mice die at birth and in the first 2–3 weeks after birth with severe breathing problems and with growth and behavioral retardation. Wnt1-Ate1 pups have prominent defects, including short palate and altered opening to the nasopharynx, and cranial defects that likely contribute to the abnormal breathing and early death. Analysis of neural crest cell movement patterns in situ and cell motility in culture shows an overall delay in the migration of Ate1 knockout cells that is likely regulated by intracellular mechanisms rather than extracellular signaling events. Taken together, our data suggest that arginylation plays a general role in the migration of the neural crest cells in development by regulating the molecular machinery that underlies cell migration through tissues and organs during morphogenesis.
Vyšlo v časopise:
Arginylation-Dependent Neural Crest Cell Migration Is Essential for Mouse Development. PLoS Genet 6(3): e32767. doi:10.1371/journal.pgen.1000878
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000878
Souhrn
Coordinated cell migration during development is crucial for morphogenesis and largely relies on cells of the neural crest lineage that migrate over long distances to give rise to organs and tissues throughout the body. Recent studies of protein arginylation implicated this poorly understood posttranslational modification in the functioning of actin cytoskeleton and in cell migration in culture. Knockout of arginyltransferase (Ate1) in mice leads to embryonic lethality and severe heart defects that are reminiscent of cell migration–dependent phenotypes seen in other mouse models. To test the hypothesis that arginylation regulates cell migration during morphogenesis, we produced Wnt1-Cre Ate1 conditional knockout mice (Wnt1-Ate1), with Ate1 deletion in the neural crest cells driven by Wnt1 promoter. Wnt1-Ate1 mice die at birth and in the first 2–3 weeks after birth with severe breathing problems and with growth and behavioral retardation. Wnt1-Ate1 pups have prominent defects, including short palate and altered opening to the nasopharynx, and cranial defects that likely contribute to the abnormal breathing and early death. Analysis of neural crest cell movement patterns in situ and cell motility in culture shows an overall delay in the migration of Ate1 knockout cells that is likely regulated by intracellular mechanisms rather than extracellular signaling events. Taken together, our data suggest that arginylation plays a general role in the migration of the neural crest cells in development by regulating the molecular machinery that underlies cell migration through tissues and organs during morphogenesis.
Zdroje
1. Bronner-FraserM
FraserSE
1991 Cell lineage analysis of the avian neural crest. Development Suppl 2 17 22
2. FraserSE
1991 Pattern formation in the vertebrate nervous system. Curr Opin Genet Dev 1 217 220
3. Le DouarinNM
1983 The Neural Crest (Developmental and Cell Biology Series): Cambridge University Press.
4. TuckerRP
2004 Neural crest cells: a model for invasive behavior. Int J Biochem Cell Biol 36 173 177
5. Saint-JeannetJ-P
2006 Neural Crest Induction and Differentiation. New Yory, NY Springer Science + Business Media, LLC
6. EchelardY
VassilevaG
McMahonAP
1994 Cis-acting regulatory sequences governing Wnt-1 expression in the developing mouse CNS. Development 120 2213 2224
7. IkeyaM
LeeSM
JohnsonJE
McMahonAP
TakadaS
1997 Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389 966 970
8. Sauka-SpenglerT
Bronner-FraserM
2008 A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9 557 568
9. KwonYT
KashinaAS
DavydovIV
HuRG
AnJY
2002 An essential role of N-terminal arginylation in cardiovascular development. Science 297 96 99
10. KurosakaS
KashinaA
2008 Cell biology of embryonic migration. Birth Defects Res C Embryo Today 84 102 122
11. LeeMJ
TasakiT
MoroiK
AnJY
KimuraS
2005 RGS4 and RGS5 are in vivo substrates of the N-end rule pathway. Proc Natl Acad Sci U S A 102 15030 15035
12. FissoloS
BongiovanniG
DeccaMB
HallakME
2000 Post-translational arginylation of proteins in cultured cells. Neurochem Res 25 71 76
13. BongiovanniG
FissoloS
BarraHS
HallakME
1999 Posttranslational arginylation of soluble rat brain proteins after whole body hyperthermia. J Neurosci Res 56 85 92
14. HallakME
BongiovanniG
1997 Posttranslational arginylation of brain proteins. Neurochem Res 22 467 473
15. SofferRL
MendelsohnN
1966 Incorporation of arginine by a soluble system from sheep thyroid. Biochem Biophys Res Commun 23 252 258
16. XuNS
ChakrabortyG
HassankhaniA
IngogliaNA
1993 N-terminal arginylation of proteins in explants of injured sciatic nerves and embryonic brains of rats. Neurochem Res 18 1117 1123
17. WangYM
IngogliaNA
1997 N-terminal arginylation of sciatic nerve and brain proteins following injury. Neurochem Res 22 1453 1459
18. DeccaMB
BoscC
LucheS
BrugiereS
JobD
2006 Protein arginylation in rat brain cytosol: a proteomic analysis. Neurochem Res 31 401 409
19. DeccaMB
CarpioMA
BoscC
GalianoMR
JobD
2006 Post-translational arginylation of calreticulin: A new isospecies of calreticulin component of stress granules. J Biol Chem
20. KopitzJ
RistB
BohleyP
1990 Post-translational arginylation of ornithine decarboxylase from rat hepatocytes. Biochem J 267 343 348
21. SofferRL
1971 Enzymatic modification of proteins. 4. Arginylation of bovine thyroglobulin. J Biol Chem 246 1481 1484
22. SofferRL
1975 Enzymatic arginylation of beta-melanocyte-stimulating hormone and of angiotensin II. J Biol Chem 250 2626 2629
23. WongCC
XuT
RaiR
BaileyAO
YatesJR3rd
2007 Global analysis of posttranslational protein arginylation. PLoS Biol 5 e258 doi:10.1371/journal.pbio.0050258
24. KarakozovaM
KozakM
WongCC
BaileyAO
YatesJR3rd
2006 Arginylation of beta-actin regulates actin cytoskeleton and cell motility. Science 313 192 196
25. RaiR
KashinaA
2005 Identification of mammalian arginyltransferases that modify a specific subset of protein substrates. Proc Natl Acad Sci U S A 102 10123 10128
26. KwonYT
KashinaAS
VarshavskyA
1999 Alternative splicing results in differential expression, activity, and localization of the two forms of arginyl-tRNA-protein transferase, a component of the N-end rule pathway. Mol Cell Biol 19 182 193
27. RaiR
WongCC
XuT
LeuNA
DongDW
2008 Arginyltransferase regulates alpha cardiac actin function, myofibril formation and contractility during heart development. Development 135 3881 3889
28. KapurRP
2000 Colonization of the murine hindgut by sacral crest-derived neural precursors: experimental support for an evolutionarily conserved model. Dev Biol 227 146 155
29. ChaiY
JiangX
ItoY
BringasPJr
HanJ
2000 Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127 1671 1679
30. JiangX
RowitchDH
SorianoP
McMahonAP
SucovHM
2000 Fate of the mammalian cardiac neural crest. Development 127 1607 1616
31. JiangX
IsekiS
MaxsonRE
SucovHM
Morriss-KayGM
2002 Tissue origins and interactions in the mammalian skull vault. Dev Biol 241 106 116
32. YoshidaT
VivatbutsiriP
Morriss-KayG
SagaY
IsekiS
2008 Cell lineage in mammalian craniofacial mesenchyme. Mech Dev 125 797 808
33. SchorleH
MeierP
BuchertM
JaenischR
MitchellPJ
1996 Transcription factor AP-2 essential for cranial closure and craniofacial development. Nature 381 235 238
34. SatokataI
MaL
OhshimaH
BeiM
WooI
2000 Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 24 391 395
35. EnglekaKA
WuM
ZhangM
AntonucciNB
EpsteinJA
2007 Menin is required in cranial neural crest for palatogenesis and perinatal viability. Dev Biol 311 524 537
36. WuM
LiJ
EnglekaKA
ZhouB
LuMM
2008 Persistent expression of Pax3 in the neural crest causes cleft palate and defective osteogenesis in mice. J Clin Invest 118 2076 2087
37. ZhangP
LiegeoisNJ
WongC
FinegoldM
HouH
1997 Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387 151 158
38. YanY
FrisenJ
LeeMH
MassagueJ
BarbacidM
1997 Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev 11 973 983
39. MorriseyEE
2003 Wnt signaling and pulmonary fibrosis. Am J Pathol 162 1393 1397
40. KonigshoffM
BalsaraN
PfaffEM
KramerM
ChrobakI
2008 Functional Wnt signaling is increased in idiopathic pulmonary fibrosis. PLoS ONE 3 e2142 doi:10.1371/journal.pone.0002142
41. BraunT
RudnickiMA
ArnoldHH
JaenischR
1992 Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71 369 382
42. GrossJB
HankenJ
2008 Review of fate-mapping studies of osteogenic cranial neural crest in vertebrates. Dev Biol 317 389 400
43. HeanueTA
PachnisV
2007 Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat Rev Neurosci 8 466 479
44. AndersonRB
StewartAL
YoungHM
2006 Phenotypes of neural-crest-derived cells in vagal and sacral pathways. Cell Tissue Res 323 11 25
45. YoungHM
NewgreenD
2001 Enteric neural crest-derived cells: origin, identification, migration, and differentiation. Anat Rec 262 1 15
46. PerrisR
PerissinottoD
2000 Role of the extracellular matrix during neural crest cell migration. Mech Dev 95 3 21
47. ChakrabortyG
IngogliaNA
1993 N-terminal arginylation and ubiquitin-mediated proteolysis in nerve regeneration. Brain Res Bull 30 439 445
48. LiuP
JenkinsNA
CopelandNG
2003 A highly efficient recombineering-based method for generating conditional knockout mutations. Genome Res 13 476 484
49. MatsuoI
KurataniS
KimuraC
TakedaN
AizawaS
1995 Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev 9 2646 2658
50. WilkinsonDG
1992 Whole mount in situ hybridization of vertebrate embryos.
WilkinsonDG
In Situ Hybridization, A Practical Approach Oxford IRL Press 75 83
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 3
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
Najčítanejšie v tomto čísle
- Papillorenal Syndrome-Causing Missense Mutations in / Result in Hypomorphic Alleles in Mouse and Human
- HAP2(GCS1)-Dependent Gamete Fusion Requires a Positively Charged Carboxy-Terminal Domain
- Initial Genomics of the Human Nucleolus
- Transgenic Rat Model of Neurodegeneration Caused by Mutation in the Gene