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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

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Genetika Reprodukčná medicína

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PLOS Genetics


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