Phosphoinositide Regulation of Integrin Trafficking Required for Muscle Attachment and Maintenance
Muscles must maintain cell compartmentalization when remodeled during development and use. How spatially restricted adhesions are regulated with muscle remodeling is largely unexplored. We show that the myotubularin (mtm) phosphoinositide phosphatase is required for integrin-mediated myofiber attachments in Drosophila melanogaster, and that mtm-depleted myofibers exhibit hallmarks of human XLMTM myopathy. Depletion of mtm leads to increased integrin turnover at the sarcolemma and an accumulation of integrin with PI(3)P on endosomal-related membrane inclusions, indicating a role for Mtm phosphatase activity in endocytic trafficking. The depletion of Class II, but not Class III, PI3-kinase rescued mtm-dependent defects, identifying an important pathway that regulates integrin recycling. Importantly, similar integrin localization defects found in human XLMTM myofibers signify conserved MTM1 function in muscle membrane trafficking. Our results indicate that regulation of distinct phosphoinositide pools plays a central role in maintaining cell compartmentalization and attachments during muscle remodeling, and they suggest involvement of Class II PI3-kinase in MTM-related disease.
Vyšlo v časopise:
Phosphoinositide Regulation of Integrin Trafficking Required for Muscle Attachment and Maintenance. PLoS Genet 7(2): e32767. doi:10.1371/journal.pgen.1001295
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001295
Souhrn
Muscles must maintain cell compartmentalization when remodeled during development and use. How spatially restricted adhesions are regulated with muscle remodeling is largely unexplored. We show that the myotubularin (mtm) phosphoinositide phosphatase is required for integrin-mediated myofiber attachments in Drosophila melanogaster, and that mtm-depleted myofibers exhibit hallmarks of human XLMTM myopathy. Depletion of mtm leads to increased integrin turnover at the sarcolemma and an accumulation of integrin with PI(3)P on endosomal-related membrane inclusions, indicating a role for Mtm phosphatase activity in endocytic trafficking. The depletion of Class II, but not Class III, PI3-kinase rescued mtm-dependent defects, identifying an important pathway that regulates integrin recycling. Importantly, similar integrin localization defects found in human XLMTM myofibers signify conserved MTM1 function in muscle membrane trafficking. Our results indicate that regulation of distinct phosphoinositide pools plays a central role in maintaining cell compartmentalization and attachments during muscle remodeling, and they suggest involvement of Class II PI3-kinase in MTM-related disease.
Zdroje
1. BrowerDL
2003 Platelets with wings: the maturation of Drosophila integrin biology. Curr Opin Cell Biol 15 607 613
2. MayerU
SaherG
FasslerR
BornemannA
EchtermeyerF
1997 Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat Genet 17 318 323
3. VolkT
FesslerLI
FesslerJH
1990 A role for integrin in the formation of sarcomeric cytoarchitecture. Cell 63 525 536
4. CaswellPT
VadrevuS
NormanJC
2009 Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol 10 843 853
5. KaistoT
RahkilaP
MarjomakiV
PartonRG
MetsikkoK
1999 Endocytosis in skeletal muscle fibers. Exp Cell Res 253 551 560
6. YuanL
FairchildMJ
PerkinsAD
TanentzapfG
2010 Analysis of integrin turnover in fly myotendinous junctions. J Cell Sci 123 939 946
7. Di PaoloG
De CamilliP
2006 Phosphoinositides in cell regulation and membrane dynamics. Nature 443 651 657
8. NicotAS
LaporteJ
2008 Endosomal phosphoinositides and human diseases. Traffic 9 1240 1249
9. Buj-BelloA
LaugelV
MessaddeqN
ZahreddineH
LaporteJ
2002 The lipid phosphatase myotubularin is essential for skeletal muscle maintenance but not for myogenesis in mice. Proc Natl Acad Sci U S A 99 15060 15065
10. LaporteJ
HuLJ
KretzC
MandelJL
KioschisP
1996 A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast. Nat Genet 13 175 182
11. BolinoA
MugliaM
ConfortiFL
LeGuernE
SalihMA
2000 Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2. Nat Genet 25 17 19
12. BergerP
BonneickS
WilliS
WymannM
SuterU
2002 Loss of phosphatase activity in myotubularin-related protein 2 is associated with Charcot-Marie-Tooth disease type 4B1. Hum Mol Genet 11 1569 1579
13. CaoC
BackerJM
LaporteJ
BedrickEJ
Wandinger-NessA
2008 Sequential actions of myotubularin lipid phosphatases regulate endosomal PI(3)P and growth factor receptor trafficking. Mol Biol Cell 19 3334 3346
14. DowlingJJ
VreedeAP
LowSE
GibbsEM
KuwadaJY
2009 Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy. PLoS Genet 5 e1000372 doi:10.1371/journal.pgen.1000372
15. KimSA
TaylorGS
TorgersenKM
DixonJE
2002 Myotubularin and MTMR2, phosphatidylinositol 3-phosphatases mutated in myotubular myopathy and type 4B Charcot-Marie-Tooth disease. J Biol Chem 277 4526 4531
16. TaylorGS
MaehamaT
DixonJE
2000 Inaugural article: myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. Proc Natl Acad Sci U S A 97 8910 8915
17. TsujitaK
ItohT
IjuinT
YamamotoA
ShishevaA
2004 Myotubularin regulates the function of the late endosome through the gram domain-phosphatidylinositol 3,5-bisphosphate interaction. J Biol Chem 279 13817 13824
18. VelichkovaM
JuanJ
KadandaleP
JeanS
RibeiroI
2010 Drosophila Mtm and class II PI3K coregulate a PI(3)P pool with cortical and endolysosomal functions. J Cell Biol 190 407 425
19. LindmoK
StenmarkH
2006 Regulation of membrane traffic by phosphoinositide 3-kinases. J Cell Sci 119 605 614
20. FalascaM
HughesWE
DominguezV
SalaG
FostiraF
2007 The role of phosphoinositide 3-kinase C2alpha in insulin signaling. J Biol Chem 282 28226 28236
21. MaffucciT
CookeFT
FosterFM
TraerCJ
FryMJ
2005 Class II phosphoinositide 3-kinase defines a novel signaling pathway in cell migration. J Cell Biol 169 789 799
22. SrivastavaS
DiL
ZhdanovaO
LiZ
VardhanaS
2009 The class II phosphatidylinositol 3 kinase C2beta is required for the activation of the K+ channel KCa3.1 and CD4 T-cells. Mol Biol Cell 20 3783 3791
23. WenPJ
OsborneSL
MorrowIC
PartonRG
DominJ
2008 Ca2+-regulated pool of phosphatidylinositol-3-phosphate produced by phosphatidylinositol 3-kinase C2alpha on neurosecretory vesicles. Mol Biol Cell 19 5593 5603
24. RoyS
VijayRaghavanK
1998 Patterning muscles using organizers: larval muscle templates and adult myoblasts actively interact to pattern the dorsal longitudinal flight muscles of Drosophila. J Cell Biol 141 1135 1145
25. WasserM
Bte OsmanZ
ChiaW
2007 EAST and Chromator control the destruction and remodeling of muscles during Drosophila metamorphosis. Dev Biol 307 380 393
26. KozopasKM
SamosCH
NusseR
1998 DWnt-2, a Drosophila Wnt gene required for the development of the male reproductive tract, specifies a sexually dimorphic cell fate. Genes Dev 12 1155 1165
27. Al-QusairiL
WeissN
ToussaintA
BerbeyC
MessaddeqN
2009 T-tubule disorganization and defective excitation-contraction coupling in muscle fibers lacking myotubularin lipid phosphatase. Proc Natl Acad Sci U S A 106 18763 18768
28. RazzaqA
RobinsonIM
McMahonHT
SkepperJN
SuY
2001 Amphiphysin is necessary for organization of the excitation-contraction coupling machinery of muscles, but not for synaptic vesicle endocytosis in Drosophila. Genes Dev 15 2967 2979
29. WilcoxM
DiAntonioA
LeptinM
1989 The function of PS integrins in Drosophila wing morphogenesis. Development 107 891 897
30. WalshEP
BrownNH
1998 A screen to identify Drosophila genes required for integrin-mediated adhesion. Genetics 150 791 805
31. ErvastiJM
2003 Costameres: the Achilles' heel of Herculean muscle. J Biol Chem 278 13591 13594
32. SparrowJC
SchockF
2009 The initial steps of myofibril assembly: integrins pave the way. Nat Rev Mol Cell Biol 10 293 298
33. PerkinsAD
EllisSJ
AsghariP
ShamsianA
MooreED
2010 Integrin-mediated adhesion maintains sarcomeric integrity. Dev Biol 338 15 27
34. MacDougallLK
GagouME
LeeversSJ
HafenE
WaterfieldMD
2004 Targeted expression of the class II phosphoinositide 3-kinase in Drosophila melanogaster reveals lipid kinase-dependent effects on patterning and interactions with receptor signaling pathways. Mol Cell Biol 24 796 808
35. ChaussadeC
PirolaL
BonnafousS
BlondeauF
Brenz-VercaS
2003 Expression of myotubularin by an adenoviral vector demonstrates its function as a phosphatidylinositol 3-phosphate [PtdIns(3)P] phosphatase in muscle cell lines: involvement of PtdIns(3)P in insulin-stimulated glucose transport. Mol Endocrinol 17 2448 2460
36. DominJ
HarperL
AubynD
WheelerM
FloreyO
2005 The class II phosphoinositide 3-kinase PI3K-C2beta regulates cell migration by a PtdIns3P dependent mechanism. J Cell Physiol 205 452 462
37. FiliN
CallejaV
WoscholskiR
ParkerPJ
LarijaniB
2006 Compartmental signal modulation: Endosomal phosphatidylinositol 3-phosphate controls endosome morphology and selective cargo sorting. Proc Natl Acad Sci U S A 103 15473 15478
38. IvaskaJ
WhelanRD
WatsonR
ParkerPJ
2002 PKC epsilon controls the traffic of beta1 integrins in motile cells. EMBO J 21 3608 3619
39. PellinenT
ArjonenA
VuoriluotoK
KallioK
FransenJA
2006 Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of beta1-integrins. J Cell Biol 173 767 780
40. PowelkaAM
SunJ
LiJ
GaoM
ShawLM
2004 Stimulation-dependent recycling of integrin beta1 regulated by ARF6 and Rab11. Traffic 5 20 36
41. NicotAS
ToussaintA
ToschV
KretzC
Wallgren-PetterssonC
2007 Mutations in amphiphysin 2 (BIN1) disrupt interaction with dynamin 2 and cause autosomal recessive centronuclear myopathy. Nat Genet 39 1134 1139
42. BeumerK
MatthiesHJ
BradshawA
BroadieK
2002 Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development. Development 129 3381 3391
43. MathewD
PopescuA
BudnikV
2003 Drosophila amphiphysin functions during synaptic Fasciclin II membrane cycling. J Neurosci 23 10710 10716
44. RegaladoMP
Terry-LorenzoRT
WaitesCL
GarnerCC
MalenkaRC
2006 Transsynaptic signaling by postsynaptic synapse-associated protein 97. J Neurosci 26 2343 2357
45. BolinoA
BolisA
PrevitaliSC
DinaG
BussiniS
2004 Disruption of Mtmr2 produces CMT4B1-like neuropathy with myelin outfolding and impaired spermatogenesis. J Cell Biol 167 711 721
46. LeeHW
KimY
HanK
KimH
KimE
2010 The phosphoinositide 3-phosphatase MTMR2 interacts with PSD-95 and maintains excitatory synapses by modulating endosomal traffic. J Neurosci 30 5508 5518
47. HayashiYK
ChouFL
EngvallE
OgawaM
MatsudaC
1998 Mutations in the integrin alpha7 gene cause congenital myopathy. Nat Genet 19 94 97
48. BarrosCS
NguyenT
SpencerKS
NishiyamaA
ColognatoH
2009 Beta1 integrins are required for normal CNS myelination and promote AKT-dependent myelin outgrowth. Development 136 2717 2724
49. JuhaszG
HillJH
YanY
SassM
BaehreckeEH
2008 The class III PI(3)K Vps34 promotes autophagy and endocytosis but not TOR signaling in Drosophila. J Cell Biol 181 655 666
50. Quinones-CoelloAT
PetrellaLN
AyersK
MelilloA
MazzalupoS
2007 Exploring strategies for protein trapping in Drosophila. Genetics 175 1089 1104
51. PulipparacharuvilS
AkbarMA
RayS
SevrioukovEA
HabermanAS
2005 Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J Cell Sci 118 3663 3673
52. WucherpfennigT
Wilsch-BrauningerM
Gonzalez-GaitanM
2003 Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol 161 609 624
53. EntchevEV
SchwabedissenA
Gonzalez-GaitanM
2000 Gradient formation of the TGF-beta homolog Dpp. Cell 103 981 991
54. ScottRC
SchuldinerO
NeufeldTP
2004 Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev Cell 7 167 178
55. TanentzapfG
BrownNH
2006 An interaction between integrin and the talin FERM domain mediates integrin activation but not linkage to the cytoskeleton. Nat Cell Biol 8 601 606
56. BogaertT
BrownN
WilcoxM
1987 The Drosophila PS2 antigen is an invertebrate integrin that, like the fibronectin receptor, becomes localized to muscle attachments. Cell 51 929 940
57. MorrisonHA
DionneH
RustenTE
BrechA
FisherWW
2008 Regulation of early endosomal entry by the Drosophila tumor suppressors Rabenosyn and Vps45. Mol Biol Cell 19 4167 4176
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 2
- 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
- Meta-Analysis of Genome-Wide Association Studies in Celiac Disease and Rheumatoid Arthritis Identifies Fourteen Non-HLA Shared Loci
- MiRNA Control of Vegetative Phase Change in Trees
- The Cardiac Transcription Network Modulated by Gata4, Mef2a, Nkx2.5, Srf, Histone Modifications, and MicroRNAs
- Genome-Wide Transcript Profiling of Endosperm without Paternal Contribution Identifies Parent-of-Origin–Dependent Regulation of