Myosin VI in PC12 cells plays important roles in cell migration and proliferation but not in catecholamine secretion

Journal of Muscle Research and Cell Motility

Volumn 32, Issue 4-5, 2011, Pages 291-302

  Majewski, Łukasz ^a   Sobczak, Magdalena ^a   Wasik, Anna ^a   Skowronek, Krzysztof ^a   Rędowicz, Maria Jolanta ^a  

^a NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

Author keywords

Actin cytoskeleton; Catecholamine secretion; Cell motility; Golgi apparatus; Myosin VI

Indexed keywords

EID: 82955163926     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-011-9279-0     Document Type: Article

References (56)

1. D Altman D Goswami, et al. 2007 Precise positioning of myosin VI on endocytic vesicles in vivo PLoS Biol 5 e210 17683200 10.1371/journal.pbio. 0050210 (Pubitemid 47328275)
2. N Ameen G Apodaca 2007 Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice Traffic 8 998 1006 17555536 10.1111/j.1600-0854.2007.00587.x 1:CAS:528:DC%2BD2sXovVylu74%3D (Pubitemid 47074034)
3. SD Arden C Puri, et al. 2007 Myosin VI is required for targeted membrane transport during cytokinesis Mol Biol Cell 18 4750 4761 17881731 10.1091/mbc.E07-02-0127 1:CAS:528:DC%2BD2sXhsVeisrfK (Pubitemid 350246678)
4. L Aschenbrenner TT Lee, et al. 2003 Myo6 facilitates the translocation of endocytic vesicles from cell peripheries Mol Biol Cell 14 2728 2743 12857860 10.1091/mbc.E02-11-0767 1:CAS:528:DC%2BD3sXlslWgtrY%3D (Pubitemid 36871517)
5. JSY Au C Puri, et al. 2007 Myosin VI is required for sorting of AP-1B-dependent cargo to the basolateral domain in polarized MDCK cells J Cell Biol 177 103 114 17403927 10.1083/jcb.200608126 1:CAS:528:DC%2BD2sXktlKltro%3D (Pubitemid 46588405)
6. MF Bader RW Holz, et al. 2002 Exocytosis: the chromaffin cell as a model system Ann NY Acad Sci 971 178 183 12438117 10.1111/j.1749-6632.2002.tb04461.x 1:CAS:528:DC%2BD38XovFalsrg%3D (Pubitemid 35305291)
7. F Buss J Kendrick-Jones 2008 How are the cellular functions of myosin VI regulated within the cell Biochem Biophys Res Commun 369 165 175 18068125 10.1016/j.bbrc.2007.11.150 1:CAS:528:DC%2BD1cXjs12rs74%3D
8. F Buss J Kendrick-Jones 2011 Multifunctional myosin VI has a multitude of cargoes Proc Natl Acad Sci USA 108 5927 5928 21464329 10.1073/pnas.1103086108 1:CAS:528:DC%2BC3MXltVymtrg%3D
9. F Buss J Kendrick-Jones, et al. 1998 The localization of myosin VI at the Golgi complex and leading edge of fibroblasts and recruitment into membrane ruffles of A431 cells after growth factor stimulation J Cell Biol 143 1535 1545 9852149 10.1083/jcb.143.6.1535 1:CAS:528:DyaK1MXotQ%3D%3D (Pubitemid 29006501)
10. F Buss SD Arden, et al. 2001 Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis EMBO J 20 3676 3684 11447109 10.1093/emboj/20.14.3676 1:CAS:528:DC%2BD3MXlsVKrsrs%3D (Pubitemid 32691779)
11. F Buss JP Luzio, et al. 2002 Myosin VI, an actin motor for membrane traffic and cell migration Traffic 3 851 858 12453148 10.1034/j.1600-0854.2002. 31201.x 1:CAS:528:DC%2BD38XpsVOrs7g%3D (Pubitemid 35460590)
12. MV Chibalina C Puri, et al. 2009 Potential roles of myosin VI in cell motility Biochem Soc Trans 37 966 970 19754433 10.1042/BST0370966 1:CAS:528:DC%2BD1MXhtFGls7fJ
13. MV Chibalina A Poliakov, et al. 2010 Myosin VI and optineurin are required for polarized EGFR delivery and directed migration Traffic 11 1290 1303 20604900 10.1111/j.1600-0854.2010.01101.x 1:CAS:528:DC%2BC3cXht1CmsLzL
14. T Dumitrescu Pene SD Rose, et al. 2005 Expression of various scinderin domains in chromaffin cells indicates that this protein acts as a molecular switch in the control of actin filament dynamics and exocytosis J Neurochem 92 780 789 15686479 10.1111/j.1471-4159.2004.02907.x (Pubitemid 40229549)
15. SC Francis C Sunshine, et al. 2002 Coordinate regulation of catecholamine uptake by rab3 and phosphoinositide 3-kinase J Biol Chem 277 7816 7823 11748228 10.1074/jbc.M109743200 1:CAS:528:DC%2BD38XitFynu7o%3D (Pubitemid 34968229)
16. ER Geisbrecht DJ Montell 2002 Myosin VI is required for E-cadherin-mediated border cell migration Nat Cell Biol 4 616 620 12134162 1:CAS:528:DC%2BD38Xls1OrtLY%3D
17. D Giner P Neco, et al. 2005 Real-time dynamics of the F-actin cytoskeleton during secretion from chromaffin cells J Cell Sci 118 2871 2880 15976446 10.1242/jcs.02419 1:CAS:528:DC%2BD2MXnsVCjtrc%3D (Pubitemid 41136364)
18. N Gotoh Q Yan, et al. 2010 Altered renal proximal tubular endocytosis and histology in mice lacking myosin-VI Cytoskeleton 67 178 192 20175219 1:CAS:528:DC%2BC3cXkvFOntrs%3D
19. R Hertzano E Shalit, et al. 2008 A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells PLoS Genet 4 e1000207 18833301 10.1371/journal.pgen.1000207
20. JL Hicks WM Deng, et al. 1999 Class VI unconventional myosin is required for spermatogenesis in Drosophila Mol Biol Cell 10 4341 4353 10588662 1:CAS:528:DyaK1MXnvFKqtr4%3D
21. JP Holt K Bottomly, et al. 2007 Assessment of myosin II, Va, VI and VIIa loss of function on endocytosis and endocytic vesicle motility in bone marrow-derived dendritic cells Cell Motil Cytoskeleton 64 756 766 17615572 10.1002/cm.20220 1:CAS:528:DC%2BD2sXhtF2rsbvK (Pubitemid 47479810)
22. V Hook MH Metz-Boutigue 2002 Protein trafficking to chromaffin granules and proteolytic processing within regulated secretory vesicles of neuroendocrine chromaffin cells Ann NY Acad Sci 971 397 405 12438158 10.1111/j.1749-6632.2002. tb04502.x 1:CAS:528:DC%2BD38XovFaltrw%3D (Pubitemid 35305332)
23. R Jahn T Lang, et al. 2003 Membrane fusion Cell 112 519 533 12600315 10.1016/S0092-8674(03)00112-0 1:CAS:528:DC%2BD3sXhs1SnsLY%3D (Pubitemid 36263084)
24. JM Jbireal C Strell, et al. 2010 The selective role of myosin VI in lymphoid leukemia cell migration Leuk Res 34 1656 1662 20493527 10.1016/j.leukres.2010.04.018
25. DJ Kurz S Decary, et al. 2000 Senescence-associated (beta)-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells J Cell Sci 113 3613 3622 11017877 1:CAS:528: DC%2BD3cXosVKgtb0%3D
26. T Lang I Wacker, et al. 2000 Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells Biophys J 78 2863 2877 10827968 10.1016/S0006-3495(00)76828-7 1:CAS:528:DC%2BD3cXjvFOhurc%3D (Pubitemid 30396920)
27. I Lister S Schmitz, et al. 2004 A monomeric myosin VI with a large working stroke EMBO J 23 1729 1738 15044955 10.1038/sj.emboj.7600180 1:CAS:528:DC%2BD2cXjt1Clsrs%3D (Pubitemid 38649636)
28. L Majewski M Sobczak, et al. 2010 Myosin VI is associated with secretory granules and is present in nucleus in adrenal medulla chromaffin cells Acta Biochim Polon 57 109 114 20198214 1:CAS:528:DC%2BC3cXktlWnurk%3D
29. S Mangold SK Wu, et al. 2011 Hepatocyte growth factor acutely perturbs actin filament anchorage at the epithelial zonula adherens Curr Biol 21 503 507 21396819 10.1016/j.cub.2011.02.018 1:CAS:528:DC%2BC3MXjsFynsb0%3D
30. TFJ Martin RN Grishanin 2003 PC12 cells as a model for studies of regulated secretion in neuronal and endocrine cells Meth Cell Biol 71 267 286 10.1016/S0091-679X(03)01012-4 1:CAS:528:DC%2BD3sXmvF2mtLg%3D (Pubitemid 137639599)
31. V Mermall JG McNally, et al. 1994 Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embryos Nature 369 560 562 8202156 10.1038/369560a0 1:CAS:528:DyaK2cXksFChtLw%3D (Pubitemid 24192523)
32. SM Morris SD Arden, et al. 2002 Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton Traffic 3 331 341 11967127 10.1034/j.1600-0854.2002.30503.x 1:CAS:528:DC%2BD38XjvFCgtbw%3D (Pubitemid 34461043)
33. P Neco O Rossetto, et al. 2003 Taipoxin induces F-actin fragmentation and enhances release of catecholamines in bovine chromaffin cells J Neurochem 85 329 337 12675909 10.1046/j.1471-4159.2003.01682.x 1:CAS:528:DC%2BD3sXjtlylsr4%3D (Pubitemid 36438329)
34. P Neco D Giner, et al. 2004 New roles of myosin II during vesicle transport and fusion in chromaffin cells J Biol Chem 279 27450 27457 15069078 10.1074/jbc.M311462200 1:CAS:528:DC%2BD2cXkvFGnt7c%3D (Pubitemid 38812584)
35. T Noguchi DJ Frank, et al. 2009 Coiled-coil-mediated dimerization is not required for myosin VI to stabilize actin during spermatid individualization in Drosophila melanogaster Mol Biol Cell 20 358 367 19005209 10.1091/mbc.E08-07- 0776 1:CAS:528:DC%2BD1MXht1Srsr0%3D
36. E Osterweil DG Wells, et al. 2005 A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis J Cell Biol 168 329 338 15657400 10.1083/jcb.200410091 1:CAS:528:DC%2BD2MXlvVGguw%3D%3D (Pubitemid 40248229)
37. C Petritsch G Tavosanis, et al. 2003 The Drosophila myosin VI Jaguar is required for basal protein targeting and correct spindle orientation in mitotic neuroblasts Dev Cell 4 273 281 12586070 10.1016/S1534-5807(03)00020-0 1:CAS:528:DC%2BD3sXhsFKntrc%3D (Pubitemid 36221803)
38. MJ Redowicz 2002 Myosins and pathology: genetics and biology Acta Biochim Pol 49 789 804 12545186 1:CAS:528:DC%2BD3sXnvVGmsw%3D%3D (Pubitemid 135702931)
39. SD Rose T Lejen, et al. 2002 Molecular motors involved in chromaffin cell secretion Ann NY Acad Sci 971 222 231 12438122 10.1111/j.1749-6632.2002. tb04466.x 1:CAS:528:DC%2BD38XovFals78%3D (Pubitemid 35305296)
40. SD Rose T Lejen, et al. 2003 Myosins II and V in chromaffin cells: myosin V is a chromaffin vesicle molecular motor involved in secretion J Neurochem 85 287 298 12675905 10.1046/j.1471-4159.2003.01649.x 1:CAS:528:DC%2BD3sXjtlymu7g%3D (Pubitemid 36438325)
41. R Rudolf T Kogel, et al. 2003 Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12 cells J Cell Sci 116 1339 1348 12615975 10.1242/jcs.00317 1:CAS:528:DC%2BD3sXivFWhu70%3D (Pubitemid 36410671)
42. N Sasakawa M Ohara-Imaizumi, et al. 2002 Roles of actin filaments and the actin-myosin interaction in the regulation of exocytosis in chromaffin cells Ann NY Acad Sci 971 273 274 12438132 10.1111/j.1749-6632.2002.tb04476.x 1:CAS:528:DC%2BD38XovFals7Y%3D (Pubitemid 35305306)
43. G Spudich MV Chibalina, et al. 2007 Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to Disabled-2 and PtdIns(4,5)P2 Nat Cell Biol 9 176 183 17187061 10.1038/ncb1531 1:CAS:528:DC%2BD2sXhtFGlsbs%3D (Pubitemid 46420860)
44. HL Sweeney A Houdusse 2007 What can myosin VI do in cells? Curr Opin Cell Biol 19 57 66 17175153 10.1016/j.ceb.2006.12.005 1:CAS:528: DC%2BD2sXpvVOgsg%3D%3D (Pubitemid 46123971)
45. JM Trifaro 2002 Molecular biology of the chromaffin cell Ann NY Acad Sci 971 11 18 12438083 10.1111/j.1749-6632.2002.tb04427.x 1:CAS:528: DC%2BD38XovFamtbw%3D
46. JM Trifaró RW Lee 1980 Morphological characteristics and stimulus-secretion coupling in bovine adrenal chromaffin cell cultures Neuroscience 5 1533 1546 7422128 10.1016/0306-4522(80)90018-4 (Pubitemid 10056768)
47. ML Vitale A Rodriguez del Castillo, et al. 1991 Cortical filamentous actin disassembly and scinderin redistribution during chromaffin cell stimulation precede exocytosis, a phenomenon not exhibited by gelsolin J Cell Biol 113 1057 1067 1645735 10.1083/jcb.113.5.1057 1:CAS:528:DyaK3MXit1Wqsrw%3D (Pubitemid 21909738)
48. (2+) -evoked catecholamine release J Neurochem 59 1717 1728 1402916 10.1111/j.1471-4159.1992.tb11003.x 1:CAS:528:DyaK38Xmt1Kqs7s%3D
49. S Vreugde C Ferrai, et al. 2006 Nuclear myosin VI enhances RNA polymerase II-dependent transcription Mol Cell 23 749 755 16949370 10.1016/j.molcel.2006. 07.005 1:CAS:528:DC%2BD28XhtVSkt7rF (Pubitemid 44292554)
50. MC Wagner B Baryłko, et al. 1992 Tissue distribution and subcellular localization of mammalian myosin I J Cell Biol 119 163 170 1527166 10.1083/jcb.119.1.163 1:CAS:528:DyaK38XlvVykuro%3D
51. CL Warner A Stewart, et al. 2003 Loss of myosin VI reduces secretion and the size of the Golgi in fibroblasts from Snell's waltzer mice EMBO J 22 569 579 12554657 10.1093/emboj/cdg055 1:CAS:528:DC%2BD3sXitlKks78%3D (Pubitemid 36193601)
52. 2+ -dependent binding of syntaxin-1A Mol Biol Cell 16 4519 4530 16030255 10.1091/mbc.E05-03-0252 1:CAS:528:DC%2BD2MXhtVygtL7J (Pubitemid 41416438)
53. AL Wells AW Lin, et al. 1999 Myosin VI is an actin-based motor that moves backwards Nature 401 505 508 10519557 10.1038/46835 1:CAS:528: DyaK1MXmslyqs7c%3D (Pubitemid 29470212)
54. H Wu JE Nash, et al. 2002 Interaction of SAP97 with minus-end directed actin motor protein myosin VI: implications for AMPA receptor trafficking J Biol Chem 277 30928 30934 12050163 10.1074/jbc.M203735200 1:CAS:528: DC%2BD38XmsFyqu70%3D (Pubitemid 34970794)
55. H Yano I Ninan, et al. 2006 BDNF-mediated neurotransmission relies on upon a myosin VI motor complex Nat Neurosci 9 1009 1018 16819522 10.1038/nn1730 1:CAS:528:DC%2BD28Xnt12jsrk%3D (Pubitemid 44264913)
56. H Yoshida W Cheng, et al. 2004 Lessons from border cell migration in the Drosophila ovary: A role for myosin VI in disseminaton of human ovarian cancer Proc Natl Acad Sci USA 101 8144 8149 15146066 10.1073/pnas.0400400101 1:CAS:528:DC%2BD2cXkslCit7o%3D (Pubitemid 38698068)