Myo19 is an outer mitochondrial membrane motor and effector of starvation-induced filopodia

Journal of Cell Science

Volumn 129, Issue 3, 2016, Pages 543-556

  Shneyer, Boris I ^a   Ušaj, Marko ^a   Henn, Arnon ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

Filopodia; Mitochondria; Myosin 19

Indexed keywords

GLUCOSE; MOLECULAR MOTOR; MYO19 PROTEIN; UNCLASSIFIED DRUG; MYO19 PROTEIN, HUMAN; MYOSIN;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL STRESS; FILOPODIUM; MITOCHONDRIAL MEMBRANE; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; RNA INTERFERENCE; U2OS CELL LINE; CELL LINE; HEK293 CELL LINE; HUMAN; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; PHYSIOLOGY; PSEUDOPODIUM; STARVATION;

CELL LINE; HEK293 CELLS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANES; MOLECULAR MOTOR PROTEINS; MYOSINS; PSEUDOPODIA; RNA INTERFERENCE; STARVATION;

EID: 84957651017     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.175349     Document Type: Article

References (71)

1. Acker, T. and Plate, K. H. (2002). A role for hypoxia and hypoxia-inducible transcription factors in tumor physiology. J. Mol. Med. 80, 562-575.
2. Adikes, R. C., Unrath, W. C., Yengo, C. M. and Quintero, O. A. (2013). Biochemical and bioinformatic analysis of the myosin-XIX motor domain. Cytoskeleton 70, 281-295.
3. Arber, S., Barbayannis, F. A., Hanser, H., Schneider, C., Stanyon, C. A., Bernard, O. and Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805-809.
4. Arismendi-Morillo, G., Hoa, N. T., Ge, L. and Jadus, M. R. (2012). Mitochondrial network in glioma's invadopodia displays an activated state both in situ and in vitro: potential functional implications. Ultrastruct. Pathol. 36, 409-414.
5. Berg, J. S. and Cheney, R. E. (2002). Myosin-X is an unconventional myosin that undergoes intrafilopodial motility. Nat. Cell Biol. 4, 246-250.
6. Bohil, A. B., Robertson, B. W. and Cheney, R. E. (2006). Myosin-X is a molecular motor that functions in filopodia formation. Proc. Natl. Acad. Sci. USA 103, 12411-12416.
7. Borgese, N., Gazzoni, I., Barberi, M., Colombo, S. and Pedrazzini, E. (2001). Targeting of a tail-anchored protein to endoplasmic reticulum and mitochondrial outer membrane by independent but competing pathways. Mol. Biol. Cell 12, 2482-2496.
8. Borgese, N., Brambillasca, S. and Colombo, S. (2007). How tails guide tailanchored proteins to their destinations. Curr. Opin. Cell Biol. 19, 368-375.
9. Bradley, T. J. and Satir, P. (1979). Evidence of microfilament-associated mitochondrial movement. J. Supramol. Struct. 12, 165-175.
10. Burnette, D. T., Manley, S., Sengupta, P., Sougrat, R., Davidson, M. W., Kachar, B. and Lippincott-Schwartz, J. (2011). A role for actin arcs in the leading-edge advance of migrating cells. Nat. Cell Biol. 13, 371-382.
11. Chada, S. R. and Hollenbeck, P. J. (2004). Nerve growth factor signaling regulates motility and docking of axonal mitochondria. Curr. Biol. 14, 1272-1276.
12. Chen, H. and Chan, D. C. (2009). Mitochondrial dynamics-fusion, fission, movement, and mitophagy-in neurodegenerative diseases. Hum. Mol. Genet. 18, R169-R176.
13. Cserzo, M., Wallin, E., Simon, I., von Heijne, G. and Elofsson, A. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: Application of the Dense Alignment Surface method.
14. Davenport, R. W., Dou, P., Mills, L. R. and Kater, S. B. (1996). Distinct calcium signaling within neuronal growth cones and filopodia. J. Neurobiol. 31, 1-15.
15. de Kroon, A. I. P. M., Dolis, D., Mayer, A., Lill, R. and de Kruijff, B. (1997). Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa. Is cardiolipin present in the mitochondrial outer membrane? Biochim. Biophys. Acta 1325, 108-116.
16. De La Cruz, E. M. and Ostap, E. M. (2004). Relating biochemistry and function in the myosin superfamily. Curr. Opin. Cell Biol. 16, 61-67.
17. Desai, S. P., Bhatia, S. N., Toner, M. and Irimia, D. (2013). Mitochondrial localization and the persistent migration of epithelial cancer cells. Biophys. J. 104, 2077-2088.
18. Diaz, B., Shani, G., Pass, I., Anderson, D., Quintavalle, M. and Courtneidge, S. A. (2009). Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci. Signal. 2, ra53.
19. Fan, X., Hussien, R. and Brooks, G. A. (2010). H2O2-induced mitochondrial fragmentation in C2C12 myocytes. Free Radic. Biol. Med. 49, 1646-1654.
20. Faulkner, A. and Jones, C. T. (1978). Some effects of glucose concentration and anoxia on glycolysis and metabolite concentrations in the perfused liver of fetal guinea pig. Biochim. Biophy. Acta 538, 106-119.
21. Federico, A., Cardaioli, E., Da Pozzo, P., Formichi, P., Gallus, G. N. and Radi, E. (2012). Mitochondria, oxidative stress and neurodegeneration. J. Neurol. Sci. 322, 254-262.
22. Folkman, J. (2002). Role of angiogenesis in tumor growth and metastasis. Semin. Oncol. 29, 15-18.
23. Fujiki, Y., Hubbard, A. L., Fowler, S. and Lazarow, P. B. (1982). Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102.
24. Gautier, R., Douguet, D., Antonny, B. and Drin, G. (2008). HELIQUEST: a web server to screen sequences with specific alpha-helical properties. Bioinformatics 24, 2101-2102.
25. Geeves, M. A., Fedorov, R. and Manstein, D. J. (2005). Molecular mechanism of actomyosin-based motility. Cell. Mol. Life Sci. 62, 1462-1477.
26. Graham, N. A., Tahmasian, M., Kohli, B., Komisopoulou, E., Zhu, M., Vivanco, I., Teitell, M. A., Wu, H., Ribas, A., Lo, R. S. et al. (2012). Glucose deprivation activates a metabolic and signaling amplification loop leading to cell death. Mol. Syst. Biol. 8, 589.
27. Hardie, D. G., Ross, F. A. and Hawley, S. A. (2012). AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat. Rev. Mol. Cell Biol. 13, 251-262.
28. Henn, A. and Sadot, E. (2014). The unique enzymatic and mechanistic properties of plant myosins. Curr. Opin. Plant Biol. 22, 65-70.
29. Henn, A., Cao, W., Licciardello, N., Heitkamp, S. E., Hackney, D. D. and De La Cruz, E. M. (2010). Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA. Proc. Natl. Acad. Sci. USA 107, 4046-4050.
30. Hirayama, A., Kami, K., Sugimoto, M., Sugawara, M., Toki, N., Onozuka, H., Kinoshita, T., Saito, N., Ochiai, A., Tomita, M. et al. (2009). Quantitative metabolome profiling of colon and stomach cancer microenvironment by capillary electrophoresis time-of-flight mass spectrometry. Cancer Res. 69, 4918-4925.
31. Hokanson, D. E. and Ostap, E. M. (2006). Myo1c binds tightly and specifically to phosphatidylinositol 4, 5-bisphosphate and inositol 1, 4, 5-trisphosphate. Proc. Natl. Acad. Sci. USA 103, 3118-3123.
32. Hristova, K., Wimley, W. C., Mishra, V. K., Anantharamiah, G. M., Segrest, J. P. and White, S. H. (1999). An amphipathic alpha-helix at a membrane interface: a structural study using a novel X-ray diffraction method. J. Mol. Biol. 290, 99-117.
33. Jalali, A., Amirian, E. S., Bainbridge, M. N., Armstrong, G. N., Liu, Y., Tsavachidis, S., Jhangiani, S. N., Plon, S. E., Lau, C. C., Claus, E. B. et al. (2015). Targeted sequencing in chromosome 17q linkage region identifies familial glioma candidates in the gliogene consortium. Sci. Rep. 5, 8278.
34. Jayashankar, V. and Rafelski, S. M. (2014). Integrating mitochondrial organization and dynamics with cellular architecture. Curr. Opin. Cell Biol. 26, 34-40.
35. Kanaji, S., Iwahashi, J., Kida, Y., Sakaguchi, M. and Mihara, K. (2000). Characterization of the signal that directs Tom20 to the mitochondrial outer membrane. J. Cell Biol. 151, 277-288.
36. Kaufmann, T., Schlipf, S., Sanz, J., Neubert, K., Stein, R. and Borner, C. (2003). Characterization of the signal that directs Bcl-x(L), but not Bcl-2, to the mitochondrial outer membrane. J. Cell Biol. 160, 53-64.
37. Korobova, F., Gauvin, T. J. and Higgs, H. N. (2014). A role for myosin II in mammalian mitochondrial fission. Curr. Biol. 24, 409-414.
38. Kyte, J. and Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
39. Lan, Y. and Papoian, G. A. (2008). The stochastic dynamics of filopodial growth. Biophys. J. 94, 3839-3852.
40. Lin, M. T. and Beal, M. F. (2006). Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787-795.
41. Machesky, L. M. (2008). Lamellipodia and filopodia in metastasis and invasion. FEBS Lett. 582, 2102-2111.
42. Mallavarapu, A. and Mitchison, T. (1999). Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J. Cell Biol. 146, 1097-1106.
43. Merritt, R. C., Manor, U., Salles, F. T., Grati, M., Dose, A. C., Unrath, W. C., Quintero, O. A., Yengo, C. M. and Kachar, B. (2012). Myosin IIIB uses an actinbinding motif in its espin-1 cargo to reach the tips of actin protrusions. Curr. Biol. 22, 320-325.
44. Miki, H., Sasaki, T., Takai, Y. and Takenawa, T. (1998). Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93-96.
45. Minin, A. A., Kulik, A. V., Gyoeva, F. K., Li, Y., Goshima, G. and Gelfand, V. I. (2006). Regulation of mitochondria distribution by RhoA and formins. J. Cell Sci. 119, 659-670.
46. Moruno, F., Perez-Jimenez, E. and Knecht, E. (2012). Regulation of autophagy by glucose in Mammalian cells. Cells 1, 372-395.
47. Nunnari, J. and Suomalainen, A. (2012). Mitochondria: in sickness and in health. Cell 148, 1145-1159.
48. Olguin-Albuerne, M. and Moran, J. (2015). ROSproduced by NOX2 control in vitro development of cerebellar granule neurons development. ASN Neuro 7, pii: 1759091415578712.
49. Otto, M. R., Lillo, M. P. and Beechem, J. M. (1994). Resolution of multiphasic reactions by the combination of fluorescence total-intensity and anisotropy stopped-flow kinetic experiments. Biophys. J. 67, 2511-2521.
50. Petrie, R. J., Doyle, A. D. and Yamada, K. M. (2009). Random versus directionally persistent cell migration. Nat. Rev. Mol. Cell Biol. 10, 538-549.
51. Pilling, A. D., Horiuchi, D., Lively, C. M. and Saxton, W. M. (2006). Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol. Biol. Cell 17, 2057-2068.
52. Quintero, O. A., DiVito, M. M., Adikes, R. C., Kortan, M. B., Case, L. B., Lier, A. J., Panaretos, N. S., Slater, S. Q., Rengarajan, M., Feliu, M. et al. (2009). Human Myo19 is a novel myosin that associates with mitochondria. Curr. Biol. 19, 2008-2013.
53. Rambold, A. S., Kostelecky, B., Elia, N. and Lippincott-Schwartz, J. (2011). Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc. Natl. Acad. Sci. USA 108, 10190-10195.
54. Rapaport, D. (2003). Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins. EMBO Rep. 4, 948-952.
55. Rohn, J. L., Patel, J. V., Neumann, B., Bulkescher, J., McHedlishvili, N., McMullan, R. C., Quintero, O. A., Ellenberg, J. and Baum, B. (2014). Myo19 ensures symmetric partitioning of mitochondria and coupling of mitochondrial segregation to cell division. Curr. Biol. 24, 2598-2605.
56. Salles, F. T., Merritt, R. C., Jr, Manor, U., Dougherty, G.W., Sousa, A. D., Moore, J. E., Yengo, C. M., Dose, A. C. and Kachar, B. (2009). Myosin IIIa boosts elongation of stereocilia by transporting espin 1 to the plus ends of actin filaments. Nat. Cell Biol. 11, 443-450.
57. Schroeder, T., Yuan, H., Viglianti, B. L., Peltz, C., Asopa, S., Vujaskovic, Z. and Dewhirst, M. W. (2005). Spatial heterogeneity and oxygen dependence of glucose consumption in R3230Ac and fibrosarcomas of the Fischer 344 rat. Cancer Res. 65, 5163-5171.
58. Sheng, Z.-H. (2014). Mitochondrial trafficking and anchoring in neurons: new insight and implications. J. Cell Biol. 204, 1087-1098.
59. Shibue, T., Brooks, M. W., Inan, M. F., Reinhardt, F. and Weinberg, R. A. (2012). The outgrowth of micrometastases is enabled by the formation of filopodium-like protrusions. Cancer Discov. 2, 706-721.
60. Spillane, M., Ketschek, A., Merianda, T. T., Twiss, J. L. and Gallo, G. (2013). Mitochondria coordinate sites of axon branching through localized intra-axonal protein synthesis. Cell Rep. 5, 1564-1575.
61. Spudich, G., Chibalina, M. V., Au, J. S.-Y., Arden, S. D., Buss, F. and Kendrick-Jones, J. (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.
62. Tait, S. W. G. and Green, D. R. (2012). Mitochondria and cell signalling. J. Cell Sci. 125, 807-815.
63. Taulet, N., Delorme-Walker, V. D. and Der Mardirossian, C. (2012). Reactive oxygen species regulate protrusion efficiency by controlling actin dynamics. PLoS ONE 7, e41342.
64. Tokuo, H. and Ikebe, M. (2004). Myosin X transports Mena/VASP to the tip of filopodia. Biochem. Biophys. Res. Commun. 319, 214-220.
65. Tredan, O., Galmarini, C. M., Patel, K. and Tannock, I. F. (2007). Drug resistance and the solid tumor microenvironment. J. Natl. Cancer Institute 99, 1441-1454.
66. Tsai, C. S. (2006). Biomacromolecules Introduction to Structure, Function and Informatics. Hoboken: John Wiley & Sons.
67. Venter, G., Oerlemans, F. T. J. J., Wijers, M., Willemse, M., Fransen, J. A. M. and Wieringa, B. (2014). Glucose controls morphodynamics of LPS-stimulated macrophages. PLoS ONE 9, e96786.
68. Watanabe, J., Asaka, Y., Mino, K. and Kanamura, S. (1996). Preparation of liposomes that mimic the membrane of endoplasmic reticulum of rat hepatocytes. J. Electron Microsc. 45, 171-176.
69. Wattenberg, B. W., Clark, D. and Brock, S. (2007). An artificial mitochondrial tail signal/anchor sequence confirms a requirement for moderate hydrophobicity for targeting. Biosci. Rep. 27, 385-401.
70. Weaver, A. M. (2009). Regulation of cancer invasion by reactive oxygen species and Tks family scaffold proteins. Sci. Signal. 2, pe56.
71. Yang, J., Jang, R., Zhang, Y. and Shen, H.-B. (2013). High-accuracy prediction of transmembrane inter-helix contacts and application to GPCR 3D structure modeling. Bioinformatics 29, 2579-2587.