Lysosome-associated membrane proteins (LAMPs) regulate intracellular positioning of mitochondria in MC3T3-E1 cells

Experimental Cell Research

Volumn 331, Issue 1, 2015, Pages 211-222

  Rajapakshe, Anupama R ^a   Podyma Inoue, Katarzyna A ^a   Terasawa, Kazue ^a   Hasegawa, Katsuya ^b   Namba, Toshimitsu ^a   Kumei, Yasuhiro ^a   Yanagishita, Masaki ^a   Hara Yokoyama, Miki ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b JAPAN AEROSPACE EXPLORATION AGENCY   (Japan)

Author keywords

Intracellular positioning; Lysosome associated membrane proteins (LAMPs); Lysosomes; Mitochondria

Indexed keywords

LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; SMALL INTERFERING RNA; LAMP1 PROTEIN, MOUSE; LYSOSOME ASSOCIATED MEMBRANE PROTEIN;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CORRELATION ANALYSIS; DENDRITE; LYSOSOME; MITOCHONDRION; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; OSTEOBLAST; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; CYTOPLASM; ENZYME IMMUNOASSAY; GENETICS; GLYCOSYLATION; INTRACELLULAR MEMBRANE; METABOLISM; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYTOPLASM; GLYCOSYLATION; IMMUNOENZYME TECHNIQUES; INTRACELLULAR MEMBRANES; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MICE; MITOCHONDRIA; OSTEOBLASTS; RNA, SMALL INTERFERING;

EID: 84921051287     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.09.014     Document Type: Article

References (44)

1. Akhmanova A., Hammer J.A. Linking molecular motors to membrane cargo. Curr. Opin. Cell Biol. 2010, 22:479-487.
2. Welte M.A. Bidirectional transport along microtubules. Curr. Biol. 2004, 14:R525-R537.
3. Bryantseva S.A., Zhapparova O.N. Bidirectional transport of organelles: unity and struggle of opposing motors. Cell Biol. Int. 2012, 36:1-6.
4. Ally S., Larson A.G., Barlan K., Rice S.E., Gelfand V.I. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J. Cell Biol. 2009, 187:1071-1082.
5. Carlsson S.R., Roth J., Piller F., Fukuda M. Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Major sialoglycoproteins carrying polylactosaminoglycan. J. Biol. Chem. 1988, 263:18911-18919.
6. Chen J.W., Pan W., D'Souza M.P., August J.T. Lysosome-associated membrane proteins: characterization of LAMP-1 of macrophage P388 and mouse embryo 3T3 cultured cells. Arch. Biochem. Biophys. 1985, 239:574-586.
7. Fukuda M., Viitala J., Matteson J., Carlsson S.R. Cloning of cDNAs encoding human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Comparison of their deduced amino acid sequences. J. Biol. Chem. 1988, 263:18920-18928.
8. Chen J.W., Cha Y., Yuksel K.U., Gracy R.W., August J.T. Isolation and sequencing of a cDNA clone encoding lysosomal membrane glycoprotein mouse LAMP-1. Sequence similarity to proteins bearing onco-differentiation antigens. J. Biol. Chem. 1988, 263:8754-8758.
9. Andrejewski N., Punnonen E.L., Guhde G., Tanaka Y., Lullmann-Rauch R., Hartmann D., von Figura K., Saftig P. Normal lysosomal morphology and function in LAMP-1-deficient mice. J. Biol. Chem. 1999, 274:12692-12701.
10. Tanaka Y., Guhde G., Suter A., Eskelinen E.L., Hartmann D., Lullmann-Rauch R., Janssen P.M., Blanz J., von Figura K., Saftig P. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000, 406:902-906.
11. Eskelinen E.L., Schmidt C.K., Neu S., Willenborg M., Fuertes G., Salvador N., Tanaka Y., Lullmann-Rauch R., Hartmann D., Heeren J., von Figura K., Knecht E., Saftig P. Disturbed cholesterol traffic but normal proteolytic function in LAMP-1/LAMP-2 double-deficient fibroblasts. Mol. Biol. Cell 2004, 15:3132-3145.
12. Beertsen W., Willenborg M., Everts V., Zirogianni A., Podschun R., Schroder B., Eskelinen E.L., Saftig P. Impaired phagosomal maturation in neutrophils leads to periodontitis in lysosomal-associated membrane protein-2 knockout mice. J. Immunol. 2008, 180:475-482. (Baltimore, Md.: 1950).
13. Huynh K.K., Eskelinen E.L., Scott C.C., Malevanets A., Saftig P., Grinstein S. LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J. 2007, 26:313-324.
14. Kimura S., Noda T., Yoshimori T. Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct. Funct. 2008, 33:109-122.
15. Zhao H. Membrane trafficking in osteoblasts and osteoclasts: new avenues for understanding and treating skeletal diseases. Traffic 2012, 13:1307-1314. (Copenhagen, Denmark).
16. Ishida Y., Yamamoto A., Kitamura A., Lamande S.R., Yoshimori T., Bateman J.F., Kubota H., Nagata K. Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection. Mol. Biol. Cell 2009, 20:2744-2754.
17. Kariya Y., Honma M., Aoki S., Chiba A., Suzuki H. Vps33a mediates RANKL storage in secretory lysosomes in osteoblastic cells. J. Bone Miner. Res. 2009, 24:1741-1752.
18. Taniguchi T., Kido S., Yamauchi E., Abe M., Matsumoto T., Taniguchi H. Induction of endosomal/lysosomal pathways in differentiating osteoblasts as revealed by combined proteomic and transcriptomic analyses. FEBS Lett. 2010, 584:3969-3974.
19. Boonrungsiman S., Gentleman E., Carzaniga R., Evans N.D., McComb D.W., Porter A.E., Stevens M.M. The role of intracellular calcium phosphate in osteoblast-mediated bone apatite formation. Proc. Natl. Acad. Sci. USA 2012, 109:14170-14175.
20. An J.H., Yang J.Y., Ahn B.Y., Cho S.W., Jung J.Y., Cho H.Y., Cho Y.M., Kim S.W., Park K.S., Kim S.Y., Lee H.K., Shin C.S. Enhanced mitochondrial biogenesis contributes to Wnt induced osteoblastic differentiation of C3H10T1/2 cells. Bone 2010, 47:140-150.
21. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 1998, 93:1147-1158.
22. Cordonnier M.N., Dauzonne D., Louvard D., Coudrier E. Actin filaments and myosin I alpha cooperate with microtubules for the movement of lysosomes. Mol. Biol. Cell 2001, 12:4013-4029.
23. Heuser J. Changes in lysosome shape and distribution correlated with changes in cytoplasmic pH. J. Cell Biol. 1989, 108:855-864.
24. Carlsson S.R., Lycksell P.O., Fukuda M. Assignment of O-glycan attachment sites to the hinge-like regions of human lysosomal membrane glycoproteins lamp-1 and lamp-2. Arch. Biochem. Biophys. 1993, 304:65-73.
25. Guo D., Keightley A., Guthrie J., Veno P.A., Harris S.E., Bonewald L.F. Identification of osteocyte-selective proteins. Proteomics 2010, 10:3688-3698.
26. Kato Y., Windle J.J., Koop B.A., Mundy G.R., Bonewald L.F. Establishment of an osteocyte-like cell line, MLO-Y4. J. Bone Miner. Res. 1997, 12:2014-2023.
27. Jordens I., Fernandez-Borja M., Marsman M., Dusseljee S., Janssen L., Calafat J., Janssen H., Wubbolts R., Neefjes J. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr. Biol. 2001, 11:1680-1685.
28. Harrison R.E., Bucci C., Vieira O.V., Schroer T.A., Grinstein S. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell. Biol. 2003, 23:6494-6506.
29. Nakae I., Fujino T., Kobayashi T., Sasaki A., Kikko Y., Fukuyama M., Gengyo-Ando K., Mitani S., Kontani K., Katada T. The arf-like GTPase Arl8 mediates delivery of endocytosed macromolecules to lysosomes in Caenorhabditis elegans. Mol. Biol. Cell 2010, 21:2434-2442.
30. Sasaki A., Nakae I., Nagasawa M., Hashimoto K., Abe F., Saito K., Fukuyama M., Gengyo-Ando K., Mitani S., Katada T., Kontani K. Arl8/ARL-8 functions in apoptotic cell removal by mediating phagolysosome formation in Caenorhabditis elegans. Mol. Biol. Cell 2013, 24:1584-1592.
31. Rosa-Ferreira C., Munro S. Arl8 and SKIP act together to link lysosomes to kinesin-1. Dev. Cell 2011, 21:1171-1178.
32. da Silva A.F., Mariotti F.R., Maximo V., Campello S. Mitochondria dynamism: of shape, transport and cell migration. Cell. Mol. Life Sci. 2014, 71:2313-2324.
33. Birsa N., Norkett R., Higgs N., Lopez-Domenech G., Kittler J.T. Mitochondrial trafficking in neurons and the role of the Miro family of GTPase proteins. Biochem. Soc. Trans. 2013, 41:1525-1531.
34. Wang T., Hong W. Interorganellar regulation of lysosome positioning by the Golgi apparatus through Rab34 interaction with Rab-interacting lysosomal protein. Mol. Biol. Cell 2002, 13:4317-4332.
35. Marsh M., Schmid S., Kern H., Harms E., Male P., Mellman I., Helenius A. Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis. J. Cell Biol. 1987, 104:875-886.
36. Wilke S., Krausze J., Bussow K. Crystal structure of the conserved domain of the DC lysosomal associated membrane protein: implications for the lysosomal glycocalyx. BMC Biol. 2012, 10:62.
37. Simons K., Sampaio J.L. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 2011, 3:a004697.
38. Kaushik S., Massey A.C., Cuervo A.M. Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. EMBO J. 2006, 25:3921-3933.
39. Klopfenstein D.R., Tomishige M., Stuurman N., Vale R.D. Role of phosphatidylinositol(4,5)bisphosphate organization in membrane transport by the Unc104 kinesin motor. Cell 2002, 109:347-358.
40. Lin S.X., Collins C.A. Immunolocalization of cytoplasmic dynein to lysosomes in cultured cells. J. Cell Sci. 1992, 101(1):125-137.
41. Roczniak-Ferguson A., Petit C.S., Froehlich F., Qian S., Ky J., Angarola B., Walther T.C., Ferguson S.M. The transcription factor TFEB links mTORC1 signaling to transcriptional control of lysosome homeostasis. Sci. Signal. 2012, 5:ra42.
42. Settembre C., Zoncu R., Medina D.L., Vetrini F., Erdin S., Erdin S., Huynh T., Ferron M., Karsenty G., Vellard M.C., Facchinetti V., Sabatini D.M., Ballabio A. A lysosome-to-nucleus signalling mechanism senses and regulates the lysosome via mTOR and TFEB. EMBO J. 2012, 31:1095-1108.
43. Prinz W.A. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 2014, 205:759-769.
44. Akisaka T., Subita G.P., Shigenaga Y. Ultrastructural observations on chick bone processed by quick-freezing and freeze-substitution. Cell Tissue Res. 1987, 247:469-475.