Tumor necrosis factor induces hyperphosphorylation of kinesin light chain and inhibits kinesin-mediated transport of mitochondria

Journal of Cell Biology

Volumn 149, Issue 6, 2000, Pages 1207-1214

  De Vos, Kurt ^a,d   Severin, Fedor ^b,c   Van Herreweghe, Franky ^a   Vancompernolle, Katia ^a   Goossens, Vera ^a   Hyman, Anthony ^b,c   Grooten, Johan ^a  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^d Columbia University ^*  (United States)

Author keywords

Microtubule; Mitogen activated protein kinase; Okadaic acid; Organelle; Phosphorylation

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CYTOKINE RECEPTOR; IMMUNOGLOBULIN LIGHT CHAIN; KINESIN; MITOGEN ACTIVATED PROTEIN KINASE; MOLECULAR MOTOR; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELL ORGANELLE; CELL STRAIN L 929; CONTROLLED STUDY; ENZYME ACTIVATION; INTRACELLULAR TRANSPORT; MICROTUBULE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CELL LINE; ENZYME ACTIVATION; ENZYME INHIBITORS; IMIDAZOLES; KINESIN; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR MOTOR PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PYRIDINES; RECEPTORS, TUMOR NECROSIS FACTOR; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 0034641135     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.6.1207     Document Type: Article

References (40)

1. Beyaert, R., A. Cuenda, W. Vanden Berghe, S. Plaisance, J.C. Lee, G. Haegeman, P. Cohen, and W. Fiers. 1996. The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO (Eur. Mol. Biol. Organ.) J. 15:1914-1923.
2. Boone, E., V. Vandevoorde, G. De Wilde, and G. Haegeman. 1998. Activation of p42/p44 mitogen-activated protein kinases (MAPK) and p38 MAPK by tumor necrosis factor (TNF) is mediated through the death domain of the 55-kDa TNF receptor. FEBS Lett. 441:275-280.
3. Brady, S.T. 1985. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature. 317:73-75.
4. Brady, S.T., and K.K. Pfister. 1991. Kinesin interactions with membrane hounded organelles in vivo and in vitro. J. Cell Sci. Suppl. 14:103-108.
5. Bulinski, J.C., T.E. McGraw, D. Gruber, H.L. Nguyen, and M.P. Sheetz. 1997. Overexpression of MAP4 inhibits organelle motility and trafficking in vivo. J. Cell Sci. 110:3055-3064.
6. Coy, D.L., W.O. Hancock, M. Wagenbach, and J. Howard. 1999. Kinesin's tail domain is an inhibitory regulator of the motor domain. Nat. Cell Biol. 1:288-292.
7. Cuenda, A., J. Rouse, Y.N. Doza, R. Meier, P. Cohen, T.F. Gallagher, P.R. Young, and J.C. Lee. 1995. SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett. 364:229-233.
8. de Cuevas, M., T. Tao, and L.S.B. Goldstein. 1992. Evidence that the stalk of Drosophila kinesin heavy chain is an α-helical coiled coil. J. Cell Biol. 116: 957-965.
9. De Vos, K., V. Goossens, E. Boone, D. Vercammen, K. Vancompernolle, P. Vandenabeele, G. Haegeman, W. Fiers, and J. Grooten. 1998. The 55-kDa tumor necrosis factor receptor induces clustering of mitochondria through its membrane-proximal region. J. Biol. Chem. 273:9673-9680.
10. Diefenbach, R.J., J.P. Mackay, P.J. Armati, and A.L. Cunningham. 1998. The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. Biochemistry. 37: 16663-16670.
11. Ebneth, A., R. Godemann, K. Stamer, S. Illenberger, B. Trinczek, and E. Mandelkow. 1998. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 143:777-794.
12. Friedman, D.S., and R.D. Vale. 1999. Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat. Cell Biol. 1:293-297.
13. Hackney, D.D., J.D. Levitt, and D.D. Wagner. 1991. Characterization of alpha 2 beta 2 and alpha 2 forms of kinesin. Biochem. Biophys. Res. Commun. 174: 810-815.
14. Hamm-Alvarez, S.F., P.Y. Kim, and M.P. Sheetz. 1993. Regulation of vesicle transport in CV-1 cells and extracts. J. Cell Sci. 106:955-966.
15. Heins, S., Y.H. Song, H. Wille, E. Mandelkow, and E.M. Mandelkow. 1991. Effect of MAP2, MAP2c, and tau on kinesin-dependent microtubule motility. J. Cell Sci. Suppl. 14:121-124.
16. Hollenbeck, P.J. 1993. Phosphorylation of neuronal kinesin heavy and light chains in vivo. J. Neurochem. 60:2265-2275.
17. Hyman, A.A. 1991. Preparation of marked microtubules for the assay of the polarity of microtubule-based motors by fluorescence. J. Cell Sci. Suppl. 14: 125-127.
18. Ingold, A.L., S.A. Cohn, and J.M. Scholey. 1988. Inhibition of kinesin-driven microtubule motility by monoclonal antibodies to kinesin heavy chains. J. Cell Biol. 107:2657-2667.
19. Khodjakov, A., E.M. Lizunova, A.A. Minin, M.P. Koonce, and F.K. Gyoeva. 1998. A specific light chain of kinesin associates with mitochondria in cultured cells. Mol. Biol. Cell. 9:333-343.
20. Lee, K.D., and P.J. Hollenbeck. 1995. Phosphorylation of kinesin in vivo correlates with organelle association and neurite outgrowth. J. Biol. Chem. 270: 5600-5605.
21. Lindesmith, L., J.M. McIlvain, Jr., Y. Argon, and M.P. Sheetz. 1997. Phosphotransferases associated with the regulation of kinesin motor activity. J. Biol. Chem. 272:22929-22933.
22. Lopez, L.A., and M.P. Sheetz. 1993. Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell. Motil. Cytoskel. 24:1-16.
23. Lopez, L.A., and M.P. Sheetz. 1995. A microtubule-associated protein (MAP2) kinase restores microtubule motility in embryonic brain. J. Biol. Chem. 270: 12511-12517.
24. Matthies, H.J., R.J. Miller, and H.C. Palfrey. 1993. Calmodulin binding to and cAMP-dependent phosphorylation of kinesin light chains modulate kinesin ATPase activity. J. Biol. Chem. 268:11176-11187.
25. McIlvain, J.M., Jr., J.K. Burkhardt, S. Hamm-Alvarez, Y. Argon, and M.P. Sheetz. 1994. Regulation of kinesin activity by phosphorylation of kinesin-associated proteins. J. Biol. Chem. 269:19176-19182.
26. Nagata, K., A. Puls, C. Futter, P. Aspenstrom, E. Schaefer, T. Nakata, N. Hirokawa, and A. Hall. 1998. The MAP kinase kinase kinase MLK2 co-localizes with activated JNK along microtubules and associates with kinesin superfamily motor KIF3. EMBO (Eur. Mol. Biol. Organ.) J. 17:149-158.
27. Nangaku, M., R. Sato-Yoshitake, Y. Okada, Y. Noda, R. Takemura, H. Yamazaki, and N. Hirokawa. 1994. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell. 79: 1209-1220.
28. Pereira, A.J., B. Dalby, R.J. Stewart, S.J. Doxsey, and L.S. Goldstein. 1997. Mitochondrial association of a plus end-directed microtubule motor expressed during mitosis in Drosophila. J. Cell Biol. 136:1081-1090.
29. Rahman, A., D.S. Friedman, and L.S. Goldstein. 1998. Two kinesin light chain genes in mice. Identification and characterization of the encoded proteins [published erratum appears in J. Biol. Chem. 1998. 273:24280]. J. Biol. Chem. 273:15395-15403.
30. Rahman, A., A. Kamal, E.A. Roberts, and L.S. Goldstein. 1999. Defective kinesin heavy chain behavior in mouse kinesin light chain mutants. J. Cell Biol. 146:1277-1288.
31. Reilein, A.R., I.S. Tint, N.I. Peunova, G.N. Enikolopov, and V.I. Gelfand. 1998. Regulation of organalle movement in melanophores by protein kinase A (PKA), protein kinase C (PKC), and protein phosphatase 2A (PP2A). J. Cell Biol. 142:803-813.
32. Sato-Yoshitake, R., H. Yorifuji, M. Inagaki, and N. Hirokawa. 1992. The phosphorylation of kinesin regulates its binding to synaptic vesicles. J. Biol. Chem. 267:23930-23936.
33. Stenoien, D.L., and S.T. Brady. 1997. Immunochemical analysis of kinesin light chain function. Mol. Biol. Cell. 8:675-689.
34. Stock, M.F., J. Guerrero, B. Cobb, C.T. Eggers, T.G. Huang, X. Li, and D.D. Hackney. 1999. Formation of the compact confomer of kinesin requires a COOH-terminal heavy chain domain and inhibits microtubule-stimulated ATPase activity. J. Biol. Chem. 274:14617-14623.
35. Tanaka, Y., Y. Kanai, Y. Okada, S. Nonaka, S. Takeda, A. Harada, and N. Hirokawa. 1998. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell. 93:1147-1158.
36. Vale, R.D., T.S. Reese, and M.P. Sheetz. 1985. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 42: 39-50.
37. Van Lint, J., P. Agostinis, V. Vandevoorde, G. Haegeman, W. Fiers, W. Merlevede, and J.R. Vandenheede. 1992. Tumor necrosis factor stimulates multiple serine/threonine protein kinases in Swiss 3T3 and L929 cells. Implication of casein kinase-2 and extracellular signal-regulated kinases in the tumor necrosis factor signal transduction pathway. J. Biol. Chem. 267:25916-25921.
38. Verhey, K.J., D.L. Lizotte, T. Abramson, L. Barenboim, B.J. Schnapp, and T.A. Rapoport. 1998. Light chain-dependent regulation of kinesin's interaction with microtubules. J. Cell Biol. 143:1053-1066.
39. Yang, J.T., R.A. Laymon, and L.S.B. Goldstein. 1989. A three-domain structure of kinesin heavy chain revealed by DNA sequence and microtubule binding analyses. Cell. 56:879-889.
40. Zhang, Y.H., J.X. Lin, Y.K. Yip, and J. Vilcek. 1988. Enhancement of cAMP levels and of protein kinase activity by tumor necrosis factor and interleukin 1 in human fibroblasts: role in the induction of interleukin 6. Proc. Natl. Acad. Sci. USA. 85:6802-6805.