Regulation of neurofilament interactions in vitro by natural and synthetic polypeptides sharing Lys-Ser-Pro sequences with the heavy neurofilament subunit NF-H: Neurofilament crossbridging by antiparallel sidearm overlapping

Medical and Biological Engineering and Computing

Volumn 36, Issue 3, 1998, Pages 371-387

  Gou, J P ^a   Gotow, T ^b   Janmey, P A ^c   Leterrier, J F ^a  

^a ANGERS UNIVERSITY HOSPITAL   (France)

^b OSAKA UNIVERSITY MEDICAL SCHOOL   (Japan)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Antiparallel interactions; Associated proteins; Crossbridging; Lysine serine proline motifs; Neurofilaments; Phosphorylation; Sidearms

Indexed keywords

AMINO ACIDS; POLYPEPTIDES; PROTEINS;

ASSOCIATED PROTEINS; NEUROFILAMENTS;

NEUROPHYSIOLOGY;

LYSINE; POLYPEPTIDE; PROLINE; PROTEIN SUBUNIT; SERINE; SYNTHETIC PEPTIDE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; NERVE FIBER; NERVE PROJECTION; NEUROFILAMENT; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; AXONS; CATTLE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GELS; MICROSCOPY, ELECTRON; NEUROFILAMENT PROTEINS; PHOSPHORYLATION; RATS; SPINAL CORD;

EID: 0032078841     PISSN: 01400118     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02522486     Document Type: Article

References (75)

1. ANDERTON, B. H., BREINBURG D., DOWNES, M. J., GREEN, P. J., TOMLINSON, B. E., ULRICH, J., WOOD, J. N. and KAHN, J. (1982): 'Monoclonal antibodies show that neurofibrillary tangles and neurofilaments share antigenic determinants,' Nature, 298, pp. 84-86
2. ARIMA, K., MURAYAMA, S., MUKOYAMA, M. and INOSE, T. (1992): 'Immunocytochemical and ultrastructural studies of neuronal and oligodentroglial cytoplasmic inclusions in multiple system atrophy. 1 Neuronal cytoplasmic inclusions,' Acta Neuropathol. Berl., 83, pp. 453-460
3. BROWN, A. and LASEK, R. J. (1993): 'Neurofilaments move apart freely when released from the circumferential constraint of the axonal plasma membrane,' Cell Motil. Cytoskel., 26, pp. 313-324
4. BROWN, A. and LASEK, R. J. (1995): 'Polylysine cross-links axoplasmic neurofilaments into tight bundles,' Cell Motil. Cytoskel., 31, pp. 9-21
5. CARDEN, M. J., SCHLAEPFER, W. W. and LEE, V. M.-Y. (1985): 'The structure, biochemical properties and immunogenicity of neurofilament peripheral regioins are determined by phosphorylation state,' J. Biol. Chem., 260, pp. 9805-9817
6. CHING, G. Y. and LIEM, R. K. H. (1993): 'Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments,' J. Cell. Biol., 122, pp. 1232-1335
7. CHOU, P. Y. and FASMAN, G. D. (1978): 'Prediction of the secondary structure of proteins from their amino acid sequence,' Adv. Enzymol., 47, pp. 45-148
8. CLEVELAND, D. W., FISHER, S. G., KIRSCHNER, M. W. and LAEMMLI, U. K. (1977): 'Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis,' J. Biol. Chem., 252, pp. 1102-1106
9. COLEMAN, M. P. and ANDERTON, B. H. (1990): 'Phosphate-dependent monoclonal antibodies to neurofilaments and Alzheimer neurofibrillary tangles recognize a synthetic phosphopeptide,' N. Neurochem. 54, pp. 1548-1555
10. DAUTIGNY, A., PHAM-DINH, D., ROUSSEL, C., FELIX, J. M., NUSSBAUM, J. L. and JOLLES, P. (1988): 'The large neuro- filament subunit (NF-H) of the rat: cDNA cloning and in situ detection,' Biochem. Biophys. Res. Commun., 154, pp. 1099-1106
11. EVER, J. and LETERRIER, J. F. (1988): 'Influence of the phosphorylation state of neurofilament proteins on the interactions between purified filaments in vitro,' Biochem. J., 252, pp. 655-660
12. EVER, J., MCLEAN, W. G. and LETERRIER, J. F. (1989): 'Effect of a single dose of ββ'-iminodipropionitrile in vivo on the properties of neurofilaments in vitro: comparison with the effect of iminodipropionitrile added directly to neurofilaments in vitro,' J. Neurochem., 52, pp. 1759-1765
13. EVER, J. and PETERSON, A. (1994): 'Neurofilament-deficient axons and perikaryal aggregates in viable transgenic mice expressing a neurofilament-β-Galactosidase fusion protein,' Neuron, 12, pp. 389-405
14. FIGLEWICZ, D. A., KRIZUS, A., MARTINOLI, M. G., MEININGER, V., DIB, G. A., ROULEAU, M. and JULIEN, J. P. (1994): 'Variants in the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis,' Hum. Mol. Gen. 3, pp. 1757-1761
15. FLIEGNER, K. H. and LIEM, R. K. H. (1991): 'Cellular and molecular biology of neuronal intermediate filaments,' Int. Rev. Cytol. 131, pp. 109-167
16. FUCHS, E. and WEBER, K. (1994): 'Intermediate filaments: structure, dynamics, function and disease,' Annu. Rev. Biochem., 63, pp. 345-382
17. GALLOAY, P. G., MULVIHILL, P. and PERRY, G. (1992): 'Filaments of Lewy bodies contain insoluble cytoskeletal elements,' Am. J. Pathol., 14, pp. 809-822
18. GOTOW, T., TAKEDA, M., TANAKA, T. and HASHIMOTO, P. H. (1992): 'Macromolecular structure of reassembled neurofilaments as revealed by the quick-freeze deep-etch mica method: Difference between NF-M and NF-H subunits in their ability to form cross-bridges,' Eur. J. Cell. Biol. 58, pp. 331-345
19. GOTOW, T., and TANAKA, J. (1994): 'Phosphorylation of neurofilament H subunit as related to arrangement of neurofilaments', J Neurosci. Res., 37, pp. 691-713
20. GOTOW, T., TANAKA, T., NAKAMURA, Y. and TAKEDA, M. (1994): 'Dephosphorylation of the largest neurofilament subunit protein influences the structure of crossbridges in reassembled neurofilaments,' J. Cell. Sci., 107, pp. 1949-1957
21. GOU, J. P., EYER, J. and LETERRIER, J. F. (1995): 'Progressive hyperphosphorylation of neurofilament heavy subunits with aging: Possible involvement in the mechanism of neurofilament accumulation,' Biochem. Biophys. Res. Comm., 215, pp. 368-376
22. GUIROY, D. C., SHANKAR, S. K., GIBBS Jr, C. J., MESSENHEIMER, J. A., DAS, S. and GAJDUSEK, D. C. (1989): 'Neuronal degeneration and neurofilament accumulation in the trigeminal ganglia in Creutzfeld-Jakob disease,' Ann. Neurol., 25, pp. 102-106
23. HEDREEN, J. C. and KOLIATSOS, V. E. (1994): 'Phosphorylated neurofilaments in neuronal pericarya and dendrites in human brain following axonal damage,' J. Neuropathol. Exp. Neurol., 53, pp. 663-671
24. HEINS, S., WONG, P. C., MÜLLER, S., GOLDIE, K., CLEVELAND, D. W. and AEBI, U. (1993): 'The rod domain of NF-L determines neurofilament architecture whereas the end domains specify filament assembly and network formation,' J. Cell. Biol., 123, pp. 1517-1533
25. HIROKAWA, N. (1982): 'Cross-linker system between neurofilaments, microtubules and membranous organelles in frog axons revealed by the quick-freeze, deep-etching method,' J. Cell. Biol., 94, pp. 129-142
26. HIROKAWA, N., GLICKSMAN, M. A. and WILLARD, M. B. (1984): 'Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton,' J. Cell. Biol., 98, pp. 1523-1536
27. HIROKAWA, N., HISANAGA, S and SHIOMURA, Y. (1988): 'MAP2 is a component of crossbridges between microtubules and neurofilaments in vivo and in vitro. Quick-freeze, deep etch immunoelectron microscopy and reconstitution studies,' J. Neurosci., 8, pp. 2769- 2779
28. HISANAGA, S. and HIROKAWA, N. (1988): 'Structure of the peripheral domains of neurofilaments revealed by low angle rotary shadowing,' J. Mol. Biol., 202, pp. 297-305
29. HISANAGA, S. and HIROKAWA, N. (1989): 'The effect of depho sphorylation on the structure of projections of neurofilaments,' J. Neurosci., 9, pp. 959-966
30. HISANAGA, S., MATSUOKA, Y., NISHIZAWA, K., SAITO, T., INAGAKI, M. and HIROKAWA, N. (1994): 'Phosphorylation of native and reassembled neurofilaments composed of NF-L, NF-M and NF-H by the catalytic subunit of cAMP-dependent protein kinase,' Mol. Biol. Cell., 5, pp. 161-172
31. INAGAKI, M., MATSUDOKA, Y., TSUJIMURA, K., ANDO, S., TOKUI, T., TAHAHASHI, T. and INAGAKI, N. (1996): 'Dynamic properties of intermediate filaments: regulation by phosphorylation,' Bioessays, 18, pp. 481-487
32. JANMEY, P. A., EUTENEUER, U., TRAUB, P. and SCHLIWA, M. (1991): 'Viscoelastic properties of vimentin compared with other filamentous biopolymer networks,' J. Cell. Biol., 113, pp. 1155-1160
33. JANMEY, P. A., HVIDT, S., KAS, J., LERCHE, D., MAGGS, A., SACKMANN, E., SCHLIWA, M. and STOSSEL, T. P. (1994): 'The mechanical properties of actin gels. Elastic modulus and filament motion,' J. Biol. Chem., 269, pp. 32503-32513
34. JULIEN, J.-P. and MUSHINSKY, W. E. (1983): 'The distribution of phosphorylation sites among identified proteolytic fragments of mammalian neurofilaments,' J. Biol. Chem., 258, pp. 4019-4025
35. JULIEN, J.-P., SMOLUK, G. D. and MUSHINSKY, W. E. (1983): 'Characteristics of the protein kinase activity associated with rat neurofilament preparations,' Biochim. Biophys. Acta, 755, pp. 25-31
36. KLEE, M. K., XU, Z., WONG, P. C. and CLEVELAND, D. W. (1993): 'Neurofilaments are obligate heteropolymers in vivo,' J. Cell. Biol., 122, pp. 1337-1350
37. KYTE, J. and DOOLITTLE, R. F. (1982): 'A simple method for displaying the hydropathic character of a protein,' J. Molecular Biol., 157, pp. 105-132
38. LAEMMLI, U. K. (1970): 'Cleavage of structural proteins during the assembly of the head of bacteriophage T4,' Nature, 221, pp. 680-685
39. LANGUI, D., PROBST, A., ANDERTON, B. H., BRION, J. P. and ULRICH, J. (1990): 'Aluminium-induced tangles in cultured rat neurones. Enhanced effect of aluminium by addition of maltol, Acta Neuropathol., 80, pp. 649-655
40. LETERRIER, J. F., LIEM, R. K. H. and SHELANSKI, M. L. (1982): 'Interactions between neurofilaments and microtubule-associated proteins: a possible mechanism for intraorganellar bridging,' J. Cell. Biol., 95, pp. 982-986
41. LETERRIER, J. F. and EYER, J. (1987): 'Properties of highly viscous gels formed by neurofilaments in vitro: a possible consequence of a specific inter-filament cross-bridging.' Biochem. J., 245, pp. 93-101
42. LETERRIER, J. F., EVER, J., WEISS D. G. and LINDEN, M. (1991): In vitro studies of the physical interactions between neurofilaments, microtubules and mitochondria isolated from the central nervous system,' in PAILLOTIN, G. (Ed.): 'The living cell in four dimensions.' Am. Inst. Phys. Conf. Proc., 226, Gif sur Yvette, France, pp. 91-105
43. LETERRIER, J. F., LANGUI, D., PROBST, A. and ULRICH, J. (1992): 'A molecular mechanism for the induction of neurofilament bundling by aluminium ions,' J. Neurochem., 58, pp. 2060-2070
44. LETERRIER, J. F., LANGUI, D., PROBST, A. and ULRICH, J. (1993): 'A molecular mechanism of aluminium neurotoxicity (Matters arising: reply),' J. Neurochem., 60, pp. 385-387
45. LETERRIER, J. F., HARTWIG, J., KAS, J., VEGNERS, R. and JANMEY, P. A. (1996): 'Mechanical effects of neurofilament crossbridges: modulation by phosphorylation, lipids, and interactions with F- actin,' J. Biol. Chem., 271, pp. 15687-15694
46. LIEBERBURG, I., SPINNER, N., SNYDER, S., ANDERSON, J., GOLDGABER, D., SMULWITZ, M., CARROLL, Z., EMANUEL, B. S., BREITNER, J. and RUBIN, L. (1989): 'Cloning of a cDNA encoding the rat high molecular weight neurofilament peptide (NF-H): Developmental and tissue expression in the rat, and mapping of its human homologue to chromosomes 1 and 22,' Proc. Natl. Acad. Sci. USA, 86, pp. 2463-2467
47. LOWRY, O. H., ROSEBROUGH, N. J., FARR, A. L. and RANDALL, R. J. (1951): 'Protein measurement using the Folin phenol reagent,' J. Biol. Chem., 193, pp. 265-275
48. MACLEAN-FLETCHER, S. D. and POLLARD, T. D. 1980): 'Viscosimetric analysis of the gelation of Acanthamoeba extracts and purification of two gelation factors,' J. Cell. Biol., 85, pp. 414-428
49. MATA, M., KUPINA, M. and FINK, D. J. (1992): 'Phosphorylation- dependent neurofilament epitopes are reduced at the node of Ranvier,' J. Neurocytol., 21, pp. 199-210
50. NAGAKAWA, T., CHEN, J., ZHANG, Z., KANAI, Y. and HIROKAWA, N. (1995): 'Two distinct functions of the carboxy-terminal tail domain of NF-M upon neurofilament assembly: cross-bridge formation and longitudinal elongation of filaments,' J. Cell. Biol. 129, pp. 411- 429
51. NAPOLITANO, E. W., CHIN, S. S., COLMAN, D. R. and LIEM, R. K. H. (1987): 'Complete amino acid sequence and in vitro expression of rat NF-M, the middle molecular weight neurofilament protein,' J. Neurosci., 7, pp. 2590-2599
52. NIXON, R. A. (1992): 'Slow axonal transport,' Curr. Opin. Cell Biol., 4, pp. 8-14
53. NIXON, R. A. (1993): 'The regulation of neurofilament protein dynamics by phosphorylation: Clues to neurofibrillary pathobiology,' Brain Pathol., 3, pp. 29-38
54. NIXON, R. A., PASKEVICH, P. A., SIHAG, R. K. and THAYER, C. Y. (1994): 'Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: Influence on regional neurofilament accumulation, interneurofilament spacing, and axon caliber,' J. Cell Biol., 126, pp. 1031-1046
55. OKABE, S., MIYASAKA, H. and HIROKAWA, N. (1993): 'Dynamics of the neuronal intermediate filament,' J. Cell. Biol., 121, pp. 375-386
56. PAPASOZOMENOS, S. C., BINDER, L. I., BENDER, P. K. and PAYNZE, M. R. (1985): 'Microtubule-associated protein 2 within axon of spinal motor neurons: association with microtubules and neurofilament in normal and β, β'-iminodipropionotile treated axons,' J. Cell Biol., 100, pp. 74-85
57. PROBST, A., LANGUI, D., LAUTENSCHLAGER, C., ULRICH, J., BRION, J. P. and ANDERTON, B. H. (1988): 'Progressive supranuclear palsy: extensive neuropil threads in addition to neurofibrillary tangles. Very similar antigenicity of subcortical neuronal pathology in progressive nuclear palsy and Alzheimer's disease,' Acta Neuropathol. Berl., 77, pp. 61-68
58. SCHAGGER, H. and VON JAGOW, G. 1987): 'Tricine-sodium dodecyl sulfate-polyacrylamide gel eletrophoresis for the separation of proteins in the range from 1 to 100 kDa,' Anal. Biochem., 166, pp. 368-379
59. SHAW, G. and HOU, Z. (1990): 'Bundling and cross-linking of intermediate filaments of the nervous system,' J. Neurosci. Res., 25, pp. 561-568
60. SHAW, G. (1991): 'Neurofilaments proteins,' in BURGOYNE, R. D. (Ed.): 'The neuronal cytoskeleton' (Wiley-Liss, New York) pp. 186-213
61. SHEA, T. B. and BEERMANN, M. L. (1994a): 'Respective roles of neurofilaments, microtubules, MAP1B, and tau in neurite out- growth and stabilization,' Mol. Biol. Cell, 5, pp. 863-875
62. SHEA, T. B. and BEERMANN, M. L. (1994b): 'Multiple interactions of aluminium with neurofilament subunits: regulation by phosphate- dependent interactions between C-terminal extensions of the high and middle molecular weight subunits,' J. Neurosci. Res., 38, pp. 160-166
63. SHETTY, K. T., LINK, W. T. and PANT, H. C. (1993): 'Cdc2-like kinase from rat spinal cord specificity phosphorylates KSPXK motifs in neurofilament proteins. Isolation and characterization,' Proc. Natl. Acad. Sci. USA, 90, pp. 6844-6848
64. SHETTY, V. K., LINK, W. T., JAFFE, H., WANG, J. and PANT, H. C. (1995): 'Neuronal cyclin-dependent kinase-5 phosphorylation sites in neurofilament protein (NF-H) are dephosphorylated by protein phosphatase 2a, J. Neurochem., 64, pp. 2681-2690
65. SMITH, M. A., RUDNICKA-NAWROT, RICHEY, P. L., PRAPROTNIK, D., MULVIHILL, P., MILLER, C. A., SAYRE, L. M. and PERRY, G. (1995): 'Carbonyl-related posttranslational modification of neurofilament protein in the neurofibrillary pathology of Alzheimer's disease,' J. Neurochem., 64, pp. 2660-2666
66. SOBUE, S., HASHIZUME, Y. YASUDA, T., MUKAI, E., KUMAGAI, T., MITSUMA, T. and TROJANOWSKI, J. Q. (1990): 'Phosphorylated high molecular weight neurofilament protein in lower motor neurons in amyotrophic lateral sclerosis and other neurodegenerative diseases involving ventral horn cells,' Acta Neuropathol., 79, pp. 402-408
67. TAKAHASHI, M., AMIN, N., GRANT, P. and PANT, H. C. (1995): 'P13suc1 associates with a cdc2-like kinase in a multimeric cytoskeletal complex in squid axoplasm,' J. Neurosci., 15, pp. 6222-6229
68. TORU-DELBAUFFE, D. and PIERRE, M. (1983): 'A rat brain protein kinase phosphorylating specifically neurofilaments,' FEBS Lett., 162, pp. 230-234
69. TORU-DELFAUFFE, D., PIERRE, M., OSTY, J., CHANTOUX, F. and FRANCON, J. (1986): 'Properties of neurofilament protein kinase,' Biochem. J., 235, pp. 283-289
70. TOWBIN, H., STAEHELIN, T. and GORDON, J. (1979): 'Electrophoresis transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications,' Proc. Natl. Acad. Sci. USA, 76, pp. 4350-4354
71. TYLER, J. M. and BRANTON, D. (1980): 'Rotary shadowing of extended molecules dried from glycerol,' J. Ultrastruct. Res., 71, pp. 95-102
72. VICKERS, J. C., DELACOURTE, A. and MORRISON, J. H. (1992): 'Progressive transformation of the cytoskeleton associated with normal aging and Alzheimer's disease,' Brain Res., 594, pp. 273- 278
73. VICKERS, J. C., RIEDERER, B. M., MARUGG, R. A., BUEE-SCHERRER, V., BUEE, L., DELACOURTE, A. and MORRISON, J. H. (1994): 'Alterations in neurofilament protein immunoreactivity in human hippocampal neurons related to normal aging and Alzheimer's disease,' Neurosci., 62, pp. 1-43
74. WILLARD, M. and SIMON, C. (1981): 'Antibody decoration of neurofilaments,' J. Cell Biol., 89, pp. 198-205
75. WOOD, J. N. and ANDERTON, B. H. (1981): 'Monoclonal antibodies to mammalian neurofilaments,' Biosci. Rep., 1, pp. 263- 268