[Frontiers in Bioscience 1, d91-116, July 1, 1996]
Reprints
PubMed
CAVEAT LECTOR



THE PATTERN AND MECHANISM OF MITOCHONDRIAL TRANSPORT IN AXONS

Peter J. Hollenbeck

Dept. of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA.

Received 05/30/96; Accepted 06/10/96; On-line 07/01/96

5. REFERENCES

1. S. T. Brady & R. J. Lasek: Axonal transport: a cellbiological method for studying proteins that associate with the cytoskeleton. Methods Cell Biol 25, 365-398 (1982)

2. B. Edmonds & E. Koenig: Powering of bulk transport (varicosities) and differential sensitivities of directional transport growing axons. Brain Res 406, 288-293 (1987)

3. P. J. Hollenbeck: Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J Cell Biol 121, 305-315 (1993)

4. R. L. Morris & P. J. Hollenbeck: Axonal transport of mitochondria along microtubules and Factin in living vertebrate neurons. J Cell Biol 131, 1315-1326 (1995)

5. S. T. Brady, R. J. Lasek, & R. D. Allen: Video microscopy of fast axonal transport in extruded axoplasm: a new model for study of molecular mechanisms. Cell Motil 5, 81-101 (1985)

6. S. T. Brady, B. W. Richards, & P. L. Leopold: Assay of vesicle motility in squid axoplasm. Methods Cell Biol 39, 191-202 (1993)

7. S. A. Cohn, W. M. Saxton, R. J. Lye, & J. M. Scholey: Analyzing microtubule motors in real time. Methods Cell Biol 39, 75-88 (1993)

8. S. T. Brady: Molecular motors in the nervous system. Neuron 7, 521-533 (1991)

9. D. A. Skoufias & J. M. Scholey: Cytoplasmic microtubulebased motor proteins. Curr Opin Cell Biol 5, 95-104 (1993)

10. M. Mooseker: Myosin superfamily: A multitude of myosins. Curr Biol 3, 245-248 (1993)

11. I. Toyoshima, H. Yu, E. R. Steuer, & M. P. Sheetz: Kinectin, a major kinesinbinding protein on ER. J Cell Biol 118, 1121-1131 (1992)

12. D. F. Bielinski, P. J. Morin, B. F. Dickey, & R. E. Fine: Low molecular weight GTPbinding proteins are associated with Neuronal organelles involved in rapid axonal transport and exocytosis. J Biol Chem 264, 18363-18367 (1989)

13. G. S. Bloom, B. W. Richards, P. L. Leopold, D. M. Ritchey, & S. T. Brady: GTPgS inhibits organelle transport along axonal microtubules. J Cell Biol 120, 467-476 (1993)

14. R. SatoYoshitake, H. Yorifuji, M. Inagaki, & N. Hirokawa: The phosphorylation of kinesin regulates its binding to synaptic vesicles. J Biol Chem 267, 23930-23936 (1992)

15. H. J. G. Matthies, R. J. Miller, & H. C. Palfrey: Calmodulin binding to and cAMPdependent phosphorylation of kinesin light chains modulate kinesin ATPase activity. J Biol Chem 268, 11176-11187 (1993)

16. P. J. Hollenbeck: Phosphorylation of neuronal kinesin heavy and light chains in vivo. J Neurochem 60, 2265-2275 (1993)

17. J. M. McIlvain,Jr., J. K. Burkhardt, S. HammAlvarez, Y. Argon, & M. P. Sheetz: Regulation of kinesin activity by phosphorylation of kinesinassociated proteins. J Biol Chem 269, 19176-19182 (1994)

18. K.D. Lee & P. J. Hollenbeck: Phosphorylation of kinesin in vivo correlates with organelle association and neurite outgrowth. J Biol Chem 270, 5600-5605 (1995)

19. S. X. Lin, K. L. Ferro, & C. A. Collins: Cytoplasmic dynein undergoes intracellular redistribution concomitant with phosphorylation of the heavy chain in response to serum starvation and okadaic acid. J Cell Biol 127, 1009-1019 (1994)

20. J. F. Dillman & K. K. Pfister: Differential phosphorylation in vivo of cytoplasmic dynein associated with anterogradely moving organelles. J Cell Biol 127, 1671-1681 (1994)

21. K. K. Pfister, M. W. Salata, J. F. Dillman, K. T. Vaughan, R. B. Vallee, E. Torre, & R. J. Lye: Differential expression and phosphorylation of the 74kDa intermediate chains of cytoplasmic dynein in cultured neurons and glia. J Biol Chem 271, 1687-1694 (1996)

22. C. C. Overly, H. I. Rieff, & P. J. Hollenbeck: Axonal and dendritic organelle transport in hippocampal neurons: differences in organization and behavior. J Cell Sci 109, 971-980 (1996)

23. J. M. Schroder: Neuropathy associated with mitochondrial disorders. Brain Pathology 3, 177-190 (1993)

24. P. C. Wong, C. A. Pardo, D. R. Borchelt, M. K. Lee, N. G. Copeland, N. A. Jenkins, S. S. Sisodia, D. W. Cleveland, & D. L. Price: An adverse property of a familial ALSlinked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14, 1105-1116 (1995)

25. E. Brouillet, B. J. Jenkins, B. T. Hyman, R. J. Ferrante, N. W. Kowall, R. Srivastava, D. S. Roy, B. R. Rosen, & M. F. Beal: Agedependent vulnerability of the striatum to the mitochondrial toxin 3nitropropionic acid. J Neurochem 60, 356-359 (1993)

26. J.F. Collard, F. Cote, & J.P. Julien: Defective axonal transport in a transgenic mouse model of amyotrophic lateral sclerosis. Nature 375, 61-64 (1995)

27. J. BereiterHahn: Behavior of mitochondria in the living cell. Intl Rev Cytol 122, 163 (1990)

28. J. BereiterHahn & M. Voth: Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microscopy Research & Technique 27, 198-219 (1994)

29. R. D. Allen, J. Metuzals, I. Tasaki, S. T. Brady, & S. P. Gilbert: Fast axonal transport in squid giant axon. Science 218, 1127-1129 (1982)

30. S. T. Brady, R. J. Lasek, & R. D. Allen: Fast axonal transport in extruded axoplasm from squid giant axon. Science 218, 1129-1131 (1982)

31. D. S. Forman, K. J. Lynch, & R. S. Smith: Organelle dynamics in lobster axons: anterograde, retrograde and stationary mitochondria. Brain Res 412, 96-106 (1987)

32. R. L. Morris & P. J. Hollenbeck: The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J Cell Sci 104, 917-927 (1993)

33. M. R. Gilbert, B. L. Harding, P. N. Hoffman, J. W. Griffin, D. L. Price, & J. C. Troncoso: Aluminuminduced neurofilamentous changes in cultured rat dorsal root ganglia explants. J Neurosci 12, 1763-1771 (1992)

34. S. A. Endow & M. A. Titus: Genetic approaches to molecular motors. Annu Rev Cell Biol 8, 29-66 (1992)

35. L. S. B. Goldstein: With apologies to Scheherazade: Tails of 1001 kinesin motors. Annu Rev Genet 27, 319-351 (1993)

36. R. D. Vale, J. M. Scholey, & M. P. Sheetz: Kinesin: possible biological roles for a new microtubule motor. Trends Biochem Sci 11, 464-468 (1986)

37. T. A. Schroer & M. P. Sheetz: Functions of microtubulebased motors. Annu Rev Physiol 53, 629-652 (1991)

38. R. B. Vallee, H. S. Shpetner, & B. M. Paschal: The role of dynein in retrograde axonal transport. Trends Neurosci 12, 66-70 (1989)

39. T. A. Schroer, E. R. Steuer, & M. P. Sheetz: Cytoplasmic dynein is a minus enddirected motor for membranous organelles. Cell 56, 937-946 (1989)

40. B. J. Schnapp & T. S. Reese: Dynein is the motor for retrograde axonal transport of organelles. Proc Natl Acad Sci USA 86, 1548-1552 (1989)

41. T. A. Schroer: Structure, function and regulation of cytoplasmic dynein. Curr Opin Cell Biol 6, 69-73 (1994)

42. T. Lorenz & M. Willard: Subcellular fractionation of intraaxonally transport polypeptides in the rabbit visual system. Proc Natl Acad Sci USA 75, 505-509 (1978)

43. W. D. Blaker, J. F. Goodrum, & P. Morell: Axonal transport of the mitochondriaspecific lipid, diphosphatidylglycerol, in the rat visual system. J Cell Biol 89, 579-584 (1981)

44. R. G. Elluru, G. S. Bloom, & S. T. Brady: Fast axonal transport of kinesin in the rat visual system: functionality of kinesin heavy chain isoforms. Molec Biol Cell 6, 21-40 (1995)

45. M. Nangaku, R. SatoYoshitake, Y. Okada, Y. Noda, R. Takemura, H. Yamazaki, & N. Hirokawa: KIF1B, a novel microtubule plus enddirected monomeric motor protein for transport of mitochondria. Cell 79, 1209-1220 (1994)

46. P. Satir, K. Barkalow, & T. Hamasaki: The control of ciliary beat frequency. Trends Cell Biol 3, 409-412 (1993)

47. C. E. Walczak & D. L. Nelson: Regulation of dyneindriven motility in cilia and flagella. Cell Motil Cytoskel 27, 101-107 (1994)

48. J. T. Stull, B. F. Bowman, P. J. Gallagher, B. P. Herring, L.C. Hsu, K. E. Kamm, Y. Kubota, S. A. Leachman, H. L. Sweeney, & M. G. Tansey: Myosin phosphorylation in smooth and skeletal muscles: Regulation and function. Prog Clin Biol Res 327, 107-126 (1990)

49. J. L. Tan, S. Ravid, & J. A. Spudich: Control of nonmuscle myosins by phosphorylation. Annu Rev Biochem 61, 721-759 (1992)

50. T. J. Chilcote & K. A. Johnson: Phosphorylation of Tetrahymena 22 S dynein. J Biol Chem 265, 17257-17266 (1990)

51. T. Hamasaki, K. Barkalow, J. Richmond, & P. Satir: cAMPstimulated phosphorylation of an axonemal polypeptide that copurifies with the 22S dynein arm regulates microtubule translocation velocity and swimming speed in Paramecium. Proc Natl Acad Sci USA 88, 7918-7922 (1991)

52. Y. Okada, R. SatoYoshitake, & N. Hirokawa: The activation of protein kinase A pathway selectively inhibits anterograde axonal transport of vesicles but not mitochondria transport or retrograde transport in vivo. J Neurosci 15, 3053-3064 (1995)

53. D. Martz, R. J. Lasek, S. T. Brady, & R. D. Allen: Mitochondrial motility in axons: membranous organelles may interact with the force generating system through multiple surface binding sites. Cell Motil 4, 89-101 (1984)

54. P. L. Leopold, A. W. McDowall, K. K. Pfister, G. S. Bloom, & S. T. Brady: Association of kinesin with characterized membranebounded organelles. Cell Motil Cytoskel 23, 19-33 (1992)

55. A. Jellali, M.H. MetzBoutigue, I. G. Surgucheva, V. Jancsik, C. Schwartz, D. Filliol, V. I. Gelfand, & A. Rendon: Structural and biochemical properties of kinesin heavy chain associated with rat brain mitochondria. Cell Motil Cytoskel 28, 79-93 (1994)

56. B. Grafstein & D. S. Forman: Intracellular transport in neurons. Physiol Rev 60, 11671283 (1980)

57. B. J. Schnapp & T. S. Reese: Cytoplasmic structure in rapidfrozen axons. J Cell Biol 94, 667-679 (1982)

58. N. Hirokawa: Crosslinker system between neurofilaments, microtubules, and membranous organelles in frog axons revealed by the quickfreeze, deepetching method. J Cell Biol 94, 129-142 (1982)

59. G. Benshalom & T. S. Reese: Ultrastructural observations on the cytoarchitecture of axons processed by rapidfreezing and freeze substitution. J Neurocytol 14, 943-960 (1985)

60. N. Hirokawa & H. Yorifuji: Cytoskeletal architecture of reactivated crayfish axons, with special reference to crossbridges among microtubules and between microtubules and membrane organelles. Cell Motil Cytoskel 6, 458-468 (1986)

61. B. J. Schnapp, R. D. Vale, M. P. Sheetz, & T. S. Reese: Single microtubules from squid axoplasm support bidirectional movement of organelles. Cell 40, 455-462 (1985)

62. R. D. Allen, D. G. Weiss, J. H. Hayden, D. T. Brown, H. Fujiwake, & M. Simpson: Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: evidence for an active role of microtubules in cytoplasmic transport. J Cell Biol 100, 1736-1752 (1985)

63. R. D. Vale, T. S. Reese, & M. P. Sheetz: Identification of a novel forcegenerating protein, kinesin, involved in microtubulebased motility. Cell 42, 39-50 (1985)

64. S. T. Brady: A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317, 73-75 (1985)

65. J. M. Scholey, M. E. Porter, P. M. Grissom, & J. R. McIntosh: Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle. Nature 318, 483-486 (1985)

66. R. B. Vallee, J. S. Wall, B. M. Paschal, & H. S. Shpetner: Microtubuleassociated protein 1C from brain is a twoheaded cytosolic dynein. Nature 332, 561-563 (1988)

67. H. S. Shpetner, B. M. Paschal, & R. B. Vallee: Characterization of the microtubuleactivated ATPase of brain cytoplasmic dynein (MAP 1C). J Cell Biol 107, 1001-1009 (1988)

68. M. P. Sheetz & J. A. Spudich: Movement of myosincoated fluorescent beads on actin cables in vitro. Nature 303, 31-35 (1983)

69. T. J. Bradley & P. Satir: Evidence of microfilamentassociated mitochondrial movement. J Supramol Struct 12, 165-175 (1979)

70. M. G. Smith, V. R. Simon, H. O'Sullivan, & L. A. Pon: OrganelleCytoskeletal interactions: actin mutations inhibit meiosisdependent mitochondrial rearrangement in the budding yeast Saccaromyces cerevisiae. Mol Biol Cell 6, 1381-1396 (1995)

71. R. E. Fine & D. Bray: Actin in growing nerve cells. Nature New Biology 234, 115-118 (1971)

72. K. Burridge & D. Bray: Purification and structural analysis of myosins from brain and other nonmuscle tissues. J Mol Biol 99, 1-14 (1975)

73. D. Li & P. D. Chantler: Evidence for a new member of the myosin I family from mammalian brain. J Neurochem 59, 1344-1351 (1992)

74. W. Sun & P. D. Chantler: A unique cellular myosin II exhibiting differential expression in the cerebral cortex. Biochem Biophys Res Commun 175, 244-249 (1991)

75. W. Sun & P. D. Chantler: Cloning of the cDNA encoding a neuronal myosin heavy chain from mammalian brain and its differential expression within the central nervous system. J Mol Biol 224, 1185-1193 (1992)

76. S. Mochida, H. Kobayashi, Y. Matsuda, Y. Yuda, K. Muramoto, & Y. Nonomura: Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron 13, 1131-1142 (1994)

77. D. Li, M. Miller, & P. D. Chantler: Association of a cellular myosin II with anionic phospholipids and the neuronal plasma membrane. Proc Natl Acad Sci USA 91, 853-857 (1994)

78. E. M. Espreafico, R. E. Cheney, M. Matteoli, & A. A. C. Nascimento: Primary structure and cellular localization of chicken brain myosinv (p190), an unconventional myosin with calmodulin light chains. J Cell Biol 119, 1541-1557 (1992)

79. R. E. Cheney, M. K. O'Shea, J. E. Heuser, M. V. Coelho, J. S. Wolenski, E. M. Espreafico, P. Forscher, R. E. Larson, & M. S. Mooseker: Brain myosinV is a twoheaded unconventional myosin with motor activity. Cell 75, 13-23 (1993)

80. T. Hasson & M. S. Mooseker: Porcine myosinVI characterization of a new mammalian uncon-ventional myosin. J Cell Biol 127, 425-440 (1994)

81. S. T. Brady, S. D. Crothers, C. Nosal, & W. O. McClure: Fast axonal transport in the presence of high Ca2+: evidence that microtubules are not required. Proc Natl Acad Sci USA 77, 5909-5913 (1980)

82. D. J. Goldberg, D. A. Harris, B. W. Lubit, & J. H. Schwartz: Analysis of the mechanism of fast axonal transport by intracellular injection of potentially inhibitory macromolecules: evidence for a possible role of actin filaments. Proc Natl Acad Sci USA 77, 7448-7452 (1980)

83. D. J. Goldberg: Microinjection into an identified axon to study the mechanism of fast axonal transport. Proc Natl Acad Sci USA 79, 4818-4822 (1982)

84. S. T. Brady, R. J. Lasek, R. D. Allen, H. L. Yin, & T. P. Stossel: Gelsolin inhibition of fast axonal transport indicates a requirement for actin micro-filaments. Nature 310, 56-58 (1984)

85. S. A. Kuznetsov, G. M. Langford, & D. G. Weiss: Actindependent organelle movement in squid axoplasm. Nature 356, 722-725 (1992)

86. E. L. Bearer, J. A. DeGiorgis, R. A. Bodner, A. W. Kao, & T. S. Reese: Evidence for myosin motors on organelles in squid axoplasm. Proc Natl Acad Sci USA 90, 11252-11256 (1993)

87. G. M. Langford, S. A. Kuznetsov, D. Johnson, D. L. Cohen, & D. G. Weiss: Movement of axoplasmic organelles on actin filaments assembled on acrosomal processes evidence for a barbedenddirected organelle motor. J Cell Sci 107, 2291-2298 (1994)

88. S. A. Kuznetsov, D. T. Rivera, F. F. Severin, D. G. Weiss, & G. M. Langford: Movement of axoplasmic organelles on actin filaments from skeletal muscle. Cell Motil Cytoskel 28, 231-242 (1994)

89. L. L. Evans & P. C. Bridgman: Particles move along actin filament bundles in nerve growth cones. Proc Natl Acad Sci USA 92, 10954-10958 (1995)

90. L. Hou, F. Lanni, & K. LubyPhelps: Tracer diffusion in Factin and Ficoll mixtures. Toward a model for cytoplasm. Biophys J 58, 31-43 (1990)

91. D. W. Provance, A. McDowall, M. Marko, & K. LubyPhelps: Cytoarchitecture of sizeexcluding compartments in living cells. J Cell Sci 106, 565-578 (1993)

92. D. Bray & M. B. Bunge: Serial analysis of microtubules in cultured rat sensory axons. J Neurocytol 10, 589-605 (1981)

93. D. W. Fawcett: The Cell. Philadelphia: W. B. Saunders Co. 1981. 1-862

94. B. S. Zielinski, M. L. Getchell, & T. V. Getchell: Ultrastructural characterisitics of sustentacular cells in control and odoranttreated olfactory mucosae of the salamander. Anat Rec 221, 769-779 (1988)

95. J. van Blerkom: Microtubule mediation of cytoplasmic and nuclear maturation during the early stages of resumed mitosis in cultured mouse oocytes. Proc Natl Acad Sci USA 88, 5031-5035 (1991)

96. J. T. Povlishock: The fine structure of axons and growth cones of the human fetal cerebral cortex. Brain Res 114, 379-391 (1976)

97. A. Peters, S. L. Palay, & H. d. Webster: The Fine Structure of the Nervous System: The Neurons and Supporting Cells. New York: Oxford University Press, 1991. 1-494

98. C. Fabricius, C.H. Berthold, & M. Rydmark: Axoplasmic organelles at nodes of Ranvier. II. Occurence and distribution in large myelinated spinal cord axons of the adult cat. J Neurocytol 22, 941-954 (1993)

99. H. H. Treeck & W. Pirsig: Differentiation of nerve endings in the cochlear nucleus on morphological and experimental basis. Acta OtoLaryngologica 87, 47-60 (1979)

100. T. Gotow, K. Miyaguchi, & P. H. Hashimoto: Cytoplasmic architecture of the axon terminal: Filamentous strands specifically associated with synaptic vesicles. Neurosci 40, 587-598 (1991)

101. N. Bogan & J. B. Cabot: Light and electron microscopic analyses of intraspinal collaterals of sympathetic preganglionic neurons. Brain Res 541, 241-251 (1991)

102. G. H. Kageyama & M. WongRiley: Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways. Neurosci 7, 2337-2361 (1982)

103. D. J. Price: Patterns of cytochrome oxidase activity in areas 17, 18, and 19 of the visual cortex of cats and kittens. Exp Brain Res 58, 125-133 (1985)

104. M. WongRiley & C. Welt: Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc Natl Acad Sci USA 77, 2333-2337 (1980)

105. M. WongRiley & E. W. Carroll: Effect of impulse blockage on cytochrome oxidase activity in monkey visual system. Nature 307, 262-264 (1984)

106. S. T. Smiley, M. Reers, C. MottolaHartshorn, M. Lin, A. Chen, T. W. Smith, G. D. Steele, & L. B. Chen: Intracellular heterogeneity in mitochondrial membrane potentials revealed by a Jaggregate-forming lipophilic cation JC1. Proc Natl Acad Sci USA 88, 3671-3675 (1991)

107. M. Reers, T. W. Smith, & L. B. Chen: Jaggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochem 30, 4480-4486 (1991)

108. E. W. Carroll & M. WongRiley: Quantitative light and electron microscopic analysis of cytochrome oxidaserich zones in the striate cortex of the squirrel monkey. J Comp Neurol 222, 1-17 (1984)

109. G. H. Kageyama & M. WongRiley: An analysis of the cellular localization of cytochrome oxidase in the lateral geniculate nucleus of the adult cat. J Comp Neurol 242, 338-357 (1985)

110. M. Marciniak: Morphometric ultrastructural evaluation of the axonal endings in the neuromuscular junctions of pigeons after long lasting limitation of movement. Exper Pathol 23, 27-34 (1983)

111. Z. Sahenk & R. J. Lasek: Inhibition of proteolysis blocks anterograderetrograde conversion of axonally transported vesicles. Brain Res 460, 199-203 (1988)

112. R. S. Smith & R. E. Snyder: Reversal of rapid axonal transport at a lesion: Leupeptin inhibits reversed protein transport, but does not inhibit reversed organelle transport. Brain Res 552, 215-227 (1991)

113. Z. Sahenk & A. Brown: Weakbase amines inhibit the anterogradetoretrograde conversion of axonally transported vesicles in nerve terminals. J Neurocytol 20, 365-375 (1991)

114. K. L. Lankford, F. G. DeMello, & W. L. Klein: D1type dopamine receptors inhibit growth cone motility in cultured retina neurons: evidence that neurotransmitters act as morphogenetic growth factors in the developing nervous system. Proc Natl Acad Sci USA 85, 4567-4571 (1988)

115. M. P. Mattson & S. B. Kater: Calcium regulation of neurite elongation and growth cone motility. J Neurosci 7, 4034-4043 (1987)

116. M. P. Mattson, A. TaylorHunter, & S. B. Kater: Neurite outgrowth in individual neurons of a neuronal population is differentially regulated by calcium and cyclic AMP. J Neurosci (1988)

117. K. L. Lankford & P. C. Letourneau: Roles of actin filaments and three secondmessenger systems in shortterm regulation of chick dorsal root ganglion neurite outgrowth. Cell Motil Cytoskel 20, 7-29 (1991)

118. S. K. Kater, M. P. Mattson, C. Cohan, & J. Connor: Calcium regulation of the neuronal growth cone. Trends Neurosci 11, 317-323 (1988)

119. J. BereiterHahn & M. Voth: Metabolic control of shape and structure of mitochondria in situ. Biol Cell 47, 309-322 (1983)

120. K. Barkalow, T. Hamasaki, & P. Satir: Regulation of 22S dynein by a 29kD light chain. J Cell Biol 126, 727-735 (1994)

121. D. S. Smith, U. Jarlfors, & M. L. Cayer: Structural crossbridges between microtubules and mitochondria in central axons of an insect (Periplaneta americana). J Cell Sci 27, 255-272 (1977)

122. E. Pannese, P. Procacci, M. Ledda, G. Arcidiacono, D. Frattola, & L. Rigamonti: Association between microtubules and mitochondria in myelinated axons of Lacerta muralis. A quantitative analysis. Cell Tiss Res 245, 1-8 (1986)

123. R. L. Price, R. J. Lasek, & M. J. Katz: Microtubules have special physical associations with smooth endoplasmic reticula and mitochondria in axons. Brain Res 540, 209-216 (1991)

124. J. F. Leterrier, D. A. Rusakov, B. D. Nelson, & M. Linden: Interactions between brain mitochondria and cytoskeleton: evidence for specialized outer membrane domains involved in the association of cytoskeletonassociated proteins to mitochondria in situ and in vitro. Microscr Res Tech 27, 233-261 (1994)

125. M. Linden, B. D. Nelson, D. Loncar, & J. F. Leterrier: Studies on the interaction between mitochondria and the cytoskeleton. J Bioenerg Biomem 21, 507-518 (1989)

126. M. Linden, B. D. Nelson, & J. F. Leterrier: The specific binding of the microtubuleassociated protein 2 (MAP2) to the outer membrane of rat brain mitochondria. Biochem J 261, 167-173 (1989)

127. D. Jung, D. Filliol, M. Miehe, & A. Rendon: Interaction of brain mitochondria with microtubules reconstituted from brain tubulin and MAP 2 or TAU. Cell Motil Cytoskel 24, 245-255 (1993)

128. J. F. Leterrier, D. A. Rusakov, & M. Linden: Statistical analysis of the surface distribution of microtubuleassociated proteins (MAPs) bound in vitro to rat brain mitochondria and labelled by 10 nm goldcoupled antibodies. Bulletin de l Association des Anatomistes 78, 47-51 (1994)

[Table of Contents ] [Previous Section]