Summary
The spatial relationship between microtubules and mitochondria was studied in myelinated axons of the ventral and dorsal spinal roots of the lizard Lacerta muralis by use of quantitative methods in single and serial sections.
Microtubules mainly occurred in groups of 3 to 10. The mean density of microtubules was found to be significantly higher close to mitochondria than in the rest of the axoplasm. In single sections, 59–62% (according to the root region examined) of the microtubule groups were found to be ‘associated’ with mitochondria; this percentage rose to 74–76% in serial sections. The examination in serial sections of progressively longer segments of the same microtubule groups showed that the longer the segments of microtubule groups examined the higher was the percentage of microtubule groups ‘associated’ with mitochondria.
The results obtained show that in the axons studied in the present research a non-accidental spatial association exists between microtubule groups and mitochondria. This evidence supports the suggestion that the microtubule groups play a role in the movement of mitochondria along the axon, even though it does not clarify the precise nature of this role.
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References
Banks P, Till R (1975) A correlation between the effects of antimitotic drugs on microtubule assembly in vitro and the inhibition of axonal transport in noradrenergic neurones. J Physiol 252:283–294
Boesch J, Marko P, Cuénod M (1972) Effects of colchicine on axonal transport of proteins in the pigeon visual pathways. Neurobiology 2:123–132
Bray D, Bunge MB (1981) Serial analysis of microtubules in cultured rat sensory axons. J Neurocytol 10:589–605
Cooper PD, Smith RS (1974) The movement of optically detectable organelles in myelinated axons of Xenopus laevis. J Physiol (Lond) 242:77–97
Dahlström A (1968) Effect of colchicine on transport of amine storage granules in sympathetic nerves of rat. Eur J Pharmacol 5:111–113
Donoso JA, Watson DF, Heller-Bettinger IE, Samson FE (1978) Maytansine action on fast axoplasmic transport and the ultrastructure of vagal axons. Cancer Res 38:1633–1637
Dowell WCT (1964) Die Entwicklung geeigneter Folien für elektronenmikroskopische Präparatträger grossen Durchlassbereichs und ihre Verwendung zur Untersuchung von Kristallen. Optik 21:47–58
Dustin P (1978) Microtubules. Springer, Berlin Heidelberg New York
Edström A, Mattsson H (1972) Fast axonal transport in vitro in the sciatic system of the frog. J Neurochem 19:205–221
England JM, Kadin ME, Goldstein MN (1973) The effect of vincristine sulphate on the axoplasmic flow of proteins in cultured sympathetic neurons. J Cell Sci 12:549–565
Fink BR, Byers MR, Middaugh ME (1973) Dynamics of colchicine effects on rapid axonal transport and axonal morphology. Brain Res 56:299–311
Flament-Durand J, Couck A-M, Dustin P (1975) Studies on the transport of secretory granules in the magnocellular hypothalamic neurons of the rat. II. Action of vincristine on axonal flow and neurotubules in the paraventricular and supraoptic nuclei. Cell Tissue Res 164:1–9
Friede RL, Samorajski T (1970) Axon caliber related to neurofilaments and microtubules in sciatic nerve fibers of rats and mice. Anat Rec 167:379–387
Ghetti B, Ochs S (1978) On the relation between microtubule density and axoplasmic transport in nerves treated with maytansine in vitro. In: N Canal, Pozza G (eds) Peripheral Neuropathies. Developments in Neurology Vol. 1:177–186, Elsevier, Amsterdam
Grafstein B, Forman DS (1980) Intracellular transport in neurons. Physiol Rev 60:1167–1283
Green LS, Donoso JA, Heller-Bettinger IE, Samson FE (1977) Axonal transport disturbances in vincristine-induced peripheral neuropathy. Ann Neurol 1:255–262
Hanson M, Edström A (1977) Fast axonal transport: Effect of antimitotic drugs and inhibitors of energy metabolism on the rate and amount of transported protein in frog sciatic nerves. J Neurobiol 8:97–108
Hirano A, Zimmerman HM (1971) Some new pathological findings in the central myelinated axon. J Neuropathol Exp Neurol 30:325–336
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 94:129–142
Hökfelt T, Dahlström A (1971) Effects of two mitosis inhibitors (colchicine and vinblastine) on the distribution and axonal transport of noradrenaline storage particles, studied by fluorescence and electron microscopy. Z Zellforsch 119:460–482
Jackson P, Diamond J (1977) Colchicine block of cholinesterase transport in rabbit sensory nerves without interference with the long-term viability of the axons. Brain Res 130:579–584
James KAC, Bray JJ, Morgan IG, Austin L (1970) The effect of colchicine on the transport of axonal protein in the chicken. Biochem J 117:767–771
Karlsson J-O, Sjöstrand J (1969) The effect of colchicine on the axonal transport of protein in the optic nerve and tract of the rabbit. Brain Res 13:617–619
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A-138A
Kendall MG, Stuart A (1958) The advanced theory of statistics. Vol 1: Distribution theory. Charles Griffin and Company Limited, London
Kendall MG, Stuart A (1961) The advanced theory of statistics. Vol 2: Inference and relationship. Charles Griffin and Company Limited, London
Krammer EB, Zenker W (1975) Effekt von Zinkionen auf Struktur und Verteilung der Neurotubuli. Acta Neuropathol 31:59–69
Lasek RJ (1970) Protein transport in neurons. Int Rev Neurobiol 13:289–324
Malbouisson AMB, Ghabriel MN, Allt G (1985) Axonal microtubules: A computer-linked quantitative analysis. Anat Embryol 171:339–344
Pannese E, Ledda M, Arcidiacono G, Rigamonti L, Procacci P (1981) Density and distribution of microtubules in the axons of the lizard dorsal roots. J Submicrosc Cytol 13:169–181
Pannese E, Procacci P, Ledda M, Arcidiacono G, Rigamonti L (1984) A quantitative study of microtubules in motor and sensory axons. Acta Anat 118:193–200
Paulson JC, McClure WO (1975) Microtubules and axoplasmic transport. Inhibition of transport by podophyllotoxin: An interaction with microtubule protein. J Cell Biol 67:461–467
Peachey LD (1958) Thin sections I. A study of section thickness and physical distortion produced during microtomy. J Biophys Biochem Cytol 4:233–242
Raine CS, Ghetti B, Shelanski ML (1971) On the association between microtubules and mitochondria within axons. Brain Res 34:389–393
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Samson F, Donoso JA, Heller-Bettinger I, Watson D, Hirnes RH (1979) Nocodazole action on tubulin assembly, axonal ultrastructure and fast axoplasmic transport. J Pharmacol Exp Ther 208:411–417
Schnapp BJ, Reese TS (1982) Cytoplasmic structure in rapid-frozen axons. J Cell Biol 94:667–679
Schnapp BJ, Vale RD, Sheetz MP, Reese TS (1985) Single microtubules from squid axoplasm support bidirectional movement of organelles. Cell 40:455–462
Smith DS, Järlfors U, Cameron BF (1975) Morphological evidence for the participation of microtubules in axonal transport. Ann NY Acad Sci 253:472–506
Smith DS, Järlfors U, Cayer ML (1977) Structural cross-bridges between microtubules and mitochondria in central axons of an insect (Periplaneta americana). J Cell Sci 27:255–272
Smith RS (1973) Microtubule and neurofilament densities in amphibian spinal root nerve fibers: Relationship to axoplasmic transport. Can J Physiol Pharmacol 51:798–806
Tsukita S, Ishikawa H (1981) The cytoskeleton in myelinated axons: Serial section study. Biomed Res 2:424–437
Weiss DG, Gross GW (1983) Intracellular transport in axonal microtubular domains I. Theoretical considerations on the essential properties of a force generating mechanism. Protoplasma 114:179–197
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Pannese, E., Procacci, P., Ledda, M. et al. Association between microtubules and mitochondria in myelinated axons of Lacerta muralis . Cell Tissue Res. 245, 1–8 (1986). https://doi.org/10.1007/BF00218080
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DOI: https://doi.org/10.1007/BF00218080