Skip to main content
Advertisement

Main menu

  • Home
  • Articles
    • Accepted manuscripts
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Cell Scientists to Watch
    • First Person
    • Sign up for alerts
  • About us
    • About JCS
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Fast-track manuscripts
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • JCS Prize
    • Manuscript transfer network
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JCS
    • Subscriptions
    • Advertising
    • Feedback
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

User menu

  • Log in
  • Log out

Search

  • Advanced search
Journal of Cell Science
  • COB
    • About The Company of Biologists
    • Development
    • Journal of Cell Science
    • Journal of Experimental Biology
    • Disease Models & Mechanisms
    • Biology Open

supporting biologistsinspiring biology

Journal of Cell Science

  • Log in
Advanced search

RSS   Twitter  Facebook   YouTube  

  • Home
  • Articles
    • Accepted manuscripts
    • Latest complete issue
    • Issue archive
    • Archive by article type
    • Special issues
    • Subject collections
    • Cell Scientists to Watch
    • First Person
    • Sign up for alerts
  • About us
    • About JCS
    • Editors and Board
    • Editor biographies
    • Travelling Fellowships
    • Grants and funding
    • Journal Meetings
    • Workshops
    • The Company of Biologists
    • Journal news
  • For authors
    • Submit a manuscript
    • Aims and scope
    • Presubmission enquiries
    • Fast-track manuscripts
    • Article types
    • Manuscript preparation
    • Cover suggestions
    • Editorial process
    • Promoting your paper
    • Open Access
    • JCS Prize
    • Manuscript transfer network
    • Biology Open transfer
  • Journal info
    • Journal policies
    • Rights and permissions
    • Media policies
    • Reviewer guide
    • Sign up for alerts
  • Contacts
    • Contact JCS
    • Subscriptions
    • Advertising
    • Feedback
Journal Articles
Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons
C.C. Overly, H.I. Rieff, P.J. Hollenbeck
Journal of Cell Science 1996 109: 971-980;
C.C. Overly
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
H.I. Rieff
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
P.J. Hollenbeck
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • Article
  • Info & metrics
  • PDF
Loading

Summary

Regional regulation of organelle transport seems likely to play an important role in establishing and maintaining distinct axonal and dendritic domains in neurons, and in managing differences in local metabolic demands. In addition, known differences in microtubule polarity and organization between axons and dendrites along with the directional selectivity of microtubule-based motor proteins suggest that patterns of organelle transport may differ in these two process types. To test this hypothesis, we compared the patterns of movement of different organelle classes in axons and different dendritic regions of cultured embryonic rat hippocampal neurons. We first examined the net direction of organelle transport in axons, proximal dendrites and distal dendrites by video-enhanced phase-contrast microscopy. We found significant regional variation in the net transport of large phase-dense vesicular organelles: they exhibited net retrograde transport in axons and distal dendrites, whereas they moved equally in both directions in proximal dendrites. No significant regional variation was found in the net transport of mitochondria or macropinosomes. Analysis of individual organelle motility revealed three additional differences in organelle transport between the two process types. First, in addition to the difference in net transport direction, the large phase-dense organelles exhibited more persistent changes in direction in proximal dendrites where microtubule polarity is mixed than in axons where microtubule polarity is uniform. Second, while the net direction of mitochondrial transport was similar in both processes, twice as many mitochondria were motile in axons than in dendrites. Third, the mean excursion length of moving mitochondria was significantly longer in axons than in dendrites. To determine whether there were regional differences in metabolic activity that might account for these motility differences, we labeled mitochondria with the vital dye, JC-1, which reveals differences in mitochondrial transmembrane potential. Staining of neurons with this dye revealed a greater proportion of highly charged, more metabolically active, mitochondria in dendrites than in axons. Together, our data reveal differences in organelle motility and metabolic properties in axons and dendrites of cultured hippocampal neurons.

  • © 1996 by Company of Biologists

REFERENCES

    1. Abelson P. H.
    (1984). An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. II. Synaptic relationships. J. Neurosci 4, 1954–1965
    OpenUrlAbstract
    1. Baas P. W.,
    2. Deitch J. S.,
    3. Black M. M. and
    4. Banker G. A.
    (1988). Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Nat. Acad. Sci. USA 85, 8335–8339
    OpenUrlAbstract/FREE Full Text
    1. Baas P. W.,
    2. Black M. M. and
    3. Banker G. A.
    (1989). Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J. Cell Biol 109, 3085–3094
    OpenUrlAbstract/FREE Full Text
    1. Baas P. W.,
    2. Slaughter T.,
    3. Brown A. and
    4. Black M. M.
    (1991). Microtubule dynamics in axons and dendrites. J. Neurosci. Res 30, 134–153
    OpenUrlCrossRefPubMedWeb of Science
    1. Black M. M. and
    2. Baas P. W.
    (1989). The basis of polarity in neurons. Trends Neurosci 12, 211–214
    OpenUrlCrossRefPubMedWeb of Science
    1. Brady S. T.,
    2. Lasek R. J. and
    3. Allen R. D.
    (1982). Fast axonal transport in extruded axoplasm from squid giant axon. Science 218, 1129–1131
    OpenUrlAbstract/FREE Full Text
    1. Brady S. T.
    (1991). Molecular motors in the nervous system. Neuron 7, 521–533
    OpenUrlCrossRefPubMedWeb of Science
    1. Bray D. and
    2. Bunge M. B.
    (1981). Serial analysis of microtubules in cultured rat sensory axons. J. Neurocytol 10, 589–605
    OpenUrlCrossRefPubMedWeb of Science
    1. Burton P. R. and
    2. Paige J. L.
    (1981). Polarity of axoplasmic microtubules in the olfactory nerve of the frog. Proc. Nat. Acad. Sci. USA 78, 3269–3273
    OpenUrlAbstract/FREE Full Text
    1. Burton P. R.
    (1987). Microtubules of frog olfactory axons: their length and number/axon. Brain Res 409, 71–78
    OpenUrlCrossRefPubMed
    1. Burton P. R.
    (1988). Dendrites of mitral cell neurons contain microtubules of opposite polarity. Brain Res 473, 107–115
    OpenUrlCrossRefPubMedWeb of Science
    1. Chen J.,
    2. Kanai Y.,
    3. Cowan N. J. and
    4. Hirokawa N.
    (1992). Projection domains of MAP2 and tau determine spacings between microtubules in dendrites and axons. Nature 360, 674–677
    OpenUrlCrossRefPubMedWeb of Science
    1. Corthesy-Theulaz I.,
    2. Pauloin A. and
    3. Pfeffer S. R.
    (1992). Cytoplasmic dynein participates in the centrosomal localization of the Golgi complex. J. Cell Biol 118, 1333–1345
    OpenUrlAbstract/FREE Full Text
    1. Dailey M. E. and
    2. Bridgman P. C.
    (1993). Vacuole dynamics in growth cones: Correlated EM and video observations. J. Neurosci 13, 3375–3393
    OpenUrlAbstract
    1. Dotti C. G.,
    2. Sullivan C. A. and
    3. Banker G. A.
    (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci 8, 1454–1468
    OpenUrlAbstract
    1. Fletcher T. L.,
    2. De Camilli P. and
    3. Banker G.
    (1994). Synaptogenesis in hippocampal cultures: Evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J. Neurosci 14, 6695–6706
    OpenUrlAbstract
    1. Gorenstein C.,
    2. Bundman M. C.,
    3. Lew P. J.,
    4. Olds J. L. and
    5. Ribak C. E.
    (1985). Dendritic transport. I. Colchicine stimulates the transport of lysosomal enzymes from cell bodies to dendrites. J. Neurosci 5, 2009–2017
    OpenUrlAbstract
    1. Gorenstein C. and
    2. Ribak C. E.
    (1985). Dendritic transport. II. Somatofugal movement of neuronal lysosomes induced by colchicine: evidence for a novel transport system in dendrites. J. Neurosci 5, 2018–2027
    OpenUrlAbstract
    1. Heidemann S. R.,
    2. Landers J. and
    3. Hamborg M.
    (1981). Polarity orientation of axonal microtubules. J. Cell Biol 91, 661–665
    OpenUrlAbstract/FREE Full Text
    1. Herman B. and
    2. Albertini D. F.
    (1984). A time-lapse video image intensification analysis of cytoplasmic organelle movements during endosome translocation. J. Cell Biol 98, 565–576
    OpenUrlAbstract/FREE Full Text
    1. Ho W. C.,
    2. Allen V. J.,
    3. van Meer G.,
    4. Berger E. G. and
    5. Kreis T. E.
    (1989). Reclustering of scattered Golgi elements occurs along microtubules. Eur. J. Cell Biol 48, 250–263
    OpenUrlPubMedWeb of Science
    1. Hollenbeck P. J. and
    2. Bray D.
    (1987). Rapidly transported organelles containing membrane and cytoskeletal components: their relation to axonal growth. J. Cell Biol 105, 2827–2835
    OpenUrlAbstract/FREE Full Text
    1. Hollenbeck P. J. and
    2. Swanson J. A.
    (1990). Radial extension of macrophage tubular lysosomes supported by kinesin. Nature 346, 864–866
    OpenUrlCrossRefPubMed
    1. Hollenbeck P. J.
    (1993). Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol 121, 305–315
    OpenUrlAbstract/FREE Full Text
    1. Johnson L. V.,
    2. Walsh M. L.,
    3. Bockus B. J. and
    4. Chen L. B.
    (1981). Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J. Cell Biol 88, 526–535
    OpenUrlAbstract/FREE Full Text
    1. Kiss J.
    (1977). Synthesis and transport of newly formed proteins in dendrites of rat hippocampal pyramid cells. An electron microscope autoradiographic study. Brain Res 124, 237–250
    OpenUrlCrossRefPubMedWeb of Science
    1. Kleiman R.,
    2. Banker G. and
    3. Steward O.
    (1994). Development of subcellular mRNA compartmentation in hippocampal neurons in culture. J. Neurosci 14, 1130–1140
    OpenUrlAbstract
    1. Lee C.,
    2. Ferguson M. and
    3. Chen L. B.
    (1989). Construction of the endoplasmic reticulum. J. Cell Biol 109, 2045–2055
    OpenUrlAbstract/FREE Full Text
    1. Leopold P. L.,
    2. McDowall A. W.,
    3. Pfister K. K.,
    4. Bloom G. S. and
    5. Brady S. T.
    (1992). Association of kinesin with characterized membrane-bounded organelles. Cell Motil. Cytoskel 23, 19–33
    OpenUrlCrossRefPubMedWeb of Science
    1. Lippincott-Schwartz J.,
    2. Cole N. B.,
    3. Marotta A.,
    4. Conrad P. A. and
    5. Bloom G. S.
    (1995). Kinesin is the motor for microtubule-associated Golgi-to-ER membrane traffic. J. Cell Biol 128, 293–306
    OpenUrlAbstract/FREE Full Text
    1. Lopez L. A. and
    2. Sheetz M. P.
    (1993). Steric inhibition of cytoplasmic dynein and kinesin motility by MAP2. Cell Motil. Cytoskel 24, 1–16
    OpenUrlCrossRefPubMedWeb of Science
    1. Lynch T. J.,
    2. Taylor J. D. and
    3. Tchen T. T.
    (1986). Regulation of pigment organelle translocation. I. Phosphorylation of the organelle-associated protein p57. J. Biol. Chem 261, 4204–4211
    OpenUrlAbstract/FREE Full Text
    1. Lynch T. J.,
    2. Wu B.-Y.,
    3. Taylor J. D. and
    4. Tchen T. T.
    (1986). Regulation of pigment organelle translocation. II. Participation of cAMP-dependent protein kinase. J. Biol. Chem 261, 4212–4216
    OpenUrlAbstract/FREE Full Text
    1. Marks D. L.,
    2. Larkin J. M. and
    3. McNiven M. A.
    (1994). Association of kinesin with the Golgi apparatus in rat hepatocytes. J. Cell Sci 107, 2417–2426
    OpenUrlAbstract/FREE Full Text
    1. Matteoni R. and
    2. Kreis T. E.
    (1987). Translocation and clustering of endosomes and lysosomes depends on microtubules. J. Cell Biol 105, 1253–1265
    OpenUrlAbstract/FREE Full Text
    1. Matus A.,
    2. Bernhardt R. and
    3. Hugh-Jones T.
    (1981). High molecular weightmicrotubule-associated proteins are preferentially associated with dendritic microtubules in brain. Proc. Nat. Acad. Sci. USA 78, 3010–3014
    OpenUrlAbstract/FREE Full Text
    1. Morris R. L. and
    2. Hollenbeck P. J.
    (1993). The regulation of bidirectional mitochondrial transport is coordinated with axonal outgrowth. J. Cell Sci 104, 917–927
    OpenUrlAbstract/FREE Full Text
    1. Nangaku M.,
    2. Sato-Yoshitake R.,
    3. Okada Y.,
    4. Noda Y.,
    5. Takemura R.,
    6. Yamazaki H. and
    7. Hirokawa N.
    (1994). KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell 79, 1209–1220
    OpenUrlCrossRefPubMedWeb of Science
    1. Okada Y.,
    2. Yamazaki H.,
    3. Sekineaizawa Y. and
    4. Hirokawa N.
    (1995). The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81, 769–780
    OpenUrlCrossRefPubMedWeb of Science
    1. Parton R. G.,
    2. Simons K. and
    3. Dotti C. G.
    (1992). Axonal and dendritic endocytic pathways in cultured neurons. J. Cell Biol 119, 123–137
    OpenUrlAbstract/FREE Full Text
    1. Reers M.,
    2. Smith T. W. and
    3. Chen L. B.
    (1991). J-aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30, 4480–4486
    OpenUrlCrossRefPubMed
    1. Rodionov V. I.,
    2. Gyoeva F. K. and
    3. Gelfand V. I.
    (1991). Kinesin is responsible for centrifugal movement of pigment granules in melanophores. Proc. Nat. Acad. Sci. USA 88, 4956–4960
    OpenUrlAbstract/FREE Full Text
    1. Rogalski A. A. and
    2. Singer S. J.
    (1984). Associations of elements of the Golgi apparatus with microtubules. J. Cell Biol 99, 1092–1100
    OpenUrlAbstract/FREE Full Text
    1. Rozdzial M. M. and
    2. Haimo L. T.
    (1986). Reactivated melanosome motility: differential regulation and nucleotide requirements of bidirectional pigment granule transport. J. Cell Biol 103, 2755–2764
    OpenUrlAbstract/FREE Full Text
    1. Rozdzial M. M. and
    2. Haimo L. T.
    (1986). Bidirectional pigment granule movements of melanophores are regulated by protein phosphorylation and dephosphorylation. Cell 47, 1061–1070
    OpenUrlCrossRefPubMedWeb of Science
    1. Schmitz F.,
    2. Wallis K. T.,
    3. Rho M.,
    4. Drenckhahn D. and
    5. Murphy D. B.
    (1994). Intracellular distribution of kinesin in chromaffin cells. Eur. J. Cell Biol 63, 77–83
    OpenUrlPubMedWeb of Science
    1. Sheetz M. P.,
    2. Steuer E. R. and
    3. Schroer T. A.
    (1989). The mechanism and regulation of fast axonal transport. Trends Neurosci 12, 474–478
    OpenUrlCrossRefPubMedWeb of Science
    1. Skoufias D. A. and
    2. Scholey J. M.
    (1993). Cytoplasmic microtubule-based motor proteins. Curr. Opin. Cell Biol 5, 95–104
    OpenUrlCrossRefPubMed
    1. Smiley S. T.,
    2. Reers M.,
    3. Mottola-Hartshorn C.,
    4. Lin M.,
    5. Chen A.,
    6. Smith T. W.,
    7. Steele G. D. and
    8. Chen L. B.
    (1991). Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregate-forming lipophilic cation JC-1. Proc. Nat. Acad. Sci. USA 88, 3671–3675
    OpenUrlAbstract/FREE Full Text
    1. Smith R. S. and
    2. Forman D. S.
    (1988). Organelle dynamics in lobster axons: anterograde and retrograde particulate organelles. Brain Res 446, 26–36
    OpenUrlCrossRefPubMedWeb of Science
    1. Swanson J. A.,
    2. Locke A.,
    3. Ansel P. and
    4. Hollenbeck P. J.
    (1992). Radial movement of lysosomes along microtubules in permeabilized macrophages. J. Cell Sci 103, 201–209
    OpenUrlAbstract/FREE Full Text
    1. Terasaki M.,
    2. Song J. D.,
    3. Wong J. R.,
    4. Weiss M. J. and
    5. Chen L. B.
    (1984). Localization of endoplasmic reticulum in living and glutaraldehyde fixed cells with fluorescent dyes. Cell 38, 101–108
    OpenUrlCrossRefPubMedWeb of Science
    1. Terasaki M.,
    2. Chen L. B. and
    3. Fujiwara K.
    (1986). Localization of endoplasmic reticulum in living and fixed cells with fluorescent dyes. J. Cell Biol 103, 1557–1568
    OpenUrlAbstract/FREE Full Text
    1. Vallee R. B. and
    2. Bloom G. S.
    (1991). Mechanisms of fast and slow axonal transport. Annu. Rev. Neurosci 14, 59–92
    OpenUrlCrossRefPubMedWeb of Science
    1. Wehland J.,
    2. Henkart M.,
    3. Klausner R. and
    4. Sandoval I. V.
    (1983). Role of microtubules in the distribution of the Golgi apparatus: effect of taxol and microinjected anti-alpha-tubulin antibodies. Proc. Nat. Acad. Sci. USA 80, 4286–4290
    OpenUrlAbstract/FREE Full Text
    1. Wuerker R. B. and
    2. Kirkpatrick J. B.
    (1972). Neuronal microtubules, neurofilaments, and microfilaments. Int. Rev. Cytol 33, 45–75
    OpenUrlCrossRefPubMedWeb of Science
    1. Yu W. Q. and
    2. Baas P. W.
    (1994). Changes in microtubule number and length during axon differentiation. J. Neurosci 14, 2818–2829
    OpenUrlAbstract
Previous ArticleNext Article
Back to top
Previous ArticleNext Article

This Issue

 Download PDF

Email

Thank you for your interest in spreading the word on Journal of Cell Science.

NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. We do not capture any email address.

Enter multiple addresses on separate lines or separate them with commas.
Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons
(Your Name) has sent you a message from Journal of Cell Science
(Your Name) thought you would like to see the Journal of Cell Science web site.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Journal Articles
Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons
C.C. Overly, H.I. Rieff, P.J. Hollenbeck
Journal of Cell Science 1996 109: 971-980;
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
Citation Tools
Journal Articles
Organelle motility and metabolism in axons vs dendrites of cultured hippocampal neurons
C.C. Overly, H.I. Rieff, P.J. Hollenbeck
Journal of Cell Science 1996 109: 971-980;

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Alerts

Please log in to add an alert for this article.

Sign in to email alerts with your email address

Article navigation

  • Top
  • Article
  • Info & metrics
  • PDF

Related articles

Cited by...

More in this TOC section

  • Involvement of actin filaments and integrins in the binding step in collagen phagocytosis by human fibroblasts
  • University administration
  • The cytoplasmic domain of the interleukin-6 receptor gp80 mediates its basolateral sorting in polarized madin-darby canine kidney cells
Show more Journal Articles

Similar articles

Other journals from The Company of Biologists

Development

Journal of Experimental Biology

Disease Models & Mechanisms

Biology Open

Advertisement

2020 at The Company of Biologists

Despite the challenges of 2020, we were able to bring a number of long-term projects and new ventures to fruition. While we look forward to a new year, join us as we reflect on the triumphs of the last 12 months.


Mole – The Corona Files

"This is not going to go away, 'like a miracle.' We have to do magic. And I know we can."

Mole continues to offer his wise words to researchers on how to manage during the COVID-19 pandemic.


Cell scientist to watch – Christine Faulkner

In an interview, Christine Faulkner talks about where her interest in plant science began, how she found the transition between Australia and the UK, and shares her thoughts on virtual conferences.


Read & Publish participation extends worldwide

“The clear advantages are rapid and efficient exposure and easy access to my article around the world. I believe it is great to have this publishing option in fast-growing fields in biomedical research.”

Dr Jaceques Behmoaras (Imperial College London) shares his experience of publishing Open Access as part of our growing Read & Publish initiative. We now have over 60 institutions in 12 countries taking part – find out more and view our full list of participating institutions.


JCS and COVID-19

For more information on measures Journal of Cell Science is taking to support the community during the COVID-19 pandemic, please see here.

If you have any questions or concerns, please do not hestiate to contact the Editorial Office.

Articles

  • Accepted manuscripts
  • Latest complete issue
  • Issue archive
  • Archive by article type
  • Special issues
  • Subject collections
  • Interviews
  • Sign up for alerts

About us

  • About Journal of Cell Science
  • Editors and Board
  • Editor biographies
  • Travelling Fellowships
  • Grants and funding
  • Journal Meetings
  • Workshops
  • The Company of Biologists

For Authors

  • Submit a manuscript
  • Aims and scope
  • Presubmission enquiries
  • Fast-track manuscripts
  • Article types
  • Manuscript preparation
  • Cover suggestions
  • Editorial process
  • Promoting your paper
  • Open Access
  • JCS Prize
  • Manuscript transfer network
  • Biology Open transfer

Journal Info

  • Journal policies
  • Rights and permissions
  • Media policies
  • Reviewer guide
  • Sign up for alerts

Contacts

  • Contact JCS
  • Subscriptions
  • Advertising
  • Feedback

Twitter   YouTube   LinkedIn

© 2021   The Company of Biologists Ltd   Registered Charity 277992