Biology Faculty: Ben Szaro

Ben G. Szaro

Professor of Biological Sciences
Ph.D., Johns Hopkins University

Office LS1059
Telephone (518) 591-8852
Fax (518) 442-4767
Email bszaro@albany.edu

Areas of Interest

  • Developmental Neurobiology
  • Molecular Neurobiology
  • Neural Regeneration
  • Neurofilaments
  • Axonal Growth
  • Xenopus laevis Embryology


Research

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In my laboratory we use the tools of modern molecular and cell biology to study axonal development. Neurofilaments are one of the principal components of the axonal cytoskeleton, and their molecular composition changes during axonal development. We hypothesize that these changes influence the structural properties of growing axons, and help them to accomodate the varying requirements for plasticity and stability that arise during development. To explore this hypothesis, we study the neurofilaments of axons in the frog, Xenopus laevis.


Xenopus laevis


Electron micrograph of X. laevis optic axon. nf, neurofilaments; mt, microtubules; mf, microfilaments


In mammals, the neurofilaments of injured peripheral axons, which can regenerate, resemble those of newly developing axons; whereas the neurofilaments of mammalian central nervous system axons, which cannot regenerate, remain adult-like after injury. The ability of axons to regenerate in mammals is controlled, at least in part, by substances produced by glial cells found along axonal pathways.

Frog optic axons, unlike those of mammals, successfully regenerate fully functional connections following nerve injury. We have shown that the neurofilament composition of these injured axons resembles that of newly developing ones. Moreover, we discovered that these regenerating axons modulate their neurofilament compositions in response to cues emanating from other cells along the visual pathway. We believe that studying what regulates neurofilament protein expression may provide clues to the riddle of why axons vary in their ability to regenerate.

We also study how changes in axonal neurofilament composition influence axonal growth and development. We alter the neurofilaments of developing axons by injecting antibodies and mRNA molecules into frog embryos. These mRNAs encode either normal or mutated frog neurofilament proteins. The axons altered by these procedures are then studied in the intact frog embryo and in tissue culture.


Tadpole that was injected at the 2-cell stage with Beta-galactosidase mRNA

Cultured neuron and muscle cell expressing Green Fluorescent Protein


Students in my laboratory learn modern techniques of molecular and cell biology
as they study the factors that influence neurofilament protein gene expression and explore how neurofilaments influence axonal growth.

Publications

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  • Liu, Y., Wang, C., Destin, G., Szaro, B.G. (2015) Microtubule-associated protein tau promotes neuronal class II beta-tubulin microtubule formation and axon elongation in embryonic Xenopus laevis. Eur. J. Neurosci. 41:1263-1275.
  • Wang, C., Szaro, B.G. (2015) A method for using direct injection of plasmid DNA to study cis-regulatory element activity in F0 Xenopus embryos and tadpoles. Dev. Biol. 398: 11-23.
  • Hutchins, E.J. and Szaro, B.G.(2013) c-Jun N-terminal kinase phosphorylation of heterogeneous nuclear ribonucleoprotein K regulates vertebrate axon outgrowth via a posttranscriptional mechanism. J. Neurosci., 33: 14666-14680.
  • Liu, Y., Yu, H., Deaton, S.K. and Szaro, B.G. (2012) Heterogeneous nuclear ribonucleoprotein K, an RNA-binding protein, is required for optic axon regeneration in Xenopus laevis. J. Neurosci., 32: 3563-74.
  • Liu, Y., Szaro, B.G. (2011) hnRNP K post-transcriptionally co-regulates multiple cytoskeletal genes needed for axonogenesis. Development 138: 3079-3090.
  • Szaro, B.G., and Strong, M.J. (2011) Regulation of cytoskeletal composition in neurons: transcriptional and post-transcriptional control in development, regeneration, and disease. Adv. Neurobiol. 3: 559-602.
  • Gibbs, K., Chittur, S., Szaro, B.G. (2011) Metamorphosis and the regenerative capacity of spinal cord axons in Xenopus laevis. Eur. J. Neurosci. 33: 9-25.
  • Szaro, B.G., and Strong, M.J. (2010) Post-transcriptional control of neurofilaments: new roles in development, regeneration and neurodegenerative disease. Trends Neurosci 33: 27-37.
  • Ananthakrishnan, L., Szaro, B.G. (2009) Transcriptional and translational dynamics of light neurofilament subunit RNAs during Xenopus laevis optic nerve regeneration. Brain Res 1250: 27-40.
  • Thyagarajan, A., and Szaro, B.G. (2008) Dynamic endogenous association of neurofilament mRNAs with K-homology domain ribonucleoproteins in developing cerebral cortex. Brain Res. 1189: 33-42.
  • Ananthakrishnan, L., Gervasi, C., and Szaro, B.G. (2008) Dynamic regulation of middle neurofilament (NF-M) RNA pools during optic nerve regeneration. Neurosci. 153: 144-153.
  • Liu, Y., Gervasi, C., and Szaro, B.G. (2008) A crucial role for hnRNP K in axon development in Xenopus laevis. Development 135: 3125- 3135.
  • Thyagarajan, A., Strong, M.J., and Szaro, B.G. (2007) Post-transcriptional control of neurofilaments in development and disease. Exp. Cell Res. 313: 2088-2097.
  • Thyagarajan, A., Strong, M.J., and Szaro, B.G. (2007) Post-transcriptional control of neurofilaments in development and disease. Exp. Cell Res. 313: 2088-2097.
  • Feng, X., Castracane, J., Tokranova, N., Gracias, A., Lnenicka, G., and Szaro, B.G. (2007) A living cell-based biosensor utilizing G-protein coupled receptors: Principles and detection methods. Biosens. Bioelect. 22: 3230-3237.
  • Gibbs, K.M., and Szaro, B.G. (2006) Regeneration of descending projections in Xenopus laevis tadpole spinal cord demonstrated by retrograde double labeling. Brain Res. 1088: 68-72.
  • Smith, A., Gervasi, C., and Szaro, B.G. (2006) Neurofilament content is correlated with branch length in developing collateral branches of Xenopus spinal cord neurons. Neurosci. Lett. 403: 283-287.
  • Gervasi C, Szaro BG. (2004) Performing functional studies of Xenopus laevis intermediate filament proteins through injection of macromolecules into early embryos. Methods Cell Biol. 78:673-701.
  • Thyagarajan A, Szaro BG. (2004) Phylogenetically conserved binding of specific K homology domain proteins to the 3'-untranslated region of the vertebrate middle neurofilament mRNA. J Biol Chem. 279:49680-8.
  • Gervasi, C., Thyagarajan, A., and Szaro, B.G. (2003) Increased expression of multiple neurofilament mRNAs during regeneration of vertebrate central nervous system axons. J. Comp. Neurol. 461:262–275.
  • Undamatla, J. and Szaro, B.G. (2001) Differential expression and localization of neuronal intermediate filament proteins within newly developing neurites in dissociated cultures of Xenopus laevis embryonic spinal cord. Cell Motil. Cytoskel. 49:16-32.
  • Walker, K.L., Yoo, H.K., Undamatla, J., and Szaro, B.G. (2001) Loss of neurofilaments alters axonal growth dynamics. J. Neurosci., 21:9655-9666.
  • Gervasi, C., Stewart, C.-B., and Szaro, B.G. (2000) Xenopus laevis peripherin (XIF3) is expressed in radial glia and proliferating neural epithelial cells as well as in neurons. J. Comp. Neurol. 423:512-531.
  • Roosa, J.R., Gervasi, C., and Szaro, B.G. (2000) Structure, biological activity of the upstream regulatory sequence, and conserved domains of a middle molecular mass neurofilament gene of Xenopus laevis. Mol. Brain Res. 82:35-51.
  • Dearborn, R.E. Jr., Szaro, B.G. and Lnenicka, G.A. (1999) Cloning and characterization of AASPs: Novel axon-associated SH3 binding-like proteins. J. Neurobiol. 38:581-594.
  • Dearborn, R.E. Jr., Szaro, B.G. and Lnenicka, G.A. (1998)Microinjection of mRNA encoding rat synapsin Ia alters synaptic physiology in identified motoneurons of the crayfish, Procambarus clarkii. J. Neurobiol. 37:224-236.
  • Zhao, Y. and Szaro, B.G. (1997) Xefiltin, a new low molecular weight neuronal intermediate filament protein of Xenopus laevis, shares sequence features with goldfish gefiltin and mammalian alpha-internexin and differs in expression from XNIF and NF-L. J. Comp. Neurol. 377:351-364.
  • Gervasi, C. and Szaro, B.G. (1997) Sequence and expression patterns of two forms of the middle molecular weight neurofilament protein (NF-M) of Xenopus laevis. Mol. Brain Res. 48:229-242.
  • Zhao, Y. and Szaro, B.G.(1997) Xefiltin, a Xenopus laevis neuronal intermediate filament protein, is expressed in actively growing optic axons during regeneration and development. J. Neurobiol. 33:811-824.
  • Lin, W. and Szaro, B.G. (1996) Effects of intermediate filament disruption on the early development of the peripheral nervous system of Xenopus laevis. Dev. Bio. 179:197-211.
  • Jian, X., Szaro, B.G. and Schmidt, J.T. (1996) Myosin light chain kinase: expression in neurons and upregulation during axon regeneration. J. Neurobiol. 31:379-391.
  • Zhao, Y. and Szaro, B.G. (1995) Pathway selection and target removal influence the neurofilament compositions of regenerating optic axons in Xenopus laevis. J. Neurosci. 15:4629-4640.
  • Gervasi, C. and Szaro, B.G. (1995) The Xenopus laevis homologue to the neuronal cyclin dependent kinase (cdk5) is expressed by gastrulation. Mol. Brain Res. 33:192-200
  • Lin, W. and Szaro, B.G. (1995) Neurofilaments help maintain normal morphologies and support elongation of neurites in Xenopus laevis cultured embryonic spinal cord neurons. J. Neurosci. 15:8331-8344.