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  • Hannes E. Buelow, Ph.D.

Hannes E. Buelow, Ph.D.

Hannes E. Buelow

Professor, Department of Genetics

Professor, Dominick P. Purpura Department of Neuroscience

Area of Research: Neural patterning with a focus on extracellular matrices using the nematode Caenorhabditis elegans; Glycosaminoglycans in development as well as health and disease.

Contact Information

718.430.3621718.430.8778hannes.buelow@einsteinmed.edu

Albert Einstein College of Medicine
Jack and Pearl Resnick Campus

1300 Morris Park Avenue
Ullmann Building, Room 709
Bronx, NY 10461

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Professional Interests

Development and function of the Nervous System

My lab uses the small nematode C. elegans with its simple and well characterized nervous system as a genetic model. We are trying to understand how growing axons and dendrites navigate the extracellular space to connect to their partners and be appropriately patterned. In addition, we are investigating how an animals experience affects connectivity, i.e. hardwiring of its nervous system. 

In one project we are studying the development of dendrites in polymodal multidendritic neurons of C. elegans. We are aiming to understand how the complex dendritic arbors that resemble menorah-like candelabras are patterned. Of particular interest are the mechanisms and molecules that promote or restrict the growth of dendrites both cell-autonomously and non-cell-autonomously. In a second project, we are investigating development and function of the connectome, i.e. the hardwiring of the nervous system. Specifically, we are interested in how an animal's experience can influence and change connectivity. To this end, we have developed methods to visualize cell-specific synaptic connections. We are now using a combination of genetic, behavioral, and imaging approaches to test how specific connections changes in response to the environment and which genes mediate these processes. In a final project, we are studying the role of proteoglycans, e.g. heparan sulfate (HS) proteoglycans in development an disease. We are asking how specific modification patterns of the polysaccharide HS determine the path of developing axons. For instance, we have shown that distinct modification patterns in HS serve specific and instructive functions during neural development leading us to formulate the ‘HS code’ hypothesis. We propose that defined combinations of modifications in the sugars of HS contain information and generate a molecular map that helps shape the nervous system. Our goal is to decipher the information contained in HS, determine the factors that create and modulate it and describe the genes that respond to it. We are also investigating a pathological dimension of HS by studying Kallmann Syndrome, a human genetic disease with specific neurological defects in which we have identified mutations in HS genes.

In summary, we are using genetic approaches coupled with biochemical and advanced imaging approaches to understand the function of genes involved in development, function, and disease of the nervous system.


Selected Publications

Rahman M., Ramirez-Suarez N.J., Diaz-Balzac C.A., and Bülow H.E. (2022) Specific N-glycan regulate an extracellular adhesion complex during somatosensory dendrite patterning, EMBO Reports, May 19,e5416310; https://doi.org/10.15252/embr.202154163.

Zhou X., Vachon C., Cizeron M., Romatif O., Bülow H.E., Jospin M., Bessereau J.L. (2021) The HSPG Syndecan is a core organizer of cholinergic synapses in C. elegans, J. Cell Biol., Sep 6;220(9), published online July 2, 2021 as https://doi.org/10.1083/jcb.202011144

Tang L.T.*, Trivedi M.*, Freund J., Salazar C.J., Lee G.L., Ramirez-Suarez N.J., Rahman M., Wang Y., Grant, B.D., Bülow H.E. (2021) The CATP-8/P5A-type ATPase is required for multiple aspects of neuronal patterning, PLoS Genetics, Jul 1;17(7):e1009475, published online July 1, 2021 as https://doi.org/10.1371/journal.pgen.1009475. PMCID: PMC8279360

Cizeron M., Granger L., Bülow H.E., Bessereau J.L. (2021) Specific heparan sulfate modifications stabilize the synaptic organizer MADD-4/Punctin at C. elegans neuromuscular junctions, GENETICS, published online May 13, 2021 as https://doi.org/10.1093/genetics/iyab073. PMCID: PMC8864735.

Cook S.J., Jarrell T.A., Britten C., Wang Y., Bloniarz A.E., Yakovlev M.A., Nguyen K.C.Q., Tang L.TZ., Bayer E.A., Duerr J.S., Bülow H.E., Hobert O., Hall D.H. & Emmons S.W. (2019) Whole-animal connectomes of both Caenorhabditis elegans sexes, Nature, 571(7763):63-71, published online on July 3, 2019 as https://doi.org/10.1038/s41586-019-1352-7.

Tang L.TH.*, Díaz-Balzac C.A.*, Rahman M., Ramirez-Suarez N.J., Salzberg Y., Lázaro-Peña M.I., and Bülow H.E. (2019) TIAM-1/GEF can shape somatosensory dendrites independently of its GEF activity by regulating F-actin localization. eLife; 8:e38949 DOI: 10.7554/eLife.38949.

Ramirez-Suarez N.J., Belalcazar H.M., Salazar C.J., Beyaz B., Raja B., Nguyen K.C.Q., Celestrin K., Fredens J., Færgeman N.J., Hall D.H., and Bülow H.E. (2019) Axon-dependent patterning and maintenance of somatosensory dendritic arbors, Dev. Cell, 48:229-244, pii: S1534-5807(18)31083-9. published online on January 17, 2019 as https://doi.org/10.1016/j.devcel.2018.12.015.

Celestrin K., Díaz-Balzac C.A., Tang L.TZ., Ackley B.D., and  Bülow H.E. (2018) Four specific Ig domains in UNC-52/Perlecan function with NID-1/Nidogen during dendrite morphogenesis in Caenorhabditis elegans. Development, 145(10):dev158881, published online on May 14, 2018 as https://doi.org/10.1242/dev.158881.

Townley, R.A., Bülow H.E. (2018) Deciphering functional glycosaminoglycan motifs in development. Curr. Op. in Struct. Biol, 50:144-514, published online on March 23, 2018 as https://doi.org/10.1016/j.sbi.2018.03.011.

Saied-Santiago K., Bülow H.E. (2018) Diverse Roles for Glycosaminoglycans in Neural Patterning. Dev. Dyn., 247(1):54-74, published online on Jul 24, 2017 as https://doi.org/10.1002/dvdy.24555. 

Lázaro-Peña M.I., Díaz-Balzac C.A., Bülow H.E., and Emmons S.W. (2018) Heparan sulfate molecules mediate synapse formation and function of male mating neural circuits in C. elegans. GENETICS, 209(1):195-208, published online on March 20, 2018 as https://doi.org/10.1534/genetics.118.300837.

Saied-Santiago K., Townley R.A., Attonito J., da Cunha D.S., Tecle E., and Bülow H.E. (2017) Coordination of heparan sulfate proteoglycans with Wnt signaling to control cellular migrations and positioning in Caenorhabditis elegans. GENETICS, 206(4):1951-1967, published online on June 2, 2017 as https://doi.org/10.1534/genetics.116.198739.

Salzberg Y., Coleman, A., Celestrin K., Biederer T., Henis-Korenblit* S., and Bülow* H.E. (2017) Reduced insulin/insulin-like growth factor receptor signaling mitigates defective dendrite morphogenesis in mutants of the ER stress sensor IRE-1. PLoS Genetics, 13(1):e1006579. published online on January 24, 2017 as https://doi.org/10.1371/journal.pgen.1006579. * corresponding authors.

Díaz-Balzac C.A., Rahman M., Lázaro-Peña M.I., Martin Hernandez L.A., Salzberg Y., Aguirre-Chen C., Kaprielian Z., and Bülow H.E. (2016) Muscle- and skin-derived cues jointly orchestrate patterning of somatosensory dendrites. Current Biology, 26:1-9, published online on July 21 as http://dx.doi.org/10.1016/j.cub.2016.07.008.

Attreed, M., Saied-Santiago, K., and Bülow H.E. (2016) Conservation of anatomically restricted glycosaminoglycan structures in divergent nematode species.  Glycobiology, 26(8):862-870, published online on April 8, 2016 as https://doi.org/10.1093/glycob/cww037.

Díaz-Balzac C.A., Lázaro-Peña M.I., Ramos-Ortiz G.O., Bülow H.E. (2015) The Adhesion molecule KAL-1/anosmin-1 regulates Neurite Branching through a SAX-7/L1CAM–EGL-15/FGFR Receptor Complex. Cell Reports, 11:1–8, published online on May 21 as http://dx.doi.org/10.1016/j.celrep.2015.04.057.

Desbois M., Cook S.J., Emmons, S.W., and Bülow H.E. (2015) Directional trans-synaptic labeling of specific synaptic connections in live animals. GENETICS, 200(3):697-705,  published online on April 27, 2015 as https://doi.org/10.1534/genetics.115.177006.

Dong X, Shen K*, and Bülow H.E.* (2015) Intrinsic and extrinsic mechanisms of dendrite morphogenesis. Annu. Rev. Physiol., 77:18.1–18.30, published onilne on October 24, 2014 as https://doi.org/10.1146/annurev-physiol-021014-071746.  * corresponding authors

Salzberg Y., Ramirez-Suarez N.J., Bülow H.E. (2014) The Proprotein Convertase KPC-1/Furin Controls Brnahcing and Self-avoidance of Sensory Dendrites of Caenorhabditis elegans. PLoS Genetics, 10(9):e1004657. published online on September 18, 2014 as https://doi.org/10.1371/journal.pgen.1004657.

Díaz-Balzac C.A., Lázaro-Peña M.I., Tecle E., Gomez N., and Bülow H.E. (2014) Complex cooperative functions of heparan sulfate proteoglycans shape nervous system development in C. elegans. G3 (Bethesda), 2014 Aug 5. pii: g3.114.012591. Published online as  https://doi.org/10.1534/g3.114.012591.

Salzberg Y., Diaz-Balzac C.A., Ramirez-Suarez N.J., Attreed M., Tecle E., Desbois M., Kaprielian Z., and Bülow H.E. (2013) Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell, 155(2): 308–320, published online on October 10 as https://doi.org/10.1371/journal.pgen.1004657.

Tecle E., Diaz-Balzac C.A., and Bülow H.E. (2013) Distinct 3-O-sulfated heparan sulfate modification patterns are required for kal-1 dependent neurite branching in a context-dependent manner in Caenorhabditis elegans. G3 (Bethesda), 3(3):541-52. https://doi.org/10.1534/g3.112.005199.

Attreed M., Desbois M., van Kuppevelt T.H., and Bülow, H.E. (2012) Direct visualization of specifically modified extracellular glycans in living animals. Nat. Methods, 9(5):477-479, published online April 1, 2012 as https://doi.org/10.1038/nmeth.1945.

Tornberg J., Sykiotis G.P., Keefe K., Plummer L., Hoang X, Hall J.E., Quinton R., Seminara S.B., Hughes V., Van Vliet G., Van Uum S., Crowley, Jr W.F., Habuchi H., Kimata K., Pitteloud N.*, Bülow, H.E.* (2011) Heparan sulfate 6-O-sulfotransferase 1, a gene involved in extracellular sugar modifications, is mutated in patients with idiopathic hypogonadotrophic hypogonadism. Proc Natl Acad Sci USA, 108(28):11524-11529, published online June 23, 2011 as https://doi.org/10.1073/pnas.1102284108. * contributed equally.

Townley R.A., and Bülow, H.E. (2011) Genetic Analysis of the Heparan modification network in Caenorhabditis elegans. J. Biol. Chem., 286:16824-16831, published March 24, 2011 as https://doi.org/10.1074/jbc.M111.227926.

Aguirre-Chen C., Bülow, H.E., and Kaprelian Z. (2011), C. elegans bicd-1, Homolog of the Drosophila Dynein Accessory Factor, Bicaudal D, Regulates the Branching of PVD Multidendritic Nociceptors. Development, 138:507-518. Published online as https://doi.org/10.1242/dev.060939.

Bhattacharya R., Townley, R.A., Berry K.L., and Bülow, H.E. (2009) The PAPS transporter pst-1/let-462 is required for heparan sulfation and is essential for viability and neural development. J Cell Science, 122:4492-4504. Published online on November 17, 2009 as https://doi.org/10.1242/jcs.050732.

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