Selected Publications

EXTRACELLULAR RECORDING OF ELECTRICAL ACTIVITY IN THE INTACT ADRENAL MEDULLA IN LIVING ANIMALS

Lopez Ruiz, J.R., S.A. Ernst, R.W. Holz, and E.L. Stuenkel. 2022. Basal and Stress-Induce Network Activity in the Adrenal Medulla In Vivo. Front Endocrinol (Lausanne). 13:875865. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9250985/pdf/fendo-13-875865.pdf

EXOCYTOSIS STUDIED BY TOTAL INTERNAL REFLECTION AND OTHER OPTICAL TECHNIQUES

Wick, P. F., Trenkle, J. M., and Holz, R.W. (1997) Punctate appearance of dopamine-b-hydroxylase on the chromaffin cell surface reflects the fusion of individual chromaffin granules upon exocytosis. Neuroscience 80: 847-860. Download

Johns, L.M., Levitan, E.S., Shelden, E.A. Holz, R.W. and Axelrod, D. (2001) Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J. Cell Biol. 153: 177-190. (TIRFM) Download

Allersma, M.W., Wang, L., Axelrod, D. and Holz, R.W. (2004) Visualization of regulated exocytosis with a granule-membrane probe using total internal reflection microscopy. Mol.Biol.Cell, 15:4658-4668 Download

Allersma, M.W., Bittner, M.A., Axelrod, D., and Holz, R.W. (2006) Motion matters: Secretory granule motion adjacent to the plasma membrane and exocytosis. Mol.Biol.Cell 17:2424-2438. Download

Degtyar, V.E., Allersma, M.W., Axelrod, D., and Holz, R.W. (2007) Increased motion and travel, rather than stable docking, characterize the last moments before secretory granule fusion. Proc.Natl.Acad.Sci (USA) 104:15929-15934.Download

Holz, R.W. and Axelrod, D. (2008) Secretory granule behaviour adjacent to the plasma membrane before and during exocytosis: total internal reflection fluorescence microscopy studies. Acta Physiol. 192:303-307.Download

Wang,L., Bittner, M.A., Axelrod,D., Holz.R.W. (2008) The structural and functional implications of linked SNARE motifs in SNAP25. Mol.Biol.Cell 19:3944-3455.Download

Anantharam,A., Onoa,B.,Edwards,R.H., Holz,R.W. & Axelrod,D. (2010) Localized topological changes of the plasma membrane upon exocytosis visualized by polarized TIRFM. J.Cell Biol. 188:415-428.Download

Anantharam,A. Axelrod, D. Holz,R.W. (2010) Polarized TIRFM reveals changes in plasma membrane topology before and during granule fusion, Cell Mol. Neurobiol. DOI 10.1007/s10571-010-9590-0 . Download

Anantharam,A., Bittner,M.A., Aikamin, R.L.,Stuenkel,E.L.,Schmid,S.L.,Axelrod,D., and Holz,R.W. (2011) A new role for the dynamin GTPase in regulation of fusion pore expansion. Mol.Biol.Cell 22:1907-1918. PMCID: PMC3103406. Download

Bittner,M.A., Aikman, R.L., Holz,R.W. (2013) A nibbling mechanism for clathrin-mediated retrieval of secretory granule membrane after exocytosis. J.Biol.Chem.288: 9177-9188. PMCID:PMC3610990 Download

Weiss, A.N., Bittner, M.A., Holz, R.W., Axelrod, D. (2014) Protein mobility within secretory granules. Biophys.J. 107: 16-25. http://www.ncbi.nlm.nih.gov/pubmed/24988337 . PMC 4478961 Download

Weiss, A.N, Anantharam, A., Bittner, M.A., Axelrod, D., Holz, R.W. (2014) Lumenal protein within secretory granules affects fusion pore expansion. Biophys.J. 107:26-33. http://www.ncbi.nlm.nih.gov/pubmed/24988338.Download

Zimmerberg J, Blank PS. It's what's inside that matters. Biophys J. 2014;107(1):5-7. (Commentary on Weiss 2014 papers) http://www.ncbi.nlm.nih.gov/pubmed/24988334 Download

Bohannon KP, Bittner MA, Lawrence DA, Axelrod D, Holz RW. Slow fusion pore expansion creates a unique reaction chamber for co-packaged cargo. J Gen Physiol. 2017:149:921-934.PMC5694939 Download [See commentary "Chemistry in a vesicle" by Meyer B. Jackson Download]

Bohannon KP, Holz RW, Axelrod D. Refractive index imaging of cells with variable-angle near TIR microscopy. Microscopy and Microanalysis. 2017, 23:978-988 Download.

Abbineni, P.S., Axelrod, D., Holz, R.W. (2018) Visualization of expanding fusion pores in secretory cells. J. Gen. Physiol. 150:1640-1646. http://jgp.rupress.org/content/jgp/150/12/1640.full.pdfPMC6279363 Download

Abbineni, P.S., Bittner, M.A., Axelrod, D., Holz, R.W. (2018) Chromograinin A, the major lumenal protein in chromaffin granules, control fusion pore expansion. J. Gen. Physiol. 150: 118-130. https://doi.org/10.1085/jgp.201812182, PMID: 30504267 Download

Abbineni, P.S., Bohannon, K.P., Bittner, M.A., Axelrod, D., Holz, R.W.(2019) Identification of β-synuclein on secretory granules in chromaffin cells and the effects of α- and β-synuclein on post-fusion BDNF discharge and fusion pore expansion. Neuroscience Lettr. 699:134-139. https://www.sciencedirect.com/science/article/pii/S0304394019300746. PMID: 30711526 Download

Abbineni, P.S., Briguglio, J.S., Chapman. E.R., Holz, R.W., Axelrod, D. (2022) VAMP2 and synaptotagmin mobility in chromaffin granule membranes: implications for regulated exocytosis. Mol. Biol. Cell. DOI: 10.1091/mbc.E21-10-0494, https://www.ncbi.nlm.nih.gov/pubmed/34851717 , PMCID: PMC9265163

PIP2 AND EXOCYTOSIS

Eberhard, D. A., Cooper, C. L., Low, M. G. and Holz, R. W. (1990) Evidence that the inositol phospholipids are necessary for exocytosis: Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP. Biochem. J. 268:15-25. Download

Holz, R. W., Hlubek, M. D., Sorenson, S. D., Fisher, S. K., Balla ,T. , Shoichiro Ozaki, S., Prestwich, G. D., Edward L. Stuenkel, E. L. , and Bittner , M. A. (2000) A pleckstrin homology domain specific for PtdIns-4-5-P2 and fused to green fluorescent protein identifies plasma membrane PtdIns-4-5-P2 as being important in exocytosis. J. Biol. Chem. 275: 17878-17885. Download

Micheva, K.D., Holz, R.W. and Smith, S. J. (2001) Regulation of presynaptic phosphatidylinositol 4,5-bisphosphate by neuronal activity. J. Cell Biol. 154: 355-368. Download

Micheva, K., Buchanan, J., Holz, R.W. and Smith, S. J. (2003) Evidence for retrograde regulation of synaptic vesicle endocytosis and recycling. Nature Neurosci. 6:925-932. Download

Bittner, M.A. and Holz, R.W. (2005) Phosphatidylinositol-4,5-bisphosphate: Actin dynamics and the regulation of ATP-dependent and -independent secretion. Molecular Pharm. 67:1089-1098.. Download

SECRETION KINETICS AND ATP

Holz, R. W., Bittner, M. A., Peppers, S. C., Senter, R. A. and Eberhard, D. A. (1989) MgATP-independent and MgATP-dependent exocytosis: evidence that MgATP primes adrenal chromaffin cells to undergo exocytosis. J. Biol. Chem. 264: 5412-5419. Download

Bittner, M. A. and Holz, R.W. (1992) Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components. J. Biol. Chem. 267:16219-16225 Download

Bittner, M. A. and Holz, R.W. (1992) A temperature-sensitive step in exocytosis. J. Biol. Chem. 267:16226-16229 Download

RAB3A, RABPHILIN3 & RIM

Holz, R.W., Brondyk, W.H., Senter, R. A., Kuizon, L. and Marcara, I. G. (1994) Evidence for the involvement of Rab3a in Ca-dependent exocytosis from adrenal chromaffin cells. J.Biol. Chem. 269:10229-102234. Download

Holz, R.W. (1995). Transient expression of GTPase in non-dividing cells. Small GTPases and their regulators: proteins involved in transport. Ed. W.E. Balch in Methods of Enzymology. 257:221-231.

Darchen, F., Senyshyn, J., Brondyk, W.H., Taatjes, D. J., Holz, R.W., Henry, J.-P., Denizot, J.-P., Macara, I.G. (1995) The GTPase rab3a is associated with large dense core vesicles in bovine chromaffin cells and rat PC12 cells. J. Cell Sci. 108:1639-1649. Download

Chung, S.-H., Takai, Y., and Holz, R.W. (1995) Evidence that the Rab3a-binding protein, Rabphlin3a, enhances regulated secretion: Studies in adrenal chromaffin cells. J. Biol. Chem. 270: 16714-16718.Download

Chung, S.-H., Stabila,P., Macara, I.G., and Holz, R. W. (1997) The importance of the Rab3a-GTP binding domain for the intracellular stability and function of Rabphilin3a in secretion. J. Neurochem. 69: 164-173.

Chung, S.-H., Song, W.-J., Kim, K., Bednarski, J. J., Chen, J., Prestwich, G. D., and Holz, R. W. (1998) The C2 domains of Rabphilin3a specifically bind PtdIns(4,5)P2-containing vesicles in a Ca2+-dependent manner: characteristics and possible physiological significance. J. Biol. Chem. 273: 10240-10248.Download

Chung, S.-H., Joberty, G., Gelino, E. A., Macara, I. G. and Holz R. W. (1999) Comparison of the effects on secretion in chromaffin and PC12 cells of Rab3 family members and mutants: evidence that inhibitory effects are independent of direct interaction with Rabphilin3. J. Biol. Chem. 274: 18113-18120. Download

Sun, L., Bittner, M. A. and Holz, R. W. (2001). Rab3a-binding and secretion-enhancing domains in Rim1 are separate and unique: studies in adrenal chromaffin cells. J. Biol. Chem. 276: 12911-12917. Download

Sun, L., Bittner, M.A., and Holz, R.W. (2003) Rim, a component of the presynaptic active zone and modulator of exocytosis, binds 14-3-3 through its N-terminus. J. Biol. Chem. 278: 38301-38309 Download

LATROTOXIN AND LATROTOXIN RECEPTORS

Krasnoperov, V. G., Bittner, M.A., Beavis, R., Kuang, Y., Salnikow, K.V., Chepurny, O. G., Little, A.R., Plotnikov,A.N., Wu, D., Holz, R.W. and Petrenko, A. G. (1997) a-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18: 25-937. Download

Bittner, M.A., Krasnoperov, V.G., Stuenkel, E. L., Petrenko, A.G., and Holz, R.W. (1998) CIRL, a Ca2+-independent receptor for a-latrotoxin, mediates effects on secretion through multiple mechanisms. J. Neuroscience 18: 2914-2922. Download

Krasnoperov, V., Bittner, M. A., Holz, R.W,, Oleg Chepurny, O., and Petrenko, A. G. (1999) Structural requirements for a-Latrotoxin binding and a-latrotoxin-stimulated secretion. J. Biol. Chem. 274: 3590-3596. Downlaod

Ichtchenko, I., Bittner, M. A., Krasnoperov,V., Little, A.R., Chepurny, O., Holz, R.W., and Petrenko, A.G. (1999) A novel ubiquitously expressed a-latrotoxin receptor is a member of the CIRL family of G protein-coupled receptors. J. Biol. Chem. 274: 5491-5498.

Hlubek, M. D., Stuenkel, E. L., Krasnoperov, V. G., Petrenko, A. G., and Holz, R. W. (2000) Calcium-independent receptor for a-Latrotoxin and neurexin 1a facilitate toxin-induced channel formation: evidence that channel formation results from tethering of toxin to membrane. Mol. Pharm. 57: 519-528. Download

Bittner, M. A. and Holz, R. W. (2000) Latrotoxin stimulates secretion in permeabilized cells by regulating an intracellular Ca2+- and ATP-dependent event: a role for protein kinase C. J. Biol. Chem. 275: 25351-25357.