Aaron Neiman, Ph.D.

Professor

Department of Biochemistry and Cell Biology

Office: Life Sciences Building Room 332

In response to starvation, diploid cells of the baker’s yeast Saccharomyces cerevisiae differentiate into haploid spores. The process of spore formation involves a form of cell division in which the four daughter nuclei produced by meiosis are encapsulated within newly formed plasma membranes termed prospore membranes. Subsequent to the closure of the prospore membrane, a complex coat called a spore wall is formed around each spore, which provides the spore with resistance to environmental stresses. Our lab is studying the molecular mechanisms underlying both the formation and growth of the prospore membrane as well as the assembly of the spore wall. These studies take us into a variety of areas of cell biology including vesicle trafficking, membrane fusion, cytokinesis, signal transduction, and extracellular matrix assembly.

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Stages of spore formation: Blue indicates the plasma membrane, red the nuclear envelope, and green the prospore membrane. The black “T”s on the periphery of the nucleus indicate the spindle poles and the thick gray represents the spore wall.

Park, J. S., Nguyen, H., Cheng, M. H., Bahar, I., and Neiman, A. M. (2025). Hinge sites in the lipid transfer channel modulate function of the yeast bridge-like transfer protein Vps13. GENETICS 12:iyaf267.

Suda, Y. and Neiman, A. M. (2025). The Predicted Structure of S. cerevisiae Ssp1 Reveals Parallel Evolution in the Pil1 BAR Domain Family Proteins of Ascomycetes. Journal of Fungi 11:661.

Weng, Q., Wan. L., Straker, G. C., Deegan, T. D., Duncker, B. P., Neiman, A. M., Luk, E., and Hollingsworth, N. M. (2024). An acidic loop in the FHA domain of the yeast meiosis-specific kinase Mek1 interacts with a specific motif in a subset of Mek1 substrates. GENETICS 9:iyae106.

Nunez, G., Zhang, K., Mogbheli, K., Hollingsworth, N. M., and Neiman, A. M. (2023). Recruitment of the lipid kinase Mss4 to the meiotic spindle pole promotes prospore membrane formation in Saccharomyces cerevisiae. Mol Biol Cell. 34(4):ar33

Park, J. S., Hu, Y., Hollingsworth, N. M., Miltenberger-Miltenyi, G., and Neiman, A. M. (2022). Interaction between VPS13A and the XK scramblase is important for VPS13A function in humans. J Cell Sci. 135(17):jcs260227

Park, J. S., Hollingsworth, N. M., and Neiman, A. M. (2021). Genetic dissection of Vps13 regulation in yeast using disease mutations from human orthologs. Int. J. Mol Sci. 22:6200

Nakamura, T. S., Suda, Y. Muneshige, K., Fujieda, Y. Okumura, Y., Inoue, I., Tanaka, T., Takahashi, T., Nakanishi, H., Gao, X-D., Okada, Y, Neiman, A. M., and Tachikawa, H. (2021) Suppression of Vps13 adaptor protein mutants reveals a role for PI4P in regulating Vps13 function. PLoS Genetics, 17:e1009727.

Bemena, L.D., Min, K., Konopka, J. B., and Neiman, A. M. (2021). A Conserved Machinery Underlies the Synthesis of a Chitosan Layer in the Candida Chlamydospore Cell Wall. mSphere 6:e00080-21.

Chrissian, C., Lin, C. P., Camacho, E., Casadevall, A., Neiman, A. M., and Stark, R. E. (2020). Unconventional constituents and shared molecular architecture of the melanized wall of C. neoformans and the spore wall of S. cerevisiae. J Fungi 6:329.

Park, J.-S. and Neiman, A. M. (2020). XK is a partner for VPS13A: a molecular link between chorea acanthocytosis and McLeod Syndrome. Mol. Biol Cell 31: 2425-2436.

Paulissen, S. M., Hunt, C. A., Seitz, B. C., Slubowski, C. J., Yu, Y., Mucelli, X., Truong, D., Wallis, Z., Nguyen, H.T., Newman-Toledo, S.,Neiman, A.M., and Huang, L. S. (2020). A Non-canonical Hippo pathway regulates spindle disassembly and cytokinesis during meiosis in Saccharomyces cerevisiae. GENETICS 216:447-462.

Zhou, S., Sternglanz, R., and Neiman, A. M. (2017). Developmentally regulated internal transcription initiation during meiosis in budding yeast. PLoS One, 12(11): e0188001.

Omerza, G., Tio, C.-W., Philips, T., Diamond, A., Neiman, A. M., and Winter, E. (2017). The meiosis-specific Cdc20 family member Ama1 promotes binding of the Ssp2 activator to the Smk1 MAP kinase. Mol Biol Cell. 29:66-74.

Nakamura, T. S., Numajiri, Y., Okumura, Y., Hidaka, J., Tanaka, T., Inoue, I., Suda, Y., Takahashi,T., Nakanishi, H., Gao, X.-D., Neiman, A. M., and Tachikawa, H. (2017). Dynamic localization of a yeast development-specific PP1 complex during prospore membrane formation is dependent on multiple localization signals and complex formation. Mol. Biol. Cell, 28:3881-3895.

Zhang, K., Needleman, L., Zhou, S., and Neiman, A. M. (2017). A novel assay reveals a maturation process during ascospore wall formation. J Fungi, 3(4), 54.

Hoffman, R. Grabinska, K., Qian, Z., Sessa, W., and Neiman, A. M. (2017). Long-chain polyprenols promote spore wall formation in Saccharomyces cerevisiae. GENETICS, 207:1371-1386.

Bemena, L. D., Mukama, O., Neiman, A. M., Li, Z., Gao, X. D., and Nakanishi, H. (2017). In vitro reconstitution of the yeast spore wall dityrosine layer discloses the mechanism of its assembly. J Biol Chem. 292:15880-15891.

Jin, L., Zhang, K., Sternglanz, R., and Neiman, A. M. (2017). Predicted RNA binding proteins Pes4 and Mip6 regulate mRNA levels, translation, and localization during sporulation in budding yeast. Mol Cell Biol. 37:e00408-00416.

Ta-Shma, A., Zhang, K., Salimova, E., Zernecke, A., Sieiro-Mosti, D., Stegner, D., Furtado, M., Shaag, A., Perles, Z., Nieswandt, B., Rein, A. J., Rosenthal, N., Neiman, A. M., and Elpeleg, O. (2017). Congenital valvular defects associated with deleterious mutations in the PLD1 gene. J Med Genet. 54:278-286.

Callender, T.L., Laureau, R., Wan, L., Chen, X., Sandhu, R., Laljee, S., Zhou, S., Suhandynata, R. T., Prugar, E., Gaines, W. A., Kwon, Y., Börner, G. V., Nicolas, A.,Neiman, A. M., and Hollingsworth, N. M. (2016). Mek1 down regulates Rad51 activity during yeast meiosis by phosphorylation of Hed1. PLoS Gen. 12:e1006226

Okada, H., Kono, K., Neiman, A. M., and Ohya, Y. (2016). Examination and disruption of the yeast cell wall. Cold Spring Harb Protoc.

Okada, H. Neiman, A. M., and Ohya, Y. (2016). Assay for spore wall integrity using a yeast predator. Cold Spring Harb Protoc.

Park, J. S., Thorsness, M. K., Policastro, R., McGoldrick L. L., Hollingsworth, N. M., Thorsness, P. E.,and Neiman, A. M. (2016) Yeast Vps13 promotes mitochondrial function and is localized at membrane contact sites. Mol. Biol. Cell 27:2435-2449.

Jin, L., Zhang, K., Xu, Y., Sternglanz, R., and Neiman, A.M. (2015). Sequestration of mRNAs modulates the timing of translation during meiosis in budding yeast. Mol Cell Biol. 35:3448-3458.

Park, J.-S., Halegoua, S., Kishida, S., and Neiman, A. M. (2015). A conserved function in phosphatidylinositol metabolism for mammalian Vps13 family proteins. PLoS One, 10:e0124836

Ucisik-Akkaya, E., Leatherwood, J. K., and Neiman, A. M. (2014). A genome wide screen for sporulation-defective mutants in Schizosaccharomyces pombe G3 4:1173-1182

Ren, J., Lin, P.-C., Pathak, M. C., Temple, B. R., Nile, A. H., Mousley, C. J., Duncan, M. C., Eckert, D. M., Leiker, T. J., Ivanova, P. T., Myers, D. S., Murphy, R. C., Brown, H. A., Versaasdonk, J., Bloom, K. S., Ortlund, E. A., Neiman, A. M., and Bankaitis, V. A. (2014). A phosphatidylinositol transfer protein integrates phosphoinositide signaling with lipid droplet metabolism to regulate a developmental program of nutrient stress-induced membrane biogenesis. Mol Biol Cell 25:712-727

Lam, C., Santore, E., Lavoie, E., Needleman, L., Fiacco, N., Kim, C., and Neiman, A. M. (2014). A visual screen of protein localization during sporulation identifies new components of prospore membrane-associated complexes in budding yeast. Euk. Cell 13:383-391.

Park, J.-S., Okumura, Y., Tachikawa, H., and Neiman, A. M. (2013). SPO71 encodes a developmental stage-specific partner for Vps13 in Saccharomyces cerevisiae. Euk Cell. 2:1530-1537.

Lin, C. P., Kim, C., Smith, S. O., and Neiman, A. M. (2013). A Highly Redundant Gene Network Controls Assembly of the Outer Spore Wall in S. cerevisiae. PLoS Gen. 9:e1003700

Park, J.-S. and Neiman, A. M. (2012). VPS13 Regulates Membrane Morphogenesis During Sporulation in Saccharomyces cerevisiae. J Cell Sci. 125:3004-3011.

Halada, G., Jha, P., Nelson, K. Zhao, W., Korach, C. S., Neiman, A. Lee, S.-J., and Mintzer, E. (2010). Formation and characterization of chitosan-based coatings on stainless steel. in Biomaterials, American Chemical Society pp 159-171.

Yu, Y., Neiman, A. M., and Sternglanz, R. (2010). The JmjC domain of Gis1 is dispensable for transcriptional activation. FEMS Yeast Res. 10:793-801.

Mathieson, E. M., Suda, Y ., Nickas, M., Snydsman, B., Davis, T. N., Muller, E. G., and Neiman, A. M. (2010). Vesicle docking to the spindle pole body is necessary to recruit the exocyst during membrane formation in Saccharomyces cerevisiae. Mol. Biol. Cell. 21:3693-3707

Mathieson, E. M,, Schwartz, C,, and Neiman, A. M. (2010). Membrane assembly modulates the stability of the meiotic spindle pole body. J Cell Sci 123:2481-2490.

Nelson, J., Huang, X., Steinbrener, J., Shapiro, D., Kirz, J., Marchesini, S., Neiman, A. M., Turner, J. J., and Jacobsen, C. (2010). High-resolution x-ray diffraction microcopy of specifically labeled yeast cells. Proc. Natl. Acad. Sci. USA 107:7235-7239.

Yang, H.-J. and Neiman , A. M. (2010). A guanine nucleotide exchange factor is a component of the meiotic spindle pole body in Schizosaccharomyces pombe. Mol Biol Cell. 12:1272-1281.

Huang, X., Nelson, J., Kirz, J., Lima, E., Marchesini, S., Miao, H., Neiman, A. M., Shapiro, D., Steinbrener, J., Stewart, A., Turner, J. J., and Jacobsen, C. (2009). Soft X-ray diffraction microscopy of a frozen hydrated yeast cell. Phys. Rev. Lett. 103:19801.

Suda, Y. S., Rodriguez, R. K., Coluccio, A. E., and Neiman, A. M. (2009). A screen for spore wall permeability mutants identifies a secreted protease required for proper spore wall assembly. PLoS One 4:e7184.

Butler, G., et al. (2009). Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459:657-662.

Ishihara, M., Suda ,Y., Inoue, I., Tanaka, T., Takahashi, T., Gao, X. D., Fukui, Y., Ihara, S., Neiman, A.M., and Tachikawa, H. (2009). A protein phosphatase I-interacting protein Ysw1 is involved in proper septin organization and prospore membrane formation during sporulation. Eukaryot Cell. 2009 8:1027-1037

Lisa-Santamaria, P., Neiman, A. M., Cuesta-Marban, A., Mollinedo, F., Revuelta, J. L., and Jimenez, A. (2009). Human initiator caspases trigger apoptotic and autophagic phenotypes in Saccharomyces cerevisiae. Biochim. Biophys. Acta 1793:561-571

Diamond, A. E., Park, J. S., Inoue, I., Tachikawa, H., and Neiman, A. M. (2009). The anaphase promoting complex subunit Ama1 links meiotic exit to cytokinesis during sporulation in Saccharomyces cerevisiae. Mol. Biol. Cell. 20:134-145.

Yang, H.-J., Nakanishi, H., Liu, S., McNew, J. A. and Neiman, A. M. (2008). Binding interactions control SNARE specificity in vivo. J. Cell Biol. 183: 1089-1100.

Elias, E. V., Quiroga, R., Gottig, N., Nakanishi, H., Nash, T. E., Neiman, A., and Lujan, H. D. (2008). Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J. Biol. Chem 283: 35996-36010.

Pablo-Hernando, M. E., Arnaiz-Pita, Y., Tachikawa, H., Del Rey, F., Neiman, A. M., Vazquez de Aldana, C. R. (2008). Septins localize to microtubules during nutritional limitation in Saccharomyces cerevisiae. BMC Cell Biol. 9:55

Coluccio, A. E., Rodriguez, R. K., Kernan, M. J., and Neiman, A. M. (2008). The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS One 3:e2873.

Yan, H., Ge, W., Chew, T. G., Chow, J. Y., McCollum D., Neiman A. M., and Balasubramanian, M. K. (2008) The meiosis-specific Sid2p-elated protein Slk1p regulates forespore membrane assembly in fission yeast. Mol Biol Cell. 19:3676-3690.

Suda, Y., Nakanishi, H., Mathieson, E. M., and Neiman, A. M. (2007). Alternative modes of organellar segregation during sporulation in Saccharomyces cerevisiae. Euk. Cell :2009-2017

Liu, S., Wilson, K. A., Rice-Stitt, T., Neiman, A. M., and McNew, J. A. (2007). In vitro fusion catalyzed by the sporulation-specific t-SNARE light chain Spo20p is stimulated by phosphatidic acid. Traffic :1630-1643.

Pablo-Hernando, M. E., Arnaiz-Pita, Y., Nakanishi, H., Dawson, D., del Rey, F., Neiman A. M., and Vazquez de Aldana, C. R. (2007). Cdc15 is required for spore morphogenesis independently of Cdc14 in Saccharomyces cerevisiae. Genetics 177:281-293.

Zeniou-Meyer M., Zabari, N. Ashery, U., Chasserot-Golaz, S., Haeberle, A. M., Demais, V., Bailly, Y., Gottfried, E., Nakanishi, H., Neiman, A. M., Du, G., Frohman, M. A., Bader, M. F., and Vitale, N. (2007) Phospholipase D1 production of phosphatidic acid at the plasma membrane promotes exocytosis of large dense-core granules at a late stage. J. Biol. Chem. 282:21746-21757.

Nakanishi, Y., Suda, Y., and Neiman, A. M. (2007). Erv14 family cargo receptors are necessary for ER exit during sporulation in Saccharomyces cerevisiae. J. Cell Sci. 120:908-916.

Ragni, E. Coluccio, A., Rolli, E., Rodriguez-Pena, J. M. Colasante, G., Arroyo, J., Neiman A. M., and Popolo, L. (2007). GAS2 and GAS4, a pair of developmentally regulated genes required for spore wall assembly in Saccharomyces cerevisiae. Euk. Cell 6:302-316.

Nakanishi, H., Morishita, M., Schwartz, C. L., Coluccio, A., Engebrecht, J., and Neiman, A. M. (2006). Phospholipase D and the SNARE Sso1p are necessary for vesicle fusion during sporulation in yeast. J Cell Sci. 119:1406-1415.

Shapiro, D., Thibault, P., Beetz, T., Elser, V., Howells, M., Jacobsen, C., Kirz, J., Lima, E., Miao, H., Neiman, A. M., Sayre, D. (2005) Biological imaging by soft x-ray diffraction microscopy. Proc. Natl. Acad. Sci. USA. 102:15343-15346.

Winters, M. J., Lamson, R. E., Nakanishi, H., Neiman, A. M., Pryciak, P. M. (2005) A membrane binding domain in the Ste5 scaffold synergizes with Gbg binding to control localization and signaling in pheromone response. Mol. Cell. 20:21-32.

Coluccio, A. Bogengruber, E., Conrad, M. N., Dresser, M., Briza, P., and Neiman A. M. (2004). A morphogenetic pathway of spore wall formation in Saccharomyces cerevisiae. Euk. Cell, 6:1464-1475

Coluccio, A. and Neiman, A. M. (2004) Interspore bridges: a new feature of the S. cerevisiae spore wall. Microbiology, 150:3189-3196.

Nickas, M.E., Diamond, A., Yang, M.-J., and Neiman, A. M. (2004). Regulation of Spindle Pole Body function by an intermediary metabolite. Mol. Biol. Cell, 15:2606-2616.

Nakanishi, H., de Los Santos, P., and Neiman, A. M. (2004). Positive and negative regulation of a SNARE protein by control of intracellular localization. Mol Biol Cell. 15:1802-1815.

Coluccio, A., Malzone, M. and Neiman A. M. (2004). Genetic evidence of a role for membrane lipid composition in the regulation of SNARE function. Genetics, 166:89-97.

Nickas, M. E., Schwartz, C., and Neiman, A. M. (2003) Ady4p and Spo74p are components of the meiotic Spindle Pole Body that promote growth of the prospore membrane in Saccharomyces cerevisiae. Euk. Cell 2:431-445.

Nickas, M. E., and Neiman, A. M. (2002) Ady3p links Spindle Pole function to spore wall synthesis in Saccharomyces cerevisiae. Genetics, 160: 1439-1450.

Tachikawa, H., Bloecher, A., Tatchell, K., and Neiman, A. M. (2001) A Gip1p-Glc7p phosphatase complex regulates septin organization and spore wall formation. J. Cell Biol. 155:797-808.

Bajgier, B. K., Malzone, M., Nickas, M. and Neiman, A. M. (2001). SPO21 is required for meiosis-specific modification of the spindle pole body in yeast. Mol. Biol. Cell. 12: 1611-1621.