Department of Biological Sciences
University of Cincinnati
PO Box 210006
Cincinnati, OH 45221-0006
614 Rieveschl Hall
Phone: (513) 556-9700
Fax: (513) 556-5299
Daniel R Buchholz
Title: Associate Professor
Office: 711A Rieveschl Hall
Research Topics: Role of hormones in development and evolution, frog metamorphosis, comparative endocrinology
- Ph.D., University of California at Berkeley, Berkeley, CA, 1999 (Integrative Biology).
- M.A., University of California at Berkeley, Berkeley, CA, 1995 (Immunology, Molecular and Cellular Biology).
- B.A., Reed College, 1992 (Biology).
The central goal in my lab is to understand the role of hormones in development and evolution. Hormones play critical roles in nearly all developmental events, including the development of many diseases. In addition, evolutionary changes in hormonal control of development underlie morpho-logical, physiological, and behavioral differences between species. Understanding hormonal regulation of development will illuminate avenues for disease treatment and will provide a basis for explaining species differences and biodiversity.
We use frogs as a model system to gain basic knowledge about hormonal control of development. Frog development is ideal for our studies because the tadpole is usually free living and because the dramatic morphological and physiological events of metamorphosis are completely dependent on hormones. To study how hormones affect development, we use the African clawed frog which is the model frog used in developmental studies. These animals are easy to maintain in the laboratory, and valuable molecular and genomic tools are available. To examine the evolution of hormonal control of development, we use a variety of frog species, which have unusual tadpoles, including carnivorous tadpoles and direct developers. We manipulate development of the frog larvae by transgenic and gene knockout techniques and/or by using hormones treatments. These manipulations are followed by examination of gross morphology, histology, and gene expression including next generation sequencing.
Peer Reviewed Publications
- Choi, J., Ishizuya-Oka, A., Buchholz, D.R. (2017) Growth, development, and intestinal remodeling occurs in the absence of thyroid hormone receptor alpha in tadpoles of Xenopus tropicalis. Endocrinol. 158:1623-1633.
- Shewade, L. Schneider, K., Brown, A., Buchholz, D.R. (2017) In-vivo regulation of Krüppel-like factor 9 by corticosteroids and their receptors across tissues in tadpoles of Xenopus tropicalis. Gen. Comp. Endocrinol. 248:79–86.[Link]
- Patmann, M.D., Shewade, L.H., Schneider, K.A., Buchholz, D.R. (2017) Xenopus Tadpole Tissue Harvest. Cold Spring Harb Protoc.
- Kulkarni, S.S., Gomez-Mestre, I. Denver, R.J. Buchholz, D.R. (2017) Genetic accommodation of the larval period via modified endocrine signalling explains phenotypic divergence among spadefoot toad species. Nature Comm. 8:993.
- Choi, J., Suzuki, K.T., Sakuma, T., Shewade, L., Yamamoto, T., and Buchholz, D.R. (2015) Unliganded thyroid hormone receptor a regulates developmental timing via gene repression in Xenopus tropicalis. Endocrinology 156:735–744.[Link]
- Burraco, P., Arribas, R., Kulkarni, S.S., Buchholz, D.R., Gomez-Mestre, I. (2015) Comparing techniques for measuring corticosterone in tadpoles. Current Zoology (61 (5): 835–845).[Link]
- Choi, J., Moskalik, C., Ng, A., Matter, S.F., Buchholz, D.R. (2015) Regulation of thyroid hormone-induced development in vivo by thyroid hormone transporters and cytosolic binding proteins. Gen. Comp. Endocrinol. (222:69–80).[Link]
- Haas, A., Pohlmeyer, J., McLeod, D.S., Kleinteich, T., Hertwig, S.T., Das, I., Buchholz, D.R. (2014) Extreme tadpoles II: The highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole. Zoomorphology 133:321–342.[Link]
- Gomez-Mestre, I. Kulkarni, S., Buchholz, D.R. (2013) Mechanisms and Consequences of Developmental Acceleration in Tadpoles Responding to Pond Drying. PLoS One 8: e84266.[Link]
- Kerney, R.R., Brittain, A.L. Hall, B.K., Buchholz, D.R. (2012) Cartilage on the move: Cartilage lineage tracing during tadpole metamorphosis. Dev. Growth, Differentiation 54:739-752.[Link]
- Kulkarni, S.S. and Buchholz, D.R. (2012) Beyond Synergy: Corticosterone and thyroid hormone have numerous interaction effects on gene regulation in Xenopus tropicalis tadpoles. Endocrinol. 153(11):5309–5324.[Link]
- Hasebe, T., Buchholz, D.R., Shi, Y.-B., Ishizuya-Oka, A. (2011). Epithelial-connective tissue interactions induced by thyroid hormone receptor are essential for adult stem cell development in the Xenopus laevis intestine. Stem Cells 29:154-161.[Link]
- Rankin, S.A., Zorn, A.M., Buchholz, D.R. (2011). New doxycycline-inducible transgenic Xenopus. Dev. Dynamics 240:1467–1474.[Link]
- Hollar, A.R., Choi, J., Grimm, A.T., Buchholz, D.R. (2011). Higher thyroid hormone receptor expression correlates with short larval periods in spadefoot toads and increases metamorphic rate. Gen. Comp. Endocrinol. 173:190-198.[Link]
- Kulkarni, S.S., Gomes-Mestre, I., Moskalik, C.L., Storz, B.L., Buchholz, D.R. (2011). Evolutionary reduction of developmental plasticity in desert spadefoot toads. J. Evol. Biol. 2 4:2445–2455. [Link]
- Heimeier, R A, Das, B, Buchholz, D R, Fiorentino, M, & Shi, Y-B (2010). Studies on Xenopus laevis intestine reveal biological pathways underlying vertebrate gut adaptation from embryo to adult. Genome biology, 11(5), R55.[Link]
- Buchholz, D R., Hollar, A R. Ledon-Retig, C (2010). Scaphiopus couchii (Couch's spadefoot). Developmental Morphology. Herpetological Review, 41(4), 480.[Link]
- Hayes, T. B., Khoury, V., Narayan, A., Nazir, M., Park, A., Brown, T., Adame, L., Chan, E., Buchholz, D., Stueve, T., Gallipeau, S. (2010). Atrazine induces complete feminization and chemical castration in male African clawed frogs (Xenopus laevis). Proceedings of the National Academy of Sciences of the United States of America, 107(10), 4612, 4617.[Link]
- Kulkarni, S.S., Singamsetty, S., & Buchholz, D.R. (2010). Corticotropin-releasing factor regulates the development in the direct developing frog, Eleutherodactylus coqui. General and comparative endocrinology, 169(3), 225-30.[Link]
- Das, B., Heimeier, R. A., Buchholz, D. R., Shi, Y. B. (2009). Identification of direct thyroid hormone response genes reveals the earliest gene regulation programs during frog metamorphosis. The Journal of biological chemistry, 284:34167-34178.[Link]
- Ishizuya-Oka, Atsuko, Hasebe, Takashi, Buchholz, Daniel R, Kajita, Mitsuko, Fu, Liezhen, & Shi, Yun-Bo (2009). Origin of the adult intestinal stem cells induced by thyroid hormone in Xenopus laevis. The FASEB journal 23(8), 2568-75.[Link]
- Heimeier, R. A., Das, B., Buchholz, D. R., Shi, Y. B. (2009). The xenoestrogen bisphenol A inhibits postembryonic vertebrate development by antagonizing gene regulation by thyroid hormone. Endocrinology, 150, 2964-2973.[Link]
- Rankin, S. A., Hasebe, T., Zorn, A. M., Buchholz, D. R. (2009). Improved cre reporter transgenic Xenopus. Developmental dynamics 238:2401-2408.[Link]
- Paul, B. D., Buchholz, D. R., Fu, L., Shi, Y. B. (2007). SRC-p300 coactivator complex is required for thyroid hormone-induced amphibian metamorphosis. The Journal of biological chemistry, 282:7472-7481.[Link]
- Sato, Y., Buchholz, D. R., Paul, B. D., Shi, Y. B. (2007). A role of unliganded thyroid hormone receptor in postembryonic development in Xenopus laevis. Mechanisms of development, 124:476-488.[Link]
- Buchholz, D. R., Heimeier, R. A., Das, B., Washington, T., Shi, Y. B. (2007). Pairing morphology with gene expression in thyroid hormone-induced intestinal remodeling and identification of a core set of TH-induced genes across tadpole tissues. Developmental biology, 303:576-590.[Link]
- Gomez-Mestre, I., Buchholz, D. R. (2006). Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proceedings of the National Academy of Sciences of the United States of America, 103(50), 19021, 19026. [Link]
- Fu, L., Tomita, A., Wang, H., Buchholz, D. R., Shi, Y. B. (2006). Transcriptional regulation of the Xenopus laevis Stromelysin-3 gene by thyroid hormone is mediated by a DNA element in the first intron. The Journal of biological chemistry, 281(25), 16870, 16878. [Link]
- Buchholz, D. R., Hayes, T. B. (2005). Variation in thyroid hormone action and tissue content underlies species differences in the timing of metamorphosis in desert frogs. Evolution & development, 7(5), 458, 467. [Link]
- Buchholz, D. R., Paul, B. D., Shi, Y. B. (2005). Gene-specific changes in promoter occupancy by thyroid hormone receptor during frog metamorphosis. Implications for developmental gene regulation. The Journal of biological chemistry, 280(50), 41222, 41228. [Link]
- Fu, L., Ishizuya-Oka, A., Buchholz, D. R., Amano, T., Matsuda, H., Shi, Y. B. (2005). A causative role of stromelysin-3 in extracellular matrix remodeling and epithelial apoptosis during intestinal metamorphosis in Xenopus laevis. The Journal of biological chemistry, 280(30), 27856, 27865. [Link]
- Paul, B. D., Fu, L., Buchholz, D. R., Shi, Y. B. (2005). Coactivator recruitment is essential for liganded thyroid hormone receptor to initiate amphibian metamorphosis. Molecular and cellular biology, 25(13), 5712, 5724. [Link]
- Paul, B. D., Buchholz, D. R., Fu, L., Shi, Y. B. (2005). Tissue- and gene-specific recruitment of steroid receptor coactivator-3 by thyroid hormone receptor during development. The Journal of biological chemistry, 280(29), 27165, 27172. [Link]
- Tomita, A., Buchholz, D. R., Shi, Y. B. (2004). Recruitment of N-CoR/SMRT-TBLR1 corepressor complex by unliganded thyroid hormone receptor for gene repression during frog development. Molecular and cellular biology, 24(8), 3337, 3346. [Link]
- Buchholz, D. R., Tomita, A., Fu, L., Paul, B. D., Shi, Y. B. (2004). Transgenic analysis reveals that thyroid hormone receptor is sufficient to mediate the thyroid hormone signal in frog metamorphosis. Molecular and cellular biology, 24(20), 9026, 9037. [Link]
- Buchholz, D. R., Ishizuya-Oka, A., Shi, Y. B. (2004). Spatial and temporal expression pattern of a novel gene in the frog Xenopus laevis: correlations with adult intestinal epithelial differentiation during metamorphosis. Gene expression patterns : GEP, 4(3), 321, 328. [Link]
- Garcia-Paris, M., Buchholz, D. R., Parra-Olea, G. (2003). Phylogenetic relationships of Pelobatoidea re-examined using mtDNA. Molecular phylogenetics and evolution, 28(1), 12, 23. [Link]
- Buchholz, D. R., Hsia, S. C., Fu, L., Shi, Y. B. (2003). A dominant-negative thyroid hormone receptor blocks amphibian metamorphosis by retaining corepressors at target genes. Molecular and cellular biology, 23(19), 6750, 6758. [Link]
- Tomita, A., Buchholz, D. R., Obata, K., Shi, Y. B. (2003). Fusion protein of retinoic acid receptor alpha with promyelocytic leukemia protein or promyelocytic leukemia zinc finger protein recruits N-CoR-TBLR1 corepressor complex to repress transcription in vivo. The Journal of biological chemistry, 278(33), 30788, 30795. [Link]
- Ruben, L. N., Ahmadi, P., Johnson, R. O., Buchholz, D. R., Clothier, R. H., Shiigi, S. (1994). Apoptosis in the thymus of developing Xenopus laevis. Developmental and comparative immunology, 18(4), 343, 352. [Link]
- Ruben, L. N., Buchholz, D. R., Ahmadi, P., Johnson, R. O., Clothier, R. H., Shiigi, S. (1994). Apoptosis in thymus of adult Xenopus laevis. Developmental and comparative immunology, 18(3), 231, 238. [Link]
- Buchholz, D.R. (2012) Chapter 16: Tet-On binary systems for tissue-specific and inducible transgene expression, pp. 265-275. In Xenopus Protocols: Post-Genomic Approaches, 2nd Ed. Eds Hoppler, S. and Vize, P. For series: Methods in Molecular Biology 917. New York: Humana Press.
- Buchholz, D.R., Moakalik, C.L., Kulkarni, S.S., Hollar, A.R., Ng. A. (2011) Chapter 5: Hormonal regulation and the evolution of amphibian metamorphic diversity. In Mechanisms of Life History Evolution. pp. 87-97. Eds. Flatt, T. and Heyland, A. Oxford University Press.[Link]
- Sachs, L.M., Buchholz, D.R. (2017) Frogs Model Man: In-vivo thyroid hormone signaling during development. genesis 55:e2300[Link]
- Buchholz, D.R. (2017) Xenopus metamorphosis as a model to study thyroid hormone receptor function during vertebrate developmental transitions. Mol. Cell. Endocrinol. 459:64-70.
- Buchholz, D.R. (2015) More similar than you think: Frog metamorphosis as a model of human perinatal endocrinology. Dev. Biol. 408:188–195.[Link]
- Kulkarni, S.S., Buchholz, D.R. (2014). Corticosteroid signaling in frog metamorphosis. Gen. Comp. Endocrinol. 203:225–231.[Link]
- Kulkarni, S.S., Buchholz, D.R. (2013) Developmental programs and endocrine disruption in frog metamorphosis: The perspective from microarray analysis. Curr. Top. Devel. Biol. 103:329-364.
- Buchholz, D. R., Paul, B. D., Fu, L., Shi, Y. B. (2006). Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. General and comparative endocrinology, 145:1-19.[Link]
Experience & Service
- Comments: The objective of this course is to learn the major concepts in endocrinology, hormonal systems, and endocrine mechanisms. Mammalian endocrinology will be emphasized, but commonalities across vertebrates will be covered. In addition, we will examine two examples of primary literature. Ultimately, the students will gain an appreciation for the fundamentals of endocrinology as well as the relevance of endocrinology in everyday life. [Link]