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3. osr1 couples intermediate mesoderm cell fate with temporal dynamics of vessel progenitor cell differentiation

Author

Perens, Elliot A, Diaz, Jessyka T, Quesnel, Agathe, Askary, Amjad, Crump, J Gage, and Yelon, Deborah

Subjects
Genetics, Stem Cell Research, Stem Cell Research - Nonembryonic - Non-Human, Animals, Basic Helix-Loop-Helix Transcription Factors, Cell Differentiation, Gene Expression Regulation, Developmental, Kidney, Mesoderm, Organogenesis, Transcription Factors, Zebrafish, Zebrafish Proteins, Intermediate mesoderm, Vessel progenitors, hand2, hand2, Biological Sciences, Medical and Health Sciences
Abstract

Transcriptional regulatory networks refine gene expression boundaries to define the dimensions of organ progenitor territories. Kidney progenitors originate within the intermediate mesoderm (IM), but the pathways that establish the boundary between the IM and neighboring vessel progenitors are poorly understood. Here, we delineate roles for the zinc-finger transcription factor Osr1 in kidney and vessel progenitor development. Zebrafish osr1 mutants display decreased IM formation and premature emergence of lateral vessel progenitors (LVPs). These phenotypes contrast with the increased IM and absent LVPs observed with loss of the bHLH transcription factor Hand2, and loss of hand2 partially suppresses osr1 mutant phenotypes. hand2 and osr1 are expressed together in the posterior mesoderm, but osr1 expression decreases dramatically prior to LVP emergence. Overexpressing osr1 during this timeframe inhibits LVP development while enhancing IM formation, and can rescue the osr1 mutant phenotype. Together, our data demonstrate that osr1 modulates the extent of IM formation and the temporal dynamics of LVP development, suggesting that a balance between levels of osr1 and hand2 expression is essential to demarcate the kidney and vessel progenitor territories.

Published
2021

4. Long-term repair of porcine articular cartilage using cryopreservable, clinically compatible human embryonic stem cell-derived chondrocytes

Author

Petrigliano, Frank A, Liu, Nancy Q, Lee, Siyoung, Tassey, Jade, Sarkar, Arijita, Lin, Yucheng, Li, Liangliang, Yu, Yifan, Geng, Dawei, Zhang, Jiankang, Shkhyan, Ruzanna, Bogdanov, Jacob, Van Handel, Ben, Ferguson, Gabriel B, Lee, Youngjoo, Hinderer, Svenja, Tseng, Kuo-Chang, Kavanaugh, Aaron, Crump, J Gage, Pyle, April D, Schenke-Layland, Katja, Billi, Fabrizio, Wang, Liming, Lieberman, Jay, Hurtig, Mark, and Evseenko, Denis

Subjects
Medical Biotechnology, Biomedical and Clinical Sciences, Osteoarthritis, Regenerative Medicine, Chronic Pain, Arthritis, Stem Cell Research, Biotechnology, Pain Research, Stem Cell Research - Induced Pluripotent Stem Cell, Stem Cell Research - Induced Pluripotent Stem Cell - Human, Aging, 5.2 Cellular and gene therapies, Development of treatments and therapeutic interventions, Musculoskeletal, Medical biotechnology, Medical physiology
Abstract

Osteoarthritis (OA) impacts hundreds of millions of people worldwide, with those affected incurring significant physical and financial burdens. Injuries such as focal defects to the articular surface are a major contributing risk factor for the development of OA. Current cartilage repair strategies are moderately effective at reducing pain but often replace damaged tissue with biomechanically inferior fibrocartilage. Here we describe the development, transcriptomic ontogenetic characterization and quality assessment at the single cell level, as well as the scaled manufacturing of an allogeneic human pluripotent stem cell-derived articular chondrocyte formulation that exhibits long-term functional repair of porcine articular cartilage. These results define a new potential clinical paradigm for articular cartilage repair and mitigation of the associated risk of OA.

Published
2021

8. Frequency of mononuclear diploid cardiomyocytes underlies natural variation in heart regeneration

Author

Patterson, Michaela, Barske, Lindsey, Van Handel, Ben, Rau, Christoph D, Gan, Peiheng, Sharma, Avneesh, Parikh, Shan, Denholtz, Matt, Huang, Ying, Yamaguchi, Yukiko, Shen, Hua, Allayee, Hooman, Crump, J Gage, Force, Thomas I, Lien, Ching-Ling, Makita, Takako, Lusis, Aldons J, Kumar, S Ram, and Sucov, Henry M

Subjects
Biological Sciences, Genetics, Heart Disease, Cardiovascular, Regenerative Medicine, Animals, Animals, Genetically Modified, Cells, Cultured, Diploidy, Gene Expression Profiling, Heart, Immunoblotting, In Situ Hybridization, Fluorescence, Mice, Inbred C57BL, Mice, Knockout, Mice, Transgenic, Microscopy, Confocal, Myocardium, Myocytes, Cardiac, Protein Kinases, Protein Serine-Threonine Kinases, Regeneration, Zebrafish, Medical and Health Sciences, Developmental Biology, Agricultural biotechnology, Bioinformatics and computational biology
Abstract

Adult mammalian cardiomyocyte regeneration after injury is thought to be minimal. Mononuclear diploid cardiomyocytes (MNDCMs), a relatively small subpopulation in the adult heart, may account for the observed degree of regeneration, but this has not been tested. We surveyed 120 inbred mouse strains and found that the frequency of adult mononuclear cardiomyocytes was surprisingly variable (>7-fold). Cardiomyocyte proliferation and heart functional recovery after coronary artery ligation both correlated with pre-injury MNDCM content. Using genome-wide association, we identified Tnni3k as one gene that influences variation in this composition and demonstrated that Tnni3k knockout resulted in elevated MNDCM content and increased cardiomyocyte proliferation after injury. Reciprocally, overexpression of Tnni3k in zebrafish promoted cardiomyocyte polyploidization and compromised heart regeneration. Our results corroborate the relevance of MNDCMs in heart regeneration. Moreover, they imply that intrinsic heart regeneration is not limited nor uniform in all individuals, but rather is a variable trait influenced by multiple genes.

Published
2017

17. Ligament injury in adult zebrafish triggers ECM remodeling and cell dedifferentiation for scar-free regeneration

Author

Anderson, Troy, primary, Mo, Julia, additional, Gagarin, Ernesto, additional, Sherwood, Desmarie, additional, Blumenkrantz, Maria, additional, Mao, Eric, additional, Leon, Gianna, additional, Chen, Hung-Jhen, additional, Tseng, Kuo-Chang, additional, Fabian, Peter, additional, Crump, J. Gage, additional, and Smeeton, Joanna, additional

Published
2023
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18. Craniofacial developmental biology in the single-cell era.

Author

Kuo-Chang Tseng and Crump, J. Gage

Subjects
*EPIBLAST, *NEURAL crest, *GENE expression, *GENETICS, *CONGENITAL disorders, *MESODERM, *DEVELOPMENTAL biology
Abstract

The evolution of a unique craniofacial complex in vertebrates made possible new ways of breathing, eating, communicating and sensing the environment. The head and face develop through interactions of all three germ layers, the endoderm, ectoderm and mesoderm, as well as the so-called fourth germ layer, the cranial neural crest. Over a century of experimental embryology and genetics have revealed an incredible diversity of cell types derived from each germ layer, signaling pathways and genes that coordinate craniofacial development, and how changes to these underlie human disease and vertebrate evolution. Yet for many diseases and congenital anomalies, we have an incomplete picture of the causative genomic changes, in particular how alterations to the non-coding genome might affect craniofacial gene expression. Emerging genomics and single-cell technologies provide an opportunity to obtain a more holistic view of the genes and gene regulatory elements orchestrating craniofacial development across vertebrates. These single-cell studies generate novel hypotheses that can be experimentally validated in vivo. In this Review, we highlight recent advances in single-cell studies of diverse craniofacial structures, as well as potential pitfalls and the need for extensive in vivo validation. We discuss how these studies inform the developmental sources and regulation of head structures, bringing new insights into the etiology of structural birth anomalies that affect the vertebrate head. [ABSTRACT FROM AUTHOR]

Published
2023
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25. Gill developmental program in the teleost mandibular arch

Author

Thiruppathy, Mathi, Fabian, Peter, Gillis, J. Andrew, Crump, J. Gage, Thiruppathy, Mathi, Fabian, Peter, Gillis, J. Andrew, and Crump, J. Gage

Abstract

© The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Thiruppathy, M., Fabian, P., Gillis, J. A., & Crump, J. G. Gill developmental program in the teleost mandibular arch. Elife, 11, (2022): e78170, https://doi.org/10.7554/eLife.78170., Whereas no known living vertebrate possesses gills derived from the jaw-forming mandibular arch, it has been proposed that the jaw arose through modifications of an ancestral mandibular gill. Here, we show that the zebrafish pseudobranch, which regulates blood pressure in the eye, develops from mandibular arch mesenchyme and first pouch epithelia and shares gene expression, enhancer utilization, and developmental gata3 dependence with the gills. Combined with work in chondrichthyans, our findings in a teleost fish point to the presence of a mandibular pseudobranch with serial homology to gills in the last common ancestor of jawed vertebrates, consistent with a gill origin of vertebrate jaws., National Institute of Dental and Craniofacial Research (5R35DE027550) - J. Gage Crump National Institute of Dental and Craniofacial Research (5K99DE029858) - Peter Fabian National Institute of Dental and Craniofacial Research (1F31DE030706) - Mathi Thiruppathy Royal Society (UF130182) & Royal Society (URF\R\191007) - J. Andrew Gillis

Published
2022

26. Notch signaling enhances bone regeneration in the zebrafish mandible

Author

Kraus, Jessica M., primary, Giovannone, Dion, additional, Rydzik, Renata, additional, Balsbaugh, Jeremy L., additional, Moss, Isaac L., additional, Schwedler, Jennifer L., additional, Bertrand, Julien Y., additional, Traver, David, additional, Hankenson, Kurt D., additional, Crump, J. Gage, additional, and Youngstrom, Daniel W., additional

Published
2022
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32. Long-term repair of porcine articular cartilage using cryopreservable, clinically compatible human embryonic stem cell-derived chondrocytes

Author

Petrigliano, Frank A., primary, Liu, Nancy Q., additional, Lee, Siyoung, additional, Tassey, Jade, additional, Sarkar, Arijita, additional, Lin, Yucheng, additional, Li, Liangliang, additional, Yu, Yifan, additional, Geng, Dawei, additional, Zhang, Jiankang, additional, Shkhyan, Ruzanna, additional, Bogdanov, Jacob, additional, Van Handel, Ben, additional, Ferguson, Gabriel B., additional, Lee, Youngjoo, additional, Hinderer, Svenja, additional, Tseng, Kuo-Chang, additional, Kavanaugh, Aaron, additional, Crump, J. Gage, additional, Pyle, April D., additional, Schenke-Layland, Katja, additional, Billi, Fabrizio, additional, Wang, Liming, additional, Lieberman, Jay, additional, Hurtig, Mark, additional, and Evseenko, Denis, additional

Published
2021
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35. The developing mouse coronal suture at single-cell resolution

Author

Farmer, D’Juan T., primary, Mlcochova, Hana, additional, Zhou, Yan, additional, Koelling, Nils, additional, Wang, Guanlin, additional, Ashley, Neil, additional, Maxson, Robert E, additional, Wilkie, Andrew O. M., additional, Crump, J Gage, additional, and Twigg, Stephen R.F., additional

Published
2021
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36. Histone H3.3 beyond cancer : Germline mutations in Histone 3 Family 3A and 3B cause a previously unidentified neurodegenerative disorder in 46 patients

Author

Bryant, Laura, Li, Dong, Cox, Samuel G., Marchione, Dylan, Joiner, Evan F., Wilson, Khadija, Janssen, Kevin, Lee, Pearl, March, Michael E., Nair, Divya, Sherr, Elliott, Fregeau, Brieana, Wierenga, Klaas J., Wadley, Alexandrea, Mancini, Grazia M. S., Powell-Hamilton, Nina, van de Kamp, Jiddeke, Grebe, Theresa, Dean, John, Ross, Alison, Crawford, Heather P., Powis, Zoe, Cho, Megan T., Willing, Marcia C., Manwaring, Linda, Schot, Rachel, Nava, Caroline, Afenjar, Alexandra, Lessel, Davor, Wagner, Matias, Klopstock, Thomas, Winkelmann, Juliane, Catarino, Claudia B., Retterer, Kyle, Schuette, Jane L., Innis, Jeffrey W., Pizzino, Amy, Lüttgen, Sabine, Denecke, Jonas, Strom, Tim M., Monaghan, Kristin G., Yuan, Zuo-Fei, Dubbs, Holly, Bend, Renee, Lee, Jennifer A., Lyons, Michael J., Hoefele, Julia, Günthner, Roman, Reutter, Heiko, Keren, Boris, Radtke, Kelly, Sherbini, Omar, Mrokse, Cameron, Helbig, Katherine L., Odent, Sylvie, Cogne, Benjamin, Mercier, Sandra, Bezieau, Stephane, Besnard, Thomas, Kury, Sebastien, Redon, Richard, Reinson, Karit, Wojcik, Monica H., Õunap, Katrin, Ilves, Pilvi, Innes, A. Micheil, Kernohan, Kristin D., Costain, Gregory, Meyn, M. Stephen, Chitayat, David, Zackai, Elaine, Lehman, Anna, Kitson, Hilary, Martin, Martin G., Martinez-Agosto, Julian A., Nelson, Stan F., Palmer, Christina G. S., Papp, Jeanette C., Parker, Neil H., Sinsheimer, Janet S., Vilain, Eric, Wan, Jijun, Yoon, Amanda J., Zheng, Allison, Brimble, Elise, Ferrero, Giovanni Battista, Radio, Francesca Clementina, Carli, Diana, Barresi, Sabina, Brusco, Alfredo, Tartaglia, Marco, Thomas, Jennifer Muncy, Umana, Luis, Weiss, Marjan M., Gotway, Garrett, Stuurman, K. E., Thompson, Michelle L., McWalter, Kirsty, Stumpel, Constance T. R. M., Stevens, Servi J. C., Stegmann, Alexander P. A., Tveten, Kristian, Vøllo, Arve, Prescott, Trine, Fagerberg, Christina, Laulund, Lone Walentin, Larsen, Martin J., Byler, Melissa, Lebel, Robert Roger, Hurst, Anna C., Dean, Joy, Schrier Vergano, Samantha A., Norman, Jennifer, Mercimek-Andrews, Saadet, Neira, Juanita, Van Allen, Margot I., Longo, Nicola, Sellars, Elizabeth, Louie, Raymond J., Cathey, Sara S., Brokamp, Elly, Heron, Delphine, Snyder, Molly, Vanderver, Adeline, Simon, Celeste, de la Cruz, Xavier, Padilla, Natalia, Crump, J. Gage, Chung, Wendy, Garcia, Benjamin, Hakonarson, Hakon H., Bhoj, Elizabeth J., Universitat Autònoma de Barcelona, Bryant, Laura, Li, Dong, Cox, Samuel G., Marchione, Dylan, Joiner, Evan F., Wilson, Khadija, Janssen, Kevin, Lee, Pearl, March, Michael E., Nair, Divya, Sherr, Elliott, Fregeau, Brieana, Wierenga, Klaas J., Wadley, Alexandrea, Mancini, Grazia M. S., Powell-Hamilton, Nina, van de Kamp, Jiddeke, Grebe, Theresa, Dean, John, Ross, Alison, Crawford, Heather P., Powis, Zoe, Cho, Megan T., Willing, Marcia C., Manwaring, Linda, Schot, Rachel, Nava, Caroline, Afenjar, Alexandra, Lessel, Davor, Wagner, Matias, Klopstock, Thomas, Winkelmann, Juliane, Catarino, Claudia B., Retterer, Kyle, Schuette, Jane L., Innis, Jeffrey W., Pizzino, Amy, Lüttgen, Sabine, Denecke, Jonas, Strom, Tim M., Monaghan, Kristin G., Yuan, Zuo-Fei, Dubbs, Holly, Bend, Renee, Lee, Jennifer A., Lyons, Michael J., Hoefele, Julia, Günthner, Roman, Reutter, Heiko, Keren, Boris, Radtke, Kelly, Sherbini, Omar, Mrokse, Cameron, Helbig, Katherine L., Odent, Sylvie, Cogne, Benjamin, Mercier, Sandra, Bezieau, Stephane, Besnard, Thomas, Kury, Sebastien, Redon, Richard, Reinson, Karit, Wojcik, Monica H., Õunap, Katrin, Ilves, Pilvi, Innes, A. Micheil, Kernohan, Kristin D., Costain, Gregory, Meyn, M. Stephen, Chitayat, David, Zackai, Elaine, Lehman, Anna, Kitson, Hilary, Martin, Martin G., Martinez-Agosto, Julian A., Nelson, Stan F., Palmer, Christina G. S., Papp, Jeanette C., Parker, Neil H., Sinsheimer, Janet S., Vilain, Eric, Wan, Jijun, Yoon, Amanda J., Zheng, Allison, Brimble, Elise, Ferrero, Giovanni Battista, Radio, Francesca Clementina, Carli, Diana, Barresi, Sabina, Brusco, Alfredo, Tartaglia, Marco, Thomas, Jennifer Muncy, Umana, Luis, Weiss, Marjan M., Gotway, Garrett, Stuurman, K. E., Thompson, Michelle L., McWalter, Kirsty, Stumpel, Constance T. R. M., Stevens, Servi J. C., Stegmann, Alexander P. A., Tveten, Kristian, Vøllo, Arve, Prescott, Trine, Fagerberg, Christina, Laulund, Lone Walentin, Larsen, Martin J., Byler, Melissa, Lebel, Robert Roger, Hurst, Anna C., Dean, Joy, Schrier Vergano, Samantha A., Norman, Jennifer, Mercimek-Andrews, Saadet, Neira, Juanita, Van Allen, Margot I., Longo, Nicola, Sellars, Elizabeth, Louie, Raymond J., Cathey, Sara S., Brokamp, Elly, Heron, Delphine, Snyder, Molly, Vanderver, Adeline, Simon, Celeste, de la Cruz, Xavier, Padilla, Natalia, Crump, J. Gage, Chung, Wendy, Garcia, Benjamin, Hakonarson, Hakon H., Bhoj, Elizabeth J., and Universitat Autònoma de Barcelona

Abstract

Germ line mutations in H3F3A and H3F3B cause a previously unidentified neurodevelopmental syndrome. Although somatic mutations in Histone 3.3 (H3.3) are well-studied drivers of oncogenesis, the role of germline mutations remains unreported. We analyze 46 patients bearing de novo germline mutations in histone 3 family 3A (H3F3A) or H3F3B with progressive neurologic dysfunction and congenital anomalies without malignancies. Molecular modeling of all 37 variants demonstrated clear disruptions in interactions with DNA, other histones, and histone chaperone proteins. Patient histone posttranslational modifications (PTMs) analysis revealed notably aberrant local PTM patterns distinct from the somatic lysine mutations that cause global PTM dysregulation. RNA sequencing on patient cells demonstrated up-regulated gene expression related to mitosis and cell division, and cellular assays confirmed an increased proliferative capacity. A zebrafish model showed craniofacial anomalies and a defect in Foxd3-derived glia. These data suggest that the mechanism of germline mutations are distinct from cancer-associated somatic histone mutations but may converge on control of cell proliferation

Published
2020

37. Zebrafish prrx1a mutants have normal hearts

Author

Genetica Groep Van Haaften, Child Health, Cancer, Medische Fysiologie, Cardiologie onderzoek 2, Onderzoek, Circulatory Health, Tessadori, Federico, de Bakker, Dennis E.M., Barske, Lindsey, Nelson, Nellie, Algra, Hermine A., Willekers, Sven, Nichols, James T., Crump, J. Gage, Bakkers, Jeroen, Genetica Groep Van Haaften, Child Health, Cancer, Medische Fysiologie, Cardiologie onderzoek 2, Onderzoek, Circulatory Health, Tessadori, Federico, de Bakker, Dennis E.M., Barske, Lindsey, Nelson, Nellie, Algra, Hermine A., Willekers, Sven, Nichols, James T., Crump, J. Gage, and Bakkers, Jeroen

Published
2020

45. Identification of the skeletal progenitor cells forming osteophytes in osteoarthritis

Author

Roelofs, Anke J, primary, Kania, Karolina, additional, Rafipay, Alexandra J, additional, Sambale, Meike, additional, Kuwahara, Stephanie T, additional, Collins, Fraser L, additional, Smeeton, Joanna, additional, Serowoky, Maxwell A, additional, Rowley, Lynn, additional, Wang, Hui, additional, Gronewold, René, additional, Kapeni, Chrysa, additional, Méndez-Ferrer, Simón, additional, Little, Christopher B, additional, Bateman, John F, additional, Pap, Thomas, additional, Mariani, Francesca V, additional, Sherwood, Joanna, additional, Crump, J Gage, additional, and De Bari, Cosimo, additional

Published
2020
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46. The Axenfeld-Rieger syndrome geneFOXC1contributes to left-right patterning

Author

Chrystal, Paul W., primary, French, Curtis R., additional, Jean, Francesca, additional, Havrylov, Serhiy, additional, van Baarle, Suey, additional, Peturson, Ann-Marie, additional, Xu, Pengfei, additional, Crump, J. Gage, additional, Pilgrim, David B., additional, Lehmann, Ordan J., additional, and Waskiewicz, Andrew J., additional

Published
2020
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