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The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors
Abstract
Pancreas development begins with the formation of buds at specific sites in the embryonic foregut endoderm. We used recombination-based lineage tracing in vivo to show that Ptf1a (also known as PTF1-p48) is expressed at these early stages in the progenitors of pancreatic ducts, exocrine and endocrine cells, rather than being an exocrine-specific gene as previously described. Moreover, inactivation of Ptf1a switches the character of pancreatic progenitors such that their progeny proliferate in and adopt the normal fates of duodenal epithelium, including its stem-cell compartment. Consistent with the proposal that Ptf1a supports the specification of precursors of all three pancreatic cell types, transgene-based expression of Pdx1, a gene essential to pancreas formation, from Ptf1a cis-regulatory sequences restores pancreas tissue to Pdx1-null mice that otherwise lack mature exocrine and endocrine cells because of an early arrest in organogenesis. These experiments provide evidence that Ptf1a expression is specifically connected to the acquisition of pancreatic fate by undifferentiated foregut endoderm.
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“Specific recombination in epithelial cells of the pancreas was confirmed by immunohistochemical stainings for tdRFP in Ptf1aCre/+ [35] x LSL-tdRFPKI/KI [55, 56] mice (Additional file 1: Fig. S3d) [56].”
From TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration (2023) · cites this paper as [35]
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Masui, T., Swift, G. H., Hale, M. A., Meredith, D. M., Johnson, J. E. B., & MacDonald, R. J. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.00549-08 · Cited by 98
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BackgroundInfluentialSelf-citationOrigin of Climbing Fiber Neurons and Their Developmental Dependence on Ptf1a
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Benitez, C. M., Goodyer, W. R., & Kim, S. K. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a012401 · Cited by 111
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InfluentialToyoda, T., Mae, S.-I., Tanaka, H., Kondo, Y., Funato, M., Hosokawa, Y., Sudo, T., Kawaguchi, Y., & Osafune, K. (2015) · Stem Cell Research · doi:10.1016/j.scr.2015.01.007 · Cited by 103
Self-citationThe Development of Beta-cell Mass: Recent Progress and Potential Role of GLP-1
Stoffers, D. (2004) · Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme · doi:10.1055/s-2004-826168 · Cited by 103
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“Cre recombinase, containing an N-terminal nuclear localization signal (Kawaguchi et al., 2002).”
BackgroundSelf-citationMartinelli, P., Cañamero, M., Pozo, N. D., Madriles, F., Zapata, A., & Real, F. (2012) · Gut · doi:10.1136/gutjnl-2012-303328 · Cited by 102
Wang, Y.-Y., Rovira, M., Yusuff, S., & Parsons, M. J. (2011) · Development · doi:10.1242/dev.059097 · Cited by 102
“…(CreERT2) has been extensively used to label embryonic pancreatic cells in the mouse and identify their ultimate fate in adult pancreas (Gu et al., 2002; Kawaguchi et al., 2002) as well as their contribution to regenerative tissues following injury (Inada et al., 2008; Solar et al., 2009).”
Wan, H., Korzh, S., Li, Z., Mudumana, S., Korzh, V., Jiang, Y.-J., Lin, S., & Gong, Z. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.01.016 · Cited by 102
Xiao, X., Wiersch, J., El-Gohary, Y., Guo, P., Prasadan, K., Paredes, J., Welsh, C., Shiota, C., & Gittes, G. K. (2013) · Diabetes · doi:10.2337/db12-1428 · Cited by 102
“Pancreas transcription factor 1a (PTF1a) promoter cre reporter (PTF1a) mice have previously been described (33).”
Transcription factor GATA-6 is expressed in the endocrine and GATA-4 in the exocrine pancreas.
Ketola, I., Otonkoski, T., Pulkkinen, M.-A., Niemi, H., Palgi, J., Jacobsen, C., Wilson, D., & Heikinheimo, M. (2004) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2004.06.007 · Cited by 100
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Genes controlling pancreas ontogeny.
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MethodHuang, M.-G., Huang, T., Xiang, Y., Xie, Z., Chen, Y., Yan, R., Xu, J., & Cheng, L.-P. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.06.031 · Cited by 99
PDX1 dynamically regulates pancreatic ductal adenocarcinoma initiation and maintenancePreprint
Roy, N., Takeuchi, K. K., Ruggeri, J. M., Bailey, P., Chang, D., Li, J., Leonhardt, L., Puri, S., Hoffman, M., Gao, S., et al. (2016) · Genes & Development · doi:10.1101/gad.291021.116 · Cited by 98
“However, ectopic Pdx1 expression in progenitors induces abundant ADM (Kawaguchi et al. 2002; Miyatsuka et al. 2006), and Elastase-Cre-driven Pdx1 overexpression in exocrine precursors triggers marked dysmorphogenesis in the exocrine pancreas (Heller et al. 2001).”
BackgroundSelf-citationBorromeo, M. D., Meredith, D., Castro, D. S., Chang, J. C., Tung, K.-C., Guillemot, F., & Johnson, J. E. (2014) · Development · doi:10.1242/dev.105866 · Cited by 97
“4kbPtf1a::mCherry line was crossed to the Ptf1a knockin mouse (Kawaguchi et al., 2002), and mCherry+ cells were isolated from Ptf1a−/+ and Ptf1a−/− neural tubes.”
MethodInfluentialYamada, M., Seto, Y., Taya, S., Owa, T., Inoue, Y., Inoue, T., Kawaguchi, Y., Nabeshima, Y., & Hoshino, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2722-13.2014 · Cited by 97
Self-citationTranscription factors and the genetic organization of brain stem respiratory neurons
Gray, P. A. (2008) · Journal of Applied Physiology · doi:10.1152/japplphysiol.01383.2007 · Cited by 94
“B: FoxP2 (magenta) is coexpressed with YFP (green) in a region corresponding to the KF nucleus in a p0 double transgenic mouse (arrow; this image is the same as Fig.”
BackgroundInfluentialFunction and regulation of zebrafish nkx2.2a during development of pancreatic islet and ducts
Pauls, S., Zecchin, E., Tiso, N., Bortolussi, M., & Argenton, F. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.024 · Cited by 84
“More recently it was shown that Ptf1a is already expressed in the pancreatic anlage where it prevents pancreatic precursors, also those of the endocrine lineage, from adopting a duodenal fate (Kawaguchi et al., 2002).”
BackgroundFlandez, M., Cendrowski, J., Cañamero, M., Salas, A., del Pozo, N., Schoonjans, K., & Real, F. X. (2014) · Gut · doi:10.1136/gutjnl-2012-304381 · Cited by 95
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Vascular instruction of pancreas development
Cleaver, O. B., & Dor, Y. (2012) · Development · doi:10.1242/dev.065953 · Cited by 99
“3), which expresses the proteins pancreatic and duodenal homeobox box 1 (PDX1) and pancreas-specific transcription factor 1 (PTF1A) (Offield et al., 1996; Kawaguchi et al., 2002; Gu et al., 2003).”
The endocrine pancreas: insights into development, differentiation, and diabetes
Mastracci, T. L., & Sussel, L. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.44 · Cited by 100
Ptf1a is expressed transiently in all types of amacrine cells in the embryonic zebrafish retina
Jusuf, P. R., & Harris, W. (2009) · Neural Development · doi:10.1186/1749-8104-4-34 · Cited by 94
“Ptf1a (pancreas transcription factor 1a) is a helix-loop-helix transcription factor that was first identified as a subunit of the trimeric PTF1 transcription factor complex [1], which is crucial for the development and maintenance of the pancreas [2-7].”
BackgroundBröhl, D., Strehle, M., Wende, H., Hori, K., Bormuth, I., Nave, K., Müller, T. H., & Birchmeier, C. (2008) · Developmental Biology · doi:10.1016/j.ydbio.2008.08.002 · Cited by 90
“The generation of the mutant Gsx1, Gsx2, Ptf1a, Pax2, Neurod1, Neurod6 (Nex allele), Lhx1, Lhx5, and Lbx1 alleles has been previously described (Torres et al., 1995; Li et al., 1996; Naya et al., 1997; Szucsik et al., 1997; Zhao et al., 1999; Kawaguchi et al., 2002; Kwan and Behringer, 2002; Goebbels et al., 2006; Sie…”
BackgroundEMT and Stemness—Key Players in Pancreatic Cancer Stem Cells
Rodríguez-Aznar, E., Wiesmüller, L., Sáinz, B., & Hermann, P. C. (2019) · Cancers · doi:10.3390/cancers11081136 · Cited by 99
Wiebe, P. O., Kormish, J., Roper, V. T., Fujitani, Y., Alston, N., Zaret, K., Wright, C., Stein, R., & Gannon, M. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.01978-06 · Cited by 93
“In Ptf1a null mice, Pdx1 expression is maintained in the dorsal pancreas (23).”
BackgroundInfluentialSelf-citationInhibition of Mist1 Homodimer Formation Induces Pancreatic Acinar-to-Ductal Metaplasia
Zhu, L., Tran, T., Rukstalis, J. M., Sun, P., Damsz, B., & Konieczny, S. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.7.2673-2681.2004 · Cited by 93
“Recent genetic studies by Kawaguchi et al. ( 19 ) have shown that Ptf1a expression is also associated with pancreatic progenitor cells that are capable of generating all three cell lineages (endocrine, exocrine, and duct), providing intriguing new evidence that Ptf1a may have additional roles in regulating endocrine a…”
BackgroundPancreas specification: a budding question
Kumar, M. E. (2003) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(03)00089-3 · Cited by 94
Zhong, F., & Jiang, Y. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00101 · Cited by 114
DOSAGE-DEPENDENT REGULATION OF PANCREATIC CANCER GROWTH AND ANGIOGENESIS BY HEDGEHOG SIGNALING
Mathew, E., Zhang, Y.-Q., Holtz, A., Kane, K. T., Song, J. Y., Allen, B. L., & di Magliano, M. P. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.09.010 · Cited by 92
“Ptf1a-Cre mice (Kawaguchi et al., 2002) were intercrossed with LSL-KrasG12D (Hingorani et al., 2003) to generate Ptf1a-Cre;LSL-KrasG12D (KC) animals.”
MethodAnnicotte, J., Fayard, E., Swift, G. H., Selander, L., Edlund, H., Tanaka, T., Kodama, T., Schoonjans, K., & Auwerx, J. H. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.19.6713-6724.2003 · Cited by 92
“It is also interesting that the basic helix-loop-helix transcription factor Ptf1a, which was first described as an exocrine-specific protein involved in exocrine pancreatic development and islet architecture (28), was recently shown to be crucial to orient undifferentiated foregut endoderm into the pancreatic fate (27…”
BackgroundSOX9 in organogenesis: shared and unique transcriptional functions
Ming, Z., Vining, B., Bagheri‐Fam, S., & Harley, V. R. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04543-4 · Cited by 100
“Repression of hepatic and intestinal genes [95, 96, 100] CDX2 [100]/Cdx2 [100], ONECUT-2 [100]/Onecut-2 [100], NKX6-3 [100]/Nkx6.”
BackgroundPinho, A. V., Rooman, I., & Real, F. (2011) · Cell Cycle · doi:10.4161/cc.10.8.15363 · Cited by 91
“For lineage tracing, Ptf1a;R26R-LSLEYFP;p53 mice were used.(51,52) All experiments were performed in accordance with institutional ethical committees and national guidelines and regulations.”
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Attali, M., Stetsyuk, V., Basmaciogullari, A., Aiello, V., Zanta-Boussif, M., Duvillié, B., & Scharfmann, R. (2007) · Diabetes · doi:10.2337/db06-1307 · Cited by 91
“At this early stage, FGF10 treatment of dorsal pancreatic endoderm explants was sufficient to increase the expression of Ptf1a, a transcription factor needed to complete pancreatic specification (36,37).”
BackgroundKimura, Y., Fukuda, A., Ogawa, S., Maruno, T., Takada, Y., Tsuda, M., Hiramatsu, Y., Araki, O., Nagao, M., Yoshikawa, T., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.03.039 · Cited by 90
Self-citationIsolation, culture and genetic manipulation of mouse pancreatic ductal cells
Reichert, M., Takano, S., Heeg, S., Bakir, B. S., Botta, G., & Rustgi, A. (2013) · Nature Protocols · doi:10.1038/nprot.2013.079 · Cited by 89
Transcriptional Maintenance of Pancreatic Acinar Identity, Differentiation, and Homeostasis by PTF1A
Hoàng, C., Hale, M. A., Azevedo-Pouly, A., Elsässer, H., Deering, T. G., Willet, S. G., Pan, F. C., Magnuson, M., Wright, C., Swift, G. H., et al. (2016) · Molecular and Cellular Biology · doi:10.1128/mcb.00358-16 · Cited by 87
“commitment to pancreatic fate (12), including the formation of”
BackgroundSelf-citationShih, H., Seymour, P. A., Patel, N., Xie, R., Wang, A., Liu, P. P., Yeo, G. W., Magnuson, M., & Sander, M. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.08.082 · Cited by 87
“Previous studies have shown that a subset of normally pancreas-fated cells adopt intestinal identity in Ptf1a null mutant mice (Kawaguchi et al., 2002).”
InfluentialConditional ablation of Notch signaling in pancreatic development
Nakhai, H., Siveke, J. T., Klein, B., Mendoza-Torres, L., Mazur, P. K., Algül, H., Radtke, F., Strobl, L. J., Zimber‐Strobl, U., & Schmid, R. M. (2008) · Development · doi:10.1242/dev.013722 · Cited by 87
“5 in all pancreatic epithelial cells, similar 2763RESEARCH ARTICLEConditional ablation of Notch D E V E LO P M E N T 2764 to that previously reported (Fujikura et al., 2007; Kawaguchi et al., 2002).”
MethodResultTranscription factors define the neuroanatomical organization of the medullary reticular formation
Gray, P. A. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00007 · Cited by 78
“We employed Atoh1βgal/+ (Atoh1-βgal) (Ben-Arie et al., 1997), Atoh1-Cre (Chen et al., 2002), Dbx1βgal/+ (Dbx1-βgal) (Pierani et al., 2001), Gad1-GFP transgenic (Chattopadhyaya et al., 2004), Lmx1b βgal/+ (Lmx1b-βgal) (Pressman et al., 2000), Ptf1aCre/+ (Kawaguchi et al., 2002), Rosa26-EYFP (Srinivas et al., 2001), and…”
SWI/SNF component ARID1A restrains pancreatic neoplasia formation
Wang, S. C., Nassour, I., Xiao, S., Zhang, S., Luo, X., Lee, J., Li, L., Sun, X., Nguyen, L. H., Chuang, J.-C., et al. (2019) · Gut · doi:10.1136/gutjnl-2017-315490 · Cited by 85
Xiao, D., Liu, X., Zhang, M., Zou, M., Deng, Q., Sun, D., Bian, X., Cai, Y., Guo, Y., Liu, S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05209-1 · Cited by 88
Seto, Y., Nakatani, T., Masuyama, N., Taya, S., Kumai, M., Minaki, Y., Hamaguchi, A., Inoue, Y., Inoue, T., Miyashita, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4337 · Cited by 85
Self-citationDong, P., Provost, E., Leach, S., & Stainier, D. (2008) · Genes & Development · doi:10.1101/gad.1663208 · Cited by 85
“Down-regulation of Ptf1a in exocrine cell culture was shown to disrupt the exocrine differentiated state (Krapp et al. 1996).”
BackgroundNgn3+ endocrine progenitor cells control the fate and morphogenesis of pancreatic ductal epithelium
Magenheim, J., Klein, A. M., Stanger, B., Ashery-Padan, R., Sosa-Pineda, B., Gu, G.-Q., & Dor, Y. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.08.006 · Cited by 84
“However, it is now clear that during development, a common group of multipotent progenitor cells in the embryonic gut, expressing specific markers such as Foxa1, Foxa2, Pdx1, Ptf1a and Sox9, give rise to both the endocrine and exocrine pancreas (Burlison et al., 2008; Gao et al., 2008; Gu et al., 2002; Kawaguchi et al…”
BackgroundLardon, J., Breuck, S. D., Rooman, I., van Lommel, L., Kruhøffer, M., Ørntoft, T., Schuit, F., & Bouwens, L. (2004) · Hepatology · doi:10.1002/hep.20213 · Cited by 84
Notch-mediated patterning and cell fate allocation of pancreatic progenitor cells
Afelik, S., Qu, X., Hasrouni, E., Bukys, M. A., Deering, T. G., Nieuwoudt, S., Rogers, W., MacDonald, R. J., & Jensen, J. N. (2012) · Development · doi:10.1242/dev.075804 · Cited by 79
“These early multipotent progenitor cells are marked by the expression of Pdx1 and Ptf1a, both of which are required for pancreatic fate specification (Afelik et al., 2006; Burlison et al., 2008; Kawaguchi et al., 2002).”
BackgroundSelf-citationBeneficial effects of prolactin and laminin on human pancreatic islet-cell cultures
Labriola, L., Montor, W. R., Krogh, K., Lojudice, F. H., Genzini, T., Goldberg, A. C., Eliaschewitz, F. G., & Sogayar, M. C. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.09.011 · Cited by 87
Asayesh, A., Sharpe, J. A., Watson, R. P., Hecksher‐Sørensen, J., Hastie, N. D., Hill, R. E., & Ahlgren, U. (2006) · Genes & Development · doi:10.1101/gad.381906 · Cited by 76
“2002) and appears to be an important step in lineage determination in favor of a pancreatic as opposed to a duodenal fate (Kawaguchi et al. 2002).”
BackgroundInfluentialNagaya, M., Katsuta, H., Kaneto, H., Bonner-Weir, S., & Weir, G. (2009) · Journal of Endocrinology · doi:10.1677/joe-08-0482 · Cited by 79
“Recent reports find thatPtf1a is expressed in the progenitors of pancreatic ducts, exocrine, and endocrine cells, rather than being an exocrine-specific gene as previously thought (Kawaguchi et al. 2002).”
BackgroundHNF1A recruits KDM6A to activate differentiated acinar cell programs that suppress pancreatic cancer
Kalisz, M., Bernardo, E., Beucher, A., Maestro, M. A., del Pozo, N., Millán, I., Haeberle, L., Schlensog, M., Safi, S. A., Knoefel, W. T., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019102808 · Cited by 77
“Four or three pancreases from, respectively, 4-day-old or adult female mice of each genotype were analyzed: Kdm6aLoxP/LoxP and Pdx1Cre; Kdm6aLoxP/LoxP or Ptf1aCre and Ptf1aCre;Hnf1aLoxP/LoxP.”
Ptf1a-mediated control of Dll1 reveals an alternative to the lateral inhibition mechanism
Ahnfelt-Rønne, J., Jørgensen, M. C., Klinck, R., Jensen, J., Füchtbauer, E., Deering, T. G., MacDonald, R. J., Wright, C. V., Madsen, O., & Serup, P. (2012) · Development · doi:10.1242/dev.071761 · Cited by 77
“…(Dll1lacZ/+) (Hrabe de Angelis et al., 1997), Tg(Hes1-EGFP)1Hri BAC transgenic (Klinck et al., 2011), Neurog3tTA/+ (Wang et al., 2009), Ptf1aCre/+ (Kawaguchi et al., 2002) and Hes1+/– (Ishibashi et al., 1995) mouse lines were all kept as heterozygotes and genotyped by PCR and Southern blotting as…”
BackgroundMethodInfluentialSelf-citationMouse models of pancreatic cancer
Leach, S. D. (2004) · Cancer Cell · doi:10.1016/s1535-6108(03)00337-4 · Cited by 72
A smad signaling network regulates islet cell proliferation
El-Gohary, Y., Tulachan, S., Wiersch, J., Guo, P., Welsh, C., Prasadan, K., Paredes, J., Shiota, C., Xiao, X., Wada, Y., et al. (2014) · Diabetes · doi:10.2337/db13-0432 · Cited by 77
“However, we feel that such a non–cell-autonomous mechanism is less likely since in the PTF1a-cre;smad7fx/fx;R26R-lsl-lacZ islets that showed a mosaic penetration of cre recombination in islet cells, non–cre-recombined cells were found to be the predominant cells that were BrdU+ (Fig.”
BackgroundInfluentialSenescence-associated SIN3B promotes inflammation and pancreatic cancer progression
Rielland, M., Cantor, D. J., Graveline, R., Hajdu, C., Mara, L., de Diego Diaz, B., Miller, G., & David, G. (2014) · Journal of Clinical Investigation · doi:10.1172/jci72619 · Cited by 76
“org Volume 124 Number 5 May 2014 tional allele were first crossed with transgenic mice expressing the Cre recombinase under the control of the pancreas-specific p48 promoter (35, 36).”
Wang, Z., Hausmann, S., Lyu, R., Li, T., Lofgren, S., Flores, N. M., Fuentes, M. E., Caporicci, M., Yang, Z., Meiners, M. J., et al. (2020) · Cancer Cell · doi:10.1016/j.ccell.2020.04.014 · Cited by 98
“EXPERIMENTAL MODEL AND SUBJECT DETAILS Mice—Ptf1a+/Cre, Pdx1Flp, Kras+/LSL-G12D, Kras+FSF-G12D, p53LoxP/LoxP, p53Frt/Frt, Rosa26FSF-CreER mice have been described before (Hingorani et al., 2003; Jonkers et al., 2001; Kawaguchi et al., 2002; Lee et al., 2012) (Schonhuber et al.”
BackgroundPrdm13 mediates the balance of inhibitory and excitatory neurons in somatosensory circuits
Chang, J. C., Meredith, D., Mayer, P. R., Borromeo, M. D., Lai, H., Ou, Y.-H., & Johnson, J. E. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.02.015 · Cited by 76
“Ptf1aCre (p48Cre), where the Ptf1a coding region is replaced by that coding for Cre recombinase was used as the Ptf1a null (Kawaguchi et al., 2002).”
MethodNeuronal Ig/Caspr Recognition Promotes the Formation of Axoaxonic Synapses in Mouse Spinal Cord
Ashrafi, S., Betley, J. N., Comer, J. D., Brenner‐Morton, S., Bar, V., Shimoda, Y., Watanabe, K., Peles, E., Jessell, T. M., & Kaltschmidt, J. A. (2014) · Neuron · doi:10.1016/j.neuron.2013.10.060 · Cited by 75
“YFP-directed fluorescent protein (YFP) (Buffelli et al., 2003; Kawaguchi et al., 2002) was expressed in 70% of GAD65 GABApre terminals and was largely excluded from GABApost terminals that form contacts on motor neurons (Betley et al.”
BackgroundInfluentialA modular and flexible ESC-based mouse model of pancreatic cancerPreprint
Saborowski, M., Saborowski, A., Morris, J. P., Bosbach, B., Dow, L. E., Pelletier, J., Klimstra, D., & Lowe, S. (2014) · Genes & Development · doi:10.1101/gad.232082.113 · Cited by 75
“Pdx1-Cre (Hingorani et al. 2003), p48-Cre (Kawaguchi et al. 2002), LSLKrasG12D (Jackson et al. 2001), LSL-p53R172H (Olive et al. 2004), CHC (Beard et al. 2006), and CAGs-LSL-RIK strains (LE Dow, Z Nasr, M Saborowski, SH Ebbesen, E Manchado, N Tasdemir, J Pelletier, and SW Lowe, in prep.) were…”
BackgroundInfluentialExocrine ontogenies: On the development of pancreatic acinar, ductal and centroacinar cells
Cleveland, M. H., Sawyer, J. M., Afelik, S., Jensen, J. N., & Leach, S. D. (2012) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2012.06.008 · Cited by 84
“While the common origin of both endocrine and exocrine cell types from pools of progenitor cells expressing these transcription factors has been indisputably established by Cre/lox-based lineage tracing strategies [35, 37, 81, 83, 84], it should be stressed that unlike imaging- and transplantation-based lineage-tracin…”
BackgroundMARSTRAND-DAUCE, L., Lorenzo, D., Chassac, A., Nicole, P., Couvelard, A., & Haumaître, C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24129946 · Cited by 105
“Hnf6 is also expressed in MPCs [49].”
BackgroundInfluentialShi, C.-J., Washington, M., Chaturvedi, R., Drosos, Y., Revetta, F. L., Weaver, C. J., Buzhardt, E., Yull, F. E., Blackwell, T. S., Sosa-Pineda, B., et al. (2014) · Laboratory Investigation · doi:10.1038/labinvest.2014.10 · Cited by 74
“Ptf1aCre (7), LSL-KrasG12D (8), and Cdkn2a+/- (9) mice have all been described.”
BackgroundPax6 is regulated by Meis and Pbx homeoproteins during pancreatic development.
Zhang, X., Rowan, S., Yue, Y., Heaney, S., Pan, Y.-W., Brendolan, A., Selleri, L., & Maas, R. (2006) · Developmental Biology · doi:10.1016/j.ydbio.2006.06.030 · Cited by 74
“These results confirm a previous demonstration that Pbx1 is required for proper pancreatic development (Kim et al., 2002) but additionally demonstrate that Pbx1 is required at 14.5 for the maintenance of pancreatic Pax6 expression.”
BackgroundResultInfluentialRen, L., Liu, C., Çifcibaşı, K., Ballmann, M., Rammes, G., Reyes, C. M., Tokalov, S. V., Klingl, A., Grünert, J., Goyal, K., et al. (2025) · Cancer Cell · doi:10.1016/j.ccell.2025.09.003 · Cited by 82
Reduction of Ptf1a Gene Dosage Causes Pancreatic Hypoplasia and Diabetes in Mice
Fukuda, A., Kawaguchi, Y., Furuyama, K., Kodama, S., Horiguchi, M., Kuhara, T., Kawaguchi, M., Terao, M., Doi, R., Wright, C., et al. (2008) · Diabetes · doi:10.2337/db07-1558 · Cited by 73
“We crossed Ptf1a and Ptf1a with Gt(ROSA)26Sor (R26r) mice, which carry a floxed lacZ gene driven by cell type–independent ROSA promoter (15), enabling us to trace the fate of all Ptf1aexpressing cells and their progeny (8).”
BackgroundMethodInfluentialSelf-citationRukstalis, J. M., Kowalik, A., Zhu, L., Lidington, D., Pin, C., & Konieczny, S. (2003) · Journal of Cell Science · doi:10.1242/jcs.00631 · Cited by 73
“Similarly, targeted disruption of the exocrine-specific factor PTF1-p48 results in a complete lack of exocrine cells within the pancreas, causing early postnatal death (Kawaguchi et al., 2002; Krapp et al., 1998).”
BackgroundmTORC2 Signaling Drives the Development and Progression of Pancreatic Cancer
Driscoll, D. R., Karim, S. A., Sano, M., Gay, D. M., Jacob, W., Yu, J. Q., Mizukami, Y., Gopinathan, A., Jodrell, D. I., Evans, T. R. J., et al. (2016) · Cancer Research · doi:10.1158/0008-5472.can-16-0810 · Cited by 78
“Loss of Rictor does not impair pancreas differentiation To determine the impact of mTORC2 inactivation on pancreas development, we generated mice lacking the essential mTORC2 subunit Rictor, specifically within the pancreas, by crossing mice bearing Ptf1a-cre and Rictorflox alleles (24,25) (Figure S1A).”
BackgroundTranscription factor regulation of pancreatic organogenesis, differentiation and maturation
Dassaye, R., Naidoo, S., & Cerf, M. E. (2015) · Islets · doi:10.1080/19382014.2015.1075687 · Cited by 80
Mastracci, T. L., Wilcox, C. L., Arnes, L., Panea, C., Golden, J. A., May, C. L., & Sussel, L. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.08.001 · Cited by 54
“Cells within this pancreatic domain that express the transcription factors Pdx1 and Ptf1a delineate the pancreatic progenitor population (Burlison et al., 2008; Kawaguchi et al., 2002; Offield et al., 1996).”
The molecular basis of transdifferentiation
Li, W.-C., Yu, W.-Y., Quinlan, J., Burke, Z., & Tosh, D. (2005) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2005.tb00489.x · Cited by 71
Progenitor cells in the adult pancreas
Holland, A. M., Gonez, L. J., & Harrison, L. (2004) · Diabetes/Metabolism Research Reviews · doi:10.1002/dmrr.430 · Cited by 71
“The ability to accurately identify parental cells and follow the differentiation of their progeny with the use of molecular tools such as fluorescent proteins and inducible gene expression systems [23,50,51] should aid in identifying pancreatic progenitors.”
BackgroundInfluentialWang, W., Friedland, S. C., Guo, B., O’Dell, M. R., Alexander, W. B., Whitney‐Miller, C. L., Agostini‐Vulaj, D., Huber, A. R., Myers, J. R., Ashton, J. M., et al. (2018) · Gut · doi:10.1136/gutjnl-2017-315541 · Cited by 96
Guney, M. A., & Gannon, M. (2009) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20156 · Cited by 70
“Lineage tracing analysis showed that Ptf1a-expressing progenitors give rise to all of the cell types in the pancreas (Kawaguchi et al., 2002).”
BackgroundInfluentialSelf-citationHald, J., Sprinkel, A., Ray, M., Serup, P., Wright, C., & Madsen, O. (2008) · Journal of Histochemistry and Cytochemistry · doi:10.1369/jhc.2008.950675 · Cited by 70
Self-citationReciprocal endoderm-mesoderm interactions mediated by fgf24 and fgf10 govern pancreas development
Manfroid, I., Delporte, F., Baudhuin, A., Motte, P., Neumann, C., Voz, M., Martial, J., & Peers, B. (2007) · Development · doi:10.1242/dev.007823 · Cited by 70
“Pdx1 and Ptf1a are among the first markers of the pancreatic commitment (Kawaguchi et al., 2002; Jonsson et al., 1994).”
BackgroundDoyle, M. J., Loomis, Z. L., & Sussel, L. (2007) · Development · doi:10.1242/dev.02763 · Cited by 81
“…are the earliestknown factors in the pancreatic progenitors, and Ngn3 (also known as Neurog3 – Mouse Genome Informatics) is essential for further specifying the endocrine progenitors (Gradwohl et al., 2000; Jonsson et al., 1994; Kawaguchi et al., 2002; Matsuoka et al., 2004; Offield et al., 1996).”
BackgroundSilva, I. B. B., Kimura, C. H., Colantoni, V. P., & Sogayar, M. C. (2022) · Stem Cell Research & Therapy · doi:10.1186/s13287-022-02977-y · Cited by 99
Pax4 acts as a key player in pancreas development and plasticity.
Napolitano, T., Avolio, F., Courtney, M., Vieira, A., Druelle, N., Ben-Othman, N., Hadzic, B., Navarro, S., & Collombat, P. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.08.013 · Cited by 68
Watanabe, S., Sanuki, R., Sugita, Y., Imai, W., Yamazaki, R., Kozuka, T., Ohsuga, M., & Furukawa, T. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0089-15.2015 · Cited by 68
Two sides of the story? Smad4 loss in pancreatic cancer versus head-and-neck cancer
Malkoski, S., & Wang, X.-J. (2012) · FEBS Letters · doi:10.1016/j.febslet.2012.01.054 · Cited by 68
“colon cancer, targeted Smad4 deletion to the pancreas did not initiate pancreatic cancer [24,25], perhaps because Smad4 does not regulate Fanc/Brca genes in simple epithelium; a hypothesis is supported by the observation that Smad4 / pancreatic tumors did not exhibit genomic instability [27].”
BackgroundPancreatic cell lineage analyses in mice
Herrera, P., Népote, V., & Delacour, A. (2002) · Endocrine · doi:10.1385/endo:19:3:267 · Cited by 68
Mahadevan, K. K., LeBleu, V. S., Ramirez, E. V., Chen, Y., Li, B., Sockwell, A. M., Gagea, M., Sugimoto, H., Sthanam, L. K., Tampe, D., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.07.025 · Cited by 76
Li, J., Wu, X., Zhou, Y., Lee, M., Guo, L., Han, W., Mo, W., Cao, W., Sun, D., Xie, R., et al. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky063 · Cited by 69
“A notable example is illustrated in Figure 2E with a focus on the epigenetic changes at the distal regulatory region of a gene encoding pancreas transcription factor 1 (PTF1A), which is known to be essential for pancreatic organogenesis (51,52).”
BackgroundTranscriptional control of mammalian pancreas organogenesis
Cano, D. A., Soria, B., Martín, F., & Rojas, A. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1510-2 · Cited by 67
Notch signaling in the pancreas: patterning and cell fate specification
Afelik, S., & Jensen, J. (2013) · Wiley Interdisciplinary Reviews: Developmental Biology · doi:10.1002/wdev.99 · Cited by 67
Molecular machinery governing GABAergic neuron specification in the cerebellum
Hoshino, M. (2008) · Cerebellum · doi:10.1080/14734220600589202 · Cited by 67
“Because the Ptf1a allele was generated by the replacement of the Ptf1a protein-encoding genomic region with a Cre recombinase-encoding cDNA (28), lineage tracing can be done by crossing these mice with Gt(ROSA)26Sor (R26R) mice which carry a modified lacZ gene driven by the cell typeindependent ROSA26 promoter (29).”
BackgroundHalbrook, C., Wen, H.-J., Ruggeri, J. M., Takeuchi, K. K., Zhang, Y.-Q., di Magliano, M. P., & Crawford, H. (2016) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2016.09.009 · Cited by 66
“Methods Mouse Strains Ptf1aCre/þ and shRen713 mice have been previously described.(41,42) The shMapk2k1 and shMap2k2 mice were generated by Mirimus Inc (Cold Spring Harbor, NY) on a mixed background and contained a ROSA26-CAG-LSL-rtTA(3)-IRES-mKate2 reverse tetracycline transactivator.”
MethodOrvis, G. D., Hartzell, A. L., Smith, J., Barraza, L., Wilson, S. L., Szulc, K., Turnbull, D., & Joyner, A. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.04.018 · Cited by 66
“The VZ expresses the pancreas transcription factor 1 alpha gene (Ptf1a) and gives rise to gamma-aminobutyric acid (GABAergic) interneurons, Purkinje cells and all glia, whereas the RL expresses Atoh1 and produces all glutamatergic neurons including those of the deep cerebellar nuclei (DCN) and granule cells (gcs) of t…”
InfluentialHistorical Perspective: Beginnings of the β-Cell
Seymour, P. A., & Sander, M. (2011) · Diabetes · doi:10.2337/db10-1068 · Cited by 66
Spence, J. R., & Wells, J. M. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21366 · Cited by 64
“For example, it is thought that all pancreatic cell types transition through a Pdx1 and a Ptf1a/p48 stage during development (Gu et al., 2002; Kawaguchi et al., 2002) and that all endocrine cells are derived from a Ngn3 progenitor cell (Gu et al.”
BackgroundSantana-Codina, N., del Rey, M. Q., Kapner, K. S., Zhang, H., Gikandi, A., Malcolm, C., Poupault, C. L., Kuljanin, M., John, K. M., Biancur, D. E., et al. (2022) · Cancer Discovery · doi:10.1158/2159-8290.cd-22-0043 · Cited by 182
Zebrafish mnx genes in endocrine and exocrine pancreas formation.
Wendik, B., Maier, E. C., & Meyer, D. (2004) · Developmental Biology · doi:10.1016/j.ydbio.2003.12.026 · Cited by 65
Metadata
- Authors
- Kawaguchi, Y., Cooper, B., Gannon, M., Ray, M., MacDonald, R. J., & Wright, C. V. E.
- Affiliations
- Vanderbilt University (US)
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Wright, Christopher V.E.
- Venue
- Nature Genetics
- Published
- 2002-08-19
- Volume
- 32
- Issue
- 1
- Pages
- 128-134
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W1993055783
- Cited by
- 1,007
- References
- 26
- Citations by year
- 2026: 18 · 2025: 30 · 2024: 18 · 2023: 39 · 2022: 23 · 2021: 39 · 2020: 39 · 2019: 44 · 2018: 43 · 2017: 44 · 2016: 44 · 2015: 62 · 2014: 54 · 2013: 65 · 2012: 68
- FWCI
- 35.56
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Keywords
- Ptf1a, pancreatic development, foregut endoderm, pancreatic progenitors, duodenal epithelium, pancreatic stem cells, PDX1, cis-regulatory sequences, lineage tracing, organogenesis
- MeSH terms
- Animals, Cell Differentiation, Duodenum, Gene Expression Regulation, Pancreas, Transcription Factors, Trans-Activators, Homeodomain Proteins, Cell Lineage, Animals, Genetically Modified, Mice
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