Differential regulation of two histidine ammonia-lyase genes during Xenopus development implicates distinct functions during thyroid hormone-induced formation of adult stem cells

Cell & Bioscience

Guihong Sun¹  Yun-Bo Shi²  Kenta Fujimoto³  Liezhen Fu²  Luan Wen²  Nga Luu² 

[1] School of Basic Medical Sciences, Wuhan University, 430072 Wuhan, P.R. China;Section on Molecular Morphogenesis, Program in Cellular Regulation and Metabolism (PCRM), Eunice Kennedy Shriver National Institute of Child Health and Human Development (NICHD), National Institutes of Health (NIH), 18 Library Dr., 20892 Bethesda, Maryland, USA;Present address: Division of Gene Structure and Function, Research Center for Genomic Medicine, Saitama Medical University, 1397-1 Yamane, 350-1241 Hidaka-shi, Saitama, Japan

关键词: Histidase;    Intestine;    Stem cells;    Thyroid hormone receptor;    Xenopus;    Metamorphosis;    Thyroid hormone;   

Others  :  791448
DOI  :  10.1186/2045-3701-3-43

 received in 2013-09-23, accepted in 2013-10-30,  发布年份 2013

【 摘 要 】

Background

Organ-specific, adult stem cells are essential for organ-homeostasis and tissue repair and regeneration. The formation of such stem cells during vertebrate development remains to be investigated. Frog metamorphosis offers an excellent opportunity to study the formation of adult stem cells as this process involves essentially the transformations of all larval tissues/organs into the adult form. Of particular interest is the remodeling of the intestine. Early studies in Xenopus laevis have shown that this process involves complete degeneration of the larval epithelium and de novo formation of adult stem cells through dedifferentiation of some larval epithelial cells. A major advantage of this metamorphosis model is its total dependence on thyroid hormone (T3). In an effort to identify genes that are important for stem cell development, we have previously carried out tissue-specific microarray analysis of intestinal gene expression during Xenopus laevis metamorphosis.

Results

We report the detailed characterization of one of the genes thus identified, the histidine ammonia-lyase (HAL) gene, which encodes an enzyme known as histidase or histidinase. We show that there are two duplicated HAL genes, HAL1 and HAL2, in both Xenopus laevis and Xenopus tropicalis, a highly related but diploid species. Interestingly, only HAL2 is highly upregulated by T3 and appears to be specifically expressed in the adult intestinal progenitor/stem cells while HAL1 is not expressed in the intestine during metamorphosis. Furthermore, when analyzed in whole animals, HAL1 appears to be expressed only during embryogenesis but not metamorphosis while the opposite appears to be true for HAL2.

Conclusions

Our results suggest that the duplicated HAL genes have distinct functions with HAL2 likely involved in the formation and/or proliferation of the adult stem cells during metamorphosis.

【 授权许可】

   
2013 Luu et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]MacDonald WC, Trier JS, Everett NB: Cell proliferation and migration in the stomach, duodenum, and rectum of man: Radioautographic studies. Gastroenterology 1964, 46:405-417.
• [2]Toner PG, Carr KE, Wyburn GM: The Digestive System: An Ultrastructural Atlas and Review. London: Butterworth; 1971.
• [3]van der Flier LG, Clevers H: Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009, 71:241-260.
• [4]Shi YB, Hasebe T, Fu L, Fujimoto K, Ishizuya-Oka A: The development of the adult intestinal stem cells: Insights from studies on thyroid hormone-dependent amphibian metamorphosis. Cell Biosci 2011, 1:30. BioMed Central Full Text
• [5]Ishizuya-Oka A, Shi YB: Evolutionary insights into postembryonic development of adult intestinal stem cells. Cell Biosci 2011, 1:37. BioMed Central Full Text
• [6]Cheng H, Leblond CP: Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Entero-endocrine cells. Am J Anat 1974, 141:503-519.
• [7]Sun G, Shi Y-B: Thyroid hormone regulation of adult intestinal stem cell development: mechanisms and evolutionary conservations. Int J Biol Sci 2012, 8:1217-1224.
• [8]McAvoy JW, Dixon KE: Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adult Xenopus laevis. J Exp Zool 1977, 202:129-138.
• [9]Sancho E, Eduard Batlle E, Clevers H: Signaling pathways in intestinal development and cancer. Annu Rev Cell DevBiol 2004, 20:695-723.
• [10]Harper J, Mould A, Andrews RM, Bikoff EK, Robertson EJ: The transcriptional repressor Blimp1/Prdm1 regulates postnatal reprogramming of intestinal enterocytes. Proc Natl Acad Sci U S A 2011, 108:10585-10590.
• [11]Kress E, Rezza A, Nadjar J, Samarut J, Plateroti M: The frizzled-related sFRP2 gene is a target of thyroid hormone receptor alpha1 and activates beta-catenin signaling in mouse intestine. J Biol Chem 2009, 284:1234-1241.
• [12]Plateroti M, Gauthier K, Domon-Dell C, Freund JN, Samarut J, Chassande O: Functional interference between thyroid hormone receptor alpha (TRalpha) and natural truncated TRDeltaalpha isoforms in the control of intestine development. Mol Cell Biol 2001, 21:4761-4772.
• [13]Flamant F, Poguet AL, Plateroti M, Chassande O, Gauthier K, Streichenberger N, Mansouri A, Samarut J: Congenital hypothyroid Pax8(-/-) mutant mice can be rescued by inactivating the TRalpha gene. Mol Endocrinol 2002, 16:24-32.
• [14]Plateroti M, Chassande O, Fraichard A, Gauthier K, Freund JN, Samarut J, Kedinger M: Involvement of T3Ralpha- and beta-receptor subtypes in mediation of T3 functions during postnatal murine intestinal development. Gastroenterology 1999, 116:1367-1378.
• [15]Muncan V, Heijmans J, Krasinski SD, Buller NV, Wildenberg ME, Meisner S, Radonjic M, Stapleton KA, Lamers WH, Biemond I, et al.: Blimp1 regulates the transition of neonatal to adult intestinal epithelium. Nat Commun 2011, 2:452.
• [16]Heimeier RA, Das B, Buchholz DR, Fiorentino M, Shi YB: Studies on Xenopus laevis intestine reveal biological pathways underlying vertebrate gut adaptation from embryo to adult. Genome Biol 2010, 11:R55. BioMed Central Full Text
• [17]Tata JR: Gene expression during metamorphosis: an ideal model for post-embryonic development. Bioessays 1993, 15:239-248.
• [18]Shi Y-B: Amphibian metamorphosis: from morphology to molecular biology. New York: John Wiley & Sons, Inc; 1999.
• [19]Shi Y-B, Ishizuya-Oka A: Biphasic intestinal development in amphibians: embryogensis and remodeling during metamorphosis. Current Topics in Develop Biol 1996, 32:205-235.
• [20]Ishizuya-Oka A, Shimozawa A: Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis in vitro. Roux’s Arch Dev Biol 1992, 201:322-329.
• [21]Ishizuya-Oka A, Shimozawa A: Inductive action of epithelium on differentiation of intestinal connective tissue of Xenopus laevis tadpoles during metamorphosis in vitro. Cell Tissue Res 1994, 277:427-436.
• [22]Hasebe T, Fu L, Miller TC, Zhang Y, Shi YB, Ishizuya-Oka A: Thyroid hormone-induced cell-cell interactions are required for the development of adult intestinal stem cells. Cell Biosci 2013, 3:18. BioMed Central Full Text
• [23]Schreiber AM, Mukhi S, Brown DD: Cell-cell interactions during remodeling of the intestine at metamorphosis in Xenopus laevis. Dev Biol 2009, 331:89-98.
• [24]Schreiber AM, Cai L, Brown DD: Remodeling of the intestine during metamorphosis of Xenopus laevis. Proc Natl Acad Sci U S A 2005, 102:3720-3725.
• [25]Ishizuya-Oka A, Hasebe T, Buchholz DR, Kajita M, Fu L, Shi YB: Origin of the adult intestinal stem cells induced by thyroid hormone in Xenopus laevis. Faseb J 2009, 23:2568-2575.
• [26]Hasebe T, Buchholz DR, Shi YB, Ishizuya-Oka A: Epithelial-connective tissue interactions induced by thyroid hormone receptor are essential for adult stem cell development in the Xenopus laevis intestine. Stem Cells 2011, 29:154-161.
• [27]Sun G, Heimeier RA, Fu L, Hasebe T, Das B, Ishizuya-Oka A, Shi Y-B: Expression profiling of intestinal tissues implicates tissue-specific genes and pathways essential for thyroid hormone-induced adult stem cell development. Endocrinology 2013, 154(11):4396-4407.
• [28]Kawai Y, Moriyama A, Asai K, Coleman-Campbell CM, Sumi S, Morishita H, Suchi M: Molecular characterization of histidinemia: identification of four missense mutations in the histidase gene. Hum Genet 2005, 116:340-346.
• [29]Suchi M, Harada N, Wada Y, Takagi Y: Molecular cloning of a cDNA encoding human histidase. Biochim Biophys Acta 1993, 1216:293-295.
• [30]Suchi M, Sano H, Mizuno H, Wada Y: Molecular cloning and structural characterization of the human histidase gene (HAL). Genomics 1995, 29:98-104.
• [31]Taylor RG, Levy HL, McInnes RR: Histidase and histidinemia. Clinical and molecular considerations. Mol Biol Med 1991, 8:101-116.
• [32]Bulfield G, Kacser H: Histidinaemia in mouse and man. Arch Dis Child 1974, 49:545-552.
• [33]Kuroda Y, Ogawa T, Ito M, Watanabe T, Takeda E, Toshima K, Miyao M: Relationship between skin histidase activity and blood histidine response to histidine intake in patients with histidinemia. J Pediatr 1980, 97:269-272.
• [34]Auerbach VH, Digeorge AM, Baldridge RC, Tourtellotte CD, Brigham MP: Histidinemia. A deficiency in histidase resulting in the urinary excretion of histidine and of imidazolepyruvic acid. J Pediatr 1962, 60:487-497.
• [35]Kacser H, Mya KM, Duncker M, Wright AF, Bulfield G, McLaren A, Lyon MF: Maternal histidine metabolism and its effect on foetal development in the mouse. Nature 1977, 265:262-266.
• [36]Ishizuya-Oka A, Ueda S: Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res 1996, 286:467-476.
• [37]Fujimoto K, Matsuura K, Das B, Fu L, Shi YB: Direct activation of xenopus iodotyrosine deiodinase by thyroid hormone receptor in the remodeling intestine during amphibian metamorphosis. Endocrinol 2012, 153:5082-5089.
• [38]Matsuura K, Fujimoto K, Das B, Fu L, Lu CD, Shi YB: Histone H3K79 methyltransferase Dot1L is directly activated by thyroid hormone receptor during Xenopus metamorphosis. Cell Biosci 2012, 2:25. BioMed Central Full Text
• [39]Sterling J, Fu L, Matsuura K, Shi Y-B: Cytological and morphological analyses reveal distinct features of intestinal development during Xenopus tropicalis metamorphosis. PLoS One 2012, 7(e47407):47401-47410.
• [40]Wang X, Matsuda H, Shi Y-B: Developmental regulation and function of thyroid hormone receptors and 9-cis retinoic acid receptors during Xenopus tropicalis metamorphosis. Endocrinology 2008, 149:5610-5618.
• [41]Das B, Heimeier RA, Buchholz DR, Shi YB: Identification of direct thyroid hormone response genes reveals the earliest gene regulation programs during frog metamorphosis. J Biol Chem 2009, 284:34167-34178.
• [42]Fu L, Das B, Mathew S, Shi YB: Genome-wide identification of Xenopus matrix metalloproteinases: conservation and unique duplications in amphibians. BMC Genomics 2009, 10:81. BioMed Central Full Text
• [43]Amaya E, Offield MF, Grainger RM: Frog genetics: Xenopus tropicalis jumps into the future. Trends Genet 1998, 14:253-255.
• [44]Bilesimo P, Jolivet P, Alfama G, Buisine N, Le Mevel S, Havis E, Demeneix BA, Sachs LM: Specific histone lysine 4 methylation patterns define TR-binding capacity and differentiate direct T3 responses. Mol Endocrinol 2011, 25:225-237.
• [45]Ishizuya-Oka A, Shimozawa A: Ultrastructural changes in the intestinal connective tissue of Xenopus laevis during metamorphosis. J Morphol 1987, 193:13-22.
• [46]Ishizuya-Oka A, Shimozawa A: Development of the connective tissue in the digestive tract of the larval and metamorphosing Xenopus laevis. Anat Anz 1987, 164:81-93.
• [47]Leloup J, Buscaglia M: La triiodothyronine: hormone de la métamorphose des amphibiens. CR Acad Sci 1977, 284:2261-2263.
• [48]Ishizuya-Oka A, Ueda S, Damjanovski S, Li Q, Liang VC, Shi Y-B: Anteroposterior gradient of epithelial transformation during amphibian intestinal remodeling: immunohistochemical detection of intestinal fatty acid-binding protein. Dev Biol 1997, 192:149-161.
• [49]Ishizuya-Oka A, Hasebe T: Establishment of intestinal stem cell niche during amphibian metamorphosis. Curr Top Dev Biol 2013, 103:305-327.
• [50]Shi YB, Matsuura K, Fujimoto K, Wen L, Fu L: Thyroid hormone receptor actions on transcription in amphibia: The roles of histone modification and chromatin disruption. Cell Biosci 2012, 2:42. BioMed Central Full Text
• [51]Fujimoto K, Nakajima K, Yaoita Y: One of the duplicated matrix metalloproteinase-9 genes is expressed in regressing tail during anuran metamorphosis. Develop Growth Differ 2006, 48:223-241.
• [52]Wang J, Alexander P, Wu L, Hammer R, Cleaver O, McKnight SL: Dependence of mouse embryonic stem cells on threonine catabolism. Science 2009, 325:435-439.
• [53]Nieuwkoop PD, Faber J: Normal table of Xenopus laevis. 1st edition. Amsterdam: North Holland Publishing; 1956.
• [54]Hasebe T, Fu L, Amano T, Shi Y-B: Evidence for a cooperative role of gelatinase A and membrane type-1 matrix metalloproteinase during Xenopus laevis development. Mech Dev 2007, 124:11-22.
• [55]Patterton D, Shi YB: Thyroid hormone-dependent differential regulation of multiple arginase genes during amphibian metamorphosis. J Biol Chem 1994, 269:25328-25334.
• [56]Sun G, Hasebe T, Fujimoto K, Lu R, Fu L, Matsuda H, Kajita M, Ishizuya-Oka A, Shi YB: Spatio-temporal expression profile of stem cell-associated gene LGR5 in the intestine during thyroid hormone-dependent metamorphosis in Xenopus laevis. PLoS One 2010, 5:e13605.
• [57]Heimeier RA, Das B, Buchholz DR, Shi YB: The xenoestrogen bisphenol A inhibits postembryonic vertebrate development by antagonizing gene regulation by thyroid hormone. Endocrinology 2009, 150:2964-2973.
• [58]Hasebe T, Hartman R, Matsuda H, Shi YB: Spatial and temporal expression profiles suggest the involvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis. Cell Tissue Res 2006, 324:105-116.