Thyroid hormone-induced cell-cell interactions are required for the development of adult intestinal stem cells

Cell & Bioscience

Atsuko Ishizuya-Oka¹  Yun-Bo Shi²  Yu Zhang²  Thomas C Miller²  Liezhen Fu²  Takashi Hasebe¹ 

[1] Department of Biology, Nippon Medical School, 2-297-2 Nakahara-ku, Kosugi-cho, Kawasaki, Kanagawa, 211-0063, Japan;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), Bethesda, Maryland, 20892, USA

关键词: Extracellular matrix (ECM);    Matrix metalloproteinase;    Cell-cell interaction;    Xenopus laevis and tropicalis;    Metamorphosis;    Apoptosis;    Dedifferentiation;    Thyroid hormone receptor;    Adult organ-specific stem cell;   

Others  :  792895
DOI  :  10.1186/2045-3701-3-18

 received in 2013-01-02, accepted in 2013-03-08,  发布年份 2013

【 摘 要 】

The mammalian intestine has long been used as a model to study organ-specific adult stem cells, which are essential for organ repair and tissue regeneration throughout adult life. The establishment of the intestinal epithelial cell self-renewing system takes place during perinatal development when the villus-crypt axis is established with the adult stem cells localized in the crypt. This developmental period is characterized by high levels of plasma thyroid hormone (T3) and T3 deficiency is known to impair intestinal development. Determining how T3 regulates adult stem cell development in the mammalian intestine can be difficult due to maternal influences. Intestinal remodeling during amphibian metamorphosis resembles perinatal intestinal maturation in mammals and its dependence on T3 is well established. A major advantage of the amphibian model is that it can easily be controlled by altering the availability of T3. The ability to manipulate and examine this relatively rapid and localized formation of adult stem cells has greatly assisted in the elucidation of molecular mechanisms regulating their formation and further revealed evidence that supports conservation in the underlying mechanisms of adult stem cell development in vertebrates. Furthermore, genetic studies in Xenopus laevis indicate that T3 actions in both the epithelium and the rest of the intestine, most likely the underlying connective tissue, are required for the formation of adult stem cells. Molecular analyses suggest that cell-cell interactions involving hedgehog and BMP pathways are critical for the establishment of the stem cell niche that is essential for the formation of the adult intestinal stem cells.

【 授权许可】

   
2013 Hasebe et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 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]Sancho E, Eduard Batlle E, Clevers H: Signaling pathways in intestinal development and cancer. Annu Rev Cell DevBiol 2004, 20:695-723.
• [4]van der Flier LG, Clevers H: Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009, 71:241-260.
• [5]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 USA 2011, 108:10585-10590.
• [6]Muncan V, Heijmans J, Krasinski SD, Buller NV, Wildenberg ME, Meisner S, Radonjic M, Stapleton KA, Lamers WH, Biemond I: Blimp1 regulates the transition of neonatal to adult intestinal epithelium. Nat Commun 2011, 2:452.
• [7]Crosnier C, Stamataki D, Lewis J: Organizing cell renewal in the intestine: stem cells, signals and combinatorial control. Nat Rev Genet 2006, 7:349-359.
• [8]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
• [9]Ishizuya-Oka A, Shi YB: Evolutionary insights into postembryonic development of adult intestinal stem cells. Cell Biosci 2011, 1:37. BioMed Central Full Text
• [10]Friedrichsen S, Christ S, Heuer H, Schäfer MKH, Mansouri A, Bauer K, Visser TJ: Regulation of iodothyronine deiodinases in the Pax8−/− mouse model of congenital hypothyroidism. Endocrinology 2003, 144:777-784.
• [11]Tata JR: Gene expression during metamorphosis: an ideal model for post-embryonic development. Bioessays 1993, 15:239-248.
• [12]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.
• [13]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.
• [14]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.
• [15]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.
• [16]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.
• [17]Plateroti M, Kress E, Mori JI, Samarut J: Thyroid hormone receptor alpha1 directly controls transcription of the beta-catenin gene in intestinal epithelial cells. Mol Cell Biol 2006, 26:3204-3214.
• [18]Sirakov M, Skah S, Nadjar J, Plateroti M: Thyroid hormone’s action on progenitor/stem cell biology: New challenge for a classic hormone? Biochim Biophys Acta 2013. in press
• [19]Sirakov M, Plateroti M: The thyroid hormones and their nuclear receptors in the gut: from developmental biology to cancer. Biochim Biophys Acta 1812, 2011:938-946.
• [20]Shi Y-B: Amphibian Metamorphosis: From morphology to molecular biology. New York: John Wiley & Sons, Inc.; 1999.
• [21]Dodd MHI, Dodd JM: The biology of metamorphosis. In Physiology of the amphibia. Edited by Lofts B. New York: Academic Press; 1976:467-599.
• [22]Gilbert LI, Tata JR, Atkinson BG: Metamorphosis: Post-embryonic reprogramming of gene expression in amphibian and insect cells. New York: Academic Press; 1996.
• [23]Sachs LM, Damjanovski S, Jones PL, Li Q, Amano T, Ueda S, Shi YB, Ishizuya-Oka A: Dual functions of thyroid hormone receptors during Xenopus development. Comp Biochem Physiol B Biochem Mol Biol 2000, 126:199-211.
• [24]Shi Y-B: Molecular biology of amphibian metamorphosis: A new approach to an old problem. Trends Endocrinol Metab 1994, 5:14-20.
• [25]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.
• [26]Ishizuya-Oka A, Ueda S: Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res 1996, 286:467-476.
• [27]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.
• [28]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.
• [29]Vukicevic S, Kleinman HK, Luyten FP, Roberts AB, Roche NS, Reddi AH: Identification of multiple active growth factors in basement membrane Matrigel suggests caution in interpretation of cellular activity related to extracellular matrix components. Exp Cell Res 1992, 202:1-8.
• [30]Schmidt JW, Piepenhagen PA, Nelson WJ: Modulation of epithelial morphogenesis and cell fate by cell-to-cell signals and regulated cell adhesion. Seminars in Cell Biol 1993, 4:161-173.
• [31]Brown KE, Yamada KM: The role of integrins during vertebrate development. Seminars in Develop Biol 1995, 6:69-77.
• [32]Werb Z, Sympson CJ, Alexander CM, Thomasset N, Lund LR, MacAuley A, Ashkenas J, Bissell MJ: Extracellular matrix remodeling and the regulation of epithelial- stromal interactions during differentiation and involution. Kidney Int Suppl 1996, 54:S68-74.
• [33]Shi Y-B, Li Q, Damjanovski S, Amano T, Ishizuya-Oka A: Regulation of apoptosis during development: Input from the extracellular matrix. Intern J of Mol Medicine 1998, 2:273-282.
• [34]Murata E, Merker HJ: Morphologic changes of the basal lamina in the small intestine of Xenopus laevis during metamorphosis. Acta Anat 1991, 140:60-69.
• [35]Ishizuya-Oka A, Shimozawa A: Ultrastructural changes in the intestinal connective tissue of Xenopus laevis during metamorphosis. J Morphol 1987, 193:13-22.
• [36]Ishizuya-Oka A, Shimozawa A: Programmed cell death and heterolysis of larval epithelial cells by macrophage-like cells in the anuran small intestine in vivo and in vitro. J Morphol 1992, 213:185-195.
• [37]Su Y, Shi Y, Stolow M, Shi Y-B: Thyroid hormone induces apoptosis in primary cell cultures of tadpole intestine: cell type specificity and effects of extracellular matrix. J Cell Biol 1997, 139:1533-1543.
• [38]Su Y, Shi Y, Shi Y-B: Cyclosporin a but not FK506 inhibits thyroid hormone-induced apoptosis in xenopus tadpole intestinal epithelium. FASEB J 1997, 11:559-565.
• [39]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.
• [40]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.
• [41]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.
• [42]Lazar MA: Thyroid hormone receptors: multiple forms, multiple possibilities. Endocr Rev 1993, 14:184-193.
• [43]Yen PM: Physiological and molecular basis of thyroid hormone action. Physiol Rev 2001, 81:1097-1142.
• [44]Tsai MJ, O’Malley BW: Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Ann Rev Biochem 1994, 63:451-486.
• [45]Laudet V, Gronemeyer H: The nuclear receptor FactsBook. San Diego: Academic Press; 2002.
• [46]Schreiber AM, Das B, Huang H, Marsh-Armstrong N, Brown DD: Diverse developmental programs of Xenopus laevis metamorphosis are inhibited by a dominant negative thyroid hormone receptor. PNAS 2001, 98:10739-10744.
• [47]Brown DD, Cai L: Amphibian metamorphosis. Dev Biol 2007, 306:20-33.
• [48]Buchholz DR, Hsia VS-C, Fu L, Shi Y-B: A dominant negative thyroid hormone receptor blocks amphibian metamorphosis by retaining corepressors at target genes. Mol Cell Biol 2003, 23:6750-6758.
• [49]Buchholz DR, Tomita A, Fu L, Paul BD, Shi Y-B: Transgenic analysis reveals that thyroid hormone receptor is sufficient to mediate the thyroid hormone signal in frog metamorphosis. Mol Cell Biol 2004, 24:9026-9037.
• [50]Buchholz DR, Paul BD, Fu L, Shi YB: Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. Gen Comp Endocrinol 2006, 145:1-19.
• [51]Shi Y-B: Dual functions of thyroid hormone receptors in vertebrate development: the roles of histone-modifying cofactor complexes. Thyroid 2009, 19:987-999.
• [52]Nakajima K, Yaoita Y: Dual mechanisms governing muscle cell death in tadpole tail during amphibian metamorphosis. Dev Dyn 2003, 227:246-255.
• [53]Denver RJ, Hu F, Scanlan TS, Furlow JD: Thyroid hormone receptor subtype specificity for hormone-dependent neurogenesis in Xenopus laevis. Dev Biol 2009, 326:155-168.
• [54]Bagamasbad P, Howdeshell KL, Sachs LM, Demeneix BA, Denver RJ: A role for basic transcription element-binding protein 1 (BTEB1) in the autoinduction of thyroid hormone receptor beta. J Biol Chem 2008, 283:2275-2285.
• [55]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.
• [56]McKenna NJ, O’Malley BW: Combinatorial control of gene expression by nuclear receptors and coregulators. Cell 2002, 108:465-474.
• [57]Horlein AJ, Naar AM, Heinzel T, Torchia J, Gloss B, Kurokawa R, Ryan A, Kamei Y, Soderstrom M, Glass CK: Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 1995, 377:397-404.
• [58]Chen JD, Evans RM: A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature 1995, 377:454-457.
• [59]Burke LJ, Baniahmad A: Co-repressors 2000. FASEB J 2000, 14:1876-1888.
• [60]Jones PL, Shi Y-B: N-CoR-HDAC corepressor complexes: Roles in transcriptional regulation by nuclear hormone receptors. In Current Topics in Microbiology and Immunology: Protein Complexes that Modify Chromatin. Volume 274. Edited by Workman JL. Berlin: Springer-Verlag; 2003:237-268.
• [61]Glass CK, Rosenfeld MG: The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 2000, 14:121-141.
• [62]Ito M, Roeder RG: The TRAP/SMCC/Mediator complex and thyroid hormone receptor function. Trends Endocrinol Metab 2001, 12:127-134.
• [63]Zhang J, Lazar MA: The mechanism of action of thyroid hormones. Annu Rev Physiol 2000, 62:439-466.
• [64]Huang Z-Q, Li J, Sachs LM, Cole PA, Wong J: A role for cofactor–cofactor and cofactor–histone interactions in targeting p300, SWI/SNF and Mediator for transcription. EMBO J 2003, 22:2146-2155.
• [65]McKenna NJ, O’Malley BW: Nuclear receptors, coregulators, ligands, and selective receptor modulators: making sense of the patchwork quilt. Ann N Y Acad Sci 2001, 949:3-5.
• [66]Rachez C, Freedman LP: Mediator complexes and transcription. Curr Opin Cell Biol 2001, 13:274-280.
• [67]Chen H, Lin RJ, Schiltz RL, Chakravarti D, Nash A, Nagy L, Privalsky ML, Nakatani Y, Evans RM: Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 1997, 90:569-580.
• [68]Demarest SJ, Martinez-Yamout M, Chung J, Chen H, Xu W, Dyson HJ, Evans RM, Wright PE: Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 2002, 415:549-553.
• [69]Onate SA, Tsai SY, Tsai MJ, O’Malley BW: Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 1995, 270:1354-1357.
• [70]Meng X, Yang YF, Cao X, Govindan MV, Shuen M, Hollenberg AN, Mymryk JS, Walfish PG: Cellular context of coregulator and adaptor proteins regulates human adenovirus 5 early region 1A-dependent gene activation by the thyroid hormone receptor. Mol Endocrinol 2003, 17:1095-1105.
• [71]Wahlstrom GM, Vennstrom B, Bolin MB: The adenovirus E1A protein is a potent coactivator for thyroid hormone receptors. Mol Endocrinol 1999, 13:1119-1129.
• [72]Sato Y, Ding A, Heimeier RA, Yousef AF, Mymryk JS, Walfish PG, Shi Y-B: The adenoviral E1A protein displaces corepressors and relieves gene repression by unliganded thyroid hormone receptors in vivo. Cell Res 2009, 19:783-792.
• [73]Perissi V, Jepsen K, Glass CK, Rosenfeld MG: Deconstructing repression: evolving models of co-repressor action. Nat Rev Genet 2010, 11:109-123.
• [74]O’Malley BW, Malovannaya A, Qin J: Minireview: nuclear receptor and coregulator proteomics–2012 and beyond. Mol Endocrinol 2012, 26:1646-1650.
• [75]Bulynko YA, O’Malley BW: Nuclear receptor coactivators: structural and functional biochemistry. Biochemistry 2011, 50:313-328.
• [76]McKenna NJ, Cooney AJ, DeMayo FJ, Downes M, Glass CK, Lanz RB, Lazar MA, Mangelsdorf DJ, Moore DD, Qin J: Minireview: Evolution of NURSA, the Nuclear Receptor Signaling Atlas. Mol Endocrinol 2009, 23:740-746.
• [77]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
• [78]Tomita A, Buchholz DR, Shi Y-B: Recruitment of N-CoR/SMRT-TBLR1 corepressor complex by unliganded thyroid hormone receptor for gene repression during frog development. Mol Cell Biol 2004, 24:3337-3346.
• [79]Sachs LM, Jones PL, Havis E, Rouse N, Demeneix BA, Shi Y-B: N-CoR recruitment by unliganded thyroid hormone receptor in gene repression during Xenopus laevis development. Mol Cell Biol 2002, 22:8527-8538.
• [80]Sato Y, Buchholz DR, Paul BD, Shi Y-B: A role of unliganded thyroid hormone receptor in postembryonic development in Xenopus laevis. Mech Dev 2007, 124:476-488.
• [81]Matsuda H, Paul BD, Choi CY, Hasebe T, Shi Y-B: Novel functions of protein arginine methyltransferase 1 in thyroid hormone receptor-mediated transcription and in the regulation of metamorphic rate in Xenopus laevis. Mol Cell Biol 2009, 29:745-757.
• [82]Paul BD, Buchholz DR, Fu L, Shi Y-B: Tissue- and gene-specific recruitment of steroid receptor coactivator-3 by thyroid hormone receptor during development. J Biol Chem 2005, 280:27165-27172.
• [83]Paul BD, Fu L, Buchholz DR, Shi Y-B: Coactivator recruitment is essential for liganded thyroid hormone receptor to initiate amphibian metamorphosis. Mol Cell Biol 2005, 25:5712-5724.
• [84]Paul BD, Buchholz DR, Fu L, Shi Y-B: SRC-p300 coactivator complex is required for thyroid hormone induced amphibian metamorphosis. J Biol Chem 2007, 282:7472-7481.
• [85]Havis E, Sachs LM, Demeneix BA: Metamorphic T3-response genes have specific co-regulator requirements. EMBO Rep 2003, 4:883-888.
• [86]Paul BD, Shi Y-B: Distinct expression profiles of transcriptional coactivators for thyroid hormone receptors during Xenopus laevis metamorphosis. Cell Res 2003, 13:459-464.
• [87]Shi Y-B, Brown DD: The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J Biol Chem 1993, 268:20312-20317.
• [88]Buchholz DR, Heimeier RA, Das B, Washington T, Shi Y-B: Pairing morphology with gene expression in thyroid hormone-induced intestinal remodeling and identification of a core set of TH-induced genes across tadpole tissues. Dev Biol 2007, 303:576-590.
• [89]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.
• [90]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
• [91]Amano T, Yoshizato K: Isolation of genes involved in intestinal remodeling during anuran metamorphosis. Wound Repair Regen 1998, 6:302-313.
• [92]Matsuura K, Fujimoto K, Fu L, Shi Y-B: Liganded thyroid hormone receptor induces nucleosome removal and histone modifications to activate transcription during larval intestinal cell death and adult stem cell development. Endocrinology 2012, 153:961-972.
• [93]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
• [94]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. Endocrinology; 2012.
• [95]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.
• [96]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.
• [97]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.
• [98]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, 7:47401-47410. e47407
• [99]Kress E, Samarut J, Plateroti M: Thyroid hormones and the control of cell proliferation or cell differentiation: paradox or duality? Mol Cell Endocrinol 2009, 313:36-49.
• [100]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.
• [101]Barrett JA, Rawloings ND, Woessner JF: Handbook of proteolytic enzymes. NY: Academic Press; 1998.
• [102]Alexander CM, Werb Z: Extracellular matrix degradation. In Cell Biology of Extracellular Matrix. 2nd edition. Edited by Hay ED. New York: Plenum Press; 1991:255-302.
• [103]Birkedal-Hansen H, Moore WGI, Bodden MK, Windsor LT, Birkedal-Hansen B, DeCarlo A, Engler JA: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 1993, 4:197-250.
• [104]McCawley LJ, Matrisian LM: Matrix metalloproteinases: they’re not just for matrix anymore! Curr Opin Cell Biol 2001, 13:534-540.
• [105]Parks WC, Mecham RP: Matrix metalloproteinases. New York: Academic Press; 1998.
• [106]Nagase H: Cell surface activation of progelatinase A (proMMP-2) and cell migration. Cell Res 1998, 8:179-186.
• [107]Pei D: Leukolysin/MMP25/MT6-MMP: a novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Res 1999, 9:291-303.
• [108]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
• [109]Uria JA, Werb Z: Matrix metalloproteinases and their expression in mammary gland. Cell Res 1998, 8:187-194.
• [110]Overall CM: Molecular determinants of metalloproteinase substrate specificity. Mol Biotechnol 2002, 22:51-86.
• [111]Mathew S, Fu L, Hasebe T, Ishizuya-Oka A, Shi YB: Tissue-dependent induction of apoptosis by matrix metalloproteinase stromelysin-3 during amphibian metamorphosis. Birth Defects Res C Embryo Today 2010, 90:55-66.
• [112]Gross J, Lapiere CM: Collagenolytic activity in amphibian tissues: A tissue culture assay. Proc Natl Acad Sci USA 1962, 48:1014-1022.
• [113]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.
• [114]Patterton D, Hayes WP, Shi YB: Transcriptional activation of the matrix metalloproteinase gene stromelysin-3 coincides with thyroid hormone-induced cell death during frog metamorphosis. Dev Biol 1995, 167:252-262.
• [115]Stolow MA, Bauzon DD, Li J, Sedgwick T, Liang VC, Sang QA, Shi YB: Identification and characterization of a novel collagenase in Xenopus laevis: possible roles during frog development. Mol Biol Cell 1996, 7:1471-1483.
• [116]Wang Z, Brown DD: Thyroid hormone-induced gene expression program for amphibian tail resorption. J Biol Chem 1993, 268:16270-16278.
• [117]Damjanovski S, Ishizuya-Oka A, Shi YB: Spatial and temporal regulation of collagenases-3, -4, and stromelysin - 3 implicates distinct functions in apoptosis and tissue remodeling during frog metamorphosis. Cell Res 1999, 9:91-105.
• [118]Fu L, Tomita A, Wang H, Buchholz DR, Shi Y-B: Transcriptional regulation of the Xenopus laevis stromelysin-3 gene by thyroid hormone is mediated by a DNA element in the first intron. J Biol Chem 2006, 281:16870-16878.
• [119]Ishizuya-Oka A, Ueda S, Shi Y-B: Transient expression of stromelysin-3 mRNA in the amphibian small intestine during metamorphosis. Cell Tissue Res 1996, 283:325-329.
• [120]Ishizuya-Oka A, Li Q, Amano T, Damjanovski S, Ueda S, Shi Y-B: Requirement for matrix metalloproteinase stromelysin-3 in cell migration and apoptosis during tissue remodeling in Xenopus laevis. J Cell Biol 2000, 150:1177-1188.
• [121]Fu L, Buchholz D, Shi YB: Novel double promoter approach for identification of transgenic animals: A tool for in vivo analysis of gene function and development of gene-based therapies. Mol Reprod Dev 2002, 62:470-476.
• [122]Fu L, Ishizuya-Oka A, Buchholz DR, Amano T, Matsuda H, Shi YB: A causative role of stromelysin-3 in extracellular matrix remodeling and epithelial apoptosis during intestinal metamorphosis in Xenopus laevis. J Biol Chem 2005, 280:27856-27865.
• [123]Murphy G, Segain J-P, O’Shea M, Cockett M, Ioannou C, Lefebvre O, Chambon P, Basset P: The 28-kDa N-terminal domain of mouse stromelysin-3- has the general properties of a weak metalloproteinase. J Biol Chem 1993, 268:15435-15441.
• [124]Pei D, Majmudar G, Weiss SJ: Hydrolytic inactivation of a breast carcinoma cell-derived serpin by human stromelysin-3. J Biol Chem 1994, 269:25849-25855.
• [125]Manes S, Mira E, Barbacid MD, Cipres A, FernandezResa P, Buesa JM, Merida I, Aracil M, Marquez G, Martinez C: Identification of insulin-like growth factor-binding protein-1 as a potential physiological substrate for human stromelysin-3. J Biol Chem 1997, 272:25706-25712.
• [126]Amano T, Kwak O, Fu L, Marshak A, Shi Y-B: The matrix metalloproteinase stromelysin-3 cleaves laminin receptor at two distinct sites between the transmembrane domain and laminin binding sequence within the extracellular domain. Cell Res 2005, 15:150-159.
• [127]Amano T, Fu L, Marshak A, Kwak O, Shi YB: Spatio-temporal regulation and cleavage by matrix metalloproteinase stromelysin-3 implicate a role for laminin receptor in intestinal remodeling during Xenopus laevis metamorphosis. Dev Dyn 2005, 234:190-200.
• [128]Mathew S, Fu L, Fiorentino M, Matsuda H, Das B, Shi Y-B: Differential regulation of cell type specific apoptosis by stromelysin-3: A potential mechanism via the cleavage of the laminin receptor during tail resorption in Xenopus laevis. J Biol Chem 2009, 284:18545-18556.
• [129]Ramalho-Santos M, Melton DA, McMahon AP: Hedgehog signals regulate multiple aspects of gastrointestinal development. Development 2000, 127:2763-2772.
• [130]Kim TH, Kim BM, Mao J, Rowan S, Shivdasani RA: Endodermal Hedgehog signals modulate Notch pathway activity in the developing digestive tract mesenchyme. Development 2011, 138:3225-3233.
• [131]Stolow MA, Shi YB: Xenopus sonic hedgehog as a potential morphogen during embryogenesis and thyroid hormone-dependent metamorphosis. Nucleic Acids Res 1995, 23:2555-2562.
• [132]Ishizuya-Oka A, Ueda S, Inokuchi T, Amano T, Damjanovski S, Stolow M, Shi Y-B: Thyroid hormone-induced expression of Sonic hedgehog correlates with adult epithelial development during remodeling of the Xenopus stomach and intestine. Differentiation 2001, 69:27-37.
• [133]Hasebe T, Kajita M, Fu L, Shi YB, Ishizuya-Oka A: Thyroid hormone-induced sonic hedgehog signal up-regulates its own pathway in a paracrine manner in the Xenopus laevis intestine during metamorphosis. Dev Dyn 2012, 241:403-414.
• [134]Ishizuya-Oka A, Ueda S, Amano T, Shimizu K, Suzuki K, Ueno N, Yoshizato K: Thyroid-hormone-dependent and fibroblast-specific expression of BMP-4 correlates with adult epithelial development during amphibian intestinal remodeling. Cell Tissue Res 2001, 303:187-195.
• [135]Ishizuya-Oka A, Hasebe T, Shimizu K, Suzuki K, Ueda S: Shh/BMP-4 signaling pathway is essential for intestinal epithelial development during Xenopus larval-to-adult remodeling. Dev Dyn 2006, 235:3240-3249.
• [136]Perrimon N: Hedgehog and beyond. Cell. 1995, 80:517-520.
• [137]Roberts DJ, Johnson RL, Burke AC, Nelson CE, Morgan BA, Tabin C: Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 1995, 121:3163-3174.
• [138]Ingham PW: Transducing Hedgehog: the story so far. EMBO J 1998, 17:3505-3511.
• [139]Young JJ, Cherone JM, Doyon Y, Ankoudinova I, Faraji FM, Lee AH, Ngo C, Guschin DY, Paschon DE, Miller JC: Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases. Proc Natl Acad Sci USA 2011, 108:7052-7057.
• [140]Lei Y, Guo X, Liu Y, Cao Y, Deng Y, Chen X, Cheng CH, Dawid IB, Chen Y, Zhao H: Efficient targeted gene disruption in Xenopus embryos using engineered transcription activator-like effector nucleases (TALENs). Proc Natl Acad Sci USA 2012, 109:17484-17489.