Origin of the adult intestinal stem cells induced by thyroid hormone in Xenopus laevis

FASEB Journal

Volumn 23, Issue 8, 2009, Pages 2568-2575

  Ishizuya Oka, Atsuko ^a   Hasebe, Takashi ^a   Buchholz, Daniel R ^b   Kajita, Mitsuko ^a   Fu, Liezhen ^c   Shi, Yun Bo ^c  

^a NIPPON MEDICAL SCHOOL   (Japan)

^b UNIVERSITY OF CINCINNATI   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

Gut remodeling; Metamorphosis; Organ culture; Tissue recombination; Transgenic frog

Indexed keywords

CYCLINE; FATTY ACID BINDING PROTEIN 2; GREEN FLUORESCENT PROTEIN; SONIC HEDGEHOG PROTEIN; THYROID HORMONE; RECOMBINANT PROTEIN;

ADULT INTESTINAL STEM CELL; ADULT STEM CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EPITHELIUM; IMMUNOHISTOCHEMISTRY; INTESTINE; LARVA; METAMORPHOSIS; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; XENOPUS LAEVIS; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECT; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORGAN CULTURE TECHNIQUE; TRANSGENIC ANIMAL;

AMPHIBIA; ANURA; ERINACEIDAE; MAMMALIA; XENOPUS LAEVIS;

ADULT STEM CELLS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL DIFFERENTIATION; GENE EXPRESSION; GREEN FLUORESCENT PROTEINS; INTESTINES; LARVA; METAMORPHOSIS, BIOLOGICAL; MODELS, BIOLOGICAL; ORGAN CULTURE TECHNIQUES; RECOMBINANT PROTEINS; THYROID HORMONES;

EID: 68849110997     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-128124     Document Type: Article

References (52)

1. Tata, J. R. (1993) Gene expression during metamorphosis: an ideal model for post- embryonic development. Bioessays 15, 239-248 (Pubitemid 23960847)
2. Shi, Y.-B. (1999) Amphibian Metamorphosis: from Morphology to Molecular Biology, John Wiley & Sons, New York
3. Marshall, J. A., and Dixon, K. E. (1978) Cell proliferation in the intestinal epithelium of Xenopus laevis tadpoles. J. Exp. Zool. 203, 31-40
4. McAvoy, J. W., and Dixon, K. E. (1977) Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adult Xenopus laevis. J. Exp. Zool. 202, 129-138
5. Shi, Y.-B., and Ishizuya-Oka, A. (1996) Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Curr. Top. Dev. Biol. 32, 205-235
6. Bjerknes, M., and Cheng, H. (1981) The stem-cell zone of the small intestinal epithelium. III. Evidence for columnar, enteroendocrine, and mucous cells in the adult mouse. Am. J. Anat. 160, 77-91 (Pubitemid 11096909)
7. Cheng, H., and Bjerknes, M. (1985) Whole population cell kinetics and postnatal development of the mouse intestinal epithelium. Anat. Rec. 211, 420-426 (Pubitemid 15081136)
8. Shi, Y.-B., and Hayes, W. P. (1994) Thyroid hormone-dependent regulation of the intestinal fatty acid-binding protein gene during amphibian metamorphosis. Dev. Biol. 161, 48-58
9. Ishizuya-Oka, A., Ueda, S., Damjanovski, S., Li, Q., Liang, V. C.-T., and Shi, Y.-B. (1997) Anteroposterior gradient of epithelial transformation during amphibian intestinal remodeling: immunohistochemical detection of intestinal fatty acid-binding protein. Dev. Biol. 192, 149-161 (Pubitemid 28015653)
10. McAvoy, J. W., and Dixon, K. E. (1978) Cell specialization in the small intestinal epithelium of adult Xenopus laevis. J. Anat. 125, 155-169
11. Ishizuya-Oka, A., and Ueda, S. (1996) Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tissue Res. 286, 467-476 (Pubitemid 26418055)
12. Nieuwkoop, P. D., and Faber, J. (1967) Normal Table of Xenopus laevis (Daudin), North-Holland Publishing, Amsterdam
13. Hourdry, J., and Dauca, M. (1977) Cytological and cytochemical changes in the intestinal epithelium during anuran metamorphosis. Int. Rev. Cytol. 5(Suppl.), 337-385 (Pubitemid 8293137)
14. Ishizuya-Oka, A., Ueda, S., Inokuchi, T., Amano, T., Damjanovski, S., Stolow, M., and Shi, Y.-B. (2001) Thyroid hormone-induced expression of sonic hedgehog correlates with adult epithelial development during remodeling of the Xenopus stomach and intestine. Differentiation 69, 27-37 (Pubitemid 33755436)
15. Hasebe, T., Kajita, M., Shi, Y.-B., and Ishizuya-Oka, A. (2008) Thyroid hormone- upregulated hedgehog interacting protein is involved in larval-to-adult intestinal remodeling by regulating sonic hedgehog signaling pathway in. Xenopus laevis. Dev. Dyn. 237, 3006-3015
16. Ishizuya-Oka, A., Shimizu, K., Sakakibara, S., Okano, H., and Ueda, S. (2003) Thyroid hormone-upregulated expression of Musashi-1 is specific for progenitor cells of the adult epithelium during amphibian gastrointestinal remodeling. J. Cell Sci. 116, 3157-3164 (Pubitemid 37038964)
17. Ishizuya-Oka, A., and Shi, Y.-B. (2007) Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis. Dev. Dyn. 236, 3358-3368 (Pubitemid 350276392)
18. De Santa Barbara, P., van den Brink, G. R., and Roberts, D. J. (2003) Development and differentiation of the intestinal epithelium. Cell. Mol. Life Sci. 60, 1322-1332
19. Kayahara, T., Sawada, M., Takaishi, S., Fukui, H., Seno, H., Fukuzawa, H., Suzuki, K., Hirai, H., Kageyama, R., Okano, H., and Chiba, T. (2003) Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine. FEBS Lett. 535, 131-135 (Pubitemid 36126368)
20. Potten, C. S., Booth, C., Tudor, G. L., Booth. D., Brady, G., Hurley, P., Ashton, G., Clarke, R., Sakakibara, S., and Okano, H. (2003) Identification of a putative intestinal stem cell and early lineage marker, Musashi-1. Differentiation 71, 28-41 (Pubitemid 38230417)
21. He, X. C., Zhang, J., Tong, W. G., Tawfik, O., Ross, J., Scoville, D. H., Tian, Q., Zeng, X., He, X., Wiedemann, L. M., Mishina, Y., and Li, L. (2004) BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-β-catenin signaling. Nat. Genet. 36, 1117-1121 (Pubitemid 41184475)
22. Dodd, M. H. I., and Dodd, J. M. (1977) The biology of metamorphosis. In Physiology of Amphibia, Vol.3 (Lofts, B., ed) pp. 467-599, Academic Press, New York
23. Kikuyama, S., Kawamura, K., Tanaka, S., and Yamamoto, K. (1993) Aspects of amphibian metamorphosis: hormonal control. Int. Rev. Cytol. 145, 105-148 (Pubitemid 23223465)
24. Ishizuya-Oka, A., and Shimozawa, A. (1991) Induction of metamorphosis by thyroid hormone in anuran small intestine cultured organotypically in vitro. In Vitro Cell. Dev. Biol. 27A, 853-857
25. Amano, T., Noro, N., Kawabata, H., Kobayashi, Y., and Yoshizato, K. (1998) Metamorphosis-associated and region-specific expression of calbindin gene in the posterior intestinal epithelium of Xenopus laevis larva. Dev. Growth Differ. 40, 177-188 (Pubitemid 28180621)
26. Schreiber, A. M., Cai, L., and Brown, D. D. (2005) Remodeling of the intestine during metamorphosis of Xenopus laevis. Proc. Natl. Acad. Sci. U. S. A. 102, 3720-3725
27. Krause, D. S., Theise, N. D., Collector, M. I., Henegariu, O., Hwang, S., Gardner, R., Neutzel, S., and Sharkis, S. J. (2001) Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105, 369-377 (Pubitemid 32455343)
28. Okamoto, R., Yajima, T., Yamazaki, M., Kanai, T., Mukai, M., Okamoto, S., Ikeda, Y., Hibi, T., Inazawa, J., and Watanabe, M. (2002) Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nat. Med. 8, 1011-1017 (Pubitemid 35033706)
29. Shi, Y.-B., Fu, L., Hasebe, T., and Ishizuya-Oka, A. (2007) Regulation of ECM remodeling and cell fate determination by matrix metalloproteinase strmoelysin-3 during thyroid hormone-dependent postembryonic development. Pharmacol. Ther. 116, 391-400 (Pubitemid 350116939)
30. Ishizuya-Oka, A., and Shimozawa, A. (1992) Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis in vitro. Roux Arch. Dev. Biol. 201, 322-329
31. Kroll, K. L., and Amaya, E. (1996) Transgenic Xenopus embryos from sperm nuclear transplantations reveal FGF signalling requirements during gastrulation. Development 122, 3173-3183
32. Buchholz, D. R., Tomita, A., Fu, L., Paul, B. D., and Shi, Y.-B. (2004) Transgenic analysis reveals that thyroid hormone receptor is sufficient to mediate the thyroid hormone signal in frog metamorphosis. Mol. Cell. Biol. 24, 9026-9037 (Pubitemid 39313907)
33. Fu, L., Buchholtz, D., and Shi, Y.-B. (2002) 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. 62, 470-476 (Pubitemid 34743058)
34. Offield, M. F., Hirsch, N., and Grainger, R. M. (2000) The development of Xenopus tropicalis transgenic lines and their use in studying lens developmental timing in living embryos. Development 127, 1789-1797 (Pubitemid 30311783)
35. Ishizuya-Oka, A., Li, Q., Amano, T., Damjanovski, S., Ueda, S., and Shi, Y.-B. (2000) Requirement for matrix metalloproteinase stromelysin-3 in cell migration and apoptosis during tissue remodeling in Xenopus laevis. J. Cell Biol. 150, 1177-1188 (Pubitemid 30688824)
36. Yoshizato, K. (1989) Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Int. Rev. Cytol. 119, 97-149
37. Yoshizato, K. (2007) Molecular mechanism and evolutional significance of epithelial-mesenchymal interactions in the body- and tail-dependent metamorphic transformation of anuran larval skin. Int. Rev. Cytol. 260, 213-260
38. Suzuki, K., Utoh, R., Kotani, K., Obara, M., and Yoshizato, K. (2002) Lineage of anuran epidermal basal cells and their differentiation potential in relation to metamorphic skin remodeling. Dev. Growth Differ. 44, 225-238 (Pubitemid 34639368)
39. Utoh, R., Shigenega, S., Watanabe, Y., and Yoshizato, K. (2003) Platelet-derived growth factor signaling as a cue of the epithelial-mesenchymal interaction required for anuran skin metamorphosis. Dev. Dyn. 227, 157-169 (Pubitemid 36666745)
40. Marshall, J. A., and Dixon, K. E. (1978) Cell specialization in the epithelium of the small intestine of feeding Xenopus laevis tadpoles. J. Anat. 126, 133-144 (Pubitemid 8320403)
41. Leloup, J., and Buscaglia, M. (1977) La triiodothyronine: hormone de la metamorphose des amphibiens. C. R. Acad. Sci. 284, 2261-2263
42. Su, Y., Shi, Y., Stolow, M. A., and Shi, Y.-B. (1997) Thyroid hormone induces apoptosis in primary cell cultures of tadpole intestine: cell type specificity and effects of extracellular matrix. J. Cell Biol. 139, 1533-1543 (Pubitemid 28013673)
43. Mukhi, S., Mao, J., and Brown, D. D. (2008) Remodeling the exocrine pancreas at metamorphosis in Xenopus laevis. Proc. Natl. Acad. Sci. U. S. A. 105, 8962-8967
44. Potten, C. S. (1998) Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 821-830
45. Potten, C. S., Booth, C., and Pritchard, D. M. (1997) The intestinal epithelial stem cell: the mucosal governor. Int. J. Exp. Pathol. 78, 219-243 (Pubitemid 27408019)
46. Blau, H. M., Brazelton, T. R., and Weimann, J. M. (2001) The evolving concept of a stem cell: entity or function? Cell 105, 829-841 (Pubitemid 32635085)
47. Mills, J. C., and Gordon, J. I. (2001) The intestinal stem cell niche: there grows the neighborhood. Proc. Natl. Acad. Sci. U. S. A. 98, 12334-12336
48. Spradling, A., Drummond-Barbosa, D., and Kai, T. (2001) Stem cells find their niche. Nature 414, 98-104 (Pubitemid 33041633)
49. Shi, Y.-B., and Brown, D. D. (1993) The earliest changes in gene expression in tadpole intestine induced by thyroid hormone. J. Biol. Chem. 268, 20312-20317 (Pubitemid 23278938)
50. Amano, T., and Yoshizato, K. (1998) Isolation of genes involved in intestinal remodeling during anuran metamorphosis. Wound Repair Reger. 6, 302-313 (Pubitemid 128656619)
51. Shimizu, K., Ishizuya-Oka, A., Amano, A., Yoshizato, K., and Ueda, S. (2002) Isolation of connective tissue-specific genes involved in Xenopus intestinal remodeling: thyroid hormone up-regulates Tolloid/BMP-1 expression. Dev. Growth Evol. 212, 357-364 (Pubitemid 36075552)
52. Buchholz, D. R., Heimeier, R. A., Das, B., Washington, T., and Shi, Y.-B. (2006) 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. 303, 576-590 (Pubitemid 46350760)