Krüppel-like factor 5 is essential for proliferation and survival of mouse intestinal epithelial stem cells

Stem Cell Research

Volumn 14, Issue 1, 2015, Pages 10-19

  Nandan, Mandayam O ^a   Ghaleb, Amr M ^a   Bialkowska, Agnieszka B ^a   Yang, Vincent W ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CRE RECOMBINASE; KRUPPEL LIKE FACTOR 5; TAMOXIFEN; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; G PROTEIN COUPLED RECEPTOR; KLF5 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; LGR5 PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; COLON; CONTROLLED STUDY; GENE DELETION; IMMUNOHISTOCHEMISTRY; INTESTINAL STEM CELL; INTESTINE CRYPT; INTESTINE EPITHELIUM CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SMALL INTESTINE; ANIMAL; C57BL MOUSE; DEFICIENCY; DRUG EFFECTS; EPITHELIUM CELL; GENETICS; INTESTINE; METABOLISM; MOUSE; PATHOLOGY; STEM CELL; TRANSGENIC MOUSE;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; EPITHELIAL CELLS; INTESTINES; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, G-PROTEIN-COUPLED; STEM CELLS; TAMOXIFEN;

EID: 84910622179     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2014.10.008     Document Type: Article

References (43)

1. Barker N., van Es J.H., Kuipers J., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
2. Barker N., van de Wetering M., Clevers H. The intestinal stem cell. Genes Dev. 2008, 22:1856-1864.
3. Bjerknes M., Cheng H. The stem-cell zone of the small intestinal epithelium. V. Evidence for controls over orientation of boundaries between the stem-cell zone, proliferative zone, and the maturation zone. Am. J. Anat. 1981, 160:105-112.
4. Booth D., Potten C.S. Protection against mucosal injury by growth factors and cytokines. J. Natl. Cancer Inst. Monogr. 2001, 16-20.
5. Cheng H., Leblond C.P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. V. Unitarian Theory of the origin of the four epithelial cell types. Am. J. Anat. 1974, 141:537-561.
6. El Marjou F., Janssen K.P., Chang B.H., et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 2004, 39:186-193.
7. Ghaleb A.M., Nandan M.O., Chanchevalap S., et al. Kruppel-like factors 4 and 5: the yin and yang regulators of cellular proliferation. Cell Res. 2005, 15:92-96.
8. Kayahara T., Sawada M., Takaishi S., et al. 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. 2003, 535:131-135.
9. Korinek V., Barker N., Morin P.J., et al. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 1997, 275:1784-1787.
10. Li L., Clevers H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327:542-545.
11. Lopez-Garcia C., Klein A.M., Simons B.D., et al. Intestinal stem cell replacement follows a pattern of neutral drift. Science 2010, 330:822-825.
12. Marshman E., Booth C., Potten C.S. The intestinal epithelial stem cell. Bioessays 2002, 24:91-98.
13. McConnell B.B., Yang V.W. Mammalian Kruppel-like factors in health and diseases. Physiol. Rev. 2010, 90:1337-1381.
14. McConnell B.B., Ghaleb A.M., Nandan M.O., et al. The diverse functions of Kruppel-like factors 4 and 5 in epithelial biology and pathobiology. Bioessays 2007, 29:549-557.
15. McConnell B.B., Bialkowska A.B., Nandan M.O., et al. Haploinsufficiency of Kruppel-like factor 5 rescues the tumor-initiating effect of the Apc(Min) mutation in the intestine. Cancer Res. 2009, 69:4125-4133.
16. McConnell B.B., Kim S.S., Yu K., et al. Kruppel-like factor 5 is important for maintenance of crypt architecture and barrier function in mouse intestine. Gastroenterology 2011, 141:1302-1313. (313 e1301-1306).
17. Morin P.J., Sparks A.B., Korinek V., et al. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997, 275:1787-1790.
18. Munoz J., Stange D.E., Schepers A.G., et al. The Lgr5 intestinal stem cell signature: robust expression of proposed quiescent '+4' cell markers. EMBO J. 2012, 31:3079-3091.
19. Nakaya T., Ogawa S., Manabe I., et al. KLF5 regulates the integrity and oncogenicity of intestinal stem cells. Cancer Res. 2014, 74:2882-2891.
20. Nandan M.O., Yoon H.S., Zhao W., et al. Kruppel-like factor 5 mediates the transforming activity of oncogenic H-Ras. Oncogene 2004, 23:3404-3413.
21. Nandan M.O., McConnell B.B., Ghaleb A.M., et al. Kruppel-like factor 5 mediates cellular transformation during oncogenic KRAS-induced intestinal tumorigenesis. Gastroenterology 2008, 134:120-130.
22. Nandan M.O., Ghaleb A.M., McConnell B.B., et al. Kruppel-like factor 5 is a crucial mediator of intestinal tumorigenesis in mice harboring combined ApcMin and KRASV12 mutations. Mol. Cancer 2010, 9:63.
23. Nandan M.O., Ghaleb A.M., Liu Y., et al. Inducible intestine-specific deletion of Kruppel-like factor 5 is characterized by a regenerative response in adult mouse colon. Dev. Biol. 2014, 387:191-202.
24. O'Brien C.A., Pollett A., Gallinger S., et al. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007, 445:106-110.
25. Pirici D., Mogoanta L., Kumar-Singh S., et al. Antibody elution method for multiple immunohistochemistry on primary antibodies raised in the same species and of the same subtype. J. Histochem. Cytochem. 2009, 57:567-575.
26. Podolsky D.K. Regulation of intestinal epithelial proliferation: a few answers, many questions. Am. J. Physiol. 1993, 264:G179-G186.
27. Ponder B.A., Schmidt G.H., Wilkinson M.M., et al. Derivation of mouse intestinal crypts from single progenitor cells. Nature 1985, 313:689-691.
28. Potten C.S., Loeffler M. Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 1990, 110:1001-1020.
29. Potten C.S., Kovacs L., Hamilton E. Continuous labelling studies on mouse skin and intestine. Cell Tissue Kinet. 1974, 7:271-283.
30. Potten C.S., Booth C., Pritchard D.M. The intestinal epithelial stem cell: the mucosal governor. Int. J. Exp. Pathol. 1997, 78:219-243.
31. Potten C.S., Owen G., Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J. Cell Sci. 2002, 115:2381-2388.
32. Potten C.S., Booth C., Tudor G.L., et al. Identification of a putative intestinal stem cell and early lineage marker; musashi-1. Differentiation 2003, 71:28-41.
33. Sangiorgi E., Capecchi M.R. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 2008, 40:915-920.
34. Sato T., Vries R.G., Snippert H.J., et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009, 459:262-265.
35. Schepers A.G., Vries R., van den Born M., et al. Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes. EMBO J. 2011, 30:1104-1109.
36. Shindo T., Manabe I., Fukushima Y., et al. Kruppel-like zinc-finger transcription factor KLF5/BTEB2 is a target for angiotensin II signaling and an essential regulator of cardiovascular remodeling. Nat. Med. 2002, 8:856-863.
37. Snippert H.J., van der Flier L.G., Sato T., et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143:134-144.
38. Sun R., Chen X., Yang V.W. Intestinal-enriched Kruppel-like factor (Kruppel-like factor 5) is a positive regulator of cellular proliferation. J. Biol. Chem. 2001, 276:6897-6900.
39. Takeda N., Manabe I., Uchino Y., et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J. Clin. Invest. 2010, 120:254-265.
40. van der Flier L.G., Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu. Rev. Physiol. 2009, 71:241-260.
41. Wong V.W., Stange D.E., Page M.E., et al. Lrig1 controls intestinal stem-cell homeostasis by negative regulation of ErbB signalling. Nat. Cell Biol. 2012, 14:401-408.
42. Yan K.S., Chia L.A., Li X., et al. The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:466-471.
43. Ziemer L.T., Pennica D., Levine A.J. Identification of a mouse homolog of the human BTEB2 transcription factor as a beta-catenin-independent Wnt-1-responsive gene. Mol. Cell. Biol. 2001, 21:562-574.