Sox9 expression marks a subset of CD24-expressing small intestine epithelial stem cells that form organoids in vitro

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 298, Issue 5, 2010, Pages

  Gracz, Adam D ^a   Ramalingam, Sendhilnathan ^a   Magness, Scott T ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Intestinal epithelial culture; SOX factors

Indexed keywords

CD24 ANTIGEN; CELL SURFACE MARKER; TRANSCRIPTION FACTOR SOX9;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL SELECTION; CONTROLLED STUDY; CYTOPLASM; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; GENOTYPE; IN VITRO STUDY; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; REPORTER GENE; SMALL INTESTINE MUCOSA; STEM CELL;

ANIMALS; ANTIGENS, CD24; CELL DIFFERENTIATION; CELL LINE; EPITHELIAL CELLS; FLOW CYTOMETRY; INTESTINE, SMALL; MICE; ORGANOIDS; SOX9 TRANSCRIPTION FACTOR; STEM CELLS;

EID: 77951496399     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00470.2009     Document Type: Article

References (46)

1. Akiyama H, Kim JE, Nakashima K, Balmes G, Iwai N, Deng JM, Zhang Z, Martin JF, Behringer RR, Nakamura T, de Crombrugghe B. Osteo-chondroprogenitor cells are derived from Sox9 expressing precursors. Proc Natl Acad Sci USA 102: 14665-14670, 2005. (Pubitemid 41457113)
2. Akiyama H, Lyons JP, Mori-Akiyama Y, Yang X, Zhang R, Zhang Z, Deng JM, Taketo MM, Nakamura T, Behringer RR, McCrea PD, de Crombrugghe B. Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Devel 18: 1072-1087, 2004. (Pubitemid 38620246)
3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100: 3983-3988, 2003. (Pubitemid 36418143)
4. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007, 2007. (Pubitemid 350014593)
5. Bastide P, Darido C, Pannequin J, Kist R, Robine S, Marty-Double C, Bibeau F, Scherer G, Joubert D, Hollande F, Blache P, Jay P. Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J Cell Biol 178: 635-648, 2007. (Pubitemid 47267275)
6. Bjerknes M, Cheng H. The stem-cell zone of the small intestinal epithelium. III. Evidence from columnar, enteroendocrine, and mucous cells in the adult mouse. Am J Anat 160: 77-91, 1981. (Pubitemid 11096909)
7. Cheng H. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. II. Mucous cells. Am J Anat 141: 481-501, 1974.
8. Cheng H. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. IV. Paneth cells. Am J Anat 141: 521-535, 1974.
9. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am J Anat 141: 461-479, 1974.
10. Cheng H, Leblond CP. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. III. Enteroendocrine cells. Am J Anat 141: 503-519, 1974.
11. Cheng H, Leblond CP. 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 141: 537-561, 1974.
12. Dekaney CM, Fong JJ, Rigby RJ, Lund PK, Henning SJ, Helmrath MA. Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice. Am J Physiol Gastrointest Liver Physiol 293: G1013-G1022, 2007.
13. Dekaney CM, Rodriguez JM, Graul MC, Henning SJ. Isolation and characterization of a putative intestinal stem cell fraction from mouse jejunum. Gastroenterology 129: 1567-1580, 2005. (Pubitemid 41597397)
14. Formeister EJ, Sionas AL, Lorance DK, Barkley CL, Lee GH, Magness ST. Distinct SOX9 levels differentially mark stem/progenitor populations and enteroendocrine cells of the small intestine epithelium. Am J Physiol Gastrointest Liver Physiol 296: G1108-G1118, 2009.
15. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925, 2003. (Pubitemid 37376918)
16. Gulati AS, Ochsner SA, Henning SJ. Molecular properties of side population-sorted cells from mouse small intestine. Am J Physiol Gastrointest Liver Physiol 294: G286-G294, 2008.
17. Hough MR, Rosten PM, Sexton TL, Kay R, Humphries RK. Mapping of CD24 and homologous sequences to multiple chromosomal loci. Genomics 22: 154-161, 1994. (Pubitemid 24234099)
18. Kay R, Rosten PM, Humphries RK. CD24, a signal transducer modulating B cell activation responses, is a very short peptide with a glycosyl phosphatidylinositol membrane anchor. J Immunol 147: 1412-1416, 1991.
19. Kay R, Takei F, Humphries RK. Expression cloning of a cDNA encoding M1/69-J11d heat-stable antigens. J Immunol 145: 1952-1959, 1990.
20. Kedinger M, Duluc I, Fritsch C, Lorentz O, Plateroti M, Freund JN. Intestinal epithelial-mesenchymal cell interactions. Ann NY Acad Sci 859: 1-17, 1998.
21. Kedinger M, Lefebvre O, Duluc I, Freund JN, Simon-Assmann P. Cellular and molecular partners involved in gut morphogenesis and differentiation. Phil Trans R Soc Lond 353: 847-856, 1998.
22. Kedinger M, Simon-Assmann P, Bouziges F, Haffen K. Epithelialmesenchymal interactions in intestinal epithelial differentiation. Scand J Gastroenterol 151: 62-69, 1988. (Pubitemid 19098627)
23. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383, 1998. (Pubitemid 28357912)
24. Lim SC, Oh SH. The role of CD24 in various human epithelial neoplasias. Pathol Res Pract 201: 479-486, 2005.
25. Mori-Akiyama Y, Akiyama H, Rowitch DH, de Crombrugghe B. Sox9 is required for determination of the chondrogenic cell lineage in the cranial neural crest. Proc Natl Acad Sci USA 100: 9360-9365, 2003. (Pubitemid 37033933)
26. Mori-Akiyama Y, van den Born M, van Es JH, Hamilton SR, Adams HP, Zhang J, Clevers H, de Crombrugghe B. SOX9 is required for the differentiation of paneth cells in the intestinal epithelium. Gastroenterology 133: 539-546, 2007. (Pubitemid 47187347)
27. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
28. Powell DW, Mifflin RC, Valentich JD, Crowe SE, Saada JI, West AB. Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am J Physiol Cell Physiol 277: C183-C201, 1999.
29. Pruszak J, Ludwig W, Blak A, Alavian K, Isacson O. CD15, CD24 and CD29 define a surface biomarker code for neural lineage differentiation of stem cells. Stem Cells 27: 2928-2940, 2009.
30. Que J, Okubo T, Goldenring JR, Nam KT, Kurotani R, Morrisey EE, Taranova O, Pevny LH, Hogan BL. Multiple dose-dependent roles for Sox2 in the patterning and differentiation of anterior foregut endoderm. Development (Cambridge, UK) 134: 2521-2531, 2007. (Pubitemid 47074146)
31. Riccio O, van Gijn ME, Bezdek AC, Pellegrinet L, van Es JH, Zimber-Strobl U, Strobl LJ, Honjo T, Clevers H, Radtke F. Loss of intestinal crypt progenitor cells owing to inactivation of both Notch1 and Notch2 is accompanied by derepression of CDK inhibitors p27Kip1 and p57Kip2. EMBO Rep 9: 377-383, 2008.
32. Rietze RL, Valcanis H, Brooker GF, Thomas T, Voss AK, Bartlett PF. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature 412: 736-739, 2001. (Pubitemid 32771996)
33. Sagiv E, Memeo L, Karin A, Kazanov D, Jacob-Hirsch J, Mansukhani M, Rechavi G, Hibshoosh H, Arber N. CD24 is a new oncogene, early at the multistep process of colorectal cancer carcinogenesis. Gastroenterology 131: 630-639, 2006. (Pubitemid 44142443)
34. Sammar M, Aigner S, Altevogt P. Heat-stable antigen (mouse CD24) in the brain: dual but distinct interaction with P-selectin and L1. Biochim Biophys Acta 1337: 287-294, 1997. (Pubitemid 27073499)
35. Sangiorgi E, Capecchi MR. Bmi1 is expressed in vivo in intestinal stem cells. Nat Genet 40: 915-920, 2008. (Pubitemid 351913652)
36. Sasaki T, Giltay R, Talts U, Timpl R, Talts JF. Expression and distribution of laminin alpha1 and alpha2 chains in embryonic and adult mouse tissues: an immunochemical approach. Exp Cell Res 275: 185-199, 2002. (Pubitemid 34948361)
37. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265, 2009.
38. Seymour PA, Freude KK, Dubois CL, Shih HP, Patel NA, Sander M. A dosage-dependent requirement for Sox9 in pancreatic endocrine cell formation. Devel Biol 323: 19-30, 2008.
39. Snippert HJ, van Es JH, van den Born M, Begthel H, Stange DE, Barker N, Clevers H. Prominin-1/CD133 marks stem cells and early progenitors in mouse small intestine. Gastroenterology 136: 2187-2194, 2009.
40. Spradling A, Drummond-Barbosa D, Kai T. Stem cells find their niche. Nature 414: 98-104, 2001. (Pubitemid 33041633)
41. Taranova OV, Magness ST, Fagan BM, Wu Y, Surzenko N, Hutton SR, Pevny LH. SOX2 is a dose-dependent regulator of retinal neural progenitor competence. Genes Devel 20: 1187-1202, 2006.
42. Van der Flier LG, Haegebarth A, Stange DE, van de Wetering M, Clevers H. OLFM4 is a robust marker for stem cells in human intestine and marks a subset of colorectal cancer cells. Gastroenterology 137: 15-17, 2009.
43. Van der Flier LG, van Gijn ME, Hatzis P, Kujala P, Haegebarth A, Stange DE, Begthel H, van den Born M, Guryev V, Oving I, van Es JH, Barker N, Peters PJ, van de Wetering M, Clevers H. Transcription factor achaete scute-like 2 controls intestinal stem cell fate. Cell 136: 903-912, 2009.
44. Van Es JH, van Gijn ME, Riccio O, van den Born M, Vooijs M, Begthel H, Cozijnsen M, Robine S, Winton DJ, Radtke F, Clevers H. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435: 959-963, 2005. (Pubitemid 40896322)
45. Wang X, Hu J, Zhao D, Wang G, Tan L, Du L, Yang J, Hou L, Zhang H, Yu Y, Zhang H, Deng H, Ding M. NestinnegCD24low/- population from fetal Nestin-EGFP transgenic mice enriches the pancreatic endocrine progenitor cells. Pancreas 31: 385-391, 2005. (Pubitemid 41566890)
46. Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294: 2155-2158, 2001. (Pubitemid 33150670)