Origin of the brush cell lineage in the mouse intestinal epithelium

Developmental Biology

Volumn 362, Issue 2, 2012, Pages 194-218

  Bjerknes, Matthew ^a   Khandanpour, Cyrus ^b,c,j   Möröy, Tarik ^b,c   Fujiyama, Tomoyuki ^d,e   Hoshino, Mikio ^d   Klisch, Tiemo J ^f   Ding, Qian ^g   Gan, Lin ^g,h   Wang, Jiafang ⁱ   Martín, Martín G ⁱ   Cheng, Hazel ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^e KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f BAYLOR COLLEGE OF MEDICINE   (United States)

^g UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^h UNIVERSITY OF ROCHESTER   (United States)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

^j UNIVERSITY HOSPITAL ESSEN   (Germany)

more..

Author keywords

Atoh1; Brush cell; Gfi1b; Hes1; Intestinal stem cell; Notch signaling; Tuft cell

Indexed keywords

CELL PROTEIN; NOTCH RECEPTOR; PROTEIN ATOH1; PROTEIN GFI1B; TRANSCRIPTION FACTOR HES 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; BRUSH BORDER; CELL COUNT; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; DAUGHTER CELL; FLUORESCENCE ACTIVATED CELL SORTING; INTESTINE EPITHELIUM CELL; MICROSCOPY; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; SIGNAL TRANSDUCTION; STEM CELL; SURVIVAL RATE; WILD TYPE;

EID: 84856089512     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.12.009     Document Type: Article

References (94)

1. Akazawa C., Ishibashi M., Shimizu C., Nakanishi S., Kageyama R. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 1995, 270:8730-8738.
2. Apelqvist Å., Li H., Sommer L., Beatus P., Anderson D.J., Honjo T., Hrabě de Angelis M., Lendahl U., Edlund H. Notch signalling controls pancreatic cell differentiation. Nature 1999, 400:877-881.
3. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
4. Ben-Arie N., Bellen H.J., Armstrong D.L., McCall A.E., Gordadze P.R., Guo Q., Matzuk M.M., Zoghbi H.Y. Math1 is essential for genesis of cerebellar granule neurons. Nature 1997, 390:169-172.
5. Bezençon C., le Coutre J., Damak S. Taste-signaling proteins are coexpressed in solitary intestinal epithelial cells. Chem. Senses 2007, 32:41-49.
6. Bezençon C., Fürholz A., Raymond F., Mansourian R., Métairon S., Le Coutre J., Damak S. Murine intestinal cells expressing Trpm5 are mostly brush cells and express markers of neuronal and inflammatory cells. J. Comp. Neurol. 2008, 509:514-525.
7. Bjerknes M., Cheng H. Stem-cell zone of the small intestinal epithelium. Anat. Rec. 1979, 193:484-485.
8. Bjerknes M., Cheng H. The stem-cell zone of the small intestinal epithelium. I. Evidence from Paneth cells in the adult mouse. Am. J. Anat. 1981, 160:51-63.
9. 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. 1981, 160:77-91.
10. Bjerknes M., Cheng H. Methods for the isolation of intact epithelium from the mouse intestine. Anat. Rec. 1981, 199:565-574.
11. Bjerknes M., Cheng H. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 1999, 116:7-14.
12. Bjerknes M., Cheng H. Gastrointestinal stem cells. II. Intestinal stem cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 289:G381-G387.
13. Bjerknes M., Cheng H. Neurogenin 3 and the enteroendocrine cell lineage in the adult mouse small intestinal epithelium. Dev. Biol. 2006, 300:722-735.
14. Bjerknes M., Cheng H. Intestinal epithelial stem cells and progenitors. Methods Enzymol. 2006, 419:337-383.
15. Bjerknes M., Cheng H. Cell lineage metastability in Gfi1-deficient mouse intestinal epithelium. Dev. Biol. 2010, 345:40-63.
16. Borghesi C., Taussig M.J., Nicoletti C. Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer's patch. Lab. Invest. 1999, 79:1393-1401.
17. Cheng H., Leblond C.P. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am. J. Anat. 1974, 141:461-480.
18. 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, 141:537-562.
19. Corish P., Tyler-Smith C. Attenuation of green fluorescent protein half-life in mammalian cells. Protein Eng. 1999, 12(12):1035-1040.
20. Crosnier C., Vargesson N., Gschmeissner S., Ariza-McNaughton L., Morrison A., Lewis J. Delta-Notch signalling controls commitment to a secretory fate in the zebrafish intestine. Development 2005, 132:1093-1104.
21. Dekaney C.M., Gulati A.S., Garrison A.P., Helmrath M.A., Henning S.J. Regeneration of intestinal stem/progenitor cells following doxorubicin treatment of mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297:G461-G470.
22. Doan L.L., Porter S.D., Duan Z., Flubacher M.M., Montoya D., Tsichlis P.N., Horwitz M., Gilks C.B., Grimes H.L. Targeted transcriptional repression of GFI1 by GFI1 and GFI1B in lymphoid cells. Nucleic Acids Res. 2004, 32:2508-2519.
23. Fortini M.E. Notch signaling: the core pathway and its posttranslational regulation. Dev. Cell 2009, 16:633-647.
24. Fre S., Huyghe M., Mourikis P., Robine S., Louvard D., Artavanis-Tsakonas S. Notch signals control the fate of immature progenitor cells in the intestine. Nature 2005, 435:964-968.
25. Fre S., Pallavi S.K., Huyghe M., Lae M., Janssen K.-P., Robine S., Artavanis-Tsakonas S., Louvard D. Notch and Wnt signals cooperatively control cell proliferation and tumorigenesis in the intestine. Proc. Natl. Acad. Sci. U.S.A. 2009, 6309-6314.
26. Fujiyama T., Yamada M., Terao M., Terashima T., Hioki H., Inoue Y.U., Inoue T., Masuyama N., Obata K., Yanagawa Y., Kawaguchi Y., Nabeshima Y., Hoshino M. Inhibitory and excitatory subtypes of cochlear nucleus neurons are defined by distinct bHLH transcription factors, Ptf1a and Atoh1. Development 2009, 136:2049-2058.
27. Garçon L., Lacout C., Svinartchouk F., Le Couédic J.P., Villeval J.L., Vainchenker W., Duménil D. Gfi-1B plays a critical role in terminal differentiation of normal and transformed erythroid progenitor cells. Blood 2005, 105:1448-1455.
28. Gebert A., Posselt W. Glycoconjugate expression defines the origin and differentiation pathway of intestinal M-cells. J. Histochem. Cytochem. 1997, 45:1341-1350.
29. Gebhard A., Gebert A. Brush cells of the mouse intestine possess a specialized glycocalyx as revealed by quantitative lectin histochemistry. Further evidence for a sensory function. J. Histochem. Cytochem. 1999, 47:799-808.
30. Gerbe F., Brulin B., Makrini L., Legraverend C., Jay P. DCAMKL-1 expression identifies tuft cells rather than stem cells in the adult mouse intestinal epithelium. Gastroenterology 2009, 137:2179-2180.
31. Gerbe F., van Es J.H., Makrini L., Brulin B., Mellitzer G., Robine S., Romagnolo B., Shroyer N.F., Bourgaux J.F., Pignodel C., Clevers H., Jay P. Distinct Atoh1 and Neurog3 requirements define tuft Cells as a new secretory cell type in the intestinal epithelium. J. Cell Biol. 2011, 192:767-780.
32. Giannakis M., Stappenbeck T.S., Mills J.C., Leip D.G., Lovett M., Clifton S.W., Ippolito J.E., Glasscock J.I., Arumugam M., Brent M.R., Gordon J.I. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J. Biol. Chem. 2006, 281:11292-11300.
33. Gierl M.S., Karoulias N., Wende H., Strehle M., Birchmeier C. The zinc-finger factor Insm1 (IA-1) is essential for the development of pancreatic beta cells and intestinal endocrine cells. Genes Dev. 2006, 20:2465-2478.
34. Helms A.W., Johnson J.E. Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development 1998, 125:919-928.
35. Hernandez A., Villegas A., Anguita E. Human promoter mutations unveil Oct-1 and GATA-1 opposite action on Gfi1b regulation. Ann. Hematol. 2010, 89:759-765.
36. Hirata H., Yoshiura S., Ohtsuka T., Bessho Y., Harada T., Yoshikawa K., Kageyama R. Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science 2002, 298:840-843.
37. Höfer D., Drenckhahn D. Cytoskeletal markers allowing discrimination between brush cells and other epithelial cells of the gut including enteroendocrine cells. Histochem. Cell Biol. 1996, 105:405-412.
38. Höfer D., Puschel B., Drenckhahn D. Taste receptor-like cells in the rat gut identified by expression of alpha-gustducin. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:6631-6634.
39. Huang D.Y., Kuo Y.Y., Lai J.S., Suzuki Y., Sugano S., Chang Z.F. GATA-1 and NF-Y cooperate to mediate erythroid-specific transcription of gfi-1b gene. Nucleic Acids Res. 2004, 32:3935-3946.
40. Iseki S., Kanda T., Hitomi M., Ono T. Ontogenic appearance of three fatty acid binding proteins in the rat stomach. Anat. Rec. 1991, 229:51-60.
41. Ito T., Udaka N., Yazawa T., Okudela K., Hayashi H., Sudo T., Guillemot F., Kageyama R., Kitamura H. Basic helix-loop-helix transcription factors regulate the neuroendocrine differentiation of fetal mouse pulmonary epithelium. Development 2000, 127:3913-3921.
42. Jacob J., Storm R., Castro D.S., Milton C., Pla P., Guillemot F., Birchmeier C., Briscoe J. Insm1 (IA-1) is an essential component of the regulatory network that specifies monoaminergic neuronal phenotypes in the vertebrate hindbrain. Development 2009, 136:2477-2485.
43. Jarriault S., Le Bail O., Hirsinger E., Pourquie O., Logeat F., Strong C.F., Brou C., Seidah N.G., Isral A. Delta-1 activation of notch-1 signaling results in HES-1 transactivation. Mol. Cell. Biol. 1998, 18:7423-7431.
44. Jenny M., Uhl C., Roche C., Duluc I., Guillermin V., Guillemot F., Jensen J., Kedinger M., Gradwohl G. Neurogenin3 is differentially required for endocrine cell fate specification in the intestinal and gastric epithelium. EMBO J. 2002, 21:6338-6347.
45. Jensen J., Pedersen E.E., Galante P., Hald J., Heller R.S., Ishibashi M., Kageyama R., Guillemot F., Serup P., Madsen O.D. Control of endodermal endocrine development by Hes-1. Nat. Genet. 2000, 24:36-44.
46. Jin G., Ramanathan V., Quante M., Baik G.H., Yang X., Wang S.S., Tu S., Gordon S.A., Pritchard D.M., Varro A., Shulkes A., Wang T.C. Inactivating cholecystokinin-2 receptor inhibits progastrin-dependent colonic crypt fission, proliferation, and colorectal cancer in mice. J. Clin. Invest. 2009, 119:2691-2701.
47. Kageyama R., Niwa Y., Shimojo H., Kobayashi T., Ohtsuka T. Ultradian oscillations in Notch signaling regulate dynamic biological events. Curr. Top. Dev. Biol. 2010, 92:311-331.
48. Kaske S., Krasteva G., Konig P., Kummer W., Hofmann T., Gudermann T., Chubanov V. TRPM5, a taste-signaling transient receptor potential ion-channel, is a ubiquitous signaling component in chemosensory cells. BMC Neurosci. 2007, 8:49.
49. Kayahara T., Sawada M., Takaishi S., Fukui H., Seno H., Fukuzawa H., Suzuki K., Hiai H., Kageyama R., Okano H., Chiba T. 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.
50. Kerneis S., Bogdanova A., Kraehenbuhl J.P., Pringault E. Conversion by Peyer's patch lymphocytes of human enterocytes into M cells that transport bacteria. Science 1997, 277:949-952.
51. Khandanpour C., Sharif-Askari E., Vassen L., Gaudreau M.C., Zhu J., Paul W.E., Okayama T., Kosan C., Möröy T. Evidence that Growth Factor Independence 1b regulates dormancy and peripheral blood mobilization of hematopoietic stem cells. Blood 2010, 116:5149-5161.
52. Kokrashvili Z., Rodriguez D., Yevshayeva V., Zhou H., Margolskee R.F., Mosinger B. Release of endogenous opioids from duodenal enteroendocrine cells requires Trpm5. Gastroenterology 2009, 137:598-606. 606.e1-2.
53. Laurent B., Randrianarison-Huetz V., Kadri Z., Romeo P.H., Porteu F., Dumenil D. Gfi-1B promoter remains associated with active chromatin marks throughout erythroid differentiation of human primary progenitor cells. Stem Cells 2009, 27:2153-2162.
54. Lee C.S., Perreault N., Brestelli J.E., Kaestner K.H. Neurogenin 3 is essential for the proper specification of gastric enteroendocrine cells and the maintenance of gastric epithelial cell identity. Genes Dev. 2002, 16:1488-1497.
55. Lelouard H., Sahuquet A., Reggio H., Montcourrier P. Rabbit M cells and dome enterocytes are distinct cell lineages. J. Cell Sci. 2001, 114:2077-2083.
56. May R., Riehl T.E., Hunt C., Sureban S.M., Anant S., Houchen C.W. Identification of a novel putative gastrointestinal stem cell and adenoma stem cell marker, doublecortin and CaM kinase-like-1, following radiation injury and in adenomatous polyposis coli/multiple intestinal neoplasia mice. Stem Cells 2008, 26:630-637.
57. May R., Sureban S.M., Hoang N., Riehl T.E., Lightfoot S.A., Ramanujam R., Wyche J.H., Anant S., Houchen C.W. Doublecortin and CaM kinase-like-1 and leucine-rich-repeat-containing G-protein-coupled receptor mark quiescent and cycling intestinal stem cells, respectively. Stem Cells 2009, 27:2571-2579.
58. Micchelli C.A., Perrimon N. Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 2006, 439:475-479.
59. Milano J., McKay J., Dagenais C., Foster-Brown L., Pognan F., Gadient R., Jacobs R.T., Zacco A., Greenberg B., Ciaccio P.J. Modulation of notch processing by gamma-secretase inhibitors causes intestinal goblet cell metaplasia and induction of genes known to specify gut secretory lineage differentiation. Toxicol. Sci. 2004, 82:341-358.
60. Miyazawa K., Aso H., Kanaya T., Kido T., Minashima T., Watanabe K., Ohwada S., Kitazawa H., Rose M.T., Tahara K., Yamasaki T., Yamaguchi T. Apoptotic process of porcine intestinal M cells. Cell Tissue Res. 2006, 323:425-432.
61. Moxey P.C., Trier J.S. Specialized cell types in the human fetal small intestine. Anat. Rec. 1978, 191:269-285.
62. Murtaugh L.C., Stanger B.Z., Kwan K.M., Melton D.A. Notch signaling controls multiple steps of pancreatic differentiation. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:14920-14925.
63. Nabeyama A., Leblond C.P. "Caveolated cells" characterized by deep surface invaginations and abundant filaments in mouse gastro-intestinal epithelia. Am. J. Anat. 1974, 140:147-165.
64. Ohlstein B., Spradling A. Multipotent Drosophila intestinal stem cells specify daughter cell fates by differential notch signaling. Science 2007, 315:988-992.
65. Osawa M., Yamaguchi T., Nakamura Y., Kaneko S., Onodera M., Sawada K., Jegalian A., Wu H., Nakauchi H., Iwama A. Erythroid expansion mediated by the Gfi-1B zinc finger protein: role in normal hematopoiesis. Blood 2002, 100:2769-2777.
66. Randrianarison-Huetz V., Laurent B., Bardet V., Blobe G.C., Huetz F., Dumenil D. Gfi-1B controls human erythroid and megakaryocytic differentiation by regulating TGF-beta signaling at the bipotent erythro-megakaryocytic progenitor stage. Blood 2010, 115:2784-2795.
67. Riccio O., van Gijn M.E., Bezdek A.C., Pellegrinet L., van Es J.H., Zimber-Strobl U., Strobl L.J., 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. 2008, 9:377-383.
68. Rose M.F., Ren J., Ahmad K.A., Chao H.T., Klisch T.J., Flora A., Greer J.J., Zoghbi H.Y. Math1 is essential for the development of hindbrain neurons critical for perinatal breathing. Neuron 2009, 64:341-354.
69. Saleque S., Cameron S., Orkin S.H. The zinc-finger proto-oncogene Gfi-1b is essential for development of the erythroid and megakaryocytic lineages. Genes Dev. 2002, 16:301-306.
70. Saleque S., Kim J., Rooke H.M., Orkin S.H. Epigenetic regulation of hematopoietic differentiation by Gfi-1 and Gfi-1b is mediated by the cofactors CoREST and LSD1. Mol. Cell 2007, 27:562-572.
71. Saqui-Salces M., Keeley T.M., Grosse A.S., Qiao X.T., El-Zaatari M., Gumucio D.L., Samuelson L.C., Merchant J.L. Gastric tuft cells express DCLK1 and are expanded in hyperplasia. Histochem. Cell Biol. 2011, Epub ahead of print. 10.1007/s00418-011-0831-1.
72. Sato A. Tuft cells. Anat. Sci. Int. 2007, 82:187-199.
73. Sato T., Vries R.G., Snippert H.J., van de Wetering M., Barker N., Stange D.E., van Es J.H., Abo A., Kujala P., Peters P.J., Clevers H. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 2009, 459:262-265.
74. Savidge T.C. The life and times of an intestinal M cell. Trends Microbiol. 1996, 4:301-306.
75. Savidge T.C., Smith M.W., James P.S., Aldred P. Salmonella-induced M-cell formation in germ-free mouse Peyer's patch tissue. Am. J. Pathol. 1991, 139:177-184.
76. Sbarbati A., Bramanti P., Benati D., Merigo F. The diffuse chemosensory system: exploring the iceberg toward the definition of functional roles. Prog. Neurobiol. 2010, 91:77-89.
77. Scholzen T., Gerdes J. The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 2000, 182:311-322.
78. Schroder N., Gossler A. Expression of Notch pathway components in fetal and adult mouse small intestine. Gene Expr. Patterns 2002, 2:247-250.
79. Shroyer N.F., Wallis D., Venken K.J., Bellen H.J., Zoghbi H.Y. Gfi1 functions downstream of Math1 to control intestinal secretory cell subtype allocation and differentiation. Genes Dev. 2005, 19:2412-2417.
80. Shroyer N.F., Helmrath M.A., Wang V.Y., Antalffy B., Henning S.J., Zoghbi H.Y. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology 2007, 132:2478-2488.
81. Stanger B.Z., Datar R., Murtaugh L.C., Melton D.A. Direct regulation of intestinal fate by Notch. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12443-12448.
82. Sureban S.M., May R., Ramalingam S., Subramaniam D., Natarajan G., Anant S., Houchen C.W. Selective blockade of DCAMKL-1 results in tumor growth arrest by a Let-7a MicroRNA-dependent mechanism. Gastroenterology 2009, 137:649-659.
83. 3H-thymidine into mice. Am. J. Anat. 1979, 156:431-451.
84. VanDussen K.L., Samuelson L.C. Mouse Atonal homolog 1 directs intestinal progenitors to secretory cell rather than absorptive cell fate. Dev. Biol. 2010, 346:215-223.
85. Vassen L., Fiolka K., Mahlmann S., Moroy T. Direct transcriptional repression of the genes encoding the zinc-finger proteins Gfi1b and Gfi1 by Gfi1b. Nucleic Acids Res. 2005, 33:987-998.
86. Vassen L., Okayama T., Moroy T. Gfi1b:green fluorescent protein knock-in mice reveal a dynamic expression pattern of Gfi1b during hematopoiesis that is largely complementary to Gfi1. Blood 2007, 109:2356-2364.
87. Ventura A., Kirsch D.G., McLaughlin M.E., Tuveson D.A., Grimm J., Lintault L., Newman J., Reczek E.E., Weissleder R., Jacks T. Restoration of p53 function leads to tumor regression in vivo. Nature 2007, 445:661-665.
88. von Furstenberg R.J., Gulati A.S., Baxi A., Doherty J.M., Stappenbeck T.S., Gracz A.D., Magness S.T., Henning S.J. Sorting mouse jejunal epithelial cells with CD24 yields a population with characteristics of intestinal stem cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 300:G409-G417.
89. Watanabe M., Tanaka H., Koizumi H., Tanimoto Y., Torii R., Yanagita T. General toxicity studies of tamoxifen in mice and rats. Jitchuken Zenrinsko Kenkyuko (CIEA Preclinical Reports) 1980, 6:1-36.
90. Wong G.T., Manfra D., Poulet F.M., Zhang Q., Josien H., Bara T., Engstrom L., Pinzon-Ortiz M., Fine J.S., Lee H.J., Zhang L., Higgins G.A., Parker E.M. Chronic treatment with the gamma-secretase inhibitor LY-411,575 inhibits beta-amyloid peptide production and alters lymphopoiesis and intestinal cell differentiation. J. Biol. Chem. Mar. 2004, 279:12876-12882.
91. Wu Y., Cain-Hom C., Choy L., Hagenbeek T.J., de Leon G.P., Chen Y., Finkle D., Venook R., Wu X., Ridgway J., Schahin-Reed D., Dow G.J., Shelton A., Stawicki S., Watts R.J., Zhang J., Choy R., Howard P., Kadyk L., Yan M., Zha J., Callahan C.A., Hymowitz S.G., Siebel C.W. Therapeutic antibody targeting of individual Notch receptors. Nature 2010, 464:1052-1057.
92. Yang Q., Bermingham N.A., Finegold M.J., Zoghbi H.Y. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 2001, 294:2155-2158.
93. Yang H., Xie X., Deng M., Chen X., Gan L. Generation and characterization of Atoh1-Cre knock-in mouse line. Genesis 2010, 48:407-413.
94. Zahn S., Hecksher-Sørensen J., Pedersen I.L., Serup P., Madsen O. Generation of monoclonal antibodies against mouse neurogenin 3: a new immunocytochemical tool to study the pancreatic endocrine progenitor cell. Hybrid. Hybridomics 2004, 23:385-388.