Paneth cells expand from newly created and preexisting cells during repair after doxorubicin-induced damage

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 305, Issue 2, 2013, Pages

  King, Stephanie L ^a   Mohiuddin, Jahan J ^a   Dekaney, Christopher M ^a  

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

Author keywords

Doxorubicin; Intermediate cell; Paneth cell

Indexed keywords

DOXORUBICIN; EPHRIN RECEPTOR B3; FIBROBLAST GROWTH FACTOR 18; FIBROBLAST GROWTH FACTOR 9; MESSENGER RNA; SONIC HEDGEHOG PROTEIN; THYMIDINE; TRANSCRIPTION FACTOR SOX9; WNT5A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL EXPANSION; CELL REGENERATION; CELL STRUCTURE; CONTROLLED STUDY; CYTOTOXICITY; FEMALE; GENE EXPRESSION; GOBLET CELL; HEDGEHOG; HUMAN; INTESTINE; INTESTINE MUCOSA; MOUSE; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING;

DOXORUBICIN; INTERMEDIATE CELL; PANETH CELL;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BETA CATENIN; DOXORUBICIN; FEMALE; FIBROBLAST GROWTH FACTORS; INTESTINAL MUCOSA; INTESTINES; MICE; MICE, INBRED C57BL; PANETH CELLS; RNA, MESSENGER; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 84880154128     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00441.2012     Document Type: Article

References (45)

1. Andreu P, Colnot S, Godard C, Gad S, Chafey P, Niwa-Kawakita M, Laurent-Puig P, Kahn A, Robine S, Perret C, Romagnolo B. Cryptrestricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development 132: 1443-1451, 2005.
2. Ayabe T, Satchell DP, Wilson CL, Parks WC, Selsted ME, Ouellette AJ. Secretion of microbicidal α-defensins by intestinal Paneth cells in response to bacteria. Nat Immunol 1: 113-118, 2000.
3. 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.
4. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, Clevers H. β-Catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111: 251-263, 2002.
5. 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 160: 51-63, 1981.
6. Bjerknes M, Cheng H. The stem-cell zone of the small intestinal epithelium. II. Evidence from Paneth cells in the newborn mouse. Am J Anat 160: 65-75, 1981.
7. Brodrick B, Vidrich A, Porter E, Bradley L, Buzan JM, Cohn SM. Fibroblast growth factor receptor-3 regulates expression of Paneth cell lineage specific genes in intestinal epithelial cells through both TCF4/β-catenin-dependent and-independent signaling pathways. J Biol Chem 286: 18515-18525, 2011.
8. Corredor J, Yan F, Shen CC, Tong W, John SK, Wilson G, Whitehead R, Polk DB. Tumor necrosis factor regulates intestinal epithelial cell migration by receptor-dependent mechanisms. Am J Physiol Cell Physiol 284: C953-C961, 2003.
9. Dekaney CM, Gulati AS, Garrison AP, Helmrath MA, Henning SJ. Regeneration of intestinal stem/progenitor cells following doxorubicin treatment of mice. Am J Physiol Gastrointest Liver Physiol 297: G461-G470, 2009.
10. Farin HF, van Es JH, Clevers H. Redundant sources of Wnt regulate intestinal stem cells and promote formation of Paneth cells. Gastroenterology 143: 1518-1529, 2012.
11. Fiorica-Howells E, Hen R, Gingrich J, Li Z, Gershon MD. 5-HT2A receptors: location and functional analysis in intestines of wild-type and 5-HT2A knockout mice. Am J Physiol Gastrointest Liver Physiol 282: G877-G893, 2002.
12. 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.
13. Fukuzawa H, Sawada M, Kayahara T, Morita-Fujisawa Y, Suzuki K, Seno H, Takaishi S, Chiba T. Identification of GM-CSF in Paneth cells using single-cell RT-PCR. Biochem Biophys Res Commun 312: 897-902, 2003.
14. Garabedian EM, Roberts LJ, McNevin MS, Gordon JI. Examining the role of Paneth cells in the small intestine by lineage ablation in transgenic mice. J Biol Chem 272: 23729-23740, 1997.
15. Helmrath MA, Fong JJ, Dekaney CM, Henning SJ. Rapid expansion of intestinal secretory lineages following a massive small bowel resection in mice. Am J Physiol Gastrointest Liver Physiol 292: G215-G222, 2007.
16. Huynh D, Dai XM, Nandi S, Lightowler S, Trivett M, Chan CK, Bertoncello I, Ramsay RG, Stanley ER. Colony stimulating factor-1 dependence of Paneth cell development in the mouse small intestine. Gastroenterology 137: 136-144, 2009.
17. Kamal M, Dehlawi MS, Brunet LR, Wakelin D. Paneth and intermediate cell hyperplasia induced in mice by helminth infections. Parasitology 125: 275-281, 2002.
18. Kim TH, Escudero S, Shivdasani RA. Intact function of Lgr5 receptorexpressing intestinal stem cells in the absence of Paneth cells. Proc Natl Acad Sci USA 109: 3932-3937, 2012.
19. Kosinski C, Stange DE, Xu C, Chan AS, Ho C, Yuen ST, Mifflin RC, Powell DW, Clevers H, Leung SY, Chen X. Indian hedgehog regulates intestinal stem cell fate through epithelial-mesenchymal interactions during development. Gastroenterology 139: 893-903, 2010.
20. Lennerz JK, Kim SH, Oates EL, Huh WJ, Doherty JM, Tian X, Bredemeyer AJ, Goldenring JR, Lauwers GY, Shin YK, Mills JC. The transcription factor MIST1 is a novel human gastric chief cell marker whose expression is lost in metaplasia, dysplasia, and carcinoma. Am J Pathol 177: 1514-1533, 2010.
21. Mills JC, Taghert PH. Scaling factors: transcription factors regulating subcellular domains. Bioessays 34: 10-16, 2012.
22. Mori-Akiyama Y, van den BM, 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.
23. Noah TK, Kazanjian A, Whitsett J, Shroyer NF. SAM pointed domain ETS factor (SPDEF) regulates terminal differentiation and maturation of intestinal goblet cells. Exp Cell Res 316: 452-465, 2010.
24. Pin CL, Bonvissuto AC, Konieczny SF. Mist1 expression is a common link among serous exocrine cells exhibiting regulated exocytosis. Anat Rec 259: 157-167, 2000.
25. Porter EM, Bevins CL, Ghosh D, Ganz T. The multifaceted Paneth cell. Cell Mol Life Sci 59: 156-170, 2002.
26. Poulsen SS, Kryger-Baggesen N, Nexo E. Immunohistochemical localization of epidermal growth factor in the second-trimester human fetus. Histochem Cell Biol 105: 111-117, 1996.
27. Poulsen SS, Nexo E, Olsen PS, Hess J, Kirkegaard P. Immunohistochemical localization of epidermal growth factor in rat and man. Histochemistry 85: 389-394, 1986.
28. Ramsey VG, Doherty JM, Chen CC, Stappenbeck TS, Konieczny SF, Mills JC. The maturation of mucus-secreting gastric epithelial progenitors into digestive-enzyme secreting zymogenic cells requires Mist1. Development 134: 211-222, 2007.
29. Sato T, van Es JH, Snippert HJ, Stange DE, Vries RG, van den Born M, Barker N, Shroyer NF, van de Wetering M, Clevers H. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature 469: 415-418, 2011.
30. Seno H, Sawada M, Fukuzawa H, Morita Y, Takaishi S, Hiai H, Chiba T. Enhanced expression of transforming growth factor (TGF)-α precursor and TGF-β1 during Paneth cell regeneration. Dig Dis Sci 46: 1004-1010, 2001.
31. Tanaka M, Riddell RH, Saito H, Soma Y, Hidaka H, Kudo H. Morphologic criteria applicable to biopsy specimens for effective distinction of inflammatory bowel disease from other forms of colitis and of Crohn's disease from ulcerative colitis. Scand J Gastroenterol 34: 55-67, 1999.
32. Van der Flier LG, Sabates-Bellver J, Oving I, Haegebarth A, De Palo M, Anti M, van Gijn ME, Suijkerbuijk S, van de WM, Marra G, Clevers H. The intestinal Wnt/TCF signature. Gastroenterology 132: 628-632, 2007.
33. van Dop WA, Heijmans J, Buller NV, Snoek SA, Rosekrans SL, Wassenberg EA, van den Bergh Weerman MA, Lanske B, Clarke AR, Winton DJ, Wijgerde M, Offerhaus GJ, Hommes DW, Hardwick JC, de Jonge WJ, Biemond I, van den Brink GR. Loss of Indian hedgehog activates multiple aspects of a wound healing response in the mouse intestine. Gastroenterology 139: 1665-1676, 2010.
34. van Es JH, Jay P, Gregorieff A, van Gijn ME, Jonkheer S, Hatzis P, Thiele A, van den BM, Begthel H, Brabletz T, Taketo MM, Clevers H. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 7: 381-386, 2005.
35. Van Landeghem L, Santoro MA, Krebs AE, Mah AT, Dehmer JJ, Gracz AD, Scull BP, McNaughton K, Magness ST, Lund PK. Activation of two distinct Sox9-EGFP-expressing intestinal stem cell populations during crypt regeneration after irradiation. Am J Physiol Gastrointest Liver Physiol 302: G1111-G1132, 2012.
36. VanDussen KL, Carulli AJ, Keeley TM, Patel SR, Puthoff BJ, Magness ST, Tran IT, Maillard I, Siebel C, Kolterud A, Grosse AS, Gumucio DL, Ernst SA, Tsai YH, Dempsey PJ, Samuelson LC. Notch signaling modulates proliferation and differentiation of intestinal crypt base columnar stem cells. Development 139: 488-497, 2012.
37. Varnat F, Heggeler BB, Grisel P, Boucard N, Corthesy-Theulaz I, Wahli W, Desvergne B. PPARβ/δ regulates Paneth cell differentiation via controlling the hedgehog signaling pathway. Gastroenterology 131: 538-553, 2006.
38. Verburg M, Renes IB, Meijer HP, Taminiau JA, Buller HA, Einerhand AW, Dekker J. Selective sparing of goblet cells and Paneth cells in the intestine of methotrexate-treated rats. Am J Physiol Gastrointest Liver Physiol 279: G1037-G1047, 2000.
39. Vidrich A, Buzan JM, Barnes S, Reuter BK, Skaar K, Ilo C, Cominelli F, Pizarro T, Cohn SM. Altered epithelial cell lineage allocation and global expansion of the crypt epithelial stem cell population are associated with ileitis in SAMP1/YitFc mice. Am J Pathol 166: 1055-1067, 2005.
40. Vidrich A, Buzan JM, Brodrick B, Ilo C, Bradley L, Fendig KS, Sturgill T, Cohn SM. Fibroblast growth factor receptor-3 regulates Paneth cell lineage allocation and accrual of epithelial stem cells during murine intestinal development. Am J Physiol Gastrointest Liver Physiol 297: G168-G178, 2009.
41. von Furstenberg RJ, Gulati AS, Baxi A, Doherty JM, Stappenbeck TS, Gracz AD, Magness ST, Henning SJ. Sorting mouse jejunal epithelial cells with CD24 yields a population with characteristics of intestinal stem cells. Am J Physiol Gastrointest Liver Physiol 300: G409-G417, 2011.
42. Walsh R, Seth R, Behnke J, Potten CS, Mahida YR. Epithelial stem cell-related alterations in Trichinella spiralis-infected small intestine. Cell Prolif 42: 394-403, 2009.
43. Wong WM, Stamp GW, Elia G, Poulsom R, Wright NA. Proliferative populations in intestinal metaplasia: evidence of deregulation in Paneth and goblet cells, but not endocrine cells. J Pathol 190: 107-113, 2000.
44. Yang Q, Bermingham NA, Finegold M, Zoghbi HY. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294: 2155-2158, 2001.
45. Zhao J, de Vera J, Narushima S, Beck EX, Palencia S, Shinkawa P, Kim KA, Liu Y, Levy MD, Berg DJ, Abo A, Funk WD. R-spondin1, a novel intestinotrophic mitogen, ameliorates experimental colitis in mice. Gastroenterology 132: 1331-1343, 2007.