Induction of Fibroblast Growth Factor 10 (FGF10) in the ileal crypt epithelium after massive small bowel resection suggests a role for FGF10 in gut adaptation

Developmental Dynamics

Volumn 238, Issue 2, 2009, Pages 294-301

  Tai, Cindy C ^a   Curtis, Jennifer L ^a   Sala, Frederic G ^b   Del Moral, Pierre M ^b   Chokshi, Nikunj ^a   Kanard, Robert J ^a   Alam, Denise Al ^b   Wang, Jin ^a   Burns, R Cartland ^c   Ford, Henri R ^a   Grishin, Anatoly ^a   Wang, Kasper S ^a   Bellusci, Saverio ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

FGF10; Growth factors; Intestinal adaptation; Short bowel syndrome; Small bowel resection

Indexed keywords

FIBROBLAST GROWTH FACTOR 10; PROTEIN KINASE B; RAF PROTEIN;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM; GOBLET CELL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SMALL INTESTINE RESECTION; STEM CELL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL LINE; CELL PROLIFERATION; FIBROBLAST GROWTH FACTOR 10; GOBLET CELLS; ILEUM; INTESTINAL MUCOSA; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RAF KINASES; RATS; RECOMBINANT PROTEINS;

MUS; RATTUS;

EID: 59649107784     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21667     Document Type: Article

References (49)

1. Amann JM, Chyla BJ, Ellis TC, Martinez A, Moore AC, Franklin JL, McGhee L, Meyers S, Ohm JE, Luce KS, Ouelette AJ, Washington MK, Thompson MA, King D, Gautam S, Coffey RJ, Whitehead RH, Hiebert SW. 2005. Mtgr1 is a transcriptional corepressor that is required for maintenance of the secretory cell lineage in the small intestine. Mol Cell Biol 25:9576-9585.
2. 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. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003-1007.
3. Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL. 1997. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 124:4867-4878.
4. Benhamou PH, Canarelli JP, Richard S, Cordonnier C, Postel JP, Grenier E, Leke A, Dupont C. 1997. Human recombinant growth hormone increases small bowel lengthening after massive small bowel resection in piglets. J Pediatr Surg 32:1332-1336.
5. Berg T, Rountree CB, Lee L, Estrada J, Sala FG, Choe A, Veltmaat JM, De Langhe S, Lee R, Tsukamoto H, Crooks GM, Bellusci S, Wang KS. 2007. Fibroblast growth factor 10 is critical for liver growth during embryogenesis and controls hepatoblast survival via beta-catenin activation. Hepatology 46:1187-1197.
6. Bernal NP, Stehr W, Zhang Y, Profitt S, Erwin CR, Warner BW. 2005. Evidence for active Wnt signaling during post-resection intestinal adaptation. J Pediatr Surg 40:1025-1029; discussion 1029.
7. Bhushan A, Itoh N, Kato S, Thiery JP, Czernichow P, Bellusci S, Scharfmann R. 2001. Fgf10 is essential for maintaining the proliferative capacity of epithelial progenitor cells during early pancreatic organogenesis. Development 128:5109-5117.
8. Burns RC, Fairbanks TJ, Sala F, De Langhe S, Mailleux A, Thiery JP, Dickson C, Itoh N, Warburton D, Anderson KD, Bellusci S. 2004. Requirement for Fibroblast Growth factor 10/ Fibroblast Growth factor receptor 2-IIIb signaling for cecal development in mouse. Dev Biol 265:61-74.
9. Cooper A, Floyd TF, Ross AJ III, Bishop HC, Templeton JM Jr, Ziegler MM. 1984. Morbidity and mortality of short-bowel syndrome acquired in infancy: an update. J Pediatr Surg 19:711-718.
10. De Moerlooze L, Spencer-Dene B, Revest J, Hajihosseini M, Rosewell I, Dickson C. 2000. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127:483-492.
11. Dignass AU, Tsunekawa S, Podolsky DK. 1994. Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology 106:1254-1262.
12. Fairbanks TJ, Sala FG, Kanard R, Curtis JL, Del Moral PM, De Langhe S, Warburton D, Anderson KD, Bellusci S, Burns RC. 2006. The fibroblast growth factor pathway serves a regulatory role in proliferation and apoptosis in the pathogenesis of intestinal atresia. J Pediatr Surg 41:132-136; discussion 132-136.
13. Franke TF, Kaplan DR, Cantley LC. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88:435-437.
14. Goulet O. 1998. Short bowel syndrome in pediatric patients. Nutrition 14:784-787.
15. Hanson WR, Osborne JW, Sharp JG. 1977. Compensation by the residual intestine after intestinal resection in the rat. I. Influence of amount of tissue removed. Gastroenterology 72:692-700.
16. Helmrath MA, VanderKolk WE, Can G, Erwin CR, Warner BW. 1996. Intestinal adaptation following massive small bowel resection in the mouse. J Am Coll Surg 183:441-449.
17. Helmrath MA, Fong JJ, Dekaney CM, Henning SJ. 2007. Rapid expansion of intestinal secretory lineages following a massive small bowel resection in mice. Am J Physiol Gastrointest Liver Physiol 292:G215-G222.
18. Jeppesen PB. 2006. The use of hormonal growth factors in the treatment of patients with short-bowel syndrome. Drugs 66:581-589.
19. Johnson WF, DiPalma CR, Ziegler TR, Scully S, Farrell CL. 2000. Keratinocyte growth factor enhances early gut adaptation in a rat model of short bowel syndrome. Vet Surg 29:17-27.
20. Juno RJ, Knott AW, Profitt SA, Jarboe MD, Zhang Y, Erwin CR, Warner BW. 2004. Preventing enterocyte apoptosis after massive small bowel resection does not enhance adaptation of the intestinal mucosa. J Pediatr Surg 39:907-911; discussion 907-911.
21. Kanard RC, Fairbanks TJ, De Langhe SP, Sala FG, Del Moral PM, Lopez CA, Warburton D, Anderson KD, Bellusci S, Burns RC. 2005. Fibroblast growth factor-10 serves a regulatory role in duodenal development. J Pediatr Surg 40:313-316.
22. Kelly RG, Brown NA, Buckingham ME. 2001. The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev Cell 1:435-440.
23. Lopez-Ilasaca M. 1998. Signaling from G-protein-coupled receptors to mitogen-activated protein (MAP)-kinase cascades. Biochem Pharmacol 56:269-277.
24. Mailleux AA, Kelly R, Veltmaat JM, De Langhe SP, Zaffran S, Thiery JP, Bellusci S. 2005. Fgf10 expression identifies parabronchial smooth muscle cell progenitors and is required for their entry into the smooth muscle cell lineage. Development 132:2157-2166.
25. McDermott FT, Roudnew B. 1977. Ileal epithelial cell migration after 40% small-bowel resection. Autoradiographic studies in the rat. Am J Dig Dis 22:637-640.
26. O'Brien DP, Nelson LA, Stern LE, Williams JL, Kemp CJ, Wang Q, Tso P, Erwin CR, Hasselgren PO, Warner BW. 2001. Epithelial permeability is not increased in rats following small bowel resection. J Surg Res 97:65-70.
27. Obertop H, Nundy S, Malamud D, Malt RA. 1977. Onset of cell proliferation in the shortened gut. Rapid hyperplasia after jejunal resection. Gastroenterology 72:267-270.
28. Ohuchi H, Hori Y, Yamasaki M, Harada H, Sekine K, Kato S, Itoh N (2000). FGF10 acts as a major ligand for FGF receptor 2 IIIb in mouse multi-organ development. Biochem Biophys Res Commun 277:643-639.
29. Ornitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol 2: REVIEWS 3005.
30. Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G, Goldfarb M. 1996. Receptor specificity of the fibroblast growth factor family. J Biol Chem 271:15292-15297.
31. Partanen J, Schwartz L, Rossant J. 1998. Opposite phenotypes of hypomorphic and Y766 phosphorylation site mutations reveal a function for Fgfr1 in anteroposterior patterning of mouse embryos. Genes Dev 12:2332-2344.
32. Pereira PM, Bines JE. 2006. New growth factor therapies aimed at improving intestinal adaptation in short bowel syndrome. J Gastroenterol Hepatol 21:932-940.
33. Quaroni A, Wands J, Trelstad RL, Isselbacher KJ. 1979. Epithelioid cell cultures from rat small intestine. Characterization by morphologic and immunologic criteria. J Cell Biol 80:248-265.
34. Ray EC, Avissar NE, Sax HC. 2002. Growth factor regulation of enterocyte nutrient transport during intestinal adaptation. Am J Surg 183:361-371.
35. Sala FG, Curtis JL, Veltmaat JM, Del Moral PM, Le LT, Fairbanks TJ, Warburton D, Ford H, Wang K, Burns RC, Bellusci S. 2006. Fibroblast growth factor 10 is required for survival and proliferation but not differentiation of intestinal epithelial progenitor cells during murine colon development. Dev Biol 299:373-385.
36. Sasaki H, Hogan BL. 1993. Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118:47-59.
37. Schoeberl B, Eichler-Jonsson C, Gilles ED, Muller G. 2002. Computational modeling of the dynamics of the MAP kinase cascade activated by surface and internalized EGF receptors. Nat Biotechnol 20:370-375.
38. Shaoul E, Reich-Slotky R, Berman B, Ron D. 1995. Fibroblast growth factor receptors display both common and distinct signaling pathways. Oncogene 10:1553-1561.
39. Sigalet DL, Martin GR, Butzner JD, Buret A, Meddings JB. 2005. A pilot study of the use of epidermal growth factor in pediatric short bowel syndrome. J Pediatr Surg 40:763-768.
40. Soo K, O'Rourke KMP, Khoo PL, Steiner KA, Wong N, Behringer RR, Tam PL. 2002. Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev Biol 247:251-270.
41. Stern LE, Erwin CR, O'Brien DP, Huang FS, Warner BW. 2001. Serum from mice after small bowel resection enhances intestinal epithelial cell growth. J Pediatr Surg 36:184-189.
42. Stollman NH, Neustater BR, Rogers AI. 1996. Short-bowel syndrome. Gastroenterologist 4:118-128.
43. Theodorou V, Boer M, Weigelt B, Jonkers J, van der Valk M, Hilkens J. 2004. Fgf10 is an oncogene activated by MMTV insertional mutagenesis in mouse mammary tumors and overexpressed in a subset of human breast carcinomas. Oncogene 23:6047-6055.
44. Veltmaat JM, Relaix F, Le LT, Kratochwil K, Sala FG, van Veelen W, Rice R, Spencer-Dene B, Mailleux AA, Rice DP, Thiery JP, Bellusci S. 2006. Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes. Development 133:2325-2335.
45. Williamson RC. 1978. Intestinal adaptation (first of two parts). Structural, functional and cytokinetic changes. N Engl J Med 298:1393-1402.
46. Yamasaki M, Miyake A, Tagashira S, Itoh N. 1996. Structure and expression of the rat mRNA encoding a novel member of the fibroblast growth factor family. J Biol Chem 271:15918-15921.
47. Yang Q, Bermingham NA, Finegold MJ, Zoghbi HY. 2001. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294:2155-2158.
48. Yang H, Wildhaber BE, Teitelbaum DH. 2003. 2003 Harry M. Vars Research Award. Keratinocyte growth factor improves epithelial function after massive small bowel resection. JPEN J Parenter Enteral Nutr 27:198-206; discussion 206-197.
49. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM. 2006. Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694-15700.