Bile salt dependent lipase promotes intestinal adaptation in rats with massive small bowel resection

Bioscience Reports

Volumn 38, Issue 3, 2018, Pages

  Yang, Yi ^a   Zheng, Tao ^a   Zhou, Jiefei ^a   Song, Huanlei ^a   Cai, Wei ^a   Qian, Linxi ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MEMBRANE PROTEIN; PROTEIN LGR5; RECOMBINANT BILE SALT DEPENDENT LIPASE; RECOMBINANT ENZYME; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN; BILE ACID; BILE SALT-STIMULATED LIPASE; CHOLESTEROL ESTERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT GAIN; CELL PROLIFERATION; CONTROLLED STUDY; DRUG MECHANISM; ENTERAL DRUG ADMINISTRATION; ENZYME ACTIVITY; FOOD INTAKE; GUT BARRIER FUNCTION; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INTESTINAL ADAPTIVE GROWTH; INTESTINE ADAPTATION; INTESTINE ANASTOMOSIS; INTESTINE CELL; INTESTINE CRYPT DEPTH; INTESTINE FUNCTION; INTESTINE MUCOSA PERMEABILITY; INTESTINE PARAMETERS; INTESTINE VILLUS HEIGHT; MALE; MORNING DOSAGE; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; POSTOPERATIVE PERIOD; PROTEIN EXPRESSION; RAT; SHORT BOWEL SYNDROME; SMALL INTESTINE RESECTION; SPRAGUE DAWLEY RAT; TISSUE REGENERATION; TREATMENT DURATION; WESTERN BLOTTING; WNT SIGNALING; ANIMAL; APOPTOSIS; DISEASE MODEL; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; INTESTINE; INTESTINE MUCOSA; PATHOLOGY; SMALL INTESTINE; SURGERY;

ANIMALS; APOPTOSIS; BILE ACIDS AND SALTS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOMODULATION; INTESTINAL MUCOSA; INTESTINE, SMALL; INTESTINES; RATS; RATS, SPRAGUE-DAWLEY; SHORT BOWEL SYNDROME; STEROL ESTERASE;

EID: 85047904270     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20180077     Document Type: Article

References (61)

1. Kelly, D.G., Tappenden, K.A. and Winkler, M.F. (2014) Short bowel syndrome: highlights of patient management, quality of life, and survival. JPEN J. Parenter. Enteral Nutr. 38, 427–437, https://doi.org/10.1177/0148607113512678
2. Goulet, O., Olieman, J., Ksiazyk, J., Spolidoro, J., Tibboe, D., Kohler, H. et al. (2013) Neonatal short bowel syndrome as a model of intestinal failure: physiological background for enteral feeding. Clin. Nutr. 32, 162–171, https://doi.org/10.1016/j.clnu.2012.09.007
3. Booth, I.W. and Lander, A.D. (1998) Short bowel syndrome. Baillieres Clin. Gastroenterol. 12, 739–773, https://doi.org/10.1016/S0950-3528(98)90006-9
4. Kocoshis, S.A. (2010) Medical management of pediatric intestinal failure. Semin. Pediatr. Surg. 19, 20–26, https://doi.org/10.1053/j.sempedsurg.2009.11.003
5. Tappenden, K.A. (2014) Intestinal adaptation following resection. JPEN J. Parenter. Enteral Nutr. 38, 23S–31S, https://doi.org/10.1177/0148607114525210
6. Suri, M., Turner, J.M., Sigalet, D.L., Wizzard, P.R., Nation, P.N., Ball, R.O. et al. (2014) Exogenous glucagon-like peptide-2 improves outcomes of intestinal adaptation in a distal-intestinal resection neonatal piglet model of short bowel syndrome. Pediatr. Res. 76, 370–377, https://doi.org/10.1038/pr.2014.97
7. Okawada, M., Holst, J.J. and Teitelbaum, D.H. (2011) Administration of a dipeptidyl peptidase IV inhibitor enhances the intestinal adaptation in a mouse model of short bowel syndrome. Surgery 150, 217–223, https://doi.org/10.1016/j.surg.2011.05.013
8. Wu, J., Chen, J., Wu, W., Shi, J., Zhong, Y., van Tol, E.A. et al. (2014) Enteral supplementation of bovine lactoferrin improves gut barrier function in rats after massive bowel resection. Br. J. Nutr. 112, 486–492, https://doi.org/10.1017/S000711451400107X
9. McKillop, A.M., O’Hare, M.M., Craig, J.S. and Halliday, H.L. (2004) Characterization of the C-terminal region of molecular forms of human milk bile salt-stimulated lipase. Acta Paediatr. 93, 10–16, https://doi.org/10.1111/j.1651-2227.2004.tb00666.x
10. Blackberg, L., Angquist, K.A. and Hernell, O. (1987) Bile-salt-stimulated lipase in human milk: evidence for its synthesis in the lactating mammary gland. FEBS Lett. 217, 37–41, https://doi.org/10.1016/0014-5793(87)81237-1
11. Stromqvist, M., Lindgren, K., Hansson, L. and Juneblad, K. (1995) Differences in the glycosylation of recombinant and native human milk bile salt-stimulated lipase revealed by peptide mapping. J. Chromatogr. A. 718, 53–58, https://doi.org/10.1016/0021-9673(95)00632-X
12. Lombardo, D. and Guy, O. (1980) Studies on the substrate specificity of a carboxyl ester hydrolase from human pancreatic juice. II. Action on cholesterol esters and lipid-soluble vitamin esters. Biochim. Biophys. Acta 611, 147–155, https://doi.org/10.1016/0005-2744(80)90050-9
13. Howles, P.N., Carter, C.P. and Hui, D.Y. (1996) Dietary free and esterified cholesterol absorption in cholesterol esterase (bile salt-stimulated lipase) gene-targeted mice. J. Biol. Chem. 271, 7196–7202, https://doi.org/10.1074/jbc.271.12.7196
14. Al-Ansari, N., Xu, G., Kollman-Bauerly, K., Coppola, C., Shefer, S., Ujhazy, P. et al. (2002) Analysis of the effect of intestinal resection on rat ileal bile Acid transporter expression and on bile Acid and cholesterol homeostasis. Pediatr. Res. 52, 286–291, https://doi.org/10.1203/00006450-200208000-00023
15. Tilson, M.D., Boyer, J.L. and Wright, H.K. (1975) Jejunal absorption of bile salts after resection of the ileum. Surgery 77, 231–234
16. Weser, E., Heller, R. and Tawil, T. (1977) Stimulation of mucosal growth in the rat ileum by bile and pancreatic secretions after jejunal resection. Gastroenterology 73, 524–529
17. Biller, J.A. (1987) Short bowel syndrome. In Pediatric Nutrition. Theory and Practice (Grand, R.I., Sutphen, J.L. and Dietz, W.H., eds), pp. 481–487, Butterworth, Stoneham, MA
18. Sukhotnik, I., Gork, A.S., Chen, M., Drongowski, R.A., Coran, A.G. and Harmon, C.M. (2003) Effect of a high fat diet on lipid absorption and fatty acid transport in a rat model of short bowel syndrome. Pediatr. Surg. Int. 19, 385–390, https://doi.org/10.1007/s00383-003-1016-3
19. Sukhotnik, I., Mor-Vaknin, N., Drongowski, R.A., Miselevich, I., Coran, A.G. and Harmon, C.M. (2004) Effect of dietary fat on early morphological intestinal adaptation in a rat with short bowel syndrome. Pediatr. Surg. Int. 20, 419–424, https://doi.org/10.1007/s00383-004-1168-9
20. Auge, N., Rebai, O., Lepetit-Thevenin, J., Bruneau, N., Thiers, J.C., Mas, E. et al. (2003) Pancreatic bile salt-dependent lipase induces smooth muscle cells proliferation. Circulation 108, 86–91, https://doi.org/10.1161/01.CIR.0000079101.69806.47
21. Howles, P.N., Stemmerman, G.N., Fenoglio-Preiser, C.M. and Hui, D.Y. (1999) Carboxyl ester lipase activity in milk prevents fat-derived intestinal injury in neonatal mice. Am. J. Physiol. 277, G653–G661
22. Rebai, O., Le Petit-Thevenin, J., Bruneau, N., Lombardo, D. and Verine, A. (2005) In vitro angiogenic effects of pancreatic bile salt-dependent lipase. Arterioscler. Thromb. Vasc. Biol. 25, 359–364, https://doi.org/10.1161/01.ATV.0000151618.49109.bd
23. Bernal, N.P., Stehr, W., Zhang, Y., Profitt, S., Erwin, C.R. and Warner, B.W. (2005) Evidence for active Wnt signaling during postresection intestinal adaptation. J. Pediatr. Surg. 40, 1025–1029, https://doi.org/10.1016/j.jpedsurg.2005.03.021
24. Hagen, T. and Vidal-Puig, A. (2002) Characterisation of the phosphorylation of beta-catenin at the GSK-3 priming site Ser45. Biochem. Biophys. Res. Commun. 294, 324–328, https://doi.org/10.1016/S0006-291X(02)00485-0
25. Orford, K., Crockett, C., Jensen, J.P., Weissman, A.M. and Byers, S.W. (1997) Serine phosphorylation-regulated ubiquitination and degradation of beta-catenin. J. Biol. Chem. 272, 24735–24738, https://doi.org/10.1074/jbc.272.40.24735
26. Zeng, X., Tamai, K., Doble, B., Li, S., Huang, H., Habas, R. et al. (2005) A dual-kinase mechanism for Wnt co-receptor phosphorylation and activation. Nature 438, 873–877, https://doi.org/10.1038/nature04185
27. Bruneau, N., Nganga, A., Bendayan, M. and Lombardo, D. (2001) Transcytosis of pancreatic bile salt-dependent lipase through human Int407 intestinal cells. Exp. Cell Res. 271, 94–108, https://doi.org/10.1006/excr.2001.5361
28. Dubois, L., Lecourtois, M., Alexandre, C., Hirst, E. and Vincent, J.P. (2001) Regulated endocytic routing modulates wingless signaling in Drosophila embryos. Cell 105, 613–624, https://doi.org/10.1016/S0092-8674(01)00375-0
29. Blitzer, J.T. and Nusse, R. (2006) A critical role for endocytosis in Wnt signaling. BMC Cell Biol. 7, 28, https://doi.org/10.1186/1471-2121-7-28
30. Crescence, L., Beraud, E., Sbarra, V., Bernard, J.P., Lombardo, D. and Mas, E. (2012) Targeting a novel onco-glycoprotein antigen at tumoral pancreatic cell surface by mAb16D10 induces cell death. J. Immunol. 189, 3386–3396, https://doi.org/10.4049/jimmunol.1102647
31. Vanderhoof, J.A. (1996) Short bowel syndrome. Clin. Perinatol. 23, 377–386
32. Teltschik, Z., Wiest, R., Beisner, J., Nuding, S., Hofmann, C., Schoelmerich, J. et al. (2012) Intestinal bacterial translocation in rats with cirrhosis is related to compromised Paneth cell antimicrobial host defense. Hepatology 55, 1154–1163, https://doi.org/10.1002/hep.24789
33. Mao, J., Hu, X., Xiao, Y., Yang, C., Ding, Y., Hou, N. et al. (2013) Overnutrition stimulates intestinal epithelium proliferation through beta-catenin signaling in obese mice. Diabetes 62, 3736–3746, https://doi.org/10.2337/db13-0035
34. Ring, A., Kim, Y.M. and Kahn, M. (2014) Wnt/catenin signaling in adult stem cell physiology and disease. Stem Cell Rev. 10, 512–525, https://doi.org/10.1007/s12015-014-9515-2
35. Miki, T., Yasuda, S.Y. and Kahn, M. (2011) Wnt/beta-catenin signaling in embryonic stem cell self-renewal and somatic cell reprogramming. Stem Cell Rev. 7, 836–846, https://doi.org/10.1007/s12015-011-9275-1
36. Barker, N., Ridgway, R.A., van Es, J.H., van de Wetering, M., Begthel, H., van den Born, M. et al. (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457, 608–611, https://doi.org/10.1038/nature07602
37. de Lau, W., Barker, N., Low, T.Y., Koo, B.K., Li, V.S., Teunissen, H. et al. (2011) Lgr5 homologues associate with Wnt receptors and mediate R-spondin signalling. Nature 476, 293–297, https://doi.org/10.1038/nature10337
38. Potten, C.S. (1990) A comprehensive study of the radiobiological response of the murine (BDF1) small intestine. Int. J. Radiat. Biol. 58, 925–973, https://doi.org/10.1080/09553009014552281
39. Cosentino, L., Shaver-Walker, P. and Heddle, J.A. (1996) The relationships among stem cells, crypts, and villi in the small intestine of mice as determined by mutation tagging. Dev. Dyn. 207, 420–428, https://doi.org/10.1002/(SICI)1097-0177(199612)207:4%3c420::AID-AJA6%3e3.0.CO;2-J
40. Fontbonne, H., Brisson, L., Verine, A., Puigserver, A., Lombardo, D. and Ajandouz el, H. (2011) Human bile salt-dependent lipase efficiency on medium-chain acyl-containing substrates: control by sodium taurocholate. J. Biochem. 149, 145–151, https://doi.org/10.1093/jb/mvq132
41. Comte, B., Franceschi, C., Sadoulet, M.O., Silvy, F., Lafitte, D., Benkoel, L. et al. (2006) Detection of bile salt-dependent lipase, a 110 kDa pancreatic protein, in urines of healthy subjects. Kidney Int. 69, 1048–1055, https://doi.org/10.1038/sj.ki.5000133
42. Wang, Y., Sheng, Z., Wang, Y., Li, Q., Gao, Y., Wang, Y. et al. (2015) Transgenic mouse milk expressing human bile salt-stimulated lipase improves the survival and growth status of premature mice. Mol. Biotechnol. 57, 287–297, https://doi.org/10.1007/s12033-014-9822-5
43. Casper, C., Carnielli, V.P., Hascoet, J.M., Lapillonne, A., Maggio, L., Timdahl, K. et al. (2014) rhBSSL improves growth and LCPUFA absorption in preterm infants fed formula or pasteurized breast milk. J. Pediatr. Gastroenterol. Nutr. 59, 61–69, https://doi.org/10.1097/MPG.0000000000000365
44. Casper, C., Hascoet, J.M., Ertl, T., Gadzinowski, J.S., Carnielli, V., Rigo, J. et al. (2016) Recombinant bile salt-stimulated lipase in preterm infant feeding: a randomized phase 3 study. PLoS ONE 11, e0156071, https://doi.org/10.1371/journal.pone.0156071
45. Booth, I.W. (1994) Enteral nutrition as primary therapy in short bowel syndrome. Gut 35 (1 Suppl.), S69–S72, https://doi.org/10.1136/gut.35.1Suppl.S69
46. Matarese, L.E. (2013) Nutrition and fluid optimization for patients with short bowel syndrome. JPEN J. Parenter. Enteral Nutr. 37, 161–170, https://doi.org/10.1177/0148607112469818
47. Ben Lulu, S., Coran, A.G., Shehadeh, N., Shamir, R., Mogilner, J.G. and Sukhotnik, I. (2012) Oral insulin stimulates intestinal epithelial cell turnover following massive small bowel resection in a rat and a cell culture model. Pediatr. Surg. Int. 28, 179–187, https://doi.org/10.1007/s00383-011-2991-4
48. Weale, A.R., Edwards, A.G., Bailey, M. and Lear, P.A. (2005) Intestinal adaptation after massive intestinal resection. Postgrad. Med. J. 81, 178–184, https://doi.org/10.1136/pgmj.2004.023846
49. Mogilner, J.G., Srugo, I., Lurie, M., Shaoul, R., Coran, A.G., Shiloni, E. et al. (2007) Effect of probiotics on intestinal regrowth and bacterial translocation after massive small bowel resection in a rat. J. Pediatr. Surg. 42, 1365–1371, https://doi.org/10.1016/j.jpedsurg.2007.03.035
50. Garcia-Urkia, N., Asensio, A.B., Zubillaga Azpiroz, I., Zubillaga Huici, P., Vidales, C., Garcia-Arenzana, J.M. et al. (2002) Beneficial effects of Bifidobacterium lactis in the prevention of bacterial translocation in experimental short bowel syndrome. Circ. Pediatr. 15, 162–165
51. Quigley, E.M. and Quera, R. (2006) Small intestinal bacterial overgrowth: roles of antibiotics, prebiotics, and probiotics. Gastroenterology 130, S78–S90, https://doi.org/10.1053/j.gastro.2005.11.046
52. Ulluwishewa, D., Anderson, R.C., McNabb, W.C., Moughan, P.J., Wells, J.M. and Roy, N.C. (2011) Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr. 141, 769–776, https://doi.org/10.3945/jn.110.135657
53. Okamoto, R. and Watanabe, M. (2004) Molecular and clinical basis for the regeneration of human gastrointestinal epithelia. J. Gastroenterol. 39, 1–6, https://doi.org/10.1007/s00535-003-1259-8
54. Sukhotnik, I., Roitburt, A., Pollak, Y., Dorfman, T., Matter, I., Mogilner, J.G. et al. (2014) Wnt/beta-catenin signaling cascade down-regulation following massive small bowel resection in a rat. Pediatr. Surg. Int. 30, 173–180, https://doi.org/10.1007/s00383-013-3447-9
55. Park, C.S., Kim, S.I., Lee, M.S., Youn, C.Y., Kim, D.J., Jho, E.H. et al. (2004) Modulation of beta-catenin phosphorylation/degradation by cyclin-dependent kinase 2. J. Biol. Chem. 279, 19592–19599, https://doi.org/10.1074/jbc.M314208200
56. Bjerknes, M. and Cheng, H. (2005) Gastrointestinal stem cells. II. Intestinal stem cells. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G381–G387, https://doi.org/10.1152/ajpgi.00160.2005
57. Dekaney, C.M., Fong, J.J., Rigby, R.J., Lund, P.K., Henning, S.J. and Helmrath, M.A. (2007) Expansion of intestinal stem cells associated with long-term adaptation following ileocecal resection in mice. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G1013–G1022, https://doi.org/10.1152/ajpgi.00218.2007
58. Schall, K.A., Holoyda, K.A., Grant, C.N., Levin, D.E., Torres, E.R., Maxwell, A. et al. (2015) Adult zebrafish intestine resection: a novel model of short bowel syndrome, adaptation, and intestinal stem cell regeneration. Am. J. Physiol. Gastrointest. Liver Physiol. 309, G135–G145, https://doi.org/10.1152/ajpgi.00311.2014
59. Cummins, A.G., Catto-Smith, A.G., Cameron, D.J., Couper, R.T., Davidson, G.P., Day, A.S. et al. (2008) Crypt fission peaks early during infancy and crypt hyperplasia broadly peaks during infancy and childhood in the small intestine of humans. J. Pediatr. Gastroenterol. Nutr. 47, 153–157, https://doi.org/10.1097/MPG.0b013e3181604d27
60. Booth, C., Booth, D., Williamson, S., Demchyshyn, L.L. and Potten, C.S. (2004) Teduglutide ([Gly2]GLP-2) protects small intestinal stem cells from radiation damage. Cell Prolif. 37, 385–400, https://doi.org/10.1111/j.1365-2184.2004.00320.x
61. Chen, Q., Cao, H.Z. and Zheng, P.S. (2014) LGR5 promotes the proliferation and tumor formation of cervical cancer cells through the Wnt/beta-catenin signaling pathway. Oncotarget 5, 9092–9105