Heparin-binding epidermal growth factor-like growth factor protects rat intestine from ischemia/reperfusion injury

Journal of Surgical Research

Volumn 87, Issue 2, 1999, Pages 225-231

  Pillai, Srikumar B ^a   Hinman, Christina E ^a   Luquette, Mark H ^a   Nowicki, Philip T ^a   Besner, Gail E ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Epidermal growth factor receptor; Heparin binding epidermal growth factor like growth factor; Intestine; Ischemia reperfusion injury; Mucosa; Protection

Indexed keywords

EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DISEASE SEVERITY; INTESTINE INJURY; INTESTINE ISCHEMIA; INTESTINE MUCOSA; MORTALITY; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION; WEIGHT GAIN;

EID: 0033404844     PISSN: 00224804     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsre.1999.5764     Document Type: Article

References (50)

1. Andersson R., Parsson H., Isaksson B., Norgren I. Acute intestinal ischemia: A 14 year retrospective investigation. Acta Chir. Scand. 150:1984;217.
2. Chiu C.-J., McArdle A. H., Brown R., Scott H. J., Gurd F. N. Intestinal mucosal lesion in low-flow states. Arch. Surg. 101:1970;478.
3. Parks D. A., Granger D. N. Contributions of ischemia and reperfusion to mucosal lesion formation. Am. J. Physiol. 250:1986;749.
4. Illyes G., Hamar J. Sequence of morphological alterations in a small intestinal ischemia/reperfusion model of the anesthetized rat: A light microscopy study. Int. J. Exp. Pathol. 73:1992;161.
5. Nilsson U. A., Schoenberg M. H., Aneman A., Poch B., Magadum S., Beger H. G., Lundgren O. Free radicals and pathogenesis during ischemia and reperfusion of the rat small intestine. Gastroenterology. 106:1994;629.
6. Thompson J. S. Differential effect of growth factors on intestinal wall components. J. Surg. Res. 61:1996;514.
7. Dignass A. U., Tsunekawa S., Podolsky D. K. Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology. 106:1994;1254.
8. Alison M. R., Sarraf C. E. The role of growth factors in gastrointestinal cell proliferation. Cell Biol. Int. 18:1994;1.
9. Burgess A. W. Growth control mechanisms in normal and transformed intestinal cells. Philos. Trans. R. Soc. Lond. Biol. 353:1998;903.
10. Murphy M. S. Growth factors and the gastrointestinal tract. Nutrition. 14:1998;771.
11. Barnard J. A., Beauchamp R. D., Russell W. E., Dubois R. N., Coffey R. J. Epidermal growth factor-related peptides and their relevance to gastrointestinal pathophysiology. Gastroenterology. 108:1995;564.
12. Saxena S. K., Thompson J. S., Sharp J. G. Role of epidermal growth factor in intestinal regeneration. Surgery. 111:1992;318.
13. Miller C. A., Debas H. T. Epidermal growth factor stimulates the restitution of rat gastric mucosa in vitro. Exp. Physiol. 80:1995;1009.
14. Konturek S. J., Cieszkowski M., Jaworek J., Brzozowski T., Gregory H. Effects of epidermal growth factor on gastrointestinal secretions. Am. J. Physiol. 246:1984;G580.
15. Konturek S. J., Dembinski A., Warzecha Z., Brzozowski T., Gregory H. Role of epidermal growth factor in healing of chronic gastroduodenal ulcers in rats. Gastroenterology. 94:1988;1300.
16. Goodlad R. A., Lee C. Y., Wright N. A. Cell proliferation in the small intestine and colon of intravenously fed rats: Effects of urogastrone-epidermal growth factor. Cell Prolif. 25:1992;393.
17. Goodlad R. A., Wilson T. J. G., Lenton W., Gregory H., McCullagh K. G., Wright N. A. Proliferative effects of urogastrone-EGF on the intestinal epithelium. Gut. 28:1987;37.
18. Goodlad R. A., Wilson T. J. G., Lenton W., Gregory H., McCullagh K. G., Wright N. A. Intravenous but not intragastric urogastrone-EGF is trophic to the intestine of parenterally fed rats. Gut. 28:1987;573.
19. Scheving L. A., Shiurba R. A., Nguyen T. D., Gray G. M. Epidermal growth factor receptor of the intestinal enterocyte: Localization to laterobasal but not brush border membrane. J. Biol. Chem. 264:1989;1735.
20. Villa X., Thompson J., Kuluz J., Schleien C. Epidermal growth factor reduces ischemia/reperfusion injury in rat small intestine. Gastroenterology. 110:1989;A372.
21. Walker-Smith J. A., Phillips A. D., Walford N., Gregort H., Fitzgerald J. D., MacCullagh K., Wright N. A. Intravenous epidermal growth factor/urogastrone increases small-intestinal cell proliferation in congenital microvillous atrophy. Lancet. 1985;1239.
22. Sullivan P. B., Brueton M. J., Tabara Z. B., Goodlad R. A., Lee C. Y., Wright N. A. Epidermal growth factor in necrotising enteritis. Lancet. 338:1991;53.
23. Besner G., Higashiyama S., Klagsbrun M. Isolation and characterization of a macrophage-derived heparin-binding growth factor. Cell Regul. 1:1990;811.
24. Higashiyama S., Abraham J. A., Miller J., Fiddes J. C., Klagsbrun M. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science. 251:1991;936.
25. Elenius K., Paul S., Allison G., Sun J., Klagsbrun M. Activation of HER4 by heparin-binding EGF-like growth factor stimulates chemotaxis but not proliferation. EMBO J. 16:1997;1268.
26. Besner G. E., Whelton D., Crissman-Combs M. A., Steffen C. L., Kim G. Y., Brigstock D. R. Interaction of heparin-binding EGF-like growth factor (HB-EGF) with the epidermal growth factor receptor: Modulation by heparin, heparinase, or synthetic heparin-binding HB-EGF fragments. Growth Factors. 7:1992;289.
27. Higashiyama S., Abraham J. A., Klagsbrun M. Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: Dependence on interactions with cell surface heparan sulfate. J. Cell Biol. 122:1993;933.
28. Hashimoto K., Higashiyama S., Asada H., Hashimura E., Kobayashi T., Sudo K., Nakagawa T., Damm D., Yoshikawa K., Taniguchi N. Heparin-binding epidermal growth factor-like growth factor is an autocrine growth factor for human keratinocytes. J. Biol. Chem. 269:1994;20060.
29. Davis-Fleischer K. M., Besner G. E. Structure and function of heparin-binding EGF-like growth factor (HB-EGF). Front. Biosci. 3:1998;288.
30. Murayama Y., Miyagawa J.-I., Higashiyama S., Kondo S., Yabum M., Isozaki K., Kayanoki Y., Kanayama S., Shinomura Y., Taniguchi N., Matsuzawa Y. Localization of heparin-binding epidermal growth factor-like growth factor in human gastric mucosa. Gastroenterology. 109:1995;1051.
31. Miyazaki Y., Shinomura S., Higashiyama S., Kanayama S., Higashimoto Y., Tsutsui S., Zushi S., Taniguchi N., Matsuzawa Y. Heparin-binding EGF-like growth factor is an autocrine growth factor for rat gastric epithelial cells. Biochem. Biophys. Res. Commun. 223:1996;36.
32. Miyazaki Y., Shinomura Y., Tsutsui S., Yasunaga Y., Zushi S., Higashiyama S., Taniguchi N., Matsuzawa Y. Oxidative stress increases gene expression of heparin-binding EGF-like growth factor and amphiregulin in cultured rat gastric epithelial cells. Biochem. Biophys. Res. Commun. 226:1996;542.
33. Barnard J. A., Graves-Deal R., Pittelkow M. R., DuBois R., Cook P., Ramsey G. W., Bishop P. R., Damstrup L., Coffey R. J. Auto- and cross-induction within the mammalian epidermal growth factor-related peptide family. J. Biol. Chem. 269:1994;22817.
34. Miyazaki Y., Shinomura Y., Tsutsui S., Zushi S., Higashimoto Y., Kanayama S., Higashiyama S., Taniguchi N., Matsuzawa Y. Gastrin induces heparin-binding epidermal growth factor-like growth factor in rat gastric epithelial cells transfected with gastrin receptor. Gastroenterology. 116:1999;78.
35. Tsutsui S., Shinomura Y., Higashiyama S., Higashimoto Y., Miyazaki Y., Kanayama S., Hiraoka S., Minami T., Kitamura S., Murayama Y., Miyagawa J., Taniguchi N., Matsuzawa Y. Induction of heparin binding epidermal growth factor-like growth factor and amphiregulin mRNAs by gastrin in the rat stomach. Biochem. Biophys. Res. Commun. 235:1997;520.
36. Pillai S. B., Turman M. A., Besner G. E. Heparin-binding EGF-like growth factor (HB-EGF) is cytoprotective for intestinal epithelial cells exposed to hypoxia. J. Pediatr. Surg. 33:1998;973.
37. Davis K. M., Brigstock D. R., Johnson P. R., Crissman-Combs M. A., McCarthy D. W., Downing M. T., Besner G. E. Production of glycosylated heparin-binding EGF-like growth factor in HeLa cells using vaccinia virus. Protein Exp. Purif. 8:1996;57.
38. Pillai S. B., Luquette M., Nowicki P. T., Besner G. E. Segmental intestinal ischemia: An improved method of producing small bowel injury. J. Invest. Surg. 11:1998;123.
39. Gallo-Payet N., Hugon J. S. Epidermal growth factor receptors in isolated adult mouse intestinal cells: Studies in vivo and in organ culture. Endocrinology. 116:1985;194.
40. Thompson J. F. Specific receptors for epidermal growth factor in rat intestinal microvillus membranes. Am. J. Physiol. 254:1988;G429.
41. Dembinski A., Gregory H., Konturek S. J., Polanski M. Trophic action of epidermal growth factor on the pancreas and gastroduodenal mucosa in rats. J. Physiol. (Lond.). 325:1982;35.
42. Ulshen M. H., Lyn-Cook L. E., Raasch R. H. Effects of intraluminal epidermal growth factor on mucosal proliferation in the small intestine of adult rats. Gastroenterology. 91:1986;1134.
43. Li A. K., Schattenkerk M. E., Huffman R. G., Ross J. S., Malt R. A. Hypersecretion of submandibular saliva in male mice: Trophic response in small intestine. Gastroenterology. 84:1983;949.
44. Thornburg W., Matrisian L., Magun B., Koldovsky O. Gastrointestinal absorption of epidermal growth factor in suckling rats. Am. J. Physiol. 246:1984;G80.
45. Purushotham K. R., Offenmuller K., Bui A. T., Zelles T., Blazsek J., Schultz G. S., Humphreys-Beher M. G. Absorption of epidermal growth factor occurs through the gastrointestinal tract and oral cavity in adult rats. Am. J. Physiol. 269:1995;G867.
46. Marcial M. A., Madara J. L. Analysis of absorptive cell occluding junction structure-function relationships in a state of enhanced junctional permeability. Lab. Invest. 56:1987;424.
47. Tice L. W., Carter R. L., Cahill M. B. Changes in tight junctions of rat intestinal crypt cells associated with changes in their mitotic activity. Tissue Cell. 11:1979;293.
48. Chailler P., Menard D. Ontogeny of EGF receptors in the human gut. Front. Biosci. 4:1999;D87.
49. Harding P. A., Davis-Fleischer K., Crissman-Combs M., Miller M., Brigstock D., Besner G. Overexpression of heparin-binding EGF-like growth factor stimulates altered cell growth and anchorage independence. Growth Factors. 17:1999;49.
50. Ono M., Raab G., Lau K., Abraham J. A., Klagsbrun M. Purification and characterization of transmembrane forms of heparin-binding EGF-like growth factor. J. Biol. Chem. 269:1994;31315.