Dipeptidylpeptidase-IV, a key enzyme for the degradation of incretins and neuropeptides: Activity and expression in the liver of lean and obese rats

European Journal of Histochemistry

Volumn 56, Issue 4, 2012, Pages 254-264

  Tarantola, E ^a   Bertone, V ^a   Milanesi, G ^a   Capelli, E ^a   Ferrigno, A ^a   Neri, D ^b   Vairetti, M ^a   Barni, S ^a   Freitas, I ^a,c  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c CNR   (Italy)

Author keywords

Bile canaliculi; Biliary tree; Dipeptidylpeptidase IV; Fatty liver; Hepatocytes; Incretins; Neuropeptides

Indexed keywords

EID: 84867759742     PISSN: 1121760X     EISSN: None     Source Type: Journal    
DOI: 10.4081/ejh.2012.e41     Document Type: Article

References (114)

1. Sun B, Jiang HC, Piao DX, Qiao HQ, Zhang L. Effects of cold preservation and warm reperfusion on rat fatty liver. World J Gastroenterol 2000;6:271-274.
2. Angele MK, Rentsch M, Hartl WH, Wittmann B, Graeb C, Jauch KW, et al. Effect of graft steatosis on liver function and organ survival after liver transplantation. Am J Surg 2008;195:214-220.
3. Fukumori T, Ohkohchi N, Tsukamoto S, Satomi S. The mechanism of injury in a steatotic liver graft during cold preservation. Transplantation 1999;67:195-200.
4. Burke A, Lucey MR. Non-alcoholic fatty liver disease, non-alcoholic steatohepatitis and orthotopic liver transplantation. Am J Transplant 2004;4:686-693.
5. Marsman H, Matsushita T, Dierkhising R, Kremers W, Rosen C, Burgart L, et al. Assessment of donor liver steatosis: pathologist or automated software? Hum Pathol 2004;35:430-435.
6. Dutkowski P, de Rougemont O, Clavien PA. Machine perfusion for 'marginal' liver grafts. Am J Transplant 2008;8:917-924.
7. Attia M, Silva MA, Mirza DF. The marginal liver donor - an update. Transpl Int 2008;21:713-724.
8. Baccarani U, Adani GL, Isola M, Avellini C, Lorenzin D, Rossetto A, et al. Steatosis of the graft is a risk factor for posttransplantation biliary complications. Transplant Proc 2009;41:1313-1315.
9. Krom RA, Sanchez-Urdazpal L. The biliary tree--the Achilles tendon of liver preservation? Transplantation 1992;53:1167.
10. Buis CI, Hoekstra H, Verdonk RC, Porte RJ. Causes and consequences of ischemic-type biliary lesions after liver transplantation. J Hepatobiliary Pancreat Surg 2006;13:517-524.
11. Koneru B, Sterling MJ, Bahramipour PF. Bile duct strictures after liver transplantation: a changing landscape of the Achilles' heel. Liver Transpl 2006;12:702-704.
12. Roma MG, Sanchez Pozzi EJ. Oxidative stress: a radical way to stop making bile. Ann Hepatol 2008;7:16-33.
13. Heidenhain C, Pratschke J, Puhl G, Neumann U, Pascher A, Veltzke-Schlieker W, et al. Incidence of and risk factors for ischemic-type biliary lesions following orthotopic liver transplantation. Transpl Int 2010;23:14-22.
14. Buis CI, Geuken E, Visser DS, Kuipers F, Haagsma EB, Verkade HJ, et al. Altered bile composition after liver transplantation is associated with the development of nonanastomotic biliary strictures. J Hepatol 2009;50:69-79.
15. Lenzen R, Bähr A, Eichstädt H, Marschall U, Bechstein WO, Neuhaus P. In liver transplantation, T tube bile represents total bile flow: physiological and scintigraphic studies on biliary secretion of organic anions. Liver Transpl Surg 1999; 5:8-15.
16. Cutrin JC, Cantino D, Biasi F, Chiarpotto E, Salizzoni M, Andorno E, et al. Reperfusion damage to the bile canaliculi in transplanted human liver. Hepatology 1996;24:1053-1057.
17. Kukan M, Haddad PS. Role of hepatocytes and bile duct cells in preservation/ reperfusion injury of liver grafts. Liver Transplant 2001;7:381-400.
18. Testa G, Malagò M, Broelseh CE. Complications of biliary tract in liver transplantation. World J Surg 2001;25: 1296-1299.
19. +. Liver Transpl 2008;14:494-503.
20. Vairetti M, Ferrigno A, Carlucci F, Tabucchi A, Rizzo V, Boncompagni E, et al. Subnormothermic machine perfusion protects steatotic livers against preservation injury: a potential for donor pool increase? Liver Transpl 2009;15:20-29.
21. Ferrigno A, Carlucci F, Tabucchi A, Tommassini V, Rizzo V, Richelmi P, et al. Different susceptibility of liver grafts from lean and obese Zucker rats to preservation injury. Cryobiology 2009;59:327-334.
22. Ferrigno A, Rizzo V, Boncompagni E, Bianchi A, Gringeri E, Neri D, et al. Machine perfusion at 20°C reduces preservation damage to livers from nonheart beating donors. Cryobiology 2011;62:152-158.
23. Boncompagni E, Gini E, Ferrigno A, Milanesi G, Gringeri E, Barni S, et al. Decreased apoptosis in fatty livers submitted to subnormothermic machine-perfusion respect to cold storage. Eur J Histochem 2011;55:e40.
24. Bertone V, Tarantola E, Ferrigno A, Gringeri E, Barni S, Vairetti M, et al. Altered alkaline phosphatase activity in the liver of obese Zucker rats respect to lean Zucker and Wistar rats discussed in terms of all putative roles ascribed to the enzyme. Eur J Histochem 2011;55:e5.
25. Chen X. Biochemical properties of recombinant prolyl dipeptidases DPP-IV and DPP8. Adv Exp Med Biol 2006;575:27-32.
26. Pro B, Dang NH. CD26/dipeptidyl peptidase IV and its role in cancer. Histol Histopathol 2004;19:1345-1351.
27. Ohnuma K, Takahashi N, Yamochi T, Hosono O, Dang NH, Morimoto C. Role of CD26/dipeptidyl peptidase IV in human T cell activation and function. Front Biosci 2008;13:2299-2310.
28. Ohnuma K, Hosono O, Dang NH, Morimoto C. Dipeptidyl peptidase in autoimmune pathophysiology. Adv Clin Chem 2011;53:51-84.
29. Hartel S, Gossrau R, Hanski C, Reutter W. Dipeptidyl peptidase (DPP) IV in rat organs. Comparison of immunohistochemistry and activity histochemistry. Histochemistry. 1988;89:151-161.
30. Ruhnke M, Gossrau R. Reaction rate measurements of proteases and glycosidases with chromogenic methods. Histochem J 1989;21:535-544.
31. Hartel-Schenk S, Gossrau R, Reutter W. Comparative immunohistochemistry and histochemistry of dipeptidyl peptidase IV in rat organs during development. Histochem J 1990;22:567-578.
32. Lojda Z, Gossrau R, Stoward PJ. Proteases. In: PJ Stoward and AG Everson Pearse (eds.) Histochemistry, Vol 3 (Fourth Edition). Edinburgh, Churchill Livingstone, 1991, pp. 281-335.
33. Stecca BA, Nardo B, Chieco P, Mazziotti A, Bolondi L, Cavallari A. Aberrant dipeptidyl peptidase IV (DPP IV/CD26) expression in human hepatocellular carcinoma. J Hepatol 1997;27:337-345.
34. Gorrell MD. Dipeptidyl peptidase IV and related enzymes in cell biology and liver disorders. Clin Sci 2005;108:1-16.
35. Chyan YJ, Chuang LM. Dipeptidyl peptidase-IV Inhibitors: an evolving treatment for type 2 diabetes from the incretin concept. Recent patents on endocrine, metabolic & immune drug discovery 2007;1:15-24. http://www.benthamscience.com/emi/samples/emi1-1/Chuang.pdf
36. DiStefano JK, Watanabe RM. Pharmacogenetics of anti-diabetes drugs. Pharmaceuticals 2010;3:2610-2646.
37. Addison D, Aguilar D. Diabetes and cardiovascular disease: the potential benefit of incretin-based therapies. Curr Atheroscler Rep 2011;13:115-122.
38. Schuppan D, Gorrell MD, Klein T, Mark M, Afdhal NH. The challenge of developing novel pharmacological therapies for nonalcoholic steatohepatitis. Liver In. 2010;30:795-808.
39. Shirakawa J, Fujii H, Ohnuma K, Sato K, Ito Y, Kaji M, et al. Diet-induced adipose tissue inflammation and liver steatosis are prevented by DPP-4 inhibition in diabetic mice. Diabetes 2011;60:1246-1257.
40. Miyazaki M, Kato M, Tanaka K, Tanaka M, Kohjima M, Nakamura K, et al. Increased hepatic expression of dipeptidyl peptidase-4 in non-alcoholic fatty liver disease and its association with insulin resistance and glucose metabolism. Mol Med Report 2012;5:729-733.
41. Vanhoof G, Goossens F, De Meester I, Hendriks D, Scharpé S. Proline motifs in peptides and their biological processing. FASEB J 1995; 9:736-744.
42. Mentlein R. Dipeptidyl-peptidase IV (CD26)-role in the inactivation of regulatory peptides. Regulatory Peptides 1999; 85:9-24.
43. Hildebrandt M, Reutter W, Arck P, Rose M, Klapp BF. A guardian angel: the involvement of dipeptidyl peptidase IV in psychoneuroendocrine function, nutrition and immune defence. Clin Sci (Lond) 2000;99:93-104.
44. Boonacker E, Van Noorden CJF. The multifunctional or moonlighting protein CD26/DPPIV. Eur J Cell Biol 2003;82:53-73.
45. McIntosh CH, Demuth HU, Kim SJ, Pospisilik JA, Pederson RA. Applications of dipeptidyl peptidase IV inhibitors in diabetes mellitus. Int J Biochem Cell Biol 2006;38:860-872.
46. Flatt PR. Dorothy Hodgkin Lecture 2008. Gastric inhibitory polypeptide (GIP) revisited: a new therapeutic target for obesitydiabetes? Diabet Med 2008;25:759-764.
47. Mentlein R. Mechanisms underlying the rapid degradation and elimination of the incretin hormones GLP-1 and GIP. Best Pract Res Clin Endocrinol Metab 2009; 4:443-452.
48. Thulesen J, Hartmann B, Orskov C, Jeppesen PB, Holst JJ, Poulsen SS. Potential targets for glucagon-like peptide 2 (GLP-2) in the rat: distribution and binding of i.v. injected (125)I-GLP-2. Peptides 2000;21:1511-1517.
49. Cheng HC, Abdel-Ghany M, Elble RC, Pauli BU. Lung endothelial dipeptidyl peptidase IV promotes adhesion and metastasis of rat breast cancer cells via tumor cell surface-associated fibronectin. J Biol Chem 1998;273:24207-24215.
50. Balaban YH, Korkusuz P, Simsek H, Gokcan H, Gedikoglu G, Pinar A, et al. Dipeptidyl peptidase IV (DDP IV) in NASH patients. Ann Hepatol 2007;6:242-250.
51. + exchanger NHE3 in rat renal proximal tubule. Am J Physiol Renal Physiol 2008;294: F414-F422.
52. Jeffery CJ. Moonlighting proteins. Trends Biochem Sci 1999;24:8-11.
53. Ejiri S. Moonlighting functions of polypeptide elongation factor 1: from actin bundling to zinc finger protein R1-associated nuclear localization. Biosci Biotechnol Biochem 2002;66:1-21.
54. Kesty NC, Roth JD, Maggs D. Hormonebased therapies in the regulation of fuel metabolism and body weight. Expert Opin Biol Ther 2008;8:1733-1747.
55. Yip RG, Wolfe MM. GIP biology and fat metabolism. Life Sci. 2000;66:91-103.
56. Nielsen LL. Incretin mimetics and DPP-IV inhibitors for the treatment of type 2 diabetes. Drug Discov Today 2005;10:703-710.
57. Brubaker PL, Drucker DJ. Minireview: Glucagon-like peptides regulate cell proliferation and apoptosis in the pancreas, gut, and central nervous system. Endocrinology 2004;145:2653-2659.
58. Seifalian AM, Piasecki C, Agarwal A, Davidson BR. The effect of graded steatosis on flow in the hepatic parenchymal microcirculation. Transplantation 1999; 68:780-784.
59. Sun CK, Zhang XY, Zimmermann A, Wheatley AM. The metabolic and microcirculatory impact of orthotopic liver transplantation on the obese Zucker rat. Transplantation 2003;75:761-769.
60. Chen D, Wang MW. Development and application of rodent models for type 2 diabetes. Diabetes Obes Metab 2005; 7:307-317.
61. Aleixandre de Artiñano A, Miguel Castro M. Experimental rat models to study the metabolic syndrome. Br J Nutr 2009; 102:1246-1253.
62. Koteish A, Diehl AM. Animal models of steatosis. Semin Liver Dis 2001;21:89-104.
63. Van Noorden CJF, Fredericks WM. Enzyme histochemistry: a laboratory manual of current methods. Oxford, Oxford University Press, Royal Microscopy Society, 1992, pp. 68-70.
64. Rose S. Gastrointestinal and hepatobiliary pathophysiology. Madison, USA, Fence Creek Publishing, 1998, pp. 80,123-134.
65. Zsembery A, Thalhammer T, Graf J. Bile formation: a concerted action of membrane transporters in hepatocytes and cholangiocytes. News Physiol Sci 2000; 15:6-11.
66. Saxena R, Theise ND, Crawford JM. Microanatomy of the human liver-exploring the hidden interfaces. Hepatology 1999;30:1339-1346.
67. Roskams TA, Theise ND, Balabaud C, Bhagat G, Bhathal PS, Bioulac-Sage P, et al. Nomenclature of the finer branches of the biliary tree: canals, ductules, and ductular reactions in human livers. Hepato - logy 2004;39:1739-1745.
68. Kanno N, LeSage G, Glaser S, Alvaro D, Alpini G. Functional heterogeneity of the intrahepatic biliary epithelium. Hepato - logy. 2000;31:555-561.
69. Strazzabosco M, Fabris L. Functional anatomy of normal bile ducts. Anat Rec (Hoboken). 2008;291:653-660.
70. Alpini G, Phillips J, La Russo N. The biology of biliary epithelia. In: IM Arias, JL Boyer, N Fausto, WB Jakoby, D Schachter and DA Shafritz (eds.) The liver: biology and pathobiology (3rd ed.) New York, USA, Raven press Ltd., 1994, pp. 623-653.
71. Lazaridis KN, Strazzabosco M, Larusso NF. The cholangiopathies: disorders of biliary epithelia. Gastroenterology 2004;127:1565-1577.
72. Gaudio E, Carpino G, Cardinale V, Franchitto A, Onori P, Alvaro D. New insights into liver stem cells. Dig Liver Dis 2009;41:455-462.
73. Kuwahara R, Kofman AV, Landis CS, Swenson ES, Barendswaard E, Theise ND. The hepatic stem cell niche: identification by label-retaining cell assay. Hepatology 2008;47:1994-2002.
74. Turner R, Lozoya O, Wang Y, Cardinale V, Gaudio E, Alpini G, et al. Human hepatic stem cell and maturational liver lineage biology. Hepatology 2011;53:1035-1045.
75. Marzioni M, Fava G, Benedetti A. Nervous and Neuroendocrine regulation of the pathophysiology of cholestasis and of biliary carcinogenesis. World J Gastroenterol 2006;12:3471-3480.
76. Busek P, Malík R, Sedo A. Dipeptidyl peptidase IV activity and/or structure homologues (DASH) and their substrates in cancer. Int J Biochem Cell Biol 2004; 36:408-421.
77. Sedo A, Malik R. Dipeptidyl peptidase IVlike molecules: homologous proteins or homologous activities? Biochim Biophys Acta 2001;1550:107-116.
78. Busek P, Krepela E, Mares V, Vlasicova K, Sevcik J, Sedo A. Expression and function of dipeptidyl peptidase IV and related enzymes in cancer. Adv Exp Med Biol 2006;575:55-62.
79. Mares V, Stremenova J, Lisá V, Kozáková H, Marek J, Syrucek M, et al. Compart - ment- and malignance-dependent up-regulation of -glutamyltranspeptidase and dipetidylpeptidase-IV activity in human brain gliomas. Histol Histopathol 2012; 27:931-940.
80. Gossrau R. Peptidases II. Localization of dipeptidylpeptidase IV (DPP IV). Histochemical and biochemical study. Histochemistry 1979;60:231-248.
81. Heymann E, Mentlein R. Liver dipeptidyl aminopeptidase IV hydrolyzes substance P. FEBS Letters 1978;91:360-364.
82. Ariyoshi M, Mizuno M, Morisue Y, Shimada M, Fujita S, Nasu J, et al. Identification of a target antigen recognized by a mouse monoclonal antibody to the bile canalicular surface of rat hepatocytes with a random phage display library. Acta Med Okayama 2002;56:187-191.
83. Grapin-Botton A. Ductal cells of the pancreas. Int J Biochem Cell Biol 2005;37:504-510.
84. Lopez-Delgado MI, Morales M, Villanueva-Peñacarrillo ML, Malaisse WJ, Valverde I. Effects of glucagon-like peptide 1 on the kinetics of glycogen synthase a in hepatocytes from normal and diabetic rats. Endocrinology 1998;139:2811-2817.
85. Redondo A, Trigo MV, Acitores A, Valverde I, Villanueva-Penacarrillo ML. Cell signaling of the GLP-1 action in rat liver. Mol Cell Endocrinol 2003;204:43-50.
86. Marzioni M, Alpini G, Saccomanno S, Candelaresi C, Venter J, Rychlicki C, et al. Glucagon-like peptide-1 and its receptor agonist exendin-4 modulate cholangiocyte adaptive response to cholestasis. Gastro enterology 2007;133:244-255.
87. Zhong Q, Bollag RJ, Dransfield DT, Gasalla-Herraiz J, Ding KH, Min L, Isales CM. Glucose-dependent insulinotropic peptide signaling pathways in endothelial cells. Peptides 2000; 21:1427-1432.
88. Flatt PR, Bailey CJ, Green BD. Dipeptidyl peptidase IV (DPP IV) and related molecules in type 2 diabetes. Front Biosci 2008;13:3648-3660.
89. Ding KH, Zhong Q, Xu J, Isales CM. Glucose-dependent insulinotropic peptide: differential effects on hepatic artery vs. portal vein endothelial cells. Am J Physiol Endocrinol Metab 2004;286:E773-E779.
90. Ding WG, Kitasato H, Kimura H. Development of neuropeptide Y innervation in the liver. Microsc Res Tech 1997;39:365-371.
91. McCuskey RS. Anatomy of efferent hepatic nerves. Anat Rec A Discov Mol Cell Evol Biol 2004;280:821-826.
92. Cho WK, Boyer J. Vasoactive intestinal polypeptide is a potent regulator of bile secretion from rat cholangiocytes. Gastroenterology 1999;117:420-428.
93. Cassiman D, Sinelli N, Bockx I, Vander Borght S, Petersen B, De Vos R, et al. Human hepatic progenitor cells express vasoactive intestinal peptide receptor type 2 and receive nerve endings. Liver Int 2007;27:323-328.
94. Onoue S, Misaka S, Yamada S. Structureactivity relationship of vasoactive intestinal peptide (VIP): potent agonists and potential clinical applications. Naunyn Schmiedebergs Arch Pharmacol 2008; 377:579-590.
95. Moody TW, Ito T, Osefo N, Jensen RT. VIP and PACAP: recent insights into their functions/roles in physiology and disease from molecular and genetic studies. Curr Opin Endocrinol Diabetes Obes 2011; 18:61-67.
96. Cho WK. Role of the neuropeptide, bombesin, in bile secretion. Yale J Biol Med. 1997; 70:409-416.
97. Ueno T, Inuzuka S, Torimura T, Sakata R, Sakamoto M, Gondo K, et al. Distribution of substance P and vasoactive intestinal peptide in the human liver: light and electron immunoperoxidase methods of observation. Am J Gastroenterol 1991;86: 1633-1637.
98. Rowland KJ, Brubaker PL. The "cryptic" mechanism of action of glucagon-like peptide-2. Am J Physiol Gastrointest Liver Physiol 2011;301:G1-G8.
99. Holst JJ, Vilsbøll T, Deacon CF. The incretin system and its role in type 2 diabetes mellitus. Mol Cell Endocrinol 2009;297:127-136.
100. Holst JJ. Glucagon and glucagon-like peptides 1 and 2. Results Probl Cell Differ 2010;50:121-135.
101. Piazza GA, Callanan HM, Mowery J, Hixson DC. Evidence for a role of dipeptidyl peptidase IV in fibronectin-mediated interactions of hepatocytes with extracellular matrix. Biochem J 1989;262:327-324.
102. Matsumoto Y, Bishop GA, McCaughan GW. Altered zonal expression of the CD26 antigen (dipeptidyl peptidase IV) in human cirrhotic liver. Hepatology 1992;15:1048-1053.
103. Stamatoglou SC, Ge RC, Mills G, Butters TD, Zaidi F, Hughes RC. Identification of a novel glycoprotein (AGp110) involved in interactions of rat liver parenchymal cells with fibronectin. J Cell Biol 1990;111: 2117-2127.
104. McCaughan GW, Gorrell MD, Bishop GA, Abbott CA, Shackel NA, McGuinness PH, et al. Molecular pathogenesis of liver disease: an approach to hepatic inflammation, cirrhosis and liver transplant tolerance. Immunol Rev 2000;174:172-191.
105. Gorrell MD, Abbott CA, Kähne T, Levy MT, Church WB, McCaughan GW. Relating structure to function in the beta-propeller domain of dipeptidylpeptidase IV. Point mutations that influence adenosine deaminase binding, antibody binding and enzyme activity. In: J Langner and S Ansorge (eds.) Cellular peptidases in immune functions and diseases 2. New York, USA Kluwer Academic/Plenum Publishers, 2000, pp. 89-95.
106. Longenecker KL, Stewart KD, Madar DJ, Jakob CG, Fry EH, Wilk S, et al. Crystal structures of DPPIV (CD 26) from rat kidney exhibit flexible accommodation of peptidase-selective inhibitors. Biochemistry 2006;45:7474-7482.
107. + exchangers of mammalian cells. J Biol Chem 1997;272:22373-2236.
108. Mennone A, Biemesderfer D, Negoianu D, Yang CL, Abbiati T, Schultheis PJ, et al. Role of sodium/hydrogen exchanger isoform NHE3 in fluid secretion and absorption in mouse and rat cholangiocytes. Am J Physiol Gastrointest Liver Physiol 2001; 280:G247-G254.
109. Pizarro M, Balasubramaniyan N, Solís N, Solar A, Duarte I, Miquel JF, et al. Bile secretory function in the obese Zucker rat: evidence of cholestasis and altered canalicular transport function. Gut 2004;53:1837-1843.
110. Geier A, Dietrich CG, Grote T, Beuers U, Prüfer T, Fraunberger P, et al. Characterization of organic anion transporter regulation, glutathione metabolism and bile formation in the obese Zucker rat. J Hepatol 2005;43:1021-1030.
111. Unniappan S, McIntosh CH, Demuth HU, Heiser U, Wolf R, Kieffer TJ. Effects of dipeptidyl peptidase IV on the satiety actions of peptide YY. Diabetologia 2006;49:1915-1923.
112. Hong WJ, Petell JK, Swank D, Sanford J, Hixson DC, Doyle D. Expression of dipeptidyl peptidase IV in rat tissues is mainly regulated at the mRNA levels. Exp Cell Res 1989;182:256-256.
113. Wang XM, Yao TW, Nadvi NA, Osborne B, McCaughan GW, Gorrell MD. Fibroblast activation protein and chronic liver disease. Front Biosci 2008;13:3168-3180.
114. Keane FM, Chowdhury S, Yao T-W, Nadvi NA, Gall MG, Chen Y, et al. Targeting dipeptidyl peptidase-4 (DPP-4) and fibroblast activation protein (FAP) for diabetes and cancer therapy. In: B Dunn (ed.) RSC Drug Discovery Series No. 18. Proteinases as drug targets. Royal Society of Chemistry, 2012, pp. 119-145.