A functional XPNPEP2 promoter haplotype leads to reduced plasma aminopeptidase P and increased risk of ACE inhibitor-induced angioedema

Human Mutation

Volumn 32, Issue 11, 2011, Pages 1326-1331

  Cilia La Corte, Amy L ^a,b   Carter, Angela M ^b   Rice, Gillian I ^a,f   Duan, Qing Ling ^c   Rouleau, Guy A ^d   Adam, Albert ^e   Grant, Peter J ^b   Hooper, Nigel M ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

^c MCGILL UNIVERSITY   (Canada)

^d UNIVERSITY OF MONTREAL   (Canada)

^e UNIVERSITÉ DE MONTRÉAL   (Canada)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

ACE inhibitor angioedema; Aminopeptidase P; Bradykinin; Haplotype; Hepatic nuclear factor 4; Transcription regulatory elements

Indexed keywords

AMINOPEPTIDASE P; BRADYKININ; BRADYKININ[8 LEUCINE 9 DEARGININE]; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR;

ADOLESCENT; ADULT; AGED; ANGIONEUROTIC EDEMA; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENHANCER REGION; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; ENZYME INHIBITION; FEMALE; GENE CONTROL; GENE DELETION; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENE OVEREXPRESSION; GENETIC POLYMORPHISM; GENETIC REGULATION; HAPLOTYPE; HUMAN; MALE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; REPORTER GENE; TRANSCRIPTION REGULATION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AMINOPEPTIDASES; ANGIOEDEMA; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; FEMALE; HAPLOTYPES; HUMANS; MALE; MIDDLE AGED; PEDIGREE; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL;

EID: 80054713052     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.21579     Document Type: Article

References (39)

1. Adam A, Cugno M, Molinaro G, Perez M, Lepage Y, Agostoni A. 2002. Aminopeptidase P in individuals with a history of angio-oedema on ACE inhibitors. Lancet 359:2088-2089.
2. Almasy L, Blangero J. 1998. Multipoint quantitative-trait linkage analysis in general pedigrees. Am J Hum Genet 62:1198-1211.
3. 9-bradykinin metabolism in patients who presented hypersensitivity reactions during hemodialysis: role of serum ace and aminopeptidase P. Peptides 20:421-430.
4. Brown NJ, Ray WA, Snowden M, Griffin MR. 1996. Black Americans have an increased rate of angiotensin converting enzyme inhibitor-associated angioedema. Clin Pharmacol Ther 60:8-13.
5. Cilia La, Corte AL, Carter AM, Turner AJ, Grant PJ, Hooper NM. 2008. The bradykinin-degrading aminopeptidase P is increased in women taking the oral contraceptive pill. J Renin Angiotensin Aldosterone Syst 9:221-225.
6. Cottrell GS, Hooper NM, Turner AJ. 2000. Cloning, expression, and characterization of human cytosolic aminopeptidase P: a single manganese(II)-dependent enzyme. Biochemistry 39:15121-15128.
7. Cugno M, Nussberger J, Cicardi M, Agostoni A. 2003. Bradykinin and the pathophysiology of angioedema. Int Immunopharmacol 3:311-317.
8. Cyr M, Lepage Y, Blais C, Jr, Gervais N, Cugno M, Rouleau JL, Adam A. 2001. Bradykinin and des-Arg(9)-bradykinin metabolic pathways and kinetics of activation of human plasma. Am J Physiol Heart Circ Physiol 281:H275-H283.
9. Duan QL, Nikpoor B, Dube MP, Molinaro G, Meijer IA, Dion P, Rochefort D, Saint-Onge J, Flury L, Brown NJ, Gainer JV, Rouleau JL, Agostoni A, Cugno M, Simon P, Clavel P, Potier J, Wehbe B, Benarbia S, Marc-Aurele J, Chanard J, Foroud T, Adam A, Rouleau GA. 2005. A variant in XPNPEP2 is associated with angioedema induced by angiotensin I-converting enzyme inhibitors. Am J Hum Genet 77:617-626.
10. Ersahin C, Simmons WH. 1997. Inhibition of both aminopeptidase P and angiotensin-converting enzyme prevents bradykinin degradation in the rat coronary circulation. J Cardiovasc Pharmacol 30:96-101.
11. Ersahin C, Szpaderska AM, Simmons WH. 2003. Rat and mouse membrane aminopeptidase P: structure analysis and tissue distribution. Arch Biochem Biophys 417:131-140.
12. Freeman MS, Mansfield MW, Barrett JH, Grant PJ. 2002a. Genetic contribution to circulating levels of haemostatic factors in healthy families with effects of known genetic polymorphisms on heritability. Arterioscler Thromb Vasc Biol 22:506-510.
13. Freeman MS, Mansfield MW, Barrett JH, Grant PJ. 2002b. Heritability of features of the insulin resistance syndrome in a community-based study of healthy families. Diabet Med 19:994-999.
14. Fryer RM, Segreti J, Banfor PN, Widomski DL, Backes BJ, Lin CW, Ballaron SJ, Cox BF, Trevillyan JM, Reinhart GA, von Geldern TW. 2008. Effect of bradykinin metabolism inhibitors on evoked hypotension in rats: rank efficacy of enzymes associated with bradykinin-mediated angioedema. Br J Pharmacol 153:947-955.
15. Hooper NM, Hryszko J, Turner AJ. 1990. Purification and characterization of pig kidney aminopeptidase P. A glycosyl-phosphatidylinositol-anchored ectoenzyme. Biochem J 267:509-515.
16. Hooper NM, Turner AJ. 1988. Ectoenzymes of the kidney microvillar membrane. Aminopeptidase P is anchored by a glycosyl-phosphatidylinositol moiety. FEBS Lett. 229:340-344.
17. Hooper NM, Turner AJ. 1989. Hydrolysis of the glycosyl-phosphatidylinositol anchors of renal microvillar peptidases by a plasma phospholipase D. Biochem Soc Trans 17:885-886.
18. Hudson BI, Stickland MH, Futers TS, Grant PJ. 2001. Effects of novel polymorphisms in the RAGE gene on transcriptional regulation and their association with diabetic retinopathy. Diabetes 50:1505-1511.
19. Israili ZH, Hall WD. 1992. Cough and angioneurotic edema associated with angiotensin-converting enzyme inhibitor therapy. A review of the literature and pathophysiology. Ann Intern Med 117:234-242.
20. Kim K-S, Kumar S, Simmons WH, Brown NJ. 2000. Inhibition of aminopeptidase P potentiates wheal response to bradykinin in angiotensin-converting enzyme inhibitor-treated humans. J Pharmacol Exp Ther 292:295-298.
21. Lausen J, Thomas H, Lemm I, Bulman M, Borgschulze M, Lingott A, Hattersley AT, Ryffel GU. 2000. Naturally occurring mutations in the human HNF4alpha gene impair the function of the transcription factor to a varying degree. Nucleic Acids Res 28:430-437.
22. Leeb-Lundberg LM, Marceau F, Muller-Esterl W, Pettibone DJ, Zuraw BL. 2005. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev 57:27-77.
23. Leenen FH, Nwachuku CE, Black HR, Cushman WC, Davis BR, Simpson LM, Alderman MH, Atlas SA, Basile JN, Cuyjet AB, Dart R, Felicetta JV, Grimm RH, Haywood LJ, Jafri SZ, Proschan MA, Thadani U, Whelton PK, Wright JT, Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial Collaborative Research Group. 2006. Clinical events in high-risk hypertensive patients randomly assigned to calcium channel blocker versus angiotensin-converting enzyme inhibitor in the antihypertensive and lipid-lowering treatment to prevent heart attack trial. Hypertension 48:374-384.
24. Lefebvre J, Murphey LJ, Hartert TV, Jiao Shan R, Simmons WH, Brown NJ. 2002. Dipeptidyl peptidase IV activity in patients with ACE-inhibitor-associated angioedema. Hypertension 39:460-464.
25. Molinaro G, Duan QL, Chagnon M, Moreau ME, Simon P, Clavel P, Lavaud S, Boileau G, Rouleau GA, Lepage Y, Adam A, Chanard J. 2006. Kinin-dependent hypersensitivity reactions in hemodialysis: metabolic and genetic factors. Kidney Int 70:1823-1831.
26. Nussberger J, Cugno M, Amstutz C, Cicardi M, Pellacani A, Agostoni A. 1998. Plasma bradykinin in angio-oedema. Lancet 351:1693-1697.
27. Prechel MM, Orawski AT, Maggiora LL, Simmons WH. 1995. Effect of a new aminopeptidase Pinhibitor, apstatin, on bradykinin degradation in the rat lung. J Pharmacol Exper Therap 275:1136-1142.
28. Ryan JW, Valido F, Berryer P, Chung AYK, Ripka JE. 1992. Purification and characterisation of guinea pig serum aminoacylproline hydrolase (aminopeptidase P). Biochim Biophys Acta 1119:140-147.
29. Schrem H, Klempnauer J, Borlak J. 2002. Liver-enriched transcription factors in liver function and development. Part I: the hepatocyte nuclear factor network and liver-specific gene expression. Pharmacol Rev 54:129-158.
30. Simmons WH. 2004. Aminopeptidase P2. In: Barrett AJ, Rawlings ND, Woessner JF, editors. Handbook of proteolytic enzymes. Amsterdam: Elsevier. p 934-937.
31. Sprinkle TJ, Caldwell C, Ryan JW. 2000. Cloning, chromosomal sublocalization of the human soluble aminopeptidase P gene (XPNPEP1) to 10q25.3 and conservation of the putative proton shuttle and metal ligand binding sites with XPNPEP2. Arch Biochem Biophys 378:51-56.
32. Sprinkle TJ, Stone AA, Venema RC, Denslow ND, Caldwell C, Ryan JW. 1998. Assignment of the membrane-bound human aminopeptidase P gene (XPNPEP2) to chromosome Xq25. Genomics 50:114-116.
33. Stephens M, Donnelly P. 2003. A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162-1169.
34. Stephens M, Smith NJ, Donnelly P. 2001. A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978-989.
35. Turner AJ, Cottrell GS. 2004. Aminopeptidase P1. In: Barrett AJ, Rawlings ND, Woessner JF, editors. Handbook of proteolytic enzymes. Amsterdam: Elsevier. p 931-933.
36. Turner AJ, Hooper NM. 2002. The angiotensin-converting enzyme gene family: genomics and pharmacology. Trends Pharmacol Sci 23:177-183.
37. Venema RC, Ju H, Zou R, Venema VJ, Ryan JW. 1997. Cloning and tissue distribution of human membrane-bound aminopeptidase P. Biochim Biophys Acta 1354:45-48.
38. Vleeming W, van Amsterdam JG, Stricker BH, de Wildt DJ. 1998. ACE inhibitor-induced angioedema. Incidence, prevention and management. Drug Saf 18:171-188.
39. Zhao T, Chang LW, McLeod HL, Stormo GD. 2004. PromoLign: a database for upstream region analysis and SNPs. Hum Mutat 23:534-539.