Role of extrahepatic UDP-glucuronosyltransferase 1A1: Advances in understanding breast milk-induced neonatal hyperbilirubinemia

Toxicology and Applied Pharmacology

Volumn 289, Issue 1, 2015, Pages 124-132

  Fujiwara, Ryoichi ^a   Maruo, Yoshihiro ^b   Chen, Shujuan ^c   Tukey, Robert H ^c  

^a KITASATO UNIVERSITY   (Japan)

^b SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bilirubin; Extra hepatic; Gilbert's Syndrome; Humanized UGT1 Mice; UDP glucuronosyltransferase 1A1

Indexed keywords

BILIRUBIN; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 1A1; GLUCURONIDE; UGT1A1 ENZYME;

BILIRUBIN METABOLISM; BREAST MILK; BREAST MILK INDUCED JAUNDICE; GENETIC ASSOCIATION; GILBERT DISEASE; HUMAN; JAUNDICE; NEONATAL HYPERBILIRUBINEMIA; NEWBORN JAUNDICE; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; CHEMISTRY; GENETIC POLYMORPHISM; GENETICS; LIVER; METABOLISM; PATHOLOGY;

BILIRUBIN; GLUCURONIDES; GLUCURONOSYLTRANSFERASE; HUMANS; JAUNDICE, NEONATAL; LIVER; MILK, HUMAN; POLYMORPHISM, GENETIC;

EID: 84945483859     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2015.08.018     Document Type: Review

References (125)

1. Agrawal S.K., Kumar P., Rathi R., Sharma N., Das R., Prasad R., Narang A. UGT1A1 gene polymorphisms in north Indian neonates presenting with unconjugated hyperbilirubinemia. Pediatr. Res. 2009, 65:675-680.
2. Alonso E.M., Whitington P.F., Whitington S.H., Rivard W.A., Given G. Enterohepatic circulation of nonconjugated bilirubin in rats fed with human milk. J. Pediatr. 1991, 118:425-430.
3. American Academy of Pediatrics, Subcommittee on Hyperbilirubinemia Management of hyperbilirubinemia in the newborn infant 35 or more weeks of gestation. Pediatrics 2004, 114:297-316.
4. Aono S., Yamada Y., Keino H., Hanada N., Nakagawa T., Sasaoka Y., Yazawa T., Sato H., Koiwai O. Identification of defect in the genes for bilirubin UDP-glucuronosyl-transferase in a patient with crigler-najjar syndrome type II. Biochem. Biophys. Res. Commun. 1993, 197:1239-1244.
5. Aoshima N., Fujie Y., Itoh T., Tukey R.H., Fujiwara R. Glucose induces intestinal human UDP-glucuronosyltransferase (UGT) 1A1 to prevent neonatal hyperbilirubinemia. Sci. Rep. 2014, 4:6343.
6. Apaydin K., Ermis B., Arasli M., Tekin I., Ankarali H. Cytokines in human milk and late-onset breast milk jaundice. Pediatr. Int. 2012, 54:801-805.
7. Arias I.M., Gartner L.M., Seifter S. Neonatal unconjugated hyperbilirubinemia associated with breast-feeding and a factor in milk that inhibits glucuronide formation in vitro. J. Clin. Invest. 1963, 42:913.
8. Arias I.M., Gartner L.M., Seifter S., Furman M. Prolonged neonatal unconjugated hyperbilirubinemia associated with breast feeding and a steroid, pregnane-3(alpha), 20(beta)-diol, in maternal milk that inhibits glucuronide formation in vitro. J. Clin. Invest. 1964, 43:2037-2047.
9. Arias I.M., Gartner L.M., Cohen M., Ezzer J.B., Levi A.J. Chorionic nonhemolytic unconjugated hyperbilirubinemia with glucuronosyl transferase deficiency. Am. J. Med. 1969, 47:395-409.
10. Assenat E., Gerbal-Chaloin S., Larrey D., Saric J., Fabre J.M., Maurel P., Vilarem M.J., Pascussi J.M. Interleukin 1beta inhibits CAR-induced expression of hepatic genes involved in drug and bilirubin clearance. Hepatology 2004, 40:951-960.
11. Azlin I., Wong F.L., Ezham M., Hafiza A., Ainoon O. Prevalence of uridine glucuronosyl transferase 1A1 (UGT1A1) mutations in Malay neonates with severe jaundice. Malays. J. Pathol. 2011, 33:95-100.
12. Babaoglu M.O., Yigit S., Aynacioglu A.S., Kerb R., Yurdakok M., Bozkurt A. Neonatal jaundice and bilirubin UDP-glucuronosyl transferase 1A1 gene polymorphism in Turkish patients. Basic Clin. Pharmacol. Toxicol. 2006, 98:377-380.
13. Beutler E., Gelbart T., Demina A. Racial variability in the UDP-glucuronosyltransferase 1 (UGT1A1) promoter: a balanced polymorphism for regulation of bilirubin metabolism?. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:8170-8174.
14. Bevan B.R., Holton J.B. Inhibition of bilirubin conjugation in rat liver slices by free fatty acids, with relevance to the problem of breast milk jaundice. Clin. Chim. Acta 1972, 41:101-107.
15. Bhutani V.K., Donn S.M., Johnson L.H. Risk management of severe neonatal hyperbilirubinemia to prevent kernicterus. Clin. Perinatol. 2005, 32(125-39):vii.
16. Bortolussi G., Zentilin L., Baj G., Giraudi P., Bellarosa C., Giacca M., Tiribelli C., Muro A.F. Rescue of bilirubin-induced neonatal lethality in a mouse model of crigler-najjar syndrome type 1 by AAV9-mediated gene transfer. FASEB J. 2012, 26:1052-1063.
17. Bosma P.J., Chowdhury N.R., Goldhoorn B.G., Hofker M.H., Oude Elferink R.P., Jansen P.L., Chowdhury J.R. Sequence of exons and the flanking regions of human bilirubin-UDP-glucuronosyltransferase gene complex and identification of a genetic mutation in a patient with crigler-najjar syndrome, type I. Hepatology 1992, 15:941-947.
18. Bosma P.J., Seppen J., Goldhoorn B., Bakker C., Oude Elferink R.P., Chowdhury J.R., Chowdhury N.R., Jansen P.L. Bilirubin UDP-glucuronosyltransferase 1 is the only relevant bilirubin glucuronidating isoform in man. J. Biol. Chem. 1994, 269:17960-17964.
19. Bosma P.J., Chowdhury J.R., Bakker C., Gantla S., de Boer A., Oostra B.A., Lindhout D., Tytgat G.N., Jansen P.L., Oude Elferink R.P., Chowdhury N.R. The genetic basis of the reduced expression of bilirubin UDP-glucuronosyltransferase 1 in Gilbert's syndrome. N. Engl. J. Med. 1995, 333:1171-1175.
20. Burchell B. Observations of uridine diphosphate glucuronyltransferase activity towards oestriol and xenobiotics in developing and cultured tissues from mouse and man. Biochem. Soc. Trans. 1973, 1:1212-1214.
21. Burchell B., Hume R. Molecular genetic basis of Gilbert's syndrome. J. Gastroenterol. Hepatol. 1999, 14:960-966.
22. Burchell B., Dutton G.J., Winsnes A. Comparison of culture-induced, Phenobarbital-induced and naturally-developing UDP-glucuronyltransferase. Enzyme 1974, 17:146-154.
23. Burchell B., Coughtrie M., Jackson M., Harding D., Fournel-Gigleux S., Leakey J., Hume R. Development of human liver UDP-glucuronosyltransferases. Dev. Pharmacol. Ther. 1989, 13:70-77.
24. Chang P.F., Lin Y.C., Liu K., Yeh S.J., Ni Y.H. Identifying term breast-fed infants at risk of significant hyperbilirubinemia. Pediatr. Res. 2013, 74:408-412.
25. Chen S., Beaton D., Nguyen N., Senekeo-Effenberger K., Brace-Sinnokrak E., Argikar U., Remmel R.P., Trottier J., Barbier O., Ritter J.K., Tukey R.H. Tissue-specific, inducible, and hormonal control of the human UDP-glucuronosyltransferase-1 (UGT1) locus. J. Biol. Chem. 2005, 280:37547-37557.
26. Chen S., Yueh M.F., Evans R.M., Tukey R.H. The pregnane-X-receptor controls hepatic glucuronidation during pregnancy and neonatal development in humanized UGT1 mice. Hepatology 2012, 56:658-667.
27. Chen S., Yueh M.F., Bigo C., Barbier O., Wang K., Karin M., Nguyen N., Tukey R.H. Intestinal glucuronidation protects against chemotherapy-induced toxicity by irinotecan (CPT-11). Proc. Natl. Acad. Sci. U. S. A. 2013, 110:19143-19148.
28. Constantopoulos A., Messaritakis J., Matsaniotis N. Breast milk jaundice; the role of lipoprotein lipase and the free fatty acids. Eur. J. Pediatr. 1980, 134:35-38.
29. Coyl D.D., Roggman L.A., Newland L.A. Stress, maternal depression, and negative mother-infant interactions in relation to infant attachment. Infant Ment. Health J. 2002, 23:145-163.
30. Crigler J.F., Najjar V.A. Congenital familial nonhemolytic jaundice with kernicterus. Pediatrics 1952, 10:169-179.
31. Crowell J.A., Treboux D. A review of adult attachment measures: implications for theory and research. Soc. Dev. 1995, 4:294-327.
32. Csala M., Marcolongo P., Lizák B., Senesi S., Margittai E., Fulceri R., Magyar J.E., Benedetti A., Bánhegyi G. Transport and transporters in the endoplasmic reticulum. Biochim. Biophys. Acta 2007, 1768:1325-1341.
33. de Wildt S.N., Kearns G.L., Leeder J.S., van den Anker J.N. Glucuronidation in humans. Pharmacogenetic and developmental aspects. Clin. Pharmacokinet. 1999, 36:439-452.
34. Dutton G.J. Acceptor substrates of UDP glucuronosyltransferase and their assay. Glucuronidation of drugs and other compounds 1980, 69-78. CRC Press, Boca Raton, FL. G.J. Dutton (Ed.).
35. Finel M., Kurkela M. The UDP-glucuronosyltransferases as oligomeric enzymes. Curr. Drug Metab. 2008, 9:70-76.
36. Fujiwara R., Itoh T. Extensive protein-protein interactions involving UDP-glucuronosyltransferase (UGT) 2B7 in human liver microsomes. Drug. Metab. Pharmacokinet. 2014, 29:259-265.
37. Fujiwara R., Itoh T. Extensive protein interactions involving cytochrome P450 3A4: a possible contributor to the formation of a metabolosome. Pharmacol. Res. Perspect. 2014, 2.
38. Fujiwara R., Nakajima M., Yamanaka H., Katoh M., Yokoi T. Interactions between human UGT1A1, UGT1A4, and UGT1A6 affect their enzymatic activities. Drug Metab. Dispos. 2007, 35:1781-1787.
39. Fujiwara R., Nakajima M., Yamanaka H., Nakamura A., Katoh M., Ikushiro S., Sakaki T., Yokoi T. Effects of coexpression of UGT1A9 on enzymatic activities of human UGT1A isoforms. Drug Metab. Dispos. 2007, 35:747-757.
40. Fujiwara R., Nakajima M., Oda S., Yamanaka H., Ikushiro S., Sakaki T., Yokoi T. Interactions between human UDP-glucuronosyltransferase (UGT) 2B7 and UGT1A enzymes. J. Pharm. Sci. 2010, 99:442-454.
41. Fujiwara R., Nguyen N., Chen S., Tukey R.H. Developmental hyperbilirubinemia and CNS toxicity in mice humanized with the UDP glucuronosyltransferase 1 (UGT1) locus. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5024-5029.
42. Fujiwara R., Chen S., Karin M., Tukey R.H. Reduced expression of UGT1A1 in intestines of humanized UGT1 mice via inactivation of NF-κB leads to hyperbilirubinemia. Gastroenterology 2012, 142:109-118.
43. Gaffney P.T., Buttenshaw R.L., Ward M., Diplock R.D. Breast milk β-glucuronidase and neonatal jaundice. Lancet 1986, 1:1161-1162.
44. Giacomini K.M., Huang S.M., Tweedie D.J., Benet L.Z., Brouwer K.L., Chu X., Dahlin A., Evers R., Fischer V., Hillgren K.M., Hoffmaster K.A., Ishikawa T., Keppler D., Kim R.B., Lee C.A., Niemi M., Polli J.W., Sugiyama Y., Swaan P.W., Ware J.A., Wright S.H., Yee S.W., Zamek-Gliszczynski M.J., Zhang L. Membrane transporters in drug development. Nat. Rev. Drug Discov. 2010, 9:215-236.
45. Gilbert A., Lereboullet P. La cholémie simple familiale. Sem. Med. 1901, 21:241-243.
46. Gourley G.R. Pathophysiology of breast-milk jaundice. Fetal and neonatal physiology 1998, 1499-1505. 2nd edition.
47. Gourley G.R. Breast-feeding, neonatal jaundice and kernicterus. Semin. Neonatol. 2002, 7:135-141.
48. Gourley G.R., Arend R.A. β-glucuronidase and hyperbilirubinemia in breast-fed and formula-fed babies. Lancet 1986, 1:644-646.
49. Hargreaves T. Effect of fatty acids on bilirubin conjugation. Arch. Dis. Child. 1973, 48:446-450.
50. Hartmann F., Bissell D.M. Metabolism of heme and bilirubin in rat and human small intestinal mucosa. J. Clin. Invest. 1982, 70:23-29.
51. Huang M.J., Kua K.E., Teng H.C., Tang K.S., Weng H.W., Huang C.S. Risk factors for severe hyperbilirubinemia in neonates. Pediatr. Res. 2004, 56:682-689.
52. Ip S., Chung M., Kulig J., O'Brien R., Sege R., Glicken S., Maisels M.J., Lau J. An evidence-based review of important issues concerning neonatal hyperbilirubinemia. Pediatrics 2004, 114:e130-e153.
53. Ishii Y., Iwanaga M., Nishimura Y., Takeda S., Ikushiro S., Nagata K., Yamazoe Y., Mackenzie P.I., Yamada H. Protein-protein interactions between rat hepatic cytochromes P450 (P450s) and UDP-glucuronosyltransferases (UGTs): evidence for the functionally active UGT in P450-UGT complex. Drug Metab. Pharmacokinet. 2007, 22:367-376.
54. Izukawa T., Nakajima M., Fujiwara R., Yamanaka H., Fukami T., Takamiya M., Aoki Y., Ikushiro S., Sakaki T., Yokoi T. Quantitative analysis of UDP-glucuronosyltransferase (UGT) 1A and UGT2B expression levels in human livers. Drug Metab. Dispos. 2009, 37:1759-1768.
55. Kamisako T., Kobayashi Y., Takeuchi K., Ishihara T., Higuchi K., Tanaka Y., Gabazza E.C., Adachi Y. Recent advances in bilirubin metabolism research: the molecular mechanism of hepatocyte bilirubin transport and its clinical relevance. J. Gastroenterol. 2000, 35:659-664.
56. Keppler D., Konig J., Buchler M. The canalicular multidrug resistance protein, cMRP/MRP2, a novel conjugate export pump expressed in the apical membrane of hepatocytes. Adv. Enzym. Regul. 1997, 37:321-333.
57. Kumral A., Ozkan H., Duman N., Yesilirmak D.C., Islekel H., Ozalp Y. Breast milk jaundice correlates with high levels of epidermal growth factor. Pediatr. Res. 2009, 66:218-221.
58. Kutsuno Y., Sumida K., Itoh T., Tukey R.H., Fujiwara R. Glucuronidation of drugs in humanized UDP-glucuronosyltransferase 1 mice: similarity with glucuronidation in human liver microsomes. Pharmacol. Res. Perspect. 2013, 1.
59. Kutsuno Y., Itoh T., Tukey R.H., Fujiwara R. Glucuronidation of drugs and drug-induced toxicity in humanized UDP-glucuronosyltransferase 1 mice. Drug Metab. Dispos. 2014, 42:1146-1152.
60. Laforgia N., Faienza M.F., Rinaldi A., D'Amato G., Rinaldi G., Iolascon A. Neonatal hyperbilirubinemia and Gilbert's syndrome. J. Perinat. Med. 2002, 30:166-169.
61. Mackenzie P.I., Bock K.W., Burchell B., Guillemette C., Ikushiro S., Iyanagi T., Miners J.O., Owens I.S., Nebert D.W. Nomenclature update for the mammalian UDP glycosyltransferase (UGT) gene superfamily. Pharmacogenet. Genomics 2005, 15:677-685.
62. Maisels M.J., Bhutani V.K., Bogen D., Newman T.B., Stark A.R., Watchko J.F. Hyperbilirubinemia in the newborn infant > or =35weeks' gestation: an update with clarifications. Pediatrics 2009, 124:1193-1198.
63. Maruo Y., Nishizawa K., Sato H., Doida Y., Shimada M. Association of neonatal hyperbilirubinemia with bilirubin UDP-glucuronosyltransferase polymorphism. Pediatrics 1999, 103:1224-1227.
64. Maruo Y., Nishizawa K., Sato H., Sawa H., Shimada M. Prolonged unconjugated hyperbilirubinemia associated with breast milk and mutations of the bilirubin uridine diphosphate- glucuronosyltransferase gene. Pediatrics 2000, 106.
65. Maruo Y., D'Addario C., Mori A., Iwai M., Takahashi H., Sato H., Takeuchi Y. Two linked polymorphic mutations (a(TA)7TAA and T-3279G) of UGT1A1 as the principal cause of Gilbert syndrome. Hum. Genet. 2004, 115:525-526.
66. Maruo Y., Morioka Y., Fujito H., Nakahara S., Yanagi T., Matsui K., Mori A., Sato H., Tukey R.H., Takeuchi Y. Bilirubin uridine diphosphate-glucuronosyltransferase variation is a genetic basis of breast milk jaundice. J. Pediatr. 2014, 165:36-41.
67. Medley M.M., Hooker R.L., Rabinowitz S., Holton R., Jaffe B.M. Correction of congenital indirect hyperbilirubinemia by small intestinal transplantation. Am. J. Surg. 1995, 169:20-27.
68. Minekawa R., Takeda T., Sakata M., Hayashi M., Isobe A., Yamamoto T., Tasaka K., Murata Y. Human breast milk suppresses the transcriptional regulation of IL-1beta-induced NF-kappaB signaling in human intestinal cells. Am. J. Physiol. Cell Physiol. 2004, 287:C1404-C1411.
69. Moghrabi N., Clarke D.J., Boxer M., Burchell B. Identification of an a-to-G missense mutation in exon 2 of the UGT1 gene complex that causes crigler-najjar syndrome type 2. Genomics 1993, 18:171-173.
70. Monaghan G., Ryan M., Seddon R., Hume R., Burchell B. Genetic variation in bilirubin UDP-glucuronosyltransferase gene promoter and Gilbert's syndrome. Lancet 1996, 347:578-581.
71. Monaghan G., McLellan A., McGeehan A., Li Volti S., Mollica F., Salemi I., Din Z., Cassidy A., Hume R., Burchell B. Gilbert's syndrome is a contributory factor in prolonged unconjugated hyperbilirubinemia of the newborn. J. Pediatr. 1999, 134:441-446.
72. Murphy J.F., Hughes I., Jones E.V., Gaskell S., Pike A.W. Pregnanediols and breast milk jaundice. Arch. Dis. Child. 1981, 56:474-476.
73. Nakajima M., Yamanaka H., Fujiwara R., Katoh M., Yokoi T. Stereoselective glucuronidation of 5-(4'-hydroxyphenyl)-5-phenylhydantoin by human UDP-glucuronosyltransferase (UGT) 1A1, UGT1A9, and UGT2B15: effects of UGT-UGT interactions. Drug Metab. Dispos. 2007, 35:1679-1686.
74. Nakamura A., Nakajima M., Yamanaka H., Fujiwara R., Yokoi T. Expression of UGT1A and UGT2B mRNA in human normal tissues and various cell lines. Drug Metab. Dispos. 2008, 36:1461-1464.
75. Newman A.J., Gross S. Hyperbilirubinemia in breast-fed infants. Pediatrics 1963, 32:995-1001.
76. Newman T.B., Easterling M.J., Goldman E.S., Stevenson D.K. Laboratory evaluation of jaundice in newborns. Frequency, cost, and yield. Am. J. Dis. Child. 1990, 144:364-368.
77. Nguyen N., Bonzo J.A., Chen S., Chouinard S., Kelner M.J., Hardiman G., Bélanger A., Tukey R.H. Disruption of the ugt1 locus in mice resembles human crigler-najjar type I disease. J. Biol. Chem. 2008, 283:7901-7911.
78. Ohno S., Nakajin S. Determination of mRNA expression of human UDP-glucuronosyltransferases and application for localization in various human tissues by real-time reverse transcriptase-polymerase chain reaction. Drug Metab. Dispos. 2009, 37:32-40.
79. Onishi S., Kawade N., Itoh S., Isobe K., Sugiyama S. Postnatal development of uridine diphosphate glucuronosyltransferase activity toward bilirubin and 2-aminophenol in human liver. Biochem. J. 1979, 184:705-707.
80. Onozawa K., Glover V., Adams D., Modi N., Kumar R.C. Infant massage improves mother-infant interaction for mothers with postnatal depression. J. Affect. Disord. 2001, 63:201-207.
81. Operaña T.N., Tukey R.H. Oligomerization of the UDP-glucuronosyltransferase 1A proteins: homo- and heterodimerization analysis by fluorescence resonance energy transfer and co-immunoprecipitation. J. Biol. Chem. 2007, 282:4821-4829.
82. Ota Y., Maruo Y., Matsui K., Mimura Y., Sato H., Takeuchi Y. Inhibitory effect of 5β-pregnane-3α,20β-diol on transcriptional activity and enzyme activity of human bilirubin UDP-glucuronosyltransferase. Pediatr. Res. 2011, 70:453-457.
83. Owens D., Evans J. Population study on Gilbert's syndrome. J. Med. Genet. 1975, 12:152-156.
84. Peters W.H., Allebes W.A., Jansen P.L., Poels L.G., Capel P.J. Characterization and tissue specificity of a monoclonal antibody against human uridine 5'-diphosphate-glucuronosyltransferase. Gastroenterology 1987, 93:162-169.
85. Ramos A., Silverberg M., Stern M. Pregnanediol and neonatal hyperbilirubinemia. Am. J. Dis. Child. 1966, 111:353-356.
86. Ritter J.K., Yeatman M.T., Ferreira P., Owens I.S. Identification of a genetic alteration in the code for bilirubin UDP-glucuronosyltransferase in the UGT1 gene complex of a crigler-najjar type I patient. J. Clin. Invest. 1992, 90:150-155.
87. Ritter J.K., Yeatman M.T., Kaiser C., Gridelli B., Owens I.S. A phenylalanine codon deletion at the UGT1 gene complex locus of a crigler-najjar type I patient generates a pH-sensitive bilirubin UDP-glucuronosyltransferase. J. Biol. Chem. 1993, 268:23573-23579.
88. Ritter J.K., Kessler F.K., Thompson M.T., Grove A.D., Auyeung D.J., Fisher R.A. Expression and inducibility of the human bilirubin UDP-glucuronosyltransferase UGT1A1 in liver and cultured primary hepatocytes: evidence for both genetic and environmental influences. Hepatology 1999, 30:476-484.
89. Robertson K.J., Clarke D., Sutherland L., Wooster R., Coughtrie M.W., Burchell B. Investigation of the molecular basis of the genetic deficiency of UDP-glucuronosyltransferase in crigler-najjar syndrome. J. Inherit. Metab. Dis. 1991, 14:563-579.
90. Rodriguez J., Rice M. Low birth weight and subsequent poor weight gain. J. Pediatr. Health Care 2014, 28:350-356.
91. Rowland A., Miners J.O., Mackenzie P.I. The UDP-glucuronosyltransferases: their role in drug metabolism and detoxification. Int. J. Biochem. Cell Biol. 2013, 45:1121-1132.
92. Salih F.M. Can sunlight replace phototherapy units in the treatment of neonatal jaundice? An in vitro study. Photodermatol. Photoimmunol. Photomed. 2001, 17:272-277.
93. Sato H., Uchida T., Toyota K., Kanno M., Hashimoto T., Watanabe M., Nakamura T., Tamiya G., Aoki K., Hayasaka K. Association of breast-fed neonatal hyperbilirubinemia with UGT1A1 polymorphisms: 211G>a (G71R) mutation becomes a risk factor under inadequate feeding. J. Hum. Genet. 2013, 58:7-10.
94. Schneider A.P. Breast milk jaundice in the newborn. A real entity. JAMA 1986, 255:3270-3274.
95. Shapiro S.M. Bilirubin toxicity in the developing nervous system. Pediatr. Neurol. 2003, 29:410-421.
96. Shapiro S.M. Definition of the clinical spectrum of kernicterus and bilirubin-induced neurologic dysfunction (BIND). J. Perinatol. 2005, 25:54-59.
97. Shapiro S.M. Chronic bilirubin encephalopathy: diagnosis and outcome. Semin. Fetal Neonatal Med. 2010, 15:157-163.
98. Shelby M.K., Cherrington N.J., Vansell N.R., Klaassen C.D. Tissue mRNA expression of the rat UDP-glucuronosyltransferase gene family. Drug Metab. Dispos. 2003, 31:326-333.
99. Shepherd S.R., Baird S.J., Hallinan T., Burchell B. An investigation of the transverse topology of bilirubin UDP-glucuronosyltransferase in rat hepatic endoplasmic reticulum. Biochem. J. 1989, 259:617-620.
100. Shibuya A., Itoh T., Tukey R.H., Fujiwara R. Impact of fatty acids on human UDP-glucuronosyltransferase 1A1 activity and its expression in neonatal hyperbilirubinemia. Sci. Rep. 2013, 3:2903.
101. Sieg A., Arab L., Schlierf G., Stiehl A., Kommerell B. Prevalence of Gilbert's syndrome in Germany. Dtsch. Med. Wochenschr. 1987, 112:1206-1208.
102. Stevenson I.H., Dutton G.J. Glucuronide synthesis in kidney and gastrointestinal tract. Biochem. J. 1962, 82:330-340.
103. Stiehm E.R., Ryan J. Breast-milk jaundice. Report of eight cases and effect of breast feeding on incidence and severity of unexplained hyperbilirubinemia. Am. J. Dis. Child. 1965, 109:212-216.
104. Strassburg C.P. Pharmacogenetics of Gilbert's syndrome. Pharmacogenomics 2008, 9:703-715.
105. Strassburg C.P., Oldhafer K., Manns M.P., Tukey R.H. Differential expression of the UGT1A locus in human liver, biliary, and gastric tissue: identification of UGT1A7 and UGT1A10 transcripts in extrahepatic tissue. Mol. Pharmacol. 1997, 52:212-220.
106. Strassburg C.P., Nguyen N., Manns M.P., Tukey R.H. Polymorphic expression of the UDP-glucuronosyltransferase UGT1A gene locus in human gastric epithelium. Mol. Pharmacol. 1998, 54:647-654.
107. Strassburg C.P., Manns M.P., Tukey R.H. Expression of the UDP-glucuronosyltransferase 1A locus in human colon. Identification and characterization of the novel extrahepatic UGT1A8. J. Biol. Chem. 1998, 273:8719-8726.
108. Strassburg C.P., Nguyen N., Manns M.P., Tukey R.H. UDP-glucuronosyltransferase activity in human liver and colon. Gastroenterology 1999, 116:149-160.
109. Strassburg C.P., Strassburg A., Nguyen N., Li Q., Manns M.P., Tukey R.H. Regulation and function of family 1 and family 2 UDP- glucuronosyltransferase genes (UGT1A, UGT2B) in human oesophagus. Biochem. J. 1999, 338(Pt 2):489-498.
110. Strassburg C.P., Strassburg A., Kneip S., Barut A., Tukey R.H., Rodeck B., Manns M.P. Developmental aspects of human hepatic drug glucuronidation in young children and adults. Gut 2002, 50:259-265.
111. Sumida K., Kawana M., Kouno E., Itoh T., Takano S., Narawa T., Tukey R.H., Fujiwara R. Importance of UDP-glucuronosyltransferase 1A1 expression in skin and its induction by UVB in neonatal hyperbilirubinemia. Mol. Pharmacol. 2013, 84:679-686.
112. Takahashi S., Nozawa M., Sugitani K., Ishida K. Effect of small bowel transplantation in the congenitally enzyme-deficient Gunn rat. Transplant. Proc. 1994, 26:1675-1678.
113. Travan L., Lega S., Crovella S., Montico M., Panontin E., Demarini S. Severe neonatal hyperbilirubinemia and UGT1A1 promoter polymorphism. J. Pediatr. 2014, 165:42-45.
114. Tukey R.H., Strassburg C.P. Human UDP-glucuronosyltransferases: metabolism, expression, and disease. Annu. Rev. Pharmacol. Toxicol. 2000, 40:581-616.
115. Tukey R.H., Strassburg C.P. Genetic multiplicity of the human UDP-glucuronosyltransferases and regulation in the gastrointestinal tract. Mol. Pharmacol. 2001, 59:405-414.
116. Vanstapel F., Blanckaert N. Topology and regulation of bilirubin UDP-glucuronyltransferase in sealed native microsomes from rat liver. Arch. Biochem. Biophys. 1988, 263:216-225.
117. Victora C.G., Vaughan J.P., Martines J.C., Barcelos L.B. Is prolonged breast-feeding associated with malnutrition?. Am. J. Clin. Nutr. 1984, 39:307-314.
118. Waddell I.D., Robertson K., Burchell A., Hume R., Burchell B. Evidence for glucuronide (small molecule) sorting by human hepatic endoplasmic reticulum. Mol. Membr. Biol. 1995, 12:283-288.
119. Watchko J.F., Oski F.A. Kernicterus in preterm newborns: past, present, and future. Pediatrics 1992, 90:707-715.
120. Williams J.A., Hyland R., Jones B.C., Smith D.A., Hurst S., Goosen T.C., Peterkin V., Koup J.R., Ball S.E. Drug-drug interactions for UDP-glucuronosyltransferase substrates: a pharmacokinetic explanation for typically observed low exposure (AUCi/AUC) ratios. Drug Metab. Dispos. 2004, 32:1201-1208.
121. Wincent E., Amini N., Luecke S., Glatt H., Bergman J., Crescenzi C., Rannug A., Rannug U. The suggested physiologic aryl hydrocarbon receptor activator and cytochrome P4501 substrate 6-formylindolo[3,2-b]carbazole is present in humans. J. Biol. Chem. 2009, 284:2690-2696.
122. Yueh M.F., Huang Y.H., Hiller A., Chen S., Nguyen N., Tukey R.H. Involvement of the xenobiotic response element (XRE) in Ah receptor-mediated induction of human UDP-glucuronosyltransferase 1A1. J. Biol. Chem. 2003, 278:15001-15006.
123. Yueh M.F., Chen S., Nguyen N., Tukey R.H. Developmental onset of bilirubin-induced neurotoxicity involves toll-like receptor 2-dependent signaling in humanized UDP-glucuronosyltransferase1 mice. J. Biol. Chem. 2014, 289:4699-4709.
124. Zanardo V., Golin R., Amato M., Trevisanuto D., Favaro F., Faggian D., Plebani M. Cytokines in human colostrum and neonatal jaundice. Pediatr. Res. 2007, 62:191-194.
125. Zhang W., He Y.J., Gan Z., Fan L., Li Q., Wang A., Liu Z.Q., Deng S., Huang Y.F., Xu L.Y., Zhou H.H. OATP1B1 polymorphism is a major determinant of serum bilirubin level but not associated with rifampicin-mediated bilirubin elevation. Clin. Exp. Pharmacol. Physiol. 2007, 34:1240-1244.