, Volume 138, Issue 7, pp 695–708 | Cite as

Mammalian carboxylesterase 3: comparative genomics and proteomics

  • Roger S. Holmes
  • Laura A. Cox
  • John L. VandeBerg


At least five families of mammalian carboxylesterases (CES) catalyse the hydrolysis or transesterification of a wide range of drugs and xenobiotics and may also participate in fatty acyl and cholesterol ester metabolism. In this study, in silico methods were used to predict the amino acid sequences, secondary and tertiary structures, and gene locations for CES3 genes and encoded proteins using data from several mammalian genome projects. Mammalian CES3 genes were located within a CES gene cluster with CES2 and CES6 genes, usually containing 13 exons transcribed on the positive DNA strand. Evidence is reported for duplicated CES3 genes for the chimp and mouse genomes. Mammalian CES3 protein subunits shared 58–97% sequence identity and exhibited sequence alignments and identities for key CES amino acid residues as well as extensive conservation of predicted secondary and tertiary structures with those previously reported for human CES1. The human genome project has previously reported CES3 mRNA isoform expression in several tissues, particularly in colon, trachea and in brain. Predicted human CES3 isoproteins were apparently derived from exon shuffling and are likely to be secreted extracellularly or retained within the cytoplasm. Mouse CES3-like transcripts were localized in specific regions of the mouse brain, including the cerebellum, and may play a role in the detoxification of drugs and xenobiotics in neural tissues and other tissues of the body. Phylogenetic analyses demonstrated the relationships and potential evolutionary origins of the mammalian CES3 family of genes which were related to but distinct from other mammalian CES gene families.


Mammals Amino acid sequence Carboxylesterase Evolution Gene duplication 



This project was supported by NIH Grants P01 HL028972 and P51 RR013986. In addition, this investigation was conducted in facilities constructed with support from Research Facilities Improvement Program Grant Numbers 1 C06 RR13556, 1 C06 RR15456, 1 C06 RR017515. We gratefully acknowledge the assistance of Dr B. Patel in studying the phylogeny of CES3 and related CES gene families.


  1. Ahmad S, Forgash AJ (1976) Nonoxidative enzymes in the metabolism of insecticides. Drug Metab Rev 5:141–164CrossRefGoogle Scholar
  2. Aida K, Moore R, Negishi M (1993) Cloning and sequencing of a novel, male-predominant carboxylesterase in mouse liver. Biochim Biophys Acta 1174:72–74PubMedGoogle Scholar
  3. Altschul F, Vyas V, Cornfield A, Goodin S, Ravikumar TS, Rubin EH, Gupta E (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  4. Becker A, Bottcher A, Lackner KJ, Fehringer P, Notka F, Aslandis C, Schmithz C (1994) Purification, cloning and expression of a human enzyme with acyl coenzyme A: cholesterol acyltransferase activity, which is identical to liver carboxylesterase. Arterioscler Thromb 14:1346–1355PubMedGoogle Scholar
  5. Bencharit S, Morton CL, Xue Y, Potter PM, Redinbo MR (2003) Structural basis of heroin and cocaine metabolism by a promiscuous human drug-processing enzyme. Nat Struct Biol 10:349–356CrossRefPubMedGoogle Scholar
  6. Bencharit S, Edwards CC, Morton CL, Howard-Williams EL, Kuhn P, Potter PM, Redinbo MR (2006) Multisite promiscuity in the processing of endogenous substrates by human carboxylesterase 1. J Mol Biol 363:201–214CrossRefPubMedGoogle Scholar
  7. Bovine Genome Project (2008)
  8. Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437:69–87CrossRefGoogle Scholar
  9. Clark HF, Gurney AL, Abaya E, Baker K, Baldwin D, Brush J, Chen J, Chow B, Chui C, Crowley C, Currell B, Deuel B, Dowd P, Eaton D, Foster J, Grimaldi C, Gu Q, Hass PE, Heldens S, Huang A, Kim HS, Klimowski L, Jin Y, Johnson S, Lee J, Lewis L, Liao D, Mark M, Robbie E, Sanchez C, Schoenfeld J, Seshagiri S, Simmons L, Singh J, Smith V, Stinson J, Vagts A, Vandlen R, Watanabe C, Wieand D, Woods K, Xie MH, Yansura D, Yi S, Yu G, Yuan J, Zhang M, Zhang Z, Goddard A, Wood WI, Godowski P, Gray A (2003) The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment. Genome Res 13:226–2270Google Scholar
  10. Cygler M, Schrag JD, Sussman JL, Harel M, Silman I, Gentry MK, Dostor BP (1993) Relationship between sequence conservation and three-dimensional structure in a large family of esterases, lipases and related proteins. Protein Sci 2:366–382PubMedCrossRefGoogle Scholar
  11. Diczfalusy MA, Bjorkkem I, Einarsson C, Hillebrant CG, Alexson SE (2001) Characterization of enzymes involved in formation of ethyl esters of long-chain fatty acids. J Lipid Res 42:1025–1032PubMedGoogle Scholar
  12. Dolinsky VW, Sipione S, Lehner R, Vance DE (2001) The cloning and expression of murine triacylglycerol hydrolase cDNA and the structure of the corresponding gene. Biochim Biophys Acta 1532:162–172PubMedGoogle Scholar
  13. Donoghue PCJ, Benton MJ (2007) Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends Genet 22:424–431Google Scholar
  14. Ecroyd H, Belghazi M, Dacheux JL, Miyazaki M, Yamashita T, Gatti JL (2006) An epididymal form of cauxin, a carboxylesterase-like enzyme, is present and active in male reproductive fluids. Biol Reprod 74:439–447CrossRefPubMedGoogle Scholar
  15. Emmanuelsson O, Brunak S, von Heijne G, Nielson H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2:953–971CrossRefGoogle Scholar
  16. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  17. Fleming CD, Bencharit S, Edwards CC, Hyatt JL, Tsurkan L, Bai F, Fraga C, Morton CL, Howard-Williams EL, Potter PM, Redinbo MR (2005) Structural insights into drug processing by human carboxylesterase 1: tamoxifen, Mevaststin, and inhibition by Benzil. J Mol Biol 352:165–177CrossRefPubMedGoogle Scholar
  18. Ghosh S (2000) Cholesteryl ester hydrolase in human monocyte/macrophage: cloning, sequencing and expression of full-length cDNA. Physiol Genomics 2:1–8PubMedGoogle Scholar
  19. Ghosh S, Mallonee DH, Grogan WM (1995) Molecular cloning and expression of rat hepatic neutral cholesteryl ester hydrolase. Biochim Biophys Acta 1259:305–312PubMedGoogle Scholar
  20. Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modelling. Electrophoresis 18:2714–2723CrossRefPubMedGoogle Scholar
  21. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  22. Holmes RS, Duley JA, Burnell JN (1983) The alcohol dehydrogenase gene complex on chromosome 3 of the mouse. In: Rattazzi MC, Scandalios JG, Whitt GS (eds) Isozymes: current topics in biological and medical research, vol 8. Alan R Liss, New York, pp 155–174Google Scholar
  23. Holmes RS, Chan J, Cox LA, Murphy WJ, VandeBerg JL (2008a) Opossum carboxylesterases: sequences, phylogeny and evidence for CES duplication events predating the marsupial-eutherian common ancestor. BMC Evol Biol 8:54CrossRefPubMedGoogle Scholar
  24. Holmes RS, Cox LA, VandeBerg JL (2008b) Mammalian carboxylesterase 5: comparative biochemistry and genomics. Comp Biochem Physiol Part D 3:195–204Google Scholar
  25. Holmes RS, Glenn JP, VandeBerg JL, Cox LA (2009a) Baboon carboxylesterases 1 and 2: sequences, structures and phylogenetic relationships with human and other primate carboxylesterases. J Med Primatol 38:27–38CrossRefPubMedGoogle Scholar
  26. Holmes RS, VandeBerg JL, Cox LA (2009b) Bovine carboxylesterases: evidence for two CES1 and five families of CES genes on chromosome 18. Comp Biochem Physiol Part D 4:11–20Google Scholar
  27. Holmes RS, VandeBerg JL, Cox LA (2009c) Horse carboxylesterases: evidence for six CES1 and four families of CES genes on chromosome 3. Comp Biochem Physiol Part D 4:54–65Google Scholar
  28. Holmes RS, VandeBerg JL, Cox LA (2009d) A new class of mammalian carboxylesterase CES6. Comp Biochem Physiol Part D 4:209–217Google Scholar
  29. Hoog J-O, Stromberg P, Hedberg JJ, Griffiths WJ (2003) The mammalian alcohol dehydrogenases interact in several pathways. Chem Biol Interact 143–144:175–181CrossRefPubMedGoogle Scholar
  30. Horse Genome Project (2008)
  31. Horton P, Nakai K (1997) Better prediction of cellular localization sites with the k nearest neighbors classifier. Proc Int Conf Intell Syst Mol Biol 5:147–152PubMedGoogle Scholar
  32. Hosokawa M, Furihata T, Yaginuma Y, Yamamoto N, Kayano N, Fujii A, Nagahara Y, Satoh T, Chiba K (2007) Genomic structure and transcriptional regulation of the rat, mouse and human carboxylesterase genes. Drug Metab Rev 39:1–15CrossRefPubMedGoogle Scholar
  33. Humerickhouse R, Lohrbach K, Li L, Bosron WF, Dolan ME (2000) Characterization of CPT-11 hydrolysis by human liver carboxylesterase isoforms h-CE1 and hCE-2. Cancer Res 60:1189–1192PubMedGoogle Scholar
  34. Imai T (2006) Human carboxylesterase isozymes: catalytic properties and rational drug design. Drug Metab Pharmacokinet 21:173–185CrossRefPubMedGoogle Scholar
  35. Imai T, Yoshigae Y, Hosokawa M, Chiba K, Otagiri M (2003) Evidence for the involvement of a pulmonary first-pass effect via carboxylesterase in the disposition of a propanolol ester derivative after intravenous administration. J Pharmacol Exp Ther 307:1234–1242CrossRefPubMedGoogle Scholar
  36. International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921CrossRefGoogle Scholar
  37. Jornvall H, Hoog J-O, Persson B, Pares X (2000) Pharmacogenetics of the alcohol dehydrogenase system. Pharmacology 61:184–191CrossRefPubMedGoogle Scholar
  38. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2003) The human genome browser at UCSC. Genome Res 12:994–1006Google Scholar
  39. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  40. Kopp J, Schwede T (2004) The SWISS-MODEL repository of annotated three-dimensional protein structure homology models. Nucleic Acids Res 32:D230–D234CrossRefPubMedGoogle Scholar
  41. Kroetz DL, McBride OW, Gonzalez FJ (1993) Glycosylation-dependent activity of Baculovirus-expressed human liver carboxylesterases: cDNA cloning and characterization of two highly similar enzyme forms. Biochemistry 32:11606–11617CrossRefPubMedGoogle Scholar
  42. Langmann T, Becker A, Aslanidis C, Notka F, Ulrich H, Schwer H, Schcmitz G (1997) Structural organization and characterization of the promoter region of a human carboxylesterase gene. Biochim Biophys Acta 1350:65–74PubMedGoogle Scholar
  43. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen T-M, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong H-W, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KG, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH, Kuan CL, Lake JH, Laramee AR, Larsen KD, Lau C, Lemon TA, Liang AJ, Liu Y, Luong LT, Michaels J, Morgan JJ, Morgan RJ, Mortrud MT, Mosqueda NF, Ng LL, Ng R, Orta GJ, Overly CC, Pak TH, Parry SE, Pathak SD, Pearson OC, Puchalski RB, Riley ZL, Rockett HR, Rowland SA, Royall JJ, Ruiz MJ, Sarno NR, Schaffnit K, Shapovalova NV, Sivisay T, Slaughterbeck CR, Smith SC, Smith KA, Smith BI, Sodt AJ, Stewart NN, Stumpf K-R, Sunkin SM, Sutram M, Tam A, Teemer CD, Thaller C, Thompson CL, Varnam LR, Visel A, Whitlock RM, Wohnoutka PE, Wolkey CK, Wong VY, Wood M, Yaylaoglu MB, Young RC, Youngstrom BL, Yuan XF, Zhang B, Zwingman TA, Jones AR (2007) Genome wide atlas of gene expression in the mouse brain. Nature 145:168–176CrossRefGoogle Scholar
  44. Leinweber FJ (1987) Possible physiological roles of carboxyl ester hydrolases. Drug Metab Rev 18:379–439CrossRefPubMedGoogle Scholar
  45. Lockridge O, Adkins S, La Due BN (1987) Location of disulfide bonds within the sequence of human serum cholinesterase. J Biol Chem 262:12945–12952PubMedGoogle Scholar
  46. Marsh S, Xiao M, Yu J, Ahluwalia R, Minton M, Freimuth RR, Kwok P-Y, McLeod HL (2004) Pharmacogenomic assessment of carboxylesterases 1 and 2. Genomics 84:661–668CrossRefPubMedGoogle Scholar
  47. Marshall SD, Putterill JJ, Plummer KM, Newcomb RD (2003) The carboxylesterase gene family from Arabidopsis thaliana. J Mol Evol 57:487–500CrossRefPubMedGoogle Scholar
  48. McGuffin LJ, Bryson K, Jones DT (2000) The PSIPRED protein structure prediction server. Bioinformatics 16:404–405CrossRefPubMedGoogle Scholar
  49. MHC Sequencing Consortium (1999) Complete sequence and map of a human major histocompatibility complex. Nature 401:921–923CrossRefGoogle Scholar
  50. Mikkelsen TS, Wakefield MJ, Aken B, Amemiya CT, Chang JL, Duke S, Garber M, Gentles AJ, Goodstadt L, Heger A, Jurka J, Kamal M, Mauceli E, Searle SMJ, Sharpe T, Baker ML, Batzer MA, Benos PV, Belov K, Clamp M, Cook A, Cuff J, Das R, Davidow L, Deakin JE, Fazzari MJ, Glass JL, Grabherr M, Greally JM, Gu W, Hore TA, Huttley GA, Kleber M, Jirtle RL, Koina E, Lee JT, Mahony S, Marra MA, Miller RD, Nicholls RD, Oda M, Papenfuss AT, Parra ZE, Pollock DD, Ray DA, Schein JE, Speed TP, Thompson K, VandeBerg JL, Wade CM, Walker JA, Waters PD, Webber C, Weidman JR, Xie X, Zody MC, Broad Institute Genome Sequencing Platform, Broad Institute Whole Genome Assembly Team, Marshall Graves JA, Ponting CP, Breen M, Samollow PB, Lander ES, Lindblad-Toh K (2007) Genome of the marsupial Monodelphis domestica reveals innovation in noncoding sequences. Nature 447:167–177CrossRefPubMedGoogle Scholar
  51. Miyazaki M, Kamiie K, Soeta S, Taira H, Yamashita T (2003) Molecular cloning and characterization of a novel carboxylesterase-like protein that is physiologically present at high concentrations in the urine of domestic cats (Felis Catus). Biochem J 370:101–110CrossRefPubMedGoogle Scholar
  52. Miyazaki K, Yamashita T, Suzuki Y, Saito Y, Soeta S, Taira H, Suzuki A (2006) A major urinary protein of the domestic cat regulates the production the production of felinine, a putative pheromone precursor. Chem Biol 13:10171–10179CrossRefGoogle Scholar
  53. Mouse Genome Sequencing Consortium (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520–562CrossRefGoogle Scholar
  54. Munger JS, Shi GP, Mark EA, Chin DT, Gerard C, Chapman HA (1991) A serine esterase released by human alveolar macrophages is closely related to liver microsomal carboxylesterases. J Biol Chem 266:18832–18838PubMedGoogle Scholar
  55. Ohtsuka K, Inoue S, Kameyama M (2003) Intracellular conversion of irinotecan to its active form, SN-38, by native carboxylesterase in human non-small cell lung cancer. Lung Cancer 41:87–198CrossRefGoogle Scholar
  56. Ota T, Suzuki Y, Nishikawa T, Otsuki T, Sugiyama T, Irie R, Wakamatsu A, Hayashi K, Sato H, Nagai K, Kimura K, Makita H, Sekine M, Obayashi M, Nishi T, Shibahara T, Tanaka T, Ishii S, Yamamoto J, Saito K, Kawai Y, Isono Y, Nakamura Y, Nagahari K, Murakami K, Yasuda T, Iwayanagi T, Wagatsuma M, Shiratori A, Sudo H, Hosoiri T, Kaku Y, Kodaira H, Kondo H, Sugawara M, Takahashi M, Kanda K, Yokoi T, Furuya T, Kikkawa E, Omura Y, Abe K, Kamihara K, Katsuta N, Sato K, Tanikawa M, Yamazaki M, Ninomiya K, Ishibashi T, Yamashita H, Murakawa K, Fujimori K, Tanai H, Kimata M, Watanabe M, Hiraoka S, Chiba Y, Ishida S, Ono Y, Takiguchi S, Watanabe S, Yosida M, Hotuta T, Kusano J, Kanehori K, Takahashi-Fujii A, Hara H, Tanase TO, Nomura Y, Togiya S, Komai F, Hara R, Takeuchi K, Arita M, Imose N, Musashino K, Yuuki H, Oshima A, Sasaki N, Aotsuka S, Yoshikawa Y, Matsunawa H, Ichihara T, Shiohata N, Sano S, Moriya S, Momiyama H, Satoh N, Takami S, Terashima Y, Suzuki O, Nakagawa S, Senoh A, Mizoguchi H, Goto Y, Shimizu F, Wakebe H, Hishigaki H, Watanabe T, Sugiyama A, Takemoto M, Kawakami B, Yamazaki M, Watanabe K, Kumagai A, Itakura S, Fukuzumi Y, Fujimori Y, Komiyama M, Tashiro H, Tanigami A, Fujiwara T, Ono T, Yamada K, Fujii Y, Ozaki K, Hirao M, Ohmori Y, Kawabata A, Hikiji T, Kobatake N, Inagaki H, Ikema Y, Okamoto S, Okitani R, Kawakami T, Noguchi S, Itoh T, Shigeta K, Senba T, Matsumura K, Nakajima Y, Mizuno T, Morinaga M, Sasaki M, Togashi T, Oyama M, Hata H, Watanabe M, Komatsu T, Mizushima-Sugano J, Satoh T, Shirai Y, Takahashi Y, Nakagawa K, Okumura K, Nagase T, Nomura N, Kikuchi H, Masuho Y, Yamashita R, Nakai K, Yada T, Nakamura Y, Ohara O, Isogai T, Sugano S (2004) Complete sequencing and characterization of 21, 243 full-length human cDNAs. Nat Genet 36:40–45CrossRefPubMedGoogle Scholar
  57. Pindel EV, Kedishvili NY, Abraham TL, Brezinski MR, Zhang A, Dean RA, Bosron WF (1997) Purification and cloning of a broad substrate specificity human liver carboxylesterase that catalyzes the hydrolysis of cocaine and heroin. J Biol Chem 272:14769–14775CrossRefPubMedGoogle Scholar
  58. Potter PM, Wolverton JS, Morton CL, Wierdl M, Danks MK (1998) Cellular localization domains of a rabbit and human carboxylesterase: influence on irinotecan (CPT-11) metabolism by the rabbit enzyme. Cancer Res 58:3627–3632PubMedGoogle Scholar
  59. Redinbo MR, Potter PN (2005) Mammalian carboxylesterases: from drug targets to protein therapeutics. Drug Discov Today 10:313–320CrossRefPubMedGoogle Scholar
  60. Robbi M, Beaufay H (1991) The COOH terminus of several liver carboxylesterases targets these enzymes to the lumen of the endoplasmic reticulum. J Biol Chem 266:20498–20503PubMedGoogle Scholar
  61. Ruppert C, Bagheri A, Markart P, Schmidt R, Seegar W, Gunther A (2006) Liver carboxylesterase cleaves surfactant protein (SP-B) and promotes surfactant subtype conversion. Biochem Biophys Res Commun 348:1449–1454CrossRefPubMedGoogle Scholar
  62. Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–426PubMedGoogle Scholar
  63. Sanghani SP, Quinney SK, Fredenberg TB, Davis WI, Murray DJ, Bosron WF (2004) Hydrolysis of irinotecan and its oxidative metabolites, 7-ethyl-10-[4-N(5-aminopentanoic acid)-1-piperidino] carbonyloxycampothecin and 7-ethyl-10-[4-(1-piperidino)-1 amino]-carbonyloxycamptothecin, by human carboxylesterases CES1A1, CES2, and a newly expressed carboxylesterase isoenzyme, CES3. Drug Metab Dispos 32:505–511CrossRefPubMedGoogle Scholar
  64. Satoh T, Hosokawa M (1998) The mammalian carboxylesterases: from molecules to functions. Ann Rev Pharmacol Toxicol 38:257–288CrossRefGoogle Scholar
  65. Satoh T, Hosokawa M (2006) Structure, function and regulation of carboxylesterases. Chem-Biol Interact 162:195–211CrossRefPubMedGoogle Scholar
  66. Satoh H, Taylor P, Bosron WF, Sanghani P, Hosokawa M, Du PB (2002) Current progress on esterases: from molecular structure to function. Drug Metab Dispos 30:488–493CrossRefPubMedGoogle Scholar
  67. Schewer H, Langmann T, Daig R, Becker A, Aslandis C, Schmidt G (1997) Molecular cloning and characterization of a novel putative carboxylesterase, present in human intestine and liver. Biochem Biophys Res Commun 233:117–120CrossRefGoogle Scholar
  68. Shibita F, Takagi Y, Kitajima M, Kuroda T, Omura T (1993) Molecular cloning and characterization of a human carboxylesterase gene. Genomics 17:76–82CrossRefGoogle Scholar
  69. Tang X, Wu H, Wu Z, Wang G, Zhu D (2008) Carboxylesterase 2 is downregulated in colorectal cancer following progression of the disease. Cancer Invest 26:178–181CrossRefPubMedGoogle Scholar
  70. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol 7: S12.
  71. Tsujita T, Okuda H (1993) Palmitoyl-coenzyme A hydrolyzing activity in rat kidney and its relationship with carboxylesterase. J Lipid Res 34:1773–1781PubMedGoogle Scholar
  72. Van De Peer Y, de Wachter R (1994) TreeCon for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Sci 10:569–570Google Scholar
  73. von Heijne G (1983) Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem 133:17–21CrossRefGoogle Scholar
  74. Wang H, Gilham D, Lehner R (2007) Proteomic and lipid characterization of apo-lipoprotein B-free luminal lipid droplets from mouse liver microsomes: implications for very low density lipoprotein assembly. J Biol Chem 282:33218–33226CrossRefPubMedGoogle Scholar
  75. Woodburne MO, Rich TH, Springer MS (2003) The evolution of tribospheny and the antiquity of mammalian clades. Mol Phylogenet Evol 28:360–385CrossRefPubMedGoogle Scholar
  76. Xu G, Zhang W, Ma MK, MacLeod HL (2002) Human carboxylesterase 2 is commonly expressed in tumor tissue and is correlated with the activation of irinotecan. Clin Cancer Res 8:2605–2611PubMedGoogle Scholar
  77. Zhen L, Rusiniak ME, Swank RT (1995) The beta-glucuronidase propeptide contains a serpin-related octamer necessary for complex formation with egasyn esterase and for retention within the endoplasmic reticulum. J Biol Chem 270:11912–11920CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Roger S. Holmes
    • 1
    • 2
    • 3
  • Laura A. Cox
    • 1
    • 2
  • John L. VandeBerg
    • 1
    • 2
  1. 1.Department of GeneticsSouthwest Foundation for Biomedical ResearchSan AntonioUSA
  2. 2.Southwest National Primate Research CenterSouthwest Foundation for Biomedical ResearchSan AntonioUSA
  3. 3.School of Biomolecular and Physical SciencesGriffith UniversityNathanAustralia

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