Reconstruction of the carnitine biosynthesis pathway from Neurospora crassa in the yeast Saccharomyces cerevisiae

Applied Microbiology and Biotechnology

Volumn 99, Issue 15, 2015, Pages 6377-6389

  Franken, Jaco ^a   Burger, Anita ^a,b   Swiegers, Jan H ^a   Bauer, Florian F ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b Technology Innovation Agency   (South Africa)

Author keywords

Biosynthesis; Carnitine; Neurospora crassa; Saccharomyces cerevisiae

Indexed keywords

AMINO ACIDS; BIOCHEMISTRY; BIOSYNTHESIS; ELECTRODEPOSITION; ELECTROSPRAY IONIZATION; ENZYMES; HYDROPHILICITY; IONIC LIQUIDS; IONIZATION OF LIQUIDS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY;

CARNITINE; CARNITINE BIOSYNTHESIS; EUKARYOTIC MICROORGANISMS; HYDROPHILIC INTERACTION LIQUID CHROMATOGRAPHIES; NEUROSPORA CRASSA; SERINE HYDROXYMETHYLTRANSFERASE; WHOLE-CELL BIOTRANSFORMATIONS; YEAST SACCHAROMYCES CEREVISIAE;

YEAST;

CARNITINE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCINE HYDROXYMETHYLTRANSFERASE; THREONINE;

BACTERIUM; BIOENGINEERING; BIOTRANSFORMATION; INDUSTRIAL WASTE; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; YEAST;

ARTICLE; BIOSYNTHESIS; CLONING VECTOR; DELETION MUTANT; ELECTROSPRAY MASS SPECTROMETRY; FUNGAL STRAIN; GENE SYNTHESIS; HYDROPHILIC INTERACTION CHROMATOGRAPHY; NEUROSPORA CRASSA; NONHUMAN; RESTRICTION SITE; SACCHAROMYCES CEREVISIAE; GENETICS; MASS SPECTROMETRY; METABOLIC ENGINEERING; METABOLISM; PROCEDURES;

BACTERIA (MICROORGANISMS); EUKARYOTA; FUNGI; NEUROSPORA CRASSA; SACCHAROMYCES CEREVISIAE;

BIOSYNTHETIC PATHWAYS; CARNITINE; MASS SPECTROMETRY; METABOLIC ENGINEERING; NEUROSPORA CRASSA; SACCHAROMYCES CEREVISIAE;

EID: 84937640392     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-6561-x     Document Type: Article

References (50)

1. Aouida M, Rubio-Texeira M, Rubio Texeira M, Thevelein JM, Poulin R, Ramotar D (2013) Agp2, a member of the yeast amino acid permease family, positively regulates polyamine transport at the transcriptional level. PLoS One 8:e65717. doi:10.1371/journal.pone.0065717
2. Berben G, Dumont J, Gilliquet V, Bolle PA, Hilger F (1991) The YDp plasmids: a uniform set of vectors bearing versatile gene disruption cassettes for Saccharomyces cerevisiae. Yeast 7:475–477. doi:10.1002/yea.320070506
3. Bernal V, Sevilla A, Cánovas M, Iborra JL (2007) Production of L-carnitine by secondary metabolism of bacteria. Microb Cell Fact 6:31. doi:10.1186/1475-2859-6-31
4. Bieber LL (1988) Carnitine. Annu Rev Biochem 57:261–283. doi:10.1146/annurev.bi.57.070188.001401
5. Bonafé L, Berger MM, Que YA, Mechanick JI (2014) Carnitine deficiency in chronic critical illness. Curr Opin Clin Nutr Metab Care 17:200–209. doi:10.1097/MCO.0000000000000037
6. Borum PR, Broquist HP (1977) Purification of S-adenosylmethionine: epsilon-N-L-lysine methyltransferase. The first enzyme in carnitine biosynthesis. J Biol Chem 252:5651–5655
7. Brass EP (2004) Carnitine and sports medicine: use or abuse? Ann N Y Acad Sci 1033:67–78. doi:10.1196/annals.1320.006
8. Calabrese V, Giuffrida Stella AM, Calvani M, Butterfield DA (2006) Acetylcarnitine and cellular stress response: roles in nutritional redox homeostasis and regulation of longevity genes. J Nutr Biochem 17:73–88. doi:10.1016/j.jnutbio.2005.03.027
9. Canelas AB, ten Pierick A, Ras C, Seifar RM, van Dam JC, van Gulik WM, Heijnen JJ (2009) Quantitative evaluation of intracellular metabolite extraction techniques for yeast metabolomics. Anal Chem 81:7379–7389. doi:10.1021/ac900999t
10. Casey GP, Xiao W, Rank GH (1988) A convenient dominant selection marker for gene transfer in industrial strains of Saccharomyces yeast: SMRI encoded resistance to the herbicide sulfometuron methyl. J Inst Brew 94:93–97. doi:10.1002/j.2050-0416.1988.tb04564.x
11. Chen Y, Abbate M, Tang L, Cai G, Gong Z, Wei R, Zhou J, Chen X (2014) L-Carnitine supplementation for adults with end-stage kidney disease requiring maintenance hemodialysis: a systematic review and meta-analysis. Am J Clin Nutr 99:408–422. doi:10.3945/ajcn.113.062802
12. Chern MK, Pietruszko R (1995) Human aldehyde dehydrogenase E3 isozyme is a betaine aldehyde dehydrogenase. Biochem Biophys Res Commun 213:561–568. doi:10.1006/bbrc.1995.2168
13. Davis RH, de Serres FJ (1970) Metabolism of amino acids and amines part A. Methods Enzymol 17:79–143. doi:10.1016/0076-6879(71)17168-17176
14. DiNicolantonio JJ, Lavie CJ, Fares H, Menezes AR, O’Keefe JH (2013) L-carnitine in the secondary prevention of cardiovascular disease: systematic review and meta-analysis. Mayo Clin Proc 88:544–551. doi:10.1016/j.mayocp.2013.02.007
15. Dunn WA, Rettura G, Seifter E, Englard S (1984) Carnitine biosynthesis from γ-butyrobetaine and from exogenous protein-bound 6-N-trimethyl-L-lysine by the perfused guinea pig liver. Effect of ascorbate deficiency on the in situ activity of γ-butyrobetaine hydroxylase. J Biol Chem 259:10764–10770
16. Franken J, Bauer FF (2010) Carnitine supplementation has protective and detrimental effects in Saccharomyces cerevisiae that are genetically mediated. FEMS Yeast Res 10:270–281
17. Franken J, Kroppenstedt S, Swiegers JH, Bauer FF (2008) Carnitine and carnitine acetyltransferases in the yeast Saccharomyces cerevisiae: a role for carnitine in stress protection. Curr Genet 53:347–360
18. Ghaddar K, Krammer E-M, Mihajlovic N, Brohée S, André B, Prévost M (2014) Converting the yeast arginine Can1 permease to a lysine permease. J Biol Chem 289:7232–7246. doi:10.1074/jbc.M113.525915
19. Gietz RD, Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534
20. Henderson JW, Brooks A (2010) Improved amino acid methods using Agilent ZORBAX Eclipse Plus C18 columns for a variety of Agilent LC instrumentation and separation goals. Agilent Technologies, Wilmington, DE. http://www.chem.agilent.com/Library/applications/5990-4547EN.pdf
21. Henderson LM, Nelson PJ, Henderson L (1982) Mammalian enzymes of trimethyllysine conversion to trimethylaminobutyrate. Fed Proc 41:2843–2847
22. Kang W-K, Lee B-U, Park Y, Koh E-S, Ju E-S, Lee J, Kim H, Choi H (2010) A microorganism of Enterobacteriaceae genus harbouring genes associated with L-carnitine biosynthesis and method of producing l-carnitine using the microorganism U.S. Patent 7718414
23. Kikonyogo A, Pietruszko R (1996) Aldehyde dehydrogenase from adult human brain that dehydrogenates γ-aminobutyraldehyde: purification, characterization, cloning and distribution. Biochem J 316(Pt 1):317–324
24. Kurys G, Shah PC, Kikonygo A, Reed D, Ambroziak W, Pietruszko R (1993) Human aldehyde dehydrogenase. cDNA cloning and primary structure of the enzyme that catalyzes dehydrogenation of 4-aminobutyraldehyde. Eur J Biochem 218:311–320
25. LaBadie J, Dunn WA, Aronson NN (1976) Hepatic synthesis of carnitine from protein-bound trimethyl-lysine. Lysosomal digestion of methyl-lysine-labelled asialo-fetuin. Biochem J 160:85–95
26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404
27. Lin SW, Chen JC, Hsu LC, Hsieh CL, Yoshida A (1996) Human γ-aminobutyraldehyde dehydrogenase (ALDH9): cDNA sequence, genomic organization, polymorphism, chromosomal localization, and tissue expression. Genomics 34:376–380. doi:10.1006/geno.1996.0300
28. Longo N, di San A, Filippo C, Pasquali M (2006) Disorders of carnitine transport and the carnitine cycle. Am J Med Genet C Semin Med Genet 142C:77–85. doi:10.1002/ajmg.c.30087
29. McCluskey K, Wiest A, Plamann M (2010) The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci 35:119–126
30. Meyer H-P, Robins KT (2005) Large scale bioprocess for the production of optically pure L-carnitine. Monatsh Chem 136:1269–1277. doi:10.1007/s00706-005-0330-y
31. Monschau N, Stahmann KP, Sahm H, McNeil JB, Bognar AL (1997) Identification of Saccharomyces cerevisiae GLY1 as a threonine aldolase: a key enzyme in glycine biosynthesis. FEMS Microbiol Lett 150:55–60
32. Moses SBG, Otero RRC, Pretorius IS (2005) Domain engineering of Saccharomyces cerevisiae exoglucanases. Biotechnol Lett 27:355–362. doi:10.1007/s10529-005-1014-8
33. Ramsay RR, Gandour RD, van der Leij FR (2001) Molecular enzymology of carnitine transfer and transport. Biochim Biophys Acta 1546:21–43
34. Servillo L, Giovane A, Cautela D, Castaldo D, Balestrieri ML (2014) Where does N(ε)-trimethyllysine for the carnitine biosynthesis in mammals come from? PLoS One 9:e84589. doi:10.1371/journal.pone.0084589
35. Shanahan C (2011) L-carnitine: getting noticed in a challenging market place. Retrieved from http://www.frost.com/reg/blog-display.do?id=28527
36. Siebert PD, Chenchik A (1993) Modified acid guanidinium thiocyanate-phenol-chloroform RNA extraction method which greatly reduces DNA contamination. Nucleic Acids Res 21:2019–2020
37. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27
38. Stein R, Englard S (1981) The use of a tritium release assay to measure 6-N-trimethyl-L-lysine hydroxylase activity: synthesis of 6-N-[3-3H]trimethyl-DL-lysine. Anal Biochem 116:230–236
39. Swiegers JH, Dippenaar N, Pretorius IS, Bauer FF (2001) Carnitine-dependent metabolic activities in Saccharomyces cerevisiae: three carnitine acetyltransferases are essential in a carnitine-dependent strain. Yeast 18:585–595. doi:10.1002/yea.712
40. Swiegers JH, Vaz FM, Pretorius IS, Wanders RJA, Bauer FF (2002) Carnitine biosynthesis in Neurospora crassa: identification of a cDNA coding for epsilon-N-trimethyllysine hydroxylase and its functional expression in Saccharomyces cerevisiae. FEMS Microbiol Lett 210:19–23
41. Tein I, Bukovac SW, Xie ZW (1996) Characterization of the human plasmalemmal carnitine transporter in cultured skin fibroblasts. Arch Biochem Biophys 329:145–155. doi:10.1006/abbi.1996.0203
42. Van Roermund CW, Elgersma Y, Singh N, Wanders RJ, Tabak HF (1995) The membrane of peroxisomes in Saccharomyces cerevisiae is impermeable to NAD(H) and acetyl-CoA under in vivo conditions. EMBO J 14:3480–3486
43. Vaz FM, Wanders RJA (2002) Carnitine biosynthesis in mammals. Biochem J 361:417–429
44. Vaz FM, van Gool S, Ofman R, Ijlst L, Wanders RJ (1998) Carnitine biosynthesis: identification of the cDNA encoding human γ-butyrobetaine hydroxylase. Biochem Biophys Res Commun 250:506–510. doi:10.1006/bbrc.1998.9343
45. Vaz FM, van Gool S, Ofman R, Ijlst L, Wanders RJ (1999) Carnitine biosynthesis. Purification of γ-butyrobetaine hydroxylase from rat liver. Adv Exp Med Biol 466:117–124
46. Vaz FM, Fouchier SW, Ofman R, Sommer M, Wanders RJ (2000) Molecular and biochemical characterization of rat γ-trimethylaminobutyraldehyde dehydrogenase and evidence for the involvement of human aldehyde dehydrogenase 9 in carnitine biosynthesis. J Biol Chem 275:7390–7394
47. Vaz FM, Ofman R, Westinga K, Back JW, Wanders RJ (2001) Molecular and biochemical characterization of rat ε-N-trimethyllysine hydroxylase, the first enzyme of carnitine biosynthesis. J Biol Chem 276:33512–33517. doi:10.1074/jbc.M105929200
48. Vogel HJ (1956) A convenient growth medium for Neurospora (Medium N). Microbial Genet Bull 13:42–43
49. Winston F, Dollard C, Ricupero-Hovasse SL (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53–55. doi:10.1002/yea.320110107
50. Winter SC (2003) Treatment of carnitine deficiency. J Inherit Metab Dis 26:171–180