Strategies of bacterial over expression of membrane transporters relevant in human health: The successful case of the three members of OCTN subfamily

Molecular Biotechnology

Volumn 54, Issue 2, 2013, Pages 724-736

  Indiveri, Cesare ^a   Galluccio, Michele ^a   Scalise, Mariafrancesca ^a   Pochini, Lorena ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

Author keywords

Carnitine; Crohn's disease; E. coli; Human health; Membrane proteins; Membrane transport; OCTN; Organic cations; Over expression

Indexed keywords

CARNITINE; CROHN'S DISEASE; E. COLI; HUMAN HEALTH; MEMBRANE PROTEINS; MEMBRANE TRANSPORT; OCTN; ORGANIC CATIONS; OVER-EXPRESSION;

BIOLOGICAL MEMBRANES; CELL CULTURE; DIAGNOSIS; ESCHERICHIA COLI; MAMMALS; PURIFICATION;

PROTEINS;

CARNITINE; HYBRID PROTEIN; MEMBRANE PROTEIN; OCTN1 PROTEIN; OCTN2 PROTEIN; OCTN3 PROTEIN; UNCLASSIFIED DRUG;

BACTERIAL STRAIN; CELL CULTURE; CELL LYSATE; CHROMATOGRAPHY; CODON; ESCHERICHIA COLI; GENE; HEALTH; HOST; HUMAN; MOLECULAR WEIGHT; NONHUMAN; PLASMID; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PURIFICATION; REVIEW; SCREENING;

ANIMALS; ESCHERICHIA COLI; GENETIC VECTORS; HUMANS; MEMBRANE TRANSPORT PROTEINS; ORGANIC CATION TRANSPORT PROTEINS; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); MAMMALIA; RATTUS;

EID: 84882431644     PISSN: 10736085     EISSN: 15590305     Source Type: Journal    
DOI: 10.1007/s12033-012-9586-8     Document Type: Review

References (99)

1. Broer, S., & Palacin, M. (2011). The role of amino acid transporters in inherited and acquired diseases. Biochemical Journal, 436, 193-211.
2. Lahjouji, K., Mitchell, G. A., & Qureshi, I. A. (2001). Carnitine transport by organic cation transporters and systemic carnitine deficiency. Molecular Genetics and Metabolism, 73, 287-297.
3. Daniel, H., & Kottra, G. (2004). The proton oligopeptide cotransporter family SLC15 in physiology and pharmacology. Pflugers Archiv: European Journal of Physiology, 447, 610-618.
4. Wright, E. M., & Turk, E. (2004). The sodium/glucose cotransport family SLC5. Pflugers Archiv: European Journal of Physiology, 447, 510-518.
5. Palmieri, F. (2008). Diseases caused by defects of mitochondrial carriers: A review. Biochimica et Biophysica Acta, 1777, 564-578.
6. Chou, J. Y., Matern, D., Mansfield, B. C., & Chen, Y. T. (2002). Type I glycogen storage diseases: Disorders of the glucose-6-phosphatase complex. Current Molecular Medicine, 2, 121-143.
7. Nakanishi, T., & Tamai, I. (2011). Solute carrier transporters as targets for drug delivery and pharmacological intervention for chemotherapy. The Journal of Pharmaceutical Sciences, 100, 3731-3750.
8. Sharom, F. J. (2011). The P-glycoprotein multidrug transporter. Essays in Biochemistry, 50, 161-178.
9. Tsuji, A. (2002). Transporter-mediated drug interactions. Drug Metabolism and Pharmacokinetics, 17, 253-274.
10. Pebay-Peyroula, E., Dahout-Gonzalez, C., Kahn, R., Trézé guet, V., Lauquin, G. J., & Brandolin, G. (2003). Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature, 426, 39-44.
11. Midgett, C. R., & Madden, D. R. (2007). Breaking the bottleneck: Eukaryotic membrane protein expression for high-resolution structural studies. Journal of Structural Biology, 160, 265-274.
12. Brinkmann, U., Mattes, R. E., & Buckel, P. (1989). High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene, 85, 109-114.
13. Kane, J. F. (1995). Effects of rare codon clusters on high-level expression of heterologous proteins in Escherichia coli. Current Opinion in Biotechnology, 6, 494-500.
14. Niimura, Y., Terabe, M., Gojobori, T., & Miura, K. (2003). Comparative analysis of the base biases at the gene terminal portions in seven eukaryote genomes. Nucleic Acids Research, 31, 5195-5201.
15. Kurland, C., & Gallant, J. (1996). Errors of heterologous protein expression. Current Opinion in Biotechnology, 7, 489-493.
16. Stenstrom, C. M., Jin, H., Major, L. L., Tate, W. P., & Isaksson, L. A. (2001). Codon bias at the 3′-side of the initiation codon is correlated with translation initiation efficiency in Escherichia coli. Gene, 263, 273-284.
17. Gonzalez de Valdivia, E. I., & Isaksson, L. A. (2004). A codon window in mRNA downstream of the initiation codon where NGG codons give strongly reduced gene expression in Escherichia coli. Nucleic Acids Research, 32, 5198-5205.
18. Bai, J., Swartz, D. J., Protasevich, I. I., Brouillette, C. G., Harrell, P. M., Hildebrandt, E., et al. (2011). A gene optimization strategy that enhances production of fully functional P-glycoprotein in Pichia pastoris. PLoS One, 6, e22577.
19. Liu, J., & Rost, B. (2001). Comparing function and structure between entire proteomes. Protein Science, 10, 1970-1979.
20. Klepsch, M. M., Persson, J. O., & de Gier, J. W. (2011). Consequences of the overexpression of a eukaryotic membrane protein, the human KDEL receptor, in Escherichia coli. Journal of Molecular Biology, 407, 532-542.
21. Eraly, S. A., Monte, J. C., & Nigam, S. K. (2004). Novel slc22 transporter homologs in fly, worm, and human clarify the phylogeny of organic anion and cation transporters. Physiological Genomics, 18, 12-24.
22. Jordan, I. K., Kondrashov, F. A., Adzhubei, I. A., Wolf, Y. I., Koonin, E. V., Kondrashov, A. S., et al. (2005). A universal trend of amino acid gain and loss in protein evolution. Nature, 433, 633-638.
23. Fiermonte, G., Walker, J. E., & Palmieri, F. (1993). Abundant bacterial expression and reconstitution of an intrinsic membrane-transport protein from bovine mitochondria. Biochemical Journal, 294(Pt 1), 293-299.
24. Indiveri, C., Iacobazzi, V., Giangregorio, N., & Palmieri, F. (1998). Bacterial overexpression, purification, and reconstitution of the carnitine/acylcarnitine carrier from rat liver mitochondria. Biochemical and Biophysical Research Communications, 249, 589-594.
25. Palmieri, F. (1994). Mitochondrial carrier proteins. FEBS Letters, 346, 48-54.
26. Harris, N. J., & Booth, P. J. (2012). Folding and stability of membrane transport proteins in vitro. Biochimica et Biophysica Acta, 1818, 1055-1066.
27. Miroux, B., & Walker, J. E. (1996). Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. Journal of Molecular Biology, 260, 289-298.
28. Wagner, S., Klepsch, M. M., Schlegel, S., Appel, A., Draheim, R., Tarry, M., et al. (2008). Tuning Escherichia coli for membrane protein overexpression. Proceedings of the National Academy of Sciences USA, 105, 14371-14376.
29. Liu, W., Wu, G., Tsai, A. L., & Kulmacz, R. J. (2011). High-yield production, purification and characterization of functional human duodenal cytochrome b in an Escherichia coli system. Protein Expression and Purification, 79, 115-121.
30. Keller, T., Schwarz, D., Bernhard, F., Dotsch, V., Hunte, C., Gorboulev, V., et al. (2008). Cell free expression and functional reconstitution of eukaryotic drug transporters. Biochemistry, 47, 4552-4564.
31. Wuu, J. J., & Swartz, J. R. (2008). High yield cell-free production of integral membrane proteins without refolding or detergents. Biochimica et Biophysica Acta, 1778, 1237-1250.
32. Schneider, B., Junge, F., Shirokov, V. A., Durst, F., Schwarz, D., Dotsch, V., et al. (2010). Membrane protein expression in cell-free systems. Methods in Molecular Biology, 601, 165-186.
33. Hino, M., Kataoka, M., Kajimoto, K., Yamamoto, T., Kido, J., Shinohara, Y., et al. (2008). Efficiency of cell-free protein synthesis based on a crude cell extract from Escherichia coli, wheat germ, and rabbit reticulocytes. Journal of Biotechnology, 133, 183-189.
34. Tanaka, K., Xu, W., Zhou, F., & You, G. (2004). Role of glycosylation in the organic anion transporter OAT1. Journal of Biological Chemistry, 279, 14961-14966.
35. Filippo, C. A., Ardon, O., & Longo, N. (2011). Glycosylation of the OCTN2 carnitine transporter: Study of natural mutations identified in patients with primary carnitine deficiency. Biochimica et Biophysica Acta, 1812, 312-320.
36. Quick, M., & Wright, E. M. (2002). Employing Escherichia coli to functionally express, purify, and characterize a human transporter. Proceedings of the National Academy of Sciences USA, 99, 8597-8601.
37. Leviatan, S., Sawada, K., Moriyama, Y., & Nelson, N. (2010). Combinatorial method for overexpression of membrane proteins in Escherichia coli. Journal of Biological Chemistry, 285, 23548-23556.
38. Pochini, L., Scalise, M., Galluccio, M., Amelio, L., & Indiveri, C. (2011). Reconstitution in liposomes of the functionally active human OCTN1 (SLC22A4) transporter overexpressed in Escherichia coli. Biochemical Journal, 439, 227-233.
39. Scalise, M., Galluccio, M., Pochini, L., & Indiveri, C. (2012). Over-expression in Escherichia coli, purification and reconstitution in liposomes of the third member of the OCTN sub-family: The mouse carnitine transporter OCTN3. Biochemical and Biophysical Research Communications, 422, 59-63.
40. Takai, K., Sawasaki, T., & Endo, Y. (2010). The wheat-germ cell-free expression system. Current Pharmaceutical Biotechnology, 11, 272-278.
41. Tate, C. G., & Blakely, R. D. (1994). The effect of N-linked glycosylation on activity of the Na(+)- and Cl(-)-dependent serotonin transporter expressed using recombinant baculovirus in insect cells. Journal of Biological Chemistry, 269, 26303-26310.
42. Mohanty, A. K., & Wiener, M. C. (2004). Membrane protein expression and production: Effects of polyhistidine tag length and position. Protein Expression and Purification, 33, 311-325.
43. Marblestone, J. G., Edavettal, S. C., Lim, Y., Lim, P., Zuo, X., & Butt, T. R. (2006). Comparison of SUMO fusion technology with traditional gene fusion systems: Enhanced expression and solubility with SUMO. Protein Science, 15, 182-189.
44. Zuo, X., Li, S., Hall, J., Mattern, M. R., Tran, H., Shoo, J., et al. (2005). Enhanced expression and purification of membrane proteins by SUMO fusion in Escherichia coli. Journal of Structural and Functional Genomics, 6, 103-111.
45. Roosild, T. P., Greenwald, J., Vega, M., Castronovo, S., Riek, R., & Choe, S. (2005). NMR structure of Mistic, a membrane-integrating protein for membrane protein expression. Science, 307, 1317-1321.
46. Dvir, H., & Choe, S. (2009). Bacterial expression of a eukaryotic membrane protein in fusion to various Mistic orthologs. Protein Expression and Purification, 68, 28-33.
47. Sato, K., Sato, M. H., Yamaguchi, A., & Yoshida, M. (1994). Tetracycline/H+ antiporter was degraded rapidly in Escherichia coli cells when truncated at last transmembrane helix and this degradation was protected by overproduced GroEL/ES. Biochemical and Biophysical Research Communications, 202, 258-264.
48. Chen, Y., Song, J., Sui, S. F., & Wang, D. N. (2003). DnaK and DnaJ facilitated the folding process and reduced inclusion body formation of magnesium transporter CorA overexpressed in Escherichia coli. Protein Expression and Purification, 32, 221-231.
49. Martinez-Alonso, M., Garcia-Fruitos, E., Ferrer-Miralles, N., Rinas, U., & Villaverde, A. (2010). Side effects of chaperone gene co-expression in recombinant protein production. Microbial Cell Factories, 9, 64.
50. Galluccio, M., Pochini, L., Amelio, L., Accardi, R., Tommasino, M., & Indiveri, C. (2009). Over-expression in E. coli and purification of the human OCTN1 transport protein. Protein Expression and Purification, 68, 215-220.
51. Galluccio, M., Amelio, L., Scalise, M., Pochini, L., Boles, E., & Indiveri, C. (2012). Over-expression in E. coli and purification of the human OCTN2 transport protein. Molecular Biotechnology, 50, 1-7.
52. Forrest, L. R., Kramer, R., & Ziegler, C. (2011). The structural basis of secondary active transport mechanisms. Biochimica et Biophysica Acta, 1807, 167-188.
53. Boudker, O., & Verdon, G. (2010). Structural perspectives on secondary active transporters. Trends in Pharmacological Sciences, 31, 418-426.
54. Maekawa, S., Mori, D., Nishiya, T., Takikawa, O., Horinouchi, T., Nishimoto, A., et al. (2007). OCTN2VT, a splice variant of OCTN2, does not transport carnitine because of the retention in the endoplasmic reticulum caused by insertion of 24 amino acids in the first extracellular loop of OCTN2. Biochimica et Biophysica Acta, 1773, 1000-1006.
55. Busch, W., & Saier, M. H., Jr. (2002). The transporter classification (TC) system. Critical Reviews in Biochemistry and Molecular Biology, 37, 287-337.
56. Tamai, I., Yabuuchi, H., Nezu, J., Sai, Y., Oku, A., Shimane, M., et al. (1997). Cloning and characterization of a novel human pH-dependent organic cation transporter, OCTN1. FEBS Letters, 419, 107-111.
57. Tamai, I., Ohashi, R., Nezu, J., Yabuuchi, H., Oku, A., Shimane, M., et al. (1998). Molecular and functional identification of sodium ion-dependent, high affinity human carnitine transporter OCTN2. Journal of Biological Chemistry, 273, 20378-20382.
58. Yabuuchi, H., Tamai, I., Nezu, J., Sakamoto, K., Oku, A., Shimane, M., et al. (1999). Novel membrane transporter OCTN1 mediates multispecific, bidirectional, and pH-dependent transport of organic cations. Journal of Pharmacology and Experimental Therapeutics, 289, 768-773.
59. Tamai, I., Ohashi, R., Nezu, J. I., Sai, Y., Kobayashi, D., Oku, A., et al. (2000). Molecular and functional characterization of organic cation/carnitine transporter family in mice. Journal of Biological Chemistry, 275, 40064-40072.
60. Wu, X., Huang, W., Prasad, P. D., Seth, P., Rajan, D. P., Leibach, F. H., et al. (1999). Functional characteristics and tissue distribution pattern of organic cation transporter 2 (OCTN2), an organic cation/carnitine transporter. Journal of Pharmacology and Experimental Therapeutics, 290, 1482-1492.
61. Koepsell, H., Lips, K., & Volk, C. (2007). Polyspecific organic cation transporters: structure, function, physiological roles, and biopharmaceutical implications. Pharmaceutical Research, 24, 1227-1251.
62. Ramsay, R. R., Gandour, R. D., & van der Leij, F. R. (2001). Molecular enzymology of carnitine transfer and transport. Biochimica et Biophysica Acta, 1546, 21-43.
63. Indiveri, C., Pochini, L., Oppedisano, F., & Tonazzi, A. (2010). The carnitine transporter network: Interactions with drugs. Current Chemical Biology, 4, 108-123.
64. Bieber, L. L. (1988). Carnitine. Annual Review of Biochemistry, 57, 261-283.
65. Owen, M. R., Corstorphine, C. C., & Zammit, V. A. (1997). Overt and latent activities of diacylglycerol acyltransferase in rat liver microsomes: Possible roles in very-low-density lipoprotein triacylglycerol secretion. Biochemical Journal, 323, 17-21.
66. Gooding, J. M., Shayeghi, M., & Saggerson, E. D. (2004). Membrane transport of fatty acylcarnitine and free l-carnitine by rat liver microsomes. European Journal of Biochemistry, 271, 954-961.
67. Tonazzi, A., Galluccio, M., Oppedisano, F., & Indiveri, C. (2006). Functional reconstitution into liposomes and characterization of the carnitine transporter from rat liver microsomes. Biochimica et Biophysica Acta, 1758, 124-131.
68. Vaz, F. M., & Wanders, R. J. (2002). Carnitine biosynthesis in mammals. Biochemical Journal, 361, 417-429.
69. Ohnishi, S., Okamura, N., Sakamoto, S., Hasegawa, H., Norikura, R., Kanaoka, E., et al. (2008). Role of Na+/l-carnitine transporter (OCTN2) in renal handling of pivaloylcarnitine and valproylcarnitine formed during pivalic acid-containing prodrugs and valproic acid treatment. Drug Metabolism and Pharmacokinetics, 23, 293-303.
70. Reda, E., D'Iddio, S., Nicolai, R., Benatti, P., & Calvani, M. (2003). The carnitine system and body composition. Acta Diabetologica, 40, S106-S113.
71. Lamhonwah, A. M., Skaug, J., Scherer, S. W., & Tein, I. (2003). A third human carnitine/organic cation transporter (OCTN3) as a candidate for the 5q31 Crohn's disease locus (IBD5). Biochemical and Biophysical Research Communications, 301, 98-101.
72. Pochini, L., Oppedisano, F., & Indiveri, C. (2004). Reconstitution into liposomes and functional characterization of the carnitine transporter from renal cell plasma membrane. Biochimica et Biophysica Acta, 1661, 78-86.
73. Kobayashi, D., Tamai, I., Sai, Y., Yoshida, K., Wakayama, T., Kido, Y., et al. (2007). Transport of carnitine and acetylcarnitine by carnitine/organic cation transporter (OCTN) 2 and OCTN3 into epididymal spermatozoa. Reproduction, 134, 651-658.
74. Xuan, W., Lamhonwah, A. M., Librach, C., Jarvi, K., & Tein, I. (2003). Characterization of organic cation/carnitine transporter family in human sperm. Biochemical and Biophysical Research Communications, 306, 121-128.
75. Lamhonwah, A. M., Hawkins, C. E., Tam, C., Wong, J., Mai, L., & Tein, I. (2008). Expression patterns of the organic cation/carnitine transporter family in adult murine brain. Brain & Development, 30, 31-42.
76. Lamhonwah, A. M., Ackerley, C. A., Tilups, A., Edwards, V. D., Wanders, R. J., & Tein, I. (2005). OCTN3 is a mammalian peroxisomal membrane carnitine transporter. Biochemical and Biophysical Research Communications, 338, 1966-1972.
77. Lamhonwah, A. M., & Tein, I. (2006). Novel localization of OCTN1, an organic cation/carnitine transporter, to mammalian mitochondria. Biochemical and Biophysical Research Communications, 345, 1315-1325.
78. Koepsell, H., & Endou, H. (2004). The SLC22 drug transporter family. Pflugers Archiv: European Journal of Physiology, 447, 666-676.
79. Gupta, S., Burckhardt, G., & Hagos, Y. (2011). SLC22 transporter family proteins as targets for cytostatic uptake into tumor cells. The Journal of Biological Chemistry, 392, 117-124.
80. Rogl, H., Kosemund, K., Kuhlbrandt, W., & Collinson, I. (1998). Refolding of Escherichia coli produced membrane protein inclusion bodies immobilised by nickel chelating chromatography. FEBS Letters, 432, 21-26.
81. Rath, A., Glibowicka, M., Nadeau, V. G., Chen, G., & Deber, C. M. (2009). Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proceedings of the National Academy of Sciences USA, 106, 1760-1765.
82. Pochini, L., Scalise, M., Galluccio, M., Pani, G., Siminovitch, K. A., & Indiveri, C. (2012). The human OCTN1 (SLC22A4) reconstituted in liposomes catalyzes acetylcholine transport which is defective in the mutant L503F associated to the Crohn's disease. Biochimica et Biophysica Acta, 1818, 559-565.
83. Pochini., L., Scalise, M., Galluccio, M. & Indiveri, C. (2012) Regulation by physiological cations of acetylcholine transport mediated by human OCTN1 (SLC22A4). Implications in the non-neuronal cholinergic system. Life Sciences. doi: org/10.1016/j.lfs.2012.04.027.
84. Longo, N., di San, Amat., Filippo, C., & Pasquali, M. (2006). Disorders of carnitine transport and the carnitine cycle. American Journal of Medical Genetics C, 142C, 77-85.
85. Rebouche, C. J. (2004). Kinetics, pharmacokinetics, and regulation of l-carnitine and acetyl-l-carnitine metabolism. The New York Academy of Sciences, 1033, 30-41.
86. Wang, Y., Ye, J., Ganapathy, V., & Longo, N. (1999). Mutations in the organic cation/carnitine transporter OCTN2 in primary carnitine deficiency. Proceedings of the National Academy of Sciences USA, 96, 2356-2360.
87. Ciarimboli, G. (2011). Role of organic cation transporters in drug-induced toxicity. Expert Opinion on Drug Metabolism and Toxicology, 7, 159-174.
88. Pochini, L., Scalise, M., & Indiveri, C. (2009). Inactivation by omeprazole of the carnitine transporter (OCTN2) reconstituted in liposomes. Chemico-Biological Interactions, 179, 394-401.
89. Nezu, J., Tamai, I., Oku, A., Ohashi, R., Yabuuchi, H., Hashimoto, N., et al. (1999). Primary systemic carnitine deficiency is caused by mutations in a gene encoding sodium ion-dependent carnitine transporter. Nature Genetics, 21, 91-94.
90. di San, Amat., Filippo, C., Pasquali, M., & Longo, N. (2006). Pharmacological rescue of carnitine transport in primary carnitine deficiency. Human Mutation, 27, 513-523.
91. Melegh, B., Bene, J., Mogyorosy, G., Havasi, V., Komlosi, K., Pajor, L., et al. (2004). Phenotypic manifestations of the OCTN2 V295X mutation: sudden infant death and carnitine-responsive cardiomyopathy in Roma families. American Journal of Medical Genetics A, 131, 121-126.
92. Xuan, C., Zhang, B. B., Yang, T., Deng, K. F., Li, M., & Tian, R. J. (2012). Association between OCTN1/2 gene polymorphisms (1672C-T, 207G-C) and susceptibility of Crohn's disease: A meta-analysis. International Journal of Colorectal Disease, 27, 11-19.
93. Martini, M., Ferrara, A. M., Giachelia, M., Panieri, E., Siminovitch, K., Galeotti, T., et al. (2012). Association of the OCTN1/1672T variant with increased risk for colorectal cancer in young individuals and ulcerative colitis patients. Inflammatory Bowel Diseases, 18, 439-448.
94. Peltekova, V. D., Wintle, R. F., Rubin, L. A., Amos, C. I., Huang, Q., Gu, X., et al. (2004). Functional variants of OCTN cation transporter genes are associated with Crohn disease. Nature Genetics, 36, 471-475.
95. Wessler, I., & Kirkpatrick, C. J. (2008). Acetylcholine beyond neurons: The non-neuronal cholinergic system in humans. British Journal of Pharmacology, 154, 1558-1571.
96. Ng, C. M., Blackman, M. R., Wang, C., & Swerdloff, R. S. (2004). The role of carnitine in the male reproductive system. Annals of the New York Academy of Sciences, 1033, 177-188.
97. Hinton, B. T., Dott, H. M., & Setchell, B. P. (1979). Measurement of the motility of rat spermatozoa collected by micropuncture from the testis and from different regions along the epididymis. Journal of Reproduction and Fertility, 55, 167-172.
98. Scalise, M., Galluccio, M., Accardi, R., Cornet, I., Tommasino, M., & Indiveri, C. (2012). Human OCTN2 (SLC22A5) is down-regulated in virus- and non virus-mediated cancer. Cell Biochemistry & Function,. doi: 10.1002/cbf.2816.
99. Tang, L., Bai, L., Wang, W. H., & Jiang, T. (2010). Crystal structure of the carnitine transporter and insights into the antiport mechanism. Nature Structural & Molecular Biology, 17, 492-496.