Engineering and characterization of human manganese superoxide dismutase mutants with high activity and low product inhibition

FEBS Journal

Volumn 273, Issue 21, 2006, Pages 4853-4861

  Chockalingam, Karuppiah ^a   Luba, James ^b   Nick, Harry S ^c   Silverman, David N ^b   Zhao, Huimin ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Directed evolution; Gene therapy; Kinetic analysis; Product inhibition

Indexed keywords

ALANINE; ASPARAGINE; CYSTEINE; GLUTAMINE; MANGANESE SUPEROXIDE DISMUTASE; MUTANT PROTEIN; SERINE;

ARTICLE; CANCER GROWTH; CATALYSIS; CONTROLLED STUDY; DIRECTED MOLECULAR EVOLUTION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME ENGINEERING; ENZYME INHIBITION; ENZYME KINETICS; ENZYME STRUCTURE; HUMAN; MICHAELIS MENTEN KINETICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION;

CATALYSIS; HUMANS; KINETICS; MODELS, MOLECULAR; MUTATION; RECOMBINANT PROTEINS; SUPEROXIDE DISMUTASE;

EID: 33750058553     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05484.x     Document Type: Article

References (43)

1. Lebovitz RM, Zhang HJ, Vogel H, Cartwright J, Dionne L, Lu NF, Huang S & Matzuk MM (1996) Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 93, 9782-9787.
2. Li YB, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson TL, Noble LJ, Yoshimura MP, Berger C, Chan PH et al. (1995) Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 11, 376-381.
3. Liu RG, Buettner GR & Oberley LW (2000) Oxygen free radicals mediate the induction of manganese superoxide dismutase gene expression by TNF-alpha. Free Radic Biol Med 28, 1197-1205.
4. Poswig A, Wenk J, Brenneisen P, Wlaschek M, Hommel C, Quel G, Faisst K, Dissemond J, Briviba K, Krieg T et al. (1999) Adaptive antioxidant response of manganese superoxide dismutase following repetitive UVA irradiation. J Invest Dermatol 112, 13-18.
5. Epperly MW, Bray JA, Krager S, Berry LM, Gooding W, Engelhardt JF, Zwacka R, Travis EL & Greenberger JS (1999) Intratracheal injection of adenovirus containing the human MnSOD transgene protects athymic nude mice from irradiation-induced organizing alveolitis. Int J Radiat Oncol Biol Phys 43, 169-181.
6. Stickle RL, Epperly MW, Klein E, Bray JA & Greenberger JS (1999) Prevention of irradiation-induced esophagitis by plasmid / liposome delivery of the human manganese superoxide dismutase transgene. Radiat Oncol Invest 7, 204-217.
7. Epperly MW, Sikora C, Defilippi S, Bray J, Koe G, Liggitt D, Luketich JD & Greenberger JS (2000) Plasmid / liposome transfer of the human manganese superoxide dismutase transgene prevents ionizing irradiation-induced apoptosis in human esophagus organ explant culture. Int J Cancer 90, 128-137.
8. Kanai AJ, Zeidel ML, Lavelle JP, Greenberger JS, Birder LA, De Groat WC, Apodaca GL, Meyers SA, Ramage R & Epperly MW (2002) Manganese superoxide dismutase gene therapy protects against irradiation-induced cystitis. Am J Physiol Renal Physiol 283, F1304-F1312.
9. Dobashi K, Ghosh B, Orak JK, Singh I & Singh AK (2000) Kidney ischemia-reperfusion: modulation of antioxidant defenses. Mol Cell Biochem 205, 1-11.
10. Wang LI, Miller DP, Sai Y, Liu G, Su L, Wain JC, Lynch TJ & Christiani DC (2001) Manganese superoxide dismutase alanine-to-valine polymorphism at codon 16 and lung cancer risk. J Natl Cancer I, 1818-1821.
11. Church SL, Grant JW, Ridnour LA, Oberley LW, Swanson PE, Meltzer PS & Trent JM (1993) Increased manganese superoxide dismutase expression suppresses the malignant phenotype of human melanoma cells. Proc Natl Acad Sci USA 90, 3113-3117.
12. Li JJ, Oberley LW, St Clair DK, Ridnour LA & Oberley TD (1995) Phenotypic changes induced in human breast cancer cells by overexpression of manganese-containing superoxide dismutase. Oncogene 10, 1989-2000.
13. Lam EWN, Zwacka R, Engelhardt JF, Davidson BL, Domann FE, Yan T & Oberley LW (1997) Adenovirus-mediated manganese superoxide dismutase gene transfer to hamster cheek pouch carcinoma cells. Cancer Res 57, 5550-5556.
14. Li N, Oberley TD, Oberley LW & Zhong WX (1998) Overexpression of manganese superoxide dismutase in DU145 human prostate carcinoma cells has multiple effects on cell phenotype. Prostate 35, 221-233.
15. Yan T, Oberley LW, Zhong WX & St Clair DK (1996) Manganese-containing superoxide dismutase overexpression causes phenotypic reversion in SV40-transformed human lung fibroblasts. Cancer Res 56, 2864-2871.
16. Liu RG, Oberley TD & Oberley LW (1997) Transfection and expression of MnSOD cDNA decreases tumor malignancy of human oral squamous carcinoma SCC-25 cells. Hum Gene Ther 8, 585-595.
17. Zhong WX, Oberley LW, Oberley TD & St Clair DK (1997) Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase. Oncogene 14, 481-490.
18. Davis CA, Hearn AS, Fletcher B, Bickford J, Garcia JE, Leveque V, Melendez JA, Silverman DN, Zucali J, Agarwal A et al. (2004) Potent anti-tumor effects of an active site mutant of human manganese-superoxide dismutase. Evolutionary conservation of product inhibition. J Biol Chem 279, 12769-12776.
19. Bull C, Niederhoffer EC, Yoshida T & Fee JA (1991) Kinetic studies of superoxide dismutases - properties of the manganese containing protein from Thermus thermophilus. J Am Chem Soc 113, 4069-4076.
20. McAdam ME, Fox RA, Lavelle F & Fielden EM (1977) A pulse-radiolysis study of the manganese-containing superoxide dismutase from Bacillus stearothermophilus: a kinetic model for the enzyme action. Biochem J 165, 71-79.
21. Hearn AS, Tu C, Nick HS & Silverman DN (1999) Characterization of the product-inhibited complex in catalysis by human manganese superoxide dismutase. J Biol Chem 274, 24457-24460.
22. Hsieh Y, Guan Y, Tu C, Bratt PJ, Angerhofer A, Lepock JR, Hickey MJ, Tainer JA, Nick HS & Silverman DN (1998) Probing the active site of human manganese superoxide dismutase: the role of glutamine 143. Biochemistry 37, 4731-4739.
23. Ramilo CA, Leveque V, Guan Y, Lepock JR, Tainer JA, Nick HS & Silverman DN (1999) Interrupting the hydrogen bond network at the active site of human manganese superoxide dismutase. J Biol Chem 274, 27711-27716.
24. Cabelli DE, Guan Y, Leveque V, Hearn AS, Tainer JA, Nick HS & Silverman DN (1999) Role of tryptophan 161 in catalysis by human manganese superoxide dismutase. Biochemistry 38, 11686-11692.
25. Leveque VJ, Stroupe ME, Lepock JR, Cabelli DE, Tainer JA, Nick HS & Silverman DN (2000) Multiple replacements of glutamine 143 in human manganese superoxide dismutase: effects on structure, stability, and catalysis. Biochemistry 39, 7131-7137.
26. Carlioz A & Touati D (1986) Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J 5, 623-630.
27. Gao BF, Flores SC, Bose SK & McCord JM (1996) A novel Escherichia coli vector for oxygen-inducible high level expression of foreign genes. Gene 176, 269-272.
28. Morimyo M, Hongo E, Hamainaba H & Machida I (1992) Cloning and characterization of the mvrC gene of Escherichia coli K-12 which confers resistance against methyl viologen toxicity. Nucleic Acids Res 20, 3159-3165.
29. Hsu JL, Hsieh Y, Tu C, O'Connor D, Nick HS & Silverman DN (1996) Catalytic properties of human manganese superoxide dismutase. J Biol Chem 271, 17687-17691.
30. Hearn AS, Stroupe ME, Cabelli DE, Lepock JR, Tainer JA, Nick HS & Silverman DN (2001) Kinetic analysis of product inhibition in human manganese superoxide dismutase. Biochemistry 40, 12051-12058.
31. Cornish-Bowden A (1995) Fundamentals of Enzyme Kinetics. 2nd edn, pp. 121-122. Portland Press Ltd., London.
32. Marklund S (1976) Spectrophotometric study of spontaneous disproportionation of superoxide anion radical and sensitive direct assay for superoxide dismutase. J Biol Chem 251, 7504-7507.
33. Silverman DN & Nick HS (2002) Catalytic pathway of manganese superoxide dismutase by direct observation of superoxide. Methods Enzymol 349, 61-74.
34. Borgstahl GEO, Pokross M, Chehab R, Sekher A & Snell EH (2000) Cryo-trapping the six-coordinate, distorted-octahedral active site of manganese superoxide dismutase. J Mol Biol 296, 951-959.
35. Maliekal J, Karapetian A, Vance C, Yikilmaz E, Wu Q, Jackson T, Brunold TC, Spiro TG & Miller AF (2002) Comparison and contrasts between the active site PKs of Mn-superoxide dismutase and those of Fe-superoxide dismutase. J Am Chem Soc 124, 15064-15075.
36. Greenleaf WB, Perry JJ, Hearn AS, Cabelli DE, Lepock JR, Stroupe ME, Tainer JA, Nick HS & Silverman DN (2004) Role of hydrogen bonding in the active site of human manganese superoxide dismutase. Biochemistry 43, 7038-7045.
37. Chockalingam K, Chen ZL, Katzenellenbogen JA & Zhao HM (2005) Directed evolution of specific receptor-ligand pairs for use in the creation of gene switches. Proc Natl Acad Sci USA 102, 5691-5696.
38. Crameri A, Raillard SA, Bermudez E & Stemmer WP (1998) DNA shuffling of a family of genes from diverse species accelerates directed evolution. Nature 391, 288-291.
39. Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
40. Thomas MR (1994) Simple, effective cleanup of DNA ligation reactions prior to electrotransformation of Escherichia coli. Biotechniques 16, 988-990.
41. Zhao H & Arnold FH (1997) Optimization of DNA shuffling for high fidelity recombination. Nucleic Acids Res 25, 1307-1308.
42. McClune GJ & Fee JA (1978) A simple system for mixing miscible organic solvents with water in 10-20 ms for the study of superoxide chemistry by stopped-flow methods. Biophys J 24, 65-69.
43. 2 in aqueous solutions by pulse radiolysis. J Phys Chem 73, 3736-3744.